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Factors Associated with Tick Bites and Pathogen Prevalence in Ticks Parasitizing Humans in Georgia, USA Elizabeth R

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Factors Associated with Tick Bites and Pathogen Prevalence in Ticks Parasitizing Humans in Georgia, USA Elizabeth R Gleim et al. Parasites & Vectors (2016) 9:125 DOI 10.1186/s13071-016-1408-6 RESEARCH Open Access Factors associated with tick bites and pathogen prevalence in ticks parasitizing humans in Georgia, USA Elizabeth R. Gleim1,2,3*, Laurel E. Garrison4,5, Marianne S. Vello4, Mason Y. Savage1,6, Gaylord Lopez7, Roy D. Berghaus8 and Michael J. Yabsley1,2 Abstract Background: The incidence and emergence of tick-borne diseases has increased dramatically in the United States during the past 30 years, yet few large-scale epidemiological studies have been performed on individuals bitten by ticks. Epidemiological information, including disease development, may provide valuable information regarding effectiveness of tick bite prevention education, pathogen transmission, human-disease dynamics, and potential implications for under reporting of tick-borne diseases. Methods: Ticks found attached to Georgia residents were submitted for identification and polymerase chain reaction (PCR) testing for Francisella tularensis, Ehrlichia, Anaplasma, Borrelia,andRickettsia spp. Tick bite victims were interviewed three weeks after the tick bite to identify various epidemiologic factors associated with infestation and if signs suggestive of a tick-borne disease had developed. Fisher’s exact test of independence was used to evaluate associations between various factors evaluated in the study. A multivariable logistic regression model was used for the prediction of non- specific illness post-tick bite. Results: From April 2005-December 2006, 444 participants submitted 597 ticks (426 Amblyomma americanum,142 Dermacentor variabilis,19A. maculatum,7Ixodes scapularis,3Amblyomma sp.) which originated from 95 counties. Only 25 (34 %) of 74 interviewed individuals purposely took tick bite prevention measures. Ticks that were PCR positive for bacterial organisms were attached to 136 participants. Of the 77 participants who developed non-specific illness, 50 did not have PCR positive ticks, whereas 27 did have PCR positive tick (s). Of those 27 individuals, 12 fit the criteria for a possible tick-borne illness (i.e., tick attached >6 h [if known], ≥4 day incubation period, and the individual exhibited clinical symptoms typical of a tick-borne illness without exhibiting cough, sore throat, or sinus congestion). Ticks from these individuals were positive for R. amblyommii (n =8),E. ewingii (n = 1), R. montana (n =1),R. rhiphicephali (n =1), and Rickettsia sp. TR-39 (n =1). Conclusions: Although illnesses reported in this study cannot definitively be connected with tick bites, it does provide insight into development, diagnosis, and treatment of possible tick-borne diseases post-tick bite. The study also provided data on pathogen prevalence, and epidemiologic factors associated with tick bites, as well as tick presence by county in Georgia. Keywords: Epidemiology, Tick-borne pathogens, Tick-borne disease, Rickettsia, Ticks, Georgia * Correspondence: [email protected] 1Southeastern Cooperative Wildlife Disease Study, College of Veterinary Medicine, The University of Georgia, 589 D.W. Brooks Dr., Wildlife Health Bldg, Athens, GA 30602, USA 2Warnell School of Forestry and Natural Resources, The University of Georgia, 180 E. Green St., Athens, GA 30602, USA Full list of author information is available at the end of the article © 2016 Gleim et al. Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Gleim et al. Parasites & Vectors (2016) 9:125 Page 2 of 13 Background Methods In the United States, at least 11 species of ticks are vectors Collection of ticks and epidemiological data of pathogens of public health importance. Of these, two From April 2005–December 2006, a state-wide media species (Amblyomma americanum and Ixodes scapularis) campaign was performed requesting that residents with are responsible for the transmission of most known patho- a tick (s) attached to them contact the Georgia Poison gens. For example, A. americanum transmits the causative Center (GPC) to enroll in the study. GPC staff answered agents of human monocytic ehrlichiosis (HME), Ehrlichia any questions regarding tick removal and tick-borne ewingii ehrlichiosis, Panola Mountain ehrlichiosis, tular- disease, described the components of the study to all emia, southern tick-associated rash illness (STARI) and callers who met the inclusion criteria (i.e., persons who the newly identified