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ABSTRACT |
 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Previous attempts to identify high-risk occupational groups for HCPS in North America by testing individuals for serologic evidence of exposure to SNV found little to no evidence of increased virus exposure.5–8 Because of the low incidence of asymptomatic infection, SNV antibodies are rarely detected in healthy persons and estimation of seroprevalence has proven of limited value as an indicator of population risk. Similarly, it is difficult to extrapolate disease risk from seroprevalence studies in rodent populations that do not concurrently consider domestic, recreational, or occupational activities of susceptible humans.9–13
A review of HCPS cases in the Centers for Disease Control and Prevention’s (CDC) registry in 2000 indicated that 16% of HCPS cases for whom exposure circumstances could be determined were likely a result of occupational exposure to SNV (CDC, unpublished data). Thirteen (27%) of 49 HCPS cases identified in California through 2007 were believed to have been exposed during work activities. Occupations included a utility worker, graduate student/field biologist, camp counselor, oil company employee, ranch hand, sanitation worker, social service volunteer, truck driver, and employees of the US Forest Service (USFS).
Forestry workers have been identified as an occupational group with elevated risk of infection with hantaviruses in Europe and Scandinavia.14–18 The Pacific Southwest Region of the USFS (Region 5) employs 
8,000 persons at 18 National Forests covering 20 million acres in California. A substantial proportion of USFS employees perform work, such as fire and timber management, in sylvatic areas where rodents are abundant and where work activities and living conditions bring them into close and frequent contact with wild rodents. This study evaluated environmental factors present at USFS facilities in California that could indicate an occupational risk of HCPS for USFS workers. The objective was to assess and document evidences of rodent infestation and SNV activity at facilities where USFS employees work and reside. These observations were subsequently used as a foundation for recommending and implementing specific risk mitigation measures and directing employee preventive education.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Each study site was visited once between September 2004 and May 2005. All accessible USFS buildings (offices, barracks, storage, etc.) at each site were inspected for potential for rodent infestation and evidence of rodent activity. Potential rodent infestation was defined as any structural deficiencies that would permit rodent entry (e.g., holes in exterior walls) and the availability of rodent attractants such as food and nesting material.
Evidence of rodent activity was characterized as indirect or direct. Indirect evidence of rodent activity included feces, nests, chew marks, or grease marks along rodent runways. Indirect evidence served as a preliminary indicator of previous or current rodent activity and was recorded as present or absent but was not quantified. Direct evidence of rodent activity was assessed by trapping. A minimum of 48 Sherman live-traps (H. B. Sherman Traps, Tallahassee, FL) baited with rolled oats were set overnight at each site. The majority of traps were placed outside the structures, immediately around the perimeter of the buildings or in undeveloped habitat up to 50 m from the buildings. Traps were placed within accessible buildings when indirect evidence of rodents was noted. Target species included the genera Peromyscus, Microtus, and Reithrodontomys known to harbor hantaviruses in California, viz. SNV, Isla Vista, and El Moro Canyon, respectively. Other species of rodents (e.g., Tamias) that were collected were considered non-targets, were released at the point of capture, and were not included in surveillance totals. Trap success was used as a comparative indicator of rodent density and calculated as the ratio of the number of rodents collected to the number of traps set, less the number of traps that contained non-target rodents or were otherwise disturbed.
Rodents were anesthetized with isoflurane and identified to sex, age, and species. Approximately 0.3 mL of blood was collected by micropipette from the retrobulbar sinus or by intracardiac puncture. Blood specimens were tested for immunoglobulin G reactive to SNV recombinant nucleocapsid protein antigen by enzyme-linked immunosorbent assay (ELISA) according to a standard protocol.19 After sampling, the rodents were humanely euthanatized, with the exception of sites at which long-term mark–recapture studies were being conducted. At these sites, rodents were released outdoors near the point of capture.
