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Survey of coyotes, red foxes and wolves from Wyoming, USA, for Echinococcus granulosus s. l.

  • Helminthology - Original Paper
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Abstract

The paraphyletic group Echinococcus granulosus sensu lato is comprised of parasitic tapeworms of wild and domestic canids such as wolves (Canis lupus) and coyotes (Canis latrans), which serve as definitive hosts, and ungulates, which are the intermediate hosts. Members of this tapeworm group are characterized by both cosmopolitan distribution and zoonotic disease potential. This survey (conducted from 2012 through 2017) was designed to provide insight into the prevalence and distribution of this parasite in wild canids in Wyoming. Echinococcus sp. infections were documented in 14 of 22 gray wolves (63.6%), 1 of 182 coyotes (0.55%) and 0 of 5 red foxes (Vulpes fulva). Echinococcus granulosus s. l. was confirmed in 4 of these 14 specimens obtained from wolves with two parasite specimens corresponding morphologically with E. canadensis (G8/G10). These results suggest that wolves serve as the major definitive host of E. granulosus s. l. in Wyoming, while coyotes do not play an equivalent role. Limited sample size precludes evaluation of the importance of the red fox as a favorable definitive host. Whereas this study documents the occurrence of E. granulosus s. l. in Wyoming, the zoonotic disease risk does not appear to be high. Education remains the key to disease prevention, coupled with good hygienic practices by humans and anthelmintic treatment of domestic dogs exhibiting elevated risk of exposure.

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Data availability

The data generated during and/or analyzed during the current study are available from the corresponding author upon reasonable request.

References

  • Alvarez Rojas CA, Romig T, Lightowlers MW (2014) Echinococcus granulosus sensu lato genotypes infecting humans – review of current knowledge. Int J Parasitol. 44:9–18

    Article  Google Scholar 

  • Buskirk SW (2016) Wild mammals of Wyoming and Yellowstone National Park. University of California Press, Oakland

    Book  Google Scholar 

  • Butler JM, Grundmann AW (1954) The intestinal helminths of the coyote Canis latrans Say, in Utah. J Parasitol 40(4):440–443

    Article  CAS  Google Scholar 

  • Cerda JR, Ballweber LR (2018) Confirmation of Echinococcus granulosus G8 and G10 in Idaho gray wolves (Canis lupus) and cervids. J Wildl Dis 54(2):403–405

    Article  Google Scholar 

  • Cerda JR, Buttke DE, Ballweber LR (2018) Echinococcus spp. tapeworms in North America. Emerging Infectious Dis 24(2):230–235

    Article  Google Scholar 

  • DePlazes P, Rinaldi L, Alvarez Rojas CA, Torgerson PR, Harandi MF, Romig T, Antolova D, Schurer JM, Lahmar S, Cringoli G, Magambo J, Thompson RCA, Jenkins EJ (2017) Global distribution of alveolar and cystic echinococcosis. Advances in Parasitol 95:315–493

    Article  CAS  Google Scholar 

  • Dovel G (2009) Two-thirds of Idaho wolf carcasses examined have thousands of hydatid disease tapeworms. The Outdoorsman, Bulletin 36 8 pp

  • Drew ML (n.d.) Echinococcus granulosus in wolves in Idaho. Idaho Department of Fish and Game publication 4 pp

  • Dubinský P, Stefancíková A, Turceková L, Macko JK, Soltýs J (1998) Development and morphological variability of Echinococcus granulosus. Parasitol Res. 84(3):221–229. https://doi.org/10.1007/s004360050386

    Article  PubMed  Google Scholar 

  • Foreyt WJ, Drew ML, Atkinson M, McCauley D (2009) Echinococcus granulosus in gray wolves and ungulates in Idaho and Montana, USA. J Wildl Dis 45(4):1208–1212

    Article  Google Scholar 

  • Freeman RS, Adorjan A, Pimlott DH (1961) Cestodes of wolves, coyotes, and coyote-dog hybrids in Ontario. Can J Zool 39:527–532

    Article  Google Scholar 

  • Harper TA, Ruttan RA, Benson WA (1955) Hydatid disease (Echinococcus granulosus) in Saskatchewan big game. Trans N Am Wildl Conf 20:198–208

