Benefits and Drawbacks of Citizen Science to Complement Traditional Data Gathering Approaches for Medically Important Hard Ticks (Acari: Ixodidae) ...
←
→
Page content transcription
If your browser does not render page correctly, please read the page content below
Journal of Medical Entomology, XX(X), 2020, 1–9 doi: 10.1093/jme/tjaa165 Forum Forum Benefits and Drawbacks of Citizen Science to Complement Traditional Data Gathering Approaches for Medically Important Hard Ticks (Acari: Ixodidae) in the Downloaded from https://academic.oup.com/jme/advance-article/doi/10.1093/jme/tjaa165/5890085 by guest on 20 December 2020 United States Lars Eisen1 and Rebecca J. Eisen Division of Vector-Borne Diseases, National Center for Emerging and Zoonotic Infectious Diseases, Centers for Disease Control and Prevention, 3156 Rampart Road, Fort Collins, CO 80521, and 1Corresponding author, e-mail: evp4@cdc.gov Subject Editor: Sarah Hamer Disclaimer: The findings and conclusions of this study are by the authors and do not necessarily represent the views of the Centers for Disease Control and Prevention. Received 27 May 2020; Editorial decision 8 July 2020 Abstract Tick-borne diseases are increasing in North America. Knowledge of which tick species and associated human pathogens are present locally can inform the public and medical community about the acarological risk for tick bites and tick-borne infections. Citizen science (also called community-based monitoring, volunteer moni- toring, or participatory science) is emerging as a potential approach to complement traditional tick record data gathering where all aspects of the work is done by researchers or public health professionals. One key question is how citizen science can best be used to generate high-quality data to fill knowledge gaps that are difficult to address using traditional data gathering approaches. Citizen science is particularly useful to generate infor- mation on human–tick encounters and may also contribute to geographical tick records to help define species distributions across large areas. Previous citizen science projects have utilized three distinct tick record data gathering methods including submission of: 1) physical tick specimens for identification by professional ento- mologists, 2) digital images of ticks for identification by professional entomologists, and 3) data where the tick species and life stage were identified by the citizen scientist. We explore the benefits and drawbacks of citizen science, relative to the traditional scientific approach, to generate data on tick records, with special emphasis on data quality for species identification and tick encounter locations. We recognize the value of citizen science to tick research but caution that the generated information must be interpreted cautiously with data quality limitations firmly in mind to avoid misleading conclusions. Key words: Ixodidae, citizen science, tick data collection, tick surveillance Background agent are whether or not 1) a human-biting tick species capable of transmitting the pathogen in question is present in the local environ- Tick-borne diseases are increasing in North America (Rosenberg et al. ment and 2) the pathogen occurs in the local populations of one or 2018). Major human-biting ixodid tick species—Ixodes scapularis several human-biting vector tick species. Most areas of the United Say, Ixodes pacificus Cooley and Kohls, Amblyomma americanum States where human populations are concentrated harbor at least one (L.), Amblyomma maculatum Koch, Dermacentor variabilis (Say), commonly human-biting vector tick species (Eisen et al. 2017, Eisen Dermacentor andersoni Stiles, Dermacentor occidentalis Marx, and and Paddock 2020) and many states are home to several different Rhipicephalus sanguineus sensu lato (Acari: Ixodidae)—collectively human-biting vector species (Merten and Durden 2000, Jordan and serve as vectors for more than 15 human pathogens, ranging from Egizi 2019). Notably, distributions of medically important ticks and viral to bacterial and parasitic agents (Eisen and Paddock 2020). The their pathogens change over time, necessitating ongoing data col- most basic risk factors for human exposure to a tick-borne disease lection. Up-to-date knowledge of which tick species and associated Published by Oxford University Press on behalf of Entomological Society of America 2020. This work is written by (a) US 1 Government employee(s) and is in the public domain in the US.
2 Journal of Medical Entomology, 2020, Vol. XX, No. XX pathogens are present in the local environment and when each tick Tick surveillance is often classified as active versus passive but as life stage is actively host-seeking is helpful for outreach campaigns some tick collection methods do not easily fit into this classification to inform the public and medical community about when and where scheme, we prefer to use more descriptive terms when describing people are at risk for exposure to ticks and tick-borne pathogens. different collection approaches. Table 1 summarizes key character- Additionally, human behavior strongly influences the risk for tick istics of different approaches for collection of ticks and detection of bites (Hook et al. 2015, Eisen and Eisen 2016, Aenishaenslin et al. pathogens in the ticks, focusing on factors that describe how tick and 2017, Stafford et al. 2017, Mead et al. 2018, Fischhoff et al. 2019, pathogen data are generated and influence how they can be inter- Jordan and Egizi 2019). These fundamental facts, together with the preted. The initial dichotomy is whether the tick collection method is understanding that geographic distributions and population dy- ‘fully quantitative’, yielding both a numerator and a denominator, or namics of vector ticks are dynamic (Randolph 2004, Ogden et al. ‘opportunistic and semi-quantitative’, producing quantitative data Downloaded from https://academic.oup.com/jme/advance-article/doi/10.1093/jme/tjaa165/5890085 by guest on 20 December 2020 2018, Sonenshine 2018, Gaff et al. 2020), must be considered when for only the numerator or denominator. Examples of outcome meas- deciding how to most effectively improve our knowledge of where, ures from commonly used tick collection methods producing fully when, and why humans are bitten by ticks potentially carrying quantitative results include the number of host-seeking ticks col- disease agents. lected per trap-day or unit area/time covered by walking, dragging, In this Forum article, we explore how citizen science may be or flagging samples; the number of ticks collected per live or recently used to complement traditional tick data collection, where all killed wild or domestic animal; or the number of recorded tick bites aspects of the work are conducted by researchers or public health or tick encounters per person and unit of time for participants in a professionals, to improve the understanding of risk for human research study where such information is specifically recorded. There bites by potentially pathogen-infected ticks. Two basic themes are is a plethora of publications describing the results of such tick collec- of crucial importance when exploring this topic: 1) data quality, tion methods from North America and Europe. including for tick species identification, pathogen detection meth- Tick collection methods best defined as opportunistic and semi- odology, and spatial precision of the tick encounter location, quantitative based on quantitative data being collected for the nu- and 2) judicious interpretation of information to account for merator (number of ticks recovered) while the denominator remains the limitations of the methodology used to generate the data. We unknown include 1) submission from the public of ticks collected first outline basic characteristics of different methods to gather from humans to public service tick identification or tick identification tick-associated data and then discuss how this relates to citizen and pathogen detection programs, where the number of individuals science. that were aware of the program and would have submitted ticks had they been encountered are unknown (Walker et al. 1998; Johnson et al. 2004; Rand et al. 2007; Xu et al. 2016, 2019; Nieto et al. 2018; Characteristics of Different Approaches to Jordan and Egizi 2019; Little et al. 2019; Elias et al. 2020); and Gathering Tick-Associated Data 2) opportunistic recovery of ticks from livestock or pets by members Epidemiological public health surveillance refers to the ongoing, sys- of the public or veterinarians during daily activities or routine health tematic collection, analysis, and interpretation of health-related data checks, without knowledge of the total number of animals that were (Thacker and Birkhead 2008). The term surveillance is used more examined for presence of ticks (Jaenson et al. 1994; Tälleklint and loosely in relation to ticks and pathogens found in ticks. Systematic Jaenson 1998; Walker et al. 1998; Guerra et al. 2001; Johnson et al. tick sampling and pathogen detection efforts are often of short