Gray Wolves As Sentinels for the Presence of . and Other Gastrointestinal Parasites in France

Overview

Journal Int J Parasitol Parasites Wildl

Date 2023 Oct 2

PMID 37780970

Authors

Gerald Umhang

Christophe Duchamp

Jean-Marc Boucher

Christophe Caillot

Leo Legras

Jean-Michel Demerson

Jeremie Lucas

Dominique Gauthier

Franck Boue

Affiliations

Soon will be listed here.

Abstract

Over the past 30 years, the gray wolf population has recovered in France, initially to wolves from Italy passing through the Alps. The population is carefully monitored, but little information is available on their helminth fauna, which includes parasites of public health importance: and . Capitalizing on the availability of 911 fecal samples collected for the noninvasive genetic monitoring of French wolf populations, along with the intestines from 15 dead wolves, the presence of species among others helminth species was evaluated in French wolves. A copro-PCR approach amplifying a large spectrum of parasites was used for fecal samples while intestines were analyzed using SCT. The fecal occurrences of (2.4%) (0.3%), and indeedother parasitic species, are similar to those of other European wolf populations including (7.2%), (2.4%), (2.4%), (1.9%), (0.3%), (0.1%), and (0.1%). The three most abundant species were also found in the intestines. Infections by are in accordance with the overlap of wolf pack areas and sheep breeding pastoral units. However, the wolf does not appear to play a significant role in the lifecycle of . The availability of this opportunistic fecal sampling of wolves in southeastern France means that they can be used as sentinels for the surveillance of in the context of its southward expansion observed in recent years.

Citing Articles

New evidence from the northern Apennines, Italy, suggests a southward expansion of Echinococcus multilocularis range in Europe.

Cafiero S, Petroni L, Natucci L, Tomassini O, Romig T, Wassermann M Sci Rep. 2025; 15(1):7353.

PMID: 40025062 PMC: 11873164. DOI: 10.1038/s41598-025-91596-7.

The grey wolf as a host of . and other helminths - a new zoonotic threat in Poland.

Karamon J, Samorek-Pierog M, Bilska-Zajac E, Korpysa-Dzirba W, Sroka J, Zdybel J J Vet Res. 2025; 68(4):539-549.

PMID: 39776693 PMC: 11702251. DOI: 10.2478/jvetres-2024-0060.

Echinococcus granulosus Sensu Stricto and Echinococcus multilocularis in a Gray Wolf (Canis lupus) in Turkey: Further Evidence for Increased Risk of Alveolar Echinococcosis in Urban Areas.

Akyuz M, Kirman R, Guven E, Balkaya I, Avcioglu H Acta Parasitol. 2024; 69(2):1319-1323.

PMID: 38662075 PMC: 11182862. DOI: 10.1007/s11686-024-00842-x.

Wildlife parasitology: sample collection and processing, diagnostic constraints, and methodological challenges in terrestrial carnivores.

Rojas A, Germitsch N, Oren S, Sazmand A, Deak G Parasit Vectors. 2024; 17(1):127.

PMID: 38481271 PMC: 10938792. DOI: 10.1186/s13071-024-06226-4.

species in wildlife.

Romig T, Wassermann M Int J Parasitol Parasites Wildl. 2024; 23:100913.

PMID: 38405672 PMC: 10884515. DOI: 10.1016/j.ijppaw.2024.100913.

References

Gawor J, Laskowski Z, Myczka A, Zwijacz-Kozica T, Salamatin R . Occurrence of spp. in red foxes and wolves in the protected area of the Tatra National Park in southern Poland - a threat to human health. Ann Agric Environ Med. 2021; 28(4):579-584. DOI: 10.26444/aaem/131649. View

Martinek K, Kolarova L, Hapl E, Literak I, Uhrin M . Echinococcus multilocularis in European wolves (Canis lupus). Parasitol Res. 2001; 87(10):838-9. DOI: 10.1007/s004360100452. View

Massolo A, Valli D, Wassermann M, Cavallero S, DAmelio S, Meriggi A . Unexpected infections in shepherd dogs and wolves in south-western Italian Alps: A new endemic area?. Int J Parasitol Parasites Wildl. 2018; 7(3):309-316. PMC: 6115541. DOI: 10.1016/j.ijppaw.2018.08.001. View

Umhang G, Woronoff-Rhen N, Combes B, Boue F . Segmental sedimentation and counting technique (SSCT): an adaptable method for qualitative diagnosis of Echinococcus multilocularis in fox intestines. Exp Parasitol. 2011; 128(1):57-60. DOI: 10.1016/j.exppara.2011.01.004. View

