The arctic fox variant of the rabies virus (RABV) is enzootic in the circumpolar north. Reports of abortive RABV exposures motivated a retrospective analysis of sera from 41 arctic foxes (Vulpes lagopus) captured at Karrak Lake in Nunavut, Canada, during 2011–15. Estimated RABV antibody prevalence among foxes was 15% (95% confidence interval, 7–28%).

Rabies in the North American arctic was first laboratory identified after a large-scale epizootic in Alaskan dogs (Canis lupus familiaris) and wild canids from 1945 to 1947 (Williams 1949) although disease that is clinically consistent with rabies had been described much earlier by indigenous Inuit (e.g., Tabel et al. 1974). The arctic fox variant of the rabies virus (RABV) occurs throughout the circumpolar north and is enzootic in arctic and subarctic North America (Kuzmin et al. 2008; Troupin et al. 2016). Arctic foxes (Vulpes lagopus) and red foxes (Vulpes vulpes) are the primary wildlife reservoirs of the arctic fox RABV variant in North America, although spillover infection can occur in any mammal (Simon et al. 2021).

Although RABV infection is nearly always fatal once the virus enters the central nervous system, abortive infections or nonlethal exposures have been described in people and animals (e.g., Gold et al. 2020). Trappers, hunters, biologists, and others who have close and recurring contact with reservoir species are at the highest risk of RABV exposure (Follmann et al. 1994; Gilbert et al. 2012). Previously, Ballard et al. (2001) had demonstrated the presence of RABV-neutralizing antibodies (RVNA) without nervous system infection among 4% of 99 arctic foxes in a cross-sectional sample from Alaska, US.

We describe an opportunistic investigation of RABV exposure among a population of arctic foxes previously under longitudinal study near Karrak Lake (67°14′N, 100°15′W), Nunavut, Northwest Territories, Canada. The objectives of our present work were to 1) estimate the seroprevalence of RABV-specific antibodies in arctic foxes as a measure of prior exposure; and 2) discuss the strength of evidence for abortive RABV infection(s) and fox survival among a population under a longitudinal study.

Fieldwork occurred near Karrak Lake in the Queen Maud Gulf Migratory Bird Sanctuary in the central Canadian Arctic. The selection of the study area, arctic fox capture protocol, and sample collection were originally designed to estimate the prevalence of Toxoplasma gondii in the fox population (Elmore et al. 2016). We retrospectively analyzed sera (n=59) from 41 individual arctic foxes, collected during 2011–15, for RABV antibodies using two methods: competitive enzyme-linked immunosorbent assay (cELISA; Fehlner-Gardiner and Wandeler 2014) and a virus-neutralization test (VNT; Knowles et al. 2009). We recaptured and collected blood from nine of the 41 individual foxes across multiple years, resulting in two to four samples annually from each of nine foxes and one sample from the remaining 32 foxes. After centrifugation, individual sera were stored in cryovials at –20 C.

Aliquots of all 59 sera were analyzed by cELISA, but only 30 sera, including those with a cELISA inhibition values >6% (n=16) and a randomly selected subset of samples with an inhibition value <6% (n=14), were also tested by VNT for RVNA. We considered samples to be “positive” for RABV-specific antibodies if the inhibition value was >19% (cELISA) or the RVNA concentration was ≥0.5 IU/mL (VNT). Although measures of sensitivity and specificity are not known for arctic foxes, the cELISA has a sensitivity of 90% and a specificity of 89% with red fox sera when compared with the VNT at the threshold of 0.5 IU/mL (Fehlner-Gardiner and Wandeler 2014).