du- 2004; Ogden et al. 2006, 2010; Raghavan et al. 2007; Rand et al. ration, for example as part of research projects, rather than ongoing 2007; Hamer et al. 2009; Rhea et al. 2011; Abdullah et al. 2016; activities spanning many years or decades. However, compilation of Hendricks et al. 2017; Laaksonen et al. 2017; Cull et al. 2018; Lee these short-term studies can reveal significant trends (Dennis et al. et al. 2019; Saleh et al. 2019; Chilton et al. 2020). Another tick col- 1998, Springer et al. 2014, Eisen et al. 2016, Lehane et al. 2020). lection method best defined as opportunistic and semi-quantitative Examples from the United States of long-term surveillance efforts, is the recovery of ticks from road-kill animals (Lorusso et al. 2011, spanning 4 to >20 years, include collection of host-seeking ticks in Szekeres et al. 2018), where the denominator can be quantified as fixed sampling sites in Maine (Elias et al. 2020), Minnesota (Bjork the number of examined animals but where an unknown proportion et al. 2018), and New York (Prusinski et al. 2014; New York State of ticks may have already dislodged from the carcasses before they Department of Health [NYSDOH] 2020a,b), and submission of were recovered and examined for ectoparasites. ticks recovered from humans or domestic animals to tick identifi- Another important factor to consider is whether the ticks were cation or tick identification and pathogen testing service programs collected while seeking a host versus recovered from a host, in- in Connecticut (Little et al. 2019, Little and Molaei 2020), Maine cluding wild animals, domestic animals, or humans (Table 1). This (Rand et al. 2007, Elias et al. 2020), Massachusetts (Xu et al. 2016), distinction has implications both for the spatial interpretation of the Michigan (Walker et al. 1998), New Jersey (Jordan and Egizi 2019), tick collection record and the detection of pathogens in the ticks. Rhode Island (Johnson et al. 2004), the Pacific Coast states (Xu et al. Collection of host-seeking ticks from the environment provides re- 2019), or U.S. Army bases across the eastern United States (Rossi cords with very high spatial precision for the location where the tick et al. 2015). Similar long-term surveillance programs for host-seeking was contacted, regardless of whether it was collected by drag or flag ticks or ticks recovered from humans or domestic animals have been sampling (the drag/flag is checked at regular, short intervals based on implemented in Canada (Ogden et al. 2006, 2010; Ripoche et al. distance traveled or time elapsed), during walking sampling (cover- 2018; Gasmi et al. 2019; Chilton et al. 2020) and Europe (Garcia- alls are checked at regular, short intervals based on distance traveled Marti et al. 2017a, b, 2018; Cull et al. 2020; Springer et al. 2020). or time elapsed), or via trapping (ixodid ticks have limited capacity Moreover, efforts are underway in the United States to strengthen for horizontal movement toward a stimulus). The geographical loca- the national capacity for systematic and sustained surveillance of tion where contact was first made between a tick and the host it was human-biting ticks and their associated disease agents (Centers recovered from is more challenging to determine as it depends on the for Disease Control and Prevention [CDC] 2018, 2020; Eisen and spatial activity range of the host species and the time elapsed since Paddock 2020). the tick encountered the host. The spatial precision for the initial
Table 1. Key characteristics of different approaches for collection of ticks and detection of pathogens in the ticks Classification of tick collec- Source of ticks Examples of tick collection methods Spatial interpretation in relation to source of recovered Pathogen interpretation in relation to source of recovered tick tion approach tick Fully quantitative (numer- Environment Systematic collection of host-seeking ticks Fine-scale determination of tick encounter location Infection indicative of transstadial passage of pathogen following ator and denominator) by dragging/flagging or walking while infectious blood meald wearing coveralls; or by tick trapping Fully quantitative (numer- Wild animals Systematic tick collection from captured Tick encounter location falling somewhere within the Not clear if the tick already was infected before the blood meal ator and denominator) vertebrates or hunter-killed deer spatial activity range of the host species the tick was or acquired the pathogen while feeding; not indicative of collected from transstadial passage of pathogene Fully quantitative (numer- Livestock (e.g., Systematic tick collection from a defined Tick encounter location falling within readily defined Not clear if the tick already was infected before the blood meal ator and denominator) cattle, sheep, and livestock population host movement range, unless livestock were moved or acquired the pathogen while feeding; not indicative of goats) by vehicle during the time period when tick encounter transstadial passage of pathogene may have occurred Fully quantitative (numer- Pets (cats, dogs, and Systematic tick collection from a defined Tick encounter location difficult to interpret without Not clear if the tick already was infected before the blood meal ator and denominator) horses) pet animal population travel and activity history for the time period when or acquired the pathogen while feeding; not indicative of the tick encounter may have occurred transstadial passage of pathogene Fully quantitative (numer- Humans (crawling Systematic tick collection from a defined Tick encounter location difficult to interpret without Infection very likely indicative of transstadial passage of pathogen ator and denominator) or attached ticks) human population travel and activity history for the time period when following previous infectious blood meal for both crawling the tick encounter may have occurred and attached ticksf Opportunistic; semi- Environment Opportunistically collected host-seeking Fine-scale determination of tick encounter location pos- Infection indicative of transstadial passage of pathogen following Journal of Medical Entomology, 2020, Vol. XX, No. XX quantitative (numerator ticks submitted by members of the sible if submission includes notes on collection loca- infectious blood meald only) publica tion (e.g., in submitter’s backyard) Opportunistic; semi- Wild animals Opportunistic tick collection from road- Tick encounter location falling somewhere within the Not clear if the tick already was infected before the blood meal quantitative (denomin- killed animalsb spatial activity range of the host species the tick was or acquired the pathogen while feeding; not indicative of ator only) collected from transstadial passage of pathogene Opportunistic; semi- Livestock (e.g., Opportunistic tick collection from live- Tick encounter location falling within readily defined Not clear if the tick already was infected before the blood meal quantitative (numerator cattle, sheep, and stock via veterinary clinic networks host movement range, unless livestock were moved or acquired the pathogen while feeding; not indicative of only) goats) during routine animal health activitiesc by vehicle during the time period when tick encounter transstadial passage of pathogene may have occurred Opportunistic; semi- Pets (cats, dogs, and Opportunistic tick collection from pets by Tick encounter location difficult to interpret without Not clear if the tick already was infected before the blood meal quantitative (numerator horses) members of the public or via veterinary travel and activity history for the time period when or acquired the pathogen while feeding; not indicative of only) clinic networks during routine animal the tick encounter may have occurred transstadial passage of pathogene health activitiesc Opportunistic; semi- Humans (crawling Opportunistic tick collection via medical Tick encounter location difficult to interpret without Infection very likely indicative of transstadial passage of pathogen quantitative (numerator or attached ticks) clinic networks during routine health travel and activity history for the time period when following previous infectious blood meal for both crawling only) activities; opportunistically collected the tick encounter may have occurred and attached ticksf ticks submitted by members of the public to tick identification/pathogen testing service programsc a Numerator (number of collected ticks) can be quantified but there is no denominator due to lack of a systematic sampling design. b Denominator for number of examined animals can be quantified but an unknown proportion of attached ticks may have already dislodged from road-killed carcasses before they were recovered and examined for ectopara- sites, therefore the numerator for number of infesting ticks cannot be reliably quantified. c Numerator (number of collected ticks) can be quantified but there is no denominator because the number of potential tick hosts from which ticks would have been recovered were the hosts infested is unknown. d With the following exceptions: 1) infection of host-seeking larval ticks with a pathogen that can be passed transovarially from the female to her offspring; and 2) infection in ticks having taken only a partial blood meal and seeking a second host to take sufficient additional blood to be able to molt to the next life stage or lay eggs. Host-seeking nymphs or adults infected with a pathogen that can be passed transovarially from the female to her offspring represent another special case where infection is indicative of transstadial passage but not necessarily of a preceding infectious blood meal for the individual tested tick. e Not all wild animal species, livestock species, or pet species serve as reservoirs for a given tick-borne pathogen; pathogen detection result should be interpreted bearing in mind the reservoir competency of the host animal for the pathogen in question. f Humans are considered dead-end hosts for tick-borne pathogens. 3 Downloaded from https://academic.oup.com/jme/advance-article/doi/10.1093/jme/tjaa165/5890085 by guest on 20 December 2020
