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Page 1: Author's personal copy - Trident

This article appeared in a journal published by Elsevier. The attachedcopy is furnished to the author for internal non-commercial researchand education use, including for instruction at the authors institution

and sharing with colleagues.

Other uses, including reproduction and distribution, or selling orlicensing copies, or posting to personal, institutional or third party

websites are prohibited.

In most cases authors are permitted to post their version of thearticle (e.g. in Word or Tex form) to their personal website orinstitutional repository. Authors requiring further information

regarding Elsevier’s archiving and manuscript policies areencouraged to visit:

http://www.elsevier.com/authorsrights

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Author's personal copy

Ticks and Tick-borne Diseases 4 (2013) 352– 358

Contents lists available at SciVerse ScienceDirect

Ticks and Tick-borne Diseases

j ourna l ho me p age: www.elsev ier .com/ locate / t tbd is

Original article

Knowledge and prevention of tick-borne diseases vary across an urban-to-ruralhuman land-use gradient

Brett R. Baylesa,∗, Gregory Evansb, Brian F. Allanc

a School of Public Health, Saint Louis University, 3545 Lafayette Ave., St. Louis, MO 63104, USAb Jiann Ping-Hsu College of Public Health, Georgia Southern University, 1332 Southern Drive, Statesboro, GA 30458, USAc Department of Entomology, University of Illinois Urbana-Champaign, 505 S. Goodwin Ave., Urbana, IL 61801, USA

a r t i c l e i n f o

Article history:Received 22 October 2012Received in revised form31 December 2012Accepted 7 January 2013Available online 26 March 2013

Keywords:EhrlichiosisHealth behaviorLone star tickTick-borne diseasesPrevention and control

a b s t r a c t

We sought to determine the behavioral risk of exposure to tick-borne diseases across a human land-usegradient in a region endemic for diseases transmitted by the lone star tick. We measured the knowledge,attitudes, and preventive behaviors of visitors to 14 suburban, exurban, and rural recreational parks. Astructured interview was conducted to determine respondents’ (n = 238) knowledge of tick-borne dis-ease risk, perceived susceptibility to tick-borne disease, and tick bite prevention behaviors. We foundsignificant differences across park types for most personal protective behaviors. Individuals in exurbanparks were more likely to perform frequent tick checks and use chemical insect repellents compared toother park types (p < 0.001), while suburban park visitors were more likely to avoid tick habitats (p < 0.05).Disparities exist in the level of knowledge, perceived personal risk, and use of preventive measures acrossthe human land-use gradient, suggesting that targeted public health intervention programs could reducebehavioral exposure risk by addressing specific gaps in knowledge and prevention.

© 2013 Elsevier GmbH. All rights reserved.

Introduction

Infectious diseases transmitted by the bite of the lone star tick,Amblyomma americanum, are increasing throughout the range ofthis arthropod disease vector (Childs and Paddock, 2003). Chiefamong these is ehrlichiosis, incidence of which has continued toincrease since it first became nationally notifiable to the Centersfor Disease Control and Prevention (CDC) in 1999 (CDC, 2011). Thehighest human incidence of ehrlichiosis occurs in the Ozark regionof Arkansas and Missouri (Dahlgren et al., 2011), where the lonestar tick (hereafter ‘LST’) has been identified as the most commonlyencountered tick species (Brown et al., 2011). In Missouri, ratesof ehrlichiosis (2.4 per 100,000 persons) and emerging rickettsialdiseases, such as Rocky Mountain spotted fever (4.6 per 100,000persons) were among the most commonly reported tick-borne dis-eases in the state in 2010 (MDHSS, 2010).

A variety of social and biological influences have contributedto increased LST-associated pathogen transmission in this region,including alterations of key ecological parameters leading to newfocal points of disease risk (Paddock and Yabsley, 2007). The emer-gence of ehrlichiosis and other tick-borne diseases into humanpopulations requires a complex interplay between landscape

∗ Corresponding author. Tel.: +1 760 703 1671.E-mail address: [email protected] (B.R. Bayles).

attributes, the resulting distribution of wildlife hosts, and humanoutdoor activities. While specific ecological factors that createareas of potentially high transmission risk for LST-associateddiseases have recently been studied in this region (Allan, 2009;Allan et al., 2010a), the influence of human behaviors within thecontext of land use in these areas of elevated risk of exposureremains poorly understood.