heartland virus [1]. Additionally, I. had an attached tick), obtained informed verbal consent, scapularis transmits the causative agents of Lyme disease, and provided tick shipping instructions to those who Borrelia miyamotoi relapsing fever, human granulocytic agreed to participate. They also collected basic contact anaplasmosis (HGA), and babesiosis. Other tick-borne information for the enrollee, date of tick removal, location diseases of importance, particularly in the Southeast, of tick attachment on the body, and county in which the include Rocky Mountain spotted fever (RMSF) and bite occurred. Rickettsia parkeri rickettsiosis. Approximately 3 weeks later, a follow-up survey was While most of these tick-borne diseases are nationally administered by Georgia Division of Public Health notifiable to the Centers for Disease Control and Pre- (GDPH) staff during which the participant was asked to vention, it is generally thought that tick-borne diseases estimate how long the tick was attached, describe the are under reported due to misdiagnosis or failure to seek setting where they were bitten, and report any illness medical treatment, report disease, or identify specific since the tick bite. For those reporting any illness the disease agents [2–4]. Furthermore, demographic and following data was collected: onset date, duration of epidemiological information is infrequently collected on illness, first symptom, and yes/no to the following list of these patients which could prove to be useful in target- symptoms: fever, chills, nausea, rash, stomach pain, ing high risk groups or behaviors [5–10]. A single study weakness/tiredness, muscle soreness, altered sense of in which epidemiologic and demographic information taste, decreased appetite, painful to look at light or sun, was collected from tick-bite victims was performed in dizziness, headache, diarrhea, joint pain, weight loss, Kentucky [11]. However, there was a small sample size vomiting, sweats, cough, confusion, and also asked if the (n = 33) and study participants were geographically and patient experienced any other symptoms. For those who demographically restricted to individuals eligible for had a rash, they were asked where on the body it was health services at a single military base. located, whether it was at the site of the tick bite, and Additionally, because being bitten by an infected tick what it looked like. Patients were also asked whether does not necessarily result in transmission of the patho- they sought medical attention, had blood drawn, and/or gen and those who do develop disease are not always was prescribed medicine for their illness. reported, information on human encounter rates with In 2006 only, participants were asked about protective infected ticks is nearly impossible to obtain. However, measures taken against ticks (both on purpose and not such data could assist in identifying geographic regions on purpose to avoid tick bites). Tick avoidance measures with high disease risk, as well as provide insights into were divided into two categories, primary (e.g., things pathogen transmission dynamics. While several studies done to prevent ticks from attaching including, but not lim- have been published regarding ticks parasitizing humans ited to, use of DEET or other repellant, keeping extremities in the eastern US, submissions were sometimes received covered by clothing, and/or not sitting on the ground) and from a broad and varied geographic range and few tested secondary protective measures (actions performed to find for pathogens or obtained epidemiological information and remove ticks once attached including checking oneself from the patients including whether disease ensued frequently for ticks while outside, full body and/or buddy [5,6,9,12]. tick checks, and taking a shower). This study was reviewed To better describe the potential public health implica- by a member of the Georgia Department of Human Re- tions of human tick attachment, the current study was con- sources Institutional Review Board and received a non- ducted. The specific objectives were to 1) determine the research determination. geographic distribution and identity of ticks found attached to humans in Georgia, 2) test ticks for suspected or known Tick identification and pathogen testing zoonotic pathogens via polymerase chain reaction (PCR), 3) Lab personnel responsible for identifying and testing ticks collect demographic, tick exposure, and bite risk data from for pathogens were blinded to whether or not the tick bite tick submitters, and 4) determine whether any submitters victim developed illness. All ticks were classified to species,
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