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Tick Biology, Ecology, and Control Subcommittee Report to the Tick-Borne Disease Working Group

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. Readers should not consider the report or any part of it to be guidance or instruction regarding the diagnosis, care, or treatment of tick-borne diseases or to supersede in any way existing guidance. All subcommittee members actively participated in the development of this report. Members voted to approve submission of the report to the Working Group and on the wording of each of the possible actions contained in the report. The vote to submit the report indicates general agreement with the content of the document, but it does not necessarily indicate complete agreement with each and every statement in the full report.

Background

The increasing incidence of tick-borne diseases poses a serious threat to public health. Currently, the U.S. Centers for Disease Control and Prevention (CDC) recognize 18 tick-borne pathogens in the United States. However, researchers and clinicians continue to discover emerging pathogens and new medical conditions associated with tick bites. Considering the current knowledge of tick biology, ecology, and approaches to control tick populations, this subcommittee sought to identify the causes for, and strategies to control, the increased number of tick-borne disease cases in the United States.

A global problem, tick-borne diseases pose a threat to the health of non-U.S. populations, as well as U.S. military personnel and civilians living and working abroad. While some of those diseases are not currently present in the United States, the recent introduction of foreign ticks increases the potential for exposure to new tick-borne pathogens. Critical to reducing the incidence of established and emerging tick-borne diseases is a required understanding of how the following factors contribute to the increased risk of tick-borne diseases: climate variability, environmental change, host and vector population increases, range expansion, human use of tick habitats, and introduction of foreign ticks. Armed with this knowledge, interventions can be adapted for effective control. These factors are, therefore, the focus of this report.

An enhanced understanding of the reasons for the rising incidence of tick-borne diseases will help scientists and health care professionals develop strategies to lower the risk for disease transmission. Additional activities and research in the following areas will ultimately provide practical approaches to reduce the risk of tick-borne diseases.

  • Identification and understanding of the environmental and human behavioral determinants (climate and habitat variability and human landscape use patterns) driving tick spread and increases in tick populations and human-tick encounters.
  • Improved communication and sharing of best practices between tick/pest management experts, human and animal health experts, and Federal agencies.
  • Improved surveillance for established and newly introduced tick vectors.
  • Development and adoption of effective management and control strategies for established and emerging tick species.
  • Identification and removal of barriers to effective management and control strategies for established and emerging tick species.

Methods

Composition of the subcommittee

At Public Meeting 9 on June 4, 2019, the Tick-Borne Disease Working Group selected Adalberto (Beto) Pérez de León, a Federal representative, and Robert (Bob) Sabatino, a public representative, to serve as co-chairs of the Tick Biology, Ecology, and Control Subcommittee. Bob Sabatino’s term on the Working Group expired on August 5, 2019, at which time he was replaced as Working Group member and subcommittee co-chair by Kevin Macaluso, also a member of the public. Bob Sabatino continued serving on the subcommittee as a patient representative.

The subcommittee was composed of Federal (3), public health (1) academic (9), and patient (3) representatives (see Table 1: Members of the Tick Biology, Ecology, and Control). The expertise in tick biology, ecology, control, and tick-borne diseases is supported by over 250 years of basic and applied research experience. The patient representatives provided perspective on the experience of those afflicted by tick-borne diseases. Due to unforeseen circumstances, two members (one academic and one patient representative) needed to excuse themselves from the subcommittee before the process was complete.

Meetings

An initial meeting was called to introduce and review relevant documents and discuss the timeline and deliverables. At this and subsequent meetings, the subcommittee worked to ascertain gaps in knowledge and identify experts who could educate the group on those topics. The committee met on a bi-weekly basis via teleconference (see Table 2: Overview of Meetings). A total of eight subject matter experts from within and outside the subcommittee gave presentations on the status of the field (see Table 3: Presenters). Discussion and questions were allowed during and after the presentations.

Development of the Report to the Tick-Borne Disease Working Group

A topic brief was developed for the purpose of identifying relevant published studies. A total of nine keyword search terms yielded over 500 peer-reviewed articles that were used to inform the subcommittee. The analysis of the literature provided both supporting and counter conclusions on the factors contributing to tick expansion.

Public comments were compiled by the Public Comment Subcommittee and made available to the Co-Chairs who then shared them with members. At least one Co-Chair and one member of the subcommittee regularly reviewed public comments for relevance to the subcommittee’s work and potential inclusion in its report. Public comments were also discussed by the group during Subcommittee meetings.

The responses to the Federal Inventory were not received in time for the Subcommittee to incorporate them into this report.

Three individuals accepted roles as leaders of the writing groups created to develop the content for the three main topic areas: biology, ecology, and control. Other members volunteered to contribute to each section based on their expertise and knowledge. The groups exchanged drafts by email and communicated during conference calls in order to avoid overlap in the sections and to determine how the topic areas were interrelated. (Appendix B contains all three writing group reports in their entirety.)

Each writing group put forth several Potential Actions for the entire Subcommittee to consider. The Potential Actions were compiled into one document. Using a PICK Chart, each member then prioritized the Potential Actions by weighing the difficulty of the action against the potential payoff. This method, along with meeting discussions, enabled the group to refine and prioritize the list of Potential Actions, which were divided into two Priority Issues.

To compile the Results and Potential Actions section, the content from the three writing group reports was organized into one narrative used to introduce and support the final list of Potential Actions. The written product was presented to the entire subcommittee and then discussion was held on content via teleconference. The main points were generally agreed upon, as they were vetted over the course of the initial meetings and were complemented by presentations by experts. During the Subcommittee’s final meeting, members voted on each Potential Action. Then once the report was finalized, members voted by email to accept it and submit it to the Tick-Borne Disease Working Group (see Table 4).

Updates to the Working Group

At Public Meeting 10 on September 12, 2019, the Subcommittee Co-Chairs presented an update to the Tick-Borne Disease Working Group using a PowerPoint presentation provided to them by the leadership and support team. To prepare their presentation, the co-chairs worked together to:

  • Provide an accounting of what had been learned and discussed at meetings, including expert presentations;
  • Outline the goals of their report to the Working Group, as agreed upon by all Subcommittee members during meetings;
  • Explain where the Subcommittee was in the process of writing its report; and
  • Identify the Subcommittee’s plan for completing its report to the Working Group.

At Public Meeting 11 on January 28 and 29, 2019, the Subcommittee Co-Chairs presented their final report to the Tick-Borne Disease Working Group using a PowerPoint presentation provided to them by the leadership and support team. To prepare their presentation, the Co-Chairs worked with the support writer to populate the slide deck using the content in the Subcommittee Report. The Co-Chairs then sent the slide deck to the Subcommittee members to provide feedback via email.

Membership Composition, Meetings, Presentations, and Decisions
The following tables reflect the membership and work completed by the Tick Biology, Ecology, and Control Subcommittee.

Table 1: Members of the Tick Biology, Ecology, and Control Subcommittee

Members

Type

Stakeholder Group

Expertise

Co-Chair
Kevin Macaluso, PhD. University of South Alabama, Mobile, AL

Public

Academic Researcher

Locke Distinguished Chair, Chair of Microbiology and Immunology, College of Medicine, University of South Alabama

Co-Chair
Adalberto (Beto) A. Pérez de León, DVM, MS, PhD

U.S. Department of Agriculture—Agricultural Research Service, Kerrville, TX

Federal

Government Researcher

Director, Knipling-Bushland U.S. Livestock Insects Research Laboratory, U.S. Department of Agriculture—Agricultural Research Service

Jill Auerbach

Hudson Valley Lyme Disease Association, NY

  • Resigned on July 23, 2019

Public

Patient Advocate

Chairperson, Hudson Valley Lyme Disease Association; Coordinator, Tick Research to Eliminate Diseases; Board Member, Stop Ticks on People (S.T.O.P.)

Tracy (Trey) Cahill,

DC Health, Washington, DC

Public

Researcher/epidemiologist

Public Health Analyst, Location Intelligence (GIS), Health Regulation and Licensing Administration, DC Health

Neeta Connally, PhD, MSPHWestern Connecticut State University, Danbury, CT

Public

Academic Researcher

Associate Professor, Principal Investigator, Tickborne Disease Prevention Laboratory, Department of Biological & Environmental Sciences Western Connecticut State University

Maria Diuk-Wasser, PhD,

Columbia University, New York, NY

Public

Academic Researcher

Associate Professor and Principal Investigator, Eco-Epidemiology Lab, Department of Ecology, Evolution, and Environmental Biology, Columbia University

Lars Eisen, PhD,

Centers for Disease Control and Prevention, Fort Collins, CO

Federal

Government Researcher

Research Entomologist, Division of Vector-Borne Diseases, National Center for Emerging and Zoonotic Infectious Diseases, Centers for Disease Control and Prevention

Dina Fonseca, PhD,

Rutgers University, The State University of New Jersey, New Brunswick, NJ

  • Resigned on September 12, 2019

Public

Academic Researcher

Professor and Director of the Center for Vector Biology, Department of Entomology, Rutgers, The State University of New Jersey

Howard Ginsberg, PhD,

U.S. Geological Survey, Kingston, RI

Federal

Government Researcher

Research Ecologist, U.S. Geological Survey, Patuxent Wildlife Research Center, Coastal Field Station, University of Rhode Island

Lonnie Marcum, PT, BSHCA,

LymeDisease.org, San Ramon, CA

Public

Health Care Provider, Patient Advocate

Physical Therapist; Health and Science Writer for LymeDisease.org

R. Michael Roe, PhD,

North Carolina State University, Raleigh, NC

Public

Academic Researcher

William Neal Reynolds Distinguished Professor, Department of Entomology, North Carolina State University

Robert (Bob) Sabatino,

Lyme Society, Inc., New York, NY

  • Membership on the Tick-Borne Disease Working Group expired on August 5, 2019 at which time he transitioned from Subcommittee Co-Chair to Member

Public

Patient Advocate

Founder and Executive Director, Lyme Society, Inc.

Daniel Sonenshine, PhD,

Old Dominion University, Norfolk, VA

Public

Academic Researcher

Eminent Professor of Biological Science, Old Dominion University; Guest Researcher, Laboratory of Malaria and Vector Research, National Institute of Allergy and Infectious Disease, National Institutes of Health

Kirby C. Stafford III, PhD,

The Connecticut Agricultural Experiment Station, New Haven, CT

  • Joined on August 5, 2019

Public

State Researcher

Chief Entomologist, Department of Entomology, Center for Vector Biology and Zoonotic Diseases, NE Regional Center for Excellence in Vector Borne Diseases, The Connecticut Agricultural Experiment Station

Pete D. Teel, PhD,

Texas A&M University, College Station, TX

Public

Academic Researcher

Regents Professor and Interim Department Head, Department of Entomology, Texas A&M University

Stephen Wikel, PhD,

Quinnipiac University, Hamden, CT

Public

Academic Researcher

Professor and Chair Emeritus of Medical Sciences, St. Vincent's Medical Center, Quinnipiac University

Table 2: Overview of Tick Biology, Ecology, and Control Meetings, 2019

Meeting #

Date

Present

Topics Addressed

1

July 18, 2019

Adalberto A. Pérez de León, DVM, MS, PhD (co-chair), Robert Sabatino (co-chair), Jill Auerbach, Neeta Connally, Lars Eisen, Dina Fonseca, Howard Ginsberg, Lonnie Marcum, R. Michael Roe, Daniel Sonenshine, Stephen Wikel, 

James Berger (DFO), Jennifer Gillissen (contractor support), Cat Thomson (contractor support)

Member introductions; Subcommittee formation and review of relevant documents; Milestones, Deliverables, Timeline; Subcommittee Report outline; Discussion of potential speakers; Date of next meeting

2

August 5, 2019

Adalberto (Beto) A. Pérez de León (co-chair), Robert (Bob) Sabatino (ch-chair), Trey Cahill, Neeta Connally, Maria Diuk-Wasser, Lars Eisen, Dina Fonseca, Howard Ginsberg, Kirby C. Stafford III, Stephen Wikel

James Berger (DFO), Jennifer Gillissen (contractor support), Cat Thomson (contractor support)

Subcommittee logistics; Topic development briefs; Presentation—Overview of Work Completed by the 2018 Disease Vectors, Surveillance, and Prevention Subcommittee by Stephen Wikel, PhD; Presentation—Concepts Vector Control: Integrated Tick Management by Kirby C. Stafford III, PhD; Identifying Potential Actions for the Subcommittee’s Report to the Tick-Borne Disease Working Group; Potential Question for the Federal Inventory

3

August 12, 2019

Kevin Macaluso (co-chair), Adalberto A. Pérez de León (co-chair), Trey Cahill, Neeta Connally, Lars Eisen, Lonnie Marcum, R. Michael Roe, Robert Sabatino, Kirby C. Stafford III, Pete D. Teel, Stephen Wikel

James Berger (DFO), Jennifer Gillissen (contractor support), Cat Thomson (contractor support)

Presentation—Tick Surveillance as a Public Health Tool by Rebecca Eisen, PhD; Topic development briefs; Reviewing written comments to the Tick-Borne Disease Working Group; Federal inventory; Potential speakers

4

August 26, 2019

Kevin Macaluso (co-chair), Adalberto A. Pérez de León (co-chair), Trey Cahill, Neeta Connally, Maria Diuk-Wasser, Lars Eisen, Howard Ginsberg, Lonnie Marcum, Robert Sabatino, Daniel Sonenshine, Kirby C. Stafford III, Pete D. Teel, Stephen Wikel

James Berger (DFO), Jennifer Gillissen (contractor support), Cat Thomson (contractor support)

Presentation—The Tick Project: Testing Environmental Interventions to Prevent Lyme and Other Tick-Borne Diseases in Our Communities by Dr. Richard S. Ostfeld; Presentation—Integrated Tick Management Solutions: Reservoir-Targeted Vaccines and Predictive Analytics by Chris Przybyszewski; Subcommittee Membership Changes; Upcoming Speaker Presentations

5

September 9, 2019

Kevin Macaluso (co-chair), Adalberto A. Pérez de León (co-chair), Trey Cahill, Neeta Connally, Lars Eisen, Howard Ginsberg, Lonnie Marcum, Daniel Sonenshine, Kirby C. Stafford III, Pete D. Teel, Stephen Wikel

James Berger (DFO), Jennifer Gillissen (contractor support), Cat Thomson (contractor support)

Presentation—Invasive Species Advisory Council White Paper: Interface Between Invasive Species and the Increased Incidence of Tick-Borne Diseases, and Implications for Federal Land Managers by Ed Clark, Ernesto Dominguez, DVM, and Jeff Morisette, PhD; Presentation—The Emergence of Lyme Disease in Michigan: Past, Present, and Future? by Jean Tsao, PhD; Dividing into Writing Groups; Reviewing the Tick Biology, Ecology, and Control PowerPoint Presentation for Meeting 10 of the Tick-Borne Disease Working Group

6

September 23, 2019

Kevin Macaluso (co-chair), Adalberto A. Pérez de León (co-chair), Trey Cahill, Neeta Connally, Maria Diuk-Wasser, Lars Eisen, Howard Ginsberg, Lonnie Marcum, R. Michael Roe, Daniel Sonenshine, Kirby C. Stafford III, Stephen Wikel

James Berger (DFO), Jennifer Gillissen (contractor support), Cat Thomson (contractor support)

September 12, 2019 Tick-Borne Disease Working Group public meeting; Subcommittee membership update; Identification of writing group members; Discussion of Topic Development Briefs; Finalizing Background and Methods sections for October 1, 2019 deadline; Strategy for writing subcommittee report content; Milestones and deliverables

7

October 10, 2019

Adalberto A. Pérez de León (co-chair), Trey Cahill, Neeta Connally, Lars Eisen, Howard Ginsberg, Lonnie Marcum, R. Michael Roe, Daniel Sonenshine, Kirby C. Stafford III, Pete D. Teel, Stephen Wikel

James Berger (DFO), Jennifer Gillissen (contractor support), Cat Thomson (contractor support)

Vote to approve Meeting 6 Summary; Explanation of guidance documents; Writing group updates and expectations; Update on CDC’s vector-borne disease prevention and control network; Discussion and preliminary vote of the Background section

8

October 21, 2019

Kevin Macaluso (co-chair), Adalberto A. Pérez de León (co-chair), Trey Cahill, Neeta Connally, Maria Diuk-Wasser, Lars Eisen, Howard Ginsberg, Lonnie Marcum,  Daniel Sonenshine, Krby C. Stafford III, Pete D. Teel

Debbie Seem (TBDWG support), Jennifer Gillissen (contractor support), Cat Thomson (contractor support)

Presentation of documents: Email regarding terminology, Writing Group Report Priorities Merged, Subcommittee Timeline, and PICK Chart; Presentation of Goals and Potential Actions: Biology; Presentation of Goals and Potential Actions: Ecology; Presentation of Goals and Potential Actions: Control; Next steps

9

November 4, 2019

Kevin Macaluso (co-chair), Adalberto A. Pérez de León (co-chair), Trey Cahill, Neeta Connally, Maria Diuk-Wasser, Lars Eisen, Howard Ginsberg, Lonnie Marcum,  Daniel Sonenshine, Krby C. Stafford III, Pete D. Teel, Stephen Wikel

James Berger (DFO), Jennifer Gillissen (contractor support), Cat Thomson (contractor support)

Submission of the draft Results and Potential Actions; Timeline for finalizing the subcommittee report; Discussion of member feedback on the Results and Potential Actions section; Public comments relevant to the Tick Biology, Ecology, and Control Subcommittee; Discussion of consolidating then prioritizing Potential Actions; Next steps

10

November 18, 2019

Kevin Macaluso (co-chair), Adalberto A. Pérez de León (co-chair), Trey Cahill, Neeta Connally, Maria Diuk-Wasser, Lars Eisen, Howard Ginsberg, Lonnie Marcum, R.Michael Roe, Daniel Sonenshine, Krby C. Stafford III, Pete D. Teel, Stephen Wikel

James Berger (DFO), Jennifer Gillissen (contractor support), Cat Thomson (contractor support)

Discussion of Priorities and Potential Actions: consolidation, prioritization, and word choice; Discussion of public comments; Next steps

11

December 2, 2019

Kevin Macaluso (co-chair), Adalberto A. Pérez de León (co-chair), Trey Cahill, Neeta Connally, Maria Diuk-Wasser, Lars Eisen, Howard Ginsberg, Lonnie Marcum, R.Michael Roe, Daniel Sonenshine, Kitby Stafford III, Pete D. Teel, Stephen Wikel

James Berger (DFO), Jennifer Gillissen (contractor support), Cat Thomson (contractor support)

Discussion of PICK chart results, Priorities, and Potential Actions; Next steps

12

December 16, 2019

Kevin Macaluso (co-chair), Adalberto A. Pérez de León (co-chair), Trey Cahill, Neeta Connally, Maria Diuk-Wasser, Lars Eisen, Howard Ginsberg, Lonnie Marcum, Daniel Sonenshine, Kitby Stafford III, Pete D. Teel, Stephen Wikel

James Berger (DFO), Jennifer Gillissen (contractor support), Cat Thomson (contractor support)

Review of complete Results and Potential Actions section; Vote on Potential Actions; Next steps

Table 3: Presenters to the Tick Biology, Ecology, and Control Subcommittee

Meeting No.

Presenter

Topics Discussed

Ok to use, cite, and describe?

2

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

Overview of Work Completed by the 2018 Disease Vectors, Surveillance, and Prevention Subcommittee

Yes

2

Kirby C. Stafford III, PhD, Chief Entomologist, Department of Entomology, Center for Vector Biology and Zoonotic Diseases, NE Regional Center for Excellence in Vector Borne Diseases, The Connecticut Agricultural Experiment Station

Concepts Vector Control: Integrated Tick Management

Yes

3

Rebecca Eisen, PhD, Research Biologist, Bacterial Diseases Branch, Division of Vector-Borne Diseases, National Center for Emerging and Zoonotic Infectious Diseases, Centers for Disease Control and Prevention

Tick Surveillance as a Public Health Tool

No—contact her before using, citing, describing

4

Richard S. Ostfeld, PhD, Disease Ecologist, Cary Institute of Ecosystem Studies

The Tick Project: Testing Environmental Interventions to Prevent Lyme and Other Tick-Borne Disease in Our Communities

Yes

4

Chris Przybyszewski, Executive Vice President, Board Secretary, US Biologic

Integrated Tick Management Solutions: Reservoir-Targeted Vaccines and Predictive Analytics

Yes

5

Ed Clark, President and Founder, The Wildlife Center of Virginia; Ernesto Dominguez, DVM, Hospital Director, The Wildlife Center of Virginia; Jeff Morisette, PhD, Chief Scientist, National Invasive Species Council, U.S. Department of the Interior

Presentation—Invasive Species Advisory Council White Paper: Interface Between Invasive Species and the Increased Incidence of Tick-Borne Diseases, and Implications for Federal Land Managers

Yes

5

Jean Tsao, PhD, Fisheries and Wildlife, Large Animal Clinical Sciences, Michigan State University

The Emergence of Lyme Disease in Michigan: Past, Present, and Future?

No—contact her before using, citing, describing

Table 4: Votes Taken by the Tick Biology, Ecology, and Control Subcommittee

Meeting #

Motion

Result

Accept/Object/Abstain/Absent

Minority Response

7

Preliminary approval of the Background section with the understanding that it could be revised at a later date

Passed

11 / 0 / 0 / 3

No

12

Approval of Potential Action 1A—final wording (two votes were received after the meeting via email)

13 / 0 / 0 / 1

No

12

Approval of Potential Action 1B final wording (two votes were received after the meeting via email)

13 / 0 / 0 / 1

No

12

Approval of Potential Action 1C final wording (two votes were received after the meeting via email)

13 / 0 / 0 / 1

No

12

Approval of Potential Action 1D final wording (two votes were received after the meeting via email)

13 / 0 / 0 / 1

No

12

Approval of Potential Action 2A final wording (two votes were received after the meeting via email)

13 / 0 / 0 / 1

No

12

Approval of Potential Action 2B final wording (two votes were received after the meeting via email)

13 / 0 / 0 / 1

No

12

Approval of Potential Action 2C final wording (two votes were received after the meeting via email)

13 / 0 / 0 / 1

No

12

Approval of Potential Action 2D final wording (two votes were received after the meeting via email)

13 / 0 / 0 / 1

No

Via email on

January 10, 2020

Final report approval

14 / 0 / 0 / 0

No

Results and Potential Actions

For consideration by the Tick-Borne Disease Working Group, the Tick Biology, Ecology, and Control Subcommittee has identified two major priorities and eight potential actions to achieve them.

