Than independently to process a site from ticks and mosquitoes

Tick Bites: Symptoms & Treatment

Ticks bites are a scourge of summer, but they don’t have to be. There are ways to avoid these arachnids, as well as safe ways to remove one that does embed itself in your skin.

Ticks can transmit diseases, such as Lyme disease and Rocky Mountain spotted fever, so it’s worth steering clear of bites, if possible.

What are ticks?

There are around 850 species of ticks worldwide, according to researchers in the department of entomology at the University of California, Davis. These critters range in size from nearly invisible to the size of a pencil eraser.

Most ticks go through four life stages, growing larger as they age, according to the Centers for Disease Control (CDC). All ticks start out as eggs and most then turn into tiny larvae with three pairs of legs (adult ticks have four pairs). A larva becomes a nymph — a smaller version of an adult tick. Finally, the nymph takes its final form as an adult tick, with males typically appearing smaller in size than females of the same species.

In order to complete this complex life cycle, ticks must take a blood meal (i.e. suck on an animal’s blood) at every stage, according to the CDC.

“Usually the immature ticks take a blood meal on mice, birds and other small animals,” said Dr. Gary Wormser, the chief of the Division of Infectious Diseases and head of the Lyme Disease Center at New York Medical College in Valhalla, New York. But adult ticks prefer larger hosts, like deer or, in some cases, humans, he added.

Many ticks only take one blood meal for every stage of their life cycle. After an adult’s final blood meal, it will mate — if it’s a female it will also lay eggs after mating — and then die, Wormser told Live Science.

Ticks are most common in humid climates, and are usually found in scrubby or grassy places where animal hosts are likely to pass by. Contrary to popular belief, they can’t leap from a blade of grass onto a host’s skin; rather, they hang on to the plant with their rear legs and hold their front legs aloft, waiting for something to brush by so they can grab on. This behavior is called “questing,” according to the CDC.

Many ticks won’t bite right away, instead preferring to search for a spot with thin skin. They like warmth, and often head for places like the groin, armpit or hair, according to the NIH. For this reason, it’s a good idea to check yourself for ticks as soon as you get indoors (or even periodically while you’re outside), so you can brush off any that haven’t yet latched on.

Tick prevention and removal

It’s no fun to cover up when the sun is hot, but long sleeves and long pants are good protection against ticks. The insecticide permethrin can be sprayed on clothing or gear (not on the skin), and kills ticks on contact, according to the New York Department of Health. (Some outdoor clothes come pre-treated with permethrin.) Deet is also an effective repellant. As a bonus, both of these chemicals keep mosquitoes away, too.

Check yourself and any pets for ticks after coming in from outdoors, particularly if you’ve been in woody or grassy areas. If you do find a tick attached to your skin, use fine-tipped tweezers and grab the arachnid as close to the skin as possible. Pull upward evenly and steadily. The goal is to remove the tick whole, without breaking its mouthparts off in your skin.

However, if the tick’s “head,” or mouthparts, can’t be removed, there’s no need to worry too much, according to Wormser.

“The tick really does cement itself into your skin, and it isn’t always possible to remove those parts right away,” Wormser said. “They’ll remove themselves, like a splinter, on their own.”

You should never try to use chemicals to remove a tick, according to the CDC. And it’s an equally bad idea to try to burn a tick that is attached to your body, said Wormser, who also advised against any kind of “invasive surgical procedures” to try to remove a tick. These remedies are more likely to make the tick cling tighter, rather than let go.

After you remove the tick, clean the site of the bite with soap and water, use rubbing alcohol or iodine to disinfect the wound, and then let it heal, according to the National Institutes of Health (NIH). Wormser recommends saving the tick that bit you in a jar or plastic baggie. You can then bring the tick with you to a healthcare professional who may be able to determine the species of the tick and how long it was attached to your body. If you’re at risk of developing a tick-borne illness, a doctor may be able to prescribe you with antibiotics before the onset of symptoms, Wormser said.

Tick-borne illnesses and symptoms

In addition to recovering the tick that bit you, it’s also a good idea to know what ticks live in your region, according to the CDC. Both adult and nymph ticks of certain species can cause disease, and being able to identify which species bit you could help you avoid panic after a bite.

