Zoonotic Infections Among Employees from Great Smoky Mountains and Rocky Mountain National Parks,2008–2009

Introduction

T he National Park Service (NPS) aims to preserve the natural resources of its parks while leaving natural ecosystems intact with minimal interference. These ecosystems include a variety of native wildlife and associated arthropods which may carry pathogens that cause zoonotic infections from direct animal or vector-borne contact (Rayor 1985; McLean et al. 1989; New et al. 1993; Taylor et al. 1997; Gese et al. 1997; Mills et al. 1998; Rhyan et al. 2001; Riley et al. 2004; Reeves 2007; Greger 2007; Winters et al. 2008).

Sporadic cases and outbreaks of zoonotic diseases have been reported previously among NPS employees and visitors. In November 2007, a wildlife biologist from Grand Canyon National Park died of pneumonic plague following transport and necropsy of an infected mountain lion carcass (Wong et al. 2009). Outbreaks of tick-borne relapsing fever have occurred among visitors staying in rustic cabins in Grand Canyon National Park (Boyer et al. 1977; Paul et al. 2002), and adjacent to Rocky Mountain National Park (ROMO; Trevejo et al. 1998). NPS employees may have prolonged exposure to wildlife and arthropods in occupational settings, possibly placing them at increased risk for zoonoses circulating within the parks. For visitors, national parks often represent unique, unfamiliar environments, and many might unknowingly participate in high-risk behaviors. However, because infected visitors may not become ill and seek care until they return home, epidemiologic links to where exposure occurred may be missed. Understanding the variety of pathogens impacting NPS staff may therefore help inform the risks for visitors as well as employees.

Materials and Methods

To determine zoonotic disease risks present at both Great Smoky Mountains (GRSM) and ROMO National Parks, we quantified background seroprevalence and measured incident infections to select zoonotic pathogens among a cohort of NPS staff members through two serosurveys conducted a year apart (2008–2009); questionnaires were also administered on potential risk factors and clinical features.

Results

Discussion

This study described prior and incident zoonotic infections among employees at the GRSM and ROMO National Parks during 2008–2009. Though other studies have investigated zoonotic disease risks among national parks (Boyer et al. 1977; McLean et al. 1989; New et al. 1993; Gese et al. 1997; Mills et al. 1998; Paul et al. 2002; Reeves 2007; Levine et al. 2008; Wong et al. 2009), none have addressed the breadth of pathogens evaluated here. These parks were selected due to their popularity among visitors and the likelihood of the presence of local zoonoses. GRSM is the most visited U.S. national park, averaging 10 million visitors per year and employing >300 permanent staff. It spans parts of Tennessee and North Carolina, states which report the greatest numbers of Rocky Mountain spotted fever (RMSF) cases (Adjemian et al. 2009; Openshaw et al. 2010). ROMO also receives millions of visitors each year, and maintains >230 permanent staff. Zoonoses previously detected in ROMO include Colorado tick fever virus, plague, tularemia, and tick-borne relapsing fever (Trevejo et al. 1998).

NPS employees have unique occupational risks for acquiring zoonotic diseases. Here, NPS employees reported spending 40% of their workday outdoors, and with primary job duties that included vegetation management, road and grounds maintenance, wildlife management, trail maintenance, and search and rescue. Similarly to other outdoor occupations, NPS employees had substantial and often prolonged exposure to ticks and mosquitos, as evidenced by noticeable and frequent insect bites (80%), and the presence of ticks on their skin or clothes (32%; Piacentino and Schwartz 2002; Cinco et al. 2004; Buczek et al. 2009). Despite this, insect repellent use was only rarely reported (Bartosik et al. 2008). As was previously observed in forestry workers, the risk of infection increased with age (Buczek et al. 2009). Additionally, NPS workers demonstrated the potential for direct zoonotic exposure through contact with dead rodents (20%), and felid or canid bites (4–6%), as is often seen in wildlife officers and veterinarians. Notably, NPS resource managers and law enforcement ranger/rescue crew members were at highest risk for incident zoonotic infections, suggesting a possible need for division-specific prevention measures.

We found evidence of high rates of prior zoonotic infections among NPS employees, in many cases exceeding expected seroprevalence rates for the general population. The seroprevalence of California serogroup viruses (31%), B. henselae (25%), spotted fever group rickettsiae (21%), and flaviviruses (5%), were greater than what is reported in the literature (Yevich et al. 1995; Reisen and Chiles 1997; Spach and Koehler 1998; Hilton et al. 1999; McCall et al. 2001; Marshall et al. 2003; Stramer et al. 2005). California serogroup bunyavirus infections detected in ROMO predominantly showed specific serological reactivity to Jamestown Canyon virus, consistent with the regional distribution of snow pool mosquito vectors, whereas those detected in GRSM were predominantly seroreactive to La Crosse virus, consistent with the distribution of Aedes triseriatus vectors (Campbell et al. 1992). Prior infection with several rare and unexpected pathogens was also identified, including the causative agents of anthrax, tularemia, and Q fever. Agents detected at levels similar to those previously reported included T. gondii (Jones et al. 2007), Colorado tick fever virus (McLean et al. 1989), E. chaffeensis, and A. phagocytophilum (Yevich et al. 1995; Demma et al. 2005), though A. phagocytophilum, which was observed in 7% of ROMO participants, is not known to occur in Colorado (Demma et al. 2005). While >7% of participants demonstrated possible prior infection with Brucella spp., these results could not be confirmed due to the potential for cross-reactivity with other bacteria, given the titer levels observed (Al Dahouk et al. 2003a, 2003b). As expected, there was no serologic evidence of prior infection with B. burgdorferi, which is not endemic in either park (Bacon et al. 2008), B. hermsii, which is most commonly transmitted to persons staying in poorly maintained rustic cabins (Boyer et al. 1977; Trevejo et al. 1998; Paul et al. 2002), or Y. pestis, which is rare, with <10 U.S. human cases reported annually (Gage and Kosoy 2005). While we cannot infer whether baseline infections occurred at the current park of employment, the background seroprevalance provides a unique cross-sectional view of this population.