    Google Scholar 

  • Hernandez F, Verdugo C, Cardenas F, Sandoval R, Morales N, Olmedo P, Bahamonde A, Aldridge D, Acosta-Jamett G (2019) Echinococcus granulosus in the endangered Patagonian huemel (Hippocamelus bisulcus). J Wildl Dis 55(3):694–698

    Article  CAS  Google Scholar 

  • Holmes JC (1961) The importance of coyotes (Canis latrans) in the maintenance of sylvatic echinococcosis: preliminary observations. J Parasitol 47(4):55

    Google Scholar 

  • Holmes JC, Podesta R (1968) The helminths of wolves and coyotes from forested regions of Alberta. Can J Zool 46:1193–1204

    Article  Google Scholar 

  • Hua R, Xie Y, Song H, Shi Y, Zhan J, Wu M, Gu X, Peng X, Yang G (2019) Echinococcus canadensis G8 tapeworm infection in a sheep, China, 2018. Emerg Infect Dis 25(7):1420–1422. https://doi.org/10.3201/eid2507.181585

    Article  PubMed  PubMed Central  Google Scholar 

  • Idaho Department of Fish and Game (2010) Parasitic tapeworm - Echinococcus granulosus Q and A. https://idfg.idaho.gov/wildlife/disease/echinococcus-granulosus/questions-and-answers. Accessed 24 September 2020

  • Idaho Department of Health and Welfare (2010) Echinococcus: focus on Idaho. Ida Dep Health and Welf Dis Bull 17(2):1–3

    Google Scholar 

  • Jenkins DJ, Romig T, Thompson RCA (2005) Emergence/re-emergence of Echinococcus spp. – a global update. Int J Parasitol 35:1205–1219

    Article  CAS  Google Scholar 

  • Johnson MR (2001) Health aspects of gray wolf restoration. In: Maehr DS, Noss RF, Larkin FL (eds) Large mammal restoration – ecological and sociological challenges in the 21st century. Island Press, Washington DC, pp 163–166

    Google Scholar 

  • Khan A, Ahmed H, Khan H, Simsek S, Kilinc SG, Kesik HK, Yayi G, Celik F, Afzal MS, Budke CM (2020) First report of Echinococcus canadensis (G6/G7) by sequence analysis from the Khyber Pakhtunkhwa province of Pakistan. Acta Trop 209:105559. https://doi.org/10.1016/j.actatropica.2020.105559

    Article  CAS  PubMed  Google Scholar 

  • Kingston N, Honess RF (1982) Platyhelminthes. In: Thorne ET, Kingston N, Jolley WR, Bergstrom RC (eds) Diseases of wildlife in Wyoming. Wyoming Game and Fish Department, Cheyenne, pp 155–187

    Google Scholar 

  • Kumaratilake LM, Thompson RC (1982) A review of the taxonomy and speciation of the genus Echinococcus Rudolphi 1801. Z Parasitenkd 68(2):121–146. https://doi.org/10.1007/BF00935054

    Article  CAS  PubMed  Google Scholar 

  • Leiby PD, Dyer WG (1971) Tapeworms. In: Davis JW, Anderson RC (eds) Parasitic Diseases of Wild Mammals. The University of Iowa Press, Ames, Iowa, pp 180–188

    Google Scholar 

  • Liccioli S, Bialowas C, Ruckstuhl KE, Massolo A (2015) Feeding ecology informs parasite epidemiology: prey selection modulates encounter rate with Echinococcus multilocularis in urban coyotes. PLoS ONE 10(3):e0121646

    Article  Google Scholar 

  • Liu IKM, Schabe CW, Schantz PM, Allison MN (1970) The occurrence of Echinococcus granulosus in coyotes (Canis latrans) in the Central Valley of California. J Parasitol 56(6):1135–1137

    Article  CAS  Google Scholar 

  • Loveless RM, Andersen FL, Ramsay MJ, Hedelius RK (1978) Echinococcus granulosus in dogs and sheep in central Utah, 1971-1976. Am J Vet Res 39(3):499–502

    CAS  PubMed  Google Scholar 

  • Lymbery AJ (2017) Phylogenetic pattern, evolutionary processes and species delimitation in the genus Echinococcus. In: Echinococcus and Echinococcosis, Part A. Advances in Parasitol 95:111–145

    Article  CAS  Google Scholar 

  • Lymbery AJ, Jenkins EJ, Schurer JM, Thompson RC (2015) Echinococcus canadensis, E. borealis, and E. intermedius. What’s in a name? Trends Parasitol 31(1):23–29. https://doi.org/10.1016/j.pt2014.11.003