The CDC offers an overview of the range of the most common tick species in different regions of the contiguous United States. Maps of the areas most affected by ticks carrying Lyme disease are provided by the American Lyme Disease Foundation.

According to the CDC there are three common signs of tick-borne illness. They are:

  • Fever and/or chills
  • Aches, pains and fatigue
  • Rash

Rashes will appear differently depending on the pathogen that’s been introduced to the body through a tick bite. Lyme disease rashes may be in the shape of a bull’s eye pattern surrounding the site of the bite and can appear anywhere from three to 30 days after a tick bites you. Southern tick-associated rash illness (STARI) causes a similar rash to Lyme’s disease, but the appearance of rashes caused by Rocky Mountain spotted fever — as well as other tick-borne illnesses — can vary widely from person-to-person, according to the CDC.

It’s important to see a healthcare professional who is familiar with tick-borne illnesses to accurately determine the cause of your symptoms. Keep a close eye on the site of the bite after the tick is gone. If a rash appears, or if you come down with a fever, see a doctor and be sure to mention the bite and where you picked up the tick.

The illnesses transmitted to people from ticks are caused by bacterial infections. The best known is likely Lyme disease, which is caused by bacteria called Borrelia burgdorferi. Most Lyme disease infections happen in the Northeast, the Pacific Northwest and in Wisconsin and Minnesota, according to the NIH.

“If you don’t treat a patient who comes in with a [Lyme] rash, it will go away on it’s own in about four weeks. However, about 80 percent of patients will not remain completely well over the course of time. A few percent will develop heart problems. About 10 to 15 percent with develop neurologic involvement [such as partial paralysis] and about 60 percent will develop arthritis,” Wormser said.

Wormser also noted that he frequently warns patients that, just because a rash associated with Lyme disease has gone away, that doesn’t mean they’re completely healed. Ongoing symptoms like aches, pains and fatigue can continue for anywhere between several weeks and six months, according to Wormser.

Another common tick-borne illness is Rocky Mountain spotted fever, which actually occurs most frequently in the eastern United States. Caused by the bacteria Rickettsia rickettsi, this disease also begins with chills, fever and pain, and progresses to include symptoms such as diarrhea, nausea, vomiting and even hallucinations. Treatment with antibiotics usually cures Rocky Mountain spotted fever, according to the NIH.

“When you get [a] disease from a tick bite, you may also get other tick-borne infections at the same time. There are at least four other tick-borne infections that you can get simultaneously in the Northeast or independently, without getting Lyme, from the same tick.”

One of these infections is called babesiosis, Wormser added. This infection is caused by bacteria and typically results in flu-like symptoms and, in some cases, a condition known as hemolytic anemia in which red blood cells are destroyed, according to the NIH. Babesiosis can be especially dangerous for people over the age of 50, as well as people with compromised immune systems, according to Wormser. CDC officials also warn that babesiosis is on the rise in the Northeast and the Midwest.

Additional reporting by Stephanie Pappas, Live Science Contributor

www.livescience.com

Disease Vectors, Surveillance, and Prevention

Report of the Disease Vectors, Surveillance, and Prevention Subcommittee 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.

Background

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

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

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

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

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

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

Key Issues and Priorities

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

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

The subcommittee discussed the issues, primarily adding, combining, and editing the draft list that was provided prior to the February 23 call. Once all the changes had been captured and the call was concluded, the revised list was sent out by e-mail to subcommittee members for additional comments and finalization. The finalized list (Table 1 below) was then distributed to the subcommittee by e-mail with the request that each subcommittee member select the top six issues, place them in ranked order, and send them by e-mail back to the subcommittee co-chairs for collation. The issues were placed in rank order based on the combined scores of the subcommittee members. During the process, it was observed by multiple subcommittee members that several of the issues in each theme could be combined. Consequently, the co-chairs selected related issues, combined them, and re-ranked them based on the subcommittee members’ votes. The top five issues were selected and placed into Table 2 (below).

