Report of the Disease Vectors, Surveillance, and Prevention Subcommittee to the Tick-Borne Disease Working Group

Appendix 1: Subcommittee Members and Support Staff

Disclaimer: Information and opinions in this report do not necessarily reflect the opinions of the working group, the U.S. Department of Health and Human Services, or any other component of the federal government.

Background

Subcommittee Formation and Charge. The Disease Vector, Surveillance, and Prevention Subcommittee was established with the charge to look closely into the current status, needs, and challenges in our understanding of tick vectors, our capacity to conduct human disease surveillance, and our capability to prevent disease. The final product of the subcommittee will be potential actions on specific activities that will lead to key improvements.

The incidence and distribution of Lyme disease and other reportable tick-borne illnesses are increasing across the United States, with over 300,000 new cases of Lyme disease alone occurring each year. In the absence of a vaccine in the U.S. against any of the tick-borne diseases, effective primary prevention relies on reducing exposure to ticks. Identifying and validating effective prevention and control strategies is critical for reducing the incidence of new cases. Additionally, in order to track the effectiveness of national prevention and control strategies, it is essential to maintain an accurate understanding of current disease burden and trends against which to measure success of national prevention goals once established.

Major challenges – disease vectors. In recent decades, the distribution of the important tick vectors of human and animal illnesses have increased steadily and significantly. The number of counties in the U.S. where Ixodes scapularis, the vector for Lyme disease, anaplasmosis, babesiosis, and Powassan virus disease, is now established has doubled in the last 20 years (Eisen, Eisen, & Beard, 2016). The reasons for the increase in tick distribution are complex and vary by region. Additionally, due to the lack of a coordinated national tick vector surveillance program, there are significant gaps in information on local distribution of tick vectors, information which is badly needed for educating the public health community, healthcare providers and the general public about local disease risk. Some additional concerns about tick vectors that have arisen over the last two decades include the emergence of Rhipicephalus sanguineus as a vector of Rocky Mountain spotted fever in the Southwest, the expansion of Amblyomma americanum up the eastern seaboard, and the increase in human host preference of nymphal Ixodes scapularis populations expanding southward through Maryland, Virginia, and into the Carolinas, and Tennessee. Additionally, there is a need to better understand the pathogens and vectors associated with tick-borne diseases in the southern states and along the Pacific Coast, and there are concerns about the risk of introduction of exotic tick species such as Haemaphysalis longicornis, which was recently identified in New Jersey.

Major challenges – surveillance. Currently seven tick-borne diseases are nationally notifiable in the U.S. In 2016, Lyme disease was the most common vector-borne disease reported and the sixth most common of all nationally notifiable diseases. While approximately 35,000 cases of Lyme disease are reported each year to the CDC, recent studies indicate that the actual number of annual cases exceeds 300,000 (Hinckley et al., 2014; Nelson et al., 2015). Under-reporting is a common phenomenon for most high-incident diseases, and Lyme disease under-reporting is further complicated by a case definition that requires both laboratory and supportive clinical data for confirmation of all but the earliest manifestations of the illness. National disease reporting, while coordinated by CDC, is formally a responsibility of state governments through the Council of State and Territorial Epidemiologists (CSTE). CSTE determines, through votes of its membership, which diseases are nationally-notifiable and the specifics of case definitions. The resulting data are submitted to CDC where the information from each state is collated and made available nationally. Accurate and up-to-date incidence data for all tick-borne diseases, including Lyme disease, are critical in order to demonstrate the burden of illness in terms of both economic cost and human suffering, to establish baselines against which to measure prevention efforts and to monitor disease emergence in new geographic areas. Under-reporting and inconsistencies in surveillance data from state to state and from year to year significantly hamper efforts to raise public awareness of the magnitude of the problem and provide data needed to evaluate prevention effectiveness.

Major challenges – prevention. Currently, no vaccines are available in the U.S. against any tick-borne disease. Consequently, primary prevention relies on methods focused on reducing exposure of people to infected ticks. The toolbox of methods and products available to protect against biting ticks contain such things as personal repellants, acaricides approved for use on people, animals, and properties, landscape management, and personal protective behaviors and actions. The available data to show that any of the tools when deployed as directed can actually prevent human illness is very limited (Connally et al., 2009b). New methods and products are badly needed as well as controlled field trials that measure epidemiologic outcomes in order to provide data-driven prevention recommendations. Additionally, the internet is all too often an easily available source of misinformation, directing those at risk to prevention methods that are ineffective and potentially harmful.

Goals of the report. A key factor that crosscuts each of these major challenges is the critical lack of resources to address these needs. The goals of the report from this subcommittee are to review the state of the science relating to the three primary areas of tick vectors, human disease surveillance, and prevention, identifying critical gaps in information and specific resource needs. Based on this assessment, prioritized recommendations will be drafted to assist in guiding national policy to address these needs.

Key Issues and Priorities

On February 23, 2018, subcommittee members of the Disease Vectors, Surveillance, and Prevention Subcommittee of the HHS Tick-Borne Disease Working Group met by conference call to discuss and formulate key themes and issues related to the subcommittee scope of interest. To get the discussion started, subcommittee members were asked to respond to (revise, add, omit, etc.) a draft list of issues that had been originally composed by committee co-chairs. The major themes were derived directly from the subcommittee name (vectors, surveillance, and prevention). The key issues were identified based on the areas of greatest need for the twofold purpose of better documenting trends and burdens in tick-borne diseases in the U.S. and identifying, developing, evaluating, and implementing effective prevention and control practices.

In an effort to inform the process, three subject matter experts were identified by the subcommittee co-chairs in conjunction with committee members and asked to give presentations at subcommittee meetings on topics that related to the three key themes. On the February 23 call, Dr. Paul Mead, Chief of the Bacterial Diseases Branch in CDC’s Division of Vector-Borne Diseases, gave a presentation on trends and burdens of tick-borne diseases in the U.S. and how disease surveillance and reporting policies and practices are managed under the direction of the Council of State and Territorial Epidemiologists in conjunction with CDC. The talk provided insight into many of the challenges surrounding surveillance and reporting for tick-borne diseases in the U.S. The second presentation was made on the March 2 call by Dr. Neeta Connally, from Western Connecticut State University, a member of the subcommittee. This talk focused on the state of the science for tick prevention and personal protective measures. This talk was highly useful for understanding the strengths, weaknesses, and challenges in prevention. The third talk was given on March 23 by Dr. Robert Lane, Professor Emeritus at the University of California, Berkeley. This talk focused on a West Coast perspective on ticks, distribution, and various differences in their behavior and pathogens, addressing another important issue to be included in the subcommittee report.

The subcommittee discussed the issues, primarily adding, combining, and editing the draft list that was provided prior to the February 23 call. Once all the changes had been captured and the call was concluded, the revised list was sent out by e-mail to subcommittee members for additional comments and finalization. The finalized list was then distributed to the subcommittee by e-mail with the request that each subcommittee member select the top six issues, place them in ranked order, and send them by e-mail back to the subcommittee co-chairs for collation. The issues were placed in rank order based on the combined scores of the subcommittee members. During the process, it was observed by multiple subcommittee members that several of the issues in each theme could be combined. Consequently, the co-chairs selected related issues, combined them, and re-ranked them based on the subcommittee members’ votes. The top five issues were selected and are listed below

On Friday, March 2, 2018, the subcommittee met again by conference call to review all the changes that were made to the complete list of issues and the final list of the top five issues in rank order. Both were voted on and approved by unanimous vote of the subcommittee to be included in the first report, and are provided below. Of note, the five priorities listed reflect equally high priorities to the subcommittee and are not weighted in terms of their importance.

Improving Issues Relevant to the Disease Vectors, Surveillance, and Prevention Subcommittee

Complete List of Issues that Could Be Addressed in First Report to Congress

Key Theme 1 and Issue - Disease

What is our current knowledge of the following topics and what can be done to increase it?

The need for better vector surveillance
Geographic distribution and host feeding behavior of tick species involved in pathogen transmission cycles
Novel and emerging pathogens including Bartonella in ticks (rapid molecular detection)
Drivers of vector range expansion and vector and disease ecology
A better understanding of vector competence and vectorial capacity

Key Theme 2 and Issues – Human Surveillance

How do CDC and CSTE work together in conducting national disease surveillance?
How do surveillance policy changes get enacted?
How can surveillance practices be improved and standardized from state-to-state and from year-to-year?
Are there additional tick-borne diseases that should be nationally-notifiable?
What is the role of other data sources and patient registries in defining national disease trends?
Would CSTE consider other surveillance data other than case numbers?

Key Theme 3 and Issues – Prevention

What tools are currently in our toolbox for tick population control and disease prevention and how extensively have they been evaluated?
How can prevention education be improved, including providing accurate information and removing both personal and public obstacles?
What are the most promising novel prevention tools that are on the horizon (eg. transgenic ticks and other novel molecular interventions such as RNAi)?
How do we encourage commercialization of effective prevention tools and products?

Prioritized List of Issues that Will Be Addressed in the First Report to Congress

The need for a better understanding of the geographic distribution of tick vectors, disease ecology and vectorial capacity, how these are changing over time, and the key entomological determinants of risks to humans, including tick behavior and vector competence.
The need for novel safe and effective tick or host-targeted interventions that have been adequately validated to reduce human disease incidence.
The need for improvements in national disease surveillance and reporting, and the potential role of other data sources and patient registries in defining national disease burdens and trends.
Detection, identification, and characterization of novel and emerging pathogens in ticks, including Bartonella, and the transmission risks of these agents by ticks to humans.
The need for better prevention education, including providing accurate information and removing both personal and public obstacles.

Methods

Table 1: Members of the Disease Vector, Surveillance, and Prevention Subcommittee

Member	Type	Stakeholder Group	Expertise
(Co-Chair) C. Ben Beard, MS, PhD, Deputy Director, Div. Vector-Borne Diseases, CDC	Federal	Public Health	40+ years of experience working in vector-borne disease prevention and control, including 27 years at CDC; has published over 130 articles, books, and book chapters collectively on infectious diseases with an emphasis on vector-borne diseases.
(Co-Chair) Patricia (Pat) Smith, President, Lyme Disease Association, Inc; Member, CDMRP Programmatic Panel; Member, Columbia Lyme & Tick-Borne Diseases Advisory Committee (NJ)	Public	Family member; Advocate	Provides physician CME education; staff/student school education; public education on ticks/TBD; Congressional & state testimonies; reviews & awards research & education grants; provides patient support; written brochures on surveillance issues; developed maps/graphs on case numbers, 30 years’ experience.
Jill Auerbach, Founder: Tick Research to Eliminate Disease, & also Stop Ticks On People (NY)	Public	Patient, Advocate	Organized many educational presentations for community on prevention, ticks, the environment; presented educational classes; presented to local, state/federal officials about the need for tick prevention research; chaired Community Advisory Board in work on 3 year CDC grant to County Department of Health, IPM work group member.
Neeta Connally, PhD, MSPH, Associate Professor, Tick-Borne Disease Prevention Laboratory, Western CT State (CT)	Public	Researcher	Vector ecology; epidemiology of tick-borne diseases; Director, WCSU Tickborne Disease Prevention Laboratory.
Katherine Feldman, DVM, MPH, Senior Epidemiologist, MITRE, MD	Public	Researcher	Tck-borne disease work for state/federal health agencies 18 yrs.; conducting and evaluating public health surveillance for Lyme & TBD; led public health investigations/responses to TBD.
Thomas N. Mather, PhD, Professor, Center for Vector-Borne Disease; Director, TickEncounter Resource Center (RI)	Public	Researcher	Professor of entomology; 35 years research on tick biology, ecology, & control; tick bite prevention; anti-tick vaccine; Tick Encounter Resource Center website; TickSpotters crowd sourced tick survey/response.
Phyllis Mervine, MA, President, LymeDisease.org.(CA)	Public	Patient, Advocate	30 years of collaboration on studies in northern California; experience as science writer and editor; career as a patient advocate; promoting public education/patient empowerment and keeping up with the research.
Robyn Nadolny, PhD, Program Coordinator, Tick-Borne Disease Laboratory, Army Public Health Center	Federal	Public Health	8 years’ experience in tick/TBD research; 16 peer-reviewed publications; field biology/ecology, tick ecology, population, establishment; tick-host interaction; tick survival in environment; tick surveillance; tick testing.
Adalberto (Beto) Perez de Leon, DVM, PhD, MS, Director, Knipling-Bushland U.S. Livestock Insects Research Laboratory, US Depart of Agriculture-Agricultural Research Service	Federal	Researcher	32 yrs. experience: discovery & product development in animal health, arthropod pest management, vector-borne diseases, biotechnology, (ticks/TBD), technological innovation in pesticide science, mechanism-based screening to discover safer parasiticides, veterinary drug delivery systems, anti-tick-vaccines, and VBD molecular diagnostics, genomics research to develop anti tick measures.
Daniel E. Sonenshine, PhD, Eminent Professor of Biological Science, Old Dominion University (VA)	Public	Researcher	200 peer-reviewed publications on ticks and tick-borne pathogens of disease in humans and animals; book "Biology of Ticks;" patented technologies pheromone-assisted methods for tick control; professor biological sciences; chapter co-author on ticks/TBD in Medical & Veterinary Entomology.
Jean I. Tsao, PhD, Associate Professor, Departments of Fisheries and Wildlife and of Large Animal Clinical Sciences, Michigan State University (MI)	Public	Researcher	Eco-epidemiology of tick-borne pathogens; emergence of ticks and tick-borne pathogens; geographic variation in Lyme disease ecology and risk.
Monica M. White, President/Co-founder, Colorado Tick-Borne Disease Awareness Association (CO)	Public	Patient, Family member, Advocate	Wildlife biologist US Forest Service (former career employee); member Public Tick IPM Working Group; TBD public conference provider; tick collection experience.
Stephen Wikel, PhD, Professor and Chair Emeritus of Medical Sciences, St. Vincent's Medical Center, Quinnipiac University (CT)	Public	Researcher	45 yrs. immunology of tick-host-pathogen interactions: cellular & molecular biology, biochemistry, genomics; T-B pathogen interactions w/host defense; tick colonies, tick-infection methods w. TB pathogens; federal review & advisory committees.

Table 2: Overview of Disease Vectors, Surveillance, Prevention Meetings

Meeting No.	Date	Present	Topics Addressed
1	February 23, 2018	Pat Smith, Ben Beard, Jill Auerbach, Neeta Connally, Katherine Feldman, Thomas N. Mather, Robin Nadolny, Adalberto Perez de Leon, Daniel E. Sonenshine, Jean I. Tsao, Monica M. White, Stephen Wikel	Roll call; Explanation of formal notetaking of subcommittee meetings; Introduction of Dr. Paul Mead & presentation title; Surveillance for Lyme Disease in the United States; Q & A for Paul Mead; Dates for next meetings; Explanation of how discussion will proceed; Brainstorming full list: “What issues need to be examined or questions need to be addressed to ensure that US responds effectively to issues of our subcommittee;” Vote full list; Decide when and how to move to the Prioritized List; Presenters needed to fill critical needs within short time frame; Call for adjournment.
2	March 2, 2018	Pat Smith, Ben Beard, Jill Auerbach, Neeta Connally, Katherine Feldman, Thomas N. Mather, Phyllis Mervine, Robin Nadolny, Adalberto Perez de Leon, Daniel E. Sonenshine, Jean I. Tsao, Monica M. White, Stephen Wikel	Roll call; Introduction of Dr. Neeta Connally and presentation Prevention; PowerPoint presentation; Q and A for Neeta; Priority Charge (Table 2)—Explanation of how discussion will proceed; Discussion and consensus/vote on the prioritized list; Next steps in the process; Announce next meeting date: March 8, 2018, 2:00PM-4:00PM; Announce Bob Lane as a speaker for March 23, 2018 meeting; Call for adjournment.
3	March 8, 2018	Pat Smith, Ben Beard, Jill Auerbach, Neeta Connally, Katherine Feldman, Thomas N. Mather, Phyllis Mervine, Robin Nadolny, Daniel E. Sonenshine, Jean I. Tsao, Monica M. White	Roll call; Discussion of next phase of report; Nominations of suggested Priority List Coordinators by Co-Chairs; Discussion of List & Volunteers for each List; Begin Writing Process; Table 2 Priority- Brainstorm, flesh out (see also Outline Subcommittee Report p.2c.iv.1a-e); Next meeting date 3/16/18 2-4; Call for Adjournment 4:00PM.
4	March 16, 2018	Pat Smith, Ben Beard, Jill Auerbach, Neeta Connally, Katherine Feldman, Phyllis Mervine, Thomas N. Mather, Robin Nadolny, Adalberto Perez de Leon, Daniel E. Sonenshine, Monica M. White, Stephen Wikel	Roll call; Vote: 1st Draft Background/Methods Report to be submitted; Updates from HHS; Full Subcommittee Discussion on Priority Group 2; Full Subcommittee Discussion on Priority Group 3; Full Subcommittee Discussion on Priority Group 4; Next meeting date 3/23 /18 2-4, Bob Lane presenting & Priority Group 5; Call for Adjournment 4:00PM.
5	March 23, 2018	Pat Smith, Ben Beard, Jill Auerbach, Neeta Connally, Katherine Feldman, Thomas N. Mather, Robin Nadolny, Daniel E. Sonenshine, Jean I. Tsao, Monica M. White, Stephen Wikel	Roll call; Introduction of Robert (Bob) Lane, PhD; Lyme Disease in California, Ecology & Epidemiology & presentation; Q & A for Robert Lane; Updates from HHS; Full Subcommittee Discussion on Priority Group 5; Update Background report 1st draft & vote to accept; Next meeting date 3-28-18, 2-4PM ET; Call for Adjournment 4:00PM.
6	March 28, 2018	Pat Smith, Ben Beard, Jill Auerbach, Neeta Connally, Katherine Feldman, Thomas N. Mather, Phyllis Mervine, Robin Nadolny, Adalberto Perez de Leon, Daniel E. Sonenshine, Jean I. Tsao, Monica M. White	Roll call; HHS updates; Putting Pen to Paper: Results Sections for Each Priority - Questions About this document; Role of Results document in 5 priority topics; Next meeting April 6 (reports ready); Call for adjournment 3:00 PM
7	April 6, 2018	Pat Smith, Ben Beard, Jill Auerbach, Neeta Connally, Katherine Feldman, Thomas N. Mather, Phyllis Mervine, Robin Nadolny, Adalberto Perez de Leon, Daniel E. Sonenshine, Jean I. Tsao, Monica M. White, Stephen Wikel	Roll call; Any HHS updates; Any required action to be taken; Discussion and questions on writing 1st draft Results section; Next meeting April 13; Call for Adjournment
8	April 13, 2018	Pat Smith, Ben Beard, Jill Auerbach, Neeta Connally, Katherine Feldman, Thomas N. Mather, Phyllis Mervine, Robin Nadolny, Jean I. Tsao, Monica M. White	Roll call; Any HHS updates; Discussion and questions on Results 1st draft; Vote on Draft to be submitted by co-chairs; Vote on Proposed actions for working group to consider; Next meeting April 20; Call for Adjournment
9	April 18, 2018	Pat Smith, Ben Beard, Jill Auerbach, Neeta Connally, Katherine Feldman, Thomas N. Mather, Phyllis Mervine, Robin Nadolny, Adalberto Perez de Leon, Daniel E. Sonenshine, Jean I. Tsao, Monica M. White	Roll call; Any HHS updates; Discussion and questions on Results 1st draft; Vote on Draft to be submitted by co-chairs; Vote on Proposed actions for working group to consider; Next meeting Thursday, April 26. Call for Adjournment 4:00PM
10	April 26, 2018	Pat Smith, Ben Beard, Jill Auerbach, Neeta Connally, Katherine Feldman, Thomas N. Mather, Phyllis Mervine, Robin Nadolny, Adalberto Perez de Leon, Jean I. Tsao, Monica M. White, Stephen Wikel either entered late or left early & may have missed a vote(s)	Roll call; Any HHS updates; Discussion and questions on Results Final; Vote on Issues/Questions & priorities; Vote on final background report; Vote on final methods report; Vote on final results written report to be submitted by co-chairs; Vote on final proposed actions for working group to consider; Closing remarks; 4:00 PM Adjournment

Table 3: Presenters to the Disease Vector, Surveillance, & Prevention Subcommittee

Meeting No.	Presenter	Topics Discussed
1	Paul Meade, MD, MPH, Chief, Bacterial Branch, DVBD, Centers for Disease Control & Prevention, Ft. Collins CO	Surveillance for Lyme in US; public health surveillance; state role; CSTE; Lyme surveillance case definition; Nationally notifiable disease surveillance system; case stats; underreported; disease burden vector distribution; canine Lyme.
2	Neeta Connally, PhD, MSPH, Tickborne Disease Prevention Laboratory, Dept. of Biological & Environmental Sciences, Western CT University	Tick-Borne Disease Prevention in the Northeastern US; tick habitat; personal protection; repellent effectivity; showering; permethrin; property management; rodent targeting; ITM; IPM; prevention sources.
3	Robert Lane, PhD, Prof. Emeritus of Med. Entomology, Dept. of Environmental Science, Policy & Management, UC Davis, Berkeley	Lyme Disease in California: Ecology and Epidemiology; history & burden of Lyme in CA; research objectives; spirochetes in CA; ticks & distribution; vertebrate hosts; maintenance & reservoir hosts; birds; risk factors & behavior; seasonal activity; nymphs vs. adults; habitat.

Table 4: Votes Taken by the Disease Vector, Surveillance, & Prevention Subcommittee

Meeting or Date	Motion	Results	Minority Response
3/2/18	Approve issues and priorities section 1st draft of the report for submission to the Working Group	Passed 12-0 (1 absent)	N/A
3/16/18	Approve 1st draft methods section of report for submission to Working Group	Passed 12-0 (1 absent)	N/A
3/23/18	Approve 1st draft background section of report for submission to Working Group	Passed 12-0 (1 absent)	N/A
4/18/18	Approve 1st draft Results section of report for submission to Working Group	Passed 12-0 (1 absent)	N/A
4/18/18	Approve Recommendations to working group in Results Report	Consent agenda all recom. Passed 12-0 (1 absent)	N/A
4/26/18	Approve Final version Results Report and All Recommendations	The overall subcommittee report was approved unanimously, with 2 minority reports (12-0-1A). Each of the five sections was approved unanimously p1(10-0-3A); p2(10-0-3A); p3(11-0-2A); p4(12-0-1A); p5(12-0-1A). (1 absent entire meeting, see Meeting 10 in table above for attendance variations)	2 Minority reports 3-7-2abstain-1A (p4 prevention programs priority action) 4-7-2A (p3 surveillance used for diagnosis)

Results and Potential Actions

Results and Potential Actions for Priority 1: The Need for a Better Understanding of the Geographic Distribution of Tick Vectors, Disease Ecology and Vectorial Capacity, How These Are Changing Over Time, and the Key Entomological Determinants of Risks to Humans, Including Tick Behavior and Vector Competence.

Topic 1. The need for improved vector surveillance

Accurate, current knowledge of the diversity, distribution, and relative abundance of ticks and their associated pathogens is critical for guiding practices aimed at the prevention, diagnosis, and treatment of tick-borne diseases by individuals, public health, and health care providers. Unfortunately, current (2018) knowledge of the risk of tick transmission of various pathogens across states is highly uneven. Up-to-date, accurate knowledge of the acarological risk of tick-borne disease is critical for:

properly targeting public health messages for the prevention of tick-borne disease;
ruling in or out a diagnosis of tick-borne disease given how most people do not recall a tick bite and how clinical signs and symptoms of many tick-borne diseases resemble other diseases with other etiologies;
guiding current tick control interventions;
guiding future tick control interventions as they become available;
measuring the impact of any tick control intervention;
detecting invading tick species and associated pathogens; and
for providing data for models to better understand what factors drive temporal and spatial variation in tick-borne disease risk, so that we can predict how disease risk might change under a range of scenarios, and then take actions to mitigate it.

Evidence and Findings.

Surveillance for ticks and the tick-borne pathogens they harbor can be conducted by several methods. All have advantages and disadvantages, including which tick species can be sampled and the resources required (for example, personnel, time, and cost). Thus, it is important to consider the objective of the surveillance, the spatial and temporal scale of resolution, and the level of certainty in the data that is desired. Is a complete inventory of all human-biting ticks and all stages desired? Is the scale of interest at the state level? county? municipality? Is the resolution of the information just about presence/absence of the tick or a relative abundance and/or relative infection prevalence of each of the pathogens? The finer the spatial scale of resolution and the more certainty around the information, the greater the effort and resources required to conduct surveillance. Surveillance can be conducted actively and passively.

Passive surveillance. Passive surveillance for ticks occurs when data are collected, usually from the public, without a controlled sampling design. Examples include tick submission programs, where ticks are submitted by various people recruited by the state health department (for example, the public at large, forestry workers, wildlife biologists, livestock producers and others). Unfortunately, there is no control over the final sampling "effort". Data obtained may be uneven regarding location and time of year, and the certainty of the data will vary. Thus, inferences made regarding the risk of contacting ticks and/or pathogens may be unreliable. Nevertheless, passive surveillance is a low-cost program compared to active surveillance and has the advantage of engaging the public, and increasing public knowledge about ticks and tick-borne pathogens and behaviors needed to prevent tick exposure. Finally, if the objective of surveillance is to understand what ticks may be biting people, livestock, and/or companion animals, the passive surveillance by the public may best represent that risk. If, however, one of the objectives of tick surveillance is to prevent and mitigate risk of emerging tick-borne disease to humans, then the use of humans as the only basis of tick surveillance results in an unfortunate paradox.

Active surveillance. This method is done by investigators using a sampling design and systematic methods such that data can be collected with minimal bias at the spatial and temporal scales needed to address the surveillance objective. Examples of methods used to conduct active surveillance include dragging/flagging for host-seeking ticks; setting out carbon dioxide traps for questing ticks; trapping wildlife for on-host ticks; and similarly, searching companion animals/livestock for on-host ticks. Active surveillance increases the certainty that data collected from various locations and times are comparable and that the resulting inferences about the relative risks of contacting various species of ticks and pathogens in different locations and times are meaningful. Active surveillance is done by expert scientists using carefully planned, consistent methods to address a specific scientific question such as acarological risk in different habitats. The probability of detection, of course, is dependent on natural variation in tick/pathogen abundance, sampling effort, and stochastic factors affecting the sampling (for example, weather, host trapability) (Estrada-Pena, Gray, Kahl, Lane, & Nijhof, 2013); thus, the lack of detection does not equate necessarily to the true absence of ticks or pathogen. Yet, if ticks and/or pathogens are detected at other areas sampled with the same effort, then one can infer that the risk is lower. Similarly, active surveillance repeated over time in the same locations will allow for the detection of invading tick and/or pathogens as well as the ability to monitor the increase in abundance of ticks and their pathogens. Active surveillance should serve to provide a reliable, science-based assessment of the risk of tick-borne disease. With these data in hand, local and regional governmental authorities can best determine how to deploy limited resources to prevent or mitigate public risk of exposure to known or emerging tick-borne diseases. The main disadvantage is that active surveillance, is resource-intensive, and thus, depending on the resources available, will limit the scale of spatial and temporal resolution.

Habitat suitability models. Tick survivorship is highly influenced by abiotic factors and the availability of hosts that often have certain habitat requirements; thus, habitat suitability models (Pavlousky, 1966) can help predict the spatial risk of coming into contact with ticks and tick-borne disease pathogens. Furthermore, these models can help extend the value of data obtained from active and passive surveillance programs in a cost-effective manner. Briefly, using distribution data of ticks and tick-borne pathogens, one can develop a mathematical model that includes the abiotic and biotic factors that best explain their presence and absence. One can then apply this model to areas where surveillance is difficult or cost-prohibitive to conduct and generate a risk map, based on the suitability of that area for the ticks/tick-borne pathogens (Ostfeld, Glass, & Keesing, 2005). Similarly, one can forecast how the risk map will change in the future, for example, under different climate scenarios. Examples of such models include for I. scapularis (Brownstein, Holford, & Fish, 2003; Diuk-Wasser et al., 2010; Guerra et al., 2002; Hahn, Jarnevich, Monaghan, & Eisen, 2016); I. pacificus (Eisen et al., 2010; Eisen, Eisen, & Lane, 2006; Hahn et al., 2016); A. americanum (Raghavan et al., 2016; Springer, Jarnevich, Barnett, Monaghan, & Eisen, 2015); and D. variabilis (James, Burdett, McCool, Fox, & Riggs, 2015; Minigan, Hager, Peregrine, & Newman, 2018).

Possible Opportunities

Standardized approaches are needed to achieve the goal of obtaining consistent, reliable data on tick distribution, tick abundance, seasonal activity, and all aspects of tick behavior for the different tick vectors. A consensus is needed about which methods to adopt in order to best achieve this goal and provide adequate funding to carry it out. The following are examples of widely used methods that should be considered:

Dragging or flagging. Dragging involves pulling a white cloth (for example, denim or similar fabric) across the vegetation for a set distance and a set period. Flagging is done similarly but the cloth is mounted on a long pole with a handle that enables the investigator to sweep it across the vegetation or in the case of many nidicolous species into rodent burrows or nests. Both methods are effective for capturing host seeking ticks and are successful for collecting all the known vector tick species except for the immature stages of several tick species and soft bodied ticks.

Chemical lures. Another method is to lure ticks to a dry ice bait station; this requires that ticks can sense carbon dioxide from a distance and have a predatory behavior to orient and crawl towards the bait. This method is highly successful for attracting lone star ticks and soft bodied ticks, but not as efficient for blacklegged ticks.

Trapping and examining animals. This is used mostly for wildlife. This method allows one to sample those ticks that cannot be sampled by dragging/flagging or dry ice baits such as the nidicolous (for example, burrow or nest dwelling) ticks.

There are other sources of data - both actively and passively collected, however, potentially available to help improve the knowledge of tick distributions (see section on opportunities in Topic 2). And, similarly, opportunities exist to use both actively and passively collected data to construct habitat suitability and climate envelope models to help inform the use of limited resources for further surveillance and public health measures (see below in Topic 2 as well)

Threats or Challenges

The major challenge is to obtain funding to carry out a systematic tick surveillance program.

Collaboration is both an opportunity and a challenge to compiling and coordinating surveillance efforts from all sources (for example, federal, state, university research efforts, citizen science and private tick testing labs).

Topic 2: Geographic distribution and host feeding behavior of tick species involved in pathogen transmission cycles

At the broadest spatial scale, risk of a tick-borne disease is defined by the geographic distribution of the tick. Thus, to predict where people are at risk for tick-borne pathogens (for ones already exist and those that may invade in the future), knowledge of the geographic distributions of vector ticks is paramount. Tick distributions are dynamic, however, thus requiring efforts to predict the current and future spatial geographic distributions of vector ticks.

Many factors contribute to the variation in the spatial risk of acquiring a tick-borne pathogen, including host-feeding behavior of ticks; tick host preferences; host-seeking behaviors; tick vector competency (for example, if a tick species can transmit disease-causing pathogens); reservoir hosts (if a vertebrate is a competent host for tick-pathogens); and the interactions between these diverse factors, which can influence local abundance of infected tick-borne disease vectors. Tick host-seeking behavior also directly affects the risk of human exposure to ticks and pathogens.

Evidence and Findings

Based on collections made by the U.S. Bureau of Entomology and Plant Quarantine, Bishop and Trembley (Bishop & Trembley, 1945) laid the foundation of our understanding of the geographic distributions of all the major human-biting ticks in the U.S. Since then, the geographic distribution of most tick vectors has expanded greatly along with the pathogens they transmit, including many that have not yet been discovered.

There have been no systematic tick surveys (with the brief exception of (Diuk-Wasser et al., 2006; Diuk-Wasser et al., 2012; Diuk-Wasser et al., 2010), and thus knowledge of the current distributions of vector ticks is heterogeneous in effort and method, and is probably the best for the species that cause the most disease burden, and/or are of the greatest nuisance. These surveys are largely related to political maps (that is, country and state records). Lack of surveillance data in certain regions, or even localities within regions, gives a potentially false perception of tick borne disease risk and hinders patient’s access to prevention education and timely, accurate diagnosis and care.

Because of the lack of habitat-based systematic collections, the existing knowledge informs the general geographic distribution but not the relative abundance of the ticks. Below, is an abbreviated description of the state of the science focusing on the most significant human-biting ticks. See (Eisen, Kugeler, Eisen, Beard, & Paddock, 2017) and (Sonenshine, 2018) for more detailed reviews.

Examples of geographic distribution of major tick disease vectors in the United States.

Blacklegged and western blacklegged tick (Ixodes scapularis and Ixodes pacificus). These two species are the primary vectors of the Lyme disease agent (Borrelia burgdorferi) as well as other serious disease-causing pathogens including Borrelia spp,(B. mayonii, B. miyamotoi, B. hermsii, and others) that cause Lyme and tick-borne relapsing fevers, Anaplasmosis, Babesiosis, and Powassan Virus. Over the last two decades, the distribution of blacklegged ticks has been continually expanding, whereas the distribution of western blacklegged ticks appears to be stable (Eisen, Kugeler, et al., 2017). However, surveillance for these ticks in many western states has been lacking. The geographic distribution now covers almost all the eastern U.S., as well as large areas in the north central U.S., southern U.S., and the Pacific coast westward into Utah. The northern distributions of the blacklegged tick are continuing to spread in all directions from two major foci in the northeast and north central U.S. (Eisen et al., 2016; Eisen, Kugeler, et al., 2017; Hahn et al., 2016; Sonenshine, 2018). Habitat suitability models were developed for the U.S. to predict localities where vectors might currently exist but not yet detected and where they may eventually spread and become established.

While the majority of cases of Lyme disease are diagnosed in foci in the Northeast and Midwest, it is important to note that the blacklegged and western blacklegged tick are well-established in other areas, including in areas where Lyme disease is considered to be endemic. Some Lyme-endemic counties in California are larger than the states of Rhode Island and Delaware (Fig 1, (Eisen et al., 2016), and the eco-epidemiology of Lyme disease in the southeastern US continues to be a subject of debate and study.

Maps showing the distribution of Lyme disease vectors in the U.S.

Figure 1. Known distribution of the Lyme disease vectors in the U.S. (left, (Eisen et al., 2016) in comparison with the distribution of Lyme disease cases reported to the CDC in 2015 (center) and average incidence reported in California (right, (Eisen et al., 2016). The tick species responsible for transmitting Lyme disease, Ixodes pacificus (in the west) and I. scapularis (in the east) have a larger geographic distribution compared with the distribution of reported cases of Lyme disease. It is important to note that while most Lyme disease cases occur in the northern eastern US, there is significant risk of acquiring Lyme disease in areas outside that region, as can be seen in California, where some of the counties in which both vector ticks are established and Lyme disease is endemic are larger than some states in the east.

Interestingly, a study of recent literature indicates that the western blacklegged tick, Ixodes pacificus, has not expanded its historic range very much if at all (although active surveillance efforts for the western blacklegged tick outside California may be limited). The reasons for this species stability are unknown but may be related to the region’s natural and biodiverse geography. Moreover, the region has been subjected to substantial anthropogenic changes in terms of urban and suburban development, increased farming and similar events, all of which patchy wilderness areas that impact animal local movements and opportunities for long range migration. Greatly improved wildlife management and expanded forestry regulations may also play a vital role in maintaining reservoir host populations at current levels.

Lone star tick (Amblyomma americanum). This species is the primary vector of human monocytotropic ehrlichiosis (HME), Ewingii ehrlichiosis, Panola Mountain ehrlichiosis, and has been implicated as the vector for Heartland virus (Godsey, Savage, Burkhalter, Bosco-Lauth, & Delorey, 2016; Savage et al., 2016); and Bourbon virus (Savage et al., 2017; Savage et al., 2018). In addition, the lone star tick has been implicated as the vector of the latter agent of the southern tick associated rash illness (STARI), the latter of which remains unidentified and is not limited to the southern USA (Feder et al., 2011; Wormser et al., 2005). Notably, the bite of the lone star tick has recently been linked to a delayed anaphylactic reaction to red meat, also known as the alpha gal allergy, which is becoming increasingly recognized as a health problem throughout this tick's range (Steinke, Platts-Mills, & Commins, 2015). Lone star ticks have also been associated with the agents of Rocky Mountain spotted fever, tularemia, and Q fever (Childs & Paddock, 2003; Jasinskas, Zhong, & Barbour, 2007), and their bite may induce tick paralysis. Except for RMSF (Levin, Zemtsova, Killmaster, Snellgrove, & Schumacher, 2017), the vector competence of lone star ticks and these diseases remains unproven (Childs & Paddock, 2003; Stromdahl & Hickling, 2012).

Studies have shown the lone star tick has been spreading northward and inland from their predominantly southern distribution and have now extended northwards into New York and the New England states up to Maine, in the Midwestern states up to southern Minnesota, and westward to Nebraska and Texas (Monzon, Atkinson, Henn, & Benach, 2016; Paddock & Yabsley, 2007; Sonenshine, 2018; Springer, Eisen, Beati, James, & Eisen, 2014). There are records of lone star ticks as far north as Maine, Iowa, and Minnesota in the US (Springer et al., 2014), but it also occurs in the northern states of Mexico (Guzmán-Cornejo, Robbins, Guglielmone, Montiel-Parra, & Pérez, 2011), but despite frequent collections in southeastern Canada, it seems not to have established populations there yet (Lindquist et al., 2016).