Reducing the burden of tick-borne disease through the use ofpersonal protective practices is considered to be an important firstline of prevention for mitigating this growing public health problem(Piesman and Eisen, 2008). The CDC has supported the use of a setof commonly recommended preventive behaviors, including per-forming frequent tick checks, applying chemical insect repellentson skin or clothing, and avoiding tick habitats (CDC, 2012). In addi-tion, tucking pants into socks and wearing long sleeves as protectiveclothing have been suggested as supplementary preventive behav-iors (Hayes and Piesman, 2003). Studies have offered empiricalsupport for these practices based on the premise that they reducethe probability of tick bites and subsequently disease transmissionfrom infected ticks (Schwartz et al., 1996; Vazquez et al., 2008;Miller et al., 2011). Efforts to understand the utility of these behav-iors have largely focused on regions endemic for Lyme disease,transmitted by the black-legged tick (Ixodes scapularis) (McKennaet al., 2004; Connally et al., 2009), and among individuals whoseoccupational exposures place them at increased risk of tick-humancontact (Schwartz and Goldstein, 1990; Nolan and Mauer, 2006).

1877-959X/$ – see front matter © 2013 Elsevier GmbH. All rights reserved.http://dx.doi.org/10.1016/j.ttbdis.2013.01.001

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While human incidence of Lyme disease in Missouri is low, supe-rior understanding of the importance of human behaviors for riskof exposure to Lyme disease may generate valuable insights intosimilar phenomena for LST-associated diseases that are endemic tothe region. For example, recreational parks have been identified asareas where Lyme transmission can occur (Li et al., 2000). However,knowledge of tick-borne disease risk and the utilization of appro-priate prevention measures among individuals visiting these parkshave been infrequently studied for Lyme disease (Hallman et al.,1995; Standaert et al., 1995), and even less so for LST-associateddiseases.

This study sought to document the knowledge, perceivedsusceptibility, and use of personal protective behaviors for LST-associated diseases among individuals visiting recreational parksacross the urban-to-rural human land-use gradient as measuredby human population density in the St. Louis, MO, metropolitanregion, an area endemic for ehrlichiosis and other LST-associateddiseases (Allan et al., 2010b), but not Lyme disease (CDC, 2012).Within this region, biological metrics of disease risk (e.g., the den-sity of infected ticks) are heterogeneous with respect to humanpopulation density (Allan et al., 2010a), generating considerablepotential variation in exposure risk. Accordingly, we sought todetermine if commonly recommended behaviors differed by thetype of park. Understanding spatial variation in how individualsinteract with their environment could provide a more refinedcontextual framework for understanding variability of pathogentransmission to humans. We further sought to identify whichdemographic and cognitive variables were predictive of the use ofpersonal protective measures across parks in the study region toelucidate the predisposing factors associated with these preventivebehaviors.

Materials and methods

Study design and population recruitment

A behavioral risk survey was administered in 14 different city,county, and state multi-use recreational areas in the Saint Louis,MO, metropolitan region. Sites were selected from those utilizedas part of a long-term ecological study to provide a representa-tive subsample of recreational areas spanning the human densityand human land-use gradients in this region. Structured interviewswere conducted from June to September 2011, coinciding with thepeak period of questing activity for the vector life stages and thereporting of human cases of LST-associated diseases (Kollars et al.,2000). Each park was visited by one of the authors (BB) during bothAM and PM hours and during a minimum of at least one weekendand one weekday.

Potential participants were approached at trail heads and parkentrances to ensure that all visitors to each park had an equal oppor-tunity to participate in the study. Visitors were considered eligible ifthey were 18 years of age or older and indicated the intent to spendtime out-of-doors in the park that day. To maintain independencebetween observations, park visitors in groups were interviewedseparately.

Survey development

Efforts to understand and predict tick-borne disease preventionbehaviors are often based on social cognitive models, including theHealth Belief Model (HBM), which posits that perceptions of sus-ceptibility to a disease and awareness of its potential health conse-quences together contribute to the adoption of behaviors believedto be effective against the health threat (Glanz et al., 2008). A ques-tionnaire was developed from an aggregate of previously validated

survey items based on HBM components used to assess humanbehavioral dimensions of tick-borne disease risk across variouspopulations (Shadick et al., 1997; Brewer et al., 2004; Herrington,2004; Gould et al., 2008; Arikan et al., 2010; Heller et al., 2010). Thissurvey was comprised of 4 thematic areas: demographic and recre-ational risk factors, knowledge of ticks and tick-borne diseases, per-ceptions of tick-borne disease risk, and utilization of commonly rec-ommended tick-borne disease prevention behaviors (Appendix A).

