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1 Canadian Cooperative Wildlife Health Centre, Department of Veterinary Pathology, Western College of Veterinary Medicine, University of Saskatchewan, Saskatoon, Saskatchewan, Canada S7N 5B4
2 Prairie Diagnostic Services, 52 Campus Drive, Saskatoon, Saskatchewan, Canada, S7N 5B4
3 National Microbiology Laboratory, Public Health Agency of Canada, 1015 Arlington St., Winnipeg, Manitoba, Canada R3E 3R2
4 Corresponding author (email: gary.wobeser{at}usask.ca)
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Some rodent species undergo sporadic irruption ("a sudden increase in an animal population" [Nichols, 2001]) during which they may damage crops and may constitute an increased risk to humans because of disease agents that they carry. Examples include "plagues" of house mice (Mus musculus) in Australia (Pech et al., 2003) and irruptions of voles (Microtus spp.) in the western United States (Beck, 1958), Sweden (Dahlstrand et al., 1971), and Mongolia (Pech et al., 2003). Although little is known about the role of infectious disease in population changes among rodents (Begon, 2003), tularemia was diagnosed in voles found dead during irruptions of Microtus californicus in California in 1927 (Perry, 1928) and Microtus montanus in Oregon and California in 1957–1958 (Jellison et al., 1958). A sudden population decline, during which many voles (Microtus agrestis, Microtus raticeps) were found dead in hay storage barns, coincided with an outbreak of respiratory tularemia among farmers in Sweden (Dahlstrand et al., 1971). Tularemia was suspected to have caused the decline of a Microtus canicaudus population in Oregon (Wolff and Edge, 2003).
We describe the occurrence of tularemia during an irruption of deer mice (Peromyscus maniculatus) in west-central Saskatchewan.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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During March 2005, as winter snow was melting, reports appeared in local media of massive numbers of dead deer mice on some highways in west-central Saskatchewan. On 18 April 2005, an adult male deer mouse was submitted for necropsy to the Canadian Cooperative Wildlife Health Centre, Saskatoon, Saskatchewan by a municipal Pest Control Officer (PCO) who had observed hundreds of dead deer mice on 13 April while checking farm buildings (N 51°20', W 109°00') near Madison, Saskatchewan. The mouse was seen to be panting heavily and died while being observed. It was held frozen until submitted. On 24 April, the senior author inspected the site where the mouse was found (Site A) and two other sites (B, C) where the PCO had seen dead deer mice (Fig. 1
). Site A consisted of granaries in a field distant from any occupied farm buildings. There was barley (Hordeum spp.) and dry peas (Pisium sativum) on the ground about the granaries. Many desiccated but intact (mummified) deer mouse carcasses were evident about the granaries and in the surrounding field. One live and many dead deer mice were found under pieces of wood on the ground about the granaries. Sites B and C were groups of granaries in fields located 12 km from site A and about 1 km apart. Mummified deer mice were evident in the grass about the buildings at site B and >50 dead deer mice and a live house mouse were found under pieces of wood lying on the ground. Three recently dead deer mice were collected. There were many mummified deer mice surrounding the granaries at site C; three recently dead deer mice found under wood lying on the ground were collected.
