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Seroepidemiologic Studies of Hantavirus Infection Among Wild Rodents in California

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Seroepidemiologic Studies of Hantavirus Infection Among Wild Rodents in California Dispatches Seroepidemiologic Studies of Hantavirus Infection Among Wild Rodents in California A total of 4,626 mammals were serologically tested for antibodies to Sin Nombre virus. All nonrodent species were antibody negative. Among wild rodents, antibody prevalence was 8.5% in murids, 1.4% in heteromyids, and < 0.1% in sciurids. Of 1,921 Peromyscus maniculatus (deer mice), 226 (11.8%) were antibody positive, including one collected in 1975. The highest antibody prevalence (71.4% of 35) was found among P. maniculatus on Santa Cruz Island, off the southern California coast. Prevalence of antibodies among deer mice trapped near sites of human cases (26.8% of 164) was significantly higher than that of mice from other sites (odds ratio = 4.5; 95% confidence interval = 1.7, 11.6). Antibody prevalence increased with rising elevation (>1,200 meters) and correlated with a spatial cluster of hantavirus pulmonary syndrome cases in the Sierra Nevada. In spring 1993, a cluster of unexplained severe cases (14 cases, 8 deaths), after New Mexico (29 acute respiratory illnesses associated with a high cases) and Arizona (22 cases). death rate was reported in the southwestern Hantaviruses are excreted in the urine, feces, United States (1). The outbreak was linked to a and saliva of asymptomatic infected rodents (16). newly recognized hantavirus strain, Sin Nombre Transmission to humans occurs when aerosols con- virus (SNV), carried by the deer mouse, Pero- taminated with the virus are inhaled (16-18). Bites myscus maniculatus (2-5). Sporadic cases of the by infected rodents or exposure to broken skin or illness, hantavirus pulmonary syndrome (HPS), mucous membranes may represent alternative were subsequently identified in other regions of routes. Although specific risk factors are poorly North America, especially the western United defined, persons engaging in activities that bring States (6,7). Three additional pathogenic viruses them in contact with rodents and/or their excre- associated with HPS were later discovered out- tions may be at a higher risk for infection (19). side the usual range of P. maniculatus: 1) Black The present study compiles retrospective and Creek Canal virus, harbored by the cotton rat, prospective serologic data to 1) confirm P. mani- Sigmodon hispidus, in Florida; 2) Bayou virus, culatus as the primary reservoir of SNV and identified in the rice rat, Oryzomys palustris, in identify alternative reservoirs, if any, in Cali- Louisiana; and 3) New York virus, isolated from the fornia; 2) assess differences in SNV seroprevalence white-footed deer mouse, Peromyscus leucopus, in in vector populations from various geographic New York (8-12). These viruses have not been regions; and 3) compare seroprevalence rates of found in California; however, two novel hanta- reservoirs collected near sites of human cases viruses, El Moro Canyon virus (EMCV) and Isla with those from other sites. Vista virus (ISLA), were recently discovered in that state (13-15). Genetic studies identified the The Study harvest mouse, Reithrodontomys megalotis, and the California meadow vole, Microtus californicus, Mammal Surveys as the reservoirs for EMCV and ISLA, res- The California Department of Health Services pectively. Human infection with EMCV and (CDHS) contacted 18 agencies (local vector ISLA has not been documented. control districts, local health and environmental Through 31 January 1997, 156 cases of HPS health departments, universities, state and were reported to the Centers for Disease Control national park and forest services, the military, and Prevention (CDC); the case-fatality rate is and wildlife refuges) involved in cross-sectional approximately 50% (T. Ksiazek, P. Rollin, unpub. surveys of California mammals to participate in data). HPS has been confirmed in 26 states, with developing a centralized, statewide database of California reporting the third largest number of SNV serologic results and ecologic data. Vol. 3, No. 2, April–June 1997 183 Emerging Infectious Diseases Dispatches Historical surveys used archived specimens were the independent variables. Data from samples collected in 1975, 1976, and 1988 and stored at collected on the Channel Islands were analyzed the University of California, Berkeley, Museum of separately from mainland data where indicated. Vertebrate Zoology, and specimens collected from 1989 through early 1993 by local vector control dis- Sin Nombre Virus Antibody Prevalence tricts. Prospective surveys and human case inves- tigations were conducted from late 1993 through California Mammals the end of 1995. Wild rodent trapping and pro- A total of 4,626 (4,549 rodent and 77 non- cessing methods were as previously described (20). rodent species) mammals representing 47 species Reports by participating agencies included were collected between 1975 and 1995 in Cali- ecologic data on individual mammals (species, age, fornia and