4 Journal of Medical Entomology, 2020, Vol. XX, No. XX tick encounter location is high for host species with limited activity 24-h rainfall or snowfall—are straightforward and can be measured ranges (for example, livestock confined to a pasture or rodents) but and recorded using simple, standardized equipment. The question less spatially distinct for mammals with larger home ranges (for ex- then becomes to what extent such general beneficial aspects of a suc- ample, deer and medium-sized carnivores) and resident or, especially, cessful citizen science program can be translated to efforts involving migrating birds. For people and pets, there is the added challenge collection of data on human-biting ticks. of needing to account for travel history when attempting to pin- At the time of this writing, the online catalog of federally funded point the likely geographical location where a tick found crawling citizen science programs (https://www.citizenscience.gov/catalog/#) or attached was first encountered. For attached ticks, the degree of includes two projects specifically focused on mosquitoes and engorgement can be useful to estimate the duration of time (number mosquito-borne disease (‘The Invasive Mosquito Project: A Public of days) elapsed since the tick found its host and attached (Piesman Education Tool’, sponsored by the U.S. Department of Agriculture, Downloaded from https://academic.oup.com/jme/advance-article/doi/10.1093/jme/tjaa165/5890085 by guest on 20 December 2020 and Spielman 1980, Yeh et al. 1995, Falco et al. 1996, Gray et al. and ‘U.S.-Mexico Border Early Warning Disease Surveillance for 2005, Meiners et al. 2006). Dengue and Chikungunya’, sponsored by the Centers for Disease As outlined in Table 1, the source of the collected ticks also Control and Prevention). Citizen science is playing an increasing role influences the interpretation of detected pathogens. For a path- in research on the distribution of mosquito species of medical im- ogen detected in a fed tick (of any life stage) recovered from an portance and their control, with recent studies from North America animal host, it often is not clear whether the tick was infected be- (Maki and Cohnstaedt 2015, Jordan et al. 2017, Johnson et al. 2018, fore starting to feed or if it acquired the pathogen while feeding. Tarter et al. 2019) as well as Europe (Kampen et al. 2015, Heym Not all wild animal species, livestock species, or pet species serve as et al. 2017, Palmer et al. 2017, Walther and Kampen 2017, Eritja reservoirs for a given tick-borne pathogen; the pathogen detection et al. 2019), Africa (Murindahabi et al. 2018), and Australia (Braz result therefore should be interpreted bearing in mind the reservoir Sousa et al. 2020). competency of the host animal for the pathogen in question as well The online catalog of federally funded citizen science programs as whether the pathogen is passed transovarially in the tick spe- does not currently include any projects involving ticks or tick- cies in question. Moreover, as noted previously for Lyme disease borne diseases but there are examples of projects run by academic spirochetes (Eisen 2020), pathogens acquired during a blood meal institutions, non-profit organizations, and county, state, or federal may be passed transstadially through the molt for some, but not entities where tick data or tick specimens provided by members of all, tick species that infest reservoir animals. Pathogen detection in the public/citizen scientists were used to further the knowledge of host-seeking nymphs or adults has the clear advantage of indicating human-biting ticks. Three different approaches were used in these that the pathogen survived the molt and was present in the tick as projects to identify ticks that members of the public found crawling it sought a new blood meal host. The final consideration then be- on or biting people or pets: 1) physical submission of ticks to profes- comes whether the tick species in question is capable of transmitting sional scientists for tick identification and, in some cases, pathogen the transstadially passed pathogen while taking a blood meal: this detection, 2) submission of digital tick images to professional scien- is often, but not always, the case across combinations of tick and tists for tick identification, and 3) submission of tick information pathogen species. where species and life stage identification was done by the citizen scientist submitter with various aids, such as online guides showing images of different tick species and life stages. Citizen Science and Tick Collection Records One example from the first category of projects involving mem- As outlined in the Crowdsourcing and Citizen Science Act of 2016 bers of the public is a study from Sweden in the early 1990s where (15 USC 3724), citizen science is increasingly recognized by fed- the public was engaged to submit collected ticks—including the eral agencies in the United States as an approach with potential to primary human-biting tick in Sweden, Ixodes ricinus (L.)—to a re- accelerate the generation of research data. An official government search project where the professionally identified ticks then formed website (https://www.citizenscience.gov/#) was developed to catalog part of the overall database to define the geographical distributions federally supported citizen science projects and provide resources of ixodid and argasid tick species across the country (Jaenson et al. to connect researchers with citizen science coordinators and prac- 1994). Requests for physical tick submissions from the public for the titioners. There are different definitions for the term citizen science specific purposes of the collection records to inform which tick spe- (also known as community-based monitoring, volunteer monitoring, cies and life stages bite humans or pets or to form part of a database or participatory science), but common themes include the participa- to define the broad geographical distributions of tick species (and in tion of non-scientists in data collection, compilation, and/or anal- some cases also the associated pathogens found in the ticks) were ysis, most often in collaboration with formally trained academic or also employed by other researchers in the United States, Canada, federal scientists (Cohn 2008, Kullenberg and Kasperowski 2016, and Europe (Smith et al. 1992, Walker et al. 1998, Goddard 2002, Bartumeus et al. 2018, Hamer et al. 2018). The longest standing cit- Ogden et al. 2006, Gleim et al. 2016, Laaksonen et al. 2017, Cull izen science project in the United States is the Cooperative Observer et al. 2018, Lewis et al. 2018, Nieto et al. 2018, Jongejan et al. 2019, Program operated by the National Weather Service (NWS) of the Lernout et al. 2019, Porter et al. 2019, Saleh et al. 2019, Salkeld National Oceanic and Atmospheric Administration. Non-scientist et al. 2019, Chilton et al. 2020). volunteers have documented local weather-related data for this fed- Another primary reason for requesting physical tick submis- eral program for more than a century since its launch in 1890 (NWS sions from the public has been the establishment of service programs 2020). Two important aspects of this highly successful citizen science that, freely or at-cost, provide professional tick identification serv- program to aid in local weather data collection are that: 1) it allowed ices, and sometimes also pathogen detection services, and commu- for logistically feasible and minimal cost measurement of weather nicate the findings back to the individual submitters. Examples of data across a large number of localities long before weather stations non-commercial entities in the United States that have provided such were capable of automated measurements and 2) the core data col- public service programs over time periods spanning many years in- lected—including daily maximum and minimum temperatures and clude the Connecticut Agricultural Experiment Station (Little et al.