Demographic and recreational behaviors were assessed aspotential mediating factors for the uptake of recommended healthbehaviors. In addition to age, gender, and other demographicinformation, recreational risk factors were obtained by asking par-ticipants to choose how often and for what length of time (lessthan 1 h, 2–4 h, all day) they engaged in a list of activities (bicycleriding, jogging, hiking, picnicking) at a park. Additional compo-nents of the survey were developed according to the conceptualframework of the HBM, including (1) knowledge and awarenessof ticks and tick-borne disease, and (2) perceived susceptibility totick-borne diseases. Participants were asked a continuum of ques-tions of increasing specificity designed to elucidate their levelsof knowledge and awareness about ticks and tick-borne diseases.Basic measures of knowledge included: being able to identify ticks,knowing ticks could spread disease to humans, having some aware-ness of Lyme disease or other tick-borne diseases. A more specificmeasure of knowledge included the ability to identify the lone startick. To ascertain perceptions of risk, participants were asked if theywere “very concerned”, “not very concerned”, or “not concerned atall” with being bitten by a tick, contracting Lyme disease, or con-tracting other tick-borne diseases while in the specific park thatday.

Finally, the questionnaire sought to determine the extent of pre-ventive behaviors performed by park visitors. Participants wereasked whether they used insect repellents and whether they wereaware of the active ingredient (DEET, permethrin, or plant-basedrepellents advertised as ‘organic’). They were then asked if theywould be wearing protective clothing while in the park, includingwearing long pants, tucking pants into socks, or wearing light-colored clothing to aid in revealing ticks. In addition, participantswere asked if they would avoid areas that may pose increasedtransmission risk, including wooded/grassy areas or walking in thecenter of trails rather than along the edges. Participants were alsoasked if they performed tick checks following time spent in thepark.

Geographic stratification

To examine differences in human behaviors across recreationalparks spanning the human land-use gradient, study sites werestratified based upon a suburban–rural classification system quan-tified via the human population density surrounding each park.Using ArcGIS version 10.0 (Environmental Systems Research Insti-tute Inc., Redlands, CA), each park was geo-coded on a map ofMissouri and a 5 km radius buffer was created around the perimeterof each site. Parks and their corresponding buffers were then over-laid on a map of census blocks with population estimates from the2010 U.S. Census obtained from the Missouri Spatial Data Informa-tion Services (MSDIS). Human population density estimates wereobtained by summing the number of residents within the circum-ference of each buffer and dividing by the total buffer area in meterssquared (Supplemental Table 1). Parks were then classified as eithersuburban (sites I, II, III, IV), exurban (sites V, VI, VII, VIII), or rural(sites IX, X, XI, XII) according to the associated human populationdensities (Fig. 1 and Supplemental Table 2) (Theobald, 2004). Twoparks (sites XIII, XIV) were omitted from this stratification due toinsufficient sample size of questionnaire respondents, yielding a

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Fig. 1. Map of study sites and the distribution of land cover in the St. Louis, Missouri region (National Land Cover Database). Red indicates urban areas, and green indicatesextent of forest cover. (For interpretation of the references to color in this figure legend, the reader is referred to the web version of the article.)

sample of 236 respondents over 12 parks equally divided amongthe 3 classifications of human density (Supplemental Table 2).

Statistical analysis

Descriptive statistics were produced for the entire sample of 12sites and again separately for the 3 stratifications of human landuse. Differences in participant characteristics and behaviors acrossthe geographically-stratified park types were assessed using �2 orFisher’s exact tests where appropriate.