USFS employees available at the time of the evaluation were asked whether they had received training in preventive measures for rodent-borne diseases. If so, they were asked to describe the general content (e.g., disinfection methods), form (e.g., written handout), and frequency (e.g., annually) of the training. Based on these responses, facilities were categorized as having employees who had little to no training in hantavirus prevention; indicated that hantavirus information was included in their Job Hazard Analysis and/or written information was provided to them but they received no formal training; were aware of or received basic hantavirus prevention training; or were aware of or received extensive hantavirus prevention training.
Results of inspection, surveillance, and testing were summarized and reported to facility staff and district rangers at each site studied. General and specific recommendations for risk mitigation and rodent control were provided.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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; Figure 1). Primary site designations were three fire stations, two fire lookouts, five ranger stations, four research facilities, and four work centers, although most sites served multiple concurrent functions. Study sites ranged from < 1 to 5 acres in size. Eight sites operated seasonally and 10 sites operated year-round. Seasonal sites were located between 1,033 and 2,342 m elevation (median = 2,090 m), whereas sites in operation year-round were located between 366 and 1,832 m (median = 1,500 m). Two sites were in the alpine habitat, 13 in coniferous forest, 2 in hardwood forest, and 1 in sage/scrub brush habitat; no sites were classified as chaparral or grassland. Seventeen sites had on-site housing for staff. The number of employees ranged from 1 to 127 per facility (5–1,182 person-months/yr). Seasonal employees ranged from 1 to 81 per facility (5–486 person-months/yr) and year-round employees ranged from 0 to 70 per facility (0–840 person-months/yr). Staff at the year-round facilities accounted for 4,363 (93%) of 4,684 total person-months/yr at all study sites.
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One night of trapping was conducted at each site, with the exception of Site 13, where two successive nights of trapping were conducted. The number of traps set ranged from 48 to 260 per site. At least one rodent was collected at 16 sites; no rodents were collected at Site 1 or Site 3. A total of 1,899 trap-nights were conducted; of these, 1,860 effective trap-nights were available for collection of target species after adjusting for captures of non-target rodents. Median trap success for the 18 sites was 13.5%; trap success was highest (54%) at Site 7, a fire lookout. Cumulative trap success was 15.7% at sites located at elevations < 1,600 m (N = 9) and 23.5% at sites above 1,600 m (N = 9). Cumulative trap success was 39.5% at the four study sites located at elevations > 2,100 m. Cumulative trap success at facilities open year-round was 17.0% compared with 22.4% at facilities open seasonally.
A total of 343 rodents were collected: 283 deer mice (Peromyscus maniculatus), 37 brush mice (Peromyscus boylii), 12 voles (Microtus spp.), 4 western harvest mice (Reithrodontomys megalotis), 3 California mice (Peromyscus californicus), 2 piñon mice (Peromyscus truei), and 2 western red-backed voles (Clethrionomys californicus). Deer mice were captured at 15 sites. Trap success for deer mice was 13.3% at year-round facilities compared with 20.5% at seasonal facilities. Deer mice were the only target rodent species collected at two (25%) of eight sites below 1,600 m elevation and at five (62.5%) of eight sites above 1,600 m. Deer mice were the only species collected at 1 of 2 alpine habitat facilities and 6 of 13 coniferous habitat facilities. Deer mice represented 31 (94%) of 33 rodents captured indoors.
Serum specimens were collected and tested from 307 of the 343 rodents captured. Thirty-four captures represented repeated trapping of the same rodent on successive trap nights, and specimens were unobtainable from an additional two rodents. Antibodies to SNV were detected in 50 (20%) of 255 deer mice and 1 (8.3%) of 12 voles; SNV antibodies were not detected in any of the other rodent species tested. Seroprevalence of SNV in deer mice ranged from 0% to 36% per site. Cumulative seroprevalence in deer mice was 15.5% (range, 0–33%) at sites below 1,600 m elevation and 22.1% (range, 0–36%) at sites above 1,600 m. The cumulative seroprevalence among deer mice was 18.8% at facilities open year-round and 20.8% at facilities open seasonally. SNV antibodies were detected in 5 (16%) of 31 deer mice captured indoors compared with 45 (20%) of 224 captured outdoors.