serologically tested for IgG antibodies and sex). Information on survey sites included to SNV (Table 1). Wild rodents (most 3,109, from county, physical location of trapline, date of the family Muridae) made up 98% of the sample, survey, elevation, and habitat. Habitat was cate- followed by Sciuridae (1,369), and Heteromyidae gorized by a single dominant vegetation type: cha- (71). Among the Muridae, 78% were deer mice or parral, conifer trees, grassland, hardwood trees, related species, 11% were wood rats, 6% were sage/scrub brush, or urban environment (21). domestic rodents (house mice, rats), 3% were harvest mice, and fewer than 1% were meadow Human Cases voles or cotton rats. Antibodies to SNV were Within 2 weeks after a confirmed diagnosis of found only among wild rodents. Prevalence of HPS, the patient or a surrogate was interviewed antibodies reactive with SNV was 8.5% among to determine potential sites of exposure to infected the Muridae, 1.4% among the Heteromyidae, and rodents. An environmental/ecologic investigation less than 0.1% among the Sciuridae. Nonrodent was conducted at possible sites of exposure (20,22). species tested included 74 carnivores (five domes- tic dogs, Canis familiaris; 26 coyotes, Canis Laboratory Studies latrans; 25 island foxes, Urocyon littoralis; six Rodent serum samples were tested by one or domestic cats, Felis domesticus; two opossums, more of six laboratories (CDC; CDHS; University Didelphis virginiana; three striped skunks, of New Mexico; University of California, Davis; Mephitis mephitis; seven raccoons, Procyon lotor), and University of Nevada, Reno). Serum samples one black-tailed jackrabbit, Lepus californicus, were examined for IgG antibodies to the SNV one Nuttall’s cottontail, Silvilagus nuttallii, and nucleocapsid protein by Western blot and/or one shrew, Sorex sp. enzyme-linked immunosorbent assay with CDC reagents (23,24). For archived specimens, liver Deer Mouse Populations tissue from frozen carcasses was used for poly- Of 1,921 P. maniculatus, 226 (11.8%) had merase chain reaction (PCR) (22,25). antibodies to SNV (Table 1). Other peromyscine- related species (e.g., cactus mice, canyon mice, Data Analysis California mice, and pinyon mice) also had Descriptive data were analyzed by Epi Info, antibodies to SNV, but prevalence was lower. In Version 6.0 (26). Frequency distributions were almost all instances, infected P. maniculatus obtained, and chi-square tests of homogeneity for were collected at the same site as SNV–antibody- two-by-two contingency tables were used to exa- positive animals of other species. mine the statistical significance of any association. Retrospectively, antibodies to SNV were A crude relationship between altitude and SNV- identified in 3 (6.0%) of 50 deer mice specimens antibody prevalence was assessed by the Mantel- collected in 1975 (1 of 22, 4.5%), 1976 (2 of 17, Cox test for trend. Adjusted odds ratios and 95% 11.8%), 1981 (0 of 2), 1992 (0 of 1), and early 1993 confidence intervals were calculated by logistic- (0 of 8). The three seropositive P. maniculatus binomial regression (27). A random effects model collected by the University of California, Ber- was chosen because of the presence of important keley in 1975 and 1976 were from Alameda, Kern, clustering effects from the sampling design. The and Mono Counties. Frozen liver tissue available presence or absence of antibodies to SNV was the from the seropositive Kern County specimen primary dependent variable, and characteristics yielded a PCR sequence of the G1 amplimer of that were identified in the descriptive analysis SNV that differed from a P. maniculatus Emerging Infectious Diseases 184 Vol. 3, No. 2, April–June 1997 Dispatches Table 1. Prevalence of antibodies to Sin Nombre virus from the Channel Islands, which differed by among wild rodents in California, 1975–1995 seven amino acid substitutions. Family/ Common No. No. % Among the deer mice for which age (1,165 Species Name Tested Pos. Pos. animals, 87% adults) and sex (1,239 animals, Heteromyidae 57% male) were available, SNV antibody preva- Dipodomys sp. kangaroo rats 28 1 3.6 lence was, respectively, 13.5% in adults and 6.7% Perognathus sp. pocket mice 43 0 0.0 in juveniles and 13.0% in males and 10.1% in SUBTOTAL 71 1 1.4 females. Differences in age (chi-square = 5.5) and Muridae sex (chi-square = 2.5) were not significant. Microtus sp. meadow voles 29 5 17.2 M. californicus California 22 5 22.7 Geographic Distribution meadow vole Thirty-four of the state’s 58 counties were M. montanus Montane vole 3 0 0.0 surveyed (Table 2). Antibodies to SNV were identi- M. townsendii Townsend’s 1 0 0.0 fied in deer mice from 21 (62%) of these counties vole (Figure 1). Most samples were from coastal Mus musculus house mouse 88 0 0.0 Neotoma sp. wood rats 330 2 0.6 counties (56%), followed by foothill/mountainous N. cinerea bushy-tailed 20 0 0.0 (36%) and inland/valley (8%) counties. Among wood rat these, the prevalence was 14.5% of 684 in the N. fuscipes dusky-footed 215 2 0.9 foothills/mountains, 11.6% of 112 on the coast, wood rat and 0.7% of 151 in the inland/valley areas.
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