Priorities and Potential Actions At-a-Glance

Priority 1: Minimize the Public Health Threat of Lyme Disease and Other Tick-Borne Diseases

Potential Action 1A: Assess and enhance the effectiveness of integrated tick management strategies.

Support continued assessment of existing and new area-wide Integrated Tick Management (ITM) strategies with the ultimate goal of reducing tick-borne disease. Create best practices for using evidence-based ITM strategies that: 1) are tick species-specific; 2) can be implemented by vector biologists, ecologists, entomologists, pest management specialists, and other practitioners of area-wide ITM; 3) consider cost-effectiveness; 4) minimize non-target effects and pesticide resistance in vector ticks; 5) maximize the likelihood of public acceptance and adoption; and 6) can demonstrate reduction of human tick bites or tick-borne disease.

Potential Action 1B: Support research on ways to disrupt tick feeding, reproduction, and pathogen transmission.

Fund research addressing the knowledge gap on target pathways that disrupt tick feeding, reproduction, and transmission of pathogens causing Lyme disease and other tick-borne diseases. Using our expanding knowledge of the genes and molecules controlling tick feeding, tick reproduction, and transmission of tick-borne pathogens, it should be possible to precisely target and block these processes. For example, develop vaccines that block tick feeding before transmission of microbes can occur, especially for use in areas where tick-borne diseases are common. Further research is needed to develop and implement the use of these methods.

Potential Action 1C: Promote development of Integrated Tick Management methods and adoption by commercial applicators.

Encourage incorporation of Integrated Tick Management (ITM) methods into the current pest control model and commercial development of new effective tick control products. These actions would: 1) expedite the implementation of existing and development of promising new intervention technologies; 2) need broad funding that incorporates basic, translational, and applied research, as well as a seed support initiatives—such as Small Business Innovation Research; and 3) facilitate the commercialization or marketing of existing and new intervention products for tick and tick-borne disease control to reach the widest possible segments of the populations at risk of Lyme disease and other tick-borne diseases.

Potential Action 1D: Encourage public-private partnerships.

Supporting these critical partnerships will expedite the progress of intervention strategies, including to commercialize and market the most promising new and/or existing technologies so as to reach the widest possible segments of the populations at risk of Lyme disease and other tick-borne diseases in the United States.

Priority 2: Establish and Sustain a National Network to Support Tick Surveillance and Control by Fiscal Year 2021

Potential Action 2A: Develop and implement best practices for tick vector surveillance.

Develop and implement evidence-based best practices for national surveillance of tick vector species, their distributions, their abundance, and their associated pathogens. This surveillance will help identify and monitor existing, emerging, and new tick vector species, their environmental drivers, as well as their associated pathogens, important to medical and veterinary public health. Specific activities will:

  1. document and monitor tick species ranges, range expansions and contractions, and geographic overlaps;
  2. identify and monitor non-native tick species to minimize the risk of invasive ticks entering the U.S. and, if possible, rapidly abate or manage establishing invasive species; and
  3. assess favorable host ranges, vegetation habitats, and the impacts of changing landscapes and other environmental factors on tick populations.

Potential Action 2B: Foster coordination among Federal, state, and local agencies.

Increase coordination and support of tick vector surveillance activities and data management across Federal, state, and local agencies, as well as experiment stations, universities, and public entities and networks.

Potential Action 2C: Provide resources for local tick management programs.

Create local tick management programs that are: 1) professionally-staffed; 2) adequately resourced to operate using Integrated Pest Management principles and follow standardized guidelines; 3) responsible for surveillance of tick vectors and their associated pathogens; 4) responsible for public outreach; and 5) applicable to control of tick vectors on publicly and/or privately-owned lands, possibly in part through homeowner incentives.

Potential Action 2D: Provide education and training to all stakeholders.

Develop and promote a broad range of improved, science-based educational materials, training programs, and outreach initiatives that provide adequate background knowledge about tick vectors and tick-borne disease prevention, for stakeholders at the local, regional, and national levels. This includes vector control professionals, health care providers, students in K-12, university students, post-doctoral fellows, those at occupational risk, and members of the general public.

Priority 1: Reduce the Public Health Threat of Lyme Disease and Other Tick-Borne Diseases

Reducing the public health threat of Lyme disease and other tick-borne diseases in the United States is feasible by taking action on this priority. Research conducted for more than a century demonstrated that deaths and clinical cases caused by tick-borne diseases of livestock can be reduced by adapting technologies for area-wide Integrated Tick Management (ITM). Similarly targeting the tick-pathogen-host interface to address tick-borne diseases affecting humans:

  1. Prevents the exposure of humans to bites by infected ticks;
  2. Minimizes the proportion of infected ticks in the environment that could bite humans; and
  3. Controls the build-up of tick populations that promote the maintenance of tick-borne pathogens across the landscape.

Adequate funding will enable the infrastructure to develop, implement, and evaluate strategies that are sufficient in scope and scale in time and space and account for biological efficacy and operational efficiencies based on sound knowledge of tick and host ecology at the local level. Findings will be used to educate and train officials, stakeholders, and practitioners of best practices.

Background

To understand the reasons why this ambitious but, nevertheless feasible approach can succeed in suppressing Lyme disease and tick-borne disease, some background is needed.

Biological and ecological factors

The blacklegged tick, Ixodes scapularis, is the primary vector of Lyme disease spirochetes (Borrelia burgdorferi and Borrelia mayonii) to humans in the eastern half of the United States, while the western blacklegged tick (Ixodes pacificus) is the primary vector for Lyme disease spirochetes along the West Coast. These ticks also play key roles in natural transmission cycles to maintain Lyme disease spirochetes. However, the ability of these bacteria to colonize the tick is related to certain protein antigens on the bacterial surface, especially the outer surface protein, OspA, which enables the bacteria to lock onto a specific receptor in the tick’s digestive tract, known as TROSPA. Lyme disease spirochetes, acquired by larval ticks via feeding on an infectious host and passed through the molt to the subsequent nymphal stage, reside in the midgut of the unfed nymphs and do not escape from the midgut and migrate to the salivary glands until a nymph attaches and starts to feed. The escape from the midgut is facilitated by another tick-specific protein, enolase, while a host-derived protein, plasminogen, disguises the microbes as they transit the tick’s body and enter the salivary glands. Finally, the Lyme disease bacteria must bind to another tick protein, SALP15, to invade the gland ducts. This transmigration requires more than 24 hours from the time of attachment (Eisen, 2018). Thus, as the tiny nymphs feed on a human or non-human animal, the bacteria are transmitted in the tick’s saliva to infect people and animals, unless the offending ticks are removed by the host within this one-day grace period.

In the United States, reported cases of all tick-borne diseases have increased over the 13-year period from 2004 to 2017, from 22,527 in 2004 to 59,349 in 2017. Lyme disease accounts for most of the cases, although thousands of cases of anaplasmosis (Anaplasma phagocytophilum), ehrlichliosis (primarily Ehrlichia chaffeensis), spotted fever type rickettsial diseases (including Rocky Mountain spotted fever), and babesiosis are reported every year, together with smaller numbers of cases of tularemia and tick-borne viral illness.

The geographic distributions of the major vectors of tick-borne disease agents in the United States have been expanding greatly since detailed continental records were reported in 1945 (Bishop & Trembley, 1945). The geographic distribution of blacklegged ticks (I. scapularis) has been continually expanding, now covering almost all the eastern United States, as well as large areas in the north central U.S. The northern populations of I. scapularis are continuing to spread in all directions from two major foci in the northeast and north central United States (Eisen et al., 2017, Sonenshine, 2018).

The distribution of western blacklegged ticks (I. pacificus) appears to have remained stable over the past two decades, covering the entire Pacific Coast and with pockets of tick presence inland as far east as the western portion of Utah (Eisen et al., 2016). While the B. burgdorferi infection rates in adult ticks are generally low (1-2%), there are Lyme disease-endemic counties in California with up to 15% of nymphal ticks infected with this pathogen and up to 50 human cases per 100,000 population. The counties with the highest average incidence of Lyme disease are located in northwestern California (Steer & Malawista, 1979; Lane, 1996, Eisen et al., 2016).

In the natural environment, the blacklegged tick (I. scapularis) is vulnerable to extreme environmental conditions, especially cold weather and desiccation. In terms of temperature, I. scapularis can survive over the winter as long as soil temperatures do not exceed subzero temperatures for more than two hours. Blacklegged ticks have a compound (glycoprotein) 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). They are also vulnerable to desiccating conditions, which is why they occur mostly in woodland and brushy habitats. This is in contrast to other tick vectors currently in the U.S., such as the lone star tick (Amblyhomma americanum), the American dog tick (Dermacentor variabilis), and the Asian longhorned tick (Haemaphysalis longicornis), which use a larger range of habitat types, including grasslands.

The black-legged tick (I. scapularis) is remarkable in its ability to feed on a large variety of vertebrate hosts, including diverse reptiles, ground feeding birds and numerous mammals. However, three animal hosts stand out as the predominant blood sources and vehicles for tick spread, namely, white-tailed deer, white-footed mice and other small mammals, and migratory birds. Knowledge of these tick-host associations will help explain why targeting these key hosts can be an important part of the Lyme disease threat reduction program.

The white-tailed deer is the key host for the adult stage of the blacklegged tick and the primary amplifying host for I. scapularis populations. Deer populations are expanding rapidly and are likely to continue to increase. Reasons include:

  1. Significant decrease in predators. For example, wolves are extinct in almost all of the lower 48 U.S. states. Additionally, numbers of hunters are declining.
  2. Changes in land use.

The western blacklegged tick (I. pacificus) has a minimum life cycle of three years, going through three active blood-feeding life stages (larva, nymph, and adult) (Padgett & Lane 2001). The larvae and nymphs of I. pacificus feed primarily on lizards, rodents (including tree squirrels), and ground-dwelling birds. Nymphs in particular feed preferentially on lizards (including the western fence lizard, Sceloporus occidentalis), which are reservoir incompetent hosts for B. burgdorferi and whose blood also contains a borreliacidal factor (Lane & Quistad,1998). Consequently, the infection rate drops from the nymphal to adult stage of I. pacificus. Peak nymphal host seeking is typically observed in May and June, depending on location. The habitat where people most commonly encounter nymphs is associated with dense woodland, where the western gray squirrel has been noted as the primary reservoir host for Lyme disease spirochetes (Lane et al, 2004).

Risk for Lyme disease increases across an urban to forest gradient (Kilpatrick et al., 2017). While it has been proposed that increased host diversity may reduce risk in less fragmented forested areas (Allan, Keesing, & Ostfeld, 2003; Brownstein, Skelly, Holford, & Fish, 2005; McClure & Diuk-Wasser, 2018), a recent study shows that there is greater richness of reservoir host species, significantly higher encounters with hosts, and significantly lower B. burgdorferi host infection in residential areas as compared to large, intact forested stands, at least in Connecticut (Linske et al., 2018). Another important factor is the creation of contiguous “green” areas where wildlife can flourish in urban areas, an admirable goal for urban dwellers but which also enhances the risk of tick-borne disease, especially Lyme disease. In New York City, numerous forested parks and green areas with vegetated buffers that are interconnected provide opportunities for wildlife to transit between them. In a study by VanAcker et al. (2018), localities with increased connectivity had higher blacklegged tick nymph densities and higher risk of tick bites on people. The authors found that the degree of park connectivity strongly determined B. burgdorferi nymphal infection prevalence and concomitant tick-borne disease, especially Lyme disease risk.

A highly fragmented landscape may support higher densities of deer, which benefit from the increased edge habitat due to the presence of preferred forage (Brownstein et al., 2005; Leopold & Brooks, 1933). In the Northeast, a combination of high deer densities (24 to 48 per square kilometer) and fragmentation of forest habitat may mean that questing adult ticks are more likely to find a host, as deer are likely to concentrate there. Halsey et al. (2018) found much higher densities of ticks feeding on all hosts in the Northeast region as compared to Southeast and Midwest regions.

Although white-tailed deer are the major amplifying hosts for the tick populations carrying Lyme disease spirochetes, migratory birds are one of the major factors contributing to the geographic expansion of the tick’s range. Migratory birds transport vast numbers of immature blacklegged ticks (I. scapularis). Migrating birds flying north along the Atlantic and mid-central U.S. flyways pick up ticks when they stop periodically to rest and forage before continuing northward. In Lyme, Connecticut, Stafford et al. (1995) examined 36 different bird species for the presence of ticks. Of the 4,065 tick larvae and nymphs found on the birds, 94.4% were I. scapularis. The rate of infection with B. burgdorferi in the immature I. scapularis found infesting the birds in this focus of Lyme disease ranged from 14.9% to 20.0%. States et al. (2014) estimated that approximately one-third of all bloodmeals by larval I. scapularis on Block Island, Rhode Island, were derived from bird hosts. Brinkerhoff et al. (2009) found that the majority (58.6%) of bird species that have been evaluated are capable of infecting larval blacklegged ticks with B. burgdorferi. In Canada, I. scapularis populations have spread into large areas of southern Quebec, Ontario and the maritime provinces. In Ontario, I. scapularis-infested localities are estimated to have expanded at the rate of 46 km/year (Clow et al., 2017).

Prevention of tick-borne disease and control of ticks

The incidence and geographic 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 estimated to occur each year. In the absence of a human vaccine in the U.S. against any of the tick-borne diseases or biting ticks, effective primary prevention relies on reducing exposure to ticks. Blacklegged ticks, Western blacklegged ticks, lone star ticks, American dog ticks, Rocky Mountain wood ticks, Pacific Coast ticks, Gulf Coast ticks, brown dog ticks, and soft bodied ticks all play important roles as vectors of a variety of human, livestock, or companion animal disease-causing agents, with several tick species capable of carrying and transmitting multiple pathogens to humans. The introduction of exotic, invasive ticks with potential new disease agents can pose additional risks to humans and livestock.

Identifying and validating effective tick control and tick bite prevention strategies is critical for reducing the incidence of new disease cases, preventing the introduction of new tick species, and limiting the spread of our native ticks. Additionally, in order to track the effectiveness of national prevention and control strategies, as they emerge, it is essential to maintain an accurate understanding of current and potential disease burdens and trends against which to measure success of national prevention goals once established.

Major challenges

Risk for exposure to ticks and tick-borne diseases may be primarily residential, recreational, work-related, or a combination thereof with unique challenges. No vaccines are currently available in the U.S. against any tick-borne disease, although a new OspA vaccine for Lyme disease is in Phase 2 trials in Europe and the U.S. Therefore, primary prevention currently relies on methods focused on reducing exposure of people to infected ticks by reducing tick abundance or the prevalence of infection in the tick in the environment combined with use of personal protection measures when spending time in tick habitat.

Consequently, the responsibility for tick bite prevention and tick control presently falls squarely on the shoulders of individuals, as organizational structure for local tick control (similar to a mosquito management program operating along well established integrated pest management guidelines) is either lacking or poorly developed and underfunded across the U.S. The toolbox of available methods and products available to protect against biting ticks contain such things as personal repellents, acaricides approved for use on clothing and gear, animals, and properties, landscape management, and personal protective behaviors, with increased attention on integrated strategies (Stafford, Williams, & Molaei, 2017). However, not all control measures may be applicable to particular tick species with different geographic distributions, hosts, ecologies, exposure risk for humans and their animals, and associated pathogens. Moreover, the available data showing that any of the available tools when deployed as directed can actually prevent human illness is very limited (Connally et al., 2009; Eisen & Gray, 2016; Garnett et al., 2011; Kilpatrick et al., 2014).

Therefore, effective control of ticks and their associated disease agents requires broader acceptance and use of current technologies, improved approaches and additional resources to scale up many of these methods, and the development of an organizational structure for addressing the tick problem at a community-level or broader scale. New methods and products, including those with a One-Health approach, in addition to controlled field trials that measure human outcomes (tick encounters and/or tick-borne disease incidence), are also badly needed. Lastly, 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, underscoring the need for improving science-based tick-borne disease prevention communication.

Summary of Evidence and Findings

A review of the scientific literature and expert presentations by the 2018 Disease Vectors, Surveillance, and Prevention Subcommittee of the Tick-Borne Disease Working Group identified the following crucial needs related to control:

  1. Reducing human exposure to vector ticks;
  2. Identifying novel methods for controlling ticks and their associated pathogens, for example, methods aimed at blocking transmission of tick-borne pathogens to humans and animals; and
  3. Adequately validating that tick-control and pathogen-transmission blocking methods can effectively reduce the incidence of tick-borne illnesses using prospective studies that measure both acarologic and human outcomes.

These objectives remain crucial. The 2018 Subcommittee’s review covered the major tick species and methods of preventing tick-encounters or reducing the risk of human tick-borne illness. It is not the purpose of this subcommittee to rehash the catalogue of methods and techniques, but expand upon it to: 1) further pinpoint the challenges and barriers to implementation to decrease the risk of tick-borne pathogen transmission; and 2) determine how tick management can be targeted to address specific tick vectors and populations at risk. Nevertheless, many of the findings in the earlier report remain relevant and are reaffirmed in this report. The tools reviewed previously that provide the framework for control efforts are listed below and these are examined from the perspective of the biology, ecology, and needs for specific tick species.

  • Personal protective measures (skin repellents, permethrin-treated clothing, tick checks and bathing or showering). Various personal protective measures could apply to all tick species
  • Residential prevention measures (synthetic acaricides, botanically-based acaricides, biological control of ticks, rodent-targeted approaches for tick control, rodent-targeted transmission blocking vaccines, deer fencing, and landscape modifications)
  • Community-level prevention (deer removal, USDA 4-poster devices, education programs).
  • Novel tick control measures (TickBot, genetic approaches, anti-tick vaccines, other novel emerging technologies)
  • Integrated Tick Management for residential or community-level prevention

Many of the barriers to the adoption or use of tick control and tick bite prevention efforts were previously identified despite overwhelming scientific data that support their safety or effectiveness. These barriers still exist.

  • 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
  • Lack of municipal/local vector-control efforts specifically aimed at ticks

Progress in public health has largely been due to improved nutrition, hygiene and sanitation, as well as use of vaccines and antibiotics (Centers for Disease Control and Prevention, 1999). Effective vaccines are available for tick-borne encephalitis (TBE) in Europe and Russia, but recent increase in TBE cases in Europe illustrates the difficulty in maintaining vaccination rates, something seen recently in the measles outbreak in the United States with a decline in vaccination rates in some communities (Patel et al., 2019). An application of an early Lyme disease model of various intervention measures in a hypothetical community found the use of a vaccine and the application of acaricides to deer produced the greatest reduction in human cases of Lyme disease under best case scenarios (Hayes, Maupin, Mount, & Piesman, 1999). The first human Lyme disease vaccine was pulled off the market in 2002 over concerns about adverse reactions and low public acceptance (Schuijt, Hovius, van der Poll, van Dam, & Fikrig, 2011). There are several canine Lyme disease vaccines available, but as noted earlier, no human vaccines are currently available in the U.S. for Lyme disease or any other tick-borne disease.

Not coincidentally, the only documentation of an impact on actual cases of Lyme disease, with some caveats (Kugeler, Jordan, Schulze, Griffith, & Mead. 2015) has been for community-level reduction of white-tailed deer (Kilpatrick, LaBonte, & Stafford, 2014) or acaricidal treatment of deer (Garnett, Connally, Stafford, & Cartter, 2011), the key for these being community-level host-targeted interventions. The complete elimination of deer, practical only on geographically isolated islands or similar isolated tracts with community support, has been shown to virtually eliminate the blacklegged tick population (Rand, Lubelczyk, Holman, LaCombe, & Smith, 2004). The larger geographic scale of some host-targeted and integrated tick management methods may be analogous to large scale sanitation efforts in the early twentieth century and may be necessary to impact human vector-borne diseases. Nevertheless, with three-quarters of Lyme disease cases probably acquired peridomestically, tick management will likely require a combination of individual property and large-area approaches.

Only recently have tick-control efforts focused on application of multiple methods for controlling ticks in an Integrated Tick Management (ITM) approach, particularly for blacklegged ticks (I. scapularis), which have mainly been conducted at residential properties (Schulze et al., 2007; Stafford, Williams, & Molaei, 2017). Some earlier work on ITM looked at combinations of spraying, vegetation management, and deer management (fencing) for the control of the lone star tick, Amblyomma americanum, in a recreational setting (Bloemer, Mount, Morris, Zimmerman, Barnard, & Snoddy, 1990). Classic Integrated Pest Management (IPM) involves the selection, integration, and implementation of several pest control actions based on predicted ecological, economic, and sociological consequences. According to the National IPM Roadmap, the purpose of IPM is to:

  • Prevent unacceptable levels of pest damage;
  • Minimize the risk to people, property, infrastructure, natural resources, and the environment; and
  • Reduce the evolution of pest resistance to pesticides and other pest management practices.

For tick-borne diseases, any part of the epidemiological triad of host, vector, and pathogen and their interactions within the local environment can be the target of control interventions. Tick control or management may have several different objectives: 1) lower direct damage to animals; 2) prevent transmission of tick-borne pathogens to animals; 3) lower nuisance to humans from ticks, and 4) prevent tick-borne disease in humans.

There is a difference between control and management, which implies an acceptable level of pest abundance and acceptable level of damage or loss. (For ticks, this is either economic gains for livestock or the risk or incidence of disease.) The objective of IPM is reduction of the pest level—or pathogen prevalence—below the economic injury level, the density at which the losses (or cost of Lyme disease) exceed the cost of control (cost-benefit or cost-efficacy analysis) (Ginsberg & Stafford, 2005). For ticks on livestock or in a recreational area, the purpose of control is to protect a commodity, (for example, cattle) or potential use of a recreational area (such as use by tourists), which is easier to define in terms of a cost/benefit analysis. By contrast, for human disease, the level of risk of a tick encounter that is tolerated may be different for recreational areas and residential areas. For some homeowners, acceptable level of risk may be extremely low or cost considerations too high and is more of a “bang for the buck” cost/efficiency paradigm (Ginsberg & Stafford, 2005). The costs for tick management interventions can be a restricting factor in acceptance and adoption of various control methods (Gould et al., 2008) and usage of tick prevention or control measures is low (Hook et al., 2015).