Occupations of USFS employees questioned about rodent-borne disease preventive training included battalion chiefs, fire crew, office administrators, district rangers, and safety officers. The number of employees questioned ranged from one to five per study site. Based on the majority of responses from employees, four sites (22%) reported little to no training; seven sites had written information included in their Job Hazard Analysis or elsewhere but no organized training; and seven sites had basic hantavirus prevention training. There were no sites at which employees had extensive training in preventive strategies for rodent-borne diseases. Five of 10 year-round facilities had organized hantavirus prevention training compared with only two of eight seasonal facilities. Employees professed the most knowledge about disinfection techniques (e.g., applying bleach to a potentially contaminated surface). Knowledge of elements of disease, including transmission and clinical symptoms, was less common.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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In this study, evidence of rodent activity and potential or actual ingress into buildings were present at all USFS facilities evaluated. Facilities on public lands such as National Forests are frequently located in areas with minimal development where natural vegetation sustains numerous sylvatic rodents. The food, equipment, and garbage of staff and visitors can further enhance the effective carrying capacity of a given area because additional foodstuffs and harborage are artificially introduced. Furthermore, these additional resources may be more readily and consistently available throughout the year compared with natural resources, possibly offering incentive for rodents to frequent the peri-domestic environment.
Rodents belonging to target species were collected at 16 of 18 sites. Because study sites were selected in part on recommendations of biologists and requests by USFS personnel, sites with recognized rodent activity may have been preferentially included in the study. Each facility in this study was surveyed only once, and data reflect rodent activity only under the specific conditions at the time of trapping. Trap success is only an approximate indicator of rodent abundance and population density is only one of numerous factors—including temperature, precipitation, lunar phase, and season—that contribute to trap success.22
Although repeated, standardized surveillance is necessary to reliably estimate rodent density, limited rodent surveillance can nevertheless lend insights into the relative abundance of different rodent species that share habitat. The overall crude trap success for deer mice (P. maniculatus) was 15.2% in this study, notably higher than other studies (1.7–5.5%).23–25 Deer mice were the predominant or only rodent species collected at most of the study sites. Reduced species diversity may facilitate virus transmission by increasing intraspecific contact—and opportunity for virus transfer—and reducing competition for limited resources from vector-incompetent species.26 Thus, the risk of hantavirus exposure for USFS staff may be substantial even in areas or under working conditions where rodent contact is infrequent if deer mice are the predominant rodent species present.27
The cumulative seroprevalence of SNV in deer mice in this study was 19.6%; this figure is appreciably higher than the California statewide average of 12.3%, but comparable to 20.0% for all hantavirus surveillance conducted to date in California USFS lands (California Department of Public Health, unpublished data). Seroprevalence of SNV in deer mice is useful as an approximate population indicator of hantavirus risk, although individual rodent seroreactivity is not directly referable to active infection and shedding of virus.28 Maximal shedding occurs during the first few weeks after infection, perhaps preceding seroconversion.29–31 Although deer mice are believed to remain infected for life, serologic antibodies may persist beyond the period of active shedding.30 Detection of serum antibodies in 20% of deer mice in this study indicates that SNV was present and actively transmitted among rodents but provides only a very crude assessment of the immediate risk of infection for humans.
This study did not directly address risk of hantavirus exposure for USFS staff who incidentally encounter deer mice while performing outdoor field duties. Although hantavirus is reservoired in wild rodents, HCPS cases are frequently associated with exposure to rodent excreta in a confined, poorly ventilated indoor space.32 The risk of infection is likely lowered outdoors where constant air turnover and UV penetration reduce the concentration and viability of virus present. In this study, evidence of rodent ingress (i.e., feces) was found not only in infrequently occupied storage areas, but also in locations such as offices and barracks where human activity is common and constant. Education and training on rodent exclusion and personal protective measures should not be limited to field personnel, but encompass all USFS staff, including those who work exclusively indoors.