Outcome variables were dichotomized to represent 4 keydomains of recommended behaviors previously shown to success-fully mitigate tick-borne disease risk: habitat avoidance, visualtick checks, protective clothing use, and insect repellent use (Clarkand Hu, 2008; Vazquez et al., 2008). Avoidance behavior indicatedwhether the participant limited time in potentially tick-infestedareas or chose to walk on the center of trails rather than trailedges. Tick check behavior was dichotomized such that checkingone’s body after visiting a park “always” or “often” indicated action,while performing this behavior less frequently indicated inaction.Protective clothing included intentionally wearing long pants or

tucking pants into socks to avoid tick contact. Insect repellent userepresented whether participants acknowledged using any type ofchemical repellent on their skin or clothing while visiting a site.Multivariate logistic regression was used to assess the potentialcontribution of demographics, knowledge, and level of perceivedsusceptibility toward each of the primary prevention outcomes. Allvariables were initially entered into the model with subsequentbackwards stepwise elimination used to arrive at parsimoniousfinal models. Measures of association were reported as adjustedodds ratios (aOR) with corresponding 95% confidence intervals (95%CI).

Statistical analyses were run using SAS version 9.2 (SAS InstituteInc., Cary, N.C.). All tests were two-tailed and considered statisti-cally significant with a p-value <0.05.

Results

Demographics and recreational activities

A total of 265 people were asked to participate, and ultimately238 consented, yielding a refusal rate of ∼10%. The overall study

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Table 1Demographic characteristics of the study sample.

Variables No. (%)

Gender, male 146 (61.3)

Age18–29 38 (16.0)30–59 155 (65.1)≥60 45 (18.9)

Race, white 229 (96.2)Day of the week, weekend 167 (70.2)Time of day, PM 135 (56.7)Time lived at current residence, yrsa 14.7 ± 11.7

Frequency of park visits>1 time per week 63 (26.47)Several days per month 48 (20.17)Several times per year 80 (33.61)First time 47 (19.75)

a Mean ± standard deviation.

sample was comprised of a larger proportion of males (61.3%)and was primarily white (96.2%) (Table 1). A majority of respon-dents indicated having had a tick bite at some point in their lives(82.4%), and most had removed a tick from a pet as well (76.9%)(Supplemental Table 4). When asked what attracted individualsto a particular park, the majority (64.7%) indicated outdoor recre-ational opportunities, including hiking (31.1%) and bicycle riding(23.1%) (Supplemental Table 3). Overall, the majority of respon-dents (61.8%) spent a minimum of at least 1 h in the park on theday of the survey (Table 1).

Knowledge and perceived susceptibility to ticks and tick-bornediseases

Nearly the entire sample claimed some knowledge or aware-ness of ticks (99.2%). While most people had heard of Lyme disease(98.7%), only 44.1% of respondents could identify any other tick-borne disease, including those more likely to occur in this region.Those in rural parks were significantly (p < 0.001) more likely to beable to name tick-borne diseases other than Lyme disease (here-after ‘other tick-borne diseases’) (68.2%) compared to respondentsin suburban (34.1%) and exurban (34.2%) parks. Awareness of LST-associated diseases remained low across all park types; however,respondents in exurban parks (19.0%) were significantly more likelyto demonstrate at least some level of awareness of the LST com-pared to other park types.

The overall level of concern of being bitten by a tick at each parkwas low across all parks types, with only 15.6% of all respondentsreporting being “very concerned”. Similarly, the overall percent-age of respondents who were “very concerned” with the threat ofcontracting Lyme disease was 20.6%. While relatively low overall,there were significant differences in the level of concern regardingthe risk of other tick-borne diseases across park types (p = 0.003).Those in suburban parks were more likely to be “not at all” con-cerned with other tick-borne diseases (88.6%) compared to exurban(75.8%) and rural (60.6%) parks. The perceived threat of contract-ing Lyme disease while at the park significantly differed by age(p = 0.01), with the age of 19–29 more likely to report being “notat all concerned” (71.1%) and less likely to report being “very con-cerned” (2.6%) compared to older age groups (Supplemental Table5).

Tick-borne disease prevention behaviors

The 4 most commonly reported preventive behaviors performedacross the entire study sample were: choosing to walk the centerof trails (54.6%), performing regular tick checks (52.5%), avoiding

wooded or grassy areas (50.8%), and using any type of chemicalinsect repellent (47.1%). The least commonly reported behaviorsincluded tucking pants into socks (16.8%), and wearing long pantsor long-sleeved shirts (24.8%). When asked how each participantchose to remove a tick once it had become attached, 60.1% acknowl-edged using tweezers (Supplemental Table 6), the recommendedmethod of tick removal (CDC, 2006).