ITM approaches can include targeting of 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; can be applied at different spatial scales (individual yards vs. neighborhoods and communities); and may also result in a slower development of pesticide-resistant ticks. The big issues in reducing tick encounters and the incidence of human disease are effectiveness, scale, cost, and implementation. More specifically, some of the questions that this committee feels need to be considered in addressing development and implementation of Integrated Tick Management or best management practices include:

  • What is the range of tick species/pathogens impacted by a given intervention, going from extremely narrow (for example, vaccination of mice or humans against B. burgdorferi) to very broad (for example, repellents or broadcast application of acaricides)?
  • What spatial scale is impacted by the intervention, going from very limited (for example, barrier spraying of acaricides along forested ecotones) to broad (for example, using deer-targeted methods) and scale-free (for example, applying repellent)?
  • Who is responsible for tick control on private properties versus community/public lands, including neighborhood greenbelts, school grounds, and city, county and state parks?
  • How can we deal with low acceptability of many current tick control methods and limited willingness to pay?
  • How should we support implementation and evaluation of current control methods versus development of potential novel technologies that require longer term research?
  • How can we get industry to invest in developing new products for an unclear public health tick control market?
  • How effective are broadcast acaricides when applied by homeowners or Pest Control Professionals?
  • How can adequate funding be secured for additional, larger scale evaluations of ITM approaches with human outcomes?
  • And when we finally have defined an area-wide ITM approach proven to reduce human tick bites and human tickborne illness, can it even be implemented unless we also develop local tick management programs with professional staff?

Repellents can be used for general protection by individuals against tick bites by all tick species. While most have been tested against American dog ticks, lone star ticks, and blacklegged ticks, data is limited or lacking on efficacy for some other tick species. Because using repellents and other personal protective measures rely on individuals to take action every time they encounter outdoor environments, such strategies may not reliably impact tick-borne disease incidence in a population. On the other hand, large-scale, long-term suppression of tick populations are likely to be more impactful for addressing the problem of tick-borne disease on a regional or national scale.

Considering integrated tactics and strategies that are applicable to the life-cycle and ecology of each tick species, we summarize the status of tick management for each of the tick species of major concern in the United States.

Control approaches and challenges for the major tick disease vectors in the United States

Blacklegged and western blacklegged tick (I. scapularis and I. pacificus). These two species are the primary vectors of the Lyme disease spirochetes B. burgdorferi (I. scapularis in the east and I. pacificus in the far west) and B. mayonii (I. scapularis in the Upper Midwest) as well as the tick-borne relapsing fever spirochete B. miyamotoi (I. scapularis and I. pacificus) and agents causing anaplasmosis (I. scapularis and I. pacificus), babesiosis (I. scapularis), ehrlichiosis (E. muris eauclairensis) (I. scapularis), and Powassan virus encephalitis (I. scapularis) (Eisen et al., 2017). Host-targeted methods with deer have been highly successful in reducing tick abundance and even some documented reduction in Lyme disease cases as previously noted. A few studies have applied integrated methods for reducing tick populations and even a reduction of tick infection prevalence (Schulze et al., 2007; Stafford, Williams, & Molaei, 2017). There are currently three studies ascertaining the use of ITM against blacklegged ticks at single versus clustered residential properties (www.backyardtickstudy.org), in neighborhoods (www.tickproject.org), and in communities (ARS Area-Wide Integrated Tick Management Study), with two of these three studies attempting to ascertain whether an ITM approach can ultimately result in a reduction of human-tick encounters and in human disease incidence.

Because human exposure to ticks is predominately peridomestic (residential) with blacklegged ticks (I. scapularis), and most Lyme disease cases are associated with this species, many of the current and newly emerging tools for tick control have been developed and evaluated for control of I. scapularis (Eisen & Dolan, 2016), targeting the questing tick reservoir hosts for B. burgdorferi (mice and chipmunks), or reproductive hosts (deer). Rodent host-targeted methods for topical acaricide application like the tick tube and fipronil-based bait box, each with their strengths and weaknesses, primarily target white-footed mice, the reservoir host for B. burgdorferiB. mayoniiB. microtiA. phagocytophilum, and B. miyamotoi. These products can be important tools in an ITM approach, but probably not as a sole tick control method. A recent comparison of the two methods found that, 1 and 2 years post-intervention, tick tubes provided 28% and 20% control of questing I. scapularis nymphs (chipmunks do not use the tick tubes), while the bait boxes resulted in 84% and 79% control, respectively (Jordan & Schulze 2019).

A rodent-targeted oral bait Lyme disease vaccine (RTV) under development by U.S. Biologic Inc. also targets the reservoir hosts and has been shown to reduce the prevalence of B. burgdorferi infection in white-footed mice (Richer, Brisson, Melo, Ostfeld, Zeidner, & Gomes-Solecki, 2014). Several studies evaluating topical application of tick-killing pesticides on white-tailed deer using U.S. Department of Agriculture 4-poster deer treatment stations resulted in significant reductions in host-seeking blacklegged ticks and lone star 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 label restrictions on deployment near residences with children due to safety concerns.

Early surveys showed that residential tick control for blacklegged ticks (I. scapularis) was largely limited to applications of synthetic acaricides by professional applicators (Schulze et al. 1997; Stafford, 1997). Area application of synthetic acaricides continues to be the primary and most efficacious method of tick control for homeowners (Eisen & Dolan 2016; Jordan & Schulze, 2019), with increasing interest in botanically-based, all “natural” products for controlling ticks due to environmental concerns. While synthetic pyrethroids offer the longest-lasting, most effective backyard control of blacklegged ticks, it is important to note that misuse or poor application can result in poor tick control, 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). This highlights the need for public-private partnerships that would enable continued research, development, and commercialization of safe and effective tick control products (Jordan & Schulze, 2019).

Natural products, largely based on the U.S. Environmental Protection Agency (EPA) 25b minimum risk list, are appealing to the public because of perceived low toxicity to humans, pets, and the environment and appealing to commercial developers because they do not require registration with the EPA or proof of efficacy to add to the pesticide label. Lack of efficacy can potentially lead to false sense of protection and greater risk of tick bite and disease. As a result, marketed products may come and go, making timely evaluations of efficacy a challenge for academic researchers. Issues with botanically-based acaricides include:

  • No or limited efficacy data, exempted from testing for toxicity, some may be toxic at higher doses, irritants, or allergens
  • Differences in tick species and stage susceptibility
  • Variable and “unknown” composition of essential oils depending on factors such as source, plant species, and extraction method
  • Efficacy of oil vs. specific components of the plant extract or oil (for example, nootkatone, carvacrol)
  • Volatility and lack of persistence, requiring frequent applications
  • Phytotoxicity

Nootkatone from Alaskan yellow cedar and grapefruit essential oil has been found effective as a killing agent for blacklegged ticks (I. scapularis) in the field (Bharadwaj, Stafford, & Behle, 2012; Eisen and Dolan, 2016) and for multiple tick species in the laboratory (Flor-Weiler, Behle, & Stafford, 2011). It has also 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. Nootkatone is being developed under the name NootkaShield™ by Evolva under license from the CDC; the registration of nootkatone as a biopesticide is under review by the EPA.

How botanically-based products are formulated may impact efficacy. In a study of a botanical acaricide and its active ingredients against larvae of the cattle tick, Rhipicephalus (Boophilusmicroplus, only geraniol exhibited acaricidal properties in a product containing rosemary oil, geraniol, peppermint oil, wintergreen oil, white mineral oil, vanillin, and polyglyceryl oleate (Singh et al., 2018). Rosemary oil and peppermint oil failed a dose-mortality response and the high response to the commercial product was attributed to synergism among the principal ingredients and other components present in the product. More work is needed on formulation chemistry and efficacy of botanical-based acaricides.

Fungal biopesticides also provide a promising alternative to synthetic acaricides. Field studies evaluating tick-killing Metarhizium anisopliae (Mbrunneum) fungi (Met52) 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 when applied appropriately (Ginsberg, Bargar, Hladik, & Lubelczyk, 2017). It has been and is currently the primary broadcast agent being used in several of the integrated tick management (ITM) studies mentioned earlier. A combination of the Met52 and fipronil rodent bait boxes reduced the risk of encountering questing nymphal ticks by 78-95% and single infected blacklegged ticks by 66% (Williams et al., 2018). However, the efficacy of this combination approach against other rodent-associated tick species has not been evaluated.

Current tools and challenges for control of blacklegged ticks

  • The widest diversity and most current tools for tick control have been developed for the blacklegged tick (I. scapularis).
  • Although integrated tick management has shown to reduce co-infection of the blacklegged tick with Bburgdorferi and other tick-borne pathogens (Little, Williams, Stafford 3rd, Linske, & Molaei, 2019), the impact of substantial reductions in the abundance of host-seeking ticks on human tick bites or human disease remains to be documented.
  • There is a lack of target thresholds for tick suppression at the local (private), municipal, and state levels.
  • Similarly, analogous to vaccination thresholds needed for “herd” protection in agriculture (Pérez de León et al., 2018), it is unknown at what level residential (for example, percent household participation) and community implementation of tick management interventions is needed to reduce human tick bites or human disease.

Lone star tick (A. americanum). This species is the primary vector of multiple pathogens causing ehrlichiosis (E. chaffeensisEhrlichia ewingii, and Panola Mountain Ehrlichia) and has also 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). The lone star tick also was implicated as the vector of Borrelia lonestari, the putative agent of southern tick associated rash illness (STARI); and was linked to a delayed allergic reaction to a number of different allergens, 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 (RMSF), tularemia, and Q fever (Childs & Paddock, 2003; Jasinskas, Zhong, & Barbour, 2007), and their bite may induce tick paralysis. Except for the RMSF agent (Levin, Zemtsova, Killmaster, Snellgrove, & Schumacher, 2017), the vector competence of lone star ticks for these disease agents remains unproven (Childs & Paddock, 2003; Stromdahl & Hickling, 2012). With increasing abundance in its “native” range in the southeastern United States and geographic expansion northward, control of this aggressive tick has become increasingly important.

Most studies on control of the lone star tick were conducted in the 1970s through 1980s, many evaluating organophosphate acaricides that are no longer used for area-wide tick control, host management and/or vegetation management. With the focus on blacklegged ticks (I. scapularis) and Lyme disease, there have been relatively few studies on the management of this tick in recent years, at least in comparison to blacklegged ticks.

Vegetation reduction has been shown to reduce the abundance of lone star ticks (Aamericanum) (reviewed by White & Gaff 2018). The combination of vegetative management, host management (deer exclusion), and application of the organophosphate chlorpyrifos in an integrated study reduced lone star ticks by up to 96% (Bloemer et al., 1990). Deer exclusion also impacted lone star ticks on Long Island (Ginsberg, Butler & Zhioua, 2002). With white-tailed deer a principal host for all stages of the tick (Paddock & Yabsley, 2007), the ARS-USDA 4-poster has been found to significantly reduce the abundance of lone star ticks (Brei et al., 2009; Carroll et al., 2003; Pound, Miller, George, & Lemeilleur, 2000; Schulze, Jordan, Hung, & Schulze, 2009). With appropriate dosing, ivermectin-treated corn has also been shown to control lone star ticks (Pound, Miller, George, Oehler, Harmel, 1996) as well as blacklegged ticks on white-tailed deer (Rand, Lacombe, Holman, Lubelczyk, & Smith, 2000). Ironically, ivermectin is an FDA-approved treatment for several human parasites and has been used to treat millions of people for onchoceriasis (González et al. 2008; Ōmura 2008), but current withdrawal requirements limit or prevent its use for the control of ticks on deer. Doramectin is used on cattle for control of cattle fever ticks, but also has withdrawal restrictions. By contrast, rodent-targeted techniques, such as the tick tubes and bait boxes, for blacklegged tick hosts would not affect lone star ticks since they do not readily use rodent hosts (Zimmerman et al., 1987).

Some research has been done more recently with current synthetic acaricides and botanically-based acaricides against lone star ticks (Schulze, Jordan, Hung, Taylor, Markowski & Chomsky 2001; Dolan et al., 2009; Jordan, Dolan, Schulze & Piesman, 2011; Jordan, Schulze, Eisen & Dolan, 2017). While primary exposure to lone star ticks by humans has probably been primarily recreational in the past, it is increasingly becoming a residential issue as well, as the tick expands its range into more densely populated areas along the northern Atlantic seaboard (Stafford, Molaei, Little, Paddock, Karpathy, Labonte, 2018; Molaei, Little, Williams, & Stafford, 2019). This tick is the dominant species submitted to the Army Public Health Center from southern installations for identification and testing from enlisted personnel, civilian employees and their families (Nadolny, 2017).

Current Tools and Challenges for Control of Lone Star Ticks

  • Regulatory restrictions on use of ivermectin for control of ticks on livestock and deer
  • Limited studies on the efficacy of current acaricides and biopesticides for control of Aamericanum
  • Lack of Integrated Tick Management (ITM) approaches for lone star ticks in residential settings

American dog tick (Dermacentor variabilis). This species is the primary vector of the bacterium that causes Rocky Mountain spotted fever (Rickettsia rickettsii), and is also known to transmit the agent of tularemia (Francisella tularensis). However, infection rates with R. rickettsii in D. variabilis have been extremely low. The American dog tick has a broad distribution, spanning the entire U.S., though this tick has a disjunct western distribution along the Pacific Coast of the U.S. and an extensive eastern distribution that extends from Canada to the Gulf of Mexico, west into Kansas and Nebraska and into Colorado (Lehane, Parise, Evans, Beati, Nicholson, & Eisen, 2019). As noted in the 2018 Disease Vectors, Surveillance, and Prevention Subcommittee Report, there have been few recent studies evaluating existing control methods. There are even fewer evaluations of control methods against D. variabilis than A. americanum (White & Gaff, 2018) and what few exist also date from the 1980s using organophosphates (White, Benach, Smith, & Ouyang, 1981). Sonenshine and Haines (1985) found that a bait box treating rodents with an insecticidal dust or oil reduced nymphal and larval American dog ticks on the rodent hosts. However, there has been little focus on evaluating the impact of newer tick tubes or bait boxes on D. variabilis. Early modeling of management strategies examined area-wide acaricide applications, acaricide baited tubes, reduction of small mammal hosts, dipping of dogs, use of canine collars, and removal of vegetation (Haile, Mount, & Cooksey, 1990), with multiple acaricide applications or a combination of baited tubes, host management and vegetative management reducing tick abundance below targeted thresholds, supporting an ITM approach.

Current Tools and Challenges for Control of American Dog Tick

  • Limited data on the incidence of tick bite encounters with American dog ticks (D. variabilis) and current importance in the transmission of human disease agents
  • Lack of studies on the efficacy of current acaricides for control of D. variabilis
  • No development for, or evaluation of, emerging tick control technologies for D. variabilis

Gulf Coast tick (Amblyomma maculatum). Historically, this tick was limited to coastal areas of the southeastern U.S., and Central and South America; however, it now also occurs in states along the Atlantic coast as far north as Virginia and Delaware (Nadolny & Gaff, 2018), as well as in the south-central U.S. as far north as Oklahoma and Kansas (Teel, Ketchum, Mock, Wright, & Strey, 2010; Paddock & Goddard, 2015). It was considered primarily a livestock pest causing weight and blood loss in cattle and a condition called gotch ear in cattle and other animals. The tick is the principal vector for hepatozonoosis, a severe and potentially fatal disease in dogs. The Gulf Coast tick can acquire and transmit Ehrlichia ruminantium, the causal agent for heartwater in wild and domestic ruminants. Paddock and Goddard (2015) emphasized the importance of A. maculatum as a potential vector for this disease if the pathogen is introduced through the “importation of exotic animals from Africa or by tick-infested migratory birds from islands in the Caribbean.”

This aggressive tick is also the major vector of a mild, spotted-fever-like illness caused by Rickettsia parkeri in humans and can cause tick paralysis (Paddock & Goddard, 2015). Similar to some Dermacentor spp. ticks, it is the adult Gulf Coast ticks that parasitize humans and transmit the agents of human disease (and may often be confused with Dermacentor ticks). This tick is associated with grass-dominated and successional habitats, not forest; and a better understanding of these open habitats, their relation to urban and suburban developments and human exposure risks is needed (Nadolny & Gaff, 2018). Compared to other tick species, there is relatively little information on the control of the Gulf Coast tick.

Current Tools and Challenges for Control of the Gulf Coast Tick

  • Research is needed to better understand the urban and suburban ecology of this tick, human exposure risks, and transmission of R. parkeri.
  • Evaluation of appropriate current tick management tools for A. maculatum to control human exposure to this tick is needed.
  • Efforts to monitor for the potential introduction of E. ruminantium need to be maintained and enhanced.

Rocky Mountain wood tick (Dermacentor andersoni) and Pacific Coast tick (Dermacentor occidentalis). The distributions of these two ticks appear to have remained stable over time. The Rocky Mountain 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; James et al., 2015). The Rocky Mountain wood tick is the primary vector of the Colorado tick fever virus (Emmons, 1988); as well as the agents of Rocky Mountain spotted fever, R. rickettsii; and tularemia, F. tularensis (Burgdorfer, 1969). It also is the cause of tick paralysis. The Pacific Coast tick is found throughout western California and Oregon. It transmits a spotted fever group rickettsia (Rickettsia philipii or Rickettsia 364D) to humans, causing Pacific Coast tick fever. Similar to D. variabilis, there have been few recent studies evaluating existing control methods and limited data on the incidence of tick bite encounters with these ticks and current importance in the transmission of human disease agents.

Brown dog tick (Rhipicephalus sanguineus). The brown dog tick has a worldwide distribution, although recent studies suggest that this species sensu lato likely comprises a complex of species (Dantas-Torres et al., 2013). Dogs are the primary host for R. sanguineus and the tick can transmit Rocky Mountain spotted fever (R. rickettsii) to both dogs and humans. Found indoors (for example, in dog kennels) in northern latitudes, populations can survive and breed successfully in nature and in human dwellings across the entire southern U.S., but mainly in areas where canine hosts are readily available. The adult stage is the main vector to humans. Climate warming could increasingly affect the role of the brown dog tick in human disease as R. sanguineus ticks exposed to high temperatures were found to attach more readily to humans (Parola, et al., 2008). On Native American reservations in Arizona, a population of this species has transmitted Rocky Mountain spotted fever group rickettsia to humans and was managed through a successful One-Health Integrated Tick Management community approach using long-acting tick collars (with flumethrin and imidacloprid), peridomestic acaricide spraying, and spay and neuter programs (Drexler et al., 2014). Given that dogs are the primary host, most research has focused on control of R. sanguineus (and other tick species) on dogs with the development of pet ectoparasite control products (flea and tick collars, topical sprays, spot-on’s, and newer oral parasiticides). Applications of these products along with treating areas where dogs are present are the main methods of control to reduce the risk for human exposure (Biggs et al., 2016). However, permethrin resistance and fipronil tolerance has been reported in the brown dog tick (Eiden, Kaufman, Oi, Allan, & Miller, 2015).

Current Challenge for Control of the Brown Dog Tick

  • Translating the now proven One-Health Integrated Tick Management approach into a sustainable tick management program

Soft ticks (Ornithodoros species). There are several species of ticks in the genus Ornithodoros associated with tick-borne relapsing fever (TBRF) in the western United States, primarily O. hermsiO. turicataO. parkeri, and O. talaje. Each is associated with its own relapsing fever spirochete: Borrelia hermsiiB. turicataeB. parkerii, and B. mazzotti, respectively. Humans mainly encounter these ticks in rodent- and tick-infested rustic cabins while sleeping (Johnson, Fischer, Raffel, & Schwan, 2016) or caves. Ornithodoros hermsi is the primary vector of one of the two principal North American agents of tick-borne relapsing fever (TBRF, that is, B. hermsii in humans) (Lopez, Krishnavahjala, Garcia, & Bermudez, 2016), which circulates sylvatically in rodents. Control efforts through rodent management and application of interior acaricides usually occurs following the occasional outbreaks at vacation cabins, although some tick control may be conducted preemptively. The distribution of Ornithodoros species is not well known. For example, Donaldson et al. (2016) used combined current and historical collection data in maximum entropy species distribution modeling to predict the potential U.S. range of this species.

Asian longhorned tick (Haemaphysalis longicornis). The Asian longhorned tick is native to temperate regions of eastern Asia, where it has been implicated as a vector of Japanese spotted fever and severe fever with thrombocytopenia syndrome (SFTS) in humans. In its native habitat, as well as in Australia and New Zealand where it is invasive, the Asian longhorned tick is also an important pest of livestock. Heavy infestations of cattle, sheep, goats, horses, and other agricultural animals can cause a high degree of morbidity and mortality, including decreased milk production in dairy cows. In addition, the Asian longhorned tick’s capacity to transmit a variety of veterinary disease agents, including bovine Babesia, AnaplasmaTheileria species, and equine Babesia species (Heath, 2002), make the tick an important species of economic concern worldwide. Recently discovered in the United States on a New Jersey sheep farm in 2017, the Asian longhorned tick has since been detected in nine U.S. states, both in the environment and parasitizing a variety of hosts, including livestock and companion animals, humans, white-tailed deer, and several other mammal and avian species (Beard et al., 2018). The capacity for this exotic tick to transmit new or existing local pathogens to humans and livestock in the U.S. is not yet well-understood, and needs more study. However, it has been found not to be a vector for B. burgdorferi sensu stricto in the laboratory (Breuner, et al., 2020).

Worldwide, control recommendations for the Asian longhorned tick include pasture mowing and vegetation management (Heath, 2016), treatment of infested livestock with ectoparasiticides, such as isoxazolines and macrocyclic lactones, and environmental application of acaricides, including organophosphates and synthetic pyrethroids (U.S. Department of Agriculture, 2019). It should be noted that the efficacy of ectoparasiticides and acaricides available in the United States have not yet been evaluated for North American populations of Asian longhorned ticks.

Current Tools and Challenges for Control of the Asian Longhorned Tick

  • Research is needed to better understand the general ecology of H. longicornis in North America, including seasonal activity, and host preferences of the different life stages, factors influencing dispersal, human and livestock exposure risks, and transmission of medical, veterinary, and wildlife pathogens.
  • Evaluation of current tick management tools for H. longicornis to control human and veterinary exposure to this tick is needed, using a One-Health Integrated Tick Management approach.
  • Efforts to monitor the distribution and spread of invasive H. longicornis need to be maintained and enhanced.

