Widespread exposure to Francisella tularensis in Rangifer tarandus in Canada and Alaska

  • Kayla J. Buhler Department of Veterinary Microbiology, Western College of Veterinary Medicine, University of Saskatchewan, Saskatoon, SK, Canada; and Inland Norway University of Applied Sciences, Koppang, Norway
  • Helen Schwantje Government of British Columbia, Nanaimo, BC, Canada
  • N. Jane Harms Government of Yukon, Whitehorse, YT, Canada
  • Heather Fenton Government of the Northwest Territories, Yellowknife, NT, Canada; and Australian Registry of Wildlife Health, Taronga Conservation Society, NSW, Australia
  • Xavier Fernandez Aguilar University of Calgary, Calgary, AB, Canada; and Departament de Medicina i Cirurgia Animals, Universitat Autònoma de Barcelona, Bellaterra, Spain
  • Susan Kutz University of Calgary, Calgary, AB, Canada
  • Lisa-Marie Leclerc Government of Nunavut, NU, Canada
  • John Blake Animal Resources Center, University of Alaska Fairbanks, Fairbanks, AK, USA
  • Emily Jenkins Department of Veterinary Microbiology, Western College of Veterinary Medicine, University of Saskatchewan, Saskatoon, SK, Canada
Keywords: Caribou, reindeer, tularemia, climate change, Arctic, zoonoses

Abstract

The range of tularemia, a disease caused by the bacterium Francisella tularensis, may expand alongside climate change in the North. Transmission occurs via biting arthropods, contaminated water sources, infected animal tissues and fluids and even aerosolized bacteria. Little research has been published on F. tularensis in northern Canada. We investigated whether Rangifer (caribou and reindeer) in Canada and Alaska are exposed to F. tularensis, as they provide significant cultural and subsistence value. From 2016 to 2020, 336 serum samples were collected from Rangifer across 17 herds, including captive reindeer in Alaska (n = 30) and wild caribou across Canada (n = 306) during collaring or harvesting efforts. Using a microagglutination test, we detected antibodies against F. tularensis in 7% of captive reindeer (CI95 2–21), 6% of migratory tundra caribou (CI95 4–11) and 10% of mountain woodland caribou (CI95 6–17), with the highest seroprevalence observed in animals from Nunavut (17%) and British Columbia, Canada (18%). Ten of the herds (n = 10/17; 59%) had at least one positive animal. Evidence of exposure to F. tularensis indicates that further studies are needed to characterize sources of transmission for Rangifer species and any potential health effects following infection.

Downloads

Download data is not yet available.

References


Abdellahoum Z., Maurin M. & Bitam I. 2020. Tularemia as a mosquito-borne disease. Microorganisms 9, article no. 26, doi: 10.3390/microorganisms9010026.


Åsbakk K., Stuen S., Hansen H. & Forbes L. 1999. A serological survey for brucellosis in reindeer in Finnmark county, northern Norway. Rangifer 19, 19–24, doi: 10.7557/2.19.1.292.


Bates D., Maechler M., Bolker B., Walker S., Christensen R.H.B., Singmann H., Dai B. & Grothendieck G. 2016. Package lme4: linear mixed-effects models using ‘Eigen’ and S4. R package version 1.1–12. Vienna: R Foundation for Statistical Computing.


Bourque M. & Higgins R. 1984. Serologic studies on brucellosis, leptospirosis and tularemia in moose (Alces alces) in Quebec. Journal of Wildlife Diseases 20, 95–99, doi: 10.7589/0090-3558-20.2.95.


Buhler K.J., Blake J., Fenton H., Solomon I.H. & Jenkins E. n.d. Revealing reservoir potential: Jamestown Canyon virus infection in reindeer (Rangifer tarandus). Unpublished ms.


Buhler K., Bouchard É., Elmore S., Samelius G., Jackson J., Tomaselli M., Fenton H., Alisauskas R. & Jenkins E. 2022. Tularemia above the treeline: climate and rodent abundance influences exposure of a sentinel species, the Arctic fox (Vulpes lagopus), to Francisella tularensis. Pathogens 12, article no. 28, doi: 10.3390/pathogens12010028.


Conlan J.W., Chen W., Shen H., Webb A. & KuoLee R. 2003. Experimental tularemia in mice challenged by aerosol or intradermally with virulent strains of Francisella tularensis: bacteriologic and histopathologic studies. Microbial Pathogenesis 34, 239–248, doi: 10.1016/S0882-4010(03)00046-9.


Culler L.E., Ayres M.P. & Virginia R.A. 2015. In a warmer Arctic, mosquitoes avoid increased mortality from predators by growing faster. Proceedings of the Royal Society B Biological Sciences 282, article no. 20151549, doi: 10.1098/rspb.2015.1549.