There were significant differences in multiple behaviors associ-ated with decreased risk in acquiring a tick-borne disease across thehuman land-use gradient (Table 2). Those in exurban parks weremore likely to perform regular tick checks following outdoor activ-ities (69.6%) compared to rural (59.1%) and suburban (34.1%) parks(p < 0.001). There were also significant differences in the applica-tion of chemical insect repellents by land-use stratification. Thosein exurban parks were more likely to use some type of repel-lent (64.6%) compared to rural (50.0%) and suburban (30.8%) parks(p < 0.001). Of those who reported using insect repellent, more peo-ple in suburban (75.0%) and exurban (74.5%) parks could identifywhether DEET was an active ingredient (p = 0.003). Overall, the useof permethrin-based repellent was low and did not differ apprecia-bly by park (∼15%). Certain types of avoidance behaviors showedsignificant differences across park types. Respondents in suburbanparks were more likely to avoid wooded or grassy areas whereticks may be found (61.5%) compared to exurban (44.3%) and rural(42.4%) parks (p = 0.03).

Results from the multivariate analysis of data across all parktypes combined show that respondents from exurban parks weremore likely to perform frequent tick checks (aOR = 3.43; 95% CI,1.75–6.69) and use any type of insect repellent (aOR = 2.51; 95%CI, 1.21–5.20) compared to other park types (Table 3). Further,respondents who reported being “very concerned” with being bit-ten by a tick were much more likely to perform frequent tickchecks (aOR = 30.14; 95% CI, 6.21–146.41), wear protective clothing(aOR = 3.44; 95% CI, 1.66–7.12), and use any type of insect repellent(aOR = 8.30; 95% CI, 3.20–21.53) compared to those who were “lessconcerned” or “not at all concerned”. Finally, only respondents whoreported being frequent visitors (more than once per week) to thepark were more likely to engage in vegetation avoidance behaviors(aOR = 2.25; 95% CI, 1.13–4.46) compared to those who visited thepark less frequently.

Discussion

Both risk and incidence of tick-borne diseases tend to be spa-tially heterogeneous (Eisen and Eisen, 2008), and human incidenceof these diseases is likely the end result of numerous ecological,demographic, and behavioral phenomena that occur over time andspace. Thus to understand this variation in disease occurrence, it isnecessary to quantify variation in both environmental risk (e.g., thedensity of ticks infected with pathogens in an area) and behavioralrisk (e.g., the behaviors that cause a person to suffer an infected tickbite). While several ecological studies have recently attempted tounderstand what factors lead to spatial variation in environmentalrisk of LST-associated disease (Yabsley et al., 2005; Brown et al.,2011), factors that may lead to spatial variation in behavioral riskare less well understood. Here, we found a significant disparitybetween the levels of knowledge, awareness, perceptions of risk,and preventive behaviors among recreational park visitors acrossa region with spatially variable risk of exposure to LST-associateddiseases.

A majority of respondents in our study had some prior con-tact with ticks, and nearly all participants knew that ticks couldspread disease in humans (97.5%). Numerous studies regardingtick-borne disease awareness have been conducted in areas whereLyme disease is endemic and have suggested that individuals in

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Table 2Risk perceptions and tick-borne disease prevention behaviors across the suburban-rural gradient.

Variable All parks (n = 238) Park type, no. (%) p value

Suburban (n = 91) Exurban (n = 79) Rural (n = 66)

Perceived susceptibilityConcerned about being bitten 0.53

Very 37 (15.6) 11 (12.1) 12 (15.2) 14 (21.2)Somewhat 75 (31.5) 30 (33.0) 23 (29.1) 22 (33.3)Not at all 126 (52.9) 50 (55.0) 44 (55.7) 30 (45.5)

Concerned about contracting Lyme disease 0.23Very 49 (20.6) 19 (20.9) 13 (16.5) 17 (25.8)Somewhat 53 (22.3) 19 (20.9) 15 (19.0) 19 (28.8)Not at all 136 (57.1) 53 (58.2) 51 (64.6) 30 (45.5)

Concerned about contracting other tick-borne diseases 0.003Very 14 (5.9) 6 (6.6) 2 (2.5) 6 (9.1)Somewhat 43 (18.1) 16 (17.6) 7 (8.9) 20 (30.3)Not at all 181 (76.1) 69 (75.8) 70 (88.6) 40 (60.6)