Possible Opportunities

Substantial reduction of Lyme disease will require a combination of modern genetic tools, modern vaccines, and by intervening into the most vulnerable elements of tick-host-pathogen processes to minimize abundance of the tick vectors, the blacklegged tick (I. scapularis), and the western blacklegged tick (I. pacificus), as well as block survival and multiplication of the pathogen (B. burgdorferi). When implemented together, these interventions will effectively minimize transmission of Lyme disease spirochetes to humans and companion animals below the level of a public health threat.

Employing Integrated Tick Management (ITM) to exploiting ecological weaknesses

Tick suppression or removal of ticks from the equation supporting tick-borne pathogens (ticks + hosts + pathogens + habitat + weather/climate = disease risk) suppresses or eliminates the risk of tick-borne diseases. Tactics that target multiple interactions in this system can be integrated into sound environmental management strategies applied over sufficiently large areas to inhibit tick population growth and dispersal, a concept known as Area-wide Integrated Tick Management. This is best accomplished using practices that reflect local and regional factors that influence tick populations and pathogen transmission patterns.

Ecological studies can help identify those factors that are critical for the maintenance of the tick or the pathogen, thus help target interventions to the ‘achilles heel’, or weakest link, in the system. Differences in the importance of various tick-borne diseases in different locales in the United States result from differences in tick species distributions, ecological community types, landscape practices, and structure of the built environment. For example, Lyme disease distribution is affected by geographical patterns of tick distribution (Eisen et al., 2016; Pepin et al., 2012), tick host-seeking behavior (Arsnoe et al., 2019), climate and tick seasonality (Gatewood et al., 2009; Ginsberg et al., 2017; Ogden et al., 2018), and landscape patterns such as habitat type, fragmentation, connectivity, and the built environment (Guerra et al., 2002; Allan et al., 2003; Linske et al., 2018; VanAcker et al., 2019).

Research to develop new control technologies and testing in appropriate locales are needed to provide tools for improved management (Eisen et al. 2012, Kilpatrick et al. 2017, Ginsberg & Couret 2019). Tick control would be most effective when interventions are effectively targeted, integrated and implemented on a broad enough scale in time and space to lower disease incidence.

Local and regional vector management programs offer the potential for sustainable programs that would include long-term surveillance of locally-important vectors and pathogens (Priority 2), allowing well-targeted and optimally-effective management interventions. Local and regional planning and design of tick control programs allows input by local stakeholders (including government agencies and people with interests in public health, environmental conservation, and community planning) to contribute to the design of vector and pathogen management programs. This approach can create public acceptance of appropriate interventions, as well as long-term attention to vector management in local planning and decision-making.

Application of Integrated Tick Management has been demonstrated against both 3-host and 1-host tick species (I. scapularis, A. americanum and Rhipcephalus annulatus and R. microplus) within agricultural, recreational and urban settings (Bloemer et al., 1990; Mount et al., 1999; Pound et al., 2009; Perez de Leon et al., 2012; Stafford et al., 2017). Howeverlong term studies of sufficient spatial scale (area-wide), particularly for 3-host species are needed to assess biological and epidemiological impacts, operational efficiencies and economic benefits, to establish best practices and guides for effective community-wide and governmental engagement (Perez de Leon et al., 2014; Stafford et al., 2017). Computer modeling has become a tool for a priori assessment of ecosystem changes impacting tick populations and for applications of tactics and strategies of tick suppression. These programs rely upon fundamentals of tick ecology for each stage of tick development, the variation of ecological elements impacting the system, and upon weather and climate drivers of tick development (Mount & Haile 1987; Wang et al., 2012; Wang et al., 2017). These tools may also be applied to operational planning and biological and operational assessment of program effectiveness.

Extensive research on tick control methods have provided diverse approaches to tick management. However, there have been few broad-scale projects that have tested control methods with appropriate controls, and in various combinations with assessment of effectiveness as a function of cost, or of interactions among different control methods. Furthermore, most of these programs are without modeling frameworks to assess cost effectiveness of different interventions. Such studies would allow optimization of Integrated Tick Management programs in terms of cost effectiveness, and should include the interests of stakeholders with regard to environmental effects of the management programs.

Large-scale biological interventions

Recent advances in molecular biology have provided new tools for identifying unique proteins, specific to either the Lyme disease agent, B. burgdorferi, and/or its vector tick, I. scapularis, the blacklegged tick. In addition, new advances in genetics have provided tools for literally changing the structure of genes (gene editing) so that they no longer function (CRISPR-cas9). Some vaccines have been developed, primarily for companion animals and cattle. We need new vaccines against specific pathogenic bacterial proteins or tick body proteins, such as an anti-tick vaccine. The sum total of these exceptionally powerful new tools is that it is now possible to deploy them in an integrated tick vector-pathogen management program to greatly reduce tick survival and the disease-causing pathogens they transmit below the threshold of a public health threat.

In addition to the Potential Actions proposed for this section, the following two methods (in order of possible risk and benefit) could be considered as a means to achieve the goal of minimizing Lyme disease as a public health threat within 20 years.

  1. Vaccinate white-tailed deer. The tools exist to do this effectively, since we have a long-standing, known efficacious vaccine, LymeRX, originally developed for treating humans, that is available today for treating companion animals. The vaccine could be incorporated into liposomes and delivered using the 4-poster self-medicating applicator with corn or similar baits containing the vaccine. Alternatively, a DNA vaccine against TROSPA could be used, which would be directed to the oocytes and block this B. burgdorferi receptor in the F1 generation (i.e., larvae). We could also use reversed antigen sequencing (RAS) to deliver the target molecule, a proven technique previously used in sand flies against Leishmania transmission. Finally, we can deliver tick salivary gland antigens via this same oral route, thereby stimulating antibodies (for example, anti-lipocalin, an antihistamine) against tick saliva and disrupt adult tick feeding on deer. The 4-poster technique has proved to be highly effective in controlling ticks on deer by administering pesticides such as permethrin but has had limited use because of concerns by state game commissions that it would cause harm to human hunters during the hunt season. However, the oral vaccine would not pose a danger to human hunters since antibodies are generated in the deer and have no activity in humans (in other words, humans do not have the bacterial proteins such as Borrelia OspA). Also, since ticks cannot reproduce without vitellogenin (Vg), incorporating an anti-Vg or vitellogenin receptor vaccine should also be considered as a means to disrupt female reproduction in deer-fed ticks.
  2. Control juvenile tick feeding on small mammals by use of orally administered self-medicating treatment with anti-OspA vaccine against the B. burgdorferi (Richer et al., 2014). This is a proven technology, with several years of success in multiple localities.

In summary, we have the tools to immediately undertake large-scale biological interventions based on vulnerabilities in the tick’s molecular composition and proven anti-tick vaccines.

Threats or challenges

  • Lack of evidence for Integrated Tick Management strategies to result in reduced human tick bites or human tick-borne illness
  • Capacity for organized tick control is either lacking or poorly developed across the United States.

Potential actions to minimize the public health threat of Lyme disease and other tick-borne diseases

The following Potential Actions should be considered as a means to achieve the priority of minimizing Lyme disease and other tick-borne diseases as public health threats. For example, in the case of Lyme disease and for the purpose of this Subcommittee, anti-tick vaccines for white-tailed deer to suppress tick populations via disruption of feeding or egg-laying in female ticks; and pathogen transmission-blocking vaccines to prevent infection in white-footed mice and other natural pathogen reservoirs.

All of the proposed actions require additional funding, which should be appropriated so that it is commensurate with the burden of tick-borne disease. Monies should be allocated to the National Institutes of Health, Centers for Disease Control and Prevention, and other Federal agencies to support laboratory investigations and field trials to minimize Lyme disease and other tick-borne diseases as public health threats. The cognizant Federal agencies can use existing peer-review processes to review proposals, fund meritorious projects, and evaluate progress in achieving this goal.

Potential Action 1A: Assess and enhance the effectiveness of Integrated Tick Management (ITM) strategies.

Support continued assessment of existing and new area-wide Integrated Tick Management (ITM) strategies with the ultimate goal of reducing tick-borne disease. Create best practices for using evidence-based ITM strategies that:

  1. are tick species-specific;
  2. can be implemented by vector biologists, ecologists, entomologists, pest management specialists, and other practitioners of area-wide ITM;
  3. consider cost-effectiveness;
  4. minimize non-target effects and pesticide resistance in vector ticks;
  5. maximize the likelihood of public acceptance and adoption; and 6) can demonstrate reduction of human tick bites or tick-borne disease.

Potential Action 1B: Support research on ways to disrupt tick feeding, reproduction, and pathogen transmission.

Fund research addressing the knowledge gap on target pathways that disrupt tick feeding, reproduction, and transmission of pathogens causing Lyme disease and other tick-borne diseases. Using our expanding knowledge of the genes and molecules controlling tick feeding, tick reproduction, and transmission of tick-borne pathogens, it should be possible to precisely target and block these processes. For example, develop vaccines that block tick feeding before transmission of microbes can occur, especially for use in areas where tick-borne diseases are common. Further research is needed to develop and implement the use of these methods.

Potential Action 1C: Promote development of Integrated Tick Management methods and adoption by commercial applicators.

Encourage incorporation of Integrated Tick Management (ITM) methods into the current pest control model and commercial development of new effective tick control products. These actions would: 1) expedite the implementation of existing and development of promising new intervention technologies; 2) need broad funding that incorporates basic, translational, and applied research, as well as a seed support initiatives—such as Small Business Innovation Research; and 3) facilitate the commercialization or marketing of existing and new intervention products for tick and tick-borne disease control to reach the widest possible segments of the populations at risk of Lyme disease and other tick-borne diseases.

Potential Action 1D: Encourage public-private partnerships.

Supporting these critical partnerships will expedite the progress of intervention strategies, including to commercialize and market the most promising new and/or existing technologies so as to reach the widest possible segments of the populations at risk of Lyme disease and other tick-borne diseases in the United States.

Vote of subcommittee members on Potential Actions 1A-1D

Vote on Potential Action 1A as written above

Number in Favor

Number Opposed

Number Abstained

Number Absent

13

0

0

1

Vote on Potential Action 1B as written above

Number in Favor

Number Opposed

Number Abstained

Number Absent

13

0

0

1

Vote on Potential Action 1C as written above

Number in Favor

Number Opposed

Number Abstained

Number Absent

13

0

0

1

Vote on Potential Action 1D as written above

Number in Favor

Number Opposed

Number Abstained

Number Absent

13

0

0

1

Minority responses

There are no minority responses.

Priority 2: Establish and Sustain a National Network to Support Tick Surveillance and Control by Fiscal Year 2021

A prerequisite to suppressing Lyme disease and other tick-borne diseases is the establishment and sustainability of a national network for tick surveillance and control. This network should provide a comprehensive focus upon ticks and tick-borne diseases, incorporating the One Health concept—which recognizes that the health of people is connected to the health of animals and the environment—with financial support for applied research on the ecological and evolutionary factors driving the spread of ticks and pathogens, sustained surveillance, data gathering, analysis of change-over-time and future predictions. The network should also provide financial support for data dissemination as well as training and education activities relevant to local, county, state, and regional levels using the organizational foundation created by the Centers for Disease Control and Prevention, via the Epidemiology and Laboratory Capacity for Infectious Disease program and the Vector-borne Disease Regional Centers of Excellence.

The goal is to establish a network that builds upon existing capabilities to provide effective surveillance of all tick species of medical or veterinary importance and their associated pathogens. The network will capture changing populations, population densities within and among tick species, geographic ranges, and the introduction of any invasive tick species. The network will also provide timely screening for pathogens by deep sequencing of bacterial, parasitic, and viral tick pathogens and will provide a database of recognized and potential emerging pathogens of human and veterinary concern.

Summary of evidence/findings

Among arthropod vectors of disease, ticks transmit the most diverse array of infectious agents, and are the most important arthropod vectors globally of humans and domestic animal pathogens (Jongejan and Uilenberg, 2004; Colwell et al., 2011; Pfӓffle et al., 2013). Tick-borne infections of humans are zoonoses of wildlife origin, similar to tick transmitted diseases of companion and domestic animal species (Baneth, 2014). Zoonoses are mutually transmissible infections between humans and other animal species (Karesh et al., 2012). Greater than 22 percent of human infectious diseases emerging between 1940 and 2004 were arthropod vector-borne zoonotic infections (Jones et al., 2008). In the United States, approximately 95 percent of reported vector-borne diseases are tick transmitted (Adams et al., 2015).

Dynamic interactions occurring among biotic and abiotic elements influence tick and tick-borne disease ecology and epidemiology on a global scale. The emergence, resurgence, and geographic spread of tick-borne infections are influenced by tick and tick-borne pathogen demography (intrinsic population growth), micro and macro climate, human behavior, travel, landscape, land use, landscape fragmentation, host animal composition and movement (including domestic, wild and exotic species), economics, politics, population growth and movement (Pavlovsky, 1966; Pfӓffle et al., 2013; Baneth, 2014; Dantas-Torres, 2015).

The relative importance of these factors in the emergence of ticks and tick-borne diseases varies over space and time, both in the U.S. and globally. This dynamic state of flux challenges our ability to predict changes, requiring constant monitoring of the abundance, prevalence, and distribution of existing pathogens and detection of new ones through a strong surveillance/monitoring system. A strong understanding of the ecological drivers coupled with constant data acquisition is needed to detect public health threats in a timely fashion, raise public awareness of the threats, and develop effective disease and vector control measures (Randolph, 2010; Perez de Leon et al., 2012; Dantas-Torres, 2015; Ostfeld and Brunner, 2015; Stone et al., 2017).

Multiple changes are occurring among the complex associations of biotic and abiotic factors at micro and macro levels that require heightened surveillance of ticks and established, resurging, and emerging tick-borne infectious agents. The geographic range of the blacklegged tick (I. scapularis) expanded significantly in the Eastern and Midwestern United States during the past 20 years (Eisen et al., 2016), from the distribution determined by a standardized collection throughout the Northeastern U.S. (Diuk-Wasser et al. 2012). Concomitant with this expanded range is an increase in incidence of reported cases of Lyme disease and other I. scapularis-vectored pathogens (Eisen et al., 2017). Between 1996 and 2016, the number of counties, in which blacklegged ticks (I. scapularis and I. pacificus) is established, doubled to 44.7 percent of all United States counties (Eisen et al., 2016). Potential geographic range of this tick exceeds the currently described distribution within the United States (Hahn et al., 2016). The I. scapularis range expanded into eastern and central Canada by approximately 2004, accompanied by the emergence of Lyme disease (Ogden & Lindsay, 2016). While in the United States, I. scapularis is considered to be reclaiming its historical geographic range in response to changes that include habitat and climate, and availability of hosts for all life cycle stages (Eisen & Eisen, 2018), some areas in Canada may exceed its historic distribution due to anthropogenic climate change. Highlighting the public health importance of this tick, I. scapularis is a competent vector and the white-footed mouse (Peromyscus leucopus) a reservoir host for an increasing number of human pathogens: B. burgdorferi, A. phagocytophilum, Babesia microti, B. miyamotoi, and Powassan virus (Eisen et al., 2017; Eisen & Eisen, 2018).

The lone star tick (A. americanum) is a tick of increasing importance due to significantly expanding geographic range, increased population density, and roles as vector of established and emerging infectious agents that include E. chaffeensis, E. ewingii, and the recently described Heartland and Bourbon viruses (Childs & Paddock, 2003; Godsey et al., 2016; Eisen et al., 2017; Savage et al., 2017). A. americanum is increasingly important medically due to its involvement in galactose-alpha-1, 3-galactose, or alpha-gal allergy, a significant cause of human allergies resulting from exposure to a number of allergens (Platts-Mills et al., 2015). Distribution of this important pest tick was historically described as the southeastern United States to west central Texas and north to Iowa; however, the geographic range now extends into the Mid-Atlantic States and New England (Molaei et al., 2019), and is regularly detected as far north as Maine (Keirans & Lacombe, 1998).

Geographic range of the Gulf Coast tick, A. maculatum, increased significantly within the United States since the first half of the twentieth century (Teel et al., 2010; Sonenshine, 2018). This tick of medical and veterinary importance, particularly associated with R. parkeri (Summer et al., 2007), was initially limited to the Gulf of Mexico coast from Texas to the Atlantic Ocean coastal South Carolina and as far as 150 miles inland along this zone. Currently, A. maculatum can be found as far north along the coast of Delaware with a range of greater than 250 miles inland and with populations also established in several Midwestern to southwestern states (Teel et al., 2010; Paddock & Goddard, 2015; Sonenshine, 2018).

An often-overlooked driver of tick and tick-borne pathogen emergence is the geographic and demographic expansion and movement of their wild and domestic host populations. Unlike mosquitoes, all stages of ticks are dependent on their hosts for blood meals, and they can only move long distance while attached to hosts. Thus, the distribution of ticks is tightly linked to that of the host animals. Global changes, including increasing movement of host animals, directly impact invasive tick species risks to the U.S. In the southwestern U.S., introgression of the tropical strain of the brown dog tick, R. sanguineus, is associated with a virulent form of R.rickettsii, causal agent of Rocky Mountain spotted fever (Villarreal et al. 2018; Eremeeva et al., 2011). Amblyomma triste, a vector of R. parkeri in South America (Venzal et al., 2004) has been confirmed in riparian canyon areas of Arizona and Texas (Mertins et al., 2010), as well as the Mexican border states of Coahuila and Sonora (Guzman-Cornejo et al., 2006). Amblyomma variegatum, the tropical bont tick originally from Africa, remains on many Caribbean islands sustained in part by interisland bird dispersal, and is a threat to both North and South America with risks of E. ruminantium and Rickettsia africae (Beati et al., 2012; U.S. Department of Agricutlure, APHIS Veterinary Services, 2008). The recent discovery of the Asian longhorned tick, H. longicornis, in the U.S. and its potential as a vector of several pathogens has impacts for both human and animal health (Beard et al., 2018). The applications of climate-based modelling to predict range expansion of ticks are among tools improving assessment of risks for both ticks and tick-borne diseases (Estrada-Pena, 2008). Examples include Haemaphysalis longicornis (Magori, 2018; Raghavan et al., 2019), A. variegatum (Estrada-Pena, Pegram, Barre, & Venzal, 2007), and Rhipicephalus (Boophilus) microplus (Estrada-Pena & Venzal, 2006).

In addition to well-established diseases, multiple emerging tick transmitted pathogens have been described during the past two decades (Eisen et al., 2017; Kernif et al., 2016). Global scope of emerging tick-borne disease causing agents includes Babesia (Vannier et al., 2015), Rickettsia (Parola et al., 2013), Ehrlichia and Anaplasma (Ismail & McBride, 2017), Borrelia (Kernif et al., 2016), and viruses (Kazimírová et al., 2017; Mansfield et al., 2017).

Recognition of the increasing complexity of tick-associated microorganisms is due in part to the application of genomics, functional genomics, next generation sequencing, and proteomics to analyses of tick microbiomes (Tijsse-Klasen et al., 2014; Narasimhan & Fikrig, 2015). Molecular techniques are now used to reverse pathogen discovery by applying these powerful tools for identification of previously unrecognized microorganisms in ticks prior to association of those microbes with disease (Parola et al., 2013). Molecular techniques were the basis for reversed discovery of the following microbes later established to be human pathogens: B. miyamotoi (Branda & Rosenberg, 2013), Neoehrlichia mikurensis (Kawahara et al., 2004), Rickettsia helvetica (Jado et al., 2007), and other Rickettsia species (Parola et al., 2013). These powerful and sensitive approaches identify tick-associated microbes that are tick symbionts, known disease causing agents, or microbes that have the potential to become emerging pathogens of human and veterinary importance.

Possible opportunities

Congress should support the central organizational and operational structure to expand in scope of vector and vector-borne disease surveillance, including a focus on ticks and tick-borne diseases. A national network should encompass working relationships across Federal, state, and local agencies and vector control districts, university and college centers and institutes, academic institution departments, land grant university agricultural experiment stations, and state, county and local public health departments. The reach and focus of these components and their activities must be to the local community level and be structured for integration of activities based upon tick ecology inherent to the locale.

Integral to these core components in defining and supporting the mission and activities of the network is engagement of stakeholders, advocacy groups, scientists from diverse disciplines, and the general public. The proposed national network should have a mandate to address all vectors and vector-borne diseases of public health importance. This approach brings together within one framework broad expertise, infrastructure, resources, educational expertise, and the ability to implement integrated control responses to vectors and vector-borne pathogen threats to medical and/or veterinary public health. The nature of disease vectors and the zoonotic nature of many vector-borne, particularly tick transmitted, diseases requires a One Health approach.

The proposed national tick surveillance network provides a platform for testing all the possible interventions that are recognized as well as emerging novel ones. This network will also serve as a framework for providing professional and public education opportunities.

Threats or challenges

  • A process for allocation of funding for surveillance would need to be strategically placed and not aggregated
  • Coordination of agency activities already in existence
  • Overcoming the disparate nature of surveillance and standardizing information from the different agencies and organizations involved

Potential Actions to establish and sustain a national network to support tick surveillance and control by FY 2021

The following Potential Actions should be considered as a means to achieve the priority of establishing and sustaining a national network to support tick surveillance and control by Fiscal Year 2021.

Potential Action 2A: Develop and implement best practices for tick vector surveillance.

Develop and implement evidence-based best practices for national surveillance of tick vector species, their distributions, their abundance, and their associated pathogens. This surveillance will help identify and monitor existing, emerging, and new tick vector species, their environmental drivers, as well as their associated pathogens, important to medical and veterinary public health. Specific activities will: 1) document and monitor tick species ranges, range expansions and contractions, and geographic overlaps; 2) identify and monitor non-native tick species to minimize the risk of invasive ticks entering the U.S. and, if possible, rapidly abate or manage establishing invasive species; and 3) assess favorable host ranges, vegetation habitats, and the impacts of changing landscapes and other environmental factors on tick populations.

Potential Action 2B: Foster coordination among Federal, state, and local agencies.

Increase coordination and support of tick surveillance activities and data management across Federal, state, and local agencies, as well as experiment stations, universities, and public entities and networks.

Potential Action 2C: Provide resources for local tick management programs.