Curry P.S., Elkin B.T., Campbell M., Nielsen K., Hutchins W., Ribble C. & Kutz S.J. 2011. Filter-paper blood samples for ELISA detection of Brucella antibodies in caribou. Journal of Wildlife Diseases 47, 12–20, doi: 10.1098/rspb.2015.1549.


Emmons R.W., Ruskin J., Bissett M.L., Uyeda D.A., Wood R.M. & Lear C.L. 1976. Tularemia in a mule deer. Journal of Wildlife Diseases 12, 459–463, doi: 10.7589/0090-3558-12.3.459.


Foley J.E. & Nieto N.C. 2010. Tularemia. Vet Microbiology 140, 332–338, doi: 10.1016/j.vetmic.2009.07.017.


Forsman M., Henningson E.W., Larsson E., Johansson T. & Sandström G. 2000. Francisella tularensis does not manifest virulence in viable but non-culturable state. FEMS Microbiology Ecology 31, 217–224, doi: 10.1111/j.1574-6941.2000.tb00686.x.


Golkocheva-Markova E., Nenova R., Stoilov R., Christova I. & Najdenski H. 2011. Cross-reactivity between yersinia outer membrane proteins and anti-Francisella and anti-Borrelia antibodies in serodiagnosis of yersinia-triggered reactive arthritis. Comptes Rendus de l’Académie Bulgare des Sciences 64, 61–66.


Government of British Columbia n.d. Woodland Caribou Plan. Swan Lake Subpopulation. Northern Mountain Caribou. Accessed on the internet at https://www.for.gov.bc.ca/ftp/HTH/external/!publish/Caribou%20Recovery%20Program/Herd%20Plans/FTP_upload_herd_plans/northern_mountain/Caribou%20Herd%20Plan%20Swan%20Lake_EN_disclaimer.pdf on 1 October 2022.


Gürcan S. 2014. Epidemiology of tularemia. Balkan Medical Journal 31, 3–10, doi: 10.5152/balkanmedj.2014.13117.


Hanke A.N., Angohiatok M., Leclerc L.M., Adams C. & Kutz S. 2021. A caribou decline foreshadowed by Inuit in the Central Canadian Arctic: a retrospective analysis. Arctic 74, 437–455, doi: 10.14430/arctic73826.


Hansen C.M. & Dresvyannikova S. 2022. Tularemia in the Arctic. In M. Tryland (ed.): Arctic One Health. Challenges for northern animals and people. Pp. 377–392. Cham, Switzerland: Springer.


Hansen C.M., Vogler A.J., Keim P., Wagner D.M. & Hueffer K. 2011. Tularemia in Alaska, 1938–2010. Acta Veterinaria Scandinavica 53, article no. 61, doi: 10.1186/1751-0147-53-61.


Hennebique A., Boisset S. & Maurin M. 2019. Tularemia as a waterborne disease: a review. Emerging Microbes & Infections 8, 1027–1042, doi: 10.1080/22221751.2019.1638734.


Jackson J., McGregor A., Cooley L., Ng J., Brown M., Ong C.W., Darcy C. & Sintchenko V. 2012. Francisella tularensis subspecies holarctica, Tasmania, Australia, 2011. Emerging Infectious Diseases 18, 1484–1486, doi: 10.3201/eid1809.111856.


Kaysser P., Seibold E., Mätz-Rensing K., Pfeffer M., Essbauer S. & Splettstoesser W.D. 2008. Re-emergence of tularemia in Germany: presence of Francisella tularensis in different rodent species in endemic areas. BMC Infectious Diseases 8, article no. 157, doi: 10.1186/1471-2334-8-157.


Keim P., Johansson A. & Wagner D.M. 2007. Molecular epidemiology, evolution, and ecology of Francisella. Annals of the New York Academy of Sciences 1105, 30–66, doi: 10.1196/annals.1409.011.


Keith L.B. 1983. Role of food in hare population cycles. Oikos 40, 385–395, doi: 10.2307/3544311.


Krebs C.J., Kenney A.J., Gilbert S., Danell K., Angerbjörn A., Erlinge S., Bromley R.G., Shank C. & Carriere S. 2002. Synchrony in lemming and vole populations in the Canadian Arctic. Canadian Journal of Zoology 80, 1323–1333, doi: 10.1139/z02-120.


Mallory C.D. & Boyce M.S. 2018. Observed and predicted effects of climate change on Arctic caribou and reindeer. Environmental Reviews 26, 13–25, doi: 10.1139/er-2017-0032.


Mallory C.D., Williamson S.N., Campbell M.W. & Boyce M.S. 2020. Response of barren-ground caribou to advancing spring phenology. Oecologia 192, 837–852, doi: 10.1007/s00442-020-04604-0.