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). No dead deer mice were found except at eight sites within a 10-km radius of the hamlet of Tyner (51°00'N, 108°25'W), at all of which mummified deer mice were evident. A farmer reported seeing many dead deer mice in this area earlier in the spring. The only specimen suitable for collection was at Site D (51°00'N, 108°37'W) located 47 km from Site A and 34 km from Sites B and C (Fig. 1). A recently dead deer mouse that was collected, a live house mouse, a live deer mouse with pups, and >20 mummified deer mice were found near granaries at this site. Precautions proposed by Mills et al. (1995) were observed when collecting dead deer mice. Necropsy and detection of F. tularensis
Necropsies were performed within a bio-safety cabinet. Samples of major organs were preserved in 10% buffered formalin and liver was frozen until used for bacteriology and/or testing by polymerase chain reaction (PCR). Fixed tissues were processed routinely, sectioned at 5 µm, and stained with hematoxylin and eosin for histology. Liver from the initial mouse from Site A was inoculated on Tryptic Soy Agar supplemented with 5% sheep blood and MacConkey’s agar plates (Becton-Dickinson-Canada, Oakville, Ontario, Canada) that were incubated at 37 C in the presence of 5% CO2. Liver from this mouse and from a single mouse from each of Sites B–D was tested for the presence of F. tularensis by PCR using primers specific for F. tularensis subsp. tularensis outer membrane protein fopA gene (Ftul-F 5' GTGTTAGGGATTTCGAGGAGT-CT-3', Ftul-R 5'-CTGGCCAGTTCTATCTT-GAGG-3') (Sibley et al., 2005). DNA was extracted with the use of standard proteinase K and phenol/chloroform extraction. The primers amplified a 459 bp product. Reagent-only (no DNA) reactions were used as negative controls to detect potential contamination, whereas DNA from cultured bacteria (field strain) was used as a positive control. Replicate unstained histolologic sections of tissues from all mice from each site (total of eight) were used for immunohistochemistry with avidin–biotin complex polyclonal anti–F. tularensis antiserum (Difco Laboratories, Detroit, Michigan, USA).
A culture of F. tularensis from the initial animal from Site A, as well as liver from one animal from each of Sites B and C that had tested positive for F. tularensis with the use of PCR were sent to the National Microbiology Laboratory, Public Health Agency of Canada, Winnipeg, Manitoba (NML) for further typing. Francisella tularensis was cultured from the specimens from Sites B and C at NML and DNA was prepared from the three cultures of F. tularensis with the use of a thermolysis procedure (Keim et al., 2000). Multiple-locus variable-number tandem repeat analysis (MLVA) was performed for molecular subtyping of the isolates. MLVA targets were PCR amplified as described in Johansson et al. (2004). Amplicons were purified with the use of Microcon centrifugal filter devices (Millipore, Billerica, Massachusetts, USA) and MLVA marker alleles were sequenced on an ABI 3100 Genetic Analyzer (Applied Biosystems, Foster City, California, USA) with the use of BigDye terminator V3.1 cycle sequencing chemistry. Bionumerics software (Applied Maths, Belgium) was used to analyze sequence data. The raw genotype scores were analyzed by using an unweighted pair group method arithmetic average (UPGMA) cluster analysis with a categorical coefficient.
Information on deer mouse populations
To collect information on the deer mouse population in west-central Saskatchewan, a questionnaire was sent during May 2005 to rural municipalities in which dead mice had been found or where large numbers of mice had been reported in the media. Based on the response to these initial questionnaires, questionnaires then were sent to additional municipalities. The initial question asked was: Have unusual numbers of deer mice been reported in your municipality at any time since January 2003? If the answer was affirmative, respondents were asked to answer further questions including: When were unusual numbers of mice first observed? Was the entire municipality involved? Did the number of mice increase suddenly or gradually? Were unusual numbers of mice associated with any particular crop? Has the number of mice remained stable, increased or decreased in the spring of 2005? Have large numbers of dead mice been observed? If so, when and where?. In total 55 municipalities were polled. Questionnaires were supplemented by telephone contact with the PCO or other knowledgeable persons in some municipalities.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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The initial mouse from Site A was submitted as an unknown diagnostic specimen. Because of the risk to laboratory personnel from Sin Nombre virus and Bartonella spp. carried by deer mice, bacteriological culture and PCR examination of liver from this animal were done within biosafety cabinets. On bacteriologic culture, small colonies grew after 48 hr of incubation on 5% blood agar but not on MacConkey’s agar. On Gram stain, the organism appeared as gram-negative coccobacilli. There was no reaction on triple sugar iron. Additional biochemical tests including oxidase, urease, and nitrate were negative, suggesting a Francisella sp.–like organism; however, the isolated organism did not require cysteine for growth. To reduce the risk of infection of laboratory personnel, bacteriologic isolation from any of the other deer mice was not attempted in the Saskatoon laboratory.
Liver from the initial mouse from Site A and from a single mouse from each of Sites B–D was examined by PCR; all were positive for F. tularensis. Sections of fixed liver from all mice collected from Sites AD were positive for F. tularensis with the use of immunohistochemistry.