Create local tick management programs that are: 1) professionally-staffed; 2) adequately resourced to operate using Integrated Pest Management principles and follow standardized guidelines; 3) responsible for surveillance of tick vectors and their associated pathogens; 4) responsible for public outreach; and 5) applicable to control of tick vectors on publicly and/or privately-owned lands, possibly in part through homeowner incentives.

Potential Action 2D: Provide education and training to all stakeholders.

Develop and promote a broad range of improved, science-based educational materials, training programs, and outreach initiatives that provide adequate background knowledge about tick vectors and tick-borne disease prevention, for stakeholders at the local, regional, and national levels. This includes vector control professionals, health care providers, students in K-12, university students, post-doctoral fellows, those at occupational risk, and members of the general public.

Vote of subcommittee members on Potential Actions 2A-2D

Vote on Potential Action 2A as written above

Number in Favor

Number Opposed

Number Abstained

Number Absent

13

0

0

1

Vote on Potential Action 2B as written above

Number in Favor

Number Opposed

Number Abstained

Number Absent

13

0

0

1

Vote on Potential Action 2C as written above

Number in Favor

Number Opposed

Number Abstained

Number Absent

13

0

0

1

Vote on Potential Action 2D as written above

Number in Favor

Number Opposed

Number Abstained

Number Absent

13

0

0

1

Minority responses

There were no minority responses.

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VanAcker, M. C., Eliza A.H. Little, E. A. H., Molaei, G., Bajwa, W. I., & Diuk-Wasser, M. A. (2019). Enhancement of Risk for Lyme Disease by Landscape Connectivity, New York, New York, USA. Emerging Infectious Diseases, 25(6), 1131-1143. doi: 10.3201/eid2506.181741

Vannier, E.G., Diuk-Wasser, M.A., Ben Mamoun, C., & Krause, P.J. (2015). Babesiosis. Infectious Disease Clinics of North America29, 357-370. doi: 10.1016/j.idc.2015.02.008

Vayssier-Taussat, M., Kazimirova, M., Hubalek, Z., Hornok, S., Farkas, R., Cosson, J. F., . . . Rizzoli, A. (2015). Emerging horizons for tick-borne pathogens: from the ‘one pathogen-one disease’ vision to the pathobiome paradigm. Future of Microbiology, 10(12), 2033-43. doi: 10.2217/fmb.15.114

Venzal, J.M., Portillo, A., Estrada-Pena, A., Castro, O., Cabrera, P. A., & Oteo, J. A. (2004). Rickettsia parkeri in Amblyomma triste from Uruguay. Emerging Infectious Diseases, 10(8), 1493-5. doi: 10.3201/eid1008.030999

Villarreal, Z., Stephenson, N., & Foley, F. (2018). Possible northward introgression of a tropical lineage of Rhipicephalus sanguineus ticks at a site of emerging Rocky Mountain spotted fever. Journal of Parasitology, 104(3), 240-245. doi: 10.1645/18-10

Wang, H-H., Corson, M. S., Grant, W. E., & Teel, P. D. (2017). Quantitative models of Rhipicephalus (Boophilus) ticks: Historical review and synthesis. Ecosphere 8(9), e01942. doi: 10.1002/ecs.2.1942

Wang, H-H., Grant, W. E., & Teel, P. D. (2012). Simulation of climate-host-parasite-landscape interactions: A spatially explicit model for ticks (Acari: Ixodidae). Ecological Modelling, 243, 42-62. doi: 10.1016/j.ecolmodel.2012.06.007

White, A., & Gaff, H. (2018). Review: Application of tick control technologies for blacklegged, lone star, and American dog ticks. Journal of Medical Entomology, 9(1), 12, 1-12. doi: 10.1093/jipm/pmy006

White, D. J., Benach, J. L., Smith, L. A., & Ouyang S. P. (1981). Control of Dermacentor variabilis. 3. An analytical study of the effect of low volume spray frequency on insecticide–stressed and nonstressed populations. Journal of the New York Entomological Society, 89(1), 23-33.

Williams, S. C., Stafford III, K. C., 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 Diseases, 18(1), 55-64. doi:10.1089/vbz.2017.2146

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Appendix A: Topic Development Brief Results—Causes of the Increase in Tick-Borne Diseases in the United States

Tick-Borne Disease Working Group Results of Topic Selection Process & Next Steps

The Tick-Borne Disease Working Group is interested in using an assessment of available literature to research the causes of the increase in tick-borne diseases in the United States. Given the large volume of original research on this topic, a new systematic literature review would be feasible.

Topic Brief

Topic Name: Increased Tick-Borne Diseases

Topic Brief Date: September 6, 2019

Date of Nomination: July 18, 2019

Nominator: Adalberto Pérez de León, DVM, PhD, MS, and Robert Sabatino

Authors: Selena Gonzales, MPH, and Christina Li, MPH

Conflict of Interest: The nominator and authors have no affiliations or financial involvement that conflict with the material presented in this report.

Background

The increasing incidence of tick-borne diseases poses a serious threat to public health (Gray & Herwaldt, 2019; Petersen, Foster, McWilliams, & Irwin, 2015; Raghavan, Goodin, Neises, Anderson, & Ganta, 2016; Raghavan, Peterson, Cobos, Ganta, & Foley, 2019). Currently, the

U.S. Centers for Disease Control and Prevention recognize 18 tick-borne pathogens in the United States. However, researchers and clinicians continue to discover emerging pathogens and new medical conditions associated with tick bites. Proposed causes for the increasing incidence of tick-borne diseases include:

  • the climate’s effects on tick biology and ecology,
  • the interaction of climatic and environmental factors,
  • changes in host availability,
  • changes in tick abundance,
  • changes in the geographic distribution of ticks, and
  • changes in the prevalence of pathogens in tick populations.

An enhanced understanding of the reasons for the rising incidence of tick-borne diseases will help scientists and health care professionals develop strategies to lower the risk for disease transmission.

Topic Nomination Development

Nominator and Stakeholder Engagement

During a conference call with the nominator, the authors reviewed and clarified the key question, guiding questions, and PICOTS (population, interventions/indicators, comparators, outcomes, timing of interest, and setting). The nominator provided final approval of those items via email.

Key Question

The key question for this topic nomination is: Considering tick biology, ecology, and control, what are the causes for the increased number of tick-borne disease cases in the United States?

Proposed Guiding Questions

Based on the variable level of evidence development, we proposed the following guiding questions.

  1. Is the problem with ticks and tick-borne diseases particular to the United States or is it a global issue?
  2. If it is a global problem, what are the particular drivers (e.g., climate variability, environmental change, host and vector population increases, range expansion) for the problem with ticks and tick-borne diseases in the United States during the past 50 years?
  3. What are the challenges for implementation research on integrated tick management focused on controlling host and vector populations to decrease the risk of tick-borne disease transmission?

Proposed PICOTS

To define inclusion criteria for the key question, we specified the PICOTS.

Key Questions and PICOTS

Topic Information

Key Question

Considering tick biology, ecology, and control, what are the causes for the increased number of tick-borne disease cases in the United States?

Population

People diagnosed with tick-borne diseases in the United States and globally

Interventions/ Indicators

Understanding how climate variability, environmental change, host and vector population increases, and range expansion increase the risk of tick-borne disease transmission so we can adapt interventions

Comparators

Compare findings from interventions/indicators to each other

Outcomes

Identifiable causes for an increase in tick-borne diseases to adapt integrated tick-management interventions targeting the vector- host-pathogen interface by disrupting vulnerabilities in the biology and ecology of ticks

Timing

Past 50 years (1968–2018)

Setting

Geographic areas with increased risk of tick-borne disease transmission in the United States

Methods

We assessed the nomination of Increased Tick-borne Diseases as a topic brief priority using the following established selection criteria. Assessment of each criterion determined the need to evaluate the next one.

  1. Determine the appropriateness of the topic.
  2. Establish the overall importance of the topic as representing a health or health care issue in the United States.
  3. Determine the desirability of a new evidence review by examining whether a systematic literature review would be duplicative.
  4. Assess the potential impact of a new systematic literature review.
  5. Assess whether the current state of the evidence allows for a systematic literature review (feasibility).
  6. Determine the potential value of a new systematic literature review.

Results

Appropriateness and Importance

This topic is appropriate and important. Lyme disease is one of the most commonly reported and widely known tick-borne diseases. However, cases of alpha-gal syndrome, anaplasmosis, babesiosis, ehrlichiosis, and rickettsiosis are now increasing, too (Gray & Herwaldt, 2019; Petersen et al., 2015; Raghavan et al., 2016; Raghavan et al., 2019).

Desirability of New Review/Duplication

A new evidence review would not be duplicative. The causes of the increase in tick-borne diseases and tick populations have not been systematically reviewed. Further research is needed to understand the increase in tick-borne diseases.

Impact of a New Evidence Review

A new systematic review may prove useful in the development of public health strategies to mitigate the impact of the growing threat of tick-borne diseases.

Feasibility of a New Evidence Review

We conducted a literature search in EBSCOhost in August 2019 using the key question, guiding questions, and PICOTS to develop keyword searches. See Appendix A for the EBSCOhost search strategy.

A new systematic literature review is likely feasible with some modifications to the selection criteria. There is adequate information to perform a systematic literature review on the causes of the increase in tick populations and tick-borne diseases.

There is little research on the targeted management of host and vector populations. The evidence base is broad and includes many articles on the management of tick-borne diseases in regards to the impact on livestock. A focused review on strategies to manage populations of tick species that cause disease in livestock might provide information that is applicable to human health.

Discussion

In the United States, ticks cause more illness in humans than any other arthropod. Lyme disease is one of the most commonly reported and widely known tick-borne diseases. However, cases of alpha-gal syndrome, anaplasmosis, babesiosis, ehrlichiosis, and rickettsiosis are now increasing, too (Gray & Herwaldt, 2019; Petersen et al., 2015; Raghavan et al., 2016; Raghavan et al., 2019).

A global problem, tick-borne diseases pose a threat to the health of non-U.S. populations as well as U.S. military personnel and civilian employees living and working abroad. Some of those diseases are not currently occurring in the United States. One notable example is tick-borne encephalitis (TBE). Endemic to various areas of Europe and Asia, TBE is becoming more common in Sweden (Jaenson et al., 2018). The virus that causes TBE is transmitted by the Ixodes ricinus tick, which also carries the spirochetes that cause Lyme disease in Europe (Hauser et al., 2018).

Themes From the Literature

In an effort to answer this topic brief’s key question, we conducted a preliminary assessment of the literature and identified the following key themes:

  • the climate’s effects on tick biology and ecology,
  • the interaction of climatic and environmental factors,
  • changes in host availability,
  • changes in tick abundance,
  • changes in the geographic distribution of ticks, andchanges in the prevalence of pathogens in tick populations.

The following section elaborates on each key theme and features highlights from the literature, as appropriate.

The Climate’s Effects on Tick Biology and Ecology

The climate has been shown to affect tick biology and ecology, which has practical implications for tick prevalence, tick distribution, and the incidence of tick-borne diseases.

A 2017 study (Ginsberg et al.) suggests that the greater number of cases of Lyme disease in the northeastern and upper midwestern regions of the United States, compared with the southern states, may be related to the effects of temperature and humidity on tick behavior. Ginsberg et al. replicated environmentally realistic conditions in their laboratory. The authors found that I. scapularis stays below the leaf litter surface in warmer, dryer areas of the southern United States and on the leaf litter surface in cooler, more humid regions of the northern United States. The study suggests people walking through the woods in warmer, dryer areas are less likely to be bitten by I. scapularis ticks and may therefore be at lower risk for infection with the pathogens that cause Lyme disease.

Estrada-Peña and Estrada-Sánchez (2014) conducted a study of development and mortality rates of I. ricinus ticks in western Europe. The authors found that the season for tick development was three times longer in southern regions of the tick’s geographic range than in northern regions. Notably, conditions were warmer and dryer in the southern regions.

However, a longer season for development was not necessarily advantageous, as it was correlated with lower tick survival rates. Although this study’s implications for the incidence of tick-borne diseases in western Europe remain unclear, the lack of clarity does suggest a need for additional research on tick development that considers tick ecology, vegetation composition, and host availability.

The Interaction of Climatic and Environmental Factors

Between 1978 and 2008, the geographic range of I. ricinus within southern Norway expanded due to a complex combination of the following climatic and environmental factors (Jore et al., 2014)

  • large diurnal changes in ground surface temperature,
  • duration of snow cover,
  • spring precipitation,
  • an abundance of red deer and farm animals, and
  • changes in land use resulting in bush encroachment of open fields.

I. ricinus transmits TBE, which poses a significant health threat to people living in southern Norway (Andreassen et al., 2012). However, Jore et al. (2014) stop short of directly linking the tick’s range expansion to the increased incidence of TBE or other tick-borne diseases in humans.

Changes in Host Availability

Some research suggests that changes in host availability might be driving the incidence of tick- borne diseases upward. The above-mentioned study by Jore et al. (2014) of I. ricinus

populations in southern Norway found that an abundance of red deer and farm animals, in combination with other factors, helped facilitate the expansion of the ticks’ geographic range over a 30-year period (1978–2008). And a recent study by Jaenson et al. (2018) suggests the increased availability of deer in Sweden may have contributed to increases in the density of I. ricinus populations and the incidence of TBE.

However, results of research on I. ricinus in eastern Russia between 1977 and 2011 seem to downplay the role of host availability in the increase of tick-borne diseases. In that study, Korotkov, Kozlova, and Kozlovskaya (2015) observed long-term growth in tick populations but little change in the number of vertebrates that ticks feed on. And a more recent study conducted by Gleim et al. (2014) in the southern United States found no relation between host abundance and tick abundance.

Changes in Tick Abundance

Several studies suggest ticks will become more abundant with continued climate change. For instance, Ogden et al. (2014) found that rising temperatures from 1971–2010 boosted the reproduction capacity of I. scapularis, which may have contributed to the emergence of Lyme disease in the northeastern United States.

Estrada-Peña, de la Fuente, Latapia, and Ortega (2015) assessed the effects of climate trends between 1901 and 2009 on the life cycle of Hyalomma marginatum, a tick species that is the main vector of Crimean-Congo hemorrhagic fever virus in the Mediterranean basin and the Middle East. According to the authors’ analysis, recent climate trends have helped H. marginatum become more abundant in areas of Europe with successfully established populations of that tick species.

However, Hauser et al. (2018) collected I. ricinus in a forest in Switzerland from 2000–2014, a time period that saw global increases in daily mean temperatures and daily mean values of relative humidity. The authors observed a decrease in the tick population and recommended further studies to assess the impact of host abundance and the role of microhabitats on tick population density.

Changes in the Geographic Distribution of Ticks

Research suggests that ticks’ widening geographic distribution has led to an increase in the incidence of Lyme disease in North America (Ogden et al., 2010; Ogden et al., 2014; Cheng et al., 2017). For example, Cheng et al. determined that, between 1979 and 2013, the range of sustainable tick habitat within Ontario expanded as a result of climate change, and populations of I. scapularis colonized new regions of the province.

Scientists predict that climate change will continue to cause shifts in the geographic distribution of ticks and the areas where tick-borne diseases are endemic (Ogden et al., 2014; Cheng et al., 2017). In some cases, the distribution will widen to include areas beyond different latitudes.

However, elevation is also an important factor to consider. For instance, in the case of

Ornithodoros hermsi, a tick species that transmits tick-borne relapsing fever in North America, we are more likely to see shifts to higher elevations where temperatures and precipitation amounts are more conducive to the tick’s survival (Sage, Johnson, Teglas, Nieto, & Schwan, 2017).

That being said, a recently published paper by MacDonald (2018) suggests climate change will lead to overall reductions in the habitat and activity of I. pacificus, a vector of Lyme disease in California. Notably, established populations of I. pacificus are found in dense forest habitats with cool and moist microclimates, and adult ticks of that species tend to be more abundant in areas with lower average winter temperatures.

Changes in the Prevalence of Pathogens in Tick Populations

Several studies indicate that the prevalence of disease-causing pathogens varies among established tick populations.

Estrada-Peña et al. (2018) analyzed data spanning 2000–2017 for a study of I. ricinus in Europe. They found a higher prevalence of Borrelia spirochetes in the tick populations of central European regions characterized by warmer temperatures, a steady rise in springtime temperatures, and less abrupt changes in vegetation from one year to the next.

Gasmi et al. (2018) analyzed tick surveillance data collected in Quebec from 2007–2015, with a focus on tick species other than I. scapularis. The analysis revealed a trend of increased abundance for the following four tick species:

  • I. cookei, the primary vector for Powassan virus;
  • Dermacentor variabilis, a vector of Rocky Mountain spotted fever (RMSF) and tularemia;
  • Rhipicephalus sanguineus, a vector of RMSF; and
  • Amblyomma americanum, a vector of tularemia and two types of ehrlichiosis.

Notably, studies to assess the prevalence of pathogens in tick species other than I. scapularis in Quebec had not been conducted. Furthermore, although I. cookei had been endemic to Quebec for many years, only six cases of Powassan encephalitis were reported between 2004 and 2014.

The low incidence of Powassan encephalitis, despite the abundance of I. cookei, seems to reinforce the findings of Ogden et al. (2010). According to their study, the establishment of B. burgdorferi in Quebec and the emergence of Lyme disease occurred several years after migratory birds brought I. scapularis into the province from the northeastern United States.

Such findings suggest a need for heightened surveillance to identify the factors that increase or decrease the prevalence of tick-borne pathogens and to determine how changes in pathogen prevalence relate to changes in tick abundance and tick distribution.

Mitigating the Public Health Threat Posed by Tick-Borne Diseases

Strategies to prevent tick-borne diseases in the general public are currently limited. Many scientists and clinicians recommend the use of personal protective measures to prevent tick bites. Landscape and environmental measures, such as prescribed burning, have also been proposed as strategies for reducing tick populations (Petersen et al., 2015; Gleim et al., 2014).

Gleim et al. (2014) evaluated the effects of long-term prescribed burning on tick population dynamics in southwestern Georgia and northwestern Florida. Results of their study, which considered differences in vegetation and microclimate, suggest that prescribed burning reduces tick counts. However, the ticks sampled by the researchers after prescribed burning were not tested for disease-causing pathogens.

To be successful, efforts to prevent Lyme disease and other tick-borne diseases require adequate support for surveillance activities. Surveillance is most likely to be effective when it determines the density of tick populations in a given area and identifies the species comprising those populations. Given the continued emergence of tick-borne diseases and pathogens, surveillance efforts should encompass all tick species that are considered vectors. Testing ticks for established and newly emerging pathogens is also warranted (Petersen et al., 2015).

Although the incidence of Lyme disease is higher in the northeastern and upper midwestern regions of the United States, broader surveillance is needed to determine the risk of acquiring the disease in other areas of North America. As reported by Feria-Arroyo et al. (2014), the southern United States is typically portrayed as low risk for Lyme disease. Yet southern states experience a steady number of Lyme disease cases each year. Moreover, contrary to the findings of previous research, results of the study by Feria-Arroyo et al. indicate that much of eastern Texas and northeastern Mexico is either already home to, or capable of sustaining, populations of I. scapularis. And B. burgdorferi was present in 45% of the I. scapularis sampled in the study.

The question of how host availability affects tick abundance and tick distribution merits further investigation. Migratory birds, deer, and cattle are commonly assumed to be the primary hosts of ticks (Ogden et al., 2010; Feria-Arroyo et al., 2014; Petersen et al., 2015). However, other vertebrates may play a role in expanding the geographic range of ticks and tick-borne pathogens. For example, the Ornithodoros turicata—a vector of the relapsing fever spirochete B. turicatae—reportedly feeds on a wide range of mammals (including humans), reptiles, and birds, but is almost never found attached to a vertebrate host (Donaldson et al., 2016). Additionally, tick distribution models should consider the role of humans’ domestic and international travel in the spread of tick-borne diseases (Feria-Arroyo et al., 2014).

SUMMARY OF FINDINGS

Appropriateness and Importance

The topic is both appropriate and important.

Duplication

A new review would not be duplicative of an existing product. We found no systematic reviews related to the scope of the nomination.

Impact

A new systematic review may prove useful in the development of public health strategies to mitigate the impact of the growing threat of tick-borne diseases.

Feasibility

A new systematic literature review is likely feasible with some modifications to the selection criteria.

