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TBRF Risk Among Cavers Austin 2017 Received: 16 January 2019 | Revised: 24 April 2019 | Accepted: 6 May 2019 DOI: 10.1111/zph.12588 ORIGINAL ARTICLE WILEY Evaluating the risk of tick-borne relapsing fever among occupational cavers—Austin, TX, 2017 Stefanie B. Campbell1 | Anna Klioueva2 | Jeff Taylor2 | Christina Nelson1 | Suzanne Tomasi3 | Adam Replogle1 | Natalie Kwit1 | Christopher Sexton1 | Amy Schwartz1 | Alison Hinckley1 1Centers for Disease Control and Prevention, Fort Collins, Colorado Abstract 2Austin Public Health, Austin, Texas Tick-borne relapsing fever (TBRF) is a potentially serious spirochetal infection caused 3Centers for Disease Control and by certain species of Borrelia and acquired through the bite of Ornithodoros ticks. In Prevention, Morgantown, West Virginia 2017, Austin Public Health, Austin, TX, identified five cases of febrile illness among Correspondence employees who worked in caves. A cross-sectional serosurvey and interview were Stefanie B. Campbell, Centers for Disease Control and Prevention, Fort Collins, CO. conducted for 44 employees at eight organizations that conduct cave-related work. Email: [email protected] Antibodies against TBRF-causing Borrelia were detected in the serum of five par- ticipants, four of whom reported recent illness. Seropositive employees entered sig- nificantly more caves (Median 25 [SD: 15] versus Median 4 [SD: 16], p = 0.04) than seronegative employees. Six caves were entered more frequently by seropositive employees posing a potentially high risk. Several of these caves were in public use areas and were opened for tours. Education of area healthcare providers about TBRF and prevention recommendations for cavers and the public are advised. KEYWORDS Borrelia, Borrelia hermsii, Borrelia turicatae, TBRF, TX 1 | INTRODUCTION cabins (Dworkin, Shoemaker, Fritz, Dowell, & Anderson, 2002). A total of 504 TBRF cases were reported from twelve western states Tick-borne relapsing fever (TBRF) in humans follows infection with during 1990–2011; 18 of these were thought to have acquired their one of several Borrelia bacteria species. These bacteria can be trans- infection in Texas (Forrester, Kjemtrup, et al., 2015). mitted rapidly to humans through the bite of Ornithodoros tick spe- In Texas, Ornithodoros turicata transmits the TBRF causative agent, cies. Ornithodoros ticks feed quickly and then detach and scatter; Borrelia turicatae (Davis, 1943; Donaldson et al., 2016; Rawlings, 1995). therefore, a victim might be unaware of the tick bite (Boyle, Wilder, The B. turicatae lifecycle is maintained in this region by small and me- Lawrence, & Lopez, 2014). TBRF is characterized by episodes of dium-sized animal hosts (Armstrong et al., 2018). Since 1930, human fever, headache, myalgia, arthralgia and chills (Dworkin, Schwan, cases of TBRF in TX have occurred sporadically with activity in caves Anderson, & Borchardt, 2008). The initial fever will last approxi- suggested as a risk factor (Dworkin et al., 2008; Forrester, Kjemtrup, mately 3 days, followed by 7 days without fever, followed by another et al., 2015; Rawlings, 1995; Weller & Graham, 1930; Wilder et al., 3 days of fever. Without antibiotic treatment, this process can repeat 2015). Weller and Graham (1930) described inspection of a cave out- several times (Davis, Vincent, & Lynch, 2002; Dworkin et al., 2008). side of Austin, TX, in which “the floor was alive with ticks.” Other spe- In the United States, most TBRF cases are attributed to infection cific risk factors for TBRF in Texas have not been described. with Borrelia hermsii with patients commonly exposed in mountain- In 2017, Austin Public Health (TX) identified an increase in re- ous areas of western states, often following stays in seasonally used ports of TBRF-like illness. In February, 11 people became ill after Zoonoses Public Health. 2019;66:579–586. wileyonlinelibrary.com/journal/zph © 2019 Blackwell Verlag GmbH | 579 580 CAMPBELL ET al. --WILEY---------------------------| attending a workshop near Austin (Bissett et al., 2018). Attendees spent time in wooded areas and near wildlife, but none reported en- tering a cave. Blood samples from four patients were tested, and Impacts all had evidence of Borrelia infection, however, not specific for re- • The findings of this investigation support the hypoth- lapsing fever agents. In June and July, five people became ill after esized association between tick-borne relapsing fever entering Austin area caves. Serum from three of the five was tested (TBRF) and cave exposure. Occupational cavers who at CDC in Fort Collins, and two had antibodies to relapsing fever entered a greater number of caves were significantly group borreliae. more likely to have serologic evidence of past exposure Austin is located in Travis County and adjacent