Journal of Medical Entomology, 2020, Vol. XX, No. XX 5 2019; Little and Molaei 2020; Connecticut Agricultural Experiment molecular assays that compare sequence data to reference sequences. Station [CAES] 2020a,b), the Maine Medical Center Research Using other methods, the expected likelihood of a correct identifica- Institute (Rand et al. 2007, Elias et al. 2020), the Monmouth County tion falls to moderate–high when the professional scientist identifies Mosquito Control Division (Jordan and Egizi 2019), the New the tick from a submitted digital image (the identification is influ- Hampshire Department of Agriculture, Markets & Food (https:// enced by both the quality of the image and the level of experience www.agriculture.nh.gov/divisions/plant-industry/tick-identification. of the person viewing it) and to low when the identification is made htm), the Texas Department of State Health Services (https://www. by a citizen scientist without formal training. In a real-world sce- dshs.texas.gov/idcu/health/zoonosis/tickBites/), the University of nario, ticks often have been attached for some period of time before Rhode Island Tick Research Laboratory (Johnson et al. 2004), the being detected and removed, and also may have been damaged in University of Massachusetts, Amherst (Xu et al. 2016, 2019), and the removal process. Compared with unfed ticks, partially or fully Downloaded from https://academic.oup.com/jme/advance-article/doi/10.1093/jme/tjaa165/5890085 by guest on 20 December 2020 the U.S. Army Public Health Command (Rossi et al. 2015). Data engorged ticks may be more difficult to identify without access to a obtained from ticks submitted by citizens to such public service tick high-quality stereo microscope. In scenarios that also include detec- identification/pathogen detection programs have secondarily been tion of pathogens in submitted ticks, typically done via detection of used to 1) clarify which tick species and life stages bite humans, when pathogen genetic material, additional concerns include the quality of during the year peak human-biting occurs, and where on the human the pathogen detection algorithm and the level of experience of the body tick bites most often occur; 2) describe changes over time for laboratory staff. Testing of ticks for presence of human pathogens annual numbers of human bites by different tick species; and 3) as- is done across a wide range of federal, state, academic, and private sess whether data on human bites by vector ticks can predict spatial laboratories but, as noted in a recent national survey on tick surveil- and inter-annual patterns of tick-borne disease case incidence. lance and control practices (Mader et al. 2020), there is currently no The best example of the second category of programs involving certification or accreditation process to ensure a quality standard for members of the public, where the tick itself is not submitted but the pathogen detection results. rather identified by a professional entomologist from a digital image Another important consideration when compiling a geograph- provided by a member of the public together with tick encounter ical database with the intent of generating a tick distribution or information, is the TickSpotters service provided through the abundance map is the distinction between absence of the tick and University of Rhode Island TickEncounter Resource Center (https:// lack of data records. In compilations of national scale data to gen- tickencounter.org/; Kopsco et al. 2020). The final category, where erate county-level distribution maps for key human-biting ticks in members of the public identify the encountered ticks themselves the United States, we therefore use the categories of established, re- and provide data on species and life stage together with additional ported, and no records (Dennis et al. 1998, Springer et al. 2014, information relating to the tick encounter, is represented by online Eisen et al. 2016, Lehane et al. 2020). Due to lack of standardized data collection tools such as the Vermont Tick Tracker (https://apps. national surveillance for ticks in the United States until very recently health.vermont.gov/vttracking/ticktracker/2019/d/index.html) and (CDC 2018, 2020; Eisen and Paddock 2020; Mader et al. 2020), recently launched apps such as the The Tick App (https://thetickapp. some counties located within model-projected distributions for a org/; Fernandez et al. 2019) and the TickTracker App (https:// given tick species but lacking tick presence records likely fall in the livlymefoundation.org/ticktracker-app/). In the sections below, we category of no tick records due to inadequate tick collection efforts place these existing approaches to engage the public in gathering of rather than the tick species truly being absent. From a public health tick-related data into the broader context of how citizen science best standpoint, incorrect depiction in a map of tick absence for an area can help improve our knowledge of tick distributions and how to where the tick species actually is present is problematic because it prevent tick bites and tick-borne disease. may lead to decreased vigilance for use of personal protective meas- ures to prevent tick bites. As long as a high-quality tick identification method is used, tick Incorporation of Citizen Science-Derived records resulting from efforts involving citizen scientists have clear potential to help fill in gaps in existing tick distribution maps, espe- Information Into Tick Record Databases and cially in areas where a tick species is present but rare and therefore Tick Distribution and Abundance Maps may not be easily recovered during routine drag/flag sampling- Maps are a means for sharing graphical information on where a based tick surveillance efforts. Such involvement by citizen scien- given tick species can be encountered or for depicting acarological tists are similar to the previously mentioned Cooperative Observer risk of encountering ticks; the accuracy of the presented map di- Program operated by the National Weather Service, as the citizen rectly reflects the quality of the data used to generate the map. This scientist tick collections facilitate data gathering across a greater is equally true for maps based on data for actual tick records and number of specific locations than otherwise possible. However, it is maps showing model-derived projections for tick presence or abun- important to follow up citizen science-derived tick species records dance. Because tick records are generated in a variety of contexts, of special interest with drag/flag sampling to confirm that the given there is a need to decide which data to include versus exclude in tick species indeed is present in the local environment. This specific a database being compiled for the specific purpose of generating strategy was used to complement backyard adult mosquito collec- maps depicting spatial tick distributions or tick abundance patterns. tions by citizen scientists in the Netherlands, where mosquito re- Primary considerations include 1) the perceived quality of the spe- cords of special interest, for example the invasive Aedes japonicus cies and life stage identification for the tick record and 2) the source japonicus (Theobald), were followed up by additional collection ef- from which the tick was recovered to inform whether or not the tick forts targeting larval or adult mosquitoes in the local environment record is relevant at the level of spatial granularity a map depic- (Walther and Kampen 2017). tion aims to achieve. The expected likelihood of a correct tick spe- Ticks recovered from people or pets (especially dogs) come with cies and life stage identification is very high when the tick specimen the added challenge of travel potentially masking the actual location is physically accessible for examination by a professional scientist where the tick encounter occurred. Unless detailed travel histories trained in tick identification or if the specimen is identified using are available for the period of time when the tick encounter may