Prevention behaviorsPerform regular tick checksa 125 (52.5) 31 (34.1) 55 (69.6) 39 (59.1) <0.001Protective clothing

Long sleeves 59 (24.8) 17 (18.7) 24 (30.4) 18 (27.3) 0.19Tuck pants into socks 40 (16.8) 11 (12.1) 17 (21.5) 12 (18.2) 0.25Light colors 80 (33.6) 28 (30.8) 30 (38.0) 20 (30.3) 0.52

Use of insect repellent 112 (47.1) 28 (30.8) 51 (64.6) 33 (50.0) <0.001DEETb 83 (74.1) 21 (75.0) 38 (74.5) 24 (72.7) 0.003Permethrinb 18 (16.1) 4 (14.3) 10 (19.6) 4 (12.1) 0.11Organicb 20 (17.9) 4 (14.3) 7 (13.7) 9 (27.3) 0.12

AvoidanceWooded areas 121 (50.8) 56 (61.5) 35 (44.3) 28 (42.4) 0.03Walks center of trails 130 (54.6) 48 (52.8) 47 (59.5) 34 (51.5) 0.56

a Defined by “always” or “most of the time”.b Of those who used any insect repellent.

these regions are relatively knowledgeable and generally aware ofthe health threats posed by this public health problem (Phillipset al., 2001; Gould et al., 2008). Lyme disease remains the pre-dominant tick-borne disease in the U.S., although, rates in Missouriare low (Bacon et al., 2008). In our study, most individuals wereaware of Lyme disease (98.7%); however, many were not awareof any other tick-borne diseases considered endemic to this studyregion (Supplemental Table 4). We found significant differences inthe awareness of other tick-borne diseases across park types, withthose in rural parks more likely to be aware that these other dis-eases exist. This disparity may be due, in part, to greater amountsof time spent outdoors as a result of occupational or recreationalopportunities. These results also suggest that knowledge of Lymedisease in the U.S. has likely pervaded into regions such as Missouri,where it is not considered endemic, potentially at the expense ofmore relevant knowledge of local tick-borne disease threats suchas ehrlichiosis.

A core tenet of the theoretical constructs underpinning manypublic health risk reduction programs is the idea that awarenessand knowledge of a health threat, combined with risk percep-tions, are important prerequisites of the adoption of risk mitigationbehaviors (Glanz et al., 2008). Results from the multivariate anal-ysis seem to support this premise, suggesting that high levelsof concern with receiving a tick bite was significantly predictiveof performing frequent tick checks, wearing protective cloth-ing, and using chemical insect repellents (Table 3). However,an examination of risk perceptions across parks showed thatthe perceived threat of exposure to ticks or tick-borne diseaseswas uniformly low across all park types. A similar divergencehas been noted in studies conducted in other tick-borne diseaseendemic regions of the country (Hallman et al., 1995; Herrington,2004). In our study, perceived susceptibility of contracting Lymedisease while in the parks remained higher than contractingother more locally relevant tick-borne diseases, which is likely

Table 3Multivariate analyses of factors associated with prevention practices.

Behavior Predictor(s) aOR (95% CI)*

Tick check Exurban park 3.43 (1.75, 6.69)***

Tick bite 3.58 (1.47, 8.74)**

Very concerned with tick bite 30.14 (6.21, 146.41)***

Very concerned with other tick-borne diseases 6.40 (1.14, 35.82)Use of tweezers to remove tick 2.10 (1.08, 3.90)Hiking while at the park 0.32 (0.16, 0.65)**

Avoidance Several visits per week 2.25 (1.13, 4.46)

Clothing Very concerned with tick bite 3.44 (1.66, 7.12)***

Use of any repellent Suburban 0.48 (0.24, 0.97)Exurban 2.51 (1.21, 5.20)Non-white 7.07 (1.19, 42.06)Very concerned with tick bite 8.30 (3.20, 21.53)***

* p < 0.05 unless otherwise noted.** p < 0.01.

*** p < 0.001.

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a consequence of low overall awareness of these other diseasethreats.