Estimated seroprevalence of RABV antibodies in the arctic fox population at Karrak Lake, 2011–15, was 15% (6 of 41 foxes; 95% confidence interval, 7–28%; Table 1). Evidence of RVNA was detected in three of 30 sera (0.5–0.84 IU/mL). Among the three RVNA-positive sera, two were positive by cELISA (values of 34% and 54%), and one was negative by cELISA (14%). Among 30 sera screened by both methods, 83% (25 of 30) of results were concordant. Two sera that had positive results by cELISA but without detectable RVNA (AF2 and AF3 in 2013) were severely hemolyzed, which can affect the reliability of either test (Fehlner-Gardiner and Wandeler 2014). The level of discordance observed between ELISA and VNT testing methods to screen for RABV antibodies among wildlife is not exceptional (e.g., Moore et al. 2017; Moore 2021).

Table 1

Results from a population of arctic foxes (Vulpes lagopus) under longitudinal study during 2011–15 near Karrak Lake, Nunavut, Canada, that tested positive for rabies virus (RABV) antibodies, by either the competitive enzyme-linked immunosorbent assay (cELISA) or the serum-virus neutralization test (VNT) or both.

Results from a population of arctic foxes (Vulpes lagopus) under longitudinal study during 2011–15 near Karrak Lake, Nunavut, Canada, that tested positive for rabies virus (RABV) antibodies, by either the competitive enzyme-linked immunosorbent assay (cELISA) or the serum-virus neutralization test (VNT) or both.
Results from a population of arctic foxes (Vulpes lagopus) under longitudinal study during 2011–15 near Karrak Lake, Nunavut, Canada, that tested positive for rabies virus (RABV) antibodies, by either the competitive enzyme-linked immunosorbent assay (cELISA) or the serum-virus neutralization test (VNT) or both.

Three foxes (AF4, AF6, and AF7) that were seronegative upon initial capture demonstrated evidence of seroconversion upon later recapture and two (AF6 and AF7) of the three foxes had concordant positive results by cELISA and VNT, indicating exposure to RABV during the study (Table 1). Foxes AF4 and AF7 subsequently were seronegative during recapture the following year(s), possibly because of waning antibody levels. Given the acutely lethal nature of clinical RABV infection, three seropositive foxes (AF3, AF4, and AF7) that were sampled or resighted in subsequent years presents evidence of survival following abortive RABV infection, yet the discordant positive results for AF3 and AF4 and remaining low number of foxes with adequate longitudinal observations limit conclusions regarding survival after abortive RABV infections among arctic foxes in this population.

The RABV seroprevalence in arctic foxes at Karrak Lake was unknown before this study; however, the virus was expected to be circulating in the area because it is enzootic in foxes from elsewhere in the circumpolar North, where it had been detected during the same period (e.g., Aenishaenslin et al. 2014). Our detection of RABV antibodies in apparently healthy and recaptured arctic foxes adds to the few longitudinal reports targeting arctic wildlife (e.g., Aenishaenslin et al. 2014); most other studies document RABV infection of arctic foxes through cross-sectional sampling (e.g., Kuzmin et al 2008).

Our results are consistent with prior findings of abortive RABV infections in reservoir hosts (Gold et al. 2020) and suggest survival of arctic foxes after exposure to RABV in the central Canadian Arctic, which is noteworthy given the reportedly high susceptibility of foxes to RABV infection. Additional sampling and/or increasing the duration of monitoring could further corroborate the evidence of abortive RABV infections and test for effects of RABV exposure on long-term survival of arctic foxes.

The authors thank D. Kellett for logistical assistance and D. Stern for housing in Cambridge Bay, Nunavut, Canada. Funding and other support for this project were provided by Environment and Climate Change Canada, USDA APHIS National Rabies Management Program, Colorado State University, Canadian Food and Inspection Agency, Polar Continental Shelf Project, Northern Scientific Training Program, and the Natural Sciences and Engineering Research Council of Canada. All procedures performed in studies involving animals were in accordance with the ethical standards of the University of Saskatchewan Committee on Animal Care and Supply (2009-0159, 1999-0029). Foxes were trapped under the following permits: Nunavut Department of Environment 2011-018, 2012-020, 2013-015 and Canadian Wildlife Service NUN-MBS-11-02, NUN-SCI-11-03, NUN-MBS-12-02, NUN-SCI-12-03.

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