There have been modeling efforts to identify factors important for predicting the current distribution of the lone star ticks (Estrada-Pena, de la Fuente, & Cabezas-Cruz, 2016; Springer et al., 2015). Lone star ticks are opportunistic parasites, and their success can be attributed to the use of all three life stages on the deer (Paddock & Yabsley, 2007), their high fecundity, and their use of many host species (for example, turkey, squirrels, voles, and birds). Although pathogens tend to be found at low prevalence in lone star ticks, their highly abundant and aggressive feeding nature that increases their risk as vectors to humans.

American dog tick (Dermacentor variabilis). This species is the primary vector of the bacteria that causes Rocky Mountain spotted fever. The American dog tick has the broadest distribution, spanning the entire U.S., though this tick has a disjunct western distribution along the Pacific Coast of the USA and an extensive eastern distribution that extends from Canada to the Gulf of Mexico, west into Kansas and Nebraska and into Colorado, making it a potentially invasive species (CDPHE, 2016; James et al., 2015). It may also be established in Alaska (Durden & Mans, 2016). Its distribution has remained relatively stable since the earliest reports, as described by Bishop and Trembley (Bishop & Trembley, 1945). However, a few new foci have been discovered further north and west as well as in southern Canada (James et al., 2015; Minigan et al., 2018). Perhaps because of their pre-existing broad distribution and a well-studied understanding of their physiological tolerances, there have not been many recent modeling efforts to predict future distribution in the U.S. Notably, there has been a recent modeling effort to predict future distributions of the American dog tick in Canada (Minigan et al., 2018).

Gulf coast tick (Amblyomma maculatum). This tick is the major vector of a mild, spotted-fever-like illness (Rickettsia parkeri). As with other Dermacentor spp ticks, it is the adult ticks that parasitize humans and transmit the agents of human disease. While mature Gulf Coast ticks are readily collected in appropriate habitats where they are abundant, immatures tend not to quest above the leaf litter, and feed mainly on small mammals and birds (Teel, Ketchum, Mock, Wright, & Strey, 2010). Previously, it was limited to coastal areas of the southeastern U.S., Central and South America; however, it is now also occur in states along the Atlantic coast as far north as Delaware, as well as in the south central U.S. as far north as Oklahoma and Kansas (Paddock & Goddard, 2015). Gulf Coast ticks have been found to prefer open habitats, such as burned areas or areas maintained in mid-succession through human intervention, and their continued range expansion into the mid-Atlantic may be facilitated by these anthropogenically-created habitat islands (Nadolny & Gaff, 2018).

Rocky Mountain Wood tick (Dermacentor andersoni) and Pacific coast tick (Dermacentor occidentalis). The distributions of these two ticks appear to have remained stable. The wood tick occupies the area between the eastern and western distribution of the American dog tick and extends into British Columbia, Alberta and Saskatchewan in Canada (Dergousoff, Galloway, Lindsay, Curry, & Chilton, 2013). In the U.S., its geographical distribution is generally restricted to higher elevations (James et al., 2006). Dermacentor andersoni is the primary vector of the Colorado tick fever virus (Emmons, 1988); as well as the agents of Rocky Mountain spotted fever, Rickettsia rickettsii; and tularemia (Burgdorfer, 1969). It also is the cause of tick paralysis and is an experimental vector of the agents of Q fever (Davis & Cox, 1938), The Pacific coast tick is found throughout western California and Oregon. It transmits Rickettsia species 364D [https://coloradoticks.org/tick-borne-diseases/pacific-coast-tick-fever/], a form of spotted fever; where nymphal and larval stages of D. occidentalis have been implicated as the primary vectors of R. philipii to humans.

Brown dog tick (Rhipicephalus sanguineus). The brown dog tick has the broadest distribution of all these ticks, but outside of southern latitudes. Recent studies suggest that this taxon comprises a complex of species, some of which remain undescribed (Dantas-Torres et al., 2013). It is mainly found indoors (for example, dog kennels). In the South (spanning the entire southern U.S.), populations can survive and breed successfully in nature, but mainly in areas where canine hosts are readily available. The adult stage is the main vector because immature stages are nidicolous (that is, found in nests/burrows), and therefore rarely contact humans. On Native American reservations in Arizona, a population of this species has transmitted Rocky Mountain spotted fever group rickettsia to humans, resulting in 19 deaths (Drexler et al., 2014). Other disease-causing agents transmitted by this tick include those of canine ehrlichiosis and canine babesiosis and other Rickettsia worldwide.

Soft tick (Ornithodoros hermsi) This tick is the primary vector of one of the two principal North American agents of tick-borne relapsing fever (TBRF, that is, Borrelia hermsii in humans (Lopez, Krishnavahjala, Garcia, & Bermudez, 2016), which circulates sylvatically in rodents. This tick occurs widely in the western USA, with collections documented in AZ, CA CO, ID, MT, NM, NV, OR, UT, and WA (Dworkin et al., 1998; Dworkin, Schwan, Anderson, & Borchardt, 2008). It also was found in British Columbia, Canada (Lindquist et al., 2016). People usually are bitten as they sleep in rustic mountain cabins that are, or have been previously infested with rodents and, because of the painless and transient nature of this tick feeding, victims may not be aware of having been bitten (Johnson, Fischer, Raffel, & Schwan, 2016). Documented outbreaks of TBRF have occurred at vacation cabins in Estes Park, Colorado (Trevejo et al., 1998); Grand Canyon National Park, AZ (Paul, Maupin, Scott-Wright, Craven, & Dennis, 2002); and the Lake Tahoe area, CA (Schwan et al., 2009). Ornithodoros hermsi is loosely restricted to coniferous forests at elevations of approximately 900 203 to 2,000 m, where its hosts are primarily sciurids (for example, tree squirrels, ground squirrels [Urocitellus spp.], chipmunks [Tamias spp.]), with a few collections from bird nests and incidentally, humans.

Possible Opportunities

Tick distributions are dynamic but knowledge of their distributions is not keeping up especially at or beyond the edges of their distributions. The following are potential opportunities to improve our knowledge of the distribution of these important tick disease vectors.

As described above, several tick species having expanding distributions (Eisen, Kugeler, et al., 2017; Sonenshine, 2018). However, there are no systematic efforts to determine the presence/absence/relative abundance of ticks to "fill in" gaps of knowledge of areas within the distribution of a given tick species and/or to track changes in the distribution as tick populations spread.

There are more sources of data, however, potentially available to help improve the knowledge of tick distributions. For example, unpublished studies, veterinary data (CAPA, 2014; Little, Beall, Bowman, Chandrashekar, & Stamaris, 2014), and citizen submissions of ticks and/or photos of ticks to state health departments, on-line private/public reference centers (for example, Tick Encounter at University of Rhode Island and various smartphone health/tick applications) (URI), if the data quality could be confirmed.

Additionally, landscape epidemiology approaches (for example, habitat suitability and climate envelope models) can be applied to try to predict where ticks presently exist as well as where they might spread. Such models have been developed for several species (see above).

Threats and Challenges

Predicting tick distributions. As with any modeling endeavor, the reliability of model predictions depends on many factors. With respect to predicting tick distributions, it is important to consider, for example, the quality and representativeness of the data used to generate the model relative to geographic region of inference desired and life history characteristics of the species. For example, for both I. scapularis and I. pacificus, models that do not take into account variation in host-seeking behavior may predict accurately their presence, but not their risk of disease.

Knowledge about feeding behavior. Feeding behavior affects what kinds of hosts on which a tick will feed, which may affect the distribution and the abundance of the tick (that is, do the ticks feed on a select few hosts or many different hosts?). Similarly, how is tick distribution related to the ranges of their hosts (that is, do ticks feed on animals with small or large home ranges and do these animals exhibit long-distance dispersal patterns?). Examples of factors that need additional study include:

Nidicolous v. non-nidicolous nature of various life stages or species
How they quest: ambush v. predatory
Where they quest: below/above vegetation
When they quest (diurnal v. nocturnal)
Generalist v. specialist host preference

Topic 3: Drivers of vector range expansion and vector/disease ecology

There is a broad consensus among scientific experts that ticks have been expanding their geographic ranges since at least the middle of the 20th century (Clow et al., 2017; Eisen et al., 2016; Hahn et al., 2016; Medlock et al., 2013; Sonenshine, 2018). The drivers of vector tick range expansion are numerous and complex, but two major factors stand out and likely explain most of the reasons for this phenomenon, namely, climate change (especially global warming) and bird migrations. Though differing viewpoints on climate change have been recently published from a Canadian researcher which in addition to migratory birds, implicates that growing public awareness is driving factor for observed changes in tick distribution (Scott & Scott, 2018). Anthropogenic changes in the landscape, increasing populations of suitable host species and suitable tick habitat (Mixson, Lydy, Dasch, & Real, 2006; Ogden et al., 2006; Ogden, St-Onge, et al., 2008) also have contributed to tick range expansions. Similarly, changing populations of predators have been proposed to have effect on major tick host populations (Levi, Kilpatrick, Mangel, & Wilmers, 2012; O'Bryan et al., 2018). The evidence for these changing conditions and their implications for human and animal health are discussed below. A better understanding of the geographic distribution of the tick vectors, disease ecology and vectorial capacity, and how these factors are changing over time will help identify the key entomological determinants of risks to humans, including tick behavior and vector competence

Evidence and Findings

Arthropod vectors of pathogens are expanding their ranges because of climate change and shifting patterns of land use, resulting in dramatic and often unpredictable effects on human and wildlife health (Kilpatrick & Randolph, 2012). In North America, climate change, especially major warming trends, have expanded northward across the continent. The result is that most of the north-central and northeastern U.S. and even extensive areas of the mid-western region now have average above freezing temperatures during the winter months. Maps from the National Oceanic and Atmospheric Administration (NOAA) show that the -10-200 F. average temperature for January, which covered most of the north central and northeastern U.S. in 1970, now covers the region from northern Michigan, Wisconsin, Minnesota, North Dakota and northern Montana in the mid-west and small, isolated areas in northern New York and New England. Ticks can survive over the winter if soil temperatures hover near or slightly below freezing. Blacklegged ticks (Ixodes scapularis) have compounds in their body fluids (hemolymph) that function like a type of anti-freeze, enabling them to survive sub-zero temperatures (Neelakanta, Sultana, Fish, Anderson, & Fikrig, 2010). Furthermore, as with other ticks and insects, given that the rates of many physiological processes are temperature-dependent, warmer temperatures (up to a point) for a longer portion of the year can improve tick survivorship rates due to increased probabilities of host-finding and developing to the next life stage (or ovipositing eggs) before the onset of colder winter temperatures (Lindsay et al., 1998; Ogden et al., 2005). Recent research findings conducted in Canada found that lack of snow cover negatively affects the survival rate of overwintering adult ticks (Scott & Scott, 2018).

Maps of tick geographic distributions were published in 1945 (Bishop & Trembley, 1945). These maps show the ranges for 4 of the most important tick vectors in the U.S. All were located in the southern or mid-central regions of the country, and none were in Canada. Since that time, the geographic range of the American dog tick, Dermacentor variabilis, now covers almost all the eastern United States as well as in isolated foci in southern Canada. The blacklegged ticks, I. scapularis, the vector of the Lyme disease agent, Borrelia burgdorferi, has expanded northward into northern New York, all of New England, and even into parts of southeastern Canada. This phenomenon is mostly related to the re-introduction and proliferation of white-tailed deer (Odocoileus virginianus), which were almost exterminated in the previous century, as well as bird migration (Scott & Scott, 2018). Similarly, lone star ticks, Amblyomma americanum, the major vector of human monocytotropic ehrlichiosis (HME), have spread northward and now covers most of the eastern U.S. as well as large areas of the mid-central United States (Monzon et al., 2016). An even more remarkable range expansion is that of the Gulf Coast Tick, Amblyomma maculatum, a major pest of cattle and other livestock as well as a vector of Rickettsia parkeri, the causative agent of a spotted fever-like illness. This species, formerly limited only to the south Atlantic and Gulf coast region of the U.S., has now spread northward along the Atlantic coast as far as Delaware, as well as in the mid-west to Oklahoma and Kansas and in parts of southern Arizona. Similar examples of tick range expansion have occurred in Europe and northern Asia, particularly for the sheep tick (Ixodes ricinus) and the taiga tick (Ixodes persculatus), vectors of the Lyme disease agent in those regions (Medlock et al., 2013).

Studies suggest the following as main driving forces of the drastic changes in the geographic ranges of these tick vectors.

Warming winter temperatures. Climate change has been forecasted to increase tick habitat in the coming years. Studies have shown that the rising temperatures in the winter can increase the survival of ticks in winter, is already facilitating tick range expansions worldwide, and is increasing the risks of tick-borne diseases (Cumming & Van Vuuren, 2006; George, 2008; Leger, Vourc'h, Vial, Chevillon, & McCoy, 2013). Maps of weather patterns accumulated during recent decades have shown the warming patterns, especially in winter months (December through March) (see Figure 2 for January mean temperature changes). However, research recently completed in Canada over a 5-year period presents a differing viewpoint on influence of climate change on tick spread and prevalence. In their studies, these workers found that when there was consistent snow cover, 90% of the adult ticks survived the winter but fewer survived when temperatures were warmer with little snow cover (Scott & Scott, 2018). This study identifies migratory birds and increased public awareness as the drivers for tick distribution changes.
Migratory birds. Of the four major North American vectors of tick-borne disease noted above, I. scapularis, A. americanum and A. maculatum readily feed on birds, especially ground-feeding birds. Ground feeding birds that become infested with immature ticks drop engorged larvae and nymphs when they stop periodically to feed during their flights to their artic nesting grounds. Following the early reports by Morshed et al. (Morshed et al., 1999) and Scott et al. (Scott et al., 2001), more recent studies have shown that tens of millions of larval and nymphal ticks, primarily I. scapularis, are deposited in numerous locations in the northern U.S. and Canada((Ogden, Lindsay, et al., 2008) during the spring migration period, often establishing new tick foci and spreading tick-borne pathogens (Loss, Noden, Hamer, & Hamer, 2016).
Changing vertebrate host populations. Ticks depend on the movements of their hosts to facilitate dispersal across the landscape, and are particularly vulnerable to environmental pressures, such as desiccation, when they live away from their hosts (Leger et al., 2013). The increasing and expanding white-tailed deer populations in the U.S. and Canada will provide optimal hosts wherever the ticks range (Paddock & Yabsley, 2007). Furthermore, changes in landscape and land use (see below) that influence the dispersal of deer and other tick hosts will also affect the spread of ticks. Accidental transport by humans, livestock, and companion animals contributes to these events, as does ticks carried by illegal trade in exotic species.
Anthropogenic factors. Land use by humans have resulted in an increased abundance and diversity of arthropod disease vectors, including mosquitoes (Norris, 2004) and ticks (Brownstein et al., 2003; Childs & Paddock, 2003). Lyme disease is the best-known tick-borne disease associated with landscape changes, as reforestation, along with white-tailed deer management, may have resulted in an increase in Lyme disease risk (Barbour & Fish, 1993). Also, forest fragmentation and loss of biodiversity have been proposed to increase human disease risk (Allan, Keesing, & Ostfeld, 2003; LoGiudice, Ostfeld, Schmidt, & Keesing, 2003; Ostfeld & Keesing, 2000) but there have been few studies actually demonstrating causal relationships (Diuk-Wasser et al., 2012; Linske, Williams, Stafford, & Ortega, 2018; Ogden & Tsao, 2009; Randolph & Dobson, 2012; Salkeld, Padgett, & Jones, 2013; Wood & Lafferty, 2013; Zolnik, Falco, Kolokotronis, & Daniels, 2015). Studies have shown that the removal of weedy species and restoration of habitat can reduce Lyme disease risk (Gilbert, 2013; Morlando, Schmidt, & LoGiudice, 2012), and the removal of invasive plant species can result in a reduction in lone star ticks and effectively reduce disease risk (Allan et al., 2010).
Invasion by exotic species. Accidental transport by humans has resulted in numerous instances of exotic ticks being relocated to new geographic regions where they may become established. Examples include the transport of Gulf Coast ticks on cattle to new locations in the southcentral and mid-western U.S., the accidental introduction of the Japanese tick (Haemaphysalis longicornis to a sheep paddock in New Jersey (Rainey, Occi, Robbins, & Egizi, 2018) and the import of African ticks to Florida by illegal trade of snakes and other reptiles.

Tick distributions may also shrink and go extinct (locally). An example is the decrease in detection of I. muris, which used to be more abundant in New England, but then declined as I. scapularis became more abundant (Spielman, Levine, & Wilson, 1984).

Opportunities

Potential opportunities include:

Documenting tick range expansions and communicating their results in real-time
Documenting the effects of climate change (for example, what is the tipping point for tick establishment?)
Documenting the effects of land use and landscape change (for example, is there an “ideal” habitat matrix that promotes or prevents tick establishment?)
Improving models that integrate GIS and field (ground-truthing) studies to provide risk assessment studies for municipal, state and even broader regional governmental authorities to best plan their tick abatement activities. Standardized modeling techniques should be established and updated frequently.
Incorporating tick abatement programs into existing mosquito control programs similar to the New Jersey model. Most communities in the U.S. have funded mosquito control organizations, but tick control is not included.
Understanding which vectors may serve as reservoir hosts for the different tick-borne diseases, and how they contribute to the enzootic cycles of TBDs. For example, white-tailed deer are poor reservoir hosts but contribute to blacklegged tick population expansions by serving as hosts for adult ticks and mass production of their egg yield.
Utilizing the roles of western vs eastern fence lizards and borrelicidal blood, which feed ticks but kill spirochetes.
Exploring the influence of opossums, snakes, lizards, and other mesopredators that may bring down populations of ticks or small mammal reservoir hosts such as mice and shrews.

Threats or Challenges

Improve surveillance for tick movement and range expansions.
Improve/Expand tick abatement programs, either independently or by incorporating them into existing mosquito control organizations (reorganize and rename as vector control organizations).
Conduct research into what factors contribute most to tick population establishment and maintenance, and how they can be interrupted (climate, landscape change, host populations).
Conduct research into understanding enzootic cycles of TBDs.
Establish public and private cooperative arrangements to facilitate marketing of existing licensed tick control strategies. This can be done by direct government support of private companies, increasing their profits and thereby incentivize much greater marketing of these technologies.
Establish public, private, and or university partnerships to help translate promising new tick-control strategies and inventions into consumer products and encourage their marketing, especially in endemic regions.
Change the Small Business Innovative Research (SBIR) program, which now includes only three phases, to add a fourth phase, namely, a Phase 4 government purchasing phase that allows direct government investment in successful companies to incentivize marketing to consumers.

Topic 4. Vector competence and vectorial capacity

Vector competence is the ability for a tick species to acquire an infectious microbe, sustain it in its tissues during its development, allow it to proliferate, and transmit it to vertebrate hosts upon which the ticks feed. Only those tick species that meet all these criteria are competent vectors. Other tick species that may acquire infectious microbes during blood feeding but cannot sustain them during their development or transmit these microbes to new vertebrate hosts are not competent. Knowledge of vector competence is important because most tick-borne pathogens that cause disease in humans and animals are limited to a few competent vectors. Detection of a human pathogen in a tick is not sufficient evidence to implicate a tick species in pathogen transmission.

Evidence and findings

Vector competence for different tick-borne pathogens is dependent upon several molecular, biochemical, and physiological factors, the most important of which is the presence of specific receptors that recognize and bind proteins on the surfaces of the microbes. Other factors include 1) the ability of the pathogens to invade the tick host cells, especially the cells of the tick’s midgut, salivary glands, and ovary; 2) their ability to disguise their surfaces to evade recognition and destruction by the tick’s immune system; and 3) the ability of the pathogens to multiply without killing or damaging their tick hosts (so-called fitness cost). Other features that contribute to the tick’s vectorial capacity are the tick’s method of blood-meal digestion, during which hemoglobin liberated from lysed erythrocytes is captured by specialized sites on the midgut epithelium and internalized for intracellular digestive processes. As a result, the midgut presents a relatively permissive microenvironment for the survival of invading microbes (Anderson & Sonenshine, 2014).

Lyme disease tick (Ixodes scapularis). This species is the primary vector of Borrelia burgdorferi, the causative agent of Lyme disease throughout most of the United States and Canada (a closely related species, I. pacificus, is the primary vector in the Pacific coast region). It is also the primary vector for other serious disease-causing pathogens including Borrelia spp, (B. mayonii, B. miyamotoi, B. hermsii, and others) that cause Lyme and tick-borne relapsing fevers, Anaplasmosis, Babesiosis, and Powassan Virus. For reasons of brevity, this review is focused primarily on the Lyme disease agent.

Receptors. For the Lyme disease agent, B. burgdorferi, the presence of a specific receptor, tick receptor for outer surface protein A, abbreviated as TROSPA, enables I. scapularis to serve as the specific vector for this pathogen within its zoogeographic range. It is likely that other, closely related species, for example, I. affinis, also carry this receptor, since these ticks also harbor the pathogen and transmit it to vertebrate hosts. Whether it also occurs in the western blacklegged tick, I. pacificus, is unknown. However, other tick species, for example, Dermacentor variabilis, which often share the same hosts as I. scapularis or I. affinis, are not competent vectors since they lack this receptor.

Factors that facilitate pathogen dispersal within the vector. I. scapularis also has a different midgut receptor, Tre31, which facilitates migration of the Lyme disease spirochetes out of the midgut. The spirochetes also are protected by plasminogen, a vertebrate host-derived protein. Once they have escaped into the hemolymph, a bacterial enzyme (enolase), degrades plasminogen to plasmin (Nogueira, Smith, Qin, & Pal, 2012). Plasmin helps disguise the spirochetes and also helps degrade tick cell membranes and intercellular matrices, further facilitating their migration to the other internal organs (Onder et al., 2012).

Binding to the salivary glands. Although most spirochetes invading the hemolymph are destroyed (Coleman et al., 1997), some reach the salivary glands where they bind to the tick’s SALP15 and other salivary gland proteins that enable them to invade these glands and also protect them from vertebrate host immune reactions (de Silva, Tyson, & Pal, 2009; Hajdusek et al., 2013). These unique molecular features of I. scapularis, believed lacking in other tick species (that is, not genus Ixodes) enhance this tick’s vectorial capacity for the Lyme disease spirochetes.

Factors contributing to hyperendemic U.S. foci. Lyme disease is reported from half the counties in the U.S. but it is much more common in certain areas, namely the northeastern and Midwestern states and the northern part of the Pacific Coast states (Lane et al., 1992). The uneven distribution may be due to differences in the feeding and questing behavior of the northern v. southern ticks and possible genetic differences in the regional populations.

Competent versus incompetent reservoir hosts. In the northern regions, I. scapularis feeds predominantly on highly competent reservoir hosts (for example, white-footed mice and ground feeding birds). In northern California, dusky-footed woodrats and western gray squirrels are the primary reservoirs for Borrelia burgdorferi (Brown & Lane, 1992; Eisen, Dolan, Piesman, & Lane, 2003; Salkeld et al., 2008). The Golden-crowned Sparrow, a non-resident species, could be an important reservoir for B. burgdorferi s.s. (Salkeld & Lane, 2010) and the Rio Grande wild turkey is an important nymph maintenance host (Newman et al., 2015). The majority of immature stages, however, feed on western fence lizards and other lizard species that are incompetent hosts (Lane & Quistad, 1998). In the southeastern and southcentral U.S., these ticks may feed on a wide variety of small mammals that may be competent reservoirs, but the immatures predominantly feed on lizards (Apperson, Levine, Evans, Braswell, & Heller, 1993) that are incompetent or weakly competent (Levin, Levine, Yang, Howard, & Apperson, 1996) or of unknown reservoir status (Clark, Hendricks, & Burge, 2005).
Questing height. Another important reason is questing height (that is, how high above the ground litter ticks climb to find hosts). The risk of encountering questing nymphal ticks, the stage that is epidemiologically most important, is much greater for northern blacklegged ticks than southern blacklegged ticks (Stromdahl & Hickling, 2012) because the latter do not frequently host-seek above the leaf litter (Arsnoe, Hickling, Ginsberg, McElreath, & Tsao, 2015). Many studies have documented how often dragging and/or flagging fails at sampling nymphal ticks in the south even when adult ticks in the area are abundant and are abundantly dragged (Diuk-Wasser et al., 2006; Diuk-Wasser et al., 2010; Goddard, 1992; Goddard & Piesman, 2006). Furthermore, ticks submitted by people in the South include mainly adult ticks and rarely nymphs (Felz, Durden, & Oliver, 1996; Goddard, 2002), whereas in the North both adult ticks and nymphs are submitted (Falco & Fish, 1988).
Western blacklegged nymphs similarly show a trend in their ability to be dragged/flagged, where nymphs in northern California may be dragged much more easily compared with nymphs in southern California (Lane, Fedorova, Kleinjan, & Maxwell, 2013). Western blacklegged ticks also are often found on the tops of downed logs in hardwood forests, where the risk has been calculated as picking up seven per hour by sitting on a log (Lane, Mun, Peribanez, & Stubbs, 2007; Lane, Steinlein, & Mun, 2004). This questing behavior would affect risk of exposure to nymphs regardless of the infection prevalence.
Possible genetic differences. It is possible that there are unrecognized genetic differences between the northern and southern tick populations that affect their behavior and may explain some of the differences noted above (Arsnoe et al., 2015; Van Zee, Piesman, Hojgaard, & Black, 2015). Several studies have also documented bacterial-induced behavioral modifications such as a greater tendency to quest at increased heights. Lane et al. suggest that borrelial infection may increase the locomotor activity and climbing behavior of the nymphal I. pacificus (Lane et al., 2007). This needs to be studied urgently.

Ongoing research outside of endemic foci. Cases of human Lyme disease continue to be diagnosed outside of the foci mentioned above, notably in the Southeastern US; understanding the ecological factors contributing to these cases continues to be a research priority. Some researchers have previously identified high rates of the Lyme disease agent and other related organisms in host-seeking ticks, as well as mammals and lizards in the Southeast (Clark, 2004; Clark et al., 2005). A cryptic cycle of the Lyme disease agent has been proposed in the Southeast, wherein non-human biting ticks such as I. affinis maintain diverse strains of the Lyme disease agent in wildlife, with “bridge vectors” occasionally able to transmit the pathogen to humans (Oliver et al., 2003; Rudenko, Golovchenko, Grubhoffer, & Oliver, 2011; Rudenko et al., 2013). A proposal that has attracted attention from the popular press has been the possibility of lone star ticks transmitting the Lyme disease agent in the south because of “selective compatibility” with the pathogen strains present (Rudenko, Golovchenko, Clark, Oliver, & Grubhoffer, 2016), and the detection of the Lyme disease agent in lone star ticks attached to human Lyme disease patients (Clark, Leydet, & Hartman, 2013) – however, an extensive literature review has since reviewed these studies and found no compelling evidence to support that lone star ticks have the capacity to vector the agent of Lyme disease (Stromdahl et al., 2018), possibly because their saliva is toxic to the agent of Lyme (Ledin et al., 2005).

Western blacklegged ticks (Ixodes pacificus). What is seen here for blacklegged ticks in the eastern US basically mirrors what is seen in western blacklegged ticks in California. There also is a north/south gradient of Lyme disease and risk of contacting nymphal ticks (Lane et al., 2013). For the western blacklegged tick, as with southern populations of the blacklegged tick, there is a predominant use of incompetent lizards compared to reservoir hosts (Lane et al., 1992) (although I. pacificus must use reservoir hosts more often than southern I. scapularis given the higher infection prevalence detected (Salkeld et al., 2008). Thus, overall, there is less B. burgdorferi (and other associated pathogens) cycling in I. pacificus v. northern populations of I. scapularis. although the diversity of B. burgdorferi sensu lato and other pathogens may be just as great or greater (see below). But, furthermore, southern I. pacificus tend to quest lower in the vegetation like southern I. scapularis, thus, again reducing risk of contact with humans.

Nidicolous ticks. Examples in the west include I. dentatus, I. affinis, I. angustus and I. spinipalpis: These Ixodes ticks and their hosts can maintain B. burgdorferi and other pathogens such as Babesia, Anaplasma, HGE and potentially other disease agents (Burkot et al., 2000; Zeidner et al., 2000) in enzootic cycles and perhaps even support a greater diversity of B. burgdorferi sensu lato (Margos et al., 2017). A similar situation occurs (as mentioned above) in the southeastern US, where more nidicolous vectors like I. affinis and I. minor maintain diverse B. burgdorferi sl enzootically (Rudenko et al., 2011; Rudenko et al., 2009). Because the questing behavior of these vectors is such that they rarely contact people (more narrow host ranges and nidicolous behavior of I. spinipalpis), they are considered 'cryptic' vectors, and not 'bridge' vectors. Thus, these vectors may be important for maintaining the pathogen in nature but not for directly transmitting pathogens to humans, although there have been reports that they have bitten humans (Damrow, Freedman, Lane, & Preston, 1989; Durden & Mans, 2016; Scott et al., 2017). They may, however, transmit pathogens to domestic animals if the latter are exposed (for example, in the case of I. affinis and (I. angustus, I. auritulus, and I. spinipalpis) were found questing openly in woodlands in a California study and represents the first collection of large numbers of openly host-seeking I. spinipalpis ticks (Eisen et al., 2006). I. angustus has recently been observed in non-nidicolous mating (Durden, Gerlach, Beckmen, & Greiman, 2018). I. spinipalpis has also been found to quest openly in wooded habitats in Colorado (Burkot et al., 2001) and has been collected from migratory birds during banding studies. The findings that I. spinipalpis quest away from rodent nests and will attach to and infect sentinel mice may be of public health importance. It suggests the potential transmission of the agents of human granulocytic ehrlichiosis, babesia and Lyme disease to other hosts by I. spinipalpis, in regions of the western United States where I. pacificus is not found (Burkot et al., 2001; Burkot et al., 2000).
Dermacentor variabilis and D. andersoni. Tick vectors of disease causing rickettsia also have unique cell surface receptors that enable them to bind these pathogenic microbes. Specific outer surface proteins on the cell surfaces of various rickettsia, e.g, rOmpA, rOmpB, GroEL, GroES, are involved in rickettsial attachment to the tick host cells, for example, to D. variabilis or D. andersoni. When the rickettsiae bind to the cell surfaces, they are internalized in tiny vesicles termed phagosomes (Chan, Cardwell, Hermanas, Uchiyama, & Martinez, 2009). In contrast to non-pathogenic bacteria which are quickly destroyed, rickettsiae lyse these inclusion bodies and escape into the cell’s cytosol. Once free, the rickettsiae hijack the cell’s actin complex by expressing a unique gene, rickA, which enables the bacteria to disseminate throughout the cell and even spread into adjacent cells, thereby multiplying rapidly throughout the tick’s tissues (Welch, Reed, & Hagland, 2012).

Thus, when these ticks ingest Rickettsia rickettsii, the bacteria that causes Rocky Mountain spotted fever, the bacteria can invade the tick host cells, multiply and disseminate throughout the tick’s organs, including the salivary glands and reproductive organs. The vectorial capacity of rickettsia-infected ticks such as D. variabilis is greatly enhanced by transovarial transmission, so that a single infected female can yield thousands of rickettisa-infected larvae and transmit the rickettsiae to numerous small mammals.

Amblyomma americanum. This species is the primary vector of the bacterium, Ehrlichia chafeensis, which causes human monocytotropic anaplasmosis (HMA). E. chafeensis bacteria use a different method for invading the tick’s cell than those described previously, binding to specific receptors in tiny pits on the cell surface known as caveolae. They bypass the more familiar method of cell entry and, once internalized, form specialized enclosures known as morulae in the epithelial cells of the midgut. Within the morulae, the bacteria down regulate reactive oxygen species (ROS) and heat shock protein expression that would otherwise prevent their growth (IJdo & Mueller, 2004). They also control actin synthesis and remodel the cell’s cytoskeleton (de la Fuente et al., 2016). After escaping from the morulae, they exploit a tick-specific salivary protein, P11, which enables them to infect the circulating hemocytes and eventually migrate to the salivary glands (Liu et al., 2011), where they bind by inducing expression of the tick’s Salp16 gene. Understanding how these bacteria exploit the A. americanum-specific proteins and cell regulatory machinery including how they suppress immune-related factors is essential to understanding vector competence for this remarkably complex pathogen-tick host association. The recurring suggestion that lone star ticks are competent vectors of the Lyme disease agent has been recently refuted (Stromdahl et al., 2018); understanding which pathogens ticks are capable of transmitting is critically important so that the appropriate problems associated with a species of tick, such as ehrlichiosis and lone star ticks, can be addressed (Stromdahl & Hickling, 2012). This also allows resources to be appropriately funneled to further investigating unsolved problems, such as the eco-epidemiology of human Lyme disease in the south, and the causative agent of STARI.

Opportunities

Examine how changes in urbanization of the landscape and invasion by non-native shrubs and other plants increase tick-borne disease risk. Recent research suggests that changes in understory structure resulting from vegetative changes helps aggregate ticks and amplifies the prevalence of B. burgdorferi (Adalsteinsson et al., 2018).
Investigate how changes in biodiversity, especially in wild hosts of vector ticks, influence the stability of their current epizootic status and the risk of spread of tick-borne diseases (TBD). Recent evidence suggests that the increasing biodiversity of tick hosts may reduce the maintenance and/or spread of tick-borne pathogens among less efficient reservoir hosts, causing a “dilution effect”. Further study is needed to examine this phenomenon, especially where TBD disease is advancing into new areas (Bouchard et al., 2013).
Investigate how cryptic vectors, tick species that are competent for the various tick-borne agents but which do not normally bite humans can maintain these disease enzootically in the natural environment. Examples include Ixodes affinis, in the southeastern U.S. (Nadolny & Gaff, 2018), which contributes to maintain enzootic cycles of Borrelia burgdorferi in the southeastern U.S. and Ixodes spinipalpis, which plays a similar role in the Pacific coast region. These cryptic vectors cycle B. burgdorferi (S.L.) enzootically. This is why we can detect these pathogens in cryptic ticks and reservoir hosts, even if their infection isn't found in high prevalence in the bridge vectors. Evidence of this phenomenon was described by MacDonald et al. (MacDonald et al., 2017) who showed that infection with the tick-borne pathogens (B. burgdorferi and related genospecies) was not predicted by the abiotic conditions that enhanced populations of I. pacificus, the vector for humans, but rather by the presence of I. spinipalpis and I. peromysci, competent vectors for these pathogens but which only occasionally bite humans. Therefore, these parthogens are still circulated enzootically in the natural environment even when it is not detected in I. scapularis.
Investigate how pathogens affect tick behavior and survivorship.

Potential Actions

Tick Environment-Habitat-Host Research. Fund field studies to identify key factors that contribute to tick presence and abundance, and how they can be interrupted (for example, climate, landscape change, or control of host populations). Particular emphasis should be placed on funding vector surveillance studies that can be compared among sites and over time to improve our understanding of tick species distribution and abundance. Fund research on enzootic cycles that sustain tick-borne pathogens in the natural environment, tick range expansions, and how they can be interrupted. Also identify and investigate Lyme disease vectors and hosts outside of the major Midwest and Northeast Lyme disease foci, to inform the medical community about the true distribution of the Lyme disease pathogen and other tick-borne pathogens, especially in the west region of and the Southeastern United States.
Tick Abatement Programs. Fund stand-alone tick control programs OR incorporate tick control programs into existing local and regional mosquito control organizations (renamed as Vector Control Programs). Also achieve tick abatement by establishing public/private/university partnerships to translate promising new tick-control inventions into consumer products. Also, enhance the Small Business Innovative Research (SBIR) program for government investment in successful companies by adding a government purchasing phase to incentivize marketing and profitability.
Disrupt Tick-Borne Disease Infection and Transmission. Fund research on modern molecular and genetic techniques (for example, gene knockdown, CRISPER/Cas9) to disrupt infection in the tick vector and transmission of tick-borne pathogens to humans and animals. Develop and disseminate vaccines against ticks to prevent the spread of these tick-borne disease agents.
Tick Basic Research. Fund research on pathogen-binding receptors and regulatory factors that enable tick-borne pathogens to infect the tick tissues, proliferate, and survive for transmission to humans and animals.
Genetically Modified Tick Population. Fund research to create a genetically modified tick population, especially for the Lyme disease ticks, Ixodes scapularis and Ixodes pacificus, for release into highly endemic regions. Fund research to study the human dimensions of acceptance/barriers of acceptance of releasing GMO ticks.

Two maps of the United States comparing average minimum January temperatures in 1970 (A) and 2016 (B). Map A shows larger dark-blue area and smaller blue-green and gray areas than Map B.

Figure 2. Maps showing the average minimum January temperatures (°F) in the continental United States: A. 1970; B. 2016. Dark Blue = –10 °F; medium blue = 11–20 °F; light blue = 21–30 °F; blue-green = 31–40 °F; gray = 41–50 °F. Photo credits: Dr. R. Ryan Lash, Traveler’s Health Branch, DGMQ, Centers for Disease Control and Prevention, Atlanta, GA

Votes of Subcommittee Members

Potential actions were presented and discussed by subcommittee members. The wording of potential actions here were voted by subcommittee members and results are presented here.

Vote: The subcommittee unanimously voted yes to accept the list of potential actions for this priority.

Number in Favor	Number Opposed	Number Abstained	Number Absent
10	0	0	3*

*One member was absent from the conference call. Two subcommittee members had to leave early because of schedule conflict.