6 Journal of Medical Entomology, 2020, Vol. XX, No. XX have occurred, and bearing in mind that people often underestimate ticks (larger and easier to spot compared to immatures) and tick the amount of time a tick has been attached before it is discovered species with more noticeable bites (for example, ticks with longer (Sood et al. 1997, Logar et al. 2002, Wilhelmsson et al. 2013), the mouthparts). Conversely, as indicated by Lyme disease patients often tick encounter location may not always be reliably determined even being unaware of a tick bite preceding the onset of symptoms (re- at the coarse county scale. A similar problem with determining finer- viewed by Eisen and Eisen 2016), the immature stages of some tick scale tick encounter locations occurs for ticks recovered from wild species—including I. scapularis for which the nymphs are recognized mammals with large home ranges and birds, especially during their as the primary vectors of Lyme disease spirochetes to humans—are migration seasons. very likely underrepresented in collections from human hosts. This The quality of information included in a database for geograph- limitation, together with potential uncertainty in the spatial location ical tick records is strongly influenced by the characteristics of the where the tick was initially encountered, must always be considered Downloaded from https://academic.oup.com/jme/advance-article/doi/10.1093/jme/tjaa165/5890085 by guest on 20 December 2020 tick identification process, together with the spatial precision for the when interpreting data on ticks recovered from humans. Long-term initial tick encounter location. Overall, the highest quality data are data sets on ticks recovered from humans are especially valuable as represented by ticks that were physically accessible to a professional they can provide crucial insights into human–tick encounters, not scientist for species identification (molecular or morphological) and only for the general seasonal patterns for encounters with different where the collection method allows for fine-scale determination of tick species and life stages, and where on the human body most bites the host-seeking location of the tick specimen (for example, drag occur, but also for changes over time to the tick species most com- sampling with locations of the drag samples recorded). Further clas- monly encountered by humans and the prevalence of pathogens har- sifications that downgrade the overall quality of a tick record (for bored by different tick species recovered from humans (Rand et al. example, tick species identification by a citizen scientist or the tick 2007; Xu et al. 2016, 2019; Jordan and Egizi 2019; Little et al. 2019, source being a human without a known travel history) are not in- Elias et al. 2020). tended to reflect poorly on any currently used method to collect data on tick records but rather to caution against interpretations that go beyond what is reasonable based on the reliability of the underlying Data Quality Considerations data. Perhaps the most difficult data quality classification problem is In this age of increasing possibilities for rapid data collection via for digital tick images examined by a professional scientist trained in emerging technologies (for example, smartphone apps) and ongoing tick identification. This method can have very high (>95%) species proliferation of scientific journals with variable standards for peer identification accuracy for commonly encountered tick species, such review, it is easier than ever before to collect large amounts of data as A. americanum, D. variabilis, and I. scapularis, when high-quality and publish the findings of a study. Moreover, there now also is the images of correctly positioned ticks are viewed by professional ento- possibility of publishing manuscripts in a citable format on pre-print mologists experienced in identifying ticks from digital images (Koffi servers (for example, https://www.biorxiv.org/) prior to peer review et al. 2017, Kopsco et al. 2020). However, in more general terms, in a scientific journal. Data quality, therefore, must be a primary con- identification of ticks from digital images is highly sensitive to both cern going forward and this should include all aspects of data collec- image quality (resolution, contrast, and tick positioning) and the tion. In the specific case of citizen science and ticks, main potential level of experience of the individuals responsible for the tick identifi- problems include tick species identification by citizen scientists cation. The method also may be prone to misclassify less commonly without corroboration by professional scientists and lack of travel encountered locally established or invasive tick species that can be histories for humans or pets during the period of time when a tick confused with more common species based solely on a digital image. discovered biting may have initially been encountered. This is not intended as a criticism of either citizen scientists or data collection via smartphone apps but rather as a reminder to both professional Citizen Science-Derived Information About scientists and citizen scientists to be judicious in the interpretation of Human–Tick Encounters data collected via emerging technologies and involving distinctions Recovery of ticks found crawling on or biting humans is perhaps the that are difficult to make unless you have specific training. When most intriguing aspect of citizen science because it provides unique used to best effect, citizen science could be a powerful force in the data that are rarely generated without the aid of citizen scientists. continuing struggle to reduce the negative societal impacts of ticks Collection of ticks from humans has the distinct benefit, relative to and tick-borne diseases. This is balanced against the risk for citizen collection of host-seeking ticks, of providing information on actual science projects to generate poor quality data (for example, through encounters with ticks (or infected ticks if they also are tested for tick species identification by citizen scientists) and potentially mis- pathogens) resulting from daily life. Collected ticks must be identi- leading information (for example, incorrect tick encounter locations) fied to species because most areas of the United States harbor mul- if used without adequate data quality safeguards and cautious inter- tiple human-biting tick species (Merten and Durden 2000). Using set pretation of project results. ratios for different tick species based on historical data for human– tick encounters as a proxy for species identification (for example, References Cited 80% I. scapularis and 20% D. variabilis) is not reliable because pop- ulation dynamics are not synchronized across years between human- Abdullah, S., C. Helps, S. Tasker, H. Newbury, and R. Wall. 2016. Ticks infesting domestic dogs in the UK: a large-scale surveillance programme. biting tick species with different host preferences and life-cycle Parasit. Vectors 9: 931. durations (Walker et al. 1998, Rand et al. 2007, Jordan and Egizi Aenishaenslin, C., C. Bouchard, J. K. Koffi, and N. H. Ogden. 2017. Exposure 2019, Pak et al. 2019, Elias et al. 2020) and additional tick species and preventive behaviours toward ticks and Lyme disease in Canada: re- may be increasing in importance as human-biters over time, as seen sults from a first national survey. Ticks Tick Borne Dis. 8: 112–118. for A. americanum in New Jersey and D. variabilis in Maine (Jordan Bartumeus, F., A. Oltra, and J. R. B. Palmer. 2018. Citizen science: a gateway and Egizi 2019, Elias et al. 2020). Moreover, data for ticks recovered for innovation in disease-carrying mosquito management? Trends from humans are likely to be skewed toward collection of adult Parasitol. 34: 727–729.