On Friday, March 2, 2018, the subcommittee met again by conference call to review all the changes that were made to Table 1 and the final list of the top five issues in rank order that were used to develop Table 2. Both Table 1 and Table 2 were voted on and approved by unanimous vote of the subcommittee to be included in the first report. Both Tables 1 and 2 are included below. Of note, the five priorities listed in Table 2 reflect equally high priorities to the subcommittee and are not weighted in terms of their importance.

Table 1-: Improving Issues relevant to the Disease Vectors, Surveillance, and Prevention Subcommittee: Complete List of Issues that Could Be Addressed in First Report to Congress

Issues:

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

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

Issues:

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

Issues:

  1. What tools are currently in our toolbox for tick population control and disease prevention and how extensively have they been evaluated?
  2. How can prevention education be improved, including providing accurate information and removing both personal and public obstacles?
  3. What are the most promising novel prevention tools that are on the horizon (eg. transgenic ticks and other novel molecular interventions such as RNAi)?
  4. How do we encourage commercialization of effective prevention tools and products?
Key Theme 1 – Disease Vectors
Key Theme 2 – Human Surveillance
Key Theme 3 – Prevention

Table 2. Improving Issues relevant to the Disease Vectors, Surveillance, and Prevention Subcommittee – Prioritized List of Issues that Will Be Addressed in the First Report to Congress

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

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

C. Ben Beard, MS, PhD

Deputy Director, Div. Vector-Borne Diseases, CDC

40+ years of experience working in vector-borne disease prevention and control, including 27 years at CDC; has published over 130 articles, books, and book chapters collectively on infectious diseases with an emphasis on vector-borne diseases.

Patricia (Pat) Smith

Family member; Advocate (non-profit)

President, Lyme Disease Association, Inc. Jackson, NJ; Member, CDMRP Programmatic Panel; Member, Columbia Lyme & Tick-Borne Diseases Advisory Committee

physician CME education; Staff/student school education; public education on ticks/TBD; Congressional & state testimonies; reviews & awards research & education grants; provides patient support; written brochures & on surveillance issues; developed maps/graphs on case numbers, 30 years’ experience.

Founder: Tick Research to Eliminate Disease, & also Stop Ticks On People, New York

organized many educational presentations for community on prevention, ticks, the environment; presented educational classes; presented to local, state/federal officials about the need for tick prevention research; chaired Community Advisory Board in work on 3 year CDC grant to County Department of Health, IPM work group member.

Neeta Connally, PhD, MSPH

Associate Professor, Tick-Borne Disease Prevention Laboratory, Western CT State

vector ecology; epidemiology of tick-borne diseases; Director, WCSU Tickborne Disease Prevention Laboratory.

Katherine Feldman, DVM, MPH

Senior Epidemiologist, MITRE

tick-borne disease work for state/federal health agencies 18 yrs.; conducting and evaluating public health surveillance for Lyme & TBD; led public health investigations/responses to TBD.

Thomas N. Mather, PhD

Professor, Center for Vector-Borne Disease; Director, TickEncounter Resource Center (RI)

professor of entomology; 35 years research on tick biology, ecology, & control; tick bite prevention; anti-tick vaccine; Tick Encounter Resource Center website; TickSpotters crowd sourced tick survey/response.

Phyllis Mervine, MA

President, LymeDisease.org (CA)

30 years of collaboration on studies in northern California; experience as science writer and editor; career as a patient advocate; promoting public education/patient empowerment and keeping up with the research.

Robyn Nadolny, PhD

Program Coordinator, Tick-Borne Disease Laboratory, Army Public Health Center

8 years’ experience in tick/TBD research; 16 peer-reviewed publications; field biology/ecology, tick ecology, population, establishment; tick-host interaction; tick survival in environment; tick surveillance; tick testing.

Adalberto (Beto) Perez de Leon, DVM, PhD, MS

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

32 yrs. experience: discovery & product development in animal health, arthropod pest management, vector-borne diseases, biotechnology, (ticks/TBD), technological innovation in pesticide science, mechanism-based screening to discover safer parasiticides, veterinary drug delivery systems, anti-tick-vaccines, and VBD molecular diagnostics, genomics research to develop anti tick measures.