Priority 2: The Need for Novel Safe and Effective Tick- or Host-Targeted Interventions That Have Been Adequately Validated to Reduce Human Disease Incidence

Despite decades of research evaluating tick- and host-targeted interventions, the incidence of tick-associated diseases of humans in the United States continues to rise. Scientists have identified a variety of bacterial, parasitic, and viral disease-causing agents that are transmitted by multiple tick species that bite humans. New tick-associated pathogens continue to be identified, further implicating vector ticks as an important threat to human health nationwide. Blacklegged ticks, Western blacklegged ticks, lone star ticks, American dog ticks, Rocky Mountain wood ticks, Pacific Coast ticks, soft bodied ticks, Gulf Coast ticks, and brown dog ticks all play important roles as vectors of a variety of human disease-causing agents, with several tick species capable of carrying and transmitting multiple pathogens to humans. A review of the scientific literature and expert presentations has identified the following crucial needs: 1) reducing human exposure to vector ticks, 2) identifying novel methods for controlling ticks and their associated pathogens, 3) further study of methods aimed at blocking transmission of tick-borne pathogens to humans and animals, and 4) adequately validating that these methods can effectively reduce the incidence of tick-borne illnesses using prospective studies that measure both acarologic and human outcomes.

Evidence and Findings

Preventing human-tick encounters can be approached in several ways. Personal protection strategies like performing tick checks or wearing tick repellent are simple to perform and inexpensive, but require daily practice to be most effective. Household-level/peridomestic (backyard) actions, on the other hand, like residential acaricide applications or landscape modifications may require more effort and cost, but require less frequent practice and individual vigilance. Finally, community-level interventions, such as deer management, community-scale tick management, and educational programming, have the potential to make maximum impact on tick populations or disease reduction; these interactions, however, may require widespread public acceptance and may also be limited by municipal or state regulations as well as by manpower required to sustain these efforts.

Personal protective measures. Personal prevention tactics are aimed primarily at shielding the body from tick bites or making ticks easier to detect and remove. Such measures include tucking pants into socks, wearing insect/tick repellent, wearing light colored clothing, performing daily tick checks, bathing frequently, and drying clothes on high heat. Several studies have evaluated the use of personal protective measures for preventing Lyme disease. Many such studies, due to the difficulties in conducting rigorous and meaningful studies, lack data to evaluate their effect for actually preventing human-tick encounters. However, there are a few personal protective measures, including the use of skin and clothing repellent, and performing tick checks and frequent bathing, that have compelling evidence to show they may offer some level of protection against human tick bites and disease.

Skin repellent. Laboratory evaluation of skin repellents suggest that products containing synthetic compounds like 20% or greater DEET, IR3535, picaridin, and synthetic oil of lemon eucalyptus (also known as p-menthane-3,8-diol or PMD), are effective for repelling ticks (Eisen & Dolan, 2016). Several studies have aimed to evaluate repellent use for protecting humans from tick bites and a few have had a protective effect. Studies have demonstrated that an effective repellent applied to skin can protect against Lyme disease (Schwartz & Goldstein, 1990; Vazquez et al., 2008) and was protective against bites from Ixodes ricinus ticks in Sweden (Gardulf, Wohlfart, & Gustafson, 2004).

Increased public demand for botanically-based “natural” repellents has led to mass commercialization of products that do not require EPA-registration and so may be labeled with claims of tick repellent effects with little or no data to support these claims. While, some botanically-based compounds and essential oils, such as geraniol, Chinese juniper oil, and intermedeol, do provide some repellent effects against certain tick species in the laboratory trials, most have short durations of repellent effect (Eisen & Dolan, 2016). In addition, active ingredients commonly found in natural tick repellents such as red cedar oil, soybean oil, and peppermint oil, have little or no published data supporting their use for repelling ticks. However, there is one botanical extract found in grapefruit skin and Alaskan yellow cedar called nootkatone that shows particular promise for preventing tick bites. It has demonstrated repellent properties against blacklegged ticks (Dietrich et al., 2006), is safe and commonly used in food and fragrances, and can be mass produced using a yeast fermentation process. In 2017, CDC entered into a licensing agreement with the biotech company Evolva, to further develop nootkatone as an active ingredient in commercially available repellent products such as repellent soaps and lotions to repel vector mosquitoes. Creating safe formulations of nootkatone, has great potential for effective tick bite prevention in the form of soap, lotion, shampoo, or spray for consumer use.

In general, skin repellents can offer a first line of personal protection against tick bites and several compounds have been identified that effectively repel ticks. Barriers to adopting repellent use should be evaluated. Furthermore, despite increased public interest in using natural products as tick repellents (Gould et al., 2008a), studies evaluating natural products specifically for preventing human-tick encounters or tick-borne diseases are mostly lacking from the scientific literature.

Protective clothing. Clothing that has been treated with permethrin insecticide has shown to protect humans from bites from blacklegged ticks in a laboratory setting (Miller, Rainone, Dyer, González, & Mather, 2011) and from lone star tick bites among outdoor workers in North Carolina (Vaughn et al., 2014). Laboratory testing factory-impregnated permethrin-treated clothing has shown that treated clothing kills and repel blacklegged ticks (Eisen, Rose, et al., 2017). Multiple studies of permethrin-treated military uniforms support the use of permethrin-treated clothing as an effective repellent and/or killing multiple tick species (Evans, Korch, & Lawson, 1990; Fryauff, Shoukry, Wassef, Gray, & Schreck, 1998; Schreck, Mount, & Carlson, 1982; Schreck, Snoddy, & Spielman, 1986). Permethrin-treated clothing has also been shown to have repellent and toxic effects on Pacific coast ticks and Western blacklegged ticks (Lane & Anderson, 1984). Overwhelming evidence suggests that permethrin-treated clothing holds promise as an effective tool for personal protection against tick bites. Unfortunately, its adoption may be limited by public aversion to use of synthetic chemicals as repellents and insecticides (Reid, Thompson, Barrett, & Connally, 2013). Prospective analysis of permethrin-treated clothing on humans for tick bite prevention is warranted and may best be achieved with concomitant study regarding reducing barriers to adopting the use of treated clothing.

Besides treating clothing with pesticide, residents of tick-endemic regions can wear long pants and light colored clothing and they can also tuck pants into socks and shirts into pants. These practices are aimed at preventing ticks from crawling under pant cuffs and by making ticks easier to detect and remove before they can attach to skin. A chemical-free line of clothing was recently developed to be worn under clothing and is meant to protect from tick and insect bites using a tight nylon and Lycra fabric weave with elastic cuffs. It is commonly marketed to sportsmen, law enforcement, and military users. Studies evaluating this clothing for preventing tick bites are thus far lacking, but the clothing has been worn in vector ecology studies for the prevention of arthropod bites by field researchers (Beck, Zavala, Montalvo, & Quintana, 2011).

Tick checks and bathing. Performing bodily inspections for crawling and attached ticks (“tick checks”) has been shown to protect against human disease (Connally et al., 2009a; Vázquez et al., 2008). In addition, bathing or showering after spending time outdoors has shown to increase the probability of finding a tick (Mead et al., 2017) and decrease the likelihood of getting Lyme disease (Connally et al., 2009). Although best practices for effective showering/bathing and tick-checking behavior for disease prevention have yet to be established, these activities are inexpensive preventative measures that can be conducted after spending time in any outdoor environment (not just one’s own backyard), and should continue to be promoted as essential components of any tick-borne disease prevention program. It is also possible that the additional use of a repellent soap (for example, nootkatone) may enhance the protective effective bathing and showering practices by further discouraging tick attachment).

Residential prevention measures. Ticks can be encountered in many locations, including those visited for recreational activities. However, the majority of the more than 300,000+ human cases of Lyme disease acquired annually, particularly in the northeastern and eastern U.S. are thought to result from tick encounters mainly in the peridomestic (residential) landscape, thereby placing the responsibility for disease prevention mostly on individual householders to take either personal and/or household-level actions that reduce tick encounters and tick bites. Exposure to lone star tick and dog tick species across the U.S. can also frequently occur peridomestically, highlighting the need for affordable and effective residential tick control interventions. Residential tick control methods include targeted or broadcast applications of synthetic or botanically-derived acaricides, implementation of biological control agents, and deployment of rodent-targeted tick/pathogen control devices or baits. Additionally, landscape modifications that can discourage ticks and hosts can be implemented in a residential environment. Despite numerous published evaluations of residential tick control interventions, more proof-of-concept population-based studies validating residential tick control methods for the reduction of human-tick encounters and tick-borne diseases are needed.

Synthetic acaricides. Numerous small-scale field studies have demonstrated significant (up to 100%) tick reduction in individual backyards after a single treatment with an effective synthetic, tick-killing product, particularly pyrethroids (Curran, Fish, & Piesman, 1993; Schulze, Jordan, & Hung, 2000; Schulze et al., 2001; Schulze, Jordan, & Krivenko, 2005; Solberg et al., 1992; Stafford, 1991). Based on those studies, residential applications of synthetic chemical acaricides are a commonly recommended public health practice for preventing tick-borne diseases (Stafford, 2004; "TickEncounter Resource Center," 2018; Town of Ridgefield, 2018). But do residential application of effective tick-killing products alone represent the most effective practice for homeowners wanting to protect their families from ticks and disease? Unfortunately for the people who want to prevent tick-borne diseases, that question remains largely unresolved. For example, in a study of 2,727 households in three Lyme disease-endemic states, a single springtime application of an acaricide applied to individual yards in tick endemic communities resulted in an average of 63% fewer host-seeking nymph stage blacklegged ticks compared to untreated yards. In this study, however, the level of vector tick control failed to significantly reduce the number of human tick encounters recorded or cases of tick-borne disease (Hinckley et al., 2016). Reasons for a lack of disease reduction at properties are unclear but there are several possible explanations. It is possible that tick populations must be reduced below a particular (yet unknown) threshold, that reducing exposure risk in one targeted area of the backyard is not adequate to prevent disease (that is, that exposure to ticks may happen outside of the residential environment or in untreated regions of the backyard), and/or that other entomologic-, host-, and human-behavioral factors play a more critical role than we currently understand. It is also possible that the lower than expected reduction in tick abundance occurred due to variation in pest control operator (PCO) application methods, leading homeowners to take fewer backyard precautions. In this case, people believing they were well-protected by the spray, may have inadvertently increased their risk for exposure to ticks.

More studies validating chemical tick control as a means to reduce human tick-encounters and disease are therefore warranted, and may be enhanced by including measurements of human behaviors (both protective and risky) and peridomestic landscape features. Additionally, the development of educational materials for PCOs regarding best-practices for residential acaricide application may help applicators achieve the level of tick control that has been seen in published small-scale field studies.

Finally, although synthetic pyrethroids may offer the longest-lasting, effective backyard control of blacklegged ticks, it is important to note that misuse or poor application can result in harmful environmental effects (for example, toxicity to aquatic vertebrates) or deleterious health consequences (for example, toxic human exposures to pesticides or a false sense of safety). The degree to which well water and other waterbodies on residential properties are affected specifically as a results of pesticides applied for tick control (as opposed to those applied for lawn maintenance and tree care, for example) needs further study. In one survey of Connecticut wells, many herbicides and synthetic pesticides commonly used on lawns and trees were found to leach into groundwater; however permethrin pesticides were not detected (Addiss, Alderman, Brown, & Wargo, 1999). Permethrin readily binds to soil, is not water-soluble (and therefore does not leach well into groundwater,) and degrades slowly in the environment (USDA, 1990; Wagenet, 1985), suggesting that permethrin acaricides can offer long-lasting tick-killing effects, without major concern for groundwater pollution compared to other pesticides. Education about judicious and best practices for using acaricides as a means for tick control would benefit homeowners and pest management officials alike. Education for commercial PCOs about the most effective methods for applying pesticides for tick control is also warranted.

Botanically-based acaricides. Studies have ascertained botanically-based, all “natural” products for controlling ticks. Such natural products are appealing to the public because of perceived low toxicity to humans, pets, and the environment. Pyrethrin soaps, derived from chrysanthemum flowers, have limited residual control because they break down quickly with exposure to light and oxygen (Eisen & Dolan, 2016). Nootkatone from Alaskan yellow cedar and grapefruit essential oil also kills multiple tick species (Flor-Weiler, Behle, & Stafford III, 2011) but also breaks down rapidly, despite efforts to prevent volatilization using a lignin-encapsulation method (Bharadwaj, Stafford, & Behle, 2012). Many other natural products, such as those with rosemary oil or garlic oil active ingredients, have been field tested on ticks with some initial levels of control that were typically not long-lasting, 1-3 weeks post-treatment (Eisen & Dolan, 2016). In light of public interest in natural products for tick control, further work towards formulating botanically-based acaricides to make them more persistent in the environment is needed before such products can reliably be promoted as an effective means for controlling residential tick populations.

Biological control of ticks. Laboratory studies have identified several species of naturally-occurring soil-dwelling bacteria and fungi that are capable of killing several species of ticks (Kirkland, Westwood, & Keyhani, 2004). Field studies evaluating tick-killing Metarhizium fungi formulations have had varying but promising results for controlling host-seeking blacklegged ticks (Bharadwaj & Stafford III, 2010; Stafford & Allan, 2010). Metarhizium is of particular interest because of its low non-target effects (Ginsberg, Bargar, Hladik, & Lubelczyk, 2017). It should be noted that application timing and prerequisite environmental conditions needed for optimal tick control may be limiting factors to using entomopathogenic agents (Eisen & Dolan, 2016). Field studies have yet to confirm consistent results for biocontrol of ticks. Furthermore, no published studies have evaluated tick-killing biocontrol agents for reducing human-tick encounters or human tick-borne illnesses, and the high cost of treatment could limit the adoption of this treatment option by homeowners.

Rodent-targeted approaches for tick control Approaching tick control at the level of rodent reservoir hosts for tick-associated pathogens is meant to kill immature ticks on their host, interrupting the cycle of pathogen transmission between ticks and rodent reservoirs. One rodent targeted approach, Damminix Tick Tubes, seeks to kill ticks on rodents by providing permethrin-treated cotton for nesting material. Studies evaluating Damminix tubes have shown varied effects, ranging from a substantial reduction of ticks on mice in a residential setting in Massachusetts (Mather, Ribeiro, Moore, & Spielman, 1988), to little or no effect in the same region (Daniels, Fish, & Falco, 1991; Ginsberg, Butler, & Zhioua, 2002; Stafford III, 1991). It is possible that differences in small mammal diversity and abundance in the treatment areas greatly affect use of the tubes by possible reservoir hosts. Furthermore, the use of permethrin-treated cotton with a similar approach in the western U.S. did not control Western blacklegged ticks on dusky-footed woodrats (Leprince & Lane, 1996).

Another rodent-targeted intervention focuses upon the passive application of tick-killing fipronil onto mice and chipmunks as they visit the Tick Box™ Tick Control System (formerly Select TCS™ and MaxForce™ Tick Control systems). Field studies evaluating the boxes have provided consistently favorable outcomes. A residential field trial of bait boxes at closely-situated properties in a small Connecticut community resulted in both a significant reduction of ticks parasitizing mice as well as a reduction of infected host-seeking ticks in subsequent years (Dolan et al., 2004). A subsequent study showed that bait box use significantly reduced host-seeking blacklegged tick nymphs in the two years after boxes were deployed (Schulze, Jordan, Williams, & Dolan, 2017). Lastly, a recently study conducted in Connecticut sought not only to reduce entomologic risk factors, but also human-tick encounters and incidence of tick-borne diseases by conducting a randomized, placebo-controlled, blinded study of bait box use at 625 residences in Lyme-endemic communities. Results of this study have not yet been published, but will provide much needed data regarding the utility of using bait boxes not only for reducing ticks and tick infection rates, but as a means of disease reduction. The use of bait boxes is somewhat limited by their inability to treat a diversity of reservoir hosts including birds and insectivores and by their high cost to install ($50 per box, averaging 15 boxes per property = $800 per property) and maintain on an annual basis (Interlandi, 2018). Nonetheless, results of bait box field trials to date have yielded promising results. More study is needed to evaluate the utility of this measure for reducing human disease tick-encounters.

Rodent targeted transmission blocking vaccines. A reservoir-targeted Borrelia burgdorferi OspA oral vaccine reduced infection in the field in a Lyme endemic area in both white-footed mouse reservoir hosts and blacklegged ticks (Gomes-Solecki, 2014; Richer et al., 2014). Oral vaccination of white-footed mice with Borrelia burgdorferi OspA containing bait protected uninfected mice from infection and reduced transmission to ticks infesting mice infected prior to oral immunization (Voordouw et al., 2013). Reservoir targeted vaccine in the field over the five-year trial resulted in cumulative anti-OspA antibody production and significant reduction of tick infection over the course of the study (Richer et al., 2014). These studies support the use of a reservoir targeted vaccine as an effective tool to reduce Lyme spirochete infection in blacklegged tick nymphs, the primary vector of Lyme bacteria to humans. It should be noted, however, that rodent vaccination is limited to a single pathogen, and this methodology will not reduce tick abundance. Thus, another approach could be small mammal-targeted anti-tick vaccines (Bensaci, Bhattacharya, Clark, & Hu, 2012), which could reduce tick abundance as well as break enzootic cycles given their importance as reservoirs.

The effect of any reservoir-targeted intervention on reducing the density of infected nymphs depends on the relative contribution of mice (or other targeted rodent species) for feeding and infecting ticks. The relative importance of mice in turn may vary spatially and temporally depending on their abundance and that of other wildlife hosts comprising both reservoirs and incompetent hosts. Thus, replicate studies should be conducted to understand how the effect of host-targeted interventions vary in different ecological contexts. Furthermore, any intervention that acts as a selection factor on ticks or pathogens may select for resistance; research is therefore required to better understand the population biology of ticks and pathogens (for example, immigration/emigration rates) to predict the evolution of resistance under different selection scenarios and ecological contexts.

Landscape modifications. Health education efforts have long promoted the use of landscape modification tactics for preventing TBD. Specifically, homeowners are encouraged to create a “tick safe zone” where families can recreate with a low risk of exposure to vector ticks (Stafford, 2004). Such landscape approaches include measures like choosing ornamental plants that are unlikely to attract deer, keeping potential rodent breeding sites far from the home (for example. log piles), and recreating in the lawn far from forested edges where ticks are more likely to be abundant. There is some evidence that deer exclusion fencing can reduce backyard tick populations as well (Daniels, Fish, & Schwartz, 1993). Studies evaluating the use of landscape modification specifically for reducing human exposures to ticks are lacking. With a recent public interest in mulch-mowing (mowing lawns without leaf removal) for increased turf and pollinator health, there are questions about how such practices may affect backyard survival of some tick species. Nonetheless, landscape modifications may offer a pesticide-free option for reducing backyard risk for tick exposure, and warrant further study.

Community-level prevention

Deer removal. White-tailed deer play an important role providing blood meals for adult stage blacklegged ticks as well as lone star ticks. Experimental removal of deer in island settings of the northeastern U.S. have resulted in reductions of blacklegged tick populations (Rand, Lubelczyk, Holman, Lacombe, & Smith, 2004; Wilson, Telford, Piesman, & Spielman, 1988). On mainland settings, there are no studies evaluating experimental deer removal for tick population control, and the threshold of deer reduction required to control ticks is yet unclear. It also seems likely that even complete elimination of deer will not completely control tick populations, as adult ticks can find alternative hosts on which to feed (Fish & Dowler, 1989). Further studies are needed to better understand how deer removal can affect tick abundance and tick infection rates, particularly on mainland settings.

USDA 4-Poster devices. Several studies evaluating topical application of tick-killing pesticides on white-tailed deer using U.S. Dept. of Agriculture 4-poster deer feeding stations resulted in significant reductions in host-seeking lone star and blacklegged ticks several years after deployment (Brei et al., 2009; Carroll et al., 2003; Pound, Miller, George, & Lemeilleur, 2000). However, deployment of 4-poster devices is currently limited by municipal and state regulations, particularly as they apply to health concerns about feeding wildlife, increasing the transmission of pathogens in deer like chronic wasting disease and bovine tuberculosis, and human safety. The possibility exists to replace corn feed with a salt lick in these devices. Such a device had been patented by Kenneth Liegner, MD before the 4 Poster Device was available. It is yet unclear how feeding salt will affect how deer feeding stations impact tick populations, however. Furthermore, pesticide resistance as a result of widespread use of 4-poster is also a consideration for future use (Eisen & Dolan, 2016). Nonetheless, use of 4-poster devices offers an effective approach to broad scale tick control in tick-endemic areas.

Lizard removal. In the western US, experimental removal of western fence lizards that play an important role as hosts to immature western blacklegged ticks resulted in fewer Lyme bacteria-infected ticks in the region (Swei, Ostfeld, Lane, & Briggs, 2011). Although the lizards are not competent reservoirs hosts for Lyme bacteria, they do play an important role in the tick life cycle, providing further evidence that a broad-scale approach to host population control has potential to affect entomologic risk for Lyme disease.

Educational programs. Another integral component of community-based prevention is the implementation of public education programs for preventing tick bites, controlling tick populations, and recognizing symptoms of tick-borne illnesses. Educational needs and barriers are discussed in detail in Priority 5.

Integrated tick management. Only recently have tick-control efforts focused on application of multiple methods for controlling ticks in an integrated tick management (ITM) approach. ITM approaches can include targeting multiple life stages (for example, tick larvae parasitizing mice and host-seeking nymphal stage ticks), can result in reduced pesticide loads dispersed into the environment, and can be applied at different spatial scales (individual yards vs. neighborhoods, communities). ITM may also resulted in a slower development of pesticide-resistant ticks. A few studies have applied integrated methods for reducing tick populations, including combinations of perimeter sprays, bait boxes, and deer treatments, which have all resulted in a reduction of tick abundance, and in some cases, in a reduction of tick infection prevalence (Schulze et al., 2008; Schulze et al., 2007; Williams, Stafford, Molaei, & Linske, 2018). Given the promising approach of using ITM, there are currently three studies ascertaining the use of ITM for preventing blacklegged tick-associated diseases at single vs. clustered residential properties (www.backyardtickstudy.org), in neighborhoods (www.tickproject.org), and in communities (ARS Area-Wide Integrated Tick Management Study). Two of these three studies attempt not only to measure a reduction of entomologic risk factors, but also to ascertain whether an ITM approach can ultimately result in a reduction of human-tick encounters and in human disease incidence.

Novel tick control methods on the horizon

TickBot. A novel robotic device known as TickBot travels by following a guide wire, dragging permethrin-treated fabric behind it. It has been shown to reduce questing lone star ticks for 24 hours in the regions where it has been tested (Gaff et al., 2015), and is currently being evaluated for its effectiveness at controlling blacklegged ticks. TickBot has the potential to control ticks in backyards or along public trails, but may require multiple visits and maintenance to sustain tick control using this methodology. Further study of this new device is warranted.

Novel genetic approaches. The development of new genetic and molecular tools is allowing for novel generation of tick-borne disease prevention tools, including methodologies aimed at creating genetically modified organisms or disrupting gene expression in ticks and reservoir hosts.

The concept of releasing transgenic organisms (for example, animals that have modified genetic material, also known as genetically modified organisms or GMOs) has long been discussed and tested for controlling populations of vector mosquitoes and crop pests, and may also offer great promise for effective vector control in regions where ticks are hyper-abundant. Transgenic ticks are currently in development at the University of Nevada-Reno, with a goal of using a new genetic tool known as CRISPR to disrupt insulin signaling, which plays a role in nutrient metabolism and therefore parasite survival in ticks (Feinberg, 2018). CRISPR technology is also being explored by researchers at the Massachusetts Institute of Technology for genetically engineering white-footed mice to become reservoir-incompetent for Lyme bacteria and other tick-borne pathogens (Harmon, 2016). The use of GMOs may offer great possibility for eradicating blacklegged ticks in hyper-abundant areas, in contrast to just control as achieved by using other technologies.

RNA interference (RNAi) is one powerful reverse genetic approach used to determine gene function and to silence tick genes (Fire et al., 1998). The use of RNA interference in ticks continues to increase from 30 early studies using this tick gene silencing technology to assess interactions at the tick-pathogen interface (de la Fuente & Contreras, 2015). A far more extensive reporting of RNA interference studies in ticks is that of Galay et al (Galay et al., 2016). RNAi works well to silence genes within tick tissues. These studies of ticks encompassed the topics of pathogen acquisition/transmission, protective antigens, structural and metabolic proteins, reproduction, digestion, and roles of salivary gland proteins (Galay et al., 2016). This technology can be used to assess potential targets for acaricides, repellents, anti-tick vaccines, and other strategies to disrupt tick physiological processes, and tick-borne pathogen interactions within the tick vector and at the host interface. It can potentially be used to disrupt virus infection within the tick (Hajdusek et al., 2013).

RNAi applied experimentally to silence tick genes is labor intensive, and slow to yield results (Lew-Tabor et al., 2011; Tuckow & Temeyer, 2015). Broad application of an RNA interference-based approach to tick and tick-borne disease control would require significant technological advances in delivery and targeting systems, as well as consideration of any off-target impacts. Practical wide scale application technologies and developing ways of prolonging the mode of action of RNA interference in the tick need to be investigated because this tool has great potential to help us discover molecules essential for controlling ticks and their ability to transmit disease-causing microbes.

Other emerging technologies. There are several potential technologies for tick/pathogen control and tick bite prevention that may have promise for reducing the incidence of human tick-borne diseases in the U.S. and warrant additional study to validate their effectiveness. Such technologies include the aforementioned nootkatone repellent and tick killing products and salt lick-baited deer feeding stations, emerging genetic tools and robotic tick control devices. Other possible technologies and methodologies that have not yet been extensively-evaluated for tick-borne disease prevention include drone-assisted area-wide tick management, controlled burning as a means of tick management, and encouraging populations of natural enemies and predators of ticks and their hosts. In addition, the relationship between plant dynamics and entomologic risk for tick-borne diseases could also be further elucidated (such as in the case of oak acorn masting in the northeastern U.S., and Sudden Oak Death in the western U.S.). Finally using semiochemicals as a means to arrest and kill vector ticks is a methodology that warrants further study. For example, one product in development, Splat TKTM, utilizes a novel attract-and-kill approach to minimize the amount of acaricide by combining it with a pheromone specific to blacklegged ticks. The pheromone causes the ticks to remain in contact with the acaricide, causing a lethal dose to be delivered. Technology such as Splat TKTM that use semiochemicals synergistically with existing vector control methods may offer options for mitigating concerns about toxicity (to the environment, animals, and humans), as well as pesticide resistance.

Opportunities

Decades of tick management research efforts have not yet resulted in a “silver bullet” approach to controlling tick populations or pathogen prevalence, or mitigating human tick-borne disease. Our extensive review of the scientific literature has allowed us to identify specific knowledge gaps and challenges for managing ticks and human disease risk in tick-endemic areas. Specifically, future opportunities for research include:

Understanding best practices for using personal protective measures, including the role of human behavior in human-tick interactions.
Evaluating minimal-risk “natural” pesticides and repellents to identify effective products.
Determining best practices for application of effective pesticides with limited environmental impact and public acceptability.
Investigating novel tools, including molecular technologies, for controlling ticks and impacting pathogen prevalence in ticks and animal reservoir hosts (for example, rodent vaccination, transgenic ticks, RNAi, semiochemical control, and so forth).
Validating the effectiveness of tick control measures for reducing human disease risk (for example. prospective, randomized, placebo-controlled human studies).
Educating community members and pest management operators about best practices for personal protection and tick control.
Investigating the role of landscape modification on tick exposure risk and the relationships between landscape dynamics and tick population dynamics.
Applying integrated tick management tools that have the greatest effectiveness for vector control while minimizing environmental impacts and pesticide resistance.
Understanding entomologic risk for tick-borne diseases at varying spatial scales, from backyard and recreational exposures to neighborhood and community approaches.
Investigating improved community-level vector-control strategies (for example, mosquito control district model)
Engaging with private and public partners to encourage development of out-of-the-box ideas for novel tick control and tick bite prevention in endemic regions.

Threats or Challenges

We have identified several challenges and threats to tick control and tick bite prevention efforts, often despite overwhelming scientific data that support safety or effectiveness:

Skepticism and public distrust of chemical pesticides and repellents
Social acceptability of deer management
Willingness to pay for effective tick-control measures
Lack of funding for large-scale neighborhood/community/area-wide studies
Increased pesticide resistance concerns, pollinator health concerns
Declining public health entomology workforce and lack of funding to support employment to sustain continued tick-borne disease prevention research
Barriers to municipal/local vector-control efforts specifically aimed at ticks

Potential Actions

Further study of proven tick-control measures (as evidence by lab and field studies) at the scale of population-based prospective studies to validate these measures for preventing human diseases
Field-trials and human studies evaluating effective natural tick-control products and natural skin repellents for tick control, tick bite, and human disease prevention (for example, use of skin lotions, soaps and repellents or tick control products containing nootkatone or other botanically-based ingredients)
Assessment of integrated tick management tools that have the greatest effectiveness for vector control while minimizing negative environmental impacts (such as groundwater pollution and non-target effects) and pesticide resistance
Continued study and development of promising novel tick- and pathogen-control measures, including molecular technologies, for impacting pathogen prevalence in ticks and animal reservoir hosts (for example, rodent vaccination, transgenic ticks, RNAi, semiochemical control, and so forth), and promotion of private and public partnerships to engage industry and other professionals to develop novel and effective products that can be marketed to the public for tick-borne disease prevention
Assessment of barriers to public adoption of prevention practices (for example, studies evaluating willingness-to-pay, social acceptability, environmental concerns, behavioral preferences, and knowledge, attitudes, and perceptions of prevention measures)

Votes of Subcommittee Members

Potential actions were presented and discussed by subcommittee members. The wording of potential actions here were voted by subcommittee members and results are presented here.

Vote: The attending subcommittee members unanimously voted yes to accept the list of potential actions for this priority.

Number in Favor	Number Opposed	Number Abstained	Number Absent
10	0	0	3*

*One subcommittee member was absent from the conference call. Two other subcommittee members had to leave early because of conflict of schedule.

Priority 3: The Need for Improvements in National Human Tick-borne Disease Surveillance and Reporting, and the Potential Role of Other Data Sources and Patient Registries in Defining National Disease Burdens and Trends

Public health surveillance is the ongoing, systematic collection, analysis, interpretation, and dissemination of data regarding a health-related event for use in public health action to reduce morbidity and mortality and to improve health (German et al., 2001). The 10th Amendment to the U.S. Constitution states that “The powers not delegated to the United States by the Constitution, nor prohibited by it to the States, are reserved to the States respectively, or to the people ("Tenth Amendment: Reserved Powers,").” Given that “public health” is not mentioned explicitly in the Constitution, the primary authorities and responsibilities for public health actions, including public health surveillance, belong to state governments.

Public health surveillance is useful to appreciate whether a disease is common or rare, to gain a general understanding of who is affected by the disease, and to monitor how the disease changes over time. Traditional public health surveillance is a passive process whereby healthcare providers and laboratories report positive diagnoses or laboratory tests to public health agencies; passive surveillance is known to have limitations, regardless of the disease under surveillance. It is unrealistic to expect that every case of disease under public health surveillance will be ascertained, especially when the disease is common. As with Lyme disease, when there are lag times for diagnostic testing, reporting and investigation, there is often significant delay from the time a patient becomes ill to when the disease is reported to public health agencies. Hence, it is also not possible to expect real time reporting of diseases as they occur or even as they are diagnosed clinically.

Notifiable diseases are those for which regular, frequent, and timely information regarding individual cases is necessary for disease prevention or control. Diseases are deemed nationally notifiable and surveillance case definitions are developed by the Council of State and Territorial Epidemiologists (CSTE). The intent of developing a surveillance case definition is to ensure that cases are counted the same way by all jurisdictions for public health purposes; surveillance case definitions include clinical, diagnostic and epidemiologic criteria that must be met in order for a case to be counted. Surveillance case definitions can have inherent limitations, such as when there are vague clinical manifestations (such as nonspecific signs and symptoms) and/or if there are limitations in the available diagnostic tests. Surveillance case definitions are not developed to guide clinical diagnosis or management, nor should they be used for those purposes.

When a disease is first considered for surveillance, or if changes are necessary to an existing case definition, a proposal for a surveillance case definition is drafted and presented to the CSTE membership by active CSTE members, typically state health department surveillance personnel familiar with and responsible for that particular disease. Proposed case definitions are discussed and modified, and ultimately voted on with one vote per state or U.S. territory. Currently, Lyme disease, babesiosis, anaplasmosis, ehrlichiosis, tularemia, and spotted fever rickettsioses are nationally notifiable tick-borne diseases ("CSTE List of Nationally Notifiable Conditions," 2013).

Given that public health surveillance is a state responsibility, it is important to note that the determination for whether a disease is reportable in a given state or territory lies with that jurisdiction, regardless of whether the disease is deemed nationally notifiable. A disease might be nationally notifiable, but not reportable in a state, as illustrated by Lyme disease which is nationally notifiable but not reportable in Hawaii (Health, 2013). This might happen if the disease does not occur naturally in that jurisdiction or there are other diseases considered of greater public health importance by that jurisdiction. States generally designate which diseases are reportable in state law or regulation, although how diseases are deemed reportable varies across jurisdictions.

Public health surveillance is conducted locally; cases of disease are reported to the local or state health department by healthcare providers, diagnostic laboratories and whoever else is required by law to report in that state. Reports are investigated by public health surveillance personnel and a determination is made as to whether the case conforms to the surveillance case definition and should be counted. If the case is counted at the local or state level and is nationally notifiable, the case is reported to the federal Centers for Disease Control and Prevention (CDC). The CDC analyzes the data to describe the patients affected by the disease (for example, young vs. old) and where the disease occurs (that is, does it occur regionally or is it distributed across the whole of the U.S.). Cases counts for notifiable diseases are published regularly (weekly or annually, depending on the disease) in the Morbidity and Mortality Weekly Report (CDC, 2017b) and summaries describing the surveillance findings are published as updated surveillance data accumulate (Schwartz, Hinckley, Mead, Hook, & Kugeler, 2017).

As the number of cases of tick-borne disease (Lyme disease in particular) has increased over time, the burden on the public health system for investigation has also increased. Further, given that no immediate community intervention is implemented when most tick-borne disease cases are detected, such as might be done for diseases with other transmission mechanisms such as foodborne or by direct contact , many public health jurisdictions have lowered the priority of conducting tick-borne disease (specifically Lyme disease) surveillance (Rutz, Hogan, Hook, Hinckley, & Feldman, 2018). Because disease surveillance (specifically Lyme disease surveillance) is conducted specific to each jurisdiction’s resources and perceived needs, surveillance practices can be variable across jurisdictions and underreporting of cases is common. Recent estimates, as determined through systematic analyses, of the actual number of cases of Lyme disease in the United States range from eight to ten times the number of cases than captured through traditional public health surveillance (Hinckley et al., 2014; Nelson et al., 2015). This section addresses three issues surrounding public health surveillance of tick-borne diseases, specifically:

How can surveillance practices be improved and standardized from state-to-state and from year-to-year?
What is the role of other data sources and patient registries in defining national disease trends?
Would the Council of State and Territorial Epidemiologists (CSTE) consider other surveillance data than case numbers?

Evidence and Findings

The committee identified improvements in national human tick-borne disease surveillance and reporting, and the potential role of other data sources and patient registries in defining national disease burdens and trends as a priority. Understanding the true burden of disease in a population and knowing who the disease affects are essential for the allocation of resources and for targeting public health interventions.

Public health surveillance is a “passive” process, whereby healthcare providers and laboratories report positive diagnoses and/or laboratory tests to public health agencies. On receipt of a positive report, public health personnel conduct investigations to collect additional information and classify the cases according to standard case definitions. Passive surveillance systems work best for diseases that are rare, involve hospitalized patients, or for which there are definitive diagnostic laboratory tests. Passive systems work less well for common diseases that are typically diagnosed in outpatient settings and for which there are no definitive laboratory tests (Cartter, Lynfield, Feldman, Hook, & Hinckley, 2018). Lyme disease, the most commonly reported vector-borne disease in the United States, falls into the latter category, and underreporting of Lyme disease is well documented and generally acknowledged (Cartter et al., 2018; Rutz, Wee, & Feldman, 2018; Schiffman et al., 2018; White et al., 2018).

There are many contributing reasons as to why Lyme disease is underreported, including the complexity of the national case definition and testing criteria (Cartter et al., 2018; CDC, 2017a; Rutz, Wee, et al., 2018; Schiffman et al., 2018; White et al., 2018). Other reasons include the effort required for healthcare providers to report and the burden on public health practitioners to conduct public health investigations for surveillance purposes. Substantial underreporting can obscure trends and may inhibit the ability to evaluate the effectiveness of interventions. Underreporting can also lead to a lack of awareness on the part of the public and the healthcare community that tick-borne diseases are a risk in a particular geographic area. This lack of awareness of Lyme and other tick-borne diseases prevents practitioners from considering them when generating differential diagnoses. The most extreme consequence of this is the possibility for disease to go unrecognized and therefore untreated, with potentially fatal consequences

Fatal Lyme Carditis Case Study. Seventeen-year-old Joseph Elone, an honor student at Poughkeepsie (NY) High School, died suddenly in August, 2013, after having been sick for about a month with flu-like symptoms. Early in his illness, the young man tested negative for Lyme disease – however, this test was administered too early to provide serologically relevant results. The patient was also dark skinned, and no erythema migrans rash was visible. Joseph had recently returned from a 2-week exposure to tick habitat during the peak of Lyme disease season, but was not prescribed antibiotics. After he died, health officials initially suspected tick-borne Powassan virus; that has since been ruled out and it was determined that Joseph in fact had disseminated Lyme disease. An autopsy showed Lyme spirochetes in his liver, heart, lungs and brain. The official cause of death was Lyme carditis—a condition which interferes with electrical signals in the heart. It is possible that the surveillance case definition was used to rule out this less common presentation of Lyme disease, based on the negative serologic test. Had antibiotics been prescribed, this young man’s life might have been saved, (Yoon et al., 2015).