Journal of Medical Entomology, 2020, Vol. XX, No. XX 7 Bjork, J., G. Liu, and D. Neitzel. 2018. Ixodes scapularis surveillance and Tick App): quantitative and qualitative study. JMIR Mhealth Uhealth pathogen infection prevalence in Minnesota, 2005–2017. In Abstract, 7: e14769. 15th International Conference on Lyme Borreliosis and Other Tick-Borne Fischhoff, I. R., S. E. Bowden, F. Keesing, and R. S. Ostfeld. 2019. Systematic Diseases, 11–14 September 2018, Atlanta, GA. review and meta-analysis of tick-borne disease risk factors in residential Braz Sousa, L., S. R. Fricker, S. S. Doherty, C. E. Webb, K. L. Baldock, and yards, neighborhoods, and beyond. BMC Infect. Dis. 19: 861. C. R. Williams. 2020. Citizen science and smartphone e-entomology en- Gaff, H., R. J. Eisen, L. Eisen, R. Nadolny, J. Bjork, and A. J. Monaghan. ables low-cost upscaling of mosquito surveillance. Sci. Total Environ. 704: 2020. LYMESIM 2.0: an updated simulation of blacklegged tick (Acari: 135349. Ixodidae) population dynamics and enzootic transmission of Borrelia Centers for Disease Control and Prevention (CDC). 2018. Surveillance burgdorferi (Spirochaetales: Spirochaetaceae). J. Med. Entomol. 57: for Ixodes scapularis and pathogens found in this tick species in the 715–727. United States. https://www.cdc.gov/ticks/resources/TickSurveillance_ Garcia-Martí, I., R. Zurita-Milla, A. Swart, K. C. van den Wijngaard, Downloaded from https://academic.oup.com/jme/advance-article/doi/10.1093/jme/tjaa165/5890085 by guest on 20 December 2020 Iscapularis-P.pdf. Accessed 27 July 2020. A. J. H. van Vliet, S. Bennema, and M. Harms. 2017a. Identifying envi- Centers for Disease Control and Prevention (CDC). 2020. Guide to the sur- ronmental and human factors associated with tick bites using volunteered veillance of metastriate ticks (Acari: Ixodidae) and their pathogens in the reports and frequent pattern mining. Trans. GIS 21: 277–299. United States. https://www.cdc.gov/ticks/pdfs/Tick_surveillance-P.pdf. Garcia-Martí, I., R. Zurita-Milla, A. J. H. van Vliet, and W. Takken. 2017b. Accessed 27 July 2020. Modelling and mapping tick dynamics using volunteered observations. Connecticut Agricultural Experiment Station (CAES). 2020a. Information Int. J. Health Geogr. 16: 41. on submitting ticks. https://portal.ct.gov/CAES/Tick-Office/Tick-Office/ Garcia-Marti, I., R. Zurita-Milla, M. G. Harms, and A. Swart. 2018. Using Information-on-Submitting-Ticks. Accessed 27 July 2020. volunteered observations to map human exposure to ticks. Sci. Rep. 8: Connecticut Agricultural Experiment Station (CAES). 2020b. Summaries 15435. of tick testing. https://portal.ct.gov/CAES/Fact-Sheets/Tick-Summary/ Gasmi, S., N. H. Ogden, M. Ripoche, P. A. Leighton, R. L. Lindsay, Summaries-of-Tick-Testing. Accessed 27 July 2020. M. P. Nelder, E. Rees, C. Bouchard, L. Vrbova, R. Rusk, et al. 2019. Chilton, N. B., P. S. Curry, L. R. Lindsay, K. Rochon, T. J. Lysyk, and Detection of municipalities at-risk of Lyme disease using passive surveil- S. J. Dergousoff. 2020. Passive and active surveillance for Ixodes lance of Ixodes scapularis as an early signal: a province-specific indicator scapularis (Acari: Ixodidae) in Saskatchewan, Canada. J. Med. Entomol. in Canada. PLoS ONE 14: e0212637. 57: 156–163. Gleim, E. R., L. E. Garrison, M. S. Vello, M. Y. Savage, G. Lopez, Cohn, J. P. 2018. Citizen science: can volunteers do real research? BioScience R. D. Berghaus, and M. J. Yabsley. 2016. Factors associated with tick bites 58: 192–197. and pathogen prevalence in ticks parasitizing humans in Georgia, USA. Cull, B., M. E. Pietzsch, K. M. Hansford, E. L. Gillingham, and J. M. Medlock. Parasit. Vectors 9: 125. 2018. Surveillance of British ticks: an overview of species records, host Goddard, J. 2002. A ten-year study of tick biting in Mississippi: implications associations, and new records of Ixodes ricinus distribution. Ticks Tick for human disease transmission. J. Agromed. 8: 25–32. Borne. Dis. 9: 605–614. Gray, J., G. Stanek, M. Kundi, and E. Kocianova. 2005. Dimensions of Cull, B., M. E. Pietzsch, E. L. Gillingham, L. McGinley, J. M. Medlock, and engorging Ixodes ricinus as a measure of feeding duration. Int. J. Med. K. M. Hansford. 2020. Seasonality and anatomical location of human tick Microbiol. 295: 567–572. bites in the United Kingdom. Zoonoses Public Health 67: 112–121. Guerra, M. A., E. D. Walker, and U. Kitron. 2001. Canine surveillance system Dennis, D. T., T. S. Nekomoto, J. C. Victor, W. S. Paul, and J. Piesman. 1998. for Lyme borreliosis in Wisconsin and northern Illinois: geographic dis- Reported distribution of Ixodes scapularis and Ixodes pacificus (Acari: tribution and risk factor analysis. Am. J. Trop. Med. Hyg. 65: 546–552. Ixodidae) in the United States. J. Med. Entomol. 35: 629–638. Hamer, S. A., J. I. Tsao, E. D. Walker, L. S. Mansfield, E. S. Foster, and Eisen, L. 2020. Vector competence studies with hard ticks and Borrelia G. J. Hickling. 2009. Use of tick surveys and serosurveys to evaluate pet burgdorferi sensu lato spirochetes: a review. Ticks Tick Borne Dis. 11: dogs as a sentinel species for emerging Lyme disease. Am. J. Vet. Res. 70: 101359. 49–56. Eisen, L., and R. J. Eisen. 2016. Critical evaluation of the linkage between Hamer, S. A., R. Curtis-Robles, and G. L. Hamer. 2018. Contributions of cit- tick-based risk measures and the occurrence of Lyme disease cases. J. Med. izen scientists to arthropod vector data in the age of digital epidemiology. Entomol. 53: 1050–1062. Curr. Opin. Insect Sci. 28: 98–104. Eisen, R. J., and C. D. Paddock. 2020. Tick and tickborne pathogen surveil- Hendricks, B., M. Mark-Carew, and J. Conley. 