Appendix A References

Andreassen, A., Jore, S., Cuber, P., Dudman, S., Tengs, T., Isaksen, K., … Vainio, K. (2012). Prevalence of tick borne encephalitis virus in tick nymphs in relation to climatic factors on the southern coast of Norway. Parasites & Vectors, 5(177). doi:10.1186/1756-3305-5-177

Cheng, A., Chen, D., Woodstock, K., Ogden, N. H., Wu, X., Wu, J. (2017). Analyzing the potential risk of climate change on Lyme disease in Eastern Ontario, Canada using time series remotely sensed temperature data and tick population modelling. Remote Sensing, 9(6), 609-622. doi:10.3390/rs9060609

Donaldson, T. G., Pèrez de León, A. A., Li, A. Y., Castro-Arellano, I, Wozniak, E., Boyle, W. K., … Lopez, J. E. (2016). Assessment of the geographic distribution of Ornithodoros turicata (Argasidae): Climate variation and host diversity. PLOS Neglected Tropical Diseases, 10(3), e0004383. doi:10.1371/journal.pntd.0004383

Estrada-Peña, A., Cutler, S., Potkonjak, A., Vassier-Tussaut, M., Van Bortel, W., Zeller, H., … Mihalca, A. D. (2018). An updated meta-analysis of the distribution and prevalence of Borrelia burgdorferi s.l. in ticks in Europe. International Journal of Health Geographics, 17(41). doi:10.1186/s12942-018-0163-7

Estrada-Peña, A., de la Fuente, J., Latapia, T., Ortega, C. (2015). The impact of climate trends on a tick affecting public health: A retrospective modeling approach for Hyalomma marginatum (Ixodidae). PLOS ONE, 10(5), e0125760. doi:10.1371/journal.pone.0125760

Estrada-Peña, A., Estrada-Sánchez, D. (2014). Deconstructing Ixodes ricinus: A partial matrix model allowing mapping of tick development, mortality and activity rates. Medical and Veterinary Entomology, 28(1), 35-49. doi:10.1111/mve.12009

Feria-Arroyo, T. P., Castro-Arellano, I., Gordillo-Perez, G., Cavazos, A. L., Vargas-Sandoval, M., Grover, A., … Esteve-Gassent, M. D. (2014). Implications of climate change on the distribution of the tick vector Ixodes scapularis and risk for Lyme disease in the Texas- Mexico transboundary region. Parasites & Vectors, 7(199). doi:10.1186/1756-3305-7-199

Gasmi, S., Bouchard, C., Ogden, N. H., Adam-Poupart, A., Pelcat, Y., Rees, E. E., … Thivierge, K. (2018). Evidence for increasing densities and geographic ranges of tick species of public health significance other than Ixodes scapularis in Québec, Canada. PLOS ONE, 13(8), e0201924. doi:10.1371/journal.pone.0201924

Ginsberg, H. S., Albert, M., Acevedo, L., Dyer, M. C., Arsnoe, I. M., Tsao, J. I., … LeBrun, R. A. (2017). Environmental factors affecting survival of immature Ixodes scapularis and implications for geographical distribution of Lyme disease: The climate/behavior hypothesis. PLOS ONE, 12(1), e0168723. doi:10.1371/journal.pone.0168723

Gleim, E. R., Conner, L. M., Berghaus, R. D., Levin, M. L., Zemtsova, G. E., Yabsley, M. J. (2014). The phenology of ticks and the effects of long-term prescribed burning on tick population dynamics in southwestern Georgia and northwestern Florida. PLOS ONE, 9(11), e112174. doi:10.1371/journal.pone.0112174

Gray, E. B., & Herwaldt, B. L. (2019). Babesiosis surveillance--United States, 2011–2015. MORBIDITY AND MORTALITY WEEKLY REPORT Surveillance Summaries, 68(6), 1-11. Retrieved from https://www.cdc.gov/mmwr/volumes/68/ss/ss6806a1.htm

Hauser, G., Rais, O., Morán Cadenas, F., Gonseth, Y., Bouzelboudjen, M., Gern, L. (2018). Influence of climatic factors on Ixodes ricinus nymph abundance and phenology over a long-term monthly observation in Switzerland (2000–2014). Parasites & Vectors, 11(289). doi:10.1186/s13071-018-2876-7

Jaenson, T. G. T., Petersson, E. H., Jaenson, D. G. E., Kindberg, J., Pettersson, J. H.-O., Hjertqvist, M., … Bengtsson, H. (2018). The importance of wildlife in the ecology and epidemiology of the TBE virus in Sweden: Incidence of human TBE correlates with abundance of deer and hares. Parasites & Vectors, 11(477). doi:10.1186/s13071-018-3057-4

Jore, S., Vanwambeke, S. O., Viljugrein, H., Isaksen, K., Kristoffersen, A. B., Woldehiwet, Z., … Hofshagen, M. (2014). Climate and environmental change drives Ixodes ricinus geographical expansion at the northern range margin. Parasites & Vectors, 7(11). doi:10.1186/1756- 3305-7-11

Korotkov, Y. U., Kozlova, T., Kozlovskaya, L. (2015). Observations on changes in abundance of questing Ixodes ricinus, castor bean tick, over a 35-year period in the eastern part of its range (Russia, Tula region). Medical and Veterinary Entomology, 29(2), 129-136. doi:10.1111/mve.12101

MacDonald, A. J. (2018). Abiotic and habitat drivers of tick vector abundance, diversity, phenology and human encounter risk in southern California. PLOS ONE, 13(7), e0201665. doi:10.1371/journal.pone.0201665

Ogden, N. H., Bouchard, C., Kurtenbach, K., Margos, G., Lindsay, L. R., Trudel, L., … Milord, F. (2010). Active and passive surveillance and phylogenetic analysis of Borrelia burgdorferi elucidate the process of Lyme disease risk emergence in Canada. Environmental Health Perspectives, 118(7). doi:10.1289/ehp.0901766

Ogden, N. H., Radojević, M., Wu, X., Duvvuri, V. R.; Leighton, P. A.; Wu, J. (2014). Estimated effects of projected climate change on the basic reproductive number of the Lyme disease vector Ixodes scapularisEnvironmental Health Perspectives, 122(6). doi:10.1289/ehp.1307799

Petersen, W. H., Foster, E., McWilliams, B., Irwin, W. (2015, January-March). Tick-borne disease surveillance. U.S. Army Medical Department Journal, 49-55. Retrieved from https://ufdc.ufl.edu/AA00062689/00037/pdf

Raghavan, R. K., Goodin, D. G., Neises, D., Anderson, G. A., Ganta, R. R. (2016). Hierarchical Bayesian spatio-temporal analysis of climatic and socio-economic determinants of Rocky Mountain spotted fever. PLOS ONE, 11(3), e0150180. doi:10.1371/journal.pone.0150180

Raghavan, R. K., Peterson, A. T., Cobos, M. E.; Ganta, R., Foley, D. (2019). Current and future distribution of the lone star tick, Amblyomma americanum (L.) (Acari: Ixodidae) in North America. PLOS ONE, 14(1), e0209082. doi:10.1371/journal.pone.0209082

Sage, K. M., Johnson, T. L., Teglas, M. B., Nieto, N. C., Schwan, T. G. (2017). Ecological niche modeling and distribution of Ornithodoros hermsi associated with tick-borne relapsing fever in western North America. PLOS Neglected Tropical Diseases, 11(10), e0006047. doi:10.1371/journal.pntd.0006047

Appendix A: Selection Criteria Assessment, Search Strategy

A literature search was conducted using EBSCOhost in August 2019. Keywords and exclusion criteria were derived from the criteria set forth in the PICOTS. Additional articles were excluded when:

  • the full article was missing or there was not enough information in the abstract,
  • the article was not from a peer-reviewed scholarly journal, or
  • the article was not relevant to the topic area.

EBSCOhost search terms

Initial search results

“tick population” AND “increase”

21

“tick” AND “climate variability”

110

“tick” AND “climate change”

209

“tick population” AND “management”

16

“tick” AND “integrated management”

18

"tick host" AND "management"

9

“Ixodes” AND “management”

87

"Ixodes host" AND "management"

0

"Ixodes” AND “host" AND "management"

54

Appendix B: Writing Group Reports

The following three reports were written by writing groups within the Subcommittee. The content in these reports was used to generate the Results and Potential Actions section of this report. Here they are presented in their original format, as written. The cited references can be found in the References section of this report.

Biology Group Report

Daniel E. Sonenshine, R. Michael Roe, Kevin Macaluso, and Beto Perez de Leon

Primary Goal: “Elimination of Lyme disease as a public health threat through area-wide integrated tick vector-pathogen management: proof of concept in Northeast and California.”

The Tick Biology group identified the primary goal as the elimination of Lyme disease as a public health threat throughout the most highly endemic regions of the United States and Canada within 20 years (Zero40 for Ld). Lyme disease elimination will be done by means of a combination of modern genetic tools, modern vaccines, and by intervening into the most vulnerable elements of tick-host-pathogen processes to suppress abundance of the tick vector, Ixodes scapularis, block survival and multiplication of the pathogen (Borrelia burgdorferi). When implemented together, these interventions will effectively disrupt transmission of Lyme disease to humans and companion animals below the threshold of a public health threat.

Background, Priority Issues, and Findings

To understand the reasons why this ambitious but, nevertheless feasible approach to Lyme disease elimination, some background is needed. The Lyme disease tick, I. scapularis, is the only native tick species vector competent for the maintaining and transmitting the bacteria that cause Lyme disease (Ld), the spirochete, B. burgdorferi. However, the ability of the bacteria to colonize the tick is related to certain protein antigens on the bacterial surface, especially the outer surface protein, OspA, which enables these bacteria to lock onto a specific receptor in the tick’s digestive tract, known as TROSPA. Ld spirochetes acquired by larval ticks multiply in the digestive tract, but do not escape and migrate to the salivary glands until the infected larvae molt to the nymphal stage and feed again. Another tick-specific protein, enolase, enables the bacteria to escape into the tick’s interior, while a host-derived protein, plasminogen, disguises the microbes as they transit the tick’s body and enter the salivary glands. Finally, the Ld bacteria must bind to another protein, SALP15, specific to this tick species, to invade the gland ducts. This transmigration requires at least 2 days! Thus, as the tiny nymphs feed on a human or non-human animal, the bacteria are transmitted in the tick’s saliva to infect people and animals, unless the offending ticks are removed by the host before this two-day window.

In the United States, reported cases of all tick-borne diseases have increased over the 13-year period from 2004 to 2017 from 22,527 in 2004 to 59,349 in 2017. Lyme disease accounts for most of the cases, although thousands of cases of Anaplasmosis (A. phagocytophilum), Ehrlichliosis (Ehrlichia chafeense), spotted fever type rickettsial diseases (including Rocky Mountain spotted fever), babesiosis, tularemia, and tick-borne viruses are reported every year.

The geographic distributions of the major vectors of tick-borne diseases in the United States have been expanding greatly since detailed continental records were reported in 1945 (Bishop and Trembley, 1945). The distribution of blacklegged ticks (I. scapularis) has been continually expanding, whereas the distribution of western blacklegged ticks (I. pacificus) appears stable (Eisen et al 2017). The geographic distribution now covers almost all the eastern United States, as well as large areas in the north central U.S. The northern distributions of the blacklegged tick are continuing to spread in all directions from two major foci in the northeast and north central US (Eisen et al. 2017, Sonenshine 2018).

In the natural environment, I. scapularis is vulnerable to extreme environmental conditions, especially cold weather. However, in contrast to other known species, I. scapularis can survive over the winter if soil temperatures do not exceed subzero temperatures for long periods of time. These ticks can survive 10 degrees below zero for up to 2 hours. Blacklegged ticks have a compound (glycoprotein) 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). They are also vulnerable to desiccating conditions, which is why they occur mostly in woodland and brushy habitats nears rivers, bays, lakes, or near the oceans.

The black-legged tick is remarkable in its ability to feed on a large variety of vertebrate hosts, including diverse reptiles, ground feeding birds and numerous mammals. However, three animal hosts stand out as the predominant food sources, namely, white-tailed deer, white-footed mice and other small mammals, and migratory birds. Knowledge of these tick-host associations will help explain why targeting these vulnerabilities can be an important part of the Lyme disease threat elimination program.

The white-tailed deer is the primary amplifying host for abundance of I. scapularis populations. Deer populations are expanding rapidly and are likely to continue to increase greatly. Reasons include:

  1. Absence of wild predators. Wolves are extinct in almost all of the lower 48 U.S. states of. Other predators such as coyotes (Canis latrans) may occasionally kill deer, but deer are not their primary prey.
  2. Fewer human hunters. Numbers of hunters are declining due to restrictions where hunting is not allowed, for example, in state parks, city parks, and suburban developments.
  3. Loss of agricultural lands, such as cultivated fields and pastures, and replacement by woodlands and expansion of national parks and wilderness areas.

Risk for Lyme disease increases across an urban to forest gradient (Kilpatrick et al. 2017), but there is greater richness of reservoir host species, significantly higher encounters with hosts, and significantly lower B. burgdorferi host infection in residential areas as compared to large, intact forested stands, at least in Connecticut (Linske et al. 2018). Another important factor is the creation of contiguous “green” areas where wildlife can flourish in urban areas, an admirable goal for urban dweller but which also enhances the risk of tick-borne disease, especially Lyme disease. In New York City, numerous forested parks and green areas with interconnected vegetated buffers that are interconnected provide opportunities for wildlife to transit between them. In a study by VanAcker et al. (2018), localities with increased connectivity had higher I. scapularis nymph densities and higher risk of tick bites on people. The authors found that the degree of park connectivity strongly determined B. burgdorferi nymphal infection prevalence and concomitant tick-borne disease, especially Lyme disease risk.

A highly fragmented landscape may support higher densities of deer, which benefit from the increased edge habitat due to the presence of preferred forage (Brownstein et al., 2005; Leopold, 1933). In the Northeast, a combination of moderate deer densities (24 to 48 per square kilometer) and fragmentation of forest habitat may mean that questing adult ticks are more likely to find a host, as deer are likely to concentrate there. Halsey et al. (2018) found much higher densities of ticks feeding on all hosts in the Northeast region as compared to Southeast and Midwest regions.

Although white-tailed deer are the major amplifying hosts for the tick populations carrying Lyme disease, migratory birds are one of the major factors contributing to the geographic expansion of the tick’s range. Migratory birds transport vast numbers of immature I. scapularis. Migrating birds flying north along the Atlantic and mid-central U.S. flyways pick up ticks when they stop periodically to rest and forage before continuing northward. In Lyme, Connecticut, Stafford et al. (1995) examined 36 different bird species for the presence of ticks. Of the 4,065 tick larvae and nymphs found on the birds, 94.4% were I. scapularis. The rate of infection with B. burgdorferi in the immature I. scapularis found infesting the birds in this focus of Lyme disease ranged from 14.9% to 20.0%. In Canada, I. scapularis populations have spread into large areas of southern Quebec, Ontario and the maritime provinces. In Ontario, I. scapularis-infested localities are estimated to have expanded at the rate of 46 km/year (Clow et al. 2017).

Opportunities

Recent advances in molecular biology have provided new tools for identifying unique proteins, specific to either the Lyme disease agent, B. burgdorferi, and/or its vector tick, I. scapularis. In addition, new advances in genetics have provided tools for literally changing the structure of genes (gene editing) so that they no longer function (CRISPR-cas9). New vaccines have also been developed, vaccines against specific pathogenic bacterial proteins (for example, LymeRX) or tick body proteins (e.g., BM86), or even an anti-tick vaccine. The sum total of these exceptionally powerful new tools is that it is now possible to deploy them in an integrated tick vector-pathogen management program to greatly reduce tick survival and the disease-causing pathogens they transmit below the threshold of a public health threat.

Methods for implementation (in order of possible risk and benefit)

The Tick Biology Subcommittee identified the following four methods as a means to achieve the goal of eliminating Lyme disease as a public health threat within 20 years.

  1. Create one or more populations of transgenic ticks, I. scapularis, using modern gene editing tools (CRISPR-Cas9) that will be biologically viable, feed and develop normally, but lack the active genes coding for lipocalins, anti-coagulants, and other salivary proteins, all of which are proteins essential for silencing host recognition of the feeding ticks and their full engorgement. This can also be used against TROPSA, the gene responsible for coding the receptor protein essential for bacteria to colonize the juvenile stages. This strategy involves changing the black-legged tick from a competent vector to an incompetent, non-vector species since the eggs deposited by fed females would hatch into larvae unable to acquire the pathogen from mice and other reservoir hosts. Other tick species that co-exist in the same habitats and on the same hosts as I. scapularis (for example, the American dog tick, Dermacentor variabilis) all feed on the same or similar hosts during their juvenile stages, but only the black-legged tick acquires and transmits the Lyme disease bacteria. Gene editing using CRISPR-Cas9 was used recently to disrupt a critically important gene in the silkworm, Bombyx mori, resulting in developmental arrestment and subsequent lethality in third instar larvae. Efforts to genetically engineer malaria-resistant mosquitoes have been in progress since the beginning this century, if not earlier (James, 2003) and genetically-engineered mosquitoes have been deployed recently in malaria-endemic regions of west Africa, with considerable success. The black-legged tick certainly merits similar efforts that would lead to a vector-incompetent population incapable of transmitting Lyme disease.
  2. Vaccinate white-tailed deer. The tools exist to do this effectively, since we have a long-standing, known efficacious vaccine, LymeRX, originally developed for treating humans, that is available today for treating companion animals. The vaccine could be incorporated into liposomes and delivered using the 4-poster self-medicating applicator with corn or similar baits containing the vaccine. Alternatively, a DNA vaccine against TROPSA could be used, which would be directed to the oocytes and block this B. burgdorferi receptor in the F1 generation (i.e., larvae). We could also use reversed antigen sequencing (RAS) to deliver the target molecule, a proven technique previously used in sand flies against Leishmania transmission. Finally, we can deliver tick salivary gland antigens via this same oral route, thereby stimulating antibodies (e.g., anti-lipocalin, an antihistamine) against tick saliva and disrupt adult tick feeding on deer. The 4-poster technique has proved to be highly effective in controlling ticks on deer by administering pesticides such as permethrin but has had limited use because of concerns by state game commissions that it would cause harm to human hunters during the hunt season. However, the oral vaccine would not pose a danger to human hunters since antibodies are generated in the deer and have no activity in humans (in other words, humans do not have the bacterial proteins such as Borrelia OspA). Also, since ticks cannot reproduce without vitellogenin (Vg), incorporating an anti-Vg or vitellogenin receptor vaccine should also be considered as a means to disrupt female reproduction in deer-fed ticks.
  3. Control juvenile tick feeding on small mammals by use of orally administered self-medicating treatment with anti-OspA vaccine against the Lyme bacteria B. burgdorferi (Richer et al. 2014). This is a proven technology, with several years of success in multiple localities.
  4. Control juvenile tick feeding on ground-feeding migratory birds through the administration of an oral self-medicating treatment with anti-OspA vaccine against B. burgdorferi.

In summary, we have the tools to immediately undertake large-scale biological interventions based on vulnerabilities in the tick’s molecular composition and proven anti-tick vaccines.

Threats or challenges to implementation

Gene editing will depend upon the ability of researchers to target the pre-vitellogenic oocytes, fertilized egg, or at best the pre-blastula stage embryo in order to alter the genes of interest before cellular multiplication. Studies to accomplish this goal are in progress in several labs, but additional funding is needed to expand these efforts and shorten the time to delivery.

A major challenge to successful gene editing will arise from public rejection of a transgenic species, as recognized in the tremendous public opposition to gene modified organisms (GMO), such as malaria mosquitoes and crop destroying insects. Hopefully, this can be overcome with education, pointing out that the genetic procedures do not lead to species eradication. Instead, they will lead to tick species that remain as pests but are otherwise harmless because they have been rendered incapable (i.e., not vector competent) of transmitting the agent of Lyme disease. Without vector-competent ticks, Lyme disease will disappear!

Possible Actions for Working Group to Consider

  1. Advise Congress to appropriate the necessary additional funds to the National Institutes of Health, Centers for Disease Control and Prevention and other federal agencies to support the laboratory investigations and subsequent “proof of concept” field trials to implement the goal of eliminating/reducing Lyme disease so to levels of incidence that no longer constitute a public health threat. The cognizant federal agencies can use existing peer-review processes to review proposals, fund meritorious projects and evaluate progress in achieving their goals.
  2. Congress should encourage public-private partnerships to help expedite the progress of these projects and, most especially, commercialize and market the most promising new technologies and/or existing technologies so as to reach the widest possible segments of the populations at risk of Lyme disease in endemic areas in the United States.
  3. Congress should encourage collaborative agreements with public health agencies in Canada to achieve similar goals in neighboring regions in Canadian provinces closest to the United States to ensure elimination of Lyme disease as a public health threat throughout North America, not just in the United States.

Ecology Group Report

Maria Diuk-Wasser, Howard Ginsberg, Stephen Wikel, and Pete Teel

Recommendation 1. Establish a National Tick and Tick-borne Disease Surveillance Network that provides a comprehensive focus upon ticks and tick-borne diseases with financial support for surveillance, data gathering, analysis of change-over-time and future predictions, as well as data dissemination, training and education activities relevant to local, county, state and regional levels using the organizational foundation created by the Centers for Disease Control and Prevention, via the Epidemiology and Laboratory Capacity for Infectious Disease program and the Vector-borne Disease Centers of Excellence.

Recommendation 2. Develop and implement integrated strategies for tick suppression and reduction of tick-borne disease risk with sufficient scope and scale in time and space to assess biological efficacy and operational efficiencies based on sound knowledge of tick and host ecology at the local level, and to utilize findings to educate and train officials, stakeholders and practitioners of best practices.

Background – Recommendation 1 – Tick Ecology Group.

Among arthropod vectors of disease, ticks transmit the most diverse array of infectious agents, and the most important arthropod vectors globally of humans and domestic animal pathogens (Jongejan and Uilenberg, 2004; Colwell et al., 2011; Pfӓffle et al., 2013). Tick-borne infections of humans are zoonoses of wildlife origin, similar to tick transmitted diseases of companion and domestic animal species (Baneth, 2014). Zoonoses are mutually transmissible infections between humans and other animal species (Karesh et al., 2012). Greater than 22 percent of human infectious diseases emerging between 1940 and 2004 were arthropod vector-borne zoonotic infections (Jones et al., 2008). In the United States, approximately 95 percent of reported vector-borne diseases are tick transmitted (Adams et al., 2017).

Dynamic interactions occurring among biotic and abiotic elements influence tick and tick-borne disease ecology and epidemiology on a global scale. The emergence, resurgence, and geographic spread of tick-borne infections are influenced by tick and tick-borne pathogen demography (intrinsic population growth), micro and macro climate, human behavior, travel, landscape, land use, landscape fragmentation, host animal composition and movement (including domestic, wild and exotic species), economics, politics, population growth and movement (Pavlovsky, 1966; Pfӓffle et al., 2013; Baneth, 2014; Dantas-Torres, 2015).

The relative importance of these factors in the emergence of ticks and tick-borne diseases varies over space and time, both in the USA and globally. This dynamic state of flux challenges our ability to predict changes, requiring constant monitoring of the abundance, prevalence and distribution of existing pathogens and detection of new ones through a strong surveillance/monitoring system. A strong understanding of the ecological drivers coupled with constant data acquisition is needed to detect public health threats in a timely fashion, raise public awareness of the threats and develop effective disease and vector control measures (Randolph, 2010; Perez de Leon et al., 2012; Dantas-Torres, 2015; Ostfeld and Brunner, 2015; Stone et al., 2017).