To add complexity to the concerns regarding underreporting, tick-borne disease reporting and public health investigations vary from state to state, further complicating the ability to make comparisons, monitor trends and detect emergence of the disease. It is therefore important that all states report Lyme and other tick-borne diseases similarly.

A review of the literature regarding public health surveillance for Lyme disease documented underreporting and provided estimates of the actual number of cases of Lyme disease (that is, the true burden of illness) that are eight to ten times the number captured by public health surveillance (Figure 3). A recent survey assessed tick-borne disease laboratory testing practices at large commercial laboratories, and the data were used to estimate the number of infections among patients from whom specimens were submitted. The authors estimated 240,000-444,000 infected source patients in 2008 (Hinckley et al., 2014). Another recent retrospective analysis used data from a nationwide health insurance claims database. That analysis yielded comparable results to the earlier study: the estimated Lyme disease incidence is approximately ten times that reported through public health surveillance (estimated 329,000 (95% credible interval 296,000–376,000) Lyme disease cases annually as compared to approximately 36,000 cases reported in 2013 through public health surveillance) (Nelson et al., 2015).

Other studies have assessed alternative approaches to Lyme disease surveillance. In New York State, a system was developed to estimate county-level Lyme disease cases based on a 20% sample of positive Lyme disease laboratory reports, thereby reducing the burden on the public health system to conduct public health investigations. The system was determined to be accurate and efficient in estimating the true number of cases and the demographic and clinical characteristics as captured by public health surveillance (Lukacik, White, Noonan-Toly, DiDonato, & Backenson, 2018). Similarly, 20% and 50% retrospective samples of Lyme disease reports in Massachusetts and Minnesota, respectively, generated estimated counts of Lyme disease that were similar to observed counts as captured through traditional public health surveillance. Moreover, demographic and clinical characteristics of cases as ascertained through sampling were not significantly different from those captured through traditional public health surveillance (Bjork, Brown, Friedlander, Schiffman, & Neitzel, 2018).

Other alternative surveillance approaches have assessed the use of administrative datasets to complement or replace public health surveillance. These approaches relied on using diagnostic codes, assigned for a patient’s medical encounter for the purposes of charging for services, to identify cases of Lyme disease. There were varying degrees of success (Clayton, Jones, Dunn, Schaffner, & Jones, 2015; Robinson, 2014; Rutz, Hogan, et al., 2018) across these approaches, and there might be other viable approaches that have yet to be explored. Underlying these approaches, however, is the reliance on standard codes that are typically part of an electronic health record and transmitted electronically. A recent assessment of medical practices that see Lyme disease patients demonstrated that most practices were able to electronically search records using specific diagnostic and billing codes, suggesting that automated, electronic reporting of cases to public health agencies is possible and could ease the reporting burden on providers (Thomas et al., 2018).

Finally, disease registries might serve as another complementary source of data to understand the number of individuals affected, characterize those affected and examine the risk factors for disease. Registries are likely more useful for rare diseases or rare manifestations of disease (for example, Lyme carditis), and would require strict criteria for inclusion. One possible model to consider for the development of a tick-borne disease registry is the congressionally mandated national registry for amyotrophic lateral sclerosis (ALS, also known as Lou Gehrig’s disease). The National ALS Registry uses administrative and self-reported data to identify cases instead of relying on provider or laboratory reports, as does traditional public health surveillance (Mehta et al., 2018).

Opportunities

The evidence we reviewed allowed us to identify potential opportunities for improving surveillance of tick-borne diseases. Chief among the opportunities is using multiple approaches to build a more robust understanding of the actual number of cases and risk of disease. “Burden of illness” studies estimate the actual number of cases by using alternative datasets and analytic methods; the results of these “burden of illness” studies can be used to complement traditional public health surveillance and present a more complete picture of the impact of the disease in a community, region, or entire country. CDC could report on its website and in written publications (for example, the Morbidity and Mortality Weekly Report) reported case counts from traditional public health surveillance in addition to estimates of the actual number of cases of disease based on “burden of illness” studies such as those conducted by Hinckley and Nelson. If adequate resources were allocated to conduct “burden of illness” studies on a regular, periodic basis (that is, annually) using consistent methodology, these estimates could be used to assess trends over time. These efforts to present a more complete picture of the impact of tick-borne disease will be for naught, however, if they are not accepted by the authoritative public health agencies, included in formal reports of disease incidence, and considered when making decisions about resource allocation.

Alternative surveillance approaches could also be used to ease the burden of tick-borne disease surveillance while providing valuable insights into disease incidence. Efforts could include systematic sampling of tick-borne disease reports for subsequent public health investigation (for example., a 20% sample of all reports are investigated, as implemented in New York State) or laboratory-only reporting. Disease registries, maintained by the public health community, healthcare systems, healthcare providers, patient advocacy groups or others, may also serve as a source of data on disease incidence. Disease registries might be particularly useful for determining the burden of illness due to rare tick-borne diseases or less common manifestations of tick-borne disease, such as Lyme carditis. Alternative approaches should include validation of these methods and the development of procedures (for example, generation of multiplication factors) to estimate true burden from these alternative approaches. Public health authorities, such as the CSTE and CDC, should accept alternative approaches to traditional public health surveillance as accepted mechanisms for characterizing how much disease occurs.

Alternative datasets (for instance tick surveillance data) can be used to build a more robust picture of risk. Data to consider for addition (and some may be of limited availability): tick surveillance data, tick testing data, companion animal tick-borne disease testing data; medical claims data; weather data; other patient data sources; data from other federal agencies including the Department of Defense. These data are frequently collected and published in white papers and in the peer-reviewed literature and provide valuable context for human case data and enhance our understanding of changing tick-borne disease risks. Considerations for this action include a) the need to determine how to integrate these datasets for a more complete picture of disease risk; b) the need to package and communicate the risks for consumption by the general public. By overlaying datasets, powerful visuals are unlocked than can tell more informative stories about risk than human surveillance data alone. For examples, see Figure 4 and the interactive map of Lyme disease risks in California (available at https://www.arcgis.com/apps/SocialMedia/index.html?appid=91d8639cf4d74b2db6cf36415f4bc9a1).

Finally, leveraging the growing use of electronic health records and the electronic exchange of health data (for example, through Health Information Exchanges) to automate, and thereby simplify, disease reporting is an opportunity to improve tick-borne disease surveillance. The education of healthcare providers could potentially improve tick-borne disease surveillance. Education could include which tick-borne diseases are notifiable, diagnostic test interpretation, and the obligation to report to public health agencies. The opportunity to educate healthcare providers could also be used to reinforce that the surveillance case definition comprises a set of criteria for how to count cases by public health agencies, and should not be used for diagnostic or clinical management purposes. Healthcare providers could be incentivized to report by ensuring that deliverables (such as annual updates from the CDC or CSTE with updated risk maps, recent range expansions, or updated diagnostic information) are made available to providers in a timely fashion. An interactive online risk index based on the location of where the tick bite was acquired would also take reported information and provide a useful tool to providers identifying tick-borne disease in their communities.

Threats or Challenges

Most tick-borne disease investigations at local health departments are triggered on receipt of a positive laboratory test. Currently, the high volume of cases of tick-borne disease, in particular Lyme disease, is such that public health investigations are limited and at times not conducted at all. However, the sheer volume of cases is not the only reason accounting for underreporting. When there are competing public health priorities for which immediate interventions can be taken, tick-borne disease investigations will often fall in priority.

Lyme disease is most typically diagnosed in outpatient settings, and understanding and interpreting the diagnostic laboratory tests is challenging even for medical professionals. Thus, patients might not be diagnosed appropriately (false positive diagnoses and false negative diagnoses might occur) or a provider may fail to recognize a situation that warrants testing or reporting, especially when a patient resides in a locality that does not appear to be at risk for Lyme disease based on reported surveillance case counts. Moreover, early Lyme disease (for instance patients with an erythema migrans rash) can (and should) be diagnosed clinically (also considering other factors such as tick exposure, tick habitat exposure, seasonality of the disease, and travel history) and not rely on diagnostic tests which are often negative early in the course of disease, as the immune system is still mounting its response. Thus, reporting of clinically diagnosed cases relies entirely on the healthcare provider, a notoriously weak link in the surveillance continuum, as there will not be a laboratory result sent to the health department.

There is also likely underreporting of rarer or lesser-known tick-borne diseases (that is, ehrlichiosis, some rickettsioses, tickborne relapsing fever) that may present with nonspecific signs (for example, “summer flu”) and might not ever get diagnosed. Because underreporting results in fewer numbers of cases reported in official surveillance summaries and reports, when erythema migrans rashes (or other Lyme disease clinical manifestations) occur outside of identified endemic states, they are often dismissed because providers do not believe that Lyme disease is present in these areas. The lack of awareness of the risks of tick-borne diseases by both the public and the healthcare community can have potentially fatal consequences.

As has been noted in the report, public health surveillance is the ongoing, systematic collection, analysis, interpretation, and dissemination of data regarding a health-related event for use in public health action to reduce morbidity and mortality and to improve health (German et al., 2001). Public health surveillance is different from clinical diagnosis, which is defined by Mosby’s Medical Dictionary, 9th Edition, as “a diagnosis made on the basis of knowledge obtained by medical history and physical examination alone, without benefit of laboratory tests or x-ray films.” CDC’s Paul Mead in his Jan 29, 2004 testimony at the Connecticut Attorney General’s Lyme disease hearing stated it as follows:

"A clinical diagnosis is made for the purpose of treating an individual patient and should consider the many details associated with that patient's illness. Surveillance case definitions are created for the purpose of standardization, not patient care; they exist so that health officials can reasonably compare the number and distribution of “cases” over space and time. Whereas physicians appropriately err on the side of over-diagnosis, thereby assuring they don't miss a case, surveillance case definitions appropriately err on the side of specificity, thereby assuring that they do not inadvertently capture illnesses due to other conditions…."

However, in Lyme disease, the line between the two has been blurred, with serious consequences for patients and the physicians who treat them. This “elephant in the room” must be addressed as we move forward with improvements in surveillance and reporting.

Public health surveillance is in the purview of public health practitioners. Clinical diagnosis is the responsibility of qualified healthcare professionals with a living patient in front of them. Misuse of the CDC surveillance case definition for clinical diagnosis has led to significant underreporting of Lyme disease.

First adopted at the CDC Dearborn (MI) conference in 1994 (LDA, 2001), the interpretation of the two-tier tests was controversial because it was based on a study of early Lyme and people with Lyme arthritis (Dressler, Whalen, Reinhardt, & Steere, 1993). Many conference participants felt it would not be sensitive enough to detect late Lyme, or neurologic Lyme, but government officials assured them that the case definition was not “written in stone,” and it was not intended for clinical diagnosis. For several years the case definition was offered with a caveat, “Not intended for clinical diagnosis,” however, gradually the cautions were dropped and the original narrow surveillance definition indeed became the standard for clinical diagnosis. Patients who fail to meet the stringent criteria for two-tier interpretation are told they don’t have Lyme disease. In a very small informal patient study pre internet design, a questionnaire was distributed by CALDA (now LymeDisease.org) from 2003-2004 through doctors’ offices throughout the US, resulting in 182 respondents. Sixty-one percent (61%) of respondents indicated they were denied a diagnosis for Lyme at least once due to a negative WB blot by CDC surveillance band criteria. Physicians who diagnose such patients risk collegial censure and disciplinary action by state medical boards, who act as enforcers. Laboratories reporting results that don’t conform to the government guidelines risk their licenses and reputations. This situation must be fixed.

Advocates and patients have for decades fought against the use of CDC surveillance criteria for diagnostic criteria. Beginning in 1990, and continuing to a lesser extent today, doctors who do not follow CDC’s surveillance criteria for diagnosis/treatment are all too frequently brought up before state medical boards on charges including malpractice. According to Lyme Disease Association testimony in 2001 before the Assembly Health Committee Lyme Hearing in New York, “we met with representatives of the OPMC [Office of Professional Medical Conduct], health department, and the Governor’s office, motivated by the fact that almost 60% of doctors who treat chronic Lyme disease in NY State have faced OPMC scrutiny the past year….The Department of Health indicated that it was not actively soliciting complaints against treating doctors. A patient letter suggesting otherwise details her call to the NYDOH and two subsequent calls from them. Only seeking information on Lyme and other tick-borne diseases, she was subject to her diagnosis being questioned, told to see another physician other than her own, received an unsolicited complaint form in the mail from the DOH, and was pressured to file a complaint against her treating doctor. The DOH doctor told her that he and the DOH could obtain anyone’s record that they chose, including hers. She never filed a complaint; however, her medical records were pulled soon after the call, and she never heard from that doctor again… Her treating physician eventually faced charges (https://lymediseaseassociation.org/about-us/speeches-a-positions/testimonies/457-ny-assembly-health-committee-lyme-hearing#_ftn9). Patients were told by physicians and by insurers over decades that they do not meet the CDC criteria for Lyme disease. Advocates and patients across the country were forced to begin state-by-state organized campaigns for passage of “doctor protection laws” to protect physicians from unwarranted medical board sanctions related to Lyme, much based on the use of surveillance criteria. Rhode Island, Connecticut, New York, California, Massachusetts, and Vermont are some examples of states that passed such laws. In some states like New Jersey and Minnesota, advocates were able to educate the medical boards about the issue, thus reducing the likelihood Lyme doctors would be sanctioned.

Advocates held meetings in Washington with federal officials including the CDC Director, and with Congressmen, who became involved in the surveillance issue at least two decades ago. Examples of Congress’ thoughts on surveillance can be found in U.S. Senate language in a Congressional appropriations bill in 2002 indicating some medical boards appear to have confused Lyme surveillance criteria with diagnostic guidelines (Cohen, 2004), and in 2010 US Senate and House appropriations language and 2018 Senate Report 115-150 which includes language which “encourages CDC to support surveillance and prevention of Lyme disease and other high-consequence tick-borne diseases in endemic areas as well as areas not yet considered endemic…. Further, the Committee is concerned by reports that cases of Lyme disease are under-reported and encourages CDC to re-evaluate surveillance criteria used to track cases of the disease while assisting States to more accurately evaluate prevalence.”

The issue of surveillance is further complicated by the case definitions being so restrictive that individuals in states that are now referred to as low incidence have significant difficulty getting diagnosed/treated, as they are told by physicians there is no Lyme there—based on CDC surveillance. An analysis by LymeDisease.org’s MyLymeData (MLD) compared the numbers of cases reported by CDC with numbers of cases enrolled in MLD state-by-state. In states not considered by CDC to be endemic, MLD cases surpassed those reported by CDC, and the map created for the data suggests a broad pattern of underreporting by CDC of Lyme in the South and West. MLD had a much smaller sample size, phase 1 questions 3,903 ("Personal communication with Lorraine Johnson, JD, MBA, Principle Investigator of MyLymeData: Preliminary Data, Phase 1 MyLymeData April 17, 2018") than CDC’s (38,069), which was 10 times higher, and a weakness in that suggestion is that the latter cases were all for 2015, while MLD collected information from participants regardless of when they were infected. However, due to discrepant sample size, CDC cases should have surpassed MLD cases across the board in every state because its sample is so much larger, yet they do not. MLD then compared dogs reported by IDEXX Labs who tested positive for Lyme and the number of patients looking for doctor referrals from International Lyme & Associated Diseases Society (ILADS). Every one of those sources reflected higher cases numbers in the South and West than CDC did. For example, IDEXX canine cases: 25,196, ILADS MD referrals: 6,994, MyLymeData: 2,367, CDC: 513.

Another example pointing to surveillance failure in the South is a recent study using insurance data claims for patients with Lyme (Gelburd, 2017). The study accessed FAIR Health’s data base of over 23 billion private healthcare claims, and it shows North Carolina (NC), for example, in the top 5 states for Lyme related insurance claims in 2016. The state does not even rank in CDC’s top 14 states for reported Lyme cases, and based on CDC 2016 numbers, the Lyme Disease Association Inc. has reported NC as number 15.

Lyme disease testing, which should be the foundation of the Lyme disease surveillance system, is more than flawed—it is dangerous. From the decision at the 1994 Dearborn conference to base the surveillance case definition on a subset of Lyme patients with early Lyme disease and arthritis to the FDA’s warning healthcare professionals against using any but FDA-approved test kits, the government’s position has doomed many patients to a life of pain and misery. Without a positive test, doctors won’t diagnose them; without a diagnosis, no one will treat them. Without a positive test, they are often not counted for surveillance purposes. Although the two-tier testing system has high specificity, 99 percent, yielding few false positives, it has a mean sensitivity of 56 percent for 6 of the commercial Lyme tests approved by the Food & Drug Administration. Compare that with screening tests for HIV/AIDS, over 99.5 percent sensitivity (Stricker & Johnson, 2007). With hundreds of strains of Borrelia burgdorferi in the US, it is easy to see why our surveillance system is missing most of them.

To be cleared by the FDA, a test must be equal to or better than other FDA-cleared tests. The only test that needs to be approved is the original test against which all subsequent tests are cleared. In the case of two-tier Lyme testing, FDA officials could not identify the original approved test to the Lyme Disease Association, Inc. on a phone conversation, which was followed up by written communications to FDA (Lyme Disease Association and other undersigned parties on Regulatory Oversight of LDT-- Docket No. FDA-2011-D-0360). Nearly all commercial serologies are based upon a single tick Borrelia strain from a tick that likely may have never tasted human blood. The popular FDA-approved MarDX test kit, used by Labcorp, Quest, ARUP and other big commercial providers, is based on a clone of a single B31 spirochete collected from a tick--not a patient--from Long Island, NY, and propagated in the laboratory. The few FDA-cleared tests that are not based upon B31 have had to be shown to be the equivalent to a "comparator," that was B31. So basically all commercial serologies are either B31 or comparable in performance (J. Burrascano, personal communication, 03/15/18). Numerous studies have shown that the sensitivity in Lyme disease test kits is poor (Bacon et al., 2003; Coulter et al., 2005; Nowakowski et al., 2001; Wormser et al., 2008)

Tick-transmitted Borrelia fall into 2 heterogeneous bacterial complexes comprised of multiple species, the relapsing fever (RF) group and the Borrelia burgdorferi sensu lato group (Kingry et al., 2017). In California, which hosts more species of Borrelia than any other state, antibodies against the strain CA5 fails to react against B31 antigen 20% of the time. So if a patient is infected with CA5, s/he is more likely to test falsely negative for Lyme disease (Lane, Lennette, & Madigan, 1990). The College of American Pathologists (CAP) found that ELISA tests do not have adequate sensitivity to be used for screening purposes (Bakken, Callister, Wand, & Schell, 1997). Stricker and Johnson found that 54 percent of patients with Lyme disease test negative using the two-tiered testing system recommended by the CDC (Stricker & Johnson, 2010). Donta found that 52 percent of patients with chronic disease are negative by ELISA but positive by Western blot (Donta, 2002).

Laboratory-developed tests (LDT) may in fact be superior to FDA-cleared tests for Lyme disease, although the government discourages their use. One lab preferred by doctors who treat Lyme disease patients, achieved top scores on proficiency tests from the state of New York, which has the most stringent standard in the country. Between 2005 and 2015, the lab received a total of 165 proficiency testing samples for Lyme serology from NY Department of Health for testing. For IgG Western blot, it scored 100% overall, and for IgM Western blot, 98.8%.

A recently published paper (Conant, Powers, Sharp, Mead, & Nelson, 2018) alleges that many clinicians misinterpret Western blot results. Demonstrating their own unfamiliarity with the variable immune responses of people infected with Lyme disease, the authors complain that clinicians "incorrectly interpreted a positive immunoglobulin M (IgM) result as an overall positive test in a patient with longstanding symptoms." Late IgM is a hallmark of late Lyme disease that was even recognized back in 1986 by Steere and others (Craft, Fischer, Shimamoto, & Steere, 1986). Antigens of Borrelia burgdorferi recognized during Lyme disease. Appearance of a new immunoglobulin M response and expansion of the immunoglobulin G response late in the illness).

For surveillance of Lyme disease, the CDC should insist on using the most sensitive tests available. By recommending that doctors use the two-tier test, the government is intruding into the realm of clinical judgment which should be the prerogative of healthcare professionals and has caused immeasurable harm to patients.

Minority Response: Patient and Advocate Minority Report on Misuse of CDC Surveillance Criteria for Diagnosis

At the Second National Conference on Serologic Diagnosis of Lyme Disease held in Dearborn, Michigan, in 1994, by the Association of State and Territorial Public Health Laboratory Directors, the U.S. Centers for Disease Control and Prevention (CDC), and the Michigan Department of Health, the CDC announced that it would be using two-tier testing as part of the surveillance case definition for Lyme disease. This proved controversial because many feared that the criteria would miss the majority of patients who were not in the narrow group the criteria had been tested on. CDC spokesmen assured everyone that the criteria were a work in progress, not "written in stone." However, healthcare professionals soon began using the two-tier testing criteria in a clinical setting, to diagnose patients. Laboratories only reported the CDC-recommended bands of the Western blot test, leaving doctors without key information that might have helped them to diagnose patients. More and more patients missed the window of early diagnosis, allowing their cases to become chronic and harder to treat, if indeed they ever did get treated.

In 2005, at a non-public meeting of the CDC Board of Counselors at the National Center for Infectious Diseases in Atlanta, Georgia, a breakout group recommended that the CDC guidelines for interpreting laboratory tests should be updated in collaboration with industry and government experts. One of the Counselors, Infectious Diseases Society of America (IDSA) president Dr Stamm, offered to assist CDC with public interface. Dismissing patient concerns, Stamm stated that CDC researchers should focus on science and not on the concerns of patient groups. He proposed that the IDSA Lyme guidelines should be updated and "a consensus document made available to physicians who need guidance ("ISDA on Lyme," 2005).” IDSA thus became the public front for CDC. CDC promoted the IDSA guidelines only, even when International Lyme and Associated Diseases Society (ILADS) guidelines were accepted by the National Guidelines Clearinghouse and met the Institutes of Medicine's rigorous standard for trustworthy guidelines while the IDSA guidelines did not.

Eventually the two-tier testing criteria were incorporated by the IDSA into its 2006 Lyme guidelines. The transformation of the testing protocol intended for surveillance into the protocol for diagnosis in a clinical setting was complete. As the IDSA states on its website:

Furthermore, when laboratory testing is done to support the original diagnosis of Lyme disease, it is essential that it be performed by well-qualified and reputable laboratories that use recommended and appropriately validated testing methods and interpretive criteria (Wormser et al., 2006).

The guidelines cite two issues of the CDC’s Morbidity and Mortality Weekly Report (MMWR) which published articles recommending the exclusive use of FDA-approved tests only, and the importance of adhering to the two-tier testing protocol.

In a 2005 survey of 182 respondents, LymeDisease.org found 73% were denied a diagnosis for Lyme at least once due to a negative ELISA by CDC criteria. Of these, 31% were denied access to a Western blot (WB) by their physicians due to a negative ELISA. Sixty-one percent (61%) of respondents were denied a diagnosis of Lyme at least once due to a negative WB blot by CDC surveillance band criteria. The authors conclude that widespread misuse of the CDC surveillance criteria for diagnostic purposes results in significant diagnostic delays and results in chronic and debilitating illness for patients nationwide (CALDA, 2005).

Today, 70% of patients enrolled in LymeDisease.org’s big data survey, MyLymeData, have late or chronic Lyme disease. Diagnostic delays are associated with false negative lab tests (37%) and positive lab tests dismissed as "false positive." (13%) Almost all of those diagnosed late (91%) remain ill (Johnson, Mervine, & Potter, 2016).

Potential Actions

This subcommittee identified five potential actions that the federal government could take to improve public health surveillance of Lyme and tick-borne diseases. These possible actions are listed in priority order (1 is the highest priority and 5 is the lowest priority; scores are available in supplement document):

Provide a more complete picture of disease risk by supplementing and integrating traditional public health surveillance data with other data sources such as tick surveillance data; tick testing data; companion animal tick-borne disease testing data; medical claims data; weather data; other patient data sources; and data from other federal agencies including the Department of Defense.
Have public health authorities formally recognize (for example, include on official websites and in official publications such as CDC annual reports) and provide resources for systematically determined, and regularly conducted, studies to determine estimates of the actual number of cases of tick-borne disease (“burden of illness” studies). Base allocations on the estimated actual number of cases of disease in addition to reported case counts.
Have public health authorities formally recognize alternative, validated systematic approaches to tick-borne disease surveillance, such as systematic sampling of tick-borne disease reports for investigation, that reduce the burden on tick-borne disease reporters but allow for comparability of surveillance findings across states and over time.
Make it easier and more likely for tick-borne disease cases to get reported to public health agencies by leveraging electronic exchange of health data and educating and incentivizing providers to report.
Public health authorities shall annually and when opportune (such as during Tick-Borne Disease Awareness Month) inform doctors, insurers, state and local health departments, the press and the public through official communication channels, including the MMWR, CDC and other official websites, that the Lyme disease surveillance criteria are not to be used for diagnostic purposes.

Reported and Estimated Confirmed Lyme Disease Cases by Year, United States, 2001 to 2016. A bar graph showing the total numbers of confirmed cases reported to CDC annually between 1991 and 2016.

Figure 3. Total confirmed case counts reported to the Centers for Disease Control and Prevention (CDC) annually, with estimated total confirmed counts derived by multiplying annual reported confirmed case counts by eight and ten. The surveillance case definition for Lyme disease changed in 2008 to incorporate both Confirmed and Probable case classifications; prior to 2008, there was only a single case classification (Confirmed). These data are estimates only, but are useful to illustrate that Lyme disease has a much greater impact in the U.S. than might be appreciated by reported case counts only. The eight and ten times correction factors derive from recent reports characterizing the degree of underreporting of Lyme disease (Hinckley et al., 2014; Nelson et al., 2015). These reports reflect similar estimates for the degree of underreporting of Lyme disease as determined by earlier studies. Thus, it is not unreasonable to apply the eight and ten times correction factors across time.

A map of the United States that shows the distribution of blacklegged ticks, lone star ticks, and both species.

Legend for a map of the United States that shows the distribution of blacklegged ticks, lone star ticks, and both species.

Figure 4. Map of county-by-county distributions of lone star ticks and blacklegged ticks, with ticks positive for the agents of ehrlichiosis and Lyme disease at military installations denoted with colored boxes (blue: blacklegged ticks; yellow: lone star ticks; green: both species). This figure combines CDC surveillance data of tick presence/absence with DOD tick testing data (?: No data; orange: Lyme; lighter red: Ehrlichiosis; dark red: Lyme and Ehrlichiosis) from the Human Tick Test Kit Program (HTTKP) to provide a proxy of risk at different Army bases (adapted from the U.S. Army Public Health Center Health of the Force Report, 2017. Circles indicate installations that submitted 50 or more ticks to the HTTKP between 2006 and 2016. The red null circles indicate installations that do not regularly submit ticks, and the HTTKP dataset cannot produce risk assessments for those installations.

Votes of Subcommittee Members

The attending subcommittee members unanimously voted yes to accept the list of potential actions for this priority.

Number in Favor	Number Opposed	Number Abstained	Number Absent*
11	0	0	2

*One subcommittee member was absent from the call. Another member left the conference call early because of schedule conflict.

The subcommittee, however, did not reach a consensus regarding the wording. While the majority of the attending subcommittee members agreed to accept this section (Priority 3) as it is, four other members disagreed with the existing wording regarding two-tier testing, and they subsequently provided their minority response.

Priority 4: Detection, Identification, and Characterization of Novel and Emerging Pathogens in Ticks, Including Bartonella, and the Transmission Risks of These Agents by Ticks to Humans.

The risk of tick-borne disease is a growing issue affecting increasing numbers of people, pets, livestock and wildlife on both a national and global scale. Many factors are thought to influence the increased reporting of known, emerging and re-emerging pathogens. Climate, urban sprawl, changing habitat conditions, migration of birds and wildlife, as well as import and travel by livestock, pets and humans may all contribute to this increased risk. Bartonellosis, once thought to be a self-limiting infection, has now been recognized as a potentially stealthy, persistent, and serious infection in humans (Breitschwerdt, Maggi, Nicholson, Cherry, & Woods, 2008). These infections are known to be transmitted to humans through contact with cats, dogs, fleas, biting flies and other vectors; however, the risk of transmission to humans by a tick vector has not been thoroughly assessed. Concurrent or prior exposure to cats or kittens and the potential for persistent Bartonella. henselae infection in children or adults with a history of tick attachment limit the utility of case-based evidence of B. henselae transmission by ticks. However, further investigations have documented concurrent infection of the central nervous system with Borrelia burgdorferi and B. henselae, supporting the possibility of the cotransmission of these pathogens by Ixodes spp. (Eskow, Rao, & Mordechai, 2001).

Early detection, identification and characterization of novel and emerging pathogens and determination of tick vector transmission risk to humans is critical in safeguarding human health, and needs to be improved. Surveillance strategies are needed to provide ongoing monitoring of changes in the geographic ranges of both ticks and tick-borne pathogens and to assess the full scope of recognized and potentially emerging disease causing organisms occurring in ticks infecting humans throughout the nation. Laboratory and field studies are required to demonstrate the competence and the ability of a tick species to vector (biological or mechanical) a microbe that can cause disease in humans, for example a pathogen, which is maintained in nature through a cycle involving other animals prone to infestation by one or different tick life cycle stages (larva, nymph, adult) during the parasitic phase of a tick's life cycle (Figure 5). However, not all microbes infecting ticks are pathogenic to humans. The epidemiology of tick-borne diseases, including incidence, prevalence, emergence, and re-emergence, is determined by physiological, behavioral, and ecological factors governing tick vector-pathogen (bacteria/virus/protozoan) and host (human, companion animal, domestic animal, and wildlife) interactions (Figure 6). These processes determine the risk for exposure to infected ticks, and the outcomes of transmission and infection (subclinical, clinical) with tick-borne microbes demonstrated to be pathogenic to humans. Previous efforts by several groups have addressed critical needs and knowledge gaps to solve the problems with tick-borne diseases of public health importance (for example: https://www.ncbi.nlm.nih.gov/books/NBK57020/; https://www.ars.usda.gov/ARSUserFiles/np104/TBD_IPM_WG_Final_White_Paper%2026%20February%202014.pdf; https://s3.amazonaws.com/climatehealth2016/low/ClimateHealth2016_05_Vector_small.pdf). However, a challenge to deliver of solutions has been the lack of sustained support and commitment for interdisciplinary groups to research, develop, and implement the next generation of technologies that can be deployed to ameliorate the impact of tick-borne diseases on humans.

Themes and Results

The salient themes and its integrated components that our group identified for priority issue #4 are listed below. Each component of this theme was systematically analyzed in order that the resulting recommend actions that will result in key improvements in the detection, identification, and characterization of novel and emerging pathogens in ticks; changes in geographic ranges and numbers of ticks; increase understanding of transmission risks of these agents by ticks to humans; and, awareness of healthcare professionals, public health authorities, and the public of the threats posed to our nation by ticks and tick-borne diseases. This document is not an exhaustive review of the scientific literature. However, selected references are cited to highlight current research issues.

Theme. Encourage commitment to establish a nationwide tick and tick-borne disease surveillance network that is a partnership among public interest groups, academic institutions, and local, state and federal government agencies to provide coordinated, standardized protocols for tick-borne disease surveillance, tick collection, identification, and analysis to identify established, emerging, and enzootic transmission cycles with zoonotic potential. Proposed network includes the coordination of local Mosquito and Tick Control Programs.

The complex, ever changing, nature of arthropod vectors and the diseases they transmit requires a surveillance network that encompasses analysis of vectors, pathogens, reservoirs, and infections that utilized long standing and new technologies to predict, prevent, detect, and control disease transmission (Thompson & Etter, 2015). Rather than create a standalone tick and tick-borne disease network, the logical approach is to combine all medically important vectors, primarily mosquitoes and ticks, within one comprehensive operational scheme (Nasci, 2008). Such integrated surveillance and response systems are effective and result in significant cost savings over specific vector and related disease approaches (Xu, Mather, Hollingsworth, & Rich, 2016). Activities of the proposed network are to provide coordinated, standardized protocols for tick and disease surveillance; tick collection, identification, and analysis; identification of established, resurging, and emerging tick-borne pathogens in field collected ticks; and, research, outreach, and education of the public, healthcare professionals, and other stakeholders.

Evidence and Findings

Tick-borne diseases are zoonoses, infections shared in nature between humans and other vertebrate animal species. Monitoring human disease is not sufficient to encompass all the factors contributing to the public health threat posed by ticks and the pathogens they transmit. Control of vector-borne diseases requires integrated approaches to develop optimal programs for efficient and effective surveillance of ticks and tick-borne diseases, preparedness and contingency planning, diagnosis, early warning of threats, control, and education of those treating as well as impacted by these diseases (Braks et al., 2014).

Opportunities

Ticks and tick-borne diseases do not recognize regional nor political boundaries. Therefore, development of a nationwide network for surveillance, diagnosis, and control of these important vectors must be part of a robust international disease monitoring network providing timely, up to date communications about ticks and tick-borne infections (Braks et al., 2014; Thompson & Etter, 2015). The recent detection of the worrisome exotic tick vector native to Asia, Haemaphysalis longicornis, in New Jersey, rang the alarm bells to fill in this significant gap (Rainey et al. 2018). Ideally, such an international consortium would share information, research endeavors, other tools, and operational strategies with participants around the world. The Centers for Disease Control and Prevention Regional Centers of Excellence for Vector-borne Diseases represents a foundational underpinning as a potential core components of a nationwide tick and tick-borne disease surveillance network partnership among public interest groups, academic institutions, and local, state, regional, and federal agencies. Activities of this network would have the ability to provide coordinated, standardized protocols for tick and disease surveillance; tick collection, identification, and analysis; identification of established, resurging, and emerging tick-borne diseases; and, research, outreach, and education of the public, healthcare providers, and other stakeholders. Many non-federal programs have been collecting tick and pathogen data with no platform for widespread sharing except formal publication. Providing a central clearinghouse for this data would allow for collation of these multiple efforts and possibly fill some of the data gaps that federal surveillance efforts have not been able to capture.

An integral ongoing activity of the proposed network is the use of high throughput sequencing strategies to identify established, resurging, and emerging pathogens in tick microbiomes from ticks collected across the nation. This critical activity is based on a principle similar to the Global Virome Project. Microbiomes analyzed on an ongoing bases will be those of the following tick vectors of zoonoses in the United States (Eisen et al., 2017): Amblyomma americanum, Amblyomma maculatum, Dermacentor andersoni, Dermacentor occidentalis, Dermacentor variabilis, Ixodes pacificus, Ixodes scapularis, Rhipicephalus sanguineus, Ornithodoros species and nidicilous (nest inhabiting) tick species that will enable systematic identification of microbes potentially pathogenic to humans and animals through further research and testing according to the Henle-Koch postulates.

The tick microbiome component will, for the first time, provide a comprehensive database of tick-borne microbes in all regions of the country and serve as the scientific underpinnings for informed, evidence-based geographic awareness of ticks and tick-borne diseases occurring in a specific area, as well as the incidence and geographic changes occurring in both tick populations and the diseases they transmit. This information is essential for informed prevention, intervention, and clinical awareness.

Threats

The Centers for Disease Control and Prevention Regional Centers of Excellence for Vector-borne Diseases comprise a unique consortia involving collaborations among the following: research institutes, departments of health, agriculture experiment stations, and academic institution departments of schools or colleges, such as medicine, veterinary medicine, and agriculture. Regional Centers of Excellence are actively engaged in surveillance, diagnostics, control, research, education and outreach. In the context of a One Health approach (see below for suggested action), the following entities should also be integral to the tick and tick-borne diseases network: Integrated Pest Management (IPM) Centers across the nation, U.S. Department of Agriculture (ARS and APHIS), Extension Service Network, and Mosquito control programs. Currently, lack of funding is an impediment to achieving this this goal with significant potential to protect the health of the nation.

Barrier. Tick Control has been placed under mosquito control programs in NJ through passage of legislation. Mosquito control programs (in NJ) currently lack the experience, education, resources and funding necessary to incorporate tick control and Tick Integrated Pest Management practices into existing programs (Public Tick IPM Working Group meeting; Frank Laufenberg 2018). Monmouth County is the exception, providing an integrated mosquito and tick control program and conducting active surveillance of ticks ("Monmouth County Mosquito Control," 2018).

There is a lack of funding resources for TBD research and prevention. Only $25 million was invested in 312,000 new cases of Lyme disease, which is only $80 per new case. As Lyme disease cases rose in 2013, the NIH reduced funding to $20 million. The total 2016 CDC funding line for Lyme disease was approximately $10.6 million dollars ("Working to solve the tick problem using IPM practices," Tick IPM Working Group).

Table 5. NIH funding of Lyme disease research compared to other diseases.