Incident infections with spotted fever group rickettsiae were noted in both parks. GRSM runs though Tennessee and North Carolina, which are among the top states for the reported incidence of RMSF (Openshaw et al. 2010). While a focus of unusually severe and fatal RMSF has been noted in western Tennessee, a milder focus has been identified in North Carolina, fueling speculation that some RMSF reports in this state may actually reflect less pathogenic spotted fever group rickettsiae circulating in the area, such as R. parkeri or R. amblyomii (Apperson et al. 2008; Adjemian et al. 2009). Spotted fever group rickettsiae also demonstrate cross-reactivity with R. typhi and R. prowazekii, both typhus group rickettsiae agents (Hechemy et al. 1989).

Incident infection was also detected for Leptospira spp., which causes leptospirosis and ranges from subclinical or mild (∼90% of infections) to severe illness (Stern et al. 2010). Leptospiral infection occurred in 6% of GRSM participants, and was significantly associated with reptile exposures and mildly associated with rodent contact. While small mammals are considered to be the only primary maintenance hosts that can transfer Leptospira to humans, Leptospira have been identified in >180 species, including reptiles (Guerra 2009). Incident infection with B. henselae, a flea-borne pathogen, was 18 times greater among those reporting contact with deceased canids. When an animal dies, ectoparasites that can carry B. henselae might jump to the nearest host available, including humans, facilitating disease transmission. Infection can also occur from contact with infected bodily fluids or tissues (Breitschwerdt et al. 2010). While canids can be infected with B. henselae (Diniz et al. 2009), their role as a reservoir for Bartonella spp. remains unclear (Chomel et al. 2006). It is possible that this finding may also reflect serologic cross-reactivity with other Bartonella spp., such as B. rochalimae and B. vinsonii berkhoffii, which have close associations with wild and domestic canids (Henn et al. 2009).

Isolated incident infections with zoonotic pathogens were also detected. Incident infection with B. anthracis, the cause of anthrax, occurred in an individual from GRSM, though B. anthracis is not known to occur in this geographic region, suggesting that exposure likely occurred elsewhere (Blackburn et al. 2007). Lastly, incident exposure to T. gondii, which causes toxoplasmosis, occurred in a GRSM participant who reported owning a cat at home. Cat feces or undercooked meat are the main sources of T. gondii exposure (Elmore et al. 2010), though transmission is relatively common (Dubey and Jones 2008), making it difficult to distinguish how exposure occurred.

When evaluated collectively, contracting any incident infection during the study period was significantly more likely to occur among NPS resource managers and law enforcement ranger/rescue crew members, and in individuals with contact with fish tissues. Given that these factors were not associated with increased risk for any one particular agent, it is likely that they serve as a proxy for other factors that are more important in the causal pathway of exposure to zoonotic diseases. Resource managers and law enforcement ranger/rescue crew members are probably more likely to spend time participating in higher-risk outdoor areas and activities given the nature of their job duties, while individuals who reported contact with fish tissues likely spend more recreational time participating in outdoor activities such as fishing, thus increasing their risk for exposure.

This study is subject to several important limitations. The small sample size limited our ability to detect incident infections and meaningfully analyze some risk factors for exposure. The exposures detected were not necessarily confined to the parks where the participants worked, as NPS employees travel often due to transfers between parks, for personal travel, and because they have a predilection for outdoor activities. Additionally, while exposures to some zoonoses induce lifelong immunity, an absence of antibody responses does not exclude prior exposure, particularly if it occurred many years ago. Though inferences about geographic distribution and other risk factors for staff are limited, park-specific similarities and differences are interesting to note and may help guide future research.

Conclusions

While risks to park visitors do not necessarily equal those of NPS employees, the prevalence and incidence described here increase our understanding of pathogens potentially circulating within both parks, and can be used to inform public health interventions for both staff and visitors. Although most zoonotic disease prevention programs rely on environmental control interventions (e.g., area-wide acaricides and animal control), and personal protection (e.g., the use of repellent and protective clothing) to reduce risk, NPS employees must almost always rely on personal protective behaviors to maintain the NPS mission of preserving the park unimpaired. Therefore, educational programs emphasizing routine insect repellent use and protective clothing should target both visitors and staff. Such training programs should be tailored to specific occupations or job categories, and all should highlight the common zoonoses detected here and their associated high-risk activities in order to increase awareness.