2017. Evaluating the utility of lance as a public health tool in the United States. J. Med. Entomol. 57. doi: companion animal tick surveillance practices for monitoring spread and 10.1093/jme/tjaa087. occurrence of human Lyme disease in West Virginia, 2014–2016. Geospat. Eisen, R. J., L. Eisen, and C. B. Beard. 2016. County-scale distribution of Health 12: 582. Ixodes scapularis and Ixodes pacificus (Acari: Ixodidae) in the continental Heym, E. C., H. Kampen, M. Fahle, T. L. Hohenbrink, M. Schäfer, United States. J. Med. Entomol. 53: 349–386. D. E. Scheuch, and D. Walther. 2017. Anopheles plumbeus (Diptera: Eisen, R. J., K. J. Kugeler, L. Eisen, C. B. Beard, and C. D. Paddock. 2017. Culicidae) in Germany: updated geographic distribution and public health Tick-borne zoonoses in the United States: persistent and emerging threats impact of a nuisance and vector mosquito. Trop. Med. Int. Health 22: to human health. Ilar J. 58: 319–335. 103–112. Elias, S. P., K. A. Maasch, N. T. Anderson, P. W. Rand, E. H. Lacombe, Hook, S. A., C. A. Nelson, and P. S. Mead. 2015. U.S. public’s experience with R. M. Robich, C. B. Lubelczyk, and R. P. Smith. 2020. Decoupling of ticks and tick-borne diseases: results from national HealthStyles surveys. blacklegged tick abundance and Lyme disease incidence in Southern Ticks Tick Borne. Dis. 6: 483–488. Maine, USA. J. Med. Entomol. 57: 755–765. Jaenson, T. G. T., L. Tälleklint, L. Lundqvist, B. Olsen, J. Chirico, and Eritja, R., I. Ruiz-Arrondo, S. Delacour-Estrella, F. Schaffner, J. Álvarez- H. Mejlon. 1994. Geographical distribution, host associations, and vector Chachero, M. Bengoa, M. Á. Puig, R. Melero-Alcíbar, A. Oltra, and roles of ticks (Acari: Ixodidae, Argasidae) in Sweden. J. Med. Entomol. F. Bartumeus. 2019. First detection of Aedes japonicus in Spain: an unex- 31: 240–256. pected finding triggered by citizen science. Parasit. Vectors 12: 53. Johnson, J. L., H. S. Ginsberg, E. Zhioua, U. G. Whitworth, Jr, D. Markowski, Falco, R. C., D. Fish, and J. Piesman. 1996. Duration of tick bites in a Lyme K. E. Hyland, and R. Hu. 2004. Passive tick surveillance, dog seroposi- disease-endemic area. Am. J. Epidemiol. 143: 187–192. tivity, and incidence of human Lyme disease. Vector Borne Zoonotic Dis. Fernandez, M. P., G. M. Bron, P. A. Kache, S. R. Larson, A. Maus, 4: 137–142. D. Gustafson, Jr, J. I. Tsao, L. C. Bartholomay, S. M. Paskewitz, and Johnson, B. J., D. Brosch, A. Christiansen, E. Wells, M. Wells, A. F. Bhandoola, M. A. Diuk-Wasser. 2019. Usability and feasibility of a smartphone app A. Milne, S. Garrison, and D. M. Fonseca. 2018. Neighbors help neighbors to assess human behavioral factors associated with tick exposure (The control urban mosquitoes. Sci. Rep. 8: 15797.
8 Journal of Medical Entomology, 2020, Vol. XX, No. XX Jongejan, F., S. de Jong, T. Voskuilen, L. van den Heuvel, R. Bouman, Meiners, T., B. Hammer, U. B. Göbel, and O. Kahl. 2006. Determining the tick H. Heesen, C. Ijzermans, and L. Berger. 2019. “Tekenscanner”: a novel scutal index allows assessment of tick feeding duration and estimation of smartphone application for companion animal owners and veterinarians infection risk with Borrelia burgdorferi sensu lato in a person bitten by an to engage in tick and tick-borne pathogen surveillance in the Netherlands. Ixodes ricinus nymph. Int. J. Med. Microbiol. 296(Suppl. 40): 103–107. Parasit. Vectors 12: 116. Merten, H. A., and L. A. Durden. 2000. A state-by-state survey of ticks re- Jordan, R. A., and A. Egizi. 2019. The growing importance of lone star ticks corded from humans in the United States. J. Vector Ecol. 25: 102–113. in a Lyme disease endemic county: passive tick surveillance in Monmouth Murindahabi, M. M., D. Asingizwe, P. M. Poortvliet, A. J. H. van Vliet, County, NJ, 2006–2016. PLoS ONE 14: e0211778. E. Hakizimana, L. Mutesa, W. Takken, and C. J. M. Koenraadt. 2018. A Jordan, R. C., A. E. Sorensen, and S. Ladeau. 2017. Citizen science as a tool citizen science approach for malaria mosquito surveillance and control in for mosquito control. J. Am. Mosq. Control Assoc. 33: 241–245. Rwanda. NJAS–Wageningen J. Life Sci. 86–87: 101–110. Kampen, H., J. M. Medlock, A. G. Vaux, C. J. Koenraadt, A. J. van Vliet, National Weather Service (NWS). 2020. Cooperative Observer Program Downloaded from https://academic.oup.com/jme/advance-article/doi/10.1093/jme/tjaa165/5890085 by guest on 20 December 2020 F. Bartumeus, A. Oltra, C. A. Sousa, S. Chouin, and D. Werner. 2015. (COOP). https://www.weather.gov/coop/overview. Accessed 27 July 2020. Approaches to passive mosquito surveillance in the EU. Parasit. Vectors New York State Department of Health (NYSDOH). 2020a. Nymph deer tick 8: 9. density chart: beginning 2008. https://health.data.ny.gov/Health/Nymph- Koffi, J. K., J. Savage, K. Thivierge, L. R. Lindsay, C. Bouchard, Y. Pelcat, Deer-Tick-Density-Chart-Beginning-2008/555i-97td. Accessed 27 July and N. H. Ogden. 2017. Evaluating the submission of digital images as 2020. a method of surveillance for Ixodes scapularis ticks. Parasitology 144: New York State Department of Health (NYSDOH). 2020b. Adult deer tick 877–883. density chart: beginning 2008. https://health.data.ny.gov/Health/Adult- Kopsco, H. L., G. Xu, C.-Y. Luo, S. M. Rich, and T. N. Mather. 2020. Deer-Tick-Density-Chart-Beginning-2008/wpzj-45q8. Accessed 27 July Crowdsourced photographs as an effective method for large-scale passive 2020. tick surveillance. J. Med. Entomol. 57: In press. Nieto, N. C., W. T. Porter, J. C. Wachara, T. J. Lowrey, L. Martin, P. J. Motyka, Kullenberg, C., and D. Kasperowski. 2016. What is citizen science? and D. J. Salkeld. 