Disease and Year	New Cases (annual)	NIH Funding
Hepatitis C (2012)	1,300	$112 million
West Nile Virus (2012	5,700	$29 million
HIV/AIDS (2012)	56,000	$3 billion (11% total NIH budget)
Influenza (2012)	73,000	$251 million
Lyme disease (2012)	312,000	$25 million
Lyme disease (2013)	363,000	$20 million

"We won't make progress until these dynamics change and without tests to diagnose and monitor Lyme and other tick-borne diseases. I have some trouble understanding how we could rapidly mobilize scientists to develop test for MERS (Middle East Respiratory Syndrome), SARS (severe acute respiratory syndrome), and Ebola, but have made little progress on Lyme over decades." Judy Stone in Ticked Off - What We Don't Know About Lyme Disease, Forbes Magazine, June 2015

Potential Actions

Apply the One Health approach (https://www.springer.com/us/book/9783642358456; https://www.usda.gov/topics/animals/one-health) to the grand challenge posed to public health by ticks and tick-borne diseases in the U.S. The public health response to these vector-borne diseases is enhanced by integrating multidisciplinary teams engaged in the surveillance of vectors and vector-borne diseases (http://ir.bellschool.anu.edu.au/sites/default/files/publications/attachments/2016-10/davies_and_youde_ch_1_2015.pdf), resulting in improved diagnosis, control and prevention responses, education, and training of healthcare, research, and operational professionals (Nasci, 2008). The proposed national network will strengthen vector and disease surveillance for these important tick-borne zoonotic diseases through partnerships between medical and veterinary public health workers, researchers, educators, and advocacy groups (Baneth, 2014; Perez de Leon et al., 2010; Wendt, Kreienbrock, & Campe, 2015).
Rather than create a standalone tick and tick-borne disease network, the logical approach is to combine all medically important vectors, primarily mosquitoes and ticks, within one comprehensive operational scheme. Such an integrated surveillance and response system is reported to be effective and result in significant cost savings over specific vector and related disease approaches (Wu et al., 2016); 3). The proposed surveillance and response system will establish local, state, and federal partnership to safeguard public health that is also linked to the National Animal Health Laboratory Network (https://www.aphis.usda.gov/aphis/ourfocus/animalhealth/lab-info-services/nahln/ct_national_animal_health_laboratory_network), and important component as we address the zoonotic disease threat to our population.
Investment to develop cost effective, long term solutions must be commensurate with the level of TBD – currently the investment falls far short of the costs.

A. Because detection of a pathogen through molecular approaches is suggestive of the role of a tick species in disease transmission, several carefully designed and well-controlled studies documenting Koch's postulates for causation of disease by a microbe are required to confirm that a tick species is a competent disease vector. These studies are crucial because they inform the risk of pathogen exposure to humans.

Establishing a direct relationship between a tick transmitted microorganism and a specific disease is not necessarily an easy process. The Henle-Koch postulates are the established standard by which a microbe is established as the etiological agent of a clinical disease (Evans, 1976). Specific elements of the postulates are (1) the parasite occurs in every case of the disease in question and under circumstances which can account for the pathological changes and clinical course of the disease; (2) it occurs in no other disease as a fortuitous and nonpathogenic parasite; and (3) after being fully isolated from the body and repeatedly grown in pure culture, it can induce the disease anew (Evans, 1976).

Xenodiagnosis seems preferable for B. burgdorferi to isolate infectious transmission (Marques et al., 2014). This has been acknowledged by Monica K. Embers, PhD, Emir Hodzic, DVM, MSci, PhD, and Linden Hu, MD and others in the research community. Xenodiagnosis is an important means to assess tick transmission potential for any suspected tick-borne infectious agent.

Evidence and Findings

Application of the Henle-Koch postulates to vector-borne diseases requires a modified approach for establishing a causal link between a vector and infectious agent. Those criteria are (1) isolation of the microbe from naturally infected arthropod vectors; (2) laboratory demonstration of the ability of the vector to become infected by obtaining a blood meal from an infected host; (3) laboratory demonstration of the ability of the vector to transmit the microbe during blood feeding; and, (4) evidence of blood feeding contact between the suspected arthropod vector and suspected vertebrate hosts under natural conditions (DeFoliart, Grimstad, & Watts, 1987).

Since B. burgdorferi is difficult to culture, xenodiagnoses, using an uninfected tick on an infected animal is able to pick up the microbe, is an effective method to do so. Xenodiagnosis involves placement of a ‘pathogen-free’ tick on an infected host animal followed by assessment of the uptake of the infected agent by the feeding tick. Monica Ember’s of Tulane University provided this in research, “Variable manifestations, diverse seroreactivity and post-treatment persistence in non-human primates exposed to Borrelia burgdorferi by tick feeding (Embers et al., 2017).” Xenodiagnosis can be utilized to assess tick transmission potential of any suspected tick-borne infectious agent.

Opportunities

Alternative approaches are available to provide evidence to establish the associations of a microbe with a specific disease. Molecular methodologies used to supplement the Henle-Koch postulates, when original criteria difficult to fulfill, include sequence-based microorganism detection and genotype-based identification (Cabezas-Cruz, Vayssier-Taussat, & Greub, 2018; Fredricks & Relman, 1996). Whole genome sequencing can also be used to identify tick associated microbes with similarities to related microorganisms in pathogen containing groups (Cosentino, Voldby Larsen, Moller Aarestrup, & Lund, 2013). Additional criteria used to establish microbe causality of a disease include epidemiologic data (Hill, 1965) and immunological criteria (Evans, 1976).

Threats

Meeting the criteria for linking a disease-causing microbe with a tick vector may not be achievable due to the absence of animal models of infection, inability to culture in the laboratory newly discovered pathogens, and lack of laboratory-reared colonies of potential tick vector species.

Disease causing microbes may be difficult to detect in perceived low incidence regions due to lack of awareness and surveillance activity for vectors, humans, companion animals, and wildlife in those regions. Critical to all these efforts is the availability of sufficient funding for TBD research and prevention. Only $25 million was invested during 2012 relative to an estimated 312,000 new cases of Lyme disease, which represents is only $80 per new case. The total 2016 CDC funding line for Lyme disease was approximately $10.6 million dollars (Public IPM Working Group 2018).

Potential Actions

Establish interdisciplinary technical committee between the American Medical Association, the Veterinary Medical Association, and the Entomological Society of America (http://www.entsoc.org/PDF/2015/ESA-PolicyStatement-Tick-borneDiseases.pdf) to produce guidance based on state of the science to study and validate tick-borne pathogens and tick vectors.
Convene group of experts to review state of the science on the application of the latest molecular techniques to detect tick microbiome organisms that will be prioritized based upon perceived disease risk potential for laboratory testing according to the Henle-Koch postulates.
Persistence of Borrelia burgdorferi infection must be acknowledged. Serological assays must be developed to determine active infection. And development of novel treatments to cure active illness must be researched and identified. Patients must be effectively treated.
Investment to develop cost effective, long term solutions must be commensurate with the level of TBD – currently the investment falls far short of the costs.

B. Establish global database of tick microbiome, which is expanding rapidly through the application of next-generation sequencing, to catalog and prioritize tick germs to be used in evaluation of disease in humans and animals.

The conventional method for identifying the causative agent of a tick-borne disease is to associate a specific illness to a history of tick bite followed by linking that illness to a specific microorganism. A classic example of this process of pathogen discovery is Lyme borreliosis (Steere et al., 2016). Early epidemiologic studies provided evidence that a tick, Ixodes scapularis, transmitted the causative agent (Steere, Broderick, & Malawista, 1978). Subsequently, the tick was shown to transmit the causative Borrelia burgdorferi spirochetes (Burgdorfer et al., 1982). However, molecular techniques are powerful tools for identification of previously unrecognized microbes in ticks (Parola et al., 2013). The tick microbiome contains endosymbionts, known tick transmitted disease-causing agents, and unknown microbes that may be linked to human disease in the future (Narasimhan & Fikrig, 2015; Tijsse-Klasen, Koopmans, & Sprong, 2014).

Evidence and Findings

Molecular techniques are the basis for the reversed discovery, identification of the microorganism prior to its association with disease, as found for the following microbes that were subsequently established to be human pathogens: Borrelia miyamotoi (Branda & Rosenberg, 2013), Neoehrlichia mikurensis (Kawahara et al., 2004), Rickettsia helvetica (Nilsson, Lindquist, & Pahlson, 1999), Rickettsia monacensis (Jado et al., 2007), and other Rickettsia species identified by genomic methods (Parola et al., 2013).

The incidence of tick-borne disease is increasing, driven by rapid geographical expansion of ticks and the discovery of new tick-associated pathogens. Ticks carry a wide range of known human and animal pathogens and are postulated to carry others with the potential to cause disease. The examination of the tick microbiome is essential in order to understand the relationship between microbes and their tick hosts and to facilitate the identification of new tick-borne pathogens. Unbiased high-throughput sequencing was used to characterize the virome of 2,021 ticks including /Ixodes scapularis/ (/n =/ 1,138), /Amblyomma americanum/ (/n =/ 720), and /Dermacentor variabilis/ (/n =/ 163), collected in New York, Connecticut, and Virginia in 2015 and 2016. Among the microbes identified were 33 viruses, including 24 apparently novel viral species. Genomic analyses using unbiased high-throughput sequencing platforms are highly valuable for investigations of tick bacterial diversity, but the examination of tick viromes has historically not been well explored (Tokarz et al., 2018).

Opportunities

Characterize the microbiomes of tick species of major and minor medical importance throughout the United States utilizing molecular techniques, including next generation sequencing methods, to identify microorganisms with known human pathogenicity and novel tick-associated microbes with yet to be established ability to cause human disease outbreaks. Individual tick species will be periodically sampled from throughout their geographic range and databases established for identification of emerging pathogens of humans and other animal species and changes in geographic range and prevalence of tick vectors. Knowledge of the intricate interactions between microbes in ticks can be exploited to innovate technologies that disrupt pathogen transmission (Bonnet, Binetruy, Hernandez-Jarguin, & Duron, 2017; Duron et al., 2017). These data will provide healthcare professionals, public health authorities, and the public with accurate information about the ticks and tick-borne infectious agents within their local regions that will result in improved nationwide disease prevention, diagnosis, and informed healthcare delivery.

Threats

Because PCR-positive results for a microbe in a tick do not correlate directly with the ability of a tick to transmit a specific pathogen, an important point to remember is that microbe DNA detected in a fed tick may be residual from a previous blood meal and not definitive evidence of a vector role for that tick (Pichon, Rogers, Egan, & Gray, 2005).

Lack of funding is an impediment to achieving this. There is a lack of funding resources for TBD research and prevention. Only $25 million was invested in 312,000 new cases of Lyme disease, which is only $80 per new case. As Lyme disease cases rose in 2013, the NIH reduced funding to $20 million. The total 2016 CDC funding line for Lyme disease was approximately $10.6 million dollars (Public IPM Working Group 2018).

Potential Actions

Establish global tick microbiome consortium similar to the Global Virome Project (http://www.globalviromeproject.org). Tick species assessed in this tiered approach for further characterization of their microbiomes include the following ixodid vectors of zoonoses in the United States (Eisen, Kugeler, et al., 2017): Amblyomma americanum, Amblyomma maculatum, Dermacentor andersoni, Dermacentor occidentalis, Dermacentor variabilis, Ixodes pacificus, Ixodes scapularis, and Rhipicephalus sanguineus, Ornithodoros spp., and nidicolous species that will enable the systematic identification of microbes potentially pathogenic to humans and animals.
Although collection of ticks for analysis of their microbiomes should occur on a continuous basis throughout the geographic range of the tick, particular effort should be directed toward collecting samples at the edges of the expanding ranges of medically important species (Childs & Paddock, 2003; Eisen & Eisen, 2018; Sonenshine, 2018) and increased efforts for collection of species that are suspect or questionable for human health risk (ex. Ixodes spinapalpis in the Rocky Mountain the Western regions) (Burkot et al., 2001).
Publicize information gained from these studies to inform public health professionals, health care providers, vector control specialists, researchers, other stakeholders, and the public of threats from ticks and tick-borne diseases.
Investment to develop cost effective, long term solutions must be commensurate with the level of TBD – currently the investment falls far short of the costs.
Utilize unbiased high-throughput sequencing to characterize the microbiome of tick species (Narasimhan & Fikrig, 2015; Tokarz et al., 2018).

C. Evaluate state of science in tick taxonomy and phylogenetics to identify technologies and processes to democratize tick identification and science-based practices to mitigate the risk for tick-borne disease transmission.

Molecular techniques are advancing our understanding of tick biodiversity. Understanding tick biodiversity within the United States is highly relevant to understanding the roles of ticks as disease vectors. Combining the application of morphological characters with molecular traits provides a powerful strategy to identify ticks, and their physiological/development state thus enhancing our ability to assess the risks of tick-borne disease transmission (Falco et al., 2018). Disease prevention is maximized the earlier and more rapidly, and this can be performed in the field (http://www.tickencounter.org/tickspotters and Tickspotters.org).

Evidence and Findings

Integrative taxonomy (classification) is enriching our understanding of tick biodiversity (Skoracka, Magalhaes, Rector, & Kuczynski, 2015). Differences in host availability across the geographic range of a tick species can result in genetic variability between populations (Kempf et al., 2011). Because vector competence and capacity have a genetic basis, different tick populations can vary in their ability to transmit pathogens to humans (Coimbra-Dores et al., 2018; de la Fuente et al., 2017; Xu et al., 2016). Digital technologies and internet-based platforms provide the media to facilitate public training and education in tick identification, which has the potential to empower citizens in their ability to prevent tick bites and exposure to tick-borne diseases (http://tickapp.tamu.edu/tickbiteprevention.html; https://itunes.apple.com/us/app/tickid/id531348104?mt=8; (Pérez de León, Teel, Li, Ponnusamy, & Roe, 2014).

Opportunities

The effectiveness of tick management efforts by local, state, and federal agencies could benefit from platforms that enhance connectivity with citizen stakeholders (for example, http://tickspotters.org/tickspotters; https://www.yelpblog.com/2016/09/yelp-government-one-year-later). Conversely, increased public participation through the use of internet-based tools could inform decisions to accelerate innovation by such agencies (for example, https://www.citizenscience.gov/; https://innovation.gov/; https://apps.health.vermont.gov/vttracking/ticktracker/2018/d/)

Threats

There exists a need to reinforce partnership with extension to strengthen tick and tick-borne disease literacy efforts, especially in high-risk areas for disease transmission where high tick densities occur. As stated earlier, lack of funding is an impediment to achieving this. There is a lack of funding resources for TBD research and prevention. Only $25 million was invested in 2012 in 312,000 new cases of Lyme disease, which is only $80 per new case. As Lyme disease cases rose in 2013, the NIH reduced funding to $20 million. The total 2016 CDC funding line for Lyme disease was approximately $10.6 million dollars (Public IPM Working Group 2018).

Potential Actions

Establish a local, state and federal tick-borne disease council within the framework of the proposed national surveillance network to develop best practices for maximal dissemination of science-based information, including interactive sites for tick identification in real time.
Promote citizen science efforts for tick surveillance and identification, and pathogen testing.
Promote tick biology literacy in early education and universities, especially in high-risk areas for disease transmission where high tick densities occur.
Investment to develop cost effective, long term solutions must be commensurate with the level of TBD – currently the investment falls far short of the costs.

D. Applied studies on tick ecology to adapt intervention strategies addressing risk factors for human exposure to infected ticks according to tick-borne disease system & geographic region.

Tick-borne diseases are dynamic systems influenced by biotic and abiotic factors. Adapting disease ecology principles to the grand challenge of tick-borne disease epidemiology and this control strategies will help understand the factors driving transmission.

Evidence and Findings

Aspects related to global change continue to alter the spatial and temporal variation of tick-borne disease risks and their incidence in human populations (Estrada-Pena & de la Fuente, 2014). Canadian researcher, John Scott, recently published a differing viewpoint stating that public awareness and bird migration are the drivers of increased recognition of tick and TBD prevalence in areas not previously detected (Scott & Scott, 2018). Anthropogenic landscape alterations across ecosystems further exacerbates the problem with ticks and tick-borne diseases in certain geographical regions (Kilpatrick et al., 2017). Hypothesis-driven research is required to fill in these knowledge gaps. The translation of this knowledge to innovate adaptive interventions will enhance the design of effective area-wide tick control strategies (Esteve-Gassent et al., 2016) (Figure 7).

Opportunities

Establish within the framework of the national surveillance network groups of researchers with diverse scientific backgrounds interested in tick-borne diseases that create interdisciplinary approaches that address the problems of ticks and tick-borne diseases from a grand challenge perspective (https://grandchallenges.org/#/map).

Threats

Failing to do thorough historical evaluation of scientific literature can result in repetitious research, or work done lacking solid foundational context. This results in a loss of knowledge base. Those who retire frequently do not have new scientists to train and replace them. Those new scientists enter fields where there is research funding more readily available.

Lack of funding is an impediment to achieving this. This is shortsighted in regard to the current and future cost both monetarily and to the wellbeing of our national population.

Potential Actions

Institute a regional scale approach to understand the ecology of tick-borne diseases.
Study each of the major zoonotic tick-borne diseases in the different ecosystems in which they occur using harmonized protocols to understand the variability in qualitative and quantitative characteristics of ecological drivers.
Link ecological data to genetic plasticity studies of tick and tick-borne pathogen populations to understand the variability in infection rates among tick populations and vertebrate reservoirs of tick-borne pathogens.
Adapt and refine predictive tools to refine the temporal and spatial aspects of integrated tick management intervention.
Investment in development of cost effective, long-term solutions that are commensurate with the levels of tick and tick-borne disease threats. Currently the investment falls far short of the costs.

An image showing the life cycle of black-legged ticks: from eggs (spring) to larva (summer), nymph (spring), and adult (fall and winter). Risk of human infection is greatest in the late spring and summer.

Figure 5. The life cycle of the blacklegged tick (ixodes scapularis) throughout the year. [Figure source: Beard, C.B., R.J. Eisen, C.M. Barker, J.F. Garofalo, M. Hahn, M. Hayden, A.J. Monaghan, N.H. Ogden, and P.J. Schramm, 2016: Ch. 5: Vectorborne Diseases. The Impacts of Climate Change on Human Health in the United States: A Scientific Assessment. U.S. Global Change Research Program, Washington, DC, 129–156 (Beard et al., 2016)].

An infographic showing the impact of climate change on Lyme and other illnesses carried by ticks

Figure 6. The impact of climate change on human health (Lyme disease) in the U.S. Climate drivers (high and low temperature extremes, changing precipitation patterns, changes in seasonal weather patterns) affect exposure pathways (earlier tick activity and range expansion northward and to higher elevations; shifting season influence host-seeking activity), which then impact health outcomes (Lyme disease and other illnesses carried by ticks). Environmental and institutional context includes changing ecosystems; changing landscapes; changes in vector and population size, density, and pathogen infection rates; and vector control and public health practices. Social and behavioral context includes social determinants of health, outdoor activity, geographic location, proximity to woodlands, and landscape design. [Figure source: Beard, C.B., R.J. Eisen, C.M. Barker, J.F. Garofalo, M. Hahn, M. Hayden, A.J. Monaghan, N.H. Ogden, and P.J. Schramm, 2016: Ch. 5: Vectorborne Diseases. The Impacts of Climate Change on Human Health in the United States: A Scientific Assessment. U.S. Global Change Research Program, Washington, DC, 129–156 (Beard et al., 2016)].

An infographic demonstrating Integrated TTBD and One Health Strategies.

Figure 7. Suggested research framework toward sustainable integrated tick and tick-borne disease management strategies in the context of global change and the One Health approach. Ecosystem Services risks and opportunities include livestock-wildlife-human interface, environmental change, landscape ecology, and climate change. Evidence-based statutes and holistic policy includes active surveillance, agriculture and ecosystem conservation linkage, adaptable to global change, and balancing diverse interests. Societal awareness and extension includes prevention and preparedness, best agronomic practices, strategic preparedness and responsiveness, and socioeconomic impacts documentation. Interdisciplinary research includes translational, identify global change drivers, testable hypotheses, basic and applied, and systems approach. [Adapted from Pérez de León AA, Teel PD, Auclair AN, Messenger MT, Guerrero FD, Schuster G, Miller RJ. 2012. Integrated strategy for sustainable cattle fever tick eradication in USA is required to mitigate the impact of global change (Perez de Leon et al., 2012)].

Note: This group voted to select one possible action from all the options in each of the five bullets it came up with for the Working Group to consider. However, the group felt that all the five possible actions selected were equally important. The consensus was to take a theme approach to synthesize the five possible actions selected, and it presents a theme encompassing the potential action for the Working Group to consider. The theme and the 5 actions are presented below.

Potential Actions

Theme: Encourage commitment to establish a nationwide tick and tick-borne disease surveillance network that is a partnership among public interest groups, academic institutions, and local, state and federal government agencies to provide coordinated, standardized protocols for tick-borne disease surveillance, tick collection, identification, and analysis to identify established, emerging, and enzootic transmission cycles with zoonotic potential. Proposed network includes the coordination of local Mosquito and Tick Control Programs.

Rather than create a standalone tick and tick-borne disease network, the logical approach is to combine all medically important vectors, primarily mosquitoes and ticks, within one comprehensive operational scheme. Such an integrated surveillance and response system is reported to be effective and result in significant cost savings over specific vector and related disease approaches (Wu et al., 2016); 3) establish state and federal partnership to safeguard public health that is also linked to the National Animal Health Laboratory Network (https://www.aphis.usda.gov/aphis/ourfocus/animalhealth/lab-info-services/nahln/ct_national_animal_health_laboratory_network).
Establish interdisciplinary technical committee between the American Medical Association, the Veterinary Medical Association, and the Entomological Society of America (http://www.entsoc.org/PDF/2015/ESA-PolicyStatement-Tick-borneDiseases.pdf) to produce guidance based on state of the science to study and validate tick-borne pathogens and tick vectors.
Establish global tick microbiome consortium similar to the Global Virome Project (http://www.globalviromeproject.org); 2) tick species to be included in tiered approach for further characterization of their microbiomes include the following ixodid vectors of zoonoses in the United States (Eisen, Kugeler, et al., 2017): Amblyomma americanum, Amblyomma maculatum, Dermacentor andersoni, Dermacentoroccidentalis, Dermacentor variabilis, Ixodes pacificus, Ixodes scapularis, and Rhipicephalus sanguineus, Ornithodoros spp., which will enable the systematic identification of microbes potentially pathogenic to humans and animals through further research and testing as described in theme 2 above.
Establish a state and federal tick-borne disease council to develop best practices for maximal dissemination of science-based information, including interactive sites for tick identification in real time.
Study each of the major zoonotic tick-borne diseases in different ecosystems using harmonized protocols to understand the variability in qualitative and quantitative characteristics of ecological drivers.

Votes of Subcommittee Members

The subcommittee unanimously voted yes to accept the list as their potential actions for this priority.

Number in Favor	Number Opposed	Number Abstained	Number Absent
12	0	0	1

Priority 5: The Need for Better Prevention Education, Including Providing Accurate Information and Removing Both Personal and Public Obstacles

Background

Better prevention education, including providing accurate information and removing both personal and public obstacles is the concern of Priority 5. A single tick-bite can result in people being infected with multiple serious diseases, some of which can create a lifetime of debilitating impacts to health, functionality and quality of life (Johnson, Wilcox, Mankoff, & Stricker, 2014) or even result in death. Prevention education is important for all U.S. residents regardless of where they live, work, recreate or travel. Our group of experts agree unanimously that tick-borne diseases can be prevented! However, while most people know something about ticks, their current knowledge or well-intentioned practices are frequently not grounded in evidence or justified by science (“just wrong enough”), thereby leaving them still at risk, or worse, at greater risk because they thought they were taking a preventive action. Educating both health professionals and the public about tick-borne disease prevention, and especially about tick biology and “right enough” best practices for tick bite protection, is a key aspect in helping avoid the many difficulties that can arise for patients following infection from a tick bite. We call for better prevention education which we believe can be achieved by

Conducting a thorough review of funded and unfunded education programs and their outcomes, if assessed, for effective disease prevention.
Requiring but also providing for appropriate resources to conduct robust assessment for all future prevention education projects funded by the federal government.
Recognizing that the tick prevention education needs differ among U.S. geographic regions but that identifying and promoting 5-6 of the most important and science-based “common thread” behavior change and/or best practices for tick bite protection and disease prevention can provide the nucleus of a unified prevention education program.
Investing in social science/health behavior expertise to help identify both general and specific barriers to implementing prevention.
Improving and investing in science communication practices among all groups practicing TBD health promotion so that more unified and science-justified messages are delivered with the highest quality standards, and with a consideration in mind for the hoped for behavior or action.
Developing new user-friendly tools and policies that both motivate and model best behaviors and practices.
Creating funding opportunities for K-12 schools, and public service announcement subsidies for communities to promote “just right enough” tick bite protection and tick-borne disease (TBD) prevention best practices.

Case Study 1 - Not Everyone Knows the Risks

As a professional wildlife biologist that spent the majority of my career working in the outdoors conducting high risk activities (hiking in shrubby grassy areas, working with horses, trapping of both large and small mammals, camping and wildland firefighting) for the United States Forest Service (USDA), I never received training nor awareness of ticks or tick-bite prevention practices or tools. Tick awareness and prevention information was not provided for employees nor visitors on any of the public land units I worked on nor visited for recreational purposes nationwide, nor was prevention a part of my formal education in becoming a professional wildlife biologist. Though agency direction regarding tick-bite prevention for employees can be found in a number of Health and Safety manuals/handbooks, this direction is not consistent among Departments nor between Agencies, and much of the information is outdated, incomplete or incorrect (USDA,USFS; USDI NPS,BLM, USFWS; OSHA). Awareness of this direction, even where it does exist, has not been shared nor implemented consistently in these agencies employing a large number of outdoor working professionals. - Monica White, patient/advocate testimony

Evidence and Findings

Tick bite prevention and control precautions are widely recommended for reducing the transmission of LD and other TBDs (Cartter, Farley, Ardito, & Hadler, 1989; Clark & Hu, 2008; Connally et al., 2009b; Daltroy et al., 2007; de Vries & van Dillen, 2002; Gould et al., 2008b; Hayes & Piesman, 2003; Poland, 2001; Shadick et al., 2016). However, few of the recommended prevention education interventions to reduce tick encounters or tick-borne disease have been thoroughly assessed. Disparities most certainly exist in the level of knowledge, perceived personal risk, and use of preventive measures across the human land-use gradient, suggesting that targeted tick prevention programs may be best suited for reducing behavioral exposure risk and that studies are needed to determine specific gaps in knowledge and prevention among different segments of the population (Bayles, Evans, & Allan, 2013).

With Lyme disease, there is ample evidence (Gould et al., 2008b; Malouin et al., 2003) suggesting that people living in Lyme disease endemic areas already are well-aware of the problem and believe that they are familiar with many of the recommended preventive best practices. Based on these studies, increasing knowledge, alone, does not appear to be effective in getting people to consistently engage in Lyme disease prevention behaviors. It appears necessary to identify particular “barriers” to implementation.

Barriers to implementing tick prevention can be related to age, culture, gender, language, perception of risk, and personal experience. Identifying such barriers may best be achieved through the use of focus group and social marketing surveys conducted with key stakeholder groups (parents, travelers, ESL school nurse educators, advocacy groups, and so forth) (Reid et al., 2013).

However, there is a different group of people that don’t necessarily live in high Lyme endemic areas but who are still at an increased risk for exposure to ticks due to the time spent performing outdoor work, travel to unknown risk areas (ex. military personnel, wildland firefighters, disaster relief workers, transmission line workers, landscapers), having close contact with wildlife (natural resource land managers, ranchers, farmers, and researchers). In addition, public lands which are managed by various State and Federal departments/agencies also provide opportunity for increased tick exposures to the public that use these lands for livestock grazing, woodcutting, hunting, outfitting and guiding, and general outdoor recreation opportunities (hiking, fishing, camping, tourism, and so forth). Public land managers, visitors to public lands, and military personnel are other stakeholder groups in need of greater tick-bite prevention education to reduce exposure to the many diseases that can be transmitted by ticks (Johnson et al., 2014). Unsuspecting visitors’ lack of knowledge of Lyme and other TBDs may put them at increased risk of disease and decreased adherence to prevention practices. There also is a great need for better awareness of existing regionally relevant prevention education. A survey conducted to assess knowledge, attitudes, and practices regarding Lyme disease prevention among employees, day visitors, and campers at Greenbelt Park (Jones, Chanlongbutra, Wong, Cunningham, & Feldman, 2016) revealed that respondents with previous Lyme disease diagnosis were more likely to adhere to tick prevention messages, such as tucking in their pants more often than those without a previous diagnosis. Day visitors were more aware of the risk than campers who tended to travel from further away. Travelers (tourists, wildland firefighters, disaster relief workers, military) may unknowing become infected during their outdoor exposures only to return home to a region of the country or the world that is inexperienced or unknowledgeable about the TBD’s that they may have been exposed to.

Outcomes from tick prevention education studies.

Studies that have embedded elements of social learning theory, or other theory-based approaches suggest that multi-faceted interventions that include i) demonstrating or practicing the desired behavior or practice such as proper tick-checking behavior or other personal protection method (modeling), ii) awareness of the consequences of a tick bite or of having a TBD (perceived susceptibility and severity), and iii) instilling the belief that each person is capable of carrying out preventive behaviors (self-efficacy) may be best for effecting desired prevention behaviors (Connally et al., 2009b; Rosenstock, Strecher, & Becker, 1988; Shadick et al., 2016). In one study among at-risk school children, the health educator not only talked about tick-checking behavior but also demonstrated it and had children replicate it. The children were learning together with peers in their classroom, making it socially acceptable and reinforcing the tick-checking behavior (Shadick et al., 2016). A similarly designed, active school educational program was successful in promoting sun protection behavior among middle school children in Colorado, New Mexico, and Arizona (Buller et al., 2006). In a study of school aged children in the Netherlands, an online educational video game may have offered a complementary role, in addition to other media, in child-specific public health education programs on ticks and Lyme (Beaujean et al., 2016).

Currently, information and materials for tick-bite protection and TBD prevention is disseminated to the public in various formats and structures. That should be a good thing, since health promotion campaigns that use multiple media channels and effectively integrate simple, easily understood messages directing people to more content-rich websites or other readily available resources are more likely to result in adoption of preventive best practices (Glanz, 2002).

Unfortunately, currently in TBD prevention, there is little coordination or consistency in message selection or source, delivery emphasis, or sensitivity to seasonal or spatial dynamics of tick encounter risk. Moreover, few programs use concepts promoting behavior change in a consistent or effective way. Various health promotion models and resources are available to help people at all levels (some work better for adults than for children) engage in behaviors that will prevent a negative health outcome (that is, contract a TBD). For example, one widely-used construct, the Health Belief Model, emphasizes that people must: (1) believe that they are susceptible and likely to fall victim to the disease, (2) believe that the disease has potentially significant adverse consequences for their well-being, (3) believe that preventive behavior is effective, and (4) believe that they have the ability to engage in the preventive behaviors. Additionally, people need to constantly be reminded of the what, when, and how-to of performing the behaviors. The goal of any health promotion effort should be focused on increasing knowledge that leads to the desired behavior/attitude change (that is, effective tick protection and/or disease prevention).

“Common thread” prevention practices.

Subcommittee members voiced overwhelming support for enhancing tick awareness and tick-bite protection education for TBD prevention at all levels from preschool to homeowners, pet owners, outdoor workers, campers, hunters, and others exposed through outdoor activities. We recognize that endemic risk varies regionally in the U.S., but that common thread prevention education and resources are needed everywhere, since people travel for recreation and work. Key prevention education themes should include

How personal protection, in particular, is a tool that can have immediate results in reducing disease risk
Knowing that different types of ticks transmit different disease-causing germs, and what those germs are for the most common types of ticks across North America
Although larger adult stage blacklegged ticks also transmit germs, it is important that people know that nymphal stage blacklegged ticks are the principle vector for germs causing Lyme disease, babesiosis, and anaplasmosis, relapsing fever, and Powassan virus; knowing how tiny and how dangerous nymphs are more effectively promotes enhanced personal protection measures when nymph-stage ticks are most active;
Tools for helping lay audiences better understand the life cycle and seasonal occurrence of the 6 most commonly encountered types of ticks would promote support and implementation of other TBD prevention interventions such as deer reduction, proper pesticide application, or personal protection;
Knowing the habitats where people are and are not at greatest risk for infection with TBDs in different regions and landscape settings would be a critical decision support tool for helping to engage people in adapting preventive behaviors.
Prevention messages should include information on how serious TBDs can be.

Important campaign messages should include: appropriate tick reduction/avoidance strategies, validated vector control strategies (see Priority 2), tick-bite management strategies, tick identification resources, and decision support for taking prevention action. Ideally, the campaign would help residents and visitors know:

Where they are at risk and the likelihood of tick encounters
The habitats and activity seasons of vector ticks
Disease associations with different types of ticks
How to conduct daily tick checks
How to safely remove a tick
How to most effectively repel ticks
How to effectively reduce tick encounter risk in the home environment
How to protect pets from ticks and how to keep pets from carrying ticks to people
The role of wildlife in propagating ticks and disseminating disease agents
That a single tick can carry concurrently more than one disease agent
That all tick bites should be treated seriously

Social science/health promotion collaboration in tick prevention.

Over the past two or more decades, there have been a multitude of Lyme disease prevention programs developed and launched. They range from school-based educational programs to local, state, and even wider prevention campaigns. Initiatives most likely to achieve their desired outcomes are likely to be those based on a clear understanding of targeted health behaviors, and the environmental context in which they occur (Medicine, 2002). Health behavior theory can play a critical role throughout the program planning process and is largely under-utilized in tick prevention education strategies.

Social marketing and health promotion theory gives planners tools for moving beyond intuition to design and evaluate health behavior and health promotion interventions based on understanding of behavior (Glanz, 2002). Using theory as a foundation for program planning and development is consistent with the current emphasis on using evidence-based interventions in public health, behavioral medicine, and medicine. Theory provides a road map for studying problems, developing appropriate interventions, and evaluating their successes. It can inform the planner’s thinking from design, through implementation and on to assessment while offering insights that translate into stronger programs. Theory can also help to explain the dynamics of health behaviors, including processes for changing them, and the influences of the many forces that affect health behaviors, including social and physical environments. Theory can help planners identify the most suitable target audiences, methods for fostering change, and outcomes for evaluation.

Translating tick science to the public.

The importance of deliberately training scientists in the skills of communicating effectively with a layperson audience should not be under-valued. At best, we stand to gain increased engagement and empowerment of tick prevention practices. At the very least, it’s critical not to leave ambiguities that are open to misinterpretation and misrepresentation by the lay audience. Every scientific field has its own jargon, and tick science, with its seemingly complex lifecycles and host associations, variety of germs and taxonomy is rife with uncommon terms. In addition, there’s often a desire among scientists to load any given discussion with all the relevant data rather than communicating just enough to convey an accurate understanding of the findings. There also seems to be a growing science literacy deficit among the lay public. Science communication is a craft, and most scientists need specific training in communicating effectively with lay audiences; when scientists translate their findings to the general public, it should not just be a dumber version of their original. Enough details matter and use of everyday terms should become best practice for all (Bucchi, 2008).

Scientists rarely receive any explicit training in communicating scientific concepts to a layperson audience. There is a growing call for incorporating formal science communications training into the undergraduate and graduate curricula of aspiring scientists to enhance the discourse between scientists and the lay public (Brownell, Price, & Steinman, 2013a). Building effective lay audience communication skills is a difficult endeavor but limited studies are encouraging; in one study, science-major undergrads and research graduate students were found to be extremely receptive to the additional communication elements added to their basic science courses, and significant gains in student perception and confidence of their communication skills were noted. Student attitudes about the importance of communicating their science to the general public were extremely positive (Brownell, Price, & Steinman, 2013b).

CDC currently offers six online health literacy courses for health professionals as well as access to tool kits and other resources (https://www.cdc.gov/healthliteracy/gettraining.html), and wider use of these tools in tick prevention education should be encouraged.

Motivating and modeling best practices.

Short videos and other new media products, especially those portraying members of the target audience, can be helpful in providing more specific “how to” decision support, and can readily be downloaded from media sites like YouTube (https://www.youtube.com/watch?v=cRpaYjGW0zY). However, it must be stressed that any tick prevention promotion should be focused on science-based best practices.

State and Federal public land managers (nature interpreters, park rangers, visitor information specialists, campground hosts, and so forth) spend much time interfacing with public land users. Employees of these agencies can have direct impact on visitors to these public lands through modeling of behavior and motivating implementation of best practices using targeted prevention outreach programs (Wong & Higgins, 2010). In addition, State and Federal natural resource agencies can motivate and model best practices for their employees through development or revision of existing tick prevention guidelines (safety manuals and handbooks) and implementation of safety incentives for integrating these best practices into agency trainings, safety tailgate sessions or Job Hazard Analysis (JHAs).

In general, campaigns utilizing multiple media channels that effectively integrate simple, easily understood messages directing people to more content-rich websites or other readily available resources are more likely to result in adoption of preventive best practices.  

Build partnerships through collaborating with educators (K-12 and beyond), healthcare providers/directors, public land managers, pest control and IPM, and private corporations that have developed or are developing tick repellents, education tools, and other products aimed at preventing tick encounters, to ensure that marketing materials all reflect best practices and science-based content. Develop incentive programs for those that model and/or promote best practices in their schools, workplaces or health insurance or patient centers.

Lyme and other non-profit TBD awareness organizations have long been champions for helping people suffering with disease. Because of their targeted market reach, significant efforts should be made to insure that Lyme/TBD non-profits receive or have access to training and sharing best practice tick prevention information.

Tick prevention tools and subsidies for schools.

Children have a higher risk of exposure to ticks through the nature of their activities in outdoor environments. Reported cases of Lyme disease are most common among boys aged 5-9 (CDC, 2017c). Tick-bite prevention education based on best practices needs to be both accurate and accessible for children at school, organized outdoor education and recreation activities, and within their families to reduce the rate of tick-borne disease infections in children. Prevention education that reaches and extends beyond K-12 to “normalize” the behaviors that reduce risk to tick-bites would further model the best practices desired in future generations.