Umhang G, Duchamp C, Boucher J, Ruette S, Boue F, Richomme C . Detection of DNA from the zoonotic raccoon roundworm Baylisascaris procyonis in a French wolf. Parasitol Int. 2020; 78:102155. DOI: 10.1016/j.parint.2020.102155. View

Umhang G, Richomme C, Hormaz V, Boucher J, Boue F . Pigs and wild boar in Corsica harbor Echinococcus canadensis G6/7 at levels of concern for public health and local economy. Acta Trop. 2014; 133:64-8. DOI: 10.1016/j.actatropica.2014.02.005. View

Lavikainen A, Laaksonen S, Beckmen K, Oksanen A, Isomursu M, Meri S . Molecular identification of Taenia spp. in wolves (Canis lupus), brown bears (Ursus arctos) and cervids from North Europe and Alaska. Parasitol Int. 2011; 60(3):289-95. DOI: 10.1016/j.parint.2011.04.004. View

Eckert J . Predictive values and quality control of techniques for the diagnosis of Echinococcus multilocularis in definitive hosts. Acta Trop. 2003; 85(2):157-63. DOI: 10.1016/s0001-706x(02)00216-4. View

Umhang G, Richomme C, Caillot C, Bastid V, Boucher J, Moyen J . Towards delimitation of the Echinococcus multilocularis parasite's southernmost range in France. Vet Parasitol Reg Stud Reports. 2022; 30:100724. DOI: 10.1016/j.vprsr.2022.100724. View

10.

Bagrade G, Kirjusina M, Vismanis K, Ozolins J . Helminth parasites of the wolf Canis lupus from Latvia. J Helminthol. 2009; 83(1):63-8. DOI: 10.1017/S0022149X08123860. View

11.

Gori F, Armua-Fernandez M, Milanesi P, Serafini M, Magi M, Deplazes P . The occurrence of taeniids of wolves in Liguria (northern Italy). Int J Parasitol Parasites Wildl. 2015; 4(2):252-5. PMC: 4443502. DOI: 10.1016/j.ijppaw.2015.04.005. View

12.

Macchioni F, Coppola F, Furzi F, Gabrielli S, Baldanti S, Boni C . Taeniid cestodes in a wolf pack living in a highly anthropic hilly agro-ecosystem. Parasite. 2021; 28:10. PMC: 7863970. DOI: 10.1051/parasite/2021008. View

13.

Grenouillet F, Umhang G, Arbez-Gindre F, Mantion G, Delabrousse E, Millon L . Echinococcus ortleppi infections in humans and cattle, France. Emerg Infect Dis. 2014; 20(12):2100-2. PMC: 4257792. DOI: 10.3201/eid2012.140641. View

14.

Borecka A, Gawor J, Zieba F . A survey of intestinal helminths in wild carnivores from the Tatra National Park, southern Poland. Ann Parasitol. 2014; 59(4):169-72. View

15.

Poglayen G, Gori F, Morandi B, Galuppi R, Fabbri E, Caniglia R . Italian wolves ( Altobello, 1921) and molecular detection of taeniids in the Foreste Casentinesi National Park, Northern Italian Apennines. Int J Parasitol Parasites Wildl. 2017; 6(1):1-7. PMC: 5284487. DOI: 10.1016/j.ijppaw.2017.01.001. View

16.

Al-Sabi M, Raaf L, Osterman-Lind E, Uhlhorn H, Kapel C . Gastrointestinal helminths of gray wolves (Canis lupus lupus) from Sweden. Parasitol Res. 2018; 117(6):1891-1898. DOI: 10.1007/s00436-018-5881-z. View

17.

Guberti V, Stancampiano L, Francisci F . Intestinal helminth parasite community in wolves (Canis lupus) in Italy. Parassitologia. 1993; 35(1-3):59-65. View

18.

Hofer S, Gloor S, Muller U, Mathis A, Hegglin D, Deplazes P . High prevalence of Echinococcus multilocularis in urban red foxes (Vulpes vulpes) and voles (Arvicola terrestris) in the city of Zürich, Switzerland. Parasitology. 2000; 120 ( Pt 2):135-42. DOI: 10.1017/s0031182099005351. View

19.

Combes B, Comte S, Raton V, Raoul F, Boue F, Umhang G . Westward spread of Echinococcus multilocularis in foxes, France, 2005-2010. Emerg Infect Dis. 2012; 18(12):2059-62. PMC: 3557902. DOI: 10.3201/eid1812.120219. View

20.

Umhang G, Comte S, Hormaz V, Boucher J, Raton V, Favier S . Retrospective analyses of fox feces by real-time PCR to identify new endemic areas of Echinococcus multilocularis in France. Parasitol Res. 2016; 115(11):4437-4441. DOI: 10.1007/s00436-016-5220-1. View