To determine the extent of diversity among the three isolates sent to NML, 25 variable-number tandem repeat (VNTR) markers were analyzed for molecular subtyping. All three isolates were designated F. tularensis subsp. holarctica. Sequence analysis of the Ft-M19 locus indicated a 30 bp deletion in this region, which has been shown to be diagnostic for F. t. holartica isolates (Farlow et al., 2001; Johansson et al., 2004). Of the 25 VNTR markers analyzed, only two hypervariable markers, Ft-M3 and Ft-M4, showed any variation (Table 1). Both markers are known, historically, to have the highest diversity index (Ft-M3: D=0.95; Ft-M4, D=0.65) among those tested (Johansson et al., 2004). At the Ft-M3 locus, isolate EBD05-005 contained 15 copies of a 9 bp tandem repeat unit, EBD05-004 had 16 copies and EBD05-003 had 19 copies. At the Ft-M4 locus, EBD05-003 had 4 copies of a 5 bp tandem repeat whereas both EBD05-004 and EBD05-005 each had 5 copies. The deer mouse MLVA profiles were compared to others in the Canadian national collection of F. tularensis bionumerics database and all three isolates represent new genotypes.
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). The actual density of mice is unknown, but comments from respondents are illustrative: "during harvesting, sieves on the combine get loaded with mice," "observed pavement with flattened mouse carcasses every foot or so," "farmers with pails of water with flip lids [homemade traps] report catching up to 75 mice a night" [in farm buildings], "people who have never had mice in their house are complaining of mice." Some other municipalities also reported that the number of deer mice may have increased, but not to an extent that they constituted a problem. The number of deer mice was reported to have increased suddenly in the summer or autumn of 2004 (6/14 respondents) or in the spring of 2005 (7/14 respondents). One respondent reported that the number of mice had increased gradually from 2002 to 2005. Deer mice were reported to be particularly numerous in association with crops of canaryseed (Phalaris canatiensis) and lentils (Lens culinaris). Respondents from 10 municipalities indicated that the mouse population declined in the spring of 2005 and many dead deer mice had been observed in eight municipalities (Fig. 2). Only one respondent recalled a similar density of deer mice at any time in the past. He reported that many deer mice occurred in one year in the 1950’s, during a period of several years with above-normal rainfall.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Factors that led to this irruption are unknown. The natural vegetation of the area was mixed grass prairie similar to grasslands in Montana, where the average number of deer mice ranged from 7.7 to 22.1/ha (Douglass et al., 2001). The area now consists of extensive grain fields with only tiny remnants of native habitat. In common with other highly modified agricultural landscapes, the area lacks bio-diversity but contains plentiful energy-rich food on a seasonal basis. Feedback mechanisms that influence rodent populations, including predator–prey, plant–herbivore, and social interactions may not occur in agricultural landscapes that are disturbed frequently (Leirs, 2003).
We believe this to be the first report of tularemia in wild deer mice, although deer mice are susceptible to experimental infection with F. t. subsp. tularensis (Stagg et al., 1956; Vest and Marchette, 1958). Francisella tularensis has been isolated from deer mice during surveys for plague, including from one mouse in Alberta (Ozburn, 1944), two of 58 pooled samples from 301 mice in California (Burroughs et al., 1945), and from ectoparasites from mice in Utah (Stagg et al., 1956). The subspecies of F. tularensis isolated in these surveys was not reported. Burroughs et al. (1945) indicated that mice in their survey were latently infected and that septicemic tularemia was not present. Vest et al. (1965) and Lane and Emmons (1977) did not isolate F. tularensis from any of 4404 and 64 deer mice collected in Utah and California, respectively.