Table 6. Tick Awareness/Prevention Learning Kits for K-12

Kit Name	Developer	Intended age/grade	Assessed	Status
What is Lyme disease	Lyme Disease Assoc (LDA)	Middle (6-7)	no	available
Tick-er tape parade	LDA	Middle (6-7)	no	available
Keeping ticks at bay	LDA	Middle (6-7)	no	available
Testing and treatment	LDA	Middle (6-7)	no	available
Daily Tick Check	TickEncounter	Elementary (3-4)	no	available
Is It A Tick?	TickEncounter	Elementary (2-3)	no	In development
TickSpotters4Schools	TickEncounter	Middle (6-7)	no	In development
Tick PSA	TickEncounter	Middle (7-8)	no	In development
Elementary School Education	Global Lyme Alliance (GLA)	Elementary (K-2)	no	available
Elementary School Education	GLA	Elementary	no	available
Middle School Education	GLA	Middle (6-8)	no	available
High School Education	GLA	High School (9-12)	no	available
NY State	NYS Education	K-12	In process	In process
TickSense	Bay Area Lyme	Middle (5-6)	No	available
Don’t Let the Ticks Bite	ME Center for Disease Control	Elementary (3-5)	No	available

Opportunities

The five Centers for Disease Control and Prevention Regional Centers of Excellence for Vector-borne Diseases (COE VBD) are unique collaborative research and training consortia comprised of academic researchers, departments of health, agriculture experiment stations and others. These centers are charged with helping to generate the necessary knowledge and capacity to enable appropriate and timely public health action for VBD throughout the U.S. Establishing these COEs represent an outstanding first step for responding appropriately to the emerging TBD threat. Among other parts of their mission, in the area of tick prevention education, they could

provide a workforce of tick experts supporting novel crowd-sourced tick surveillance nationally
perform applied research to assess products and programs aimed at preventing tick encounters
be trained in and practice effective science communication for translating science-based risks and solutions to lay audiences.

The COEs represent a great and largely under-utilized resource in the area of tick prevention education.

Finding a tick biting (or crawling on your clothes or in your home) is perhaps one of the most engage-able moments for tick prevention education. More than just a crowd-sourced tick survey, TickSpotters (www.tickencounter.org/tickspotters/submit_form or mobile www.tickspotters.org) is also a fast and free digital portal providing people access to a tick expert as well as expert tick prevention education. Every digital submission gets a response guiding tick encounter victims to best next action resources, but all submissions that include a clear picture get a tick identification confirmation, and a personalized riskiness assessment based on the type of tick, its feeding status, and the likely location it was acquired. Those submissions also get their response, usually within 24 hours, containing TickSmart best next actions and future tick prevention recommendations tailored to the tick encounter scenario and any other information provided. Having already serviced 44,000 submissions, the geo-referenced database stands to provide a rich source of information on peoples’ tick encounter experiences and effectiveness of tick prevention education messages. There are many other citizen science driven programs (TickReport, I-Tick, Bay Area Lyme Foundation, Ticknology, TickTracker App and others) striving to increase tick surveillance and prevention education through public participation. Collaboration between all of these programs potentially could provide both better data and prevention messaging.

Closing the current large gap between the knowledge and accomplishments of tick scientists and the needs of the lay public at risk represents a largely untouched opportunity. Effective behavior change and adoption may lay in the power of relationships, and something that commercial marketers know well is that branding is nothing more or less than a relationship (McDivitt, 2003). Brands can be thought of as a “container of possibilities,” with the most trusted brands holding the greatest possibilities. Part of following a social marketing approach to better tick prevention education, is to promote distinctive brands that have adopted consensus best prevention practices and that i ) contain core call-to-action messages; ii) use social marketing-based strategies for removing implementation barriers; and iii) consistently promote science-based tools and actions that use clear, stakeholder-appropriate messaging (school-age children, adults working with school-age children, outdoor workers, homeowners, pet owners, people engaging in higher tick risk recreational activities, and so forth).

Community partnerships and citizen volunteer buy-in are likely to be critical to the success of state- or region-wide social marketing campaigns for implementing effective tick bite protection for preventing TBDs. One goal of the campaign should be to align as many stakeholder groups and interests (town Boards of Health, school nurse educators, veterinary clinics, camp directors, state and local parks and recreation departments, Lyme and TBD advocacy and support groups, local business owners, healthcare providers, and so forth) into a cohesive group under the guidance of a single initiative. Identification of critical elements including highly credible sources of evidence-based information used in developing campaign messages, and a readily identifiable “branding” for all components of the campaign (that is, TickSmart, BLAST, other). Forming strategic alliances and brand penetration will help promote further media promotion, sustainability, and resource development, all critical to maximizing reach and success of the campaign.

State Medical Societies should be encouraged to develop a user-friendly resource (Physician TBD Prevention Primer) and CME programs, to promote provider involvement in prevention. Veterinary health care providers also should be included in the prevention effort; a model hybrid in-person/on-line TickSmartä Certification training program recently was launched for veterinarians and vet techs to earn CME credits. Another method to effectively and economically disseminate information on prevention is to involve health care insurers who frequently send messages on health promotion and disease prevention.

Professional pest control operators (PCOs) should be considered first-line responders to the tick infestation facing communities, neighborhoods, and individual households; as such this group has a professional and moral obligation to comply with best practice standards, including application of validated effective products and methods of application. The opportunity for tick prevention education within this group could be tied to state PCO licensure and renewal.

Development of a Federal service-wide tick-borne diseases prevention program, with an emphasis on providing standardized guidance and educational materials that can be utilized and tailored by individual parks, monuments, forests, military bases, and other publicly managed lands to meet their needs for both employees of these departments and the public land users. Revision or addendum of existing federal agencies’ Health & Safety Manuals/Handbooks for employees that can be used to develop Job Hazard Analysis, Tailgate Safety Sessions, seasonal employee trainings, and other documented safety messaging and practices.

Educational signs alerting public to the risk of ticks at recreation areas, kiosks, trailheads, picnic grounds, and camping areas. The use of billboards and mobile programmable signs with simple prevention messages are another potential tool for increasing awareness of ticks to masses of people; especially travelers.

Threats or Challenges

Results from nationally representative HealthStyles surveys conducted in 2009, 2011, and 2012 indicate that exposure to ticks is common (21% of households report at least one tick encounter annually), and awareness of LD is widespread especially in the highly endemic northeastern U.S. Nevertheless, use of TBD prevention measures is relatively infrequent among the U.S. public (Hook, Nelson, & Mead, 2015), and highlights the need to better understand barriers to using effective prevention measures. We believe that one such potential barrier originates from the rampant re-stating of misinformation on the internet and even by well-meaning media resources; omission, misinterpretation or misstating of science-based findings by entities of public trust (for example, Federal and state Department of Health, academicians, and so forth) commonly leads to conflicted knowledge and perceptions among the lay public who rarely have ready access to a credible arbiter to provide perspective. For example, anecdotal evidence from over 40,000 tick encounter self-reports to a crowd-sourced tick survey (TickSpotters), suggests an exceptionally low degree of tick literacy. Lack of accurate tick identification skills coupled with misinformed knowledge and practices among a large proportion of tick-bite victims and their health practitioners, if uncorrected, could lead to even greater risk for TBDs; taking a “just wrong enough” action could result in an unwarranted sense of protection.

Though many prevention programs have been developed specifically for Lyme disease, there are few programs that address the risk of tick bites in general. Much of what has been developed lacks regional relevance for areas of the country that are not known to be endemic for blacklegged ticks, and yet risks of many other serious and potentially deadly diseases from alternate vectors in these regions exist. Lack of perceived risk has hindered surveillance activities, awareness and prevention education for these regions. The public within these regions are in need of prevention education that is both relevant to their region of residency as well as addressing the elevated risk of Lyme and other TBDs disease with travel.

Case Study 2 – Misinformation Barrier

The science - Hosts as ecological traps for the vector of Lyme disease. Keesing et al., Proc Biol Sci 2009

The findings - we found that some host species (for example, opossums, squirrels) that are abundantly parasitized in nature kill 83–96% of the ticks that attempt to attach and feed, while other species are more permissive of tick feeding.

The Twitter feed…

But take a look at just a couple of the thousands of tweeter posts…

“Saw an opossum in my yard and thought Yay it'll eat all the ticks.” @joyochs

“My son works in Oneonta and told me he had 2 ticks on him Thursday before the storm. He thought the cold killed them, but they don't. Wanted to know what does & I said get a Goose or an Opossum, don't rely on the State to spray!”- @Norie57

The Outcome – The Health Belief Model purports that people will more likely carry out a practice if they have confidence it will work, and mixed messages, such as the hope from helpful opossums, likely shake that confidence - people may not take effective preventive action.

Social media is a powerful tool and is full of recommendations regarding “natural” and “do-it-yourself” recipes and methods for repelling, removing, and controlling ticks that are not based in science nor supported by objective evidence. People are potentially at greater risk of tick exposure and diseases by following what they determine for themselves or believe to be “best practices”. Even credible arbiters may be presenting information that can be misinterpreted due to the complexity of tick biology, distribution and behavior (see Case Study 2). Tick questing and feeding behavior, regional distribution maps, seasonal occurrence, and disease transmission times all can vary making having an absolute message challenging. Even the same species of tick (Ixodes scapularis) may transmit different microbes to a host at different rates (Dolan et al., 2017; Ebel & Kramer, 2004).

Many of the “best practices” that current prevention education and messages promote is the use of repellents, the majority of which are made with chemicals (CDC, 2016; EPA, 2017). Though the effectiveness of using protective clothing (permethrin) and skin repellents is high for the prevention of tick-bites (CDC, 2017c; EPA, 2017; Ford, Nadolny, Stromdahl, & Hickling, 2015), the use of chemicals (either on skin or on clothing) are not yet widely accepted nor implemented regularly for tick prevention. In a survey conducted at the Greenbelt National Park (Jones et al., 2016), it was found that less than half of the survey participants usually or always used repellent preventive measures (permethrin-impregnated clothing, skin treatment). Employees at Greenbelt Park reported not taking repellent-related prevention measures because they did not like the way repellent smelled or felt, they were concerned about repellent safety, it was hard to remember to use repellent, or they were unaware of repellent-based preventive measures. Because of examples like this, development of prevention education must therefore take into consideration attitudes, concerns, and ease of implementation to achieve behavior change of the target audiences.

Significant additional resources and incentives will likely be needed to fund collaborations between tick scientists and social scientist with expertise in social marketing and behavior change theory, and to increase effective science communications to lay audiences.

In the absence of standardized best practices for tick management across all regions, PCOs are left without guidance regarding science-based recommendations for products, methods, and practices, all of which may impede development of effective continuing education materials.

Potential Actions

Focus future tick prevention education on those practices and activities with positively measured outcomes such as reductions in the number of ticks found on study participants or outcomes related to the tick encounters (bites, disease) a documented increase in knowledge, or the adoption of specific prevention behaviors; encourage a pipeline of innovation to science-based prevention education by providing additional funding for practitioners (both individuals and entities) proposing to conduct objective assessments of their intervention or tool.
Recommend significant additional funding for CDC-supported regional Centers of Excellence in Vectorborne Disease (COEs) to expand their training, internship, and cross-discipline collaboration opportunities in high priority tick prevention education programs, including: servicing national crowd-sourced tick surveillance programs, conducting health promotion and social marketing studies, conducting applied studies to validate or dispel commonly promoted tools and strategies for tick prevention, and science communications training.
Incentivize innovation in best K-12 learning practices as well as evaluate the effectiveness of available and new learning kit resources.
Invest in programs that already effectively link the best of tick science to peoples’ lived experiences with ticks (that is, Cooperative Extension, academic-based tick prevention resources, advocacy groups), and update existing regionally- and occupationally-relevant targeted public health intervention programs (including federal agency safety manuals and handbooks) to reduce physical and behavioral tick exposure risk by addressing specific gaps in knowledge and prevention.
Develop best practice tick control training materials (on-line training, videos) for PCOs, and make continuing education (CE) compliance a requirement for continuing PCO licensure.

Minority Response: Investment in Prevention Programs (Bullet 4)

As the report mentions, there are established programs which are dedicated or charged with furthering prevention education, many of which have been in existence decades (for example, Cooperative Extension, academic-based tick prevention resources). Many of the existing programs and resources are focused in regions where the black-legged tick is prevalent and the risk of Lyme disease is high, leaving a large portion of the country lacking both the awareness and resources necessary for prevention relevant in their home states and for their travel experiences to higher prevalence regions.

Unfortunately, these existing programs and resources have been ineffective in reaching people that live in many perceived low tick or tick-borne disease incidence states. People that live in low incidence states lack awareness needed to practice prevention and to access accurate and timely diagnosis and treatment for tick-borne diseases. Tick-borne disease prevention is a relevant issue for all people regardless of where they live, work, recreate or travel. Investment in programs already established and investment in new innovative or regionally relevant programs that can link the best science to peoples' actual experiences with ticks is essential to improving prevention education nationwide. Restricting investment to only already established programs may reduce opportunity for improved prevention programs and resources in regions or states with low tick and tick-borne disease incidence, leaving a huge segment of the population uneducated and unprepared for the growing risks of tick-borne diseases nationally.

Votes of Subcommittee Members

The subcommittee unanimously voted yes to accept the list of potential actions for this priority.

Number in Favor	Number Opposed	Number Abstained	Number Absent
12	0	0	1

The subcommittee, however, did not reach a consensus regarding the wording in the fourth action. (7-3-2abstain-1A). While the majority of the attending subcommittee members agreed to accept this specific action as it is, three other members noted that the word “already” should be removed from this action, and they subsequently provided their minority response, above).

Discussion

Big Picture summary

Tick-borne diseases represent a highly significant and emerging public health concern in the U.S. According to a report just released by CDC (Rosenberg et al., 2018), tick-borne diseases have more than doubled in the last 13 years and now represent 77% of all reported vector-borne diseases in the U.S. The number of new Lyme disease cases alone in the U.S. has been estimated to exceed 300,000 new cases per year (Hinckley et al., 2014; Nelson et al., 2015). Efforts to prevent and control novel and emerging tick-borne diseases are hindered by a number of challenges. Due to the lack of a coordinated national tick vector surveillance program, there are significant gaps in information on local distribution of tick vectors. This information is badly needed for educating the public health community, health care providers and the general public about local disease risk. There is also a need to better understand the pathogens and vectors associated with tick-borne diseases, particularly in the southern and western U.S. highlighted by the recent discovery in New Jersey of the exotic tick vector species Haemaphysalis longicornis; there are ongoing concerns about the risk of introduction of both exotic tick species and pathogens. Under-reporting and inconsistencies in surveillance data from state to state and from year to year significantly hamper efforts to raise public awareness of the magnitude of the problem and provide data needed to evaluate prevention effectiveness. New methods and products are badly needed for killing and repelling ticks as well as controlled field trials that measure epidemiologic outcomes in order to provide data-driven prevention recommendations. Finally, current federal funding to support surveillance and prevention activities, as well as basic and applied research on tick biology, ecology, and control is severely inadequate to address one of the largest public health problems in the U.S.

Limitations

There were two primary challenges the subcommittee faced in completing this report. The first was a lack of adequate time to research, draft, review, discuss, and revise important report content prior to voting on the final version. A second challenge related to the limitations on the numbers of issues, questions, and priorities that could be addressed in this report. It is the hope of this subcommittee that future reports that are drafted in subsequent years as an activity of the Working Group will address additional questions and needs that were not covered in the current report due to challenges and limitations stated above.

References

Adalsteinsson, S. A., Shriver, W. G., Hojgaard, A., Bowman, J. L., Brisson, D., D'Amico, V., & Buler, J. J. (2018). Multiflora rose invasion amplifies prevalence of Lyme disease pathogen, but not necessarily Lyme disease risk. Parasit Vectors, 11(1), 54. doi:10.1186/s13071-018-2623-0

Addiss, S. S., Alderman, N. O., Brown, D. R., & Wargo, J. (1999). A survey of private drinking water wells for lawn and tree care pesticides in a Connecticut town: Environment and Human Health, Inc.

Allan, B. F., Dutra, H. P., Goessling, L. S., Barnett, K., Chase, J. M., Marquis, R. J., . . . Orrock, J. L. (2010). Invasive honeysuckle eradication reduces tick-borne disease risk by altering host dynamics. Proc Natl Acad Sci U S A, 107(43), 18523-18527. doi:10.1073/pnas.1008362107

Allan, B. F., Keesing, F., & Ostfeld, R. S. (2003). Effect of Forest Fragmentation on Lyme Disease Risk. Conservation Biology, 17(1), 267-272.

Anderson, J. F., & Sonenshine, D. E. (2014). Mouthparts and digestive system: anatomy and molecular biology of feeding and digestion Biology of Ticks (Vol. 1, pp. 122-162). New York, NY: Oxford Universtiy Press.

Apperson, C. S., Levine, J. F., Evans, T. L., Braswell, A., & Heller, J. (1993). Relative utilization of reptiles and rodents as hosts by immature Ixodes scapularis (Acari: Ixodidae) in the coastal plain of North Carolina, USA. Exp Appl Acarol, 17(10), 719-731.

Arsnoe, I. M., Hickling, G. J., Ginsberg, H. S., McElreath, R., & Tsao, J. I. (2015). Different populations of blacklegged tick nymphs exhibit differences in questing behavior that have implications for human lyme disease risk. PLoS One, 10(5), e0127450. doi:10.1371/journal.pone.0127450

Bacon, R. M., Biggerstaff, B. J., Schriefer, M. E., Gilmore, R. D., Jr., Philipp, M. T., Steere, A. C., . . . Johnson, B. J. B. (2003). Serodiagnosis of Lyme Disease by Kinetic Enzyme-Linked Immunosorbent Assay Using Recombinant VlsE1 or Peptide Antigens of Borrelia burgdorferi Compared with 2-Tiered Testing Using Whole-Cell Lysates. The Journal of Infectious Diseases, 187, 1187-1199.

Bakken, L. L., Callister, S. M., Wand, P. J., & Schell, R. F. (1997). Interlaboratory comparison of test results for detection of Lyme disease by 516 participants in the Wisconsin State Laboratory of Hygiene/College of American Pathologists Proficiency Testing Program. J Clin Microbiol, 35(3), 537-543.

Baneth, G. (2014). Tick-borne infections of animals and humans: a common ground. Int J Parasitol, 44(9), 591-596. doi:10.1016/j.ijpara.2014.03.011

Barbour, A. G., & Fish, D. (1993). The biological and social phenomenon of Lyme disease. Science, 260(5114), 1610-1616.

Bayles, B. R., Evans, G., & Allan, B. F. (2013). Knowledge and prevention of tick-borne diseases vary across an urban-to-rural human land-use gradient. Ticks Tick Borne Dis, 4(4), 352-358. doi:10.1016/j.ttbdis.2013.01.001

Beard, C. B., Eisen, R. J., Barker, C. M., Garofalo, J. F., Hahn, M., Hayden, M., . . . Schramm, P. J. (2016) Impacts of Climate Change on Human Health in the United States: A Scientific Assessment (pp. 129-156). Washington DC: Skyhorse Publishing.

Beaujean, D. J., Gassner, F., Wong, A., Steenbergen, J. E., Crutzen, R., & Ruwaard, D. (2016). Education on tick bite and Lyme borreliosis prevention, aimed at schoolchildren in the Netherlands: comparing the effects of an online educational video game versus a leaflet or no intervention. BMC Public Health, 16(1), 1163. doi:10.1186/s12889-016-3811-5

Beck, D. L., Zavala, J., Montalvo, E. O., & Quintana, F. G. (2011). Meteorological indicators for Amblyomma cajennense and population dynamics in the Tamaulipan Biotic Province in Texas. J Vector Ecol, 36(1), 135-146. doi:10.1111/j.1948-7134.2011.00150.x

Bensaci, M., Bhattacharya, D., Clark, R., & Hu, L. T. (2012). Oral vaccination with vaccinia virus expressing the tick antigen subolesin inhibits tick feeding and transmission of Borrelia burgdorferi. Vaccine, 30(42), 6040-6046. doi:10.1016/j.vaccine.2012.07.053

Bharadwaj, A., & Stafford III, K. C. (2010). Evaluation of Metarhizium anisopliae strain F52 (Hypocreales: Clavicipitaceae) for control of Ixodes scapularis (Acari: Ixodidae). Journal of Medical Entomology, 47(5), 862-867.

Bharadwaj, A., Stafford, K. C., 3rd, & Behle, R. W. (2012). Efficacy and environmental persistence of nootkatone for the control of the blacklegged tick (Acari: Ixodidae) in residential landscapes. J Med Entomol, 49(5), 1035-1044.

Bishop, F., & Trembley, H. L. (1945). Distribution and hosts of certain North American ticks. J. Parasitol., 31(1), 1-54.

Bjork, J., Brown, C., Friedlander, H., Schiffman, E., & Neitzel, D. (2018). Validation of Random Sampling as an Estimation Procedure for Lyme Disease Surveillance in Massachusetts and Minnesota. Zoonoses Public Health, 65(2), 266-274. doi:10.1111/zph.12297

Bonnet, S. I., Binetruy, F., Hernandez-Jarguin, A. M., & Duron, O. (2017). The Tick Microbiome: Why Non-pathogenic Microorganisms Matter in Tick Biology and Pathogen Transmission. Front Cell Infect Microbiol, 7, 236. doi:10.3389/fcimb.2017.00236

Bouchard, C., Beauchamp, G., Leighton, P. A., Lindsay, R., Belanger, D., & Ogden, N. H. (2013). Does high biodiversity reduce the risk of Lyme disease invasion? Parasit Vectors, 6, 195. doi:10.1186/1756-3305-6-195

Braks, M., Medlock, J. M., Hubalek, Z., Hjertqvist, M., Perrin, Y., Lancelot, R., . . . Sprong, H. (2014). Vector-borne disease intelligence: strategies to deal with disease burden and threats. Front Public Health, 2, 280. doi:10.3389/fpubh.2014.00280

Branda, J. A., & Rosenberg, E. S. (2013). Borrelia miyamotoi: a lesson in disease discovery. Ann Intern Med, 159(1), 61-62. doi:10.7326/0003-4819-159-1-201307020-00009

Brei, B., Brownstein, J. S., George, J. E., Pound, J. M., Miller, J. A., Daniels, T. J., . . . Fish, D. (2009). Evaluation of the United States Department Of Agriculture Northeast Area-wide Tick Control Project by meta-analysis. Vector Borne Zoonotic Dis, 9(4), 423-430. doi:10.1089/vbz.2008.0150

Breitschwerdt, E. B., Maggi, R. G., Nicholson, W. L., Cherry, N. A., & Woods, C. W. (2008). Bartonella sp. bacteremia in patients with neurological and neurocognitive dysfunction. J Clin Microbiol, 46(9), 2856-2861. doi:10.1128/JCM.00832-08

Brown, R. N., & Lane, R. S. (1992). Lyme disease in California: a novel enzootic transmission cycle of Borrelia burgdorferi. Science, 256(5062), 1439-1442.

Brownell, S. E., Price, J. V., & Steinman, L. (2013a). Science Communication to the General Public: Why We Need to Teach Undergraduate and Graduate Students this Skill as Part of Their Formal Scientific Training. J Undergrad Neurosci Educ, 12(1), E6-E10.

Brownell, S. E., Price, J. V., & Steinman, L. (2013b). A writing-intensive course improves biology undergraduates' perception and confidence of their abilities to read scientific literature and communicate science. Adv Physiol Educ, 37(1), 70-79. doi:10.1152/advan.00138.2012

Brownstein, J. S., Holford, T. R., & Fish, D. (2003). A climate-based model predicts the spatial distribution of the Lyme disease vector Ixodes scapularis in the United States. Environ Health Perspect, 111(9), 1152-1157.

Bucchi, M. (2008). Handbook of public communication of science and technology New York, New York: Routledge.

Buller, D. B., Taylor, A. M., Buller, M. K., Powers, P. J., Maloy, J. A., & Beach, B. H. (2006). Evaluation of the Sunny Days, Healthy Ways sun safety curriculum for children in kindergarten through fifth grade. Pediatr Dermatol, 23(4), 321-329. doi:10.1111/j.1525-1470.2006.00270.x

Burgdorfer, W. (1969). Ecology of tick vectors of American spotted fever. Bull World Health Organ, 40(3), 375-381.

Burgdorfer, W., Barbour, A. G., Hayes, S. F., Benach, J. L., Grunwaldt, E., & Davis, J. P. (1982). Lyme disease-a tick-borne spirochetosis? Science, 216(4552), 1317-1319.

Burkot, T. R., Maupin, G. O., Schneider, B. S., Denatale, C., Happ, C. M., Rutherford, J. S., & Zeidner, N. S. (2001). Use of a sentinel host system to study the questing behavior of Ixodes spinipalpis and its role in the transmission of Borrelia bissettii, human granulocytic ehrlichiosis, and Babesia microti. Am J Trop Med Hyg, 65(4), 293-299.

Burkot, T. R., Schneider, B. S., Pieniazek, N. J., Happ, C. M., Rutherford, J. S., Slemenda, S. B., . . . Zeidner, N. S. (2000). Babesia microti and Borrelia bissettii transmission by Ixodes spinipalpis ticks among prairie voles, Microtus ochrogaster, in Colorado. Parasitology, 121 Pt 6, 595-599.

Cabezas-Cruz, A., Vayssier-Taussat, M., & Greub, G. (2018). Tick-borne pathogen detection: what's new? Microbes Infect. doi:10.1016/j.micinf.2017.12.015

CALDA. (2005). CDC Survey Results. The Lyme Times, 41, 36. Retrieved from https://www.lymedisease.org/members/lyme-times/archive/2005-spring-toc/

CAPA. (2014). Parasite Prevalence Map. Retrieved from www.petsandparasites.org/parasite-prevalence-maps - 2017/all/lyme-disease/dog/united-states/),

Carroll, J. F., Allen, P. C., Hill, D. E., Pound, J. M., Miller, J. A., & George, J. E. (2003). Control of Ixodes scapularis and Amblyomma americanum through use of the ‘4-poster’treatment device on deer in Maryland Ticks and Tick-Borne Pathogens (pp. 289-296): Springer, Dordrecht.

Cartter, M. L., Farley, T. A., Ardito, H. A., & Hadler, J. L. (1989). Lyme disease prevention--knowledge, beliefs, and behaviors among high school students in an endemic area. Conn Med, 53(6), 354-356.

Cartter, M. L., Lynfield, R., Feldman, K. A., Hook, S. A., & Hinckley, A. F. (2018). Lyme disease surveillance in the United States: Looking for ways to cut the Gordian knot. Zoonoses Public Health, 65(2), 227-229. doi:10.1111/zph.12448

CDC. (2016). Natural Tick Repellents and Pesticides. Retrieved from https://www.cdc.gov/lyme/prev/natural-repellents.html

CDC. (2017a). Lyme Disease (Borrelia burgdorferi) 2017 Case Definition. Retrieved from https://wwwn.cdc.gov/nndss/conditions/lyme-disease/case-definition/2017/

CDC. (2017b). Morbidity and Mortality Weekly Report (MMWR). Retrieved from https://www.cdc.gov/mmwr/about.html

CDC. (2017c). Preventing Tick-Bites on People. Retrieved from https://www.cdc.gov/lyme/prev/on_people.html

CDPHE. (2016). Colorado Department of Public Health and Environment. Retrieved from https://docs.google.com/document/d/1OrQPQj9KNNAz7AfD3W7nsqvc-5ZfYt7wRB_9Fnvoyqg/pub

Chan, Y. G., Cardwell, M. M., Hermanas, T. M., Uchiyama, T., & Martinez, J. J. (2009). Rickettsial outer-membrane protein B (rOmpB) mediates bacterial invasion through Ku70 in an actin, c-Cbl, clathrin and caveolin 2-dependent manner. Cell Microbiol, 11(4), 629-644. doi:10.1111/j.1462-5822.2008.01279.x

Childs, J. E., & Paddock, C. D. (2003). The ascendancy of Amblyomma americanum as a vector of pathogens affecting humans in the United States. Annu Rev Entomol, 48, 307-337. doi:10.1146/annurev.ento.48.091801.112728

Clark, K. (2004). Borrelia species in host-seeking ticks and small mammals in northern Florida. J Clin Microbiol, 42(11), 5076-5086. doi:10.1128/JCM.42.11.5076-5086.2004

Clark, K., Hendricks, A., & Burge, D. (2005). Molecular identification and analysis of Borrelia burgdorferi sensu lato in lizards in the southeastern United States. Appl Environ Microbiol, 71(5), 2616-2625. doi:10.1128/AEM.71.5.2616-2625.2005

Clark, K. L., Leydet, B., & Hartman, S. (2013). Lyme borreliosis in human patients in Florida and Georgia, USA. Int J Med Sci, 10(7), 915-931. doi:10.7150/ijms.6273

Clark, R. P., & Hu, L. T. (2008). Prevention of lyme disease and other tick-borne infections. Infect Dis Clin North Am, 22(3), 381-396, vii. doi:10.1016/j.idc.2008.03.007

Clayton, J. L., Jones, S. G., Dunn, J. R., Schaffner, W., & Jones, T. F. (2015). Enhancing Lyme Disease Surveillance by Using Administrative Claims Data, Tennessee, USA. Emerg Infect Dis, 21(9), 1632-1634. doi:10.3201/eid2109.150344

Clow, K. M., Leighton, P. A., Ogden, N. H., Lindsay, L. R., Michel, P., Pearl, D. L., & Jardine, C. M. (2017). Northward range expansion of Ixodes scapularis evident over a short timescale in Ontario, Canada. PLoS One, 12(12), e0189393. doi:10.1371/journal.pone.0189393

Cohen, M. A. (2004). Lyme Disease Update: Science, Policy and Law: Lyme Disease Association.

Coimbra-Dores, M. J., Maia-Silva, M., Marques, W., Oliveira, A. C., Rosa, F., & Dias, D. (2018). Phylogenetic insights on Mediterranean and Afrotropical Rhipicephalus species (Acari: Ixodida) based on mitochondrial DNA. Exp Appl Acarol. doi:10.1007/s10493-018-0254-y

Coleman, J. L., Gebbia, J. A., Piesman, J., Degen, J. L., Bugge, T. H., & Benach, J. L. (1997). Plasminogen is required for efficient dissemination of B. burgdorferi in ticks and for enhancement of spirochetemia in mice. Cell, 89(7), 1111-1119.

Conant, J. L., Powers, J., Sharp, G., Mead, P. S., & Nelson, C. A. (2018). Lyme Disease Testing in a High-Incidence State: Clinician Knowledge and Patterns. Am J Clin Pathol, 149(3), 234-240. doi:10.1093/ajcp/aqx153

Connally, N. P., Durante, A. J., Yousey-Hindes, K., Meek, J. I., Nelson, R., & Heimer, R. (2009a). Peridomestic Lyme disease prevention: results of a population-based case control study. American Journal of Preventive Medicine, 37(3), 201-206.

Connally, N. P., Durante, A. J., Yousey-Hindes, K. M., Meek, J. I., Nelson, R. S., & Heimer, R. (2009b). Peridomestic Lyme disease prevention: results of a population-based case-control study. Am J Prev Med, 37(3), 201-206. doi:10.1016/j.amepre.2009.04.026

Cosentino, S., Voldby Larsen, M., Moller Aarestrup, F., & Lund, O. (2013). PathogenFinder--distinguishing friend from foe using bacterial whole genome sequence data. PLoS One, 8(10), e77302. doi:10.1371/journal.pone.0077302

Coulter, P., Lema, C., Flayhart, D., Linhardt, A. S., Aucott, J. N., Auwaerter, P. G., & Dumler, J. S. (2005). Two-year evaluation of Borrelia burgdorferi culture and supplemental tests for definitive diagnosis of Lyme disease. J Clin Microbiol, 43(10), 5080-5084. doi:10.1128/JCM.43.10.5080-5084.2005

Craft, J. E., Fischer, D. K., Shimamoto, G. T., & Steere, A. C. (1986). Antigens of Borrelia burgdorferi recognized during Lyme disease. Appearance of a new immunoglobulin M response and expansion of the immunoglobulin G response late in the illness. J Clin Invest, 78(4), 934-939. doi:10.1172/JCI112683

CSTE List of Nationally Notifiable Conditions. (2013). Retrieved from https://c.ymcdn.com/sites/cste.site-ym.com/resource/resmgr/CSTENotifiableConditionListA.pdf

Cumming, G. S., & Van Vuuren, D. P. (2006). Will climate change affect ectoparasite species ranges? Global Ecology and Biogeography, 15(5), 486-497.

Curran, K. L., Fish, D., & Piesman, J. (1993). Reduction of nymphal Ixodes dammini (Acari: Ixodidae) in a residential suburban landscape by area application of insecticides. Journal of Medical Entomology, 30(1), 107-113.

Daltroy, L. H., Phillips, C., Lew, R., Wright, E., Shadick, N. A., & Liang, M. H. (2007). A controlled trial of a novel primary prevention program for Lyme disease and other tick-borne illnesses. Health Educ Behav, 34(3), 531-542. doi:10.1177/1090198106294646

Damrow, T., Freedman, H., Lane, R. S., & Preston, K. L. (1989). Is Ixodes (ixodiopsis) angustus a vector of Lyme disease in Washington State? West J Med, 150(5), 580-582.

Daniels, T. J., Fish, D., & Falco, R. C. (1991). Evaluation of host-targeted acaricide for reducing risk of Lyme disease in southern New York state. Journal of Medical Entomology, 28(4), 537-543.

Daniels, T. J., Fish, D., & Schwartz, I. (1993). Reduced abundance of Ixodes scapularis (Acari: Ixodidae) and Lyme disease risk by deer exclusion. J Med Entomol, 30(6), 1043-1049.

Dantas-Torres, F., Latrofa, M. S., Annoscia, G., Giannelli, A., Parisi, A., & Otranto, D. (2013). Morphological and genetic diversity of Rhipicephalus sanguineus sensu lato from the New and Old Worlds. Parasit Vectors, 6, 213. doi:10.1186/1756-3305-6-213

Davis, G. E., & Cox, H. R. (1938). A filter-passing infectious agent isolated from ticks: isofation from D. Andersoni, Reactions in animals and filtration experiments. . Pub Health Rep, 53(2239), 1938.

de la Fuente, J., Antunes, S., Bonnet, S., Cabezas-Cruz, A., Domingos, A. G., Estrada-Pena, A., . . . Rego, R. O. M. (2017). Tick-Pathogen Interactions and Vector Competence: Identification of Molecular Drivers for Tick-Borne Diseases. Front Cell Infect Microbiol, 7, 114. doi:10.3389/fcimb.2017.00114

de la Fuente, J., & Contreras, M. (2015). Tick vaccines: current status and future directions. Expert Rev Vaccines, 14(10), 1367-1376. doi:10.1586/14760584.2015.1076339

de la Fuente, J., Villar, M., Cabezas-Cruz, A., Estrada-Pena, A., Ayllon, N., & Alberdi, P. (2016). Tick-Host-Pathogen Interactions: Conflict and Cooperation. PLoS Pathog, 12(4), e1005488. doi:10.1371/journal.ppat.1005488

de Silva, A. M., Tyson, K. R., & Pal, U. (2009). Molecular characterization of the tick-Borrelia interface. Front Biosci (Landmark Ed), 14, 3051-3063.

de Vries, H., & van Dillen, S. (2002). Prevention of Lyme disease in Dutch children: analysis of determinants of tick inspection by parents. Prev Med, 35(2), 160-165.

DeFoliart, G. R., Grimstad, P. R., & Watts, D. M. (1987). Advances in mosquito-borne arbovirus/vector research. Annu Rev Entomol, 32, 479-505. doi:10.1146/annurev.en.32.010187.002403

Dergousoff, S. J., Galloway, T. D., Lindsay, L. R., Curry, P. S., & Chilton, N. B. (2013). Range expansion of Dermacentor variabilis and Dermacentor andersoni (Acari: Ixodidae) near their northern distributional limits. J Med Entomol, 50(3), 510-520.

Dietrich, G., Dolan, M. C., Peralta-Cruz, J., Schmidt, J., Piesman, J., Eisen, R. J., & Karchesy, J. J. (2006). Repellent activity of fractioned compounds from Chamaecyparis nootkatensis essential oil against nymphal Ixodes scapularis (Acari: Ixodidae). Journal of Medical Entomology, 43(5), 957-961.

Diuk-Wasser, M. A., Gatewood, A. G., Cortinas, M. R., Yaremych-Hamer, S., Tsao, J., Kitron, U., . . . Fish, D. (2006). Spatiotemporal patterns of host-seeking Ixodes scapularis nymphs (Acari: Ixodidae) in the United States. J Med Entomol, 43(2), 166-176.

Diuk-Wasser, M. A., Hoen, A. G., Cislo, P., Brinkerhoff, R., Hamer, S. A., Rowland, M., . . . Fish, D. (2012). Human risk of infection with Borrelia burgdorferi, the Lyme disease agent, in eastern United States. Am J Trop Med Hyg, 86(2), 320-327. doi:10.4269/ajtmh.2012.11-0395

Diuk-Wasser, M. A., Vourc'h, G., Cislo, P., Hoen, A. G., Melton, F., Hamer, S. A., . . . Fish, D. (2010). Field and climate‐based model for predicting the density of host‐seeking nymphal Ixodes scapularis, an important vector of tick‐borne disease agents in the eastern United States. Global Ecology and Biogeography, 19(4), 504-514.

