Prevalence of Alaria infection in companion animals in north central Oklahoma from 2006 through 2015 and detection in wildlife

Eileen M. Johnson Department of Veterinary Pathobiology, Center for Veterinary Health Sciences, Oklahoma State University, Stillwater, OK 74078.

Search for other papers by Eileen M. Johnson in
Current site
Google Scholar
PubMed
Close
 DVM, PhD
,
Yoko Nagamori Department of Veterinary Pathobiology, Center for Veterinary Health Sciences, Oklahoma State University, Stillwater, OK 74078.

Search for other papers by Yoko Nagamori in
Current site
Google Scholar
PubMed
Close
 DVM
,
Rebecca A. Duncan-Decocq Department of Veterinary Pathobiology, Center for Veterinary Health Sciences, Oklahoma State University, Stillwater, OK 74078.

Search for other papers by Rebecca A. Duncan-Decocq in
Current site
Google Scholar
PubMed
Close
 MS
,
Patrick N. Whitley USDA APHIS Wildlife Service, 2800 N Lincoln Blvd, Oklahoma City, OK 73105.

Search for other papers by Patrick N. Whitley in
Current site
Google Scholar
PubMed
Close
,
Akhilesh Ramachandran Department of Veterinary Pathobiology, Center for Veterinary Health Sciences, Oklahoma State University, Stillwater, OK 74078.

Search for other papers by Akhilesh Ramachandran in
Current site
Google Scholar
PubMed
Close
 BVSc&AH, PhD
, and
Mason V. Reichard Department of Veterinary Pathobiology, Center for Veterinary Health Sciences, Oklahoma State University, Stillwater, OK 74078.

Search for other papers by Mason V. Reichard in
Current site
Google Scholar
PubMed
Close
 PhD

Abstract

OBJECTIVE To determine the prevalence of Alaria infection in cats and dogs in north central Oklahoma over various periods and investigate whether wild animal species in this region were also infected.

DESIGN Combined cross-sectional study and case series.

SAMPLE Results of parasitological testing of fecal samples from 5,417 client-owned dogs and 1,246 client-owned cats (2006 through 2014); fecal samples from 837 shelter or rescue dogs and 331 shelter or rescue cats (2013 and 2014) and 268 feral cats (2015); tongue or jowl samples from cadavers of 43 wild pigs, 3 opossums, and 1 raccoon; and intestinal tract segments from cadavers of 48 cats and 5 coyotes.

PROCEDURES Various parasite recovery techniques were performed to detect various Alaria stages in samples. Recovered adult trematodes and mesocercariae were used for PCR assay and sequencing of the 28S rRNA gene.

RESULTS Prevalence of Alaria infection was significantly higher in feral cats (9.0%) than in shelter or rescue cats (0.6%) and client-owned cats (1.4%) and in shelter or rescue dogs (1.8%) than in client-owned dogs (0.2%). Mesocercariae were recovered from tissue samples from 11 (26%) wild pigs and 1 opossum. Amplicon sequences from adult trematodes and mesocercariae were 100% identical to each other and 99% homologous to GenBank sequences of Alaria alata and Alaria mustelae.

CONCLUSIONS AND CLINICAL RELEVANCE Prevalence of Alaria infection in the study area has increased in dogs and cats since 1990, when infections were rare. Prevalence in wild pigs was similar to that in Eurasia, where A alata is considered an emerging zoonotic parasite.

Abstract

OBJECTIVE To determine the prevalence of Alaria infection in cats and dogs in north central Oklahoma over various periods and investigate whether wild animal species in this region were also infected.

DESIGN Combined cross-sectional study and case series.

SAMPLE Results of parasitological testing of fecal samples from 5,417 client-owned dogs and 1,246 client-owned cats (2006 through 2014); fecal samples from 837 shelter or rescue dogs and 331 shelter or rescue cats (2013 and 2014) and 268 feral cats (2015); tongue or jowl samples from cadavers of 43 wild pigs, 3 opossums, and 1 raccoon; and intestinal tract segments from cadavers of 48 cats and 5 coyotes.

PROCEDURES Various parasite recovery techniques were performed to detect various Alaria stages in samples. Recovered adult trematodes and mesocercariae were used for PCR assay and sequencing of the 28S rRNA gene.