Daniel E. Sonenshine, PhD

Eminent Professor of Biological Science, Old Dominion University

200 peer-reviewed publications on ticks and tick-borne pathogens of disease in humans and animals; book “Biology of Ticks;” patented technologies pheromone-assisted methods for tick control; professor biological sciences; chapter co-author on ticks/TBD in Medical & Veterinary Entomology.

Jean I. Tsao, PhD

Associate Professor, Departments of Fisheries and Wildlife and of Large Animal Clinical Sciences, Michigan State University

Eco-epidemiology of tick-borne pathogens; emergence of ticks and tick-borne pathogens; geographic variation in Lyme disease ecology and risk.

Patient, Family member, Advocate (nonprofit)

President/Co-founder, Colorado Tick-Borne Disease Awareness Association (CO)

wildlife biologist US Forest Service (former career employee); member Public Tick IPM Working Group; TBD public conference provider; tick collection experience.

Stephen Wikel, PhD

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

45 yrs. immunology of tick-host-pathogen interactions: cellular & molecular biology, biochemistry, genomics; T-B pathogen interactions w/host defense; tick colonies, tick-infection methods w. TB pathogens; federal review & advisory committees.

Table 2 Overview of Disease Vectors, Surveillance, Prevention Meetings

Type Stakeholder Group Expertise
Co-Chairs

February 23, 2018

Thomas N. Mather

Adalberto Perez de Leon

Daniel E. Sonenshine

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

Thomas N. Mather

Adalberto Perez de Leon

Daniel E. Sonenshine

Roll call; Introduction of Dr. Neeta Connally and presentation Prevention; PowerPoint presentation; Q and A for Neeta; Priority Charge (Table 2)—Explanation of how discussion will proceed; Discussion and consensus/vote on the prioritized list; Next steps in the process; Announce next meeting date: March 8, 2018, 2:00PM-4:00PM; Announce Bob Lane as a speaker for March 23, 2018 meeting; Call for adjournment.

Thomas N. Mather

Daniel E. Sonenshine

Roll call; Discussion of next phase of report; Nominations of suggested Priority List Coordinators by Co-Chairs; Discussion of List & Volunteers for each List; Begin Writing Process; Table 2 Priority– Brainstorm, flesh out (see also Outline Subcommittee Report p.2c.iv.1a-e); Next meeting date 3/16/18 2-4; Call for Adjournment 4:00PM.

Thomas N. Mather

Adalberto Perez de Leon

Daniel E. Sonenshine

Roll call; Vote: 1st Draft Background/Methods Report to be submitted; Updates from HHS; Full Subcommittee Discussion on Priority Group 2; Full Subcommittee Discussion on Priority Group 3; Full Subcommittee Discussion on Priority Group 4; Next meeting date 3/23 /18 2-4, Bob Lane presenting & Priority Group 5; Call for Adjournment 4:00PM.

5

Thomas N. Mather

Daniel E. Sonenshine

Roll call; Introduction of Robert (Bob) Lane, PhD; Lyme Disease in California, Ecology & Epidemiology & presentation; Q & A for Robert Lane; Updates from HHS; Full Subcommittee Discussion on Priority Group 5; Update Background report 1st draft & vote to accept; Next meeting date 3-28-18, 2-4PM ET; Call for Adjournment 4:00PM.

Thomas N. Mather

Adalberto Perez de Leon

Daniel E. Sonenshine

Roll call; HHS updates; Putting Pen to Paper: Results Sections for Each Priority – Questions About this document; Role of Results document in 5 priority topics; Next meeting April 6 (reports ready); Call for adjournment 3:00 PM

Thomas N. Mather

Adalberto Perez de Leon

Daniel E. Sonenshine

Roll call; Any HHS updates; Any required action to be taken; Discussion and questions on writing 1st draft Results section; Next meeting April 13; Call for Adjournment

Thomas N. Mather

Roll call; Any HHS updates; Discussion and questions on Results 1st draft; Vote on Draft to be submitted by co-chairs; Vote on Proposed actions for working group to consider; Next meeting April 20; Call for Adjournment