Dolan, M. C., Breuner, N. E., Hojgaard, A., Boegler, K. A., Hoxmeier, J. C., Replogle, A. J., & Eisen, L. (2017). Transmission of the Lyme Disease Spirochete Borrelia mayonii in Relation to Duration of Attachment by Nymphal Ixodes scapularis (Acari: Ixodidae). J Med Entomol, 54(5), 1360-1364. doi:10.1093/jme/tjx089

Dolan, M. C., Maupin, G. O., Schneider, B. S., Denatale, C., Hamon, N., Cole, C., . . . Stafford, K. C., III. (2004). Control of Immature Ixodes scapularis (Acari: Ixodidae) on Rodent Reservoirs of Borrelia burgdorferi in a Residential Community of Southeastern Connecticut. Journal of Medical Entomology, 41(6), 1043-1054.

Donta, S. T. (2002). Late and chronic Lyme disease. Med Clin North Am, 86(2), 341-349, vii.

Dressler, F., Whalen, J. A., Reinhardt, B. N., & Steere, A. C. (1993). Western blotting in the serodiagnosis of Lyme disease. J Infect Dis, 167(2), 392-400.

Drexler, N., Miller, M., Gerding, J., Todd, S., Adams, L., Dahlgren, F. S., . . . McQuiston, J. H. (2014). Community-based control of the brown dog tick in a region with high rates of Rocky Mountain spotted fever, 2012-2013. PLoS One, 9(12), e112368. doi:10.1371/journal.pone.0112368

Durden, L. A., Gerlach, R. F., Beckmen, K. B., & Greiman, S. E. (2018). Hyperparasitism and Non-Nidicolous Mating by Male Ixodes angustus Ticks (Acari: Ixodidae). J Med Entomol. doi:10.1093/jme/tjy012

Durden, L. A., & Mans, B. J. (2016). Tick paralysis: some host and tick perspectives. In J. J. Janovy & G. W. Esch (Eds.), A Century of Parasitology: Discoveries, Ideas and Lessons Learned by Scientists Who Published in the Journal of Parasitology, 1914-2014 (pp. 167-176): Wiley.

Duron, O., Binetruy, F., Noel, V., Cremaschi, J., McCoy, K. D., Arnathau, C., . . . Chevillon, C. (2017). Evolutionary changes in symbiont community structure in ticks. Mol Ecol, 26(11), 2905-2921. doi:10.1111/mec.14094

Dworkin, M. S., Anderson, D. E., Jr., Schwan, T. G., Shoemaker, P. C., Banerjee, S. N., Kassen, B. O., & Burgdorfer, W. (1998). Tick-borne relapsing fever in the northwestern United States and southwestern Canada. Clin Infect Dis, 26(1), 122-131.

Dworkin, M. S., Schwan, T. G., Anderson, D. E., Jr., & Borchardt, S. M. (2008). Tick-borne relapsing fever. Infect Dis Clin North Am, 22(3), 449-468, viii. doi:10.1016/j.idc.2008.03.006

Ebel, G. D., & Kramer, L. D. (2004). Short report: duration of tick attachment required for transmission of powassan virus by deer ticks. Am J Trop Med Hyg, 71(3), 268-271.

Eisen, L., & Dolan, M. C. (2016). Evidence for Personal Protective Measures to Reduce Human Contact With Blacklegged Ticks and for Environmentally Based Control Methods to Suppress Host-Seeking Blacklegged Ticks and Reduce Infection with Lyme Disease Spirochetes in Tick Vectors and Rodent Reservoirs. J Med Entomol. doi:10.1093/jme/tjw103

Eisen, L., Dolan, M. C., Piesman, J., & Lane, R. S. (2003). Vector competence of Ixodes pacificus and I. spinipalpis (Acari: Ixodidae), and reservoir competence of the dusky-footed woodrat (Neotoma fuscipes) and the deer mouse (Peromyscus maniculatus), for Borrelia bissettii. J Med Entomol, 40(3), 311-320.

Eisen, L., Rose, D., Prose, R., Breuner, N. E., Dolan, M. C., Thompson, K., & Connally, N. (2017). Bioassays to evaluate non-contact spatial repellency, contact irritancy, and acute toxicity of permethrin-treated clothing against nymphal Ixodes scapularis ticks. Ticks and tick-borne diseases, 8(6), 837-849.

Eisen, R. J., & Eisen, L. (2018). The Blacklegged Tick, Ixodes scapularis: An Increasing Public Health Concern. Trends Parasitol, 34(4), 295-309. doi:10.1016/j.pt.2017.12.006

Eisen, R. J., Eisen, L., & Beard, C. B. (2016). County-Scale Distribution of Ixodes scapularis and Ixodes pacificus (Acari: Ixodidae) in the Continental United States. J Med Entomol, 53(2), 349-386. doi:10.1093/jme/tjv237

Eisen, R. J., Eisen, L., Girard, Y. A., Fedorova, N., Mun, J., Slikas, B., . . . Lane, R. S. (2010). A spatially-explicit model of acarological risk of exposure to Borrelia burgdorferi-infected Ixodes pacificus nymphs in northwestern California based on woodland type, temperature, and water vapor. Ticks Tick Borne Dis, 1(1), 35-43. doi:10.1016/j.ttbdis.2009.12.002

Eisen, R. J., Eisen, L., & Lane, R. S. (2006). Predicting density of Ixodes pacificus nymphs in dense woodlands in Mendocino County, California, based on geographic information systems and remote sensing versus field-derived data. Am J Trop Med Hyg, 74(4), 632-640.

Eisen, R. J., Kugeler, K. J., Eisen, L., Beard, C. B., & Paddock, C. D. (2017). Tick-Borne Zoonoses in the United States: Persistent and Emerging Threats to Human Health. ILAR J, 1-17. doi:10.1093/ilar/ilx005

Embers, M. E., Hasenkampf, N. R., Jacobs, M. B., Tardo, A. C., Doyle-Meyers, L. A., Philipp, M. T., & Hodzic, E. (2017). Variable manifestations, diverse seroreactivity and post-treatment persistence in non-human primates exposed to Borrelia burgdorferi by tick feeding. PLoS One, 12(12), e0189071. doi:10.1371/journal.pone.0189071

Emmons, R. W. (1988). Ecology of Colorado tick fever. Annu Rev Microbiol, 42, 49-64. doi:10.1146/annurev.mi.42.100188.000405

EPA. (2017). Find the Repellent That is Right for You. Retrieved from https://www.epa.gov/insect-repellents/find-repellent-right-you

Eskow, E., Rao, R. V., & Mordechai, E. (2001). Concurrent infection of the central nervous system by Borrelia burgdorferi and Bartonella henselae: evidence for a novel tick-borne disease complex. Arch Neurol, 58(9), 1357-1363.

Esteve-Gassent, M. D., Castro-Arellano, I., Feria-Arroyo, T. P., Patino, R., Li, A. Y., Medina, R. F., . . . Rodriguez-Vivas, R. I. (2016). Translating Ecology, Physiology, Biochemistry, and Population Genetics Research to Meet the Challenge of Tick and Tick-Borne Diseases in North America. Arch Insect Biochem Physiol, 92(1), 38-64. doi:10.1002/arch.21327

Estrada-Pena, A., & de la Fuente, J. (2014). The ecology of ticks and epidemiology of tick-borne viral diseases. Antiviral Res, 108, 104-128. doi:10.1016/j.antiviral.2014.05.016

Estrada-Pena, A., de la Fuente, J., & Cabezas-Cruz, A. (2016). A comparison of the performance of regression models of Amblyomma americanum (L.) (Ixodidae) using life cycle or landscape data from administrative divisions. Ticks Tick Borne Dis, 7(4), 624-630. doi:10.1016/j.ttbdis.2016.01.010

Estrada-Pena, A., Gray, J. S., Kahl, O., Lane, R. S., & Nijhof, A. M. (2013). Research on the ecology of ticks and tick-borne pathogens--methodological principles and caveats. Front Cell Infect Microbiol, 3, 29. doi:10.3389/fcimb.2013.00029

Evans, A. S. (1976). Causation and disease: the Henle-Koch postulates revisited. Yale J Biol Med, 49(2), 175-195.

Evans, S. R., Korch, G. W., & Lawson, M. A. (1990). Comparative field evaluation of permethrin and DEET-treated military uniforms for personal protection against ticks (Acari). Journal of Medical Entomology, 27(5), 829-834.

Falco, R. C., Daniels, T. J., Vinci, V., McKenna, D., Scavarda, C., & Wormser, G. P. (2018). Assessment of Duration of Tick Feeding by the Scutal Index Reduces Need for Antibiotic Prophylaxis after Ixodes Scapularis Tick Bites. Clin Infect Dis. doi:10.1093/cid/ciy221

Falco, R. C., & Fish, D. (1988). Ticks parasitizing humans in a Lyme disease endemic area of southern New York State. Am J Epidemiol, 128(5), 1146-1152.

Feder, H. M., Jr., Hoss, D. M., Zemel, L., Telford, S. R., 3rd, Dias, F., & Wormser, G. P. (2011). Southern Tick-Associated Rash Illness (STARI) in the North: STARI following a tick bite in Long Island, New York. Clin Infect Dis, 53(10), e142-146. doi:10.1093/cid/cir553

Feinberg, R. (2018). Generating first-ever transgenic ticks to help fight tick-borne diseases. NEVADAToday. Retrieved from https://www.unr.edu/nevada-today/news/2018/cabnr-lab-generates-transgenic-ticks

Felz, M. W., Durden, L. A., & Oliver, J. H., Jr. (1996). Ticks parasitizing humans in Georgia and South Carolina. J Parasitol, 82(3), 505-508.

Fire, A., Xu, S., Montgomery, M. K., Kostas, S. A., Driver, S. E., & Mello, C. C. (1998). Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans. Nature, 391(6669), 806-811. doi:10.1038/35888

Fish, D., & Dowler, R. C. (1989). Host associations of ticks (Acari: Ixodidae) parasitizing medium-sized mammals in a Lyme disease endemic area of southern New York. J Med Entomol, 26(3), 200-209.

Flor-Weiler, L. B., Behle, R. W., & Stafford III, K. C. (2011). Susceptibility of four tick species, Amblyomma americanum, Dermacentor variabilis, Ixodes scapularis, and Rhipicephalus sanguineus (Acari: Ixodidae), to nootkatone from essential oil of grapefruit. Journal of Medical Entomology, 48(2), 322-326.

Ford, K., Nadolny, R., Stromdahl, E., & Hickling, G. (2015). Tick surveillance and disease prevention on the Appalachian Trail. Park Science, 32(1), 36-41.

Fredricks, D. N., & Relman, D. A. (1996). Sequence-based identification of microbial pathogens: a reconsideration of Koch's postulates. Clin Microbiol Rev, 9(1), 18-33.

Fryauff, D. J., Shoukry, M. A., Wassef, H. Y., Gray, G., & Schreck, C. E. (1998). Contact toxicity of permethrin-impregnated fabric to Hyalomma anatolicum excavatum (Acari: Ixodidae): Effects of laundering and exposure and recovery times. Journal of Medical Entomology, 35(3), 335-339.

Gaff, H. D., White, A., Leas, K., Kelman, P., Squire, J. C., Livingston, D. L., . . . Sonenshine, D. E. (2015). TickBot: a novel robotic device for controlling tick populations in the natural environment. Ticks Tick Borne Dis, 6(2), 146-151. doi:10.1016/j.ttbdis.2014.11.004

Galay, R. L., Hernandez, E. P., Talactac, M. R., Maeda, H., Kusakisako, K., Umemiya-Shirafuji, R., . . . Tanaka, T. (2016). Induction of gene silencing in Haemaphysalis longicornis ticks through immersion in double-stranded RNA. Ticks Tick Borne Dis, 7(5), 813-816. doi:10.1016/j.ttbdis.2016.03.018

Gardulf, A., Wohlfart, I., & Gustafson, R. (2004). A prospective cross-over field trial shows protection of lemon eucalyptus extract against tick bites. J Med Entomol, 41(6), 1064-1067.

Gelburd, R. (2017). A Window Into Lyme Disease Using Private Claims Data. Retrieved from http://www.ajmc.com/contributor/robin-gelburd-jd/2017/07/a-window-into-lyme-disease-using-private-claims-data

George, J. E. (2008). The effects of global change on the threat of exotic arthropods and arthropod-borne pathogens to livestock in the United States. Ann N Y Acad Sci, 1149, 249-254. doi:10.1196/annals.1428.084

German, R. R., Lee, L. M., Horan, J. M., Milstein, R. L., Pertowski, C. A., Waller, M. N., . . . Prevention. (2001). Updated guidelines for evaluating public health surveillance systems: recommendations from the Guidelines Working Group. MMWR Recomm Rep, 50(RR-13), 1-35; quiz CE31-37.

Gilbert, L. (2013). Can restoration of afforested peatland regulate pests and disease? Journal of Applied Ecology, 50(5), 1226-1233.

Ginsberg, H. S., Bargar, T. A., Hladik, M. L., & Lubelczyk, C. (2017). Management of Arthropod Pathogen Vectors in North America: Minimizing Adverse Effects on Pollinators. J Med Entomol, 54(6), 1463-1475. doi:10.1093/jme/tjx146

Ginsberg, H. S., Butler, M., & Zhioua, E. (2002). Effect of deer exclusion by fencing on abundance of Amblyomma americanum (Acari: Ixodidae) on Fire Island, New York, USA. Journal of vector ecology, 27(2), 215-221.

Glanz, K. (2002). Health Behavior and Health Education: Theory, Research, and

Practice: Wiley, John & Sons, Inc.

Goddard, J. (1992). Ecological studies of adult Ixodes scapularis in central Mississippi: questing activity in relation to time of year, vegetation type, and meteorologic conditions. J Med Entomol, 29(3), 501-506.

Goddard, J. (2002). A ten-year study of tick biting in Mississippi: implications for human disease transmission. J Agromedicine, 8(2), 25-32. doi:10.1300/J096v08n02_06

Goddard, J., & Piesman, J. (2006). New records of immature Ixodes scapularis from Mississippi. J Vector Ecol, 31(2), 421-422.

Godsey, M. S., Jr., Savage, H. M., Burkhalter, K. L., Bosco-Lauth, A. M., & Delorey, M. J. (2016). Transmission of Heartland Virus (Bunyaviridae: Phlebovirus) by Experimentally Infected Amblyomma americanum (Acari: Ixodidae). J Med Entomol. doi:10.1093/jme/tjw080

Gomes-Solecki, M. (2014). Blocking pathogen transmission at the source: reservoir targeted OspA-based vaccines against Borrelia burgdorferi. Front Cell Infect Microbiol, 4, 136. doi:10.3389/fcimb.2014.00136

Gould, L. H., Nelson, R. S., Griffith, K. S., Hayes, E. B., Piesman, J., Mead, P. S., & Cartter, M. L. (2008a). Knowledge, attitudes, and behaviors regarding Lyme disease prevention among Connecticut residents, 1999-2004. Vector-Borne and Zoonotic Diseases, 8(6), 769-776.

Gould, L. H., Nelson, R. S., Griffith, K. S., Hayes, E. B., Piesman, J., Mead, P. S., & Cartter, M. L. (2008b). Knowledge, attitudes, and behaviors regarding Lyme disease prevention among Connecticut residents, 1999-2004. Vector Borne Zoonotic Dis, 8(6), 769-776. doi:10.1089/vbz.2007.0221

Guerra, M., Walker, E., Jones, C., Paskewitz, S., Cortinas, M. R., Stancil, A., . . . Kitron, U. (2002). Predicting the risk of Lyme disease: habitat suitability for Ixodes scapularis in the north central United States. Emerg Infect Dis, 8(3), 289-297. doi:10.3201/eid0803.010166

Guzmán-Cornejo, C., Robbins, R. G., Guglielmone, A. A., Montiel-Parra, G., & Pérez, T. M. (2011). The Amblyomma (Acari, Ixodida, Ixodidae) of Mexico: identification keys, distribution and hosts. Zootaxa, 2998, 16-38.

Hahn, M. B., Jarnevich, C. S., Monaghan, A. J., & Eisen, R. J. (2016). Modeling the Geographic Distribution of Ixodes scapularis and Ixodes pacificus (Acari: Ixodidae) in the Contiguous United States. J Med Entomol. doi:10.1093/jme/tjw076

Hajdusek, O., Sima, R., Ayllon, N., Jalovecka, M., Perner, J., de la Fuente, J., & Kopacek, P. (2013). Interaction of the tick immune system with transmitted pathogens. Front Cell Infect Microbiol, 3, 26. doi:10.3389/fcimb.2013.00026

Harmon, A. (2016). Fighting Lyme Disease in the Genes of Nantucket’s Mice. The New York Times. Retrieved from https://www.nytimes.com/2016/06/08/science/ticks-lyme-disease-mice-nantucket.html

Hayes, E. B., & Piesman, J. (2003). How can we prevent Lyme disease? N Engl J Med, 348(24), 2424-2430. doi:10.1056/NEJMra021397

Health, H. S. D. o. (2013). Infectious Disease. Retrieved from https://health.hawaii.gov/docd/files/2013/05/INFECTIOUS-DISEASE-REPORTABLE-FLYER.pdf

Hill, A. B. (1965). The Environment and Disease: Association or Causation? Proc R Soc Med, 58, 295-300.

Hinckley, A. F., Connally, N. P., Meek, J. I., Johnson, B. J., Kemperman, M. M., Feldman, K. A., . . . Mead, P. S. (2014). Lyme disease testing by large commercial laboratories in the United States. Clin Infect Dis, 59(5), 676-681. doi:10.1093/cid/ciu397

Hinckley, A. F., Meek, J. I., Ray, J. A., Niesobecki, S. A., Connally, N. P., Feldman, K. A., . . . Lukacik, G. (2016). Effectiveness of Residential Acaricides to Prevent Lyme and Other Tickborne Diseases in Humans. Journal of Infectious Diseases, jiv775.

Hook, S. A., Nelson, C. A., & Mead, P. S. (2015). U.S. public's experience with ticks and tick-borne diseases: Results from national HealthStyles surveys. Ticks Tick Borne Dis, 6(4), 483-488. doi:10.1016/j.ttbdis.2015.03.017

IJdo, J. W., & Mueller, A. C. (2004). Neutrophil NADPH oxidase is reduced at the Anaplasma phagocytophilum phagosome. Infect Immun, 72(9), 5392-5401. doi:10.1128/IAI.72.9.5392-5401.2004

Interlandi, J. (2018). Bait boxes are a safe way to keep ticks out of your yard. Retrieved from https://www.consumerreports.org/pest-control/bait-boxes-are-a-safe-way-to-keep-ticks-out-of-your-yard/

ISDA on Lyme. (2005). Retrieved from https://sites.google.com/site/idsaonlyme/cdc-position

Jado, I., Oteo, J. A., Aldamiz, M., Gil, H., Escudero, R., Ibarra, V., . . . Anda, P. (2007). Rickettsia monacensis and human disease, Spain. Emerg Infect Dis, 13(9), 1405-1407. doi:10.3201/eid1309.060186

James, A. M., Burdett, C., McCool, M. J., Fox, A., & Riggs, P. (2015). The geographic distribution and ecological preferences of the American dog tick, Dermacentor variabilis (Say), in the U.S.A. Med Vet Entomol, 29(2), 178-188. doi:10.1111/mve.12099

James, A. M., Freier, J. E., Keirans, J. E., Durden, L. A., Mertins, J. W., & Schlater, J. L. (2006). Distribution, seasonality, and hosts of the Rocky Mountain wood tick in the United States. J Med Entomol, 43(1), 17-24.

Jasinskas, A., Zhong, J., & Barbour, A. G. (2007). Highly prevalent Coxiella sp. bacterium in the tick vector Amblyomma americanum. Appl Environ Microbiol, 73(1), 334-336. doi:10.1128/AEM.02009-06

Johnson, L., Mervine, P., & Potter, M. (2016). Using a New Patient-Powered Research Tool to Answer Critical Questions about Lyme Disease (A Poster). Paper presented at the Columbia University/Lyme Disease Association Conference, St Paul, MN.

Johnson, L., Wilcox, S., Mankoff, J., & Stricker, R. B. (2014). Severity of chronic Lyme disease compared to other chronic conditions: a quality of life survey. PeerJ, 2, e322. doi:10.7717/peerj.322

Johnson, T. L., Fischer, R. J., Raffel, S. J., & Schwan, T. G. (2016). Host associations and genomic diversity of Borrelia hermsii in an endemic focus of tick-borne relapsing fever in western North America. Parasit Vectors, 9(1), 575. doi:10.1186/s13071-016-1863-0

Jones, E. H., Chanlongbutra, A., Wong, D., Cunningham, F., & Feldman, K. A. (2016). Knowledge, attitudes, and practices regarding Lyme disease prevention among employees, day visitors, and campers at Greenbelt Park. Park Science, 32(2), 46-53.

Kawahara, M., Rikihisa, Y., Isogai, E., Takahashi, M., Misumi, H., Suto, C., . . . Tsuji, M. (2004). Ultrastructure and phylogenetic analysis of 'Candidatus Neoehrlichia mikurensis' in the family Anaplasmataceae, isolated from wild rats and found in Ixodes ovatus ticks. Int J Syst Evol Microbiol, 54(Pt 5), 1837-1843. doi:10.1099/ijs.0.63260-0

Kempf, F., De Meeus, T., Vaumourin, E., Noel, V., Taragel'ova, V., Plantard, O., . . . McCoy, K. D. (2011). Host races in Ixodes ricinus, the European vector of Lyme borreliosis. Infect Genet Evol, 11(8), 2043-2048. doi:10.1016/j.meegid.2011.09.016

Kilpatrick, A. M., Dobson, A. D. M., Levi, T., Salkeld, D. J., Swei, A., Ginsberg, H. S., . . . Diuk-Wasser, M. A. (2017). Lyme disease ecology in a changing world: consensus, uncertainty and critical gaps for improving control. Philos Trans R Soc Lond B Biol Sci, 372(1722). doi:10.1098/rstb.2016.0117

Kilpatrick, A. M., & Randolph, S. E. (2012). Drivers, dynamics, and control of emerging vector-borne zoonotic diseases. Lancet, 380(9857), 1946-1955. doi:10.1016/S0140-6736(12)61151-9

Kingry, L. C., Anacker, M., Pritt, B., Bjork, J., Respicio-Kingry, L., Liu, G., . . . Petersen, J. M. (2017). Surveillance for and Discovery of Borrelia Species in US Patients Suspected of Tickborne Illness. Clin Infect Dis. doi:10.1093/cid/cix1107

Kirkland, B. H., Westwood, G. S., & Keyhani, N. O. (2004). Pathogenicity of entomopathogenic fungi Beauveria bassiana and Metarhizium anisopliae to Ixodidae tick species Dermacentor variabilis, Rhipicephalus sanguineus, and Ixodes scapularis. J Med Entomol, 41(4), 705-711.

Lane, R. S., & Anderson, J. R. (1984). Efficacy of permethrin as a repellent and toxicant for personal protection against the Pacific Coast tick and the Pajaroello tick (Acari: Ixodidae and Argasidae). J Med Entomol, 21(6), 692-702.

Lane, R. S., Fedorova, N., Kleinjan, J. E., & Maxwell, M. (2013). Eco-epidemiological factors contributing to the low risk of human exposure to ixodid tick-borne borreliae in southern California, USA. Ticks Tick Borne Dis, 4(5), 377-385. doi:10.1016/j.ttbdis.2013.02.005

Lane, R. S., Lennette, E. T., & Madigan, J. E. (1990). Interlaboratory and intralaboratory comparisons of indirect immunofluorescence assays for serodiagnosis of Lyme disease. J Clin Microbiol, 28(8), 1774-1779.

Lane, R. S., Manweiler, S. A., Stubbs, H. A., Lennette, E. T., Madigan, J. E., & Lavoie, P. E. (1992). Risk factors for Lyme disease in a small rural community in northern California. Am J Epidemiol, 136(11), 1358-1368.

Lane, R. S., Mun, J., Peribanez, M. A., & Stubbs, H. A. (2007). Host-seeking behavior of Ixodes pacificus (Acari: Ixodidae) nymphs in relation to environmental parameters in dense-woodland and woodland-grass habitats. J Vector Ecol, 32(2), 342-357.

Lane, R. S., & Quistad, G. B. (1998). Borreliacidal factor in the blood of the western fence lizard (Sceloporus occidentalis). J Parasitol, 84(1), 29-34.

Lane, R. S., Steinlein, D. B., & Mun, J. (2004). Human behaviors elevating exposure to Ixodes pacificus (Acari: Ixodidae) nymphs and their associated bacterial zoonotic agents in a hardwood forest. J Med Entomol, 41(2), 239-248. doi:10.1603/0022-2585-41.2.239

LDA. (2001). Conflicts of Interest in Lyme Disease: Laboratory Testing, Vaccination, and Treatment Guidelines. Retrieved from https://lymediseaseassociation.org/images/pdf/ConflictReport.pdf

Ledin, K. E., Zeidner, N. S., Ribeiro, J. M., Biggerstaff, B. J., Dolan, M. C., Dietrich, G., . . . Piesman, J. (2005). Borreliacidal activity of saliva of the tick Amblyomma americanum. Med Vet Entomol, 19(1), 90-95. doi:10.1111/j.0269-283X.2005.00546.x

Leger, E., Vourc'h, G., Vial, L., Chevillon, C., & McCoy, K. D. (2013). Changing distributions of ticks: causes and consequences. Exp Appl Acarol, 59(1-2), 219-244. doi:10.1007/s10493-012-9615-0

Leprince, D. J., & Lane, R. S. (1996). Evaluation of permethrin-impregnated cotton balls as potential nesting material to control ectoparasites of woodrats in California. J Med Entomol, 33(3), 355-360.

Levi, T., Kilpatrick, A. M., Mangel, M., & Wilmers, C. C. (2012). Deer, predators, and the emergence of Lyme disease. Proc Natl Acad Sci U S A, 109(27), 10942-10947. doi:10.1073/pnas.1204536109

Levin, M., Levine, J. F., Yang, S., Howard, P., & Apperson, C. S. (1996). Reservoir competence of the southeastern five-lined skink (Eumeces inexpectatus) and the green anole (Anolis carolinensis) for Borrelia burgdorferi. Am J Trop Med Hyg, 54(1), 92-97.

Levin, M. L., Zemtsova, G. E., Killmaster, L. F., Snellgrove, A., & Schumacher, L. B. M. (2017). Vector competence of Amblyomma americanum (Acari: Ixodidae) for Rickettsia rickettsii. Ticks Tick Borne Dis, 8(4), 615-622. doi:10.1016/j.ttbdis.2017.04.006

Lew-Tabor, A. E., Kurscheid, S., Barrero, R., Gondro, C., Moolhuijzen, P. M., Rodriguez Valle, M., . . . Bellgard, M. I. (2011). Gene expression evidence for off-target effects caused by RNA interference-mediated gene silencing of Ubiquitin-63E in the cattle tick Rhipicephalus microplus. Int J Parasitol, 41(9), 1001-1014. doi:10.1016/j.ijpara.2011.05.003

Lindquist, E. E. G., T. D., Artsob, H., Lindsay, L. R., Drebot, M., Wood, H., & Robbins, R. G. (2016). A handbook to the ticks of Canada. Biological Survey of Canada Monograph, 7, 1-317.

Lindsay, L. R., Barker, I. K., Surgeoner, G. A., McEwen, S. A., Gillespie, T. J., & Addison, E. M. (1998). Survival and development of the different life stages of Ixodes scapularis (Acari: Ixodidae) held within four habitats on Long Point, Ontario, Canada. J Med Entomol, 35(3), 189-199.

Linske, M. A., Williams, S. C., Stafford, K. C., 3rd, & Ortega, I. M. (2018). Ixodes scapularis (Acari: Ixodidae) Reservoir Host Diversity and Abundance Impacts on Dilution of Borrelia burgdorferi (Spirochaetales: Spirochaetaceae) in Residential and Woodland Habitats in Connecticut, United States. J Med Entomol. doi:10.1093/jme/tjx237

Little, S. E., Beall, M. J., Bowman, D. D., Chandrashekar, R., & Stamaris, J. (2014). Canine infection with Dirofilaria immitis, Borrelia burgdorferi, Anaplasma spp., and Ehrlichia spp. in the United States, 2010-2012. Parasit Vectors, 7, 257. doi:10.1186/1756-3305-7-257

Liu, L., Narasimhan, S., Dai, J., Zhang, L., Cheng, G., & Fikrig, E. (2011). Ixodes scapularis salivary gland protein P11 facilitates migration of Anaplasma phagocytophilum from the tick gut to salivary glands. EMBO Rep, 12(11), 1196-1203. doi:10.1038/embor.2011.177

LoGiudice, K., Ostfeld, R. S., Schmidt, K. A., & Keesing, F. (2003). The ecology of infectious disease: effects of host diversity and community composition on Lyme disease risk. Proc Natl Acad Sci U S A, 100(2), 567-571. doi:10.1073/pnas.0233733100

Lopez, J. E., Krishnavahjala, A., Garcia, M. N., & Bermudez, S. (2016). Tick-Borne Relapsing Fever Spirochetes in the Americas. Vet Sci, 3(3). doi:10.3390/vetsci3030016

Loss, S. R., Noden, B. H., Hamer, G. L., & Hamer, S. A. (2016). A quantitative synthesis of the role of birds in carrying ticks and tick-borne pathogens in North America. Oecologia, 182(4), 947-959. doi:10.1007/s00442-016-3731-1

Lukacik, G., White, J., Noonan-Toly, C., DiDonato, C., & Backenson, P. B. (2018). Lyme Disease Surveillance Using Sampling Estimation: Evaluation of an Alternative Methodology in New York State. Zoonoses Public Health, 65(2), 260-265. doi:10.1111/zph.12261

MacDonald, A. J., Hyon, D. W., Brewington, J. B., 3rd, O'Connor, K. E., Swei, A., & Briggs, C. J. (2017). Lyme disease risk in southern California: abiotic and environmental drivers of Ixodes pacificus (Acari: Ixodidae) density and infection prevalence with Borrelia burgdorferi. Parasit Vectors, 10(1), 7. doi:10.1186/s13071-016-1938-y

Malouin, R., Winch, P., Leontsini, E., Glass, G., Simon, D., Hayes, E. B., & Schwartz, B. S. (2003). Longitudinal evaluation of an educational intervention for preventing tick bites in an area with endemic lyme disease in Baltimore County, Maryland. Am J Epidemiol, 157(11), 1039-1051.

Margos, G., Fedorova, N., Kleinjan, J. E., Hartberger, C., Schwan, T. G., Sing, A., & Fingerle, V. (2017). Borrelia lanei sp. nov. extends the diversity of Borrelia species in California. Int J Syst Evol Microbiol, 67(10), 3872-3876. doi:10.1099/ijsem.0.002214

Marques, A., Telford, S. R., 3rd, Turk, S. P., Chung, E., Williams, C., Dardick, K., . . . Hu, L. T. (2014). Xenodiagnosis to detect Borrelia burgdorferi infection: a first-in-human study. Clin Infect Dis, 58(7), 937-945. doi:10.1093/cid/cit939

Mather, T. N., Ribeiro, J., Moore, S. I., & Spielman, A. (1988). Reducing transmission of Lyme disease spirochetes in a suburban setting. Annals of the New York Academy of Sciences, 539(1), 402-403.

McDivitt, J. (2003). Is there a role for branding in social marketing? Social Marketing Quarterly, 9(3), 11-17.

Mead, P., Hook, S., Niesobecki, S., Ray, J., Meek, J., Delorey, M., . . . Hinckley, A. (2017). Risk factors for tick exposure in suburban settings in the Northeastern United States. Ticks and tick-borne diseases.

Medicine, I. o. (2002). Speaking of Health: Assessing Health Communications Strategies for Diverse Populations. Washington DC: National Academies Press.

Medlock, J. M., Hansford, K. M., Bormane, A., Derdakova, M., Estrada-Pena, A., George, J. C., . . . Van Bortel, W. (2013). Driving forces for changes in geographical distribution of Ixodes ricinus ticks in Europe. Parasit Vectors, 6, 1. doi:10.1186/1756-3305-6-1

Mehta, P., Kaye, W., Raymond, J., Wu, R., Larson, T., Punjani, R., . . . Horton, K. (2018). Prevalence of Amyotrophic Lateral Sclerosis - United States, 2014. MMWR Morb Mortal Wkly Rep, 67(7), 216-218. doi:10.15585/mmwr.mm6707a3

Miller, N. J., Rainone, E. E., Dyer, M. C., González, M. L., & Mather, T. N. (2011). Tick bite protection with permethrin-treated summer-weight clothing. Journal of Medical Entomology, 48(2), 327-333.

Minigan, J. N., Hager, H. A., Peregrine, A. S., & Newman, J. A. (2018). Current and potential future distribution of the American dog tick (Dermacentor variabilis, Say) in North America. Ticks Tick Borne Dis, 9(2), 354-362. doi:10.1016/j.ttbdis.2017.11.012

Mixson, T. R., Lydy, S. L., Dasch, G. A., & Real, L. A. (2006). Inferring the population structure and demographic history of the tick, Amblyomma americanum Linnaeus. J Vector Ecol, 31(1), 181-192.

Monmouth County Mosquito Control. (2018). Retrieved from https://co.monmouth.nj.us/page.aspx?ID=177

Monzon, J. D., Atkinson, E. G., Henn, B. M., & Benach, J. L. (2016). Population and Evolutionary Genomics of Amblyomma americanum, an Expanding Arthropod Disease Vector. Genome Biol Evol, 8(5), 1351-1360. doi:10.1093/gbe/evw080

Morlando, S., Schmidt, S. J., & LoGiudice, K. (2012). Reduction in Lyme disease risk as an economic benefit of habitat restoration. Restoration Ecology, 20(4), 498-504.

Morshed, M. G., Scott, J. D., Banerjee, S. N., Banerjee, M., Fitzgerald, T., Fernando, K., . . . Isaac-Renton, J. (1999). First isolation of Lyme disease spirochete, Borrelia burgdorferi, from blacklegged tick, Ixodes scapularis, removed from a bird in nova Scotia, Canada. Can Commun Dis Rep, 25(18), 153-155.

Nadolny, R. M., & Gaff, H. D. (2018). Natural history of Ixodes affinis in Virginia. Ticks Tick Borne Dis, 9(1), 109-119. doi:10.1016/j.ttbdis.2017.09.016

Narasimhan, S., & Fikrig, E. (2015). Tick microbiome: the force within. Trends Parasitol, 31(7), 315-323. doi:10.1016/j.pt.2015.03.010

Nasci, R. S. (2008). Integration of strategies: surveillance, diagnosis, response. In, Vector-borne Diseases: Understanding the Environmental, Human Health, and Ecological Connections.

Neelakanta, G., Sultana, H., Fish, D., Anderson, J. F., & Fikrig, E. (2010). Anaplasma phagocytophilum induces Ixodes scapularis ticks to express an antifreeze glycoprotein gene that enhances their survival in the cold. J Clin Invest, 120(9), 3179-3190. doi:10.1172/JCI42868

Nelson, C. A., Saha, S., Kugeler, K. J., Delorey, M. J., Shankar, M. B., Hinckley, A. F., & Mead, P. S. (2015). Incidence of Clinician-Diagnosed Lyme Disease, United States, 2005-2010. Emerg Infect Dis, 21(9), 1625-1631. doi:10.3201/eid2109.150417

Newman, E. A., Eisen, L., Eisen, R. J., Fedorova, N., Hasty, J. M., Vaughn, C., & Lane, R. S. (2015). Borrelia burgdorferi sensu lato spirochetes in wild birds in northwestern California: associations with ecological factors, bird behavior and tick infestation. PLoS One, 10(2), e0118146. doi:10.1371/journal.pone.0118146

Nilsson, K., Lindquist, O., & Pahlson, C. (1999). Association of Rickettsia helvetica with chronic perimyocarditis in sudden cardiac death. Lancet, 354(9185), 1169-1173. doi:10.1016/S0140-6736(99)04093-3

Nogueira, S. V., Smith, A. A., Qin, J. H., & Pal, U. (2012). A surface enolase participates in Borrelia burgdorferi-plasminogen interaction and contributes to pathogen survival within feeding ticks. Infect Immun, 80(1), 82-90. doi:10.1128/IAI.05671-11

Norris, D. E. (2004). Mosquito-borne diseases as a consequence of land use change. EcoHealth, 1(1), 19-24.