to Hays and to TBRF bacteria. Williamson Counties. The three counties encompass 2,791 square • Certain caves appeared to be riskier than others for miles in southern central Texas (United States Census Bureau, exposure to TBRF bacteria. Six caves were found to be 2010). Within these three counties, there are 1,338 documented higher risk in this investigation, five of which are located caves, of the 5,600 in Texas (Texas Speleological Society, 2016). in southwest Austin. Monitoring this part of Austin Near Austin, a number of organizations employ people who enter through tick sampling and additional ecologic assess- caves or assess karst features for various occupation-related du- ment is needed. ties. State and local government organizations employ park rang- • The cave environment presents challenges to standard ers, biologists, surveyors, mammalogists, geologists, environmental tick bite prevention practices because of its sensitive conservationists and natural resource specialists. Private consult- ecosystem that could be harmed by chemical acaricides. ing companies employ people with similar titles and most often People entering caves should be aware of TBRF and focus on performing karst surveys. Occupational cavers usually utilize alternative protective measures, such as wearing enter multiple caves in their duty area during all seasons and can long clothing. spend hours in each cave. For this investigation, Austin Public health worked with CDC to: (a) determine the frequency, duration and types of cave exposures among occupational cavers; (b) document the frequency of seropos- 2.2 | Data collection itivity for TBRF, occurrence of illness consistent with TBRF, and the clinical spectrum of illnesses experienced by occupational cavers; We developed a questionnaire to collect demographic information, em- and (c) identify any differences in exposure, risk factors, or preven- ployment history, cave exposure, work-related activities in caves, use of tive strategies between seronegative and seropositive occupational protective measures in caves, and illness history. Participating employ- cavers. ees who provided informed consent were interviewed in person dur- ing October 9 to 13, 2017. To capture cave exposure, employees were asked to name and rank their top 10 most frequently entered caves in 2 | METHODS the past 12 months. We asked about the duration of time (in hours) that employees spent in their top 10 most frequently visited caves. 2.1 | Inclusion criteria of organizations and employees 2.3 | Serological testing A local recreational caving group was consulted prior to the inves- tigation. They provided information on government and private Serum samples were collected from participants at the time of organizations in Hays, Travis and Williamson counties, TX, that interview. The CDC laboratory in Fort Collins, CO performed se- employed at least one person who entered caves for their job. In rology on the samples using two-tier testing (enzyme immuno- addition, they identified a list of caves that are open to the pub- assay and Western immunoblot) in which antibody reactivity to lic and/or perceived to be caves of risk for TBRF. Caves of risk for B. hermsii antigens was assessed (Fritz et al., 2004; Trevejo et al., TBRF included ones where the tick vector had been previously 1998). Samples having positive results for both assays were inter- seen or ones that people entered and then became ill a few days preted as evidence of previous infection. TBRF serologic tests at later. Organizations were contacted, and employees were invited to CDC utilize B. hermsii antigen since the majority of cases in the participate. All identified government organizations in the inclusion United States are caused by B. hermsii, and it has been shown that area of Travis, Williamson and Hays counties that employed at least TBRF caused by B. turicatae is detectable by the current tests one occupational caver participated. Of the ten identified private (Christensen et al., 2017). organizations, four agreed to participate. In total, eight government and private organizations participated and 46 employees were en- 2.4 | PCR and DNA sequencing rolled. A point of contact for each organization received an email 1 week prior to the study with information describing the purpose To confirm that utilizing B. hermsii reagents to screen for antibodies and logistics of the investigation. to B. turicatae was appropriate, DNA sequencing was performed on ET al 581 ---------------------------WILEY--CAMPBELL . | TABLE 1 Demographic characteristics of employees surveyed Biosystems). Sequence files were assembled with Seq Builder Pro from eight organizations that employ occupational cavers (n = 44)— (DNAStar), and contig files with trimmed ends (556 bp) were aligned Austin,
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