    Article  Google Scholar 

  • Miller MJ (1953) Hydatid infection in Canada. Can Med Assoc J 68:423

    CAS  PubMed  PubMed Central  Google Scholar 

  • Montana Fish, Wildlife and Parks (2010) Echinococcus fact sheet. Montana Fish, Wildlife and Parks publication, January 21 3 pp

  • Moro P, Schantz PM (2009) Echinococcosis: a review. Int J Infect Dis 13:125–133

    Article  CAS  Google Scholar 

  • Rausch RL (1986) Life-cycle patterns and geographic distribution of Echinococcus species. In: Thompson RCA (ed) The biology of Echinococcus and hydatid disease. George Allen and Unwin Publishers, London, UK, pp 44–80

    Google Scholar 

  • Romano MN, Brunetti OA, Schwabe CW, Rosen MN (1974) Probable transmission of E. granulosus between deer and coyotes in California. J Wildl Dis 10:225–227

    Article  CAS  Google Scholar 

  • Romig T, DePlazes P, Jenkins D, Giraudoux P, Massolo A, Craig PS, Wassermann M, Takahashi K, de la Rue M (2017) Ecology and life cycle patterns of Echinococcus species. Advances in Parasitol 95:213–314

    Article  CAS  Google Scholar 

  • Santa MA, Pastran SA, Klein C, Duignan P, Ruckstuhl K, Romig T, Massolo A (2018) Detecting co-infections of Echinococcus multilocularis and Echinococcus canadensis in coyotes and red foxes in Alberta, Canada using real-time PCR. Int J Parasitol 7:111–115

    Google Scholar 

  • Schurer JM, Bouchard E, Bryant A, Revell S, Chavis G, Lichtenwalner A, Jenkins EJ (2018) Echinococcus in wild canids in Québec (Canada) and Maine (USA). PLoS Negl Trop Dis. 12(8):e0006712. https://doi.org/10.1371/journal.pntd.0006712

    Article  PubMed  PubMed Central  Google Scholar 

  • Seesee FM, Sterner MC, Worley DE (1983) Helminths of the coyote in Montana. J Wildl Dis 19(1):54–55

    Article  CAS  Google Scholar 

  • Sweatman GK (1952) Distribution and incidence of Echinococcus granulosus in man and other animals with special reference to Canada. Can J Public Health 43:480–486

    CAS  PubMed  Google Scholar 

  • Thompson RCA (2017) Biology and systematics of Echinococcus. In: Echinococcus and Echinococcosis, Part A. Advances in Parasitol 95:65–109

    Article  CAS  Google Scholar 

  • Torgerson PR, Budke CM (2003) Echinococcosis – an international public health challenge. Res Vet Sci 74:191–202

    Article  CAS  Google Scholar 

Download references

Acknowledgments

We would like to thank Brian DeBolt and Mike Boyce, Wyoming Game and Fish Department, and Mike Jimenez, US Fish and Wildlife Service (retired), for collection of wolf samples. Troy Aleshire, Dan Braig, Jim Angal, Emily Hepler, and Joel Modey with the US Department of Agriculture Wildlife Services provided samples from coyotes and red foxes.

Funding

This study was funded by the United States Department of Agriculture (USDA) Wildlife Services National Wildlife Disease Program.

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Authors

Contributions

Data collection and sample processing were conducted by David Fowler and Katherine Bardsley. Berit Bangoura identified the parasite specimens. The manuscript was prepared by Michael Pipas and Berit Bangoura.

Corresponding author

Correspondence to Michael J. Pipas.

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No ethical approval is required, as no human participants were involved in this study.

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No human participants were involved in this study.

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No human participants were involved in this study.

Conflict of interest

The authors declare no conflict of interest.

Welfare of animals

All samples were collected from wild animals euthanized during the course of wildlife damage management activities conducted by USDA Wildlife Services and the Wyoming Game and Fish Department.

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Section Editor: Bruno Gottstein

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Pipas, M.J., Fowler, D.R., Bardsley, K.D. et al. Survey of coyotes, red foxes and wolves from Wyoming, USA, for Echinococcus granulosus s. l.. Parasitol Res 120, 1335–1340 (2021). https://doi.org/10.1007/s00436-021-07059-1

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  • DOI: https://doi.org/10.1007/s00436-021-07059-1

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