Thomas N. Mather

Adalberto Perez de Leon

Daniel E. Sonenshine

Roll call; Any HHS updates; Discussion and questions on Results 1st draft; Vote on Draft to be submitted by co-chairs; Vote on Proposed actions for working group to consider; Next meeting Thursday April 26 Call for Adjournment 4:00PM

Thomas N. Mather

Adalberto Perez de Leon*

*either entered late or left early & may have missed a vote(s)

Roll call; Any HHS updates; Discussion and questions on Results Final; Vote on Issues/Questions & priorities; Vote on final background report; Vote on final methods report; Vote on final results written report to be submitted by co-chairs; Vote on final proposed actions for working group to consider; Closing remarks; 4:00 PM Adjournment

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

Meeting No. Date Present Topics Addressed

Paul Meade, MD, MPH

Chief, Bacterial Branch, DVBD, Centers for Disease Control & Prevention

Surveillance for Lyme in US; public health surveillance; state role; CSTE; Lyme surveillance case definition; Nationally notifiable disease surveillance system; case stats; underreported; disease burden vector distribution; canine Lyme.

Neeta Connally, PhD, MSPH

Tickborne Disease Prevention Laboratory, Dept. of Biological & Environmental Sciences, Western CT University

Tick-Borne Disease Prevention in the Northeastern US; tick habitat; personal protection; repellent effectivity; showering; permethrin; property management; rodent targeting; ITM; IPM; prevention sources.

Robert Lane, PhD

Prof. Emeritus of Med. Entomology, Dept. of Environmental Science, Policy & Management, UC Davis, Berkeley

Lyme Disease in California: Ecology and Epidemiology; history & burden of Lyme in CA; research objectives; spirochetes in CA; ticks & distribution; vertebrate hosts; maintenance & reservoir hosts; birds; risk factors & behavior; seasonal activity; nymphs vs. adults; habitat.

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

Meeting No. Presenter Topics Discussed

Approve issues and priorities section 1st draft of the report for submission to the Working Group

Approve 1st draft methods section of report for submission to Working Group

Approve 1st draft background section of report for submission to Working Group

Approve 1st draft Results section of report for submission to Working Group

Approve Recommendations to working group in Results

Consent agenda all recom.

Approve Final version Results Report & All Recommendations

The overall subcommittee report was approved unanimously, with 2 minority reports (12-0-1A).

Each of the five sections was approved unanimously

(1 absent entire meeting, see Meeting 10 in table above for attendance variations)

2 Minority reports

3-7-2abstain-1A (p4 prevention programs priority action)

4-7-2A (p3 surveillance used for diagnosis)

Results and Potential Actions

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

Topic 1. The need for improved vector surveillance

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

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

Evidence and Findings

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

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

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

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

Possible Opportunities

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

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

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

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

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

Threats or Challenges

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

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

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

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

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

Evidence and Findings

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

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

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

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

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

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

Images will be available in this report in the near future.

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

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

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

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

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

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

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

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

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

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

Possible Opportunities

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

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

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

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

Threats and Challenges

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

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

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

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

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

Evidence and Findings

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

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

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

Opportunities

Potential opportunities include:

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

Threats or Challenges

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

Topic 4. Vector competence and vectorial capacity

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

Evidence and findings

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

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

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

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

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

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

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

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

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

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

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

Opportunities

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

Potential Actions

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

Images will be available in this report in the near future.

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

Votes of Subcommittee Members

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

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

Meeting or Date Motion Result Minority Response

10

0

0

3*

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

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

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

Evidence and Findings

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

Another rodent-targeted intervention focuses upon the passive application of tick-killing fipronil onto mice and chipmunks as they visit the Tick Box™ Tick Control System (formerly Select TCS™ and MaxForce™ Tick Control systems). Field studies evaluating the boxes have prov >

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

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

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

Community-level prevention

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

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

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

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

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

Novel tick control methods on the horizon

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

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

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

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

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

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

Opportunities

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

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

Threats or Challenges

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

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

Potential Actions

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

Votes of Subcommittee Members

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

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

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