Mörschel F.M. & Klein D.R. 1997. Effects of weather and parasitic insects on behavior and group dynamics of caribou of the Delta Herd, Alaska. Canadian Journal of Zoology 75, 1659–1670, doi: 10.1139/z97-793.


Nordstoga A., Handeland K., Johansen T.B., Iversen L., Gavier-Widen D., Mattsson R., Larssen K., Afset J.E. & Næverdal L.A. 2014. Tularaemia in Norwegian dogs. Veterinary Microbiology 173, 318–321, doi: 10.1016/j.vetmic.2014.06.031.


Omland T., Christiansen E., Jonsson B., Kapperud G. & Wiger R. 1977. A survey of tularemia in wild mammals from Fennoscandia. Journal of Wildlife Diseases 13, 393–399, doi: 10.7589/0090-3558-13.4.393.


Petersen J.M., Mead P.S. & Schriefer M.E. 2009. Francisella tularensis: an arthropod-borne pathogen. Veterinary Research 40, article no. 07. doi: 10.1051/vetres:2008045


Sato T., Fujita H., Ohara Y. & Homma M. 1990. Microagglutination test for early and specific serodiagnosis of tularemia. Journal of Clinical Microbiology 28, 2372–2374, doi: 10.1128/JCM.28.10.2372-2374.1990.


Schulze C., Heuner K., Myrtennäs K., Karlsson E., Jacob D., Kutzer P., Grobe K., Forsman M. & Grunow R. 2016. High and novel genetic diversity of Francisella tularensis in Germany and indication of environmental persistence. Epidemiology & Infection 144, 3025–3036. doi: 10.1017/S0950268816001175.


Sergeant E.S.G. 2019. Epitools epidemiological calculators. Ausvet. Accessed on the internet at http://epitools.ausvet.com.au on 24 September 2022.


Sjostedt A. 2007. Tularemia: history, epidemiology, pathogen physiology, and clinical manifestations. Annals of the New York Academy of Sciences 1105, 1–29, doi: 10.1196/annals.1409.009.


Smith M.M., Van Hemert C., Atwood T.C., Sinnett D.R., Hupp J.W., Meixell B.W., Gustine D.D., Adams L.G. & Ramey A.M. 2022. A serological survey of Francisella tularensis exposure in wildlife on the Arctic coastal plain of Alaska. Journal of Wildlife Diseases 58, 746–755, doi: 10.7589/JWD-D-21-00162.


Snowden J. & Simonsen K.A. 2022. Tularemia. Treasure Island, FL: StatPearls Publishing. Accessed on the internet at https://www.ncbi.nlm.nih.gov/books/NBK430905/ on 4 June 2024.


Syrjälä H., Koskela P., Ripatti T., Salminen A. & Herva E. 1986. Agglutination and ELISA methods in the diagnosis of tularemia in different clinical forms and severities of the disease. Journal of Infectious Diseases 153, 142–145, doi: 10.1093/infdis/153.1.142.


Triebenbach A.N., Vogl S.J., Lotspeich-Cole L., Sikes D.S., Happ G.M. & Hueffer K. 2010. Detection of Francisella tularensis in Alaskan mosquitoes (Diptera: Culicidae) and assessment of a laboratory model for transmission. Journal of Medical Entomology 47, 639–648, doi: 10.1093/jmedent/47.4.639.


Vors L.S. & Boyce M.S. 2009. Global declines of caribou and reindeer. Global Change Biology 15, 2626–2633, doi: 10.1111/j.1365-2486.2009.01974.x.


Tärnvik A. (ed.) 2007. WHO guidelines on tularaemia. Geneva: WHO Press.


Zarnke R.L. & Ballard W.B. 1987. Serologic survey for selected microbial pathogens of wolves in Alaska, 1975–1982. Journal of Wildlife Diseases 23, 77–85, doi: 10.7589/0090-3558-23.1.77.


Zarnke R.L., Ver Hoef J.M. & DeLong R.A. 2004. Serologic survey for selected disease agents in wolves (Canis lupus) from Alaska and the Yukon Territory, 1984–2000. Journal of Wildlife Diseases 40, 632–638, doi: 10.7589/0090-3558-40.4.632.


Zellner B. & Huntley J.F. 2019. Ticks and tularemia: do we know what we don’t know? Frontiers in Cellular and Infection Microbiology 9, article no. 146. doi: 10.3389/fcimb.2019.00146.
Published
2024-07-18
How to Cite
Buhler K. J., Schwantje H., Harms N. J., Fenton H., Fernandez Aguilar X., Kutz S., Leclerc L.-M., Blake J., & Jenkins E. (2024). Widespread exposure to <em>Francisella tularensis</em> in <em>Rangifer tarandus</em&gt; in Canada and Alaska. Polar Research, 43. https://doi.org/10.33265/polar.v43.9288
Section
Research Articles

Most read articles by the same author(s)