Multiple changes are occurring among the complex associations of biotic and abiotic factors at micro and macro levels that require heightened surveillance of ticks and established, resurging, and emerging tick-borne infectious agents. I. scapularis geographic range expanded significantly in the Eastern and Midwestern United States during the past 20 years (Eisen et al., 2016), from the distribution determined by a standardized collection throughout the Northeastern US (Diuk-Wasser et al 2012). Concomitant with this expanded range is an increase in incidence of reported cases of Lyme disease and other I. scapularis-vectored pathogens (Eisen et al., 2017). Between 1996 and 2016, the number of counties, in which I. scapularis is established, doubled to 44.7 percent of all United States counties (Eisen et al., 2016). Potential geographic range of this tick exceeds the currently described distribution within the United States (Hahn et al., 2016). I. scapularis range expanded into eastern and central Canada by approximately 2004, accompanied by the emergence of Lyme disease (Ogden and Lindsay, 2016). While in the United States, I. scapularis is considered to be reclaiming its historical geographic range in response to changes that include habitat and climate, and availability of hosts for all life cycle stages (Eisen and Eisen, 2018), some areas in Canada may exceed its historic distribution due to anthropogenic climate change . Highlighting the public health importance of this tick, I. scapularis is a competent vector and Peromyscus leucopus a reservoir host for an increasing number of human pathogens: B. burgdorferi, Anaplasma phagocytophilum, Babesia microti, B. miyamotoi, and Powassan virus (Eisen et al., 2017; Eisen and Eisen, 2018).

Amblyomma americanum is a tick of increasing importance due to significantly expanding geographic range, increased population density, and roles as vector of established and emerging infectious agents that include Ehrlichia chaffeensis, Ehrlichia ewingii, and the recently described Heartland and Bourbon viruses (Childs and Paddock, 2003; Godsey et al., 2016; Eisen et al., 2017; Savage et al., 2017). Amblyomma americanum is increasingly important medically due to the ability of its saliva to induce galactose-alpha-1, 3-galactose, alpha-gal, red meat allergy, a significant cause of human anaphylaxis (Platts-Mills et al., 2015). Distribution of this important pest tick was historically described as the southeastern United States to west central Texas and north to Iowa; however, the geographic range now extends into the Mid-Atlantic States and New England as far north as Maine (Keirans and Lacombe, 1998).

Geographic range of the Gulf Coast tick, Amblyomma maculatum, increased significantly within the United States since the first half of the twentieth century (Teel et al., 2010; Sonenshine, 2018). This tick of medical and veterinary importance, particularly associated with Rickettsia parkeri (Summer et al., 2007), was initially limited to the Gulf of Mexico coast from Texas to the Atlantic Ocean coastal South Carolina and as far as 150 miles inland along this zone. Currently, Amblyomma maculatum can be found as far north along the coast of Delaware with a range of greater than 250 miles inland and with populations also established in several Midwestern to southwestern states (Teel et al., 2010; Paddock and Goddard, 2015; Sonenshine, 2018).

An often overlooked driver of tick and tick-borne pathogen emergence is the geographic and demographic expansion and movement of their wild and domestic host populations. Unlike mosquitoes, all stages of ticks are dependent on their hosts for blood meals and they can only move long distance while attached to hosts. Thus, the distribution of ticks is tightly linked to that of the host animals. Global changes, including increasing movement of host animals, directly impact invasive tick species risks to the USA. In the Southwestern US, introgression of the tropical strain of the brown dog tick, Rhipicephalus sanguineus, is associated with a virulent form of Rickettsia rickettsii, causal agent of Rocky Mountain spotted fever (Villarreal et al. 2018; Eremeeva et al., 2011). Amblyomma triste, a vector of Rickettsia parkeri in South America (Venzal et al., 2004) has been confirmed in riparian canyon areas of Arizona and Texas (Mertins et al. 2010) as well as the Mexican border states of Coahuila and Sonora (Guzman-Cornejo et al. 2006). Amblyomma variegatum, the tropical bont tick originally from Africa, remains on many Caribbean islands sustained in part by interisland bird dispersal, and is a threat to both North and South America with risks of Ehrichia ruminantium and Rickettsia africae (Beati et al., 2012; USDA, APHIS Veterinary Services 2008). The recent discovery of the Asian longhorned tick, Haemaphysalis longicornis, in the US and its potential as a vector of several pathogens has impacts for both human and animal health (Beard et al., 2018). The applications of climate-based modelling to predict range expansion of ticks are among tools improving assessment of risks for both ticks and tick-borne diseases (Estrada Pena, 2008). Examples include Haemaphysalis longicornis (Magori 2018; Raghavan et al., 2019), Amblyomma variegatum (Estrada Pena et al., 2007), and Rhipicephalus (Boophilus) microplus (Estrada Pena & Venzal, 2006).

In addition to well-established diseases, multiple emerging tick transmitted pathogens have been described during the past two decades (Eisen et al., 2017; Kernif et al., 2016). Global scope of emerging tick-borne disease causing agents includes Babesia (Vannier et al., 2015), Rickettsia (Parola et al., 2013), Ehrlichia and Anaplasma (Ismail and McBride, 2017), Borrelia (Kernif et al., 2016), and viruses (Kazimírová et al., 2017; Mansfield et al., 2017).

Recognition of the increasing complexity of tick-associated microorganisms is due in part to the application of genomics, functional genomics, next generation sequencing, and proteomics to analyses of tick microbiomes (Tijsse-Klasen et al., 2014; Narasimhan and Fikrig, 2015). Molecular techniques are now used to reverse pathogen discovery by applying these powerful tools for identification of previously unrecognized microorganisms in ticks prior to association of those microbes with disease (Parola et al., 2013). Molecular techniques were the basis for reversed discovery of the following microbes later established to be human pathogens: B. miyamotoi (Branda and Rosenberg, 2013), Neoehrlichia mikurensis (Kawahara et al., 2004), Rickettsia helvetica (Jado et al., 2007), and other Rickettsia species (Parola et al., 2013). These powerful and sensitive approaches is to identify tick associated microbes that are tick symbionts, known disease causing agents, or microbes that have the potential to become emerging pathogens of human and veterinary importance.

Methods – Recommendation 1 – Tick Ecology Group

The CDC Vector-borne Disease Centers of Excellence should provide the central organizational and operational structure to expand in scope of vector and vector-borne disease surveillance, including a focus on ticks and tick-borne diseases. A national network should encompass working relationships across federal, state, and local agencies and vector control districts, university and college centers and institutes, academic institution departments, land grant university agricultural experiment stations, and state, county and local public health departments. The reach and focus of these components and their activities must be to the local community level and be structured for integration of activities based upon tick ecology inherent to the locale. Integral to these core components in the defining and supporting the mission and activities of the network is engagement of stakeholders, advocacy groups, scientists from diverse disciplines, and the general public. Proposed National Network should have a mandate to address all vectors and vector-borne diseases of public health importance. This approach brings together within one framework broad expertise, infrastructure, resources, educational expertise, and the ability to implement integrated control responses to vectors and vector-borne pathogen threats to medical and/or veterinary public health. The nature of disease vectors and the zoonotic nature of many vector-borne, particularly tick transmitted, diseases requires a One Health approach.

Network Mission Relative to Ticks

  1. Develop and implement evidenced-based best practices for national surveillance of tick species, their distributions, and their abundance. Activities will document tick species range, range expansions and contractions, changes in tick species geographic overlaps, identify invasive tick species, assess potential favorable host range, vegetation habitats and the impacts of changing landscapes and environmental factors.
  2. Implement holistic approaches to rural and urban area-wide integrated tick management appropriate to the features and needs of specific areas supported by risk assessment models for vector and disease control decision support systems.
  3. Characterize the microbiomes and viromes of tick species collected during surveillance activities to determine the presence of tick-borne microbes that are established, emerging, and potential future agents of medical and veterinary public health importance. Data sets generated will provide accurate information regarding tick-borne pathogens in specific geographic regions at levels of granularity that are of value to healthcare providers, public health authorities, tick control programs, medical insurance companies, researchers, and the public. All data generated would be freely accessible by interested parties.
  4. Establish network-wide research funding mechanisms that incorporate competitive grants for basic, translational and applied research, and a Small Business Innovation Research type seed support initiative to facilitate commercialization of products for vector and vector-borne disease control.
  5. Develop a broad range of educational and outreach initiatives that increase general public awareness and understanding of vectors and vector-borne diseases, particularly ticks and tick-borne pathogens. This should include tick safety education, training of vector control workers, training for those occupationally exposed, public education, K-12 educational materials, undergraduate and graduate education (M.Sc., Ph.D.) programs with participating universities, and support of post-doctoral fellows. Public education is an important factor in developing the support needed to develop this National Network.

Background – Recommendation 2 – Tick Ecology Group

Tick suppression or removal of ticks from the equation supporting tick-borne pathogens (ticks+hosts+pathogens+habitat+weather/climate=disease risk) also suppresses or eliminates the risk of tick-borne diseases. Tactics that target multiple interactions in this system can be integrated into sound environmental management strategies applied over sufficiently large areas to inhibit tick population growth and dispersal, a concept known as Area-wide Integrated Tick Management. This is best accomplished using practices that reflect local and regional factors that influence tick populations and pathogen transmission patterns. Ecological studies can help identify those factors that are critical for the maintenance of the tick or the pathogen, thus help targeting interventions to the ‘achilles heel’/weakest link in the system. Differences in the importance of various tick-borne diseases in different locales in the United States result from differences in tick species distributions, ecological community types, landscape practices, and structure of the built environment. For example, Lyme disease distribution is affected by geographical patterns of tick distribution (Eisen et al., 2016; Pepin et al. 2012), tick host-seeking behavior (Arsnoe et al. 2019), climate and tick seasonality (Gatewood et al. 2009, Ginsberg et al. 2017, Ogden et al. 2018), and landscape patterns such as habitat type, fragmentation, connectivity, and the built environment (Guerra et al. 2002, Allan et al. 2003, Linske et al. 2018, VanAcker et al. 2019). Research to develop new control technologies and testing in appropriate locales are needed to provide tools for improved management (Eisen et al. 2012, Kilpatrick et al. 2017, Ginsberg & Couret 2019). Tick control would be most effective when interventions are effectively targeted, integrated and implemented on a broad enough scale in time and space to lower disease incidence.

Local and regional vector management programs offer the potential for sustainable programs that would include long-term surveillance of locally-important vectors and pathogens (recommendation 1), allowing well-targeted and optimally-effective management interventions. Local and regional planning and design of tick control programs allows input by local stakeholders (including government agencies and people with interests in public health, environmental conservation, and community planning) to contribute to the design of vector and pathogen management programs. This approach can create public acceptance of appropriate interventions, as well as long-term attention to vector management in local planning and decision-making.

Application of Integrated Tick Management has been demonstrated against both 3-host and 1-host tick species (I. scapularis, Amblyomma americanum and Rhipcephalus annulatus and R. microplus) within agricultural, recreational and urban settings (Bloemer et al., 1990; Mount et al., 1999; Pound et al., 2009; Perez de Leon et al., 2012; Stafford et al 2017). However, long term studies of sufficient spatial scale (area-wide), particularly for 3-host species are needed to assess biological and epidemiological impacts, operational efficiencies and economic benefits, to establish best practices and guides for effective community wide and governmental engagement (Perez de Leon et al., 2014; Stafford et al., 2017). Computer modeling has become a tool for a priori assessment of ecosystem changes impacting tick populations and for applications of tactics and strategies of tick suppression. These programs rely upon fundamentals of tick ecology for each stage of tick development, the variation of ecological elements impacting the system, and upon weather/climate drivers of tick development (Mount and Haile 1987; Wang et al., 2012; Wang et al., 2017). These tools may also be applied to operational planning and biological and operational assessment of program effectiveness.

Methods – Recommendation 2 – Tick Ecology Group

Extensive research on tick control methods have provided diverse approaches to tick management. However, there have been few broad-scale projects that have tested control methods with appropriate controls, and in various combinations with assessment of effectiveness as a function of cost, or of interactions among different control methods. Furthermore, most of these programs are without modeling frameworks to assess cost effectiveness of different interventions. Such studies would allow optimization of Integrated Tick Management programs in terms of cost effectiveness, and should include the interests of stakeholders with regard to environmental effects of the management programs.

  1. Develop and implement long-term, large area-based tick suppression programs utilizing integrated tactics and strategies applicable to the ecology of targeted tick species and within the characteristics of the subject landscape, including geospatial, physical, socioeconomic attributes and governmental organization. This definition is otherwise known as Area-wide Integrated Tick Management.
  2. Assess Area-wide Integrated Tick Management programs for biological efficacy with respect to tick suppression and impact on incidence of tick-borne disease based upon pre-program norms. Assess operational efficiencies and effectiveness for economic cost:benefit analysis. Assess programmatic success and define best practices for expanding applications of Area-wide Integrated Tick Management. A goal is to develop holistic approaches to rural and urban area-wide integrated tick management appropriate to the features and needs of specific areas.
  3. Establish a network of funding mechanisms to support pilot testing of Area-wide Integrated Tick Management programs that includes program level research and assessment to identify and refine best practices and to guide changes in programs for adoption of new technologies.
  4. Continuously evaluate and appropriately incorporate new tick suppression technologies and applications into Area-wide Integrated Tick Management programs to improve program effectiveness.
  5. Establish best practices for building local-based networks of multidisciplinary practitioners to participate in Area-wide Integrated Tick Management programs.
  6. Provide training and guidance for local government participation in implementing and sustaining Area-wide Integrated Tick Management programs, and develop a broad range of educational and outreach initiatives that increase general public- and practitioner awareness and understanding of vectors and vector-borne diseases, particularly ticks and tick-borne pathogens. This should include tick safety education, training of vector control workers and other practitioners, training for those occupationally exposed, public education, K-12 educational materials, undergraduate and graduate education (M.Sc., Ph.D.) programs with participating universities, and support of post-doctoral fellows. Public education is an important factor in developing and sustaining Area-wide Integrated Tick Management programs.

Tick Control Group Report

Kirby Stafford, Trey Cahill, Neeta Connally, Lars Eisen, Lonnie Marcum, Bob Sabatino

Background

The incidence and geographic 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 estimated to occur each year. In the absence of a human vaccine in the U.S. against any of the tick-borne diseases or biting ticks, effective primary prevention relies on reducing exposure to ticks. Blacklegged ticks, Western blacklegged ticks, lone star ticks, American dog ticks, Rocky Mountain wood ticks, Pacific Coast ticks, Gulf Coast ticks, brown dog ticks, and soft bodied ticks all play important roles as vectors of a variety of human, livestock, or companion animal disease-causing agents, with several tick species capable of carrying and transmitting multiple pathogens to humans. The introduction of exotic, invasive ticks with potential new disease agents can pose additional risks to humans and livestock. Identifying and validating effective tick control and tick bite prevention strategies is critical for reducing the incidence of new disease cases, preventing the introduction of new tick species, and limiting the spread of our native ticks. Additionally, in order to track the effectiveness of national prevention and control strategies, as they emerge, it is essential to maintain an accurate understanding of current and potential disease burdens and trends against which to measure success of national prevention goals once established.

Key Questions - What are the challenges for (1) implementation research on single-property scale and area-wide integrated tick management focused on controlling host and vector populations to decrease the risk of tick-borne pathogen transmission; and (2) operational implementation of proven area-wide integrated tick management interventions?

Outcomes - Identifiable causes for an increase in tick-borne diseases to adapt integrated tick management interventions targeting the vector-host-pathogen interface by exploiting vulnerabilities in the biology and ecology of ticks.

Major challenges – Control. Risk for exposure to ticks and tick-borne diseases may be primarily residential, recreational, work related, or a combination thereof with unique challenges. No vaccines are currently available in the U.S. against any tick-borne disease, although a new OspA vaccine for Lyme disease is in Phase 2 trials in Europe and the U.S. Therefore, primary prevention currently relies on methods focused on reducing exposure of people to infected ticks by reducing tick abundance or the prevalence of infection in the tick in the environment combined with use of personal protection measures when spending time in tick habitat. Consequently, the responsibility for tick bite prevention and tick control presently falls squarely on the shoulders of individuals, as organizational structure for local tick control (similar to a mosquito management program operating along well established integrated pest management guidelines) is either lacking or poorly developed and underfunded across the U.S. The toolbox of available methods and products available to protect against biting ticks contain such things as personal repellents, acaricides approved for use on clothing and gear, animals, and properties, landscape management, and personal protective behaviors, with increased attention on integrated strategies (Stafford, Williams, Molaei, 2017). However, not all control measures may be applicable to a particular tick species with different geographic distributions, hosts, ecologies, exposure risk for humans and their animals, and associated pathogens. Moreover, the available data showing that any of the available tools when deployed as directed can actually prevent human illness is very limited (Connally et al., 2009, Eisen and Gray, 2016). Therefore, effective control of ticks and their associated disease agents requires broader acceptance and use of current technologies, improved approaches and additional resources to scale up many of these methods, and the development of an organizational structure for addressing the tick problem at a community-level or broader scale. New methods and products, including those with a One-Health approach, in addition to controlled field trials that measure human outcomes (tick encounters and/or tick-borne disease incidence), are also badly needed. Lastly, 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, underscoring the need for improving science-based tick-borne disease prevention communication.

Results and Potential Actions

A review of the scientific literature and expert presentations by the previous Disease Vectors, Surveillance, and Prevention Subcommittee identified the following crucial needs related to control: 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. These objectives remain crucial. Their review covered the major tick species and methods of preventing tick-encounters or reducing the risk of human tick-borne illness. It is not the purpose of this subcommittee to rehash the catalogue of methods and techniques, but expand upon it to further pinpoint the challenges and barriers to implementation to decrease the risk of tick-borne pathogen transmission and, in addition, how tick management can be targeted to address specific tick vectors and populations at risk. Nevertheless, many of the findings in the earlier report remain relevant and are reaffirmed in this report. The tools reviewed previously that provide the framework for control efforts are listed below and these are examined from the perspective of the biology, ecology, and needs for specific tick species.

  1. Personal protective measures (skin repellents, permethrin-treated clothing, tick checks and bathing or showering). Various personal protective measures could apply to all tick species.
  2. Residential prevention measures (synthetic acaricides, botanically-based acaricides, biological control of ticks, rodent-targeted approaches for tick control, rodent-targeted transmission blocking vaccines, deer fencing, and landscape modifications).
  3. Community-level prevention (deer removal, USDA 4-poster devices, education programs).
  4. Novel tick control measures (TickBot, genetic approaches, anti-tick vaccines, other novel emerging technologies).
  5. Integrated Tick Management for residential or community-level prevention.

Many of the barriers to the adoption or use of tick control and tick bite prevention efforts were previously identified despite overwhelming scientific data that support their safety or effectiveness. These barriers still exist.

  • 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.
  • Lack of municipal/local vector-control efforts specifically aimed at ticks.

Progress in public health has largely been due to improved nutrition, hygiene and sanitation, use of vaccines and antibiotics (CDC 1999). Effective vaccines are available for tick-borne encephalitis (TBE) in Europe and Russia, but recent increase in TBE cases in Europe illustrates the difficulty in maintaining vaccination rates, something seen recently in the measles outbreak in the United States with a decline in vaccination rates in some communities (Patel et al. 2019). An application of an early Lyme disease model of various intervention measures in a hypothetical community found the use of a vaccine and the application of acaricides to deer produced the greatest reduction in human cases of Lyme disease under best case scenarios (Hayes, Maupin, Mount, and Piesman, 1999). The first human Lyme disease vaccine was pulled off the market in 2002 over concerns about adverse reactions and low public acceptance (Schuijt, Hovius, van der Poll, van Dam, Fikrig, 2011). There are several canine Lyme disease vaccines available, but as noted earlier, no human vaccines are currently available in the U.S. for Lyme disease or any other tick-borne disease. Not coincidentally, the only documentation of an impact on cases of Lyme disease, with some caveats (Kugeler, Jordan, Schulze, Griffith, Mead. 2015) has been for community level reduction of white-tailed deer (Kilpatrick, LaBonte, Stafford 2014) or acaricidal treatment of deer (Garnett, Connally, Stafford, Cartter, 2011), the key for these being community level host-targeted interventions. The complete elimination of deer, practical only on geographically isolated islands or similar isolated tracts with community support, has been shown to virtually eliminate the blacklegged tick population (Rand, Lubelczyk, Holman, LaCombe, Smith, 2004). The larger geographic scale of some host-targeted and integrated tick management methods may be analogous to large scale sanitation efforts in the early twentieth century and may be necessary to impact human vector-borne diseases. Nevertheless, with three-quarters of Lyme disease cases probably acquired peridomestically, tick management will likely require a combination of individual property and large-area approaches.

Only recently have tick-control efforts focused on application of multiple methods for controlling ticks in an integrated tick management (ITM) approach, particularly for I. scapularis, which have mainly been conducted at residential properties (Schulze et al., 2007; Stafford, Williams, Molaei, 2017). Some earlier work on ITM looked at combinations of spraying, vegetation management, and deer management (fencing) for the control of the lone star tick, Amblyomma americanum, in a recreational setting (Bloemer, Mount, Morris, Zimmerman, Barnard, Snoddy, 1990). Classic Integrated Pest Management (IPM) involves the selection, integration, and implementation of several pest control actions based on predicted ecological, economic, and sociological consequences. According to the National IPM Roadmap, the purpose of IPM is to:

  • Prevent unacceptable levels of pest damage.
  • Minimize the risk to people, property, infrastructure, natural resources and the environment.
  • Reduce the evolution of pest resistance to pesticides and other pest management practices.

For tick-borne diseases, any part of the epidemiological triad of host, vector, and pathogen and their interactions within the local environment can be the target of control interventions. Tick control or management may have several different objectives: 1) lower direct damage to animals; 2) prevent transmission of tick-borne pathogens to animals; 3) lower nuisance to humans from ticks, and 4) prevent tick-borne disease in humans. There is a difference between control and management, which implies an acceptable level of pest abundance and acceptable level of damage or loss (i.e., for ticks this is either economic gains for livestock or the risk or incidence of disease). The objective of IPM is reduction of the pest level (or pathogen prevalence) below the economic injury level, the density at which the losses (i.e., cost of Lyme disease) exceed the cost of control (cost-benefit or cost-efficacy analysis) (Ginsberg & Stafford 2005). For ticks on livestock or in a recreational area, the purpose of control is to protect a commodity (e.g., cattle) or potential use of a recreational area (e.g., use by tourists) which is easier to define in terms of a cost/benefit analysis. By contrast, for human disease, the level of risk of a tick encounter that is tolerated may be different for recreational areas and residential areas. For some homeowners, acceptable level of risk may be extremely low or cost considerations too high and is more of a ‘bang for the buck’ cost/efficiency paradigm (Ginsberg & Stafford 2005). The costs for tick management interventions can be a restricting factor in acceptance and adoption of various control methods (Gould et al., 2008) and usage of tick prevention or control measures is low (Hook et al. 2015).