Nowakowski, J., Schwartz, I., Liveris, D., Wang, G., Aguero-Rosenfeld, M. E., Girao, G., . . . Lyme Disease Study, G. (2001). Laboratory diagnostic techniques for patients with early Lyme disease associated with erythema migrans: a comparison of different techniques. Clin Infect Dis, 33(12), 2023-2027. doi:10.1086/324490

O'Bryan, C. J., Braczkowski, A. R., Beyer, H. L., Carter, N. H., Watson, J. E. M., & McDonald-Madden, E. (2018). The contribution of predators and scavengers to human well-being. Nat Ecol Evol, 2(2), 229-236. doi:10.1038/s41559-017-0421-2

Ogden, N. H., Bigras-Poulin, M., O'Callaghan, C. J., Barker, I. K., Lindsay, L. R., Maarouf, A., . . . Charron, D. (2005). A dynamic population model to investigate effects of climate on geographic range and seasonality of the tick Ixodes scapularis. Int J Parasitol, 35(4), 375-389. doi:10.1016/j.ijpara.2004.12.013

Ogden, N. H., Lindsay, L. R., Hanincova, K., Barker, I. K., Bigras-Poulin, M., Charron, D. F., . . . Thompson, R. A. (2008). Role of migratory birds in introduction and range expansion of Ixodes scapularis ticks and of Borrelia burgdorferi and Anaplasma phagocytophilum in Canada. Appl Environ Microbiol, 74(6), 1780-1790. doi:10.1128/AEM.01982-07

Ogden, N. H., Maarouf, A., Barker, I. K., Bigras-Poulin, M., Lindsay, L. R., Morshed, M. G., . . . Charron, D. F. (2006). Climate change and the potential for range expansion of the Lyme disease vector Ixodes scapularis in Canada. Int J Parasitol, 36(1), 63-70. doi:10.1016/j.ijpara.2005.08.016

Ogden, N. H., St-Onge, L., Barker, I. K., Brazeau, S., Bigras-Poulin, M., Charron, D. F., . . . Thompson, R. A. (2008). Risk maps for range expansion of the Lyme disease vector, Ixodes scapularis, in Canada now and with climate change. Int J Health Geogr, 7, 24. doi:10.1186/1476-072X-7-24

Ogden, N. H., & Tsao, J. I. (2009). Biodiversity and Lyme disease: dilution or amplification? Epidemics, 1(3), 196-206. doi:10.1016/j.epidem.2009.06.002

Oliver, J. H., Jr., Lin, T., Gao, L., Clark, K. L., Banks, C. W., Durden, L. A., . . . Chandler, F. W., Jr. (2003). An enzootic transmission cycle of Lyme borreliosis spirochetes in the southeastern United States. Proc Natl Acad Sci U S A, 100(20), 11642-11645. doi:10.1073/pnas.1434553100

Onder, O., Humphrey, P. T., McOmber, B., Korobova, F., Francella, N., Greenbaum, D. C., & Brisson, D. (2012). OspC is potent plasminogen receptor on surface of Borrelia burgdorferi. J Biol Chem, 287(20), 16860-16868. doi:10.1074/jbc.M111.290775

Ostfeld, R. S., Glass, G. E., & Keesing, F. (2005). Spatial epidemiology: an emerging (or re-emerging) discipline. Trends Ecol Evol, 20(6), 328-336. doi:10.1016/j.tree.2005.03.009

Ostfeld, R. S., & Keesing, F. (2000). Biodiversity and Disease Risk: the Case of Lyme Disease. Conservation Biology, 14(3), 722-728.

Paddock, C. D., & Goddard, J. (2015). The Evolving Medical and Veterinary Importance of the Gulf Coast tick (Acari: Ixodidae). J Med Entomol, 52(2), 230-252. doi:10.1093/jme/tju022

Paddock, C. D., & Yabsley, M. J. (2007). Ecological havoc, the rise of white-tailed deer, and the emergence of Amblyomma americanum-associated zoonoses in the United States. In J. E. Childs, J. S. Mackenzie, & J. A. Richt (Eds.), Wildlife and Emerging Zoonotic Diseases: The Biology, Circumstances and Consequences of Cross-Species Transmission (Vol. 315, pp. 289-324). Springer-Verlag Berlin Heidelberg: Springer Science & Business Media.

Parola, P., Paddock, C. D., Socolovschi, C., Labruna, M. B., Mediannikov, O., Kernif, T., . . . Raoult, D. (2013). Update on tick-borne rickettsioses around the world: a geographic approach. Clin Microbiol Rev, 26(4), 657-702. doi:10.1128/CMR.00032-13

Paul, W. S., Maupin, G., Scott-Wright, A. O., Craven, R. B., & Dennis, D. T. (2002). Outbreak of tick-borne relapsing fever at the north rim of the Grand Canyon: evidence for effectiveness of preventive measures. Am J Trop Med Hyg, 66(1), 71-75.

Pavlousky, E. N. (1966). Natural nidality of transmissible diseases, with special reference to the landscape epidemiology of zooanthroponoses: London. Urbana: University of Illinois Press, Illinois 61801, U.S.A.

Perez de Leon, A. A., Strickman, D. A., Knowles, D. P., Fish, D., Thacker, E., de la Fuente, J., . . . Development in the, U. S. (2010). One Health approach to identify research needs in bovine and human babesioses: workshop report. Parasit Vectors, 3(1), 36. doi:10.1186/1756-3305-3-36

Perez de Leon, A. A., Teel, P. D., Auclair, A. N., Messenger, M. T., Guerrero, F. D., Schuster, G., & Miller, R. J. (2012). Integrated Strategy for Sustainable Cattle Fever Tick Eradication in USA is Required to Mitigate the Impact of Global Change. Front Physiol, 3, 195. doi:10.3389/fphys.2012.00195

Pérez de León, A. A., Teel, P. D., Li, A., Ponnusamy, L., & Roe, R. M. (2014). Advancing integrated tick management to mitigate burden of tick-borne diseases. Outlooks Pest Manag(25), 382-389.

PHC. 2017 Health of the Force Report - U.S. Army Public Health Center. Retrieved from https://phc.amedd.army.mil/Periodical Library/2017HealthoftheForceweb.pdf

Pichon, B., Rogers, M., Egan, D., & Gray, J. (2005). Blood-meal analysis for the identification of reservoir hosts of tick-borne pathogens in Ireland. Vector Borne Zoonotic Dis, 5(2), 172-180. doi:10.1089/vbz.2005.5.172

Poland, G. A. (2001). Prevention of Lyme disease: a review of the evidence. Mayo Clin Proc, 76(7), 713-724. doi:10.4065/76.7.713

Pound, J. M., Miller, J. A., George, J. E., & Lemeilleur, C. A. (2000). The '4-poster' passive topical treatment device to apply acaricide for controlling ticks (Acari: Ixodidae) feeding on white-tailed deer. J Med Entomol, 37(4), 588-594.

Raghavan, R. K., Goodin, D. G., Hanzlicek, G. A., Zolnerowich, G., Dryden, M. W., Anderson, G. A., & Ganta, R. R. (2016). Maximum Entropy-Based Ecological Niche Model and Bio-Climatic Determinants of Lone Star Tick (Amblyomma americanum) Niche. Vector Borne Zoonotic Dis, 16(3), 205-211. doi:10.1089/vbz.2015.1837

Rainey, T., Occi, J. L., Robbins, R. G., & Egizi, A. (2018). Discovery of Haemaphysalis longicornis (Ixodida: Ixodidae) Parasitizing a Sheep in New Jersey, United States. J Med Entomol. doi:10.1093/jme/tjy006

Rand, P. W., Lubelczyk, C., Holman, M. S., Lacombe, E. H., & Smith, R. P., Jr. (2004). Abundance of Ixodes scapularis (Acari: Ixodidae) after the complete removal of deer from an isolated offshore island, endemic for Lyme Disease. J Med Entomol, 41(4), 779-784.

Randolph, S. E., & Dobson, A. D. (2012). Pangloss revisited: a critique of the dilution effect and the biodiversity-buffers-disease paradigm. Parasitology, 139(7), 847-863. doi:10.1017/S0031182012000200

Reid, J. R., Thompson, K., Barrett, D., & Connally, N. P. (2013, August, 18-21, 2013). Identifying barriers to chemical Lyme disease prevention methods. Paper presented at the 13th International Conference on Lyme Borreliosis and other Tick Borne Diseases, Boston, MA, USA.

Richer, L. M., Brisson, D., Melo, R., Ostfeld, R. S., Zeidner, N., & Gomes-Solecki, M. (2014). Reservoir targeted vaccine against Borrelia burgdorferi: a new strategy to prevent Lyme disease transmission. J Infect Dis, 209(12), 1972-1980. doi:10.1093/infdis/jiu005

Robinson, S. (2014). Lyme Disease in Maine: a Comparison of NEDSS Surveillance Data and Maine Health Data Organization Hospital Discharge data. Online J Public Health Inform, 5(3), 231. doi:10.5210/ojphi.v5i3.4990

Rosenberg, R., Lindsey, N. P., Fischer, M., Gregory, C. J., Hinckley, A. F., Mead, P. S., . . . Petersen, L. R. (2018). Vital Signs: Trends in Reported Vectorborne Disease Cases — United States and Territories, 2004–2016. . MMWR Morb Mortal Wkly Rep, 67, 496-501. Retrieved from https://www.cdc.gov/mmwr/volumes/67/wr/mm6717e1.htm?s_cid=mm6717e1_w

Rosenstock, I. M., Strecher, V. J., & Becker, M. H. (1988). Social learning theory and the Health Belief Model. Health Educ Q, 15(2), 175-183.

Rudenko, N., Golovchenko, M., Clark, K., Oliver, J. H., & Grubhoffer, L. (2016). Detection of Borrelia burgdorferi sensu stricto in Amblyomma americanum ticks in the southeastern United States: the case of selective compatibility. Emerg Microbes Infect, 5, e48. doi:10.1038/emi.2016.45

Rudenko, N., Golovchenko, M., Grubhoffer, L., & Oliver, J. H., Jr. (2011). Borrelia carolinensis sp. nov., a novel species of the Borrelia burgdorferi sensu lato complex isolated from rodents and a tick from the south-eastern USA. Int J Syst Evol Microbiol, 61(Pt 2), 381-383. doi:10.1099/ijs.0.021436-0

Rudenko, N., Golovchenko, M., Honig, V., Mallatova, N., Krbkova, L., Mikulasek, P., . . . Oliver, J. H., Jr. (2013). Detection of Borrelia burgdorferi sensu stricto ospC alleles associated with human lyme borreliosis worldwide in non-human-biting tick Ixodes affinis and rodent hosts in Southeastern United States. Appl Environ Microbiol, 79(5), 1444-1453. doi:10.1128/AEM.02749-12

Rudenko, N., Golovchenko, M., Lin, T., Gao, L., Grubhoffer, L., & Oliver, J. H., Jr. (2009). Delineation of a new species of the Borrelia burgdorferi Sensu Lato Complex, Borrelia americana sp. nov. J Clin Microbiol, 47(12), 3875-3880. doi:10.1128/JCM.01050-09

Rutz, H., Hogan, B., Hook, S., Hinckley, A., & Feldman, K. (2018). Exploring an alternative approach to Lyme disease surveillance in Maryland. Zoonoses Public Health, 65(2), 254-259. doi:10.1111/zph.12446

Rutz, H. J., Wee, S. B., & Feldman, K. A. (2018). Characterizing Lyme Disease Surveillance in an Endemic State. Zoonoses Public Health, 65(2), 247-253. doi:10.1111/zph.12275

Salkeld, D. J., & Lane, R. S. (2010). Community ecology and disease risk: lizards, squirrels, and the Lyme disease spirochete in California, USA. Ecology, 91(1), 293-298.

Salkeld, D. J., Leonhard, S., Girard, Y. A., Hahn, N., Mun, J., Padgett, K. A., & Lane, R. S. (2008). Identifying the reservoir hosts of the Lyme disease spirochete Borrelia burgdorferi in California: the role of the western gray squirrel (Sciurus griseus). Am J Trop Med Hyg, 79(4), 535-540.

Salkeld, D. J., Padgett, K. A., & Jones, J. H. (2013). A meta-analysis suggesting that the relationship between biodiversity and risk of zoonotic pathogen transmission is idiosyncratic. Ecol Lett, 16(5), 679-686. doi:10.1111/ele.12101

Savage, H. M., Burkhalter, K. L., Godsey, M. S., Jr., Panella, N. A., Ashley, D. C., Nicholson, W. L., & Lambert, A. J. (2017). Bourbon Virus in Field-Collected Ticks, Missouri, USA. Emerg Infect Dis, 23(12), 2017-2022. doi:10.3201/eid2312.170532

Savage, H. M., Godsey, M. S., Jr., Panella, N. A., Burkhalter, K. L., Ashley, D. C., Lash, R. R., . . . Nicholson, W. L. (2016). Surveillance for Heartland Virus (Bunyaviridae: Phlebovirus) in Missouri During 2013: First Detection of Virus in Adults of Amblyomma americanum (Acari: Ixodidae). J Med Entomol, 53(3), 607-612. doi:10.1093/jme/tjw028

Savage, H. M., Godsey, M. S., Jr., Panella, N. A., Burkhalter, K. L., Manford, J., Trevino-Garrison, I. C., . . . Raghavan, R. K. (2018). Surveillance for Tick-Borne Viruses Near the Location of a Fatal Human Case of Bourbon Virus (Family Orthomyxoviridae: Genus Thogotovirus) in Eastern Kansas, 2015. J Med Entomol. doi:10.1093/jme/tjx251

Schiffman, E. K., McLaughlin, C., Ray, J. A. E., Kemperman, M. M., Hinckley, A. F., Friedlander, H. G., & Neitzel, D. F. (2018). Underreporting of Lyme and Other Tick-Borne Diseases in Residents of a High-Incidence County, Minnesota, 2009. Zoonoses Public Health, 65(2), 230-237. doi:10.1111/zph.12291

Schreck, C., Mount, G., & Carlson, D. (1982). Pressurized sprays of permethrin on clothing for personal protection against the lone star tick (Acari: Ixodidae). Journal of economic entomology, 75(6), 1059-1061.

Schreck, C., Snoddy, E., & Spielman, A. (1986). Pressurized sprays of permethrin or DEET on military clothing for personal protection against Ixodes dammini (Acari: Ixodidae). Journal of Medical Entomology, 23, 396-399.

Schulze, L., Jordan, R. A., Dolan, M. C., Dietrich, G., Healy, S. P., & Piesman, J. (2008). Ability of 4-poster passive topical treatment devices for deer to sustain low population levels of Ixodes scapularis (Acari: Ixodidae) after integrated tick management in a residential landscape. J Med Entomol, 45(5), 899-904.

Schulze, T. L., Jordan, R. A., & Hung, R. W. (2000). Effects of granular carbaryl application on sympatric populations of Ixodes scapularis and Amblyomma americanum (Acari: Ixodidae) nymphs. Journal of Medical Entomology, 37(1), 121-125.

Schulze, T. L., Jordan, R. A., Hung, R. W., Taylor, R. C., Markowski, D., & Chomsky, M. S. (2001). Efficacy of granular deltamethrin against Ixodes scapularis and Amblyomma americanum (Acari: Ixodidae) nymphs. Journal of Medical Entomology, 38(2), 344-346.

Schulze, T. L., Jordan, R. A., & Krivenko, A. J. (2005). Effects of barrier application of granular deltamethrin on subadult Ixodes scapularis (Acari: Ixodidae) and nontarget forest floor arthropods. Journal of economic entomology, 98(3), 976-981.

Schulze, T. L., Jordan, R. A., Schulze, C. J., Healy, S. P., Jahn, M. B., & Piesman, J. (2007). Integrated use of 4-Poster passive topical treatment devices for deer, targeted acaricide applications, and Maxforce TMS bait boxes to rapidly suppress populations of Ixodes scapularis (Acari: Ixodidae) in a residential landscape. J Med Entomol, 44(5), 830-839.

Schulze, T. L., Jordan, R. A., Williams, M., & Dolan, M. C. (2017). Evaluation of the SELECT Tick Control System (TCS), a Host-Targeted Bait Box, to Reduce Exposure to Ixodes scapularis (Acari: Ixodidae) in a Lyme Disease Endemic Area of New Jersey. Journal of Medical Entomology.

Schwan, T. G., Raffel, S. J., Schrumpf, M. E., Schrumpf, M. E., Webster, L. S., Marques, A. R., . . . Hu, R. (2009). Tick-borne relapsing fever and Borrelia hermsii, Los Angeles County, California, USA. Emerg Infect Dis, 15(7), 1026-1031. doi:10.3201/eid1507.090223

Schwartz, A. M., Hinckley, A. F., Mead, P. S., Hook, S. A., & Kugeler, K. J. (2017). Surveillance for Lyme Disease - United States, 2008-2015. MMWR Surveill Summ, 66(22), 1-12. doi:10.15585/mmwr.ss6622a1

Schwartz, B. S., & Goldstein, M. D. (1990). Lyme disease in outdoor workers: risk factors, preventive measures, and tick removal methods. Am J Epidemiol, 131(5), 877-885.

Scott, J. D., Clark, K. L., Foley, J. E., Anderson, J. F., Durden, L. A., Manord, J. M., & Smith, M. L. (2017). Detection of Borrelia Genomospecies 2 in Ixodes spinipalpis Ticks Collected from a Rabbit in Canada. J Parasitol, 103(1), 38-46. doi:10.1645/16-127

Scott, J. D., Fernando, K., Banerjee, S. N., Durden, L. A., Byrne, S. K., Banerjee, M., . . . Morshed, M. G. (2001). Birds disperse ixodid (Acari: Ixodidae) and Borrelia burgdorferi-infected ticks in Canada. J Med Entomol, 38(4), 493-500. doi:10.1603/0022-2585-38.4.493

Scott, J. D., & Scott, C. M. (2018). Lyme Disease Propelled by Borrelia burgdorferi-Infected Blacklegged Ticks, Wild Birds and Public Awareness ─ Not Climate Change. J Veter Sci Med, 6(1), 8.

Shadick, N. A., Zibit, M. J., Nardone, E., DeMaria, A., Jr., Iannaccone, C. K., & Cui, J. (2016). A School-Based Intervention to Increase Lyme Disease Preventive Measures Among Elementary School-Aged Children. Vector Borne Zoonotic Dis, 16(8), 507-515. doi:10.1089/vbz.2016.1942

Skoracka, A., Magalhaes, S., Rector, B. G., & Kuczynski, L. (2015). Cryptic speciation in the Acari: a function of species lifestyles or our ability to separate species? Exp Appl Acarol, 67(2), 165-182. doi:10.1007/s10493-015-9954-8

Solberg, V., Neidhardt, K., Sardelis, M., Hoffmann, F., Stevenson, R., Boobar, L., & Harlan, H. (1992). Field evaluation of two formulations of cyfluthrin for control of Ixodes dammini and Amblyomma americanum (Acari: Ixodidae). Journal of Medical Entomology, 29(4), 634-638.

Sonenshine, D. E. (2018). Range Expansion of Tick Disease Vectors in North America: Implications for Spread of Tick-Borne Disease. Int J Environ Res Public Health, 15(3). doi:10.3390/ijerph15030478

Spielman, A., Levine, J. F., & Wilson, M. L. (1984). Vectorial capacity of North American Ixodes ticks. Yale J Biol Med, 57(4), 507-513.

Springer, Y. P., Eisen, L., Beati, L., James, A. M., & Eisen, R. J. (2014). Spatial distribution of counties in the continental United States with records of occurrence of Amblyomma americanum (Ixodida: Ixodidae). J Med Entomol, 51(2), 342-351.

Springer, Y. P., Jarnevich, C. S., Barnett, D. T., Monaghan, A. J., & Eisen, R. J. (2015). Modeling the Present and Future Geographic Distribution of the Lone Star Tick, Amblyomma americanum (Ixodida: Ixodidae), in the Continental United States. Am J Trop Med Hyg, 93(4), 875-890. doi:10.4269/ajtmh.15-0330

Stafford III, K. C. (1991). Effectiveness of host-targeted permethrin in the control of Ixodes dammini (Acari: Ixodidae). Journal of Medical Entomology, 28(5), 611-617.

Stafford, K. C. (2004). Tick management handbook. An integrated guide for homeowners, pest control operators and public health officials for the prevention of tick-associated diseases. New Haven, USA: The Connecticut Agricultural Experiment Station. Retrieved from http://www.ct.gov/caes/lib/caes/documents/special_features/tickhandbook.pdf

Stafford, K. C., & Allan, S. A. (2010). Field applications of entomopathogenic fungi Beauveria bassiana and Metarhizium anisopliae F52 (Hypocreales: Clavicipitaceae) for the control of Ixodes scapularis (Acari: Ixodidae). Journal of Medical Entomology, 47(6), 1107-1115.

Stafford, K. I. (1991). Effectiveness of carbaryl applications for the control of Ixodes dammini (Acari: Ixodidae) nymphs in an endemic residential area. Journal of Medical Entomology, 28(1), 32-36.

Steere, A. C., Broderick, T. F., & Malawista, S. E. (1978). Erythema chronicum migrans and Lyme arthritis: epidemiologic evidence for a tick vector. Am J Epidemiol, 108(4), 312-321.

Steere, A. C., Strle, F., Wormser, G. P., Hu, L. T., Branda, J. A., Hovius, J. W., . . . Mead, P. S. (2016). Lyme borreliosis. Nat Rev Dis Primers, 2, 16090. doi:10.1038/nrdp.2016.90

Steinke, J. W., Platts-Mills, T. A., & Commins, S. P. (2015). The alpha-gal story: lessons learned from connecting the dots. J Allergy Clin Immunol, 135(3), 589-596; quiz 597. doi:10.1016/j.jaci.2014.12.1947

Stricker, R. B., & Johnson, L. (2007). Lyme wars: let's tackle the testing. BMJ, 335(7628), 1008. doi:10.1136/bmj.39394.676227.BE

Stricker, R. B., & Johnson, L. (2010). Lyme disease diagnosis and treatment: lessons from the AIDS epidemic. Minerva Med, 101(6), 419-425.

Stromdahl, E. Y., & Hickling, G. J. (2012). Beyond Lyme: aetiology of tick-borne human diseases with emphasis on the south-eastern United States. Zoonoses Public Health, 59 Suppl 2, 48-64. doi:10.1111/j.1863-2378.2012.01475.x

Stromdahl, E. Y., Nadolny, R. M., Hickling, G. J., Hamer, S. A., Ogden, N. H., Casal, C., . . . Pilgard, M. A. (2018). Amblyomma americanum (Acari: Ixodidae) Ticks Are Not Vectors of the Lyme Disease Agent, Borrelia burgdorferi (Spirocheatales: Spirochaetaceae): A Review of the Evidence. J Med Entomol. doi:10.1093/jme/tjx250

Swei, A., Ostfeld, R. S., Lane, R. S., & Briggs, C. J. (2011). Impact of the experimental removal of lizards on Lyme disease risk. Proc Biol Sci, 278(1720), 2970-2978. doi:10.1098/rspb.2010.2402

Teel, P. D., Ketchum, H. R., Mock, D. E., Wright, R. E., & Strey, O. F. (2010). The Gulf Coast tick: a review of the life history, ecology, distribution, and emergence as an arthropod of medical and veterinary importance. J Med Entomol, 47(5), 707-722.

Tenth Amendment: Reserved Powers. Retrieved from https://www.gpo.gov/fdsys/pkg/GPO-CONAN-1992/pdf/GPO-CONAN-1992-10-11.pdf

Thomas, N., Rutz, H. J., Hook, S. A., Hinckley, A. F., Lukacik, G., Backenson, B. P., . . . White, J. L. (2018). Assessing diagnostic coding practices among a sample of healthcare facilities in Lyme disease endemic areas: Maryland and New York - A Brief Report. Zoonoses Public Health, 65(2), 275-278. doi:10.1111/zph.12414

Thompson, P. N., & Etter, E. (2015). Epidemiological surveillance methods for vector-borne diseases. Rev Sci Tech, 34(1), 235-247.

TickEncounter Resource Center. (2018). Retrieved from http://tickencounter.org/prevention

Tijsse-Klasen, E., Koopmans, M. P., & Sprong, H. (2014). Tick-borne pathogen - reversed and conventional discovery of disease. Front Public Health, 2, 73. doi:10.3389/fpubh.2014.00073

Tokarz, R., Sameroff, S., Tagliafierro, T., Jain, K., Williams, S. H., Cucura, D. M., . . . Lipkin, W. I. (2018). Identification of Novel Viruses in Amblyomma americanum, Dermacentor variabilis, and Ixodes scapularis Ticks. mSphere, 3(2). doi:10.1128/mSphere.00614-17

Town of Ridgefield, C. (2018). BLAST Lyme & Tick-Borne Disease Prevention Program. Retrieved from https://www.ridgefieldct.org/blast-lyme-tick-borne-disease-prevention-program

Trevejo, R. T., Schriefer, M. E., Gage, K. L., Safranek, T. J., Orloski, K. A., Pape, W. J., . . . Campbell, G. L. (1998). An interstate outbreak of tick-borne relapsing fever among vacationers at a Rocky Mountain cabin. Am J Trop Med Hyg, 58(6), 743-747.

Tuckow, A. P., & Temeyer, K. B. (2015). Discovery, adaptation and transcriptional activity of two tick promoters: Construction of a dual luciferase reporter system for optimization of RNA interference in rhipicephalus (boophilus) microplus cell lines. Insect Mol Biol, 24(4), 454-466. doi:10.1111/imb.12172

URI. TickEncounter Resource Center. Retrieved from http://www.tickencounter.org/current_tick_activity

USDA. (1990). SCS/ARS/CES Pesticide Properties Database: Version 2.0 (Summary). Syracuse, NY: USDA-Soil Conservation Service.

Van Zee, J., Piesman, J. F., Hojgaard, A., & Black, W. I. (2015). Nuclear Markers Reveal Predominantly North to South Gene Flow in Ixodes scapularis, the Tick Vector of the Lyme Disease Spirochete. PLoS One, 10(11), e0139630. doi:10.1371/journal.pone.0139630

Vaughn, M. F., Funkhouser, S. W., Lin, F.-C., Fine, J., Juliano, J. J., Apperson, C. S., & Meshnick, S. R. (2014). Long-lasting permethrin impregnated uniforms: a randomized-controlled trial for tick bite prevention. American Journal of Preventive Medicine, 46(5), 473-480.

Vazquez, M., Muehlenbein, C., Cartter, M., Hayes, E. B., Ertel, S., & Shapiro, E. D. (2008). Effectiveness of personal protective measures to prevent Lyme disease. Emerg Infect Dis, 14(2), 210-216. doi:10.3201/eid1402.070725

Vázquez, M., Muehlenbein, C., Cartter, M., Hayes, E. B., Ertel, S., & Shapiro, E. D. (2008). Effectiveness of personal protective measures to prevent Lyme disease. Emerging Infectious Diseases, 14(2), 210.

Voordouw, M. J., Tupper, H., Onder, O., Devevey, G., Graves, C. J., Kemps, B. D., & Brisson, D. (2013). Reductions in human Lyme disease risk due to the effects of oral vaccination on tick-to-mouse and mouse-to-tick transmission. Vector Borne Zoonotic Dis, 13(4), 203-214. doi:10.1089/vbz.2012.1003

Wagenet, L. P. (1985). A review of physical-chemical parameters related to the soil and groundwater fate of selected pesticides in New York State, Report No. 30. Ithaca, NY: Cornell University Agricultural Experiment Station.

Welch, M. D., Reed, S. C. O., & Hagland, C. M. (2012). Establishing intracellular infections: escape from the phagosome and intracellular colonization Intracellular Pathogens II: Rickettsiales (pp. 154).

Wendt, A., Kreienbrock, L., & Campe, A. (2015). Zoonotic disease surveillance--inventory of systems integrating human and animal disease information. Zoonoses Public Health, 62(1), 61-74. doi:10.1111/zph.12120

White, J., Noonan-Toly, C., Lukacik, G., Thomas, N., Hinckley, A., Hook, S., & Backenson, P. B. (2018). Lyme Disease Surveillance in New York State: an Assessment of Case Underreporting. Zoonoses Public Health, 65(2), 238-246. doi:10.1111/zph.12307

Williams, S. C., Stafford, K. C., 3rd, Molaei, G., & Linske, M. A. (2018). Integrated Control of Nymphal Ixodes scapularis: Effectiveness of White-Tailed Deer Reduction, the Entomopathogenic Fungus Metarhizium anisopliae, and Fipronil-Based Rodent Bait Boxes. Vector Borne Zoonotic Dis, 18(1), 55-64. doi:10.1089/vbz.2017.2146

Wilson, M. L., Telford, S. R., 3rd, Piesman, J., & Spielman, A. (1988). Reduced abundance of immature Ixodes dammini (Acari: Ixodidae) following elimination of deer. J Med Entomol, 25(4), 224-228.

Wong, D., & Higgins, C. L. (2010). Park rangers as public health educators: the Public Health in the Parks Grants Initiative. Am J Public Health, 100(8), 1370-1373. doi:10.2105/AJPH.2009.179622

Wood, C. L., & Lafferty, K. D. (2013). Biodiversity and disease: a synthesis of ecological perspectives on Lyme disease transmission. Trends Ecol Evol, 28(4), 239-247. doi:10.1016/j.tree.2012.10.011

Working to solve the tick problem using IPM practices. (Tick IPM Working Group). Retrieved from https://tickipmwg.wordpress.com/

Wormser, G. P., Dattwyler, R. J., Shapiro, E. D., Halperin, J. J., Steere, A. C., Klempner, M. S., . . . Nadelman, R. B. (2006). The clinical assessment, treatment, and prevention of lyme disease, human granulocytic anaplasmosis, and babesiosis: clinical practice guidelines by the Infectious Diseases Society of America. Clin Infect Dis, 43(9), 1089-1134. doi:10.1086/508667

Wormser, G. P., Masters, E., Nowakowski, J., McKenna, D., Holmgren, D., Ma, K., . . . Nadelman, R. B. (2005). Prospective clinical evaluation of patients from Missouri and New York with erythema migrans-like skin lesions. Clin Infect Dis, 41(7), 958-965. doi:10.1086/432935

Wormser, G. P., Nowakowski, J., Nadelman, R. B., Visintainer, P., Levin, A., & Aguero-Rosenfeld, M. E. (2008). Impact of clinical variables on Borrelia burgdorferi-specific antibody seropositivity in acute-phase sera from patients in North America with culture-confirmed early Lyme disease. Clin Vaccine Immunol, 15(10), 1519-1522. doi:10.1128/CVI.00109-08

Wu, Y., Ling, F., Hou, J., Guo, S., Wang, J., & Gong, Z. (2016). Will integrated surveillance systems for vectors and vector-borne diseases be the future of controlling vector-borne diseases? A practical example from China. Epidemiol Infect, 144(9), 1895-1903. doi:10.1017/S0950268816000297

Xu, G., Mather, T. N., Hollingsworth, C. S., & Rich, S. M. (2016). Passive Surveillance of Ixodes scapularis (Say), Their Biting Activity, and Associated Pathogens in Massachusetts. Vector Borne Zoonotic Dis, 16(8), 520-527. doi:10.1089/vbz.2015.1912

Yoon, E. C., Vail, E., Kleinman, G., Lento, P. A., Li, S., Wang, G., . . . Fallon, J. T. (2015). Lyme disease: a case report of a 17-year-old male with fatal Lyme carditis. Cardiovasc Pathol, 24(5), 317-321. doi:10.1016/j.carpath.2015.03.003

Zeidner, N. S., Burkot, T. R., Massung, R., Nicholson, W. L., Dolan, M. C., Rutherford, J. S., . . . Maupin, G. O. (2000). Transmission of the agent of human granulocytic ehrlichiosis by Ixodes spinipalpis ticks: evidence of an enzootic cycle of dual infection with Borrelia burgdorferi in Northern Colorado. J Infect Dis, 182(2), 616-619. doi:10.1086/315715

Zolnik, C. P., Falco, R. C., Kolokotronis, S. O., & Daniels, T. J. (2015). No Observed Effect of Landscape Fragmentation on Pathogen Infection Prevalence in Blacklegged Ticks (Ixodes scapularis) in the Northeastern United States. PLoS One, 10(10), e0139473. doi:10.1371/journal.pone.0139473

Appendix 1. Subcommittee Members and Support Staff

Subcommittee Members

Pat Smith Subcommittee Co-Chair; Lyme Disease Association

Ben Beard Subcommittee Co-Chair; CDC

Jill Auerbach, Founder, Tick Research to Eliminate Diseases; Founder, Stop Ticks on People (S.T.O.P.)

Neeta Connally, PhD, MSPH, Associate Professor, Tick-borne Disease Prevention Laboratory, Western Connecticut State

Katherine Feldman, DVM, MPH, Senior Epidemiologist, MITRE

Thomas N. Mather, PhD, Professor, Center for Vector-Borne Disease; Director, TickEncounter Resource Center

Phyllis Mervine, President, LymeDisease.org

Colonel Robin Nadolny, PhD, Medical Service Team Lead, Tick-Borne Disease Laboratory, Army Public Health Center

Adalberto Perez de Leon, DVM, PhD, MS, Director, Knipling-Bushland U.S. Livestock Insects Research Laboratory, United States Department of Agriculture-Agricultural Research Service

Daniel E. Sonenshine, PhD, Eminent Professor of Biological Science, Old Dominion University

Jean I. Tsao, PhD, Associate Professor, Departments of Fisheries and Wildlife and of Large Animal Clinical Sciences, Michigan State University

Monica M. White, President and Co-founder, Colorado Tick-Borne Disease Awareness Association

Stephen Wikel, PhD, Professor and Chair Emeritus of Medical Sciences, St. Vincent’s Medical Center, Quinnipiac University

Support Staff

James Berger, Designated Federal Officer; Office of HIV/AIDS and Infectious Disease Policy, U.S. Department of Health and Human Services

Yanni Wang, PhD, Contractor/Writer, Kauffman & Associates, Inc.

Appendix 2. Subcommittee Agendas and Top-Line Issues

Meeting 1, February 23, 2018

Agenda

Roll call
Explanation of formal notetaking of subcommittee meetings
Introduction of Dr. Paul Mead and presentation title
Invited presentation on surveillance for Lyme disease in the United States
Q&A
Dates for next meetings
Explanation of how discussion will proceed
Brainstorming full list: “What issues need to be examined or questions need to be addressed to ensure that US responds effectively to issues of our subcommittee.”
Vote full list; decide when and how to move to the Prioritized List
Presenters needed to fill critical needs within short time frame
Call for adjournment

Summary

Invited speaker Paul Mead provided an overview of surveillance for nationally notifiable diseases with a focus on Lyme disease. The subcommittee devoted the rest of the conference call to generating a full list of key issues related to disease vectors, surveillance, and prevention; and planning for upcoming subcommittee meetings.

Meeting 2, March 2, 2018

Agenda

Roll call
Introduction of Dr. Neeta Connally and presentation title
Invited presentation
Q&A
Priority Charge (Table 2) – Explanation of how discussion will proceed
Discussion and consensus/vote on the prioritized list
Next steps in the process
Announcement of the next meeting date
Call for adjournment

Summary

Subcommittee member Neeta Connally provided an overview of studies focused on preventing diseases caused by blacklegged ticks. The subcommittee members discussed the Complete and Prioritized Lists of Issues that were due March 2, 2018.

Meeting 3, March 8, 2018

Agenda

Roll call
Discussion of the next phase of the report
Begin writing process: Background, State of Science, Greatest Needs, Recommendations
Nominations of suggested priority list coordinators by Co-Chairs
Discussion of the List of the Prioritized Issues and volunteers for each priority
Table 2 Prioritized Issues: Brainstorm and flesh out contents
Announcement of the next meeting date
Call for adjournment

Summary

Co-Chair Pat Smith provided an update on the timeline, and Co-Chair Ben Beard explained the writing process. The subcommittee discussed strategies for the group to effectively work together on writing the final report, and brainstormed topics that need to be discussed in Key Issue 1.

Meeting 4, March 16, 2018

Agenda

Roll call
Vote on the first draft of the Background and Methods sections
Updates from HHS
Full subcommittee discussion on Priority 2
Full subcommittee discussion on Priority 3
Full subcommittee discussion on Priority 4
Announcement of the next meeting date
Call for adjournment

Summary

The subcommittee voted on the first draft of the Background and Methods Section, and discussed contents for Priorities 2, 3, and 4.

Meeting 5, March 23, 2018

Agenda

Roll call
Introduction of Robert (Bob) Lane, PhD
Invited presentation
Q&A
Discussion of priority 5
Discussion of and voting on the Background section
Announcement of the next meeting date
Call for adjournment

Summary

Robert (Bob) Lane provided an overview of his decades-long research on Lyme disease in California. The subcommittee discussed and voted on the first draft of the Background Section.

Meeting 6, March 28, 2018

Agenda

Roll call
HHS updates
Discussion of the Results section
Announcement of the next meeting date
Call for adjournment

Summary

The subcommittee reviewed the timeline for the final report and milestone reports to the Working Group, and they discussed how to develop the Results Section following the guidelines from the U.S. Department of Health and Human Services (HHS).

Meeting 7, April 6, 2018

Agenda

Roll call
HHS updates
Discussion of the Results section
Announcement of the next meeting date
Call for adjournment

Summary

Co-Chair Pat Smith provided updates from HHS. The subcommittee discussed how to develop and finalize the Results Section following the guidelines from HHS.

Meeting 8, April 13, 2018

Agenda

Roll call
HHS updates
Discussion of the Results section
Announcement of the next meeting date
Call for adjournment

Summary

The co-chairs answered questions the subcommittee members had regarding writing the Results section. The subcommittee acknowledged challenges of writing a well-researched report within a short timeframe. They discussed how to revise the draft, and made plans for voting on the first draft.

Meeting 9, April 18, 2018

Agenda

Roll call
Discussion of the Results section
Vote
Call for adjournment

Summary

The subcommittee reviewed and voted on 1) the first draft of the Results section, and 2) the “potential actions for the working group to consider.” They also made plans to further revise and finalize the section.

Meeting 10, April 26, 2018

Agenda

Roll call
Vote on the first three sections of the report to the working group
Vote on the final version of the Results section to be submitted by the Co-Chairs
Vote on the final lists of proposed actions for the working group to consider
Closing remarks
Call for adjournment

Summary

The subcommittee discussed and voted on the final version of the Results section and potential actions for the Working Group to consider.

Content created by Office of HIV/AIDS and Infectious Disease Policy
Content last reviewed on May 9, 2018