2018. Using citizen science to describe the prevalence A scientometric meta-analysis. PLoS ONE 11: e0147152. and distribution of tick bite and exposure to tick-borne diseases in the Laaksonen, M., E. Sajanti, J. J. Sormunen, R. Penttinen, J. Hänninen, United States. PLoS One 13: e0199644. K. Ruohomäki, I. Sääksjärvi, E. J. Vesterinen, I. Vuorinen, J. Hytönen, Ogden, N. H., L. Trudel, H. Artsob, I. K. Barker, G. Beauchamp, D. F. Charron, et al. 2017. Crowdsourcing-based nationwide tick collection reveals the M. A. Drebot, T. D. Galloway, R. O’Handley, R. A. Thompson, et al. distribution of Ixodes ricinus and I. persulcatus and associated pathogens 2006. Ixodes scapularis ticks collected by passive surveillance in Canada: in Finland. Emerg. Microbes Infect. 6: e31. analysis of geographic distribution and infection with Lyme borreliosis Lee, X., D. S. Murphy, D. H. Johnson, and S. M. Paskewitz. 2019. Passive agent Borrelia burgdorferi. J. Med. Entomol. 43: 600–609. animal surveillance to identify ticks in Wisconsin, 2011–2017. Insects 10: Ogden, N. H., C. Bouchard, K. Kurtenbach, G. Margos, L. R. Lindsay, 289. L. Trudel, S. Nguon, and F. Milord. 2010. Active and passive surveillance Lehane, A., C. Parise, C. Evans, L. Beati, W. L. Nicholson, and R. J. Eisen. and phylogenetic analysis of Borrelia burgdorferi elucidate the process of 2020. Reported county-level distribution of the American dog tick Lyme disease risk emergence in Canada. Environ. Health Perspect. 118: (Acari: Ixodidae) in the contiguous United States. J. Med. Entomol. 57: 909–914. 131–155. Ogden, N. H., G. Pang, H. S. Ginsberg, G. J. Hickling, R. L. Burke, L. Beati, Lernout, T., N. De Regge, K. Tersago, M. Fonville, V. Suin, and H. Sprong. and J. I. Tsao. 2018. Evidence for geographic variation in life-cycle pro- 2019. Prevalence of pathogens in ticks collected from humans through cesses affecting phenology of the Lyme disease vector Ixodes scapularis citizen science in Belgium. Parasit. Vectors 12: 550. (Acari: Ixodidae) in the United States. J. Med. Entomol. 55: 1386–1401. Lewis, J., C. R. Boudreau, J. W. Patterson, J. Bradet-Legris, and V. K. Lloyd. Pak, D., S. B. Jacobs, and J. M. Sakamoto. 2019. A 117-year retrospective 2018. Citizen science and community engagement in tick surveillance—a analysis of Pennsylvania tick community dynamics. Parasit. Vectors 12: Canadian case study. Healthcare 6: 22. 189. Little, E. A. H., and G. Molaei. 2020. Passive tick surveillance: exploring Palmer, J. R. B., A. Oltra, F. Collantes, J. A. Delgado, J. Lucientes, S. Delacour, spatiotemporal associations of Borrelia burgdorferi (Spirochaetales: M. Bengoa, R. Eritja, and F. Bartumeus. 2017. Citizen science provides Spirochaetaceae), Babesia microti (Piroplasmida: Babesiidae), and a reliable and scalable tool to track disease-carrying mosquitoes. Nat. Anaplasma phagocytophilum (Rickettsiales: Anaplasmataceae) infection Commun. 8: 916. in Ixodes scapularis (Acari: Ixodidae). Vector Borne Zoonotic Dis. 20: Piesman, J., and A. Spielman. 1980. Human babesiosis on Nantucket Island: 177–186. prevalence of Babesia microti in ticks. Am. J. Trop. Med. Hyg. 29: Little, E. A. H., J. F. Anderson, K. C. Stafford, 3rd, L. Eisen, R. J. Eisen, and 742–746. G. Molaei. 2019. Predicting spatiotemporal patterns of Lyme disease inci- Porter, W. T., P. J. Motyka, J. Wachara, Z. A. Barrand, Z. Hmood, dence from passively collected surveillance data for Borrelia burgdorferi M. McLaughlin, K. Pemberton, and N. C. Nieto. 2019. Citizen science sensu lato-infected Ixodes scapularis ticks. Ticks Tick Borne Dis. 10: informs human-tick exposure in the Northeastern United States. Int. 970–980. J. Health Geogr. 18: 9. Logar, M., E. Ruzić-Sabljić, and F. Strle. 2002. Comparison of self-assessment Prusinski, M. A., J. E. Kokas, K. T. Hukey, S. J. Kogut, J. Lee, and and scutal index for the duration of Ixodes ricinus tick attachment. Wien. P. B. Backenson. 2014. Prevalence of Borrelia burgdorferi (Spirochaetales: Klin. Wochenschr. 114: 489–492. Spirochaetaceae), Anaplasma phagocytophilum (Rickettsiales: Lorusso, V., R. P. Lia, F. Dantas-Torres, E. Mallia, S. Ravagnan, G. Capelli, Anaplasmataceae), and Babesia microti (Piroplasmida: Babesiidae) in and D. Otranto. 2011. Ixodid ticks of road-killed wildlife species in Ixodes scapularis (Acari: Ixodidae) collected from recreational lands in the southern Italy: new tick-host associations and locality records. Exp. Appl. Hudson Valley Region, New York State. J. Med. Entomol. 51: 226–236. Acarol. 55: 293–300. Raghavan, M., N. Glickman, G. Moore, R. Caldanaro, H. Lewis, and Mader, E. M., C. Ganser, A. Geiger, L. C. Harrington, J. Foley, R. L. Smith, L. Glickman. 2007. Prevalence of and risk factors for canine tick infes- N. Mateus-Pinilla, P. D. Teel, and R. J. Eisen. 2020. A survey of tick sur- tation in the United States, 2002-2004. Vector Borne Zoonotic Dis. 7: veillance and control practices in the United States. J. Med. Entomol. 57. 65–75. doi: 10.1093/jme/tjaa094. Rand, P. W., E. H. Lacombe, R. Dearborn, B. Cahill, S. Elias, C. B. Lubelczyk, Maki, E., and L. Cohnstaedt. 2015. Crowdsourcing for large-scale mosquito G. A. Beckett, and R. P. Smith, Jr. 2007. Passive surveillance in Maine, an (Diptera: Culicidae) sampling. Can. Entomol. 147: 118–123. area emergent for tick-borne diseases. J. Med. Entomol. 44: 1118–1129. Mead, P., S. Hook, S. Niesobecki, J. Ray, J. Meek, M. Delorey, C. Prue, and Randolph, S. E. 2004. Tick ecology: processes and patterns behind the epide- A. Hinckley. 2018. Risk factors for tick exposure in suburban settings in miological risk posed by ixodid ticks as vectors. Parasitology 129(Suppl.): the Northeastern United States. Ticks Tick Borne Dis. 9: 319–324. S37–S65.
You can also read