The chance of disease transmission is a function of the proba-bility of human exposure to an infected tick, which can be reducedwith the utilization of commonly recommended preventive behav-iors (CDC, 2012). Here, we found significant differences betweenboth the frequency and type of preventive behaviors performedin recreational parks across a gradient of human land use. Thosein exurban parks were more likely to perform frequent tick checksand use insect repellents, while those in suburban parks were morelikely to avoid tick habitats (Table 2). Conversely, those in ruralparks were less likely to avoid tick habitat, which is troublesomegiven that rural areas have been shown to be risk factors for tick-borne disease (Belongia et al., 1999). This may be due, in part, to therecreational intentions of park visitors in rural areas (e.g. hiking inwilderness areas with poor visible paths).

Observed differences in behaviors across parks, coupled withresults from the multivariate analysis, demonstrate a unique set ofpotential mediating factors on the uptake of preventive behaviorsthat may be inherent to outdoor recreational parks. For exam-ple, different parks lend themselves to different opportunities forrecreational activities (e.g. hiking through wooded areas or ridinga bike on a paved path), which may in turn influence the extentto which personal protective behaviors are either performed or notperformed. Few respondents reported wearing protective clothing,which may be influenced by characteristically high temperaturesduring summer months as well as with particular activities (e.g.jogging) that may discourage some from these types of preven-tive practices. Gould et al. (2008) found that certain behaviorswere less likely to be performed because they were viewed astoo troublesome (Gould et al., 2008). We found that study partic-ipants engaged in a wide variety of park activities (SupplementalTable 4), which may explain variation in the type of preventivebehaviors performed and may ultimately contribute to alteredlevels of personal risk. Several studies have demonstrated thatparticular park activities (e.g. hiking) may differentially influencetick-borne disease risk (Smith et al., 2001; Richter and Matuschka,2011).

It is important to note potential limitations of this study. Weascertained preventive behaviors by self-report, which may be sub-ject to reporting and recall bias. In addition, since these behaviorswere not directly observed and relied on self-report, it is impos-sible to determine whether they were performed correctly. Parkswere chosen to represent a subsample of a larger research projectinvestigating the ecology of LST-associated pathogens in the region,so study sites were not chosen completely at random. Individ-uals were recruited as part of a non-random convenience sample,which may diminish the generalizability of the point estimatesproduced. However, parks were chosen that allowed for similarcontact opportunities at trail heads and parking lots, thus havinglittle impact on the internal validity of the statistical comparisonsbetween parks.

The results of this study may be used to more effectivelyguide future public health promotion campaigns. In recent years,collaborations between public health officials and park rangershave demonstrated that such partnerships may be valuable toolsfor improving health promotion among park visitors (Wong andHiggins, 2010). Results from theory-based public health interven-tions have shown that visual cues that create parallels betweenpreventive behaviors and common everyday activities (e.g. per-forming a tick check while showering after a park visit) are effectivecomponents of health promotion programs (Daltroy et al., 2007).While not quantified specifically, many parks in the study wereobserved to have bulletin boards at trail heads that providedbasic information about health threats, including tick-borne dis-eases. These locations may serve as relatively inexpensive, highly

visible focal points for the dissemination of these and other perti-nent health promotion messages. The results from our study may beuseful for refining such messages. For example, in rural areas, whereuse of repellents containing permethrin was low, public informa-tion displays could emphasize the efficacy of this repellent relativeto other compounds. In addition, parks where avoidance behaviorswere not commonly practiced may benefit from tailored messagesfor park visitors (e.g. park maps) demonstrating where tick habitatmay be found.

Tick-borne disease prevention campaigns are doomed to failureunless at-risk populations are willing to accept them (Hayes et al.,1999). Our study identifies barriers and misconceptions amongindividuals in recreational parks that can be used to create effective,theory-based interventions. We found that significant disparitiesexist in the awareness of locally pertinent disease threats, percep-tions of personal risk, and the utilization of recommended personalprevention behaviors in recreational parks across a gradient of vari-able tick-borne disease risk. Ultimately, to successfully curb thegrowing threat posed by LST and other emerging tick-borne diseasethreats, behavioral exposure risk must be reduced by addressingspecific gaps in both perceptions and prevention.

Acknowledgments

We thank Lindsay Brewster, Travis Mohrman, and numerousrecreational park managers for assistance with this study. Fundingwas provided by Environmental Protection Agency grant 834495and by the North Central Integrated Pest Management Center ofthe United States Department of Agriculture. The authors declareno competing interests.

Appendix A. Supplementary data

Supplementary data associated with this article can be found, inthe online version, at doi:10.1016/j.ttbdis.2013.01.001.

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