The organism isolated from the initial mouse from Site A was atypical in that cysteine was not required in media for growth. Bernard et al. (1994) reported that seven isolates of F. tularensis from humans in Canada lacked a requirement for cysteine and speculated that strains that lack a requirement for cysteine and enriched media for growth may have reduced virulence. The organisms from mice from Sites A–C were identified as F. t. subsp. holarctica with the use of MLVA. We note that MLVA should be used with caution for assigning F. tularensis subspecies; however, Type A and Type B biovars were consistently distinguished by the concurrent use of six VNTR loci (Farlow et al., 2001; Johansson et al., 2004). This subspecies is considered to be less virulent than F. t. subsp. tularensis and is usually associated with voles and muskrats (Ondatra zibethicus) in North America and with water rats (Arvicola terrestris) and microtine voles in Eurasia (Bell, 1980). Most human cases of tularemia in Saskatchewan have been linked to contact with muskrats (Martin et al.,1982). Epizootics of Type B tularemia occur in varying hares (Lepus timidus) in Sweden and Finland, but hares are thought to be accidental rather than reservoir hosts of the disease (Mörner et al., 1988). Multiple-locus variable-number tandem repeat analysis, which uses VNTR-based polymorphisms, provides a high level of discrimination among F. tularensis isolates. Two of 25 VNTRs tested in this study were polymorphic among the three deer mouse isolates. Comparison of VNTR profiles with those in the Canadian F. tularensis database, with the use of a categorical coefficient and UPGMA cluster analysis, resulted in three new genotypes.
Tularemia only is obvious when many animals die of the disease or humans become infected. Deer mice are nocturnal and secretive, so mortality caused by tularemia is unlikely to be observed in populations at low density. The epidemiology of the disease is extremely diverse (Bell, 1980) and the reservoir for the bacterium is unclear (Tärnvik et al., 1996). Francisella tularensis is believed to be an obligate host-dependent bacterium (Larsson et al., 2005) and although it is associated with rodents and lagomorphs, it is unclear if these mammals are true reservoirs of the bacterium (Ellis et al., 2002). Bell and Stewart (1975) proposed that chronic nephritis in voles, resulting in water contamination, might be a method by which F. t. subsp. holarctica may persist. This seems an unlikely source of infection for deer mice living in agricultural fields in a semiarid environment. Isolation of F. tularensis from live-trapped deer mice living in dry fields without access to standing water (Burroughs et al., 1945) suggests that subclinically infected deer mice might be a reservoir.
The diagnosis of tularemia coincided temporally with a reported decline in the number of deer mice in 10 municipalities. The disease was diagnosed in dead mice at four widely separated sites located in two of these municipalities. During the survey on May 3, 15 sites were examined in five municipalities that reported large numbers of deer mice. Dead mice were found in two municipalities that reported mouse mortality; no dead mice were found at 4 sites in three municipalities in which mortality was not reported. The actual spatial extent of the disease and its impact on the deer mouse population are unknown. Based on the mummified condition of most mice found in April and May, much of the mortality probably occurred during March or earlier. The number of mummified carcasses suggests that mortality exceeded the ability of predators and scavengers to remove sick and dead mice before carcasses desiccated.
Public health officials were advised of the diagnosis of tularemia in deer mice but there were no reported cases of human tularemia in the area, although many dead mice were present in and around farm buildings and equipment. Humans have been infected with type B tularemia through contact with dead animals, contaminated food and water, ticks and biting insects, inhalation, and bite wounds (Bell, 1980; Ellis et al., 2002). Respiratory infection as a result of inhalation of dust occurred in buildings contaminated by rodent carcasses in Sweden (Dahlstrand et al., 1971; Tärnvik et al., 2004) and in association with haying and threshing in Finland (Syrjälä et al., 1985). During the investigation, several individuals volunteered that their dogs and cats caught many deer mice. Transmission of tularemia to humans by cats has been reported (Baldwin et al., 1991; Capellan and Fong, 1993), including an instance in which a cysteine-independent strain of F. tularensis was transmitted by a cat bite (Bernard et al., 1994). Occurrence of human tularemia is grossly underestimated, because of the relatively benign nature of human disease caused by some strains of F. tularensis (Ellis et al., 2002). During an irruption of M. montanus in Oregon, there was extensive environmental contamination with F. tularensis, but no overt human tularemia outbreak (Kartman et al., 1958). However, retrospective serology identified 12 human cases, none of which had been suspected to have had tularemia (Osgood et al., 1958). It was concluded that mild and atypical clinical symptoms, perhaps related to the low virulence of the organism, failed to arouse the suspicion of either patients or physicians.
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ACKNOWLEDGMENTS |
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LITERATURE CITED |
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Received for publication 23 January 2006.
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