Environmental factors typically associated with risk for hantavirus transmission (i.e., more deer mice, higher seroprevalence) tended to occur at seasonal sites at higher elevations (e.g., fire lookouts). The fewer staff who work at these sites may be exposed to a substantial ambient virus load when they re-open facilities that mice occupied over the winter. Seasonal staff should be instructed in procedures for decreasing risk both before closing (e.g., removing rodent incentives and properly sealing structures) and during re-opening (e.g., thoroughly ventilating closed structures before entering.) In addition, the surrounding habitat and support structures (sometimes including restrooms and shelters) at these sites may be visited by large numbers of backpackers, skiers, and other members of the public for whom education of rodent-borne viral diseases and instructions for personal protection should be provided.
Knowledge and awareness about hantavirus prevention varied among employees both between and within sites. Year-round employees were more likely than seasonal employees to know about elements of disease, including transmission and clinical symptoms, and to have received training on prevention practices. However, because general staff awareness was assessed only by individual interview of personnel available during site visits, the breadth, validity, and efficacy of employee education was not assessed. Nevertheless, this study revealed several common deficiencies in employees’ understanding. For example, although surface disinfection with a diluted bleach or quaternary ammonium solution was the most common preventive measure practiced, knowledge of this and other techniques did not necessarily ensure that they were implemented appropriately. Improved understanding of the ecology of SNV and the situations that increase the risk of rodent-to-human virus transmission would allow employees to better comprehend the specific intent of preventive measures and may better motivate their habitual practice.
HCPS is a public health disease for which there is no vaccine, pharmacologic prophylaxis, or specific treatment currently available. Although relatively uncommon, HCPS is frequently fatal, and measures to minimize risk of infection should be approached in a rational and consistent manner. Disease prevention requires reasonable efforts by employers to inform employees of the health risks posed by rodents infected with SNV, other hantaviruses, and other zoonotic agents and to provide a safe rodent-free indoor work environment. Through simple and relatively inexpensive improvements, such as sealing conduit exits, clearing brush around buildings, and maintaining a regular trapping schedule, potential exposure to rodents and disease agents they carry can be dramatically reduced.
Received August 20, 2007. Accepted for publication October 23, 2007.
Acknowledgments: The authors thank Joe Burns, Larry Bronson, Dick Davis, Jonathan Kwan, Charlie Smith, and Jim Tucker (Vector-Borne Disease Section, California Department of Public Health) and Jason Stull (Veterinary Public Health Section, California Department of Public Health) for assistance with field surveillance and Barryett Enge (Viral and Rickettsial Disease Laboratory, California Department of Public Health) for laboratory assistance.
Financial support: This study was partially funded through a cost-share agreement between the California Department of Public Health and the US Department of Agriculture Forest Service.
* Address correspondence to Curtis L. Fritz, California Department of Public Health, MS 7307, PO Box 997377, Sacramento, CA 95899–7377. E-mail: cfritz{at}cdph.ca.gov 
Authors’ addresses: Jessica R. Levine and Curtis L. Fritz, California Department of Public Health, Division of Communicable Disease Control, Sacramento, CA 95899–7377 (Ms. Levine’s current address: School of Veterinary Medicine, University of California, Davis, CA 95616). Mark G. Novak, California Department of Public Health, Division of Communicable Disease Control, Elk Grove, CA 95624.
Reprints requests: Curtis L. Fritz, California Department of Public Health, MS 7307, PO Box 997377, Sacramento, CA 95899-7377, Telephone: 916-552-9730, Fax: 916-552-9725, E-mail: cfritz{at}cdph.ca.gov.
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| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
