Abstract
Tularemia is a widely spread zoonotic disease in the northern hemisphere, caused by the bacterium Francisella tularensis. In humans, tularemia is an acute febrile illness with incidence peaks in late summer to early autumn of outbreak years, but there is no early warning system in place that can reduce the impact of disease by providing timely risk information. In this study, we revisit previously unpublished data on F. tularensis in water, sediment, soil, and small mammals from 1984 in northern Sweden. In addition, we used human case data from the national surveillance system for tularemia in the same year. In the environmental and small mammal material, bank vole (Myodes glareolus) samples from urine and bladder were the only samples that tested positive for F. tularensis. The prevalence of F. tularensis among trapped bank voles was 13.5%, although all six bank voles that were retrieved from owl nest boxes in early May tested positive. Forty-two human tularemia cases were reported from August to December in 1984. Based on these results, we encourage investigating the potential role of tularemia-infected bank voles retrieved from owl nest boxes in spring as an early warning for outbreaks of tularemia among humans in summer and autumn of the same year.
Introduction
Early warning systems are important to mitigate outbreak magnitudes of infectious diseases. Traditionally, such systems rely on disease alerts, that is, early reports of human disease. In zoonotic diseases, high prevalence of zoonotic pathogens and/or outbreaks among reservoir animals can provide a more effective early warning due to the time lag between outbreaks in animals and humans. For some rodent-borne zoonoses such early warnings have been developed. For example, outbreaks of Nephropathia epidemica caused by the Puumala orthohantavirus can be predicted by the density and spatial distribution of the host rodent species (Khalil et al. 2019).
Predators and scavengers remove diseased animals from species communities, an ecosystem service contributing to maintain ecosystem and human health (O'Bryan et al. 2018). By selectively preying on infected and even diseased animals, predators can act as sentinels of human disease outbreaks and provide early warnings. For example, owls selectively prey on bank voles (Myodes glareolus) infected with Puumala orthohantavirus (Khalil et al. 2016). Several owl species cache food in their nests, and voles cached in nest boxes can easily be retrieved and analyzed for pathogen prevalence (cf. Khalil et al. 2016).
Tularemia is a widely spread zoonotic disease in the northern hemisphere, caused by the bacterium Francisella tularensis. In humans, it can cause acute febrile illness with peaks in summer and autumn of outbreak years (Rossow et al. 2014). As far as we know, there is no early warning system in place for outbreaks among humans. In this study, we revisit previously unpublished Swedish data on presence of F. tularensis in water, sediment, soil and small mammals (live-trapped and from owl nest boxes) and focus on the potential of infected voles in food caches in nest boxes of owls as sentinels of tularemia outbreaks.
Material and Methods
Field sampling
Small mammals were live-trapped with Ugglan traps in the county of Västerbotten (100 traps) in northern Sweden in 1984. Traps were placed in field habitats, road ditches, and spruce forest. Repeated trapping was performed (May 24–25, June 4–7, June 18–19, July 23–25, and September 4–5). Traps were baited with oats, cooking oil, and dried apple, and checked after 24 h. In addition, small mammals were sampled from Tengmalm's Owl (Aegolius funereus) boxes on May 10; from boxes established for owl monitoring in 1980 (Hörnfeldt et al. 1990). Urine and blood samples were taken of anesthetized small mammals in the field. After sampling, the animals were euthanized. Samples of surface water (n = 17), sediment in running water (n = 17), and soil (n = 25) were taken concurrently with small mammal trappings and in vicinity of trapping sites. In total, 6 field voles (Microtus agrestis) and 37 bank voles were trapped. Nine small mammals from owl boxes were included in the study, namely six bank voles, two field voles, and one Laxmann's shrew (Sorex caecutiens).
Laboratory analyses
In the laboratory, the bladder was removed from all specimens and either urine and serum or bladder and serum were analyzed in all specimens. Enzyme-linked immunosorbent assay (ELISA) was performed on environmental and biotic samples as essentially described by Voller et al. (1978) and modified by Sandström et al. (1986), except that dilute samples of sera, urine, or bladder rinse solution were coated on the microplates. In ELISA, antigen A2:1 (Sandström et al. 1984) and anti-A2:1 antibodies were used (Sandström et al. 1986).
Tularemia surveillance among humans
In Sweden, tularemia is a notifiable disease since 1968. Data on tularemia cases occurring in 1984 were collected from the national system for communicable disease surveillance, maintained by the Public Health Agency of Sweden. Data use was approved by the regional ethical review board in Umeå, Sweden (2014-204-31M).
Results
No water, sediment, soil, field vole, or shrew sample tested positive for F. tularensis. However, 11 bank voles tested positive; all 6 bank voles from nest boxes and 5 of 37 trapped bank voles (13.5%; 3 in urine and 2 in bladder). There was a moderately sized tularemia outbreak in Sweden in 1984 with 42 human cases reported. The start of illness occurred between August and December. Disease was contracted in northern Sweden.
Discussion
Pathogen prevalence in trapped rodents can be an important indicator of forthcoming disease outbreaks in humans (Khalil et al. 2019). However, if rodents suffer or even die from pathogen infection, rodent surveillance using live- or snap-trapping is not an efficient surveillance method; especially as diseased animals are likely rapidly consumed by predators and scavengers (Origgi et al. 2015). Rodent species (primarily families of Cricetidae and Muridae) are notoriously sensitive to F. tularensis. They develop acute tularemia within a few days after infection and mortality rate is high (Rossow et al. 2014, Origgi et al. 2015). In this perspective, the here identified prevalence of 13.5% in bank voles trapped in a period of 2 months provides some, but limited, help for predicting a tularemia outbreak. Instead, the 100% prevalence (even though based on only six specimens) of F. tularensis among bank voles from owl boxes is highly encouraging and indicates that owls (here Tengmalm's Owl) (1) selectively prey on infected/diseased voles and (2) thereby could be used as sentinels of tularemia outbreaks in humans. Our owl results are especially promising considering the home range size of Tengmalm's Owl—a specialist predator on voles—of ∼200 ha (Sonerud et al. 1986), that is, covering hundreds of bank vole territories. Hence, using targeted control of owl boxes for F. tularensis infected bank voles during the owls' breeding season in spring could enable an effective screening of entire landscapes that risk tularemia outbreaks in humans during autumn and winter. We are fully aware of the limited sample sizes in our study. However, considering the promising results, follow-up studies based on larger samples should validate in properly designed field tests, supported by experiments, if owls and potentially other predators contribute to ecosystem and human health by selective predation on infected/diseased prey species.
Footnotes
Acknowledgments
We thank Kersti Gustafsson for field sampling and late Ulla Eriksson for laboratory analyses.
Author Disclosure Statement
No conflicting financial interests exist.
Funding Information
This project was funded by the Swedish research council for sustainable development FORMAS (grant no. 2017-00578). Owl monitoring was supported by the Swedish Environmental Protection Agency and Olle och Signhild Engkvists Stiftelser.