ITM approaches can include targeting of 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, can be applied at different spatial scales (individual yards vs. neighborhoods, communities) and may also result in a slower development of pesticide-resistant ticks. The big issues in reducing tick encounters and the incidence of human disease are effectiveness, scale, cost, and implementation. More specifically, some of the questions that this committee feels need to be considered in addressing development and implementation of integrated tick management or best management practices include:

  • What is the range of tick species/pathogens can be impacted by a given intervention, going from extremely narrow (e.g., vaccination of mice or humans against B. burgdorferi) to very broad (e.g., repellents, broadcast application of acaricides)?
  • What spatial scale is impacted by the intervention, going from very limited (e.g., barrier spraying of acaricides along forested ecotones) to broad (e.g., using deer-targeted methods) and scale-free (e.g., applying repellent).
  • Who is responsible for tick control on private properties versus community/public lands, including neighborhood greenbelts, school grounds, and city, county and state parks?
  • How can we deal with low acceptability of many current tick control methods and limited willingness to pay?
  • How should we support implementation and evaluation of current control methods versus development of potential novel technologies that require longer term research?
  • How can we get industry to invest in developing new products for an unclear public health tick control market?
  • How effective are broadcast acaricides when applied by homeowners or Pest Control Professionals?
  • How can adequate funding be secured for additional, larger scale evaluations of ITM approaches with human outcomes?
  • And when we finally have defined an area-wide ITM approach proven to reduce human tick bites and human tickborne illness, can it even be implemented unless we also develop local tick management programs with professional staff?

Repellents can be used for general protection by individuals against tick bites by all tick species. While most have been tested against D. variabilis, A. americanum, and I. scapularis, data is limited or lacking on efficacy for some other tick species. Because using repellents and other personal protective measures rely on individuals to take action every time they encounter outdoor environments, such strategies may not reliably impact tick-borne disease incidence in a population. On the other hand, large scale, long-term suppression of tick populations are likely to be more impactful for addressing the problem of tick-borne disease on a regional or national scale. Considering integrated tactics and strategies that are applicable to the life-cycle and ecology of each tick species, we summarize the status of tick management for each of the tick species of major concern in the United States:

Control approaches and challenges for the major tick disease vectors in the United States

Blacklegged and western blacklegged tick (I. scapularis and I. pacificus). These two species are the primary vectors of the Lyme disease spirochetes B. burgdorferi (I. scapularis in the east and I. pacificus in the far west) and B. mayonii (I. scapularis in the Upper Midwest) as well as the tick-borne relapsing fever spirochete B. miyamotoi (I. scapularis and I. pacificus) and agents causing anaplasmosis (I. scapularis and I. pacificus), babesiosis (I. scapularis), ehrlichiosis (E. muris eauclairensis) (I. scapularis), and Powassan virus encephalitis (I. scapularis) (Eisen et al. 2017). Host-targeted methods with deer have been highly successful in reducing tick abundance and even some documented reduction in Lyme disease cases as previously noted. A few studies have applied integrated methods for reducing tick populations and even a reduction of tick infection prevalence (Schulze et al., 2007; Stafford, Williams, Molaei, 2017). There are currently three studies ascertaining the use of ITM against blacklegged ticks at single vs. clustered residential properties (www.backyardtickstudy.org), in neighborhoods (www.tickproject.org), and in communities (ARS Area-Wide Integrated Tick Management Study), with two of these three studies attempting to ascertain whether an ITM approach can ultimately result in a reduction of human-tick encounters and in human disease incidence.

Because human exposure to ticks is predominately peridomestic (residential) with I. scapularis and most Lyme disease cases are associated with this species, many of the current and newly emerging tools for tick control have been developed and evaluated for control of I. scapularis (Eisen & Dolan, 2016), targeting the questing tick, reservoir hosts for B. burgdorferi (i.e., mice and chipmunks), or reproductive hosts (i.e., deer). Rodent host-targeted methods for topical acaricide application like the tick tube and fipronil-based bait box, each with their strengths and weaknesses, primarily target white-footed mice, the reservoir host for B. burgdorferiB. mayoniiB. microtiA. phagocytophilum, and B. miyamotoi. These products can be important tools in an ITM approach, but probably not as a sole tick control method. A recent comparison of the two methods found that tick tubes provided 28 and 20% control of questing I. scapularis nymphs, 1 yr and 2 yr post-intervention (chipmunks do not use the tick tubes) while the bait boxes resulted in 84 and 79% control 1 yr and 2 yr post-intervention (Jordan & Schulze 2019). A rodent-targeted oral bait Lyme disease vaccine (RTV) under development by U.S. Biologic Inc. also targets the reservoir hosts and has been shown to reduce the prevalence of B. burgdorferi infection in white-footed mice (Richer, Brisson, Melo, Ostfeld, Zeidner & Gomes-Solecki, 2014). Several studies evaluating topical application of tick-killing pesticides on white-tailed deer using U.S. Dept. of Agriculture 4-poster deer treatment stations resulted in significant reductions in host-seeking blacklegged ticks and lone star 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 label restrictions on deployment near residences with children due to safety concerns.

Early surveys showed that residential tick control for I. scapularis was largely limited to applications of synthetic acaricides by professional applicators (Schulze et al. 1997; Stafford 1997). Area application of synthetic acaricides continues to be the primary and most efficacious method of tick control for homeowners (Eisen & Dolan 2016), with increasing interest in botanically-based, all “natural” products for controlling ticks due to environmental concerns. While synthetic pyrethroids offer the longest-lasting, most effective backyard control of blacklegged ticks, it is important to note that misuse or poor application can result in poor tick control, 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). Natural products, largely based on the U.S. Environmental Protection Agency (EPA) 25b minimum risk list, are appealing to the public because of perceived low toxicity to humans, pets, and the environment and appealing to commercial developers because they do not require registration with the EPA or proof of efficacy to add to the pesticide label. Lack of efficacy can potentially lead to false sense of protection and greater risk of tick bite and disease. As a result, marketed products may come and go, making timely evaluations of efficacy a challenge for academic researchers. Issues with botanically-based acaricides include:

  • No or limited efficacy data, exempted from testing for toxicity, some may be toxic at higher doses, irritants, or allergens.
  • Differences in tick species and stage susceptibility.
  • Variable and “unknown” composition of essential oils depending on source, plant species, extraction method, etc.
  • Efficacy of oil vs. specific components of the plant extract or oil (e.g., nookatone, carvacrol).
  • Volatility and lack of persistence, requiring frequent applications.
  • Phytotoxicity.

Nootkatone from Alaskan yellow cedar and grapefruit essential oil has been found effective as a killing agent for I. scapularis in the field (Bharadwaj, Stafford, & Behle, 2012; Eisen and Dolan, 2016) and for multiple tick species in the laboratory (Flor-Weiler, Behle, & Stafford, 2011). It has also 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. Nootkatone is being developed under the name ‘NootkaShield™’ by Evolva under license from the CDC; the registration of nootkatone as a biopesticide is under review by the EPA. How botanically-based products are formulated may impact efficacy. In a study of a botanical acaricide and its active ingredients against larvae of Rhipicephalus (Boophilusmicroplus, only geraniol exhibited acaricidal properties in a product containing rosemary oil, geraniol, peppermint oil, wintergreen oil, white mineral oil, vanillin, and polyglyceryl oleate (Singh et al., 2018). Rosemary oil and peppermint oil failed a dose-mortality response and the high response to the commercial product was attributed to synergism among the principal ingredients and other components present in the product. More work is needed on formulation chemistry and efficacy of botanical-based acaricides. Fungal biopesticides also provide a promising alternative to synthetic acaricides. Field studies evaluating tick-killing Metarhizium anisopliae (Mbrunneum) fungi (Met52) 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 has been and is currently the primary broadcast agent being used in several of the ITM studies mentioned earlier. A combination of the Met52 and fipronil rodent bait boxes reduced the risk of encountering questing nymphal ticks by 78-95% and single infected blacklegged ticks by 66% (Williams et al. 2018). However, the efficacy of this combination approach against other rodent-associated tick species has not been evaluated.

Current Tools and Challenges for Control of Blacklegged Ticks

  • The widest diversity and most current tools for tick control have been developed for I. scapularis.
  • Substantial reductions in the abundance of host-seeking ticks has thus far shown little to no documented impact on human tick bites or human
  • There is a lack of target thresholds for tick suppression at the local (private), municipal, and state levels.
  • Similarly, analogous to vaccination thresholds needed for “herd” protection, it is unknown at what level residential (e.g., percent household participation) and community level implementation of tick management interventions is needed to reduce human tick bites or human disease.

Lone star tick (Amblyomma americanum). This species is the primary vector of multiple pathogens causing ehrlichiosis (Ehrlichia chaffeensisEhrlichia ewingii, and Panola Mountain Ehrlichia) and has also 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). The lone star tick also was implicated as the vector of Borrelia lonestari, the putative agent of southern tick associated rash illness (STARI); and was 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 the Rocky Mountain spotted fever (RMSF) agent (Levin, Zemtsova, Killmaster, Snellgrove, & Schumacher, 2017), the vector competence of lone star ticks for these disease agents remains unproven (Childs & Paddock, 2003; Stromdahl & Hickling, 2012). With increasing abundance in its “native” range in the southeastern United States and geographic expansion northward, control of this aggressive tick has become increasingly important.

Most studies on control of the lone star tick were conducted in the 1970s through 1980s, many evaluating organophosphate acaricides that are no longer used for area-wide tick control, host management and/or vegetation management. With the focus on blacklegged ticks and Lyme disease, there have been relatively few studies on the management of this tick in recent years, at least in comparison to I. scapularis. Vegetation reduction has been shown to reduce the abundance of Aamericanum (reviewed by White & Gaff 2018). The combination of vegetative management, host management (deer exclusion), and application of the organophosphate chlorpyrifos in an integrated study reduced lone star ticks by up to 96% (Bloemer et al. 1990). Deer exclusion also impacted Aamericanum on Long Island (Ginsberg, Butler & Zhioua, 2002). With white-tailed deer a principal host for all stages of the tick (Paddock & Yabsley, 2007), the ARS-USDA 4-poster has been found to significantly reduce the abundance of lone star ticks (Brei et al., 2009; Carroll et al., 2003; Pound, Miller, George, & Lemeilleur, 2000; Schulze, Jordan, Hung, Schulze, 2009). With appropriate dosing, ivermectin-treated corn has also been shown to control A. americanum (Pound, Miller, George, Oehler, Harmel, 1996) as well as I. scapularis on white-tailed deer (Rand, Lacombe, Holman, Lubelczyk, Smith 2000). Ironically, ivermectin is a U.S. Food and Drug Administration (FDA)-approved treatment for several human parasites and has been used to treat millions of people for onchoceriasis (González et al. 2008; Ōmura 2008), but current withdrawal requirements limit or prevent its use for the control of ticks on deer. Doramectin is used on cattle for control of cattle fever ticks, but also has withdrawal restrictions. By contrast, rodent targeted techniques such as the tick tubes and bait boxes for I. scapularis hosts would not affect lone star ticks since they do not readily use rodent hosts (Zimmerman et al. 1987). Some research has been done more recently with current synthetic acaricides and botanically-based acaricides against A. americanum (Schulze, Jordan, Hung, Taylor, Markowski & Chomsky 2001; Dolan et al., 2009; Jordan, Dolan, Schulze & Piesman 2011; Jordan, Schulze, Eisen & Dolan, 2017). While primary exposure to A. americanum by humans has probably been primarily recreational in the past, it is increasingly becoming a residential issue as well as the tick expands its range into more densely populated areas along the northern Atlantic seaboard (Stafford, Molaei, Little, Paddock, Karpathy, Labonte, 2018). This tick is the dominant species submitted to the Army Public Health Center from southern installations for identification and testing from enlisted personnel, civilian employees and their families (Robyn Nadolny, Tick-Borne Disease Lab and DOD Human Tick Test Kit Program Update. Online Powerpoint presentation to Tick IPM Working Group, October 10, 2017).

Current Tools and Challenges for Control of Lone Star Ticks

  • Regulatory restrictions on use of ivermectin for control of ticks on livestock and deer
  • Limited studies on the efficacy of current acaricides and biopesticides for control of Aamericanum
  • Lack of integrated tick management (ITM) approaches for lone star ticks in residential settings

American dog tick (Dermacentor variabilis). This species is the primary vector of the bacterium that causes Rocky Mountain spotted fever (Rickettsia rickettsii), and is also known to transmit the agent of tularemia (Francisella tularensis). However, infection rates with R. rickettsii in D. variabilis have been extremely low. The American dog tick has a broad distribution, spanning the entire U.S., though this tick has a disjunct western distribution along the Pacific Coast of the U.S. and an extensive eastern distribution that extends from Canada to the Gulf of Mexico, west into Kansas and Nebraska and into Colorado (Lehane, Parise, Evans, Beati, Nicholson, & Eisen, 2019). As noted in the previous subcommittee report, there have been few recent studies evaluating existing control methods. There are even fewer evaluations of control methods against D. variabilis than A. americanum (White & Gaff 2018) and what few exist also date from the 1980s using organophosphates (White, Benach, Smith & Ouyang 1981). Sonenshine & Haines (1985) found a bait box treating rodents with an insecticidal dust or oil reduced nymphal and larval American dog ticks on the rodent hosts. However, there has been little focus on evaluating the impact of newer tick tubes or bait boxes on D. variabilis. Early modeling of management strategies examined area-wide acaricide applications, acaricide baited tubes, reduction of small mammal hosts, dipping of dogs, use of canine collars, and removal of vegetation (Haile, Mount, & Cooksey 1990) with multiple acaricide applications or a combination of baited tubes, host management and vegetative management reducing tick abundance below targeted thresholds, supporting an ITM approach.

Current Tools and Challenges for Control of American Dog Tick

  • Limited data on the incidence of tick bite encounters with American dog ticks and current importance in the transmission of human disease agents.
  • Lack of studies on the efficacy of current acaricides for control of D. variabilis.
  • No development for, or evaluation of, emerging tick control technologies for D. variabilis.

Gulf coast tick (Amblyomma maculatum). Historically, this tick was limited to coastal areas of the southeastern U.S., Central and South America; however, it now also occurs in states along the Atlantic coast as far north as Virginia and Delaware (Nadolny and Gaff 2018), as well as in the south central U.S. as far north as Oklahoma and Kansas (Teel, Ketchum, Mock, Wright & Strey 2010; Paddock & Goddard, 2015). It was considered primarily a livestock pest causing weight and blood loss in cattle and a condition called gotch ear in cattle and other animals. The tick is the principal vector for hepatozonoosis, a severe and potentially fatal disease in dogs. The Gulf Coast tick can acquire and transmit Ehrlichia ruminantium, the causal agent for heartwater in wild and domestic ruminants. Paddock & Goddard (2015) emphasized the importance of A. maculatum as a potential vector for this disease if the pathogen is introduced through the “importation of exotic animals from Africa or by tick-infested migratory birds from islands in the Caribbean”.

This aggressive tick is also the major vector of a mild, spotted-fever-like illness caused by Rickettsia parkeri in humans and can cause tick paralysis (Paddock & Goddard 2015). Similar to some Dermacentor spp. ticks, it is the adult ticks that parasitize humans and transmit the agents of human disease (and may often be confused with Dermacentor ticks). This tick is associated with grass dominated and successional habitats, not forest, and a better understanding of these open habitats, their relation to urban and suburban developments and human exposure risks is needed (Nadolny and Gaff 2018). Compared to other tick species, there is relatively little information on the control of the Gulf Coast tick.

Current Tools and Challenges for Control of the Gulf Coast Tick

  • Research is needed to better understand the urban and suburban ecology of this tick, human exposure risks, and transmission of R. parkeri.
  • Evaluation of appropriate current tick management tools for A. maculatum to control human exposure to this tick is needed.
  • Efforts to monitor for the potential introduction of E. ruminantium need to be maintained and enhanced.

Rocky Mountain Wood tick (Dermacentor andersoni) and Pacific Coast tick (Dermacentor occidentalis). The distributions of these two ticks appear to have remained stable over time. The Rocky Mountain 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; James et al. 2015). 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, Francisella tularensis (Burgdorfer, 1969). It also is the cause of tick paralysis. The Pacific coast tick is found throughout western California and Oregon. It transmits a spotted fever group rickettsia (Rickettsia philipii or Rickettsia 364D) to humans, causing Pacific Coast tick fever. Similar to D. variabilis, there have been few recent studies evaluating existing control methods and limited data on the incidence of tick bite encounters with these ticks and current importance in the transmission of human disease agents.

Brown dog tick (Rhipicephalus sanguineus). The brown dog tick has a worldwide distribution, although recent studies suggest that this species sensu lato likely comprises a complex of species (Dantas-Torres et al., 2013). Dogs are the primary host for R. sanguineus and the tick can transmit R. rickettsii to both dogs and humans. Found indoors (for example, in dog kennels) in northern latitudes, populations can survive and breed successfully in nature and in human dwellings across the entire the southern U.S., but mainly in areas where canine hosts are readily available. The adult stage is the main vector to humans. Climate warming could increasingly affect the role of the brown dog tick in human disease as R. sanguineus ticks exposed to high temperatures were found to attach more readily to humans (Parola, Socolovschi, Jeanjean, Bitam, Fournier, Sotto, Labauge & Raoult, 2008). On Native American reservations in Arizona, a population of this species has transmitted Rocky Mountain spotted fever group rickettsia to humans and was managed through a successful One-Health ITM community approach using long-acting tick collars (w/ flumethrin & imidacloprid), peridomestic acaricide spraying, and spay and neuter programs (Drexler et al., 2014). Given that dogs are the primary host, most research has focused on control of R. sanguineus (and other tick species) on dogs with the development of pet ectoparasite control products (flea/tick collars, topical sprays, spot-on’s, and newer oral parasiticides). Applications of these products along with treating areas where dogs are present are the main methods of control to reduce the risk for human exposure (Biggs et al. 2016). However, permethrin resistance and fipronil tolerance has been reported in R. sanguineus (Eiden, Kaufman, Oi, Allan & Miller, 2015).

Current Challenge for Control of the Brown Dog Tick

  • Translating the now proven One-Health ITM approach into a sustainable tick management program.

Soft ticks (Ornithodoros species). There are several species of ticks in the genus Ornithodoros associated with tick-borne relapsing fever (TBRF) in the western United States, primarily O. hermsiO. turicataO. parkeri, and O. talaje. Each is associated with its own relapsing fever spirochete: Borrelia hermsiiB. turicataeB. parkerii, and B. mazzotti, respectively. Humans mainly encounter these ticks in rodent- and tick-infested rustic cabins while sleeping (Johnson, Fischer, Raffel, & Schwan, 2016) or caves. Ornithodoros hermsi is the primary vector of one of the two principal North American agents of tick-borne relapsing fever (TBRF, that is, B. hermsii in humans (Lopez, Krishnavahjala, Garcia, & Bermudez, 2016), which circulates sylvatically in rodents. Control efforts through rodent management and application of interior acaricides usually occurs following the occasional outbreaks at vacation cabins, although some tick control may be conducted preemptively.

Asian longhorned tick (Haemaphysalis longicornis). The Asian longhorned tick is native to temperate regions of eastern Asia, where it has been implicated as a vector of Japanese spotted fever and severe fever with thrombocytopenia syndrome (SFTS) in humans. In its native habitat, as well as in Australia and New Zealand where it is invasive, the Asian longhorned tick is also an important pest of livestock. Heavy infestations of cattle, sheep, goats, horses and other agricultural animals can cause a high degree of morbidity and mortality, including decreased milk production in dairy cows. In addition, the Asian longhorned tick’s capacity to transmit a variety of veterinary disease agents, including bovine Babesia, Anaplasma, and Theileria species, and equine Babesia species (Heath 2002), make the tick an important species of economic concern worldwide. Recently discovered in the United States on a New Jersey sheep farm in 2017, the Asian longhorned tick has since been detected in nine U.S. states, both in the environment and parasitizing a variety of hosts, including livestock and companion animals, humans, white-tailed deer, and several other mammal and avian species (Beard et al. 2018). The capacity for this exotic tick to transmit new or existing local pathogens to humans and livestock in the U.S. is not yet well-understood, and needs more study. Worldwide, control recommendations for the Asian longhorned tick include pasture mowing and vegetation management (Heath 2016), treatment of infested livestock with ectoparasiticides such as isoxazolines and macrocyclic lactones, and environmental application of acaricides, including organophosphates and synthetic pyrethroids (USDA 2019). It should be noted that the efficacy of ectoparasiticides and acaricides available in the United States have not yet been evaluated for North American populations of Asian longhorned ticks.

Current Tools and Challenges for Control of the Asian Longhorned Tick

  • Research is needed to better understand the general ecology of H. longicornis in North America, including seasonal activity, and host preferences of the different life stages, factors influencing dispersal, human and livestock exposure risks, and transmission of medical, veterinary, and wildlife pathogens.
  • Evaluation of current tick management tools for H. longicornis to control human and veterinary exposure to this tick is needed, using a One-Health ITM approach.
  • Efforts to monitor the distribution and spread of invasive H. longicornis need to be maintained and enhanced.

Potential Actions:

  1. Develop species-specific vector control plans.
  2. Develop action plans to improve monitoring for invasive ticks, minimize the risk of invasive ticks entering the U.S. and to track and rapidly abate or manage establishing invasive species, if possible.
  3. Promote best practices on the use of acaricides that minimize risk for pollinators and minimizing negative environmental impacts (such as groundwater pollution and other non-target effects).
  4. Establish efficacy standards for 25b exempt products targeting public health pests.
  5. Enhance tick awareness and science-based tick-bite prevention and tick control education.
  6. Demonstrate that area-wide ITM approaches can reduce human tick bites and human tick-borne illness while also minimizing non-target effects and pesticide resistance.
  7. Develop a framework and guidelines for evaluating pesticide resistance in ticks of veterinary and medical importance.
  8. Incorporate or integrate ITM methods into the current commercial pest control model and support commercial development of new effective tick control products.
  9. Create a training program for professionally-staffed and adequately-resourced local tick management programs to operate using IPM principles and with responsibility for surveillance of ticks and tick-borne pathogens, public outreach, and management of ticks on publicly and privately owned lands, possibly through homeowner incentives.
Content created by Office of HIV/AIDS and Infectious Disease Policy
Content last reviewed on January 23, 2020