RESULTS Prevalence of Alaria infection was significantly higher in feral cats (9.0%) than in shelter or rescue cats (0.6%) and client-owned cats (1.4%) and in shelter or rescue dogs (1.8%) than in client-owned dogs (0.2%). Mesocercariae were recovered from tissue samples from 11 (26%) wild pigs and 1 opossum. Amplicon sequences from adult trematodes and mesocercariae were 100% identical to each other and 99% homologous to GenBank sequences of Alaria alata and Alaria mustelae.

CONCLUSIONS AND CLINICAL RELEVANCE Prevalence of Alaria infection in the study area has increased in dogs and cats since 1990, when infections were rare. Prevalence in wild pigs was similar to that in Eurasia, where A alata is considered an emerging zoonotic parasite.

Contributor Notes

Address correspondence to Dr. Johnson (eileen.johnson@okstate.edu).
  • 1. Möhl K, Große K, Hamedy A, et al. Biology of Alaria spp. and human exposition risk to Alaria mesocercariae—a review. Parasitol Res 2009; 105: 115.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 2. Pearson JC. Studies on the life cycles and morphology of the larval stages of Alaria arisaemoides Augustine and Uribe, 1927 and Alaria canis Larue and Fallis, 1936 (Trematoda: Diplostomatidae). Can J Zool 1956; 34: 295387.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 3. Shoop WL, Corkum KC. Maternal transmission by Alaria marcianae (Trematoda) and the concept of amphiparatenesis. J Parasitol 1987; 73: 110115.

  • 4. Foster GW, Kinsella JM, Sheppard BJ, et al. Transmammary infection of free-ranging Florida panther neonates by Alaria marcianae (Trematoda: Diplostomatidae). J Parasitol 2009; 95: 238239.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 5. Pence DB, Knowlton FF, Windberg LA. Transmission of A ncylostoma caninum and Alaria marcianae in coyotes (Canis latrans). J Wildl Dis 1988; 24: 560563.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 6. Wasiluk A. Alaria alata infection—threatening yet rarely detected trematodiasis. J Lab Diagn 2013; 49: 3337.

  • 7. Portier J, Jouet D, Vallee I, et al. Detection of Planorbis planorbis and Anisus vortex as first intermediate hosts of Alaria alata (Goeze 1792) in natural conditions in France: molecular evidence. Vet Parasitol 2012; 190: 151158.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 8. Patrelle C, Portier C, Jouet D, et al. Prevalence and intensity of Alaria alata (Goeze, 1792) in water frogs and brown frogs in natural conditions. Parasitol Res 2015; 114: 44054412.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 9. Fernandes BJ, Cooper JD, Cullen JB, et al. Systemic infection with Alaria americana (Trematoda). Can Med Assoc J 1976; 115: 11111114.

    • Search Google Scholar
    • Export Citation
  • 10. Otranto D, Eberhard ML. Zoonotic helminths affecting the human eye. Parasit Vectors 2011; 4: 121.

  • 11. Odening K. The “Duncker muscle fluke” can be transmitted experimentally to monkeys (in Germany). Monatsh Vet Med 1961; 16: 395399.

    • Search Google Scholar
    • Export Citation
  • 12. Rentería-Solis ZM, Hamedy A, Michler F, et al. Alaria alata mesocercariae in raccoons (Procyon lotor) in Germany. Parasitol Res 2013; 112: 35953600.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 13. Portier J, Vallée I, Lacour SA, et al. Increasing circulation of Alaria alata mesocercaria in wild boar populations of the Rhine valley, France, 2007–2011. Vet Parasitol 2014; 199: 153159.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 14. Riehn K, Große K, Hamedy A, et al. Detection of Alaria spp. mesocercariae in game meat in Germany. In: Paulsen P, Bauer A, Vodnansky M, et al, eds. Game meat hygiene in focus. Wageningen, The Netherlands: Wageningen Academic Publishers, 2011;119125.

    • Search Google Scholar
    • Export Citation
  • 15. Paulsena P, Ehebruster J, Irschik I, et al. Findings of Alaria alata metacercariae in wild boars (Sus scrofa) in Eastern Austria. Eur J Wildl Res 2012; 58: 991995.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 16. Paulsen P, Forejtek P, Hutarova Z, et al. Alaria alata mesocercariae in wild boar (Sus scrofa, Linnaeus, 1758) in south regions of the Czech Republic. Vet Parasitol 2013; 197: 384387.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 17. Portier J, Jouet D, Ferte H, et al. New data in France on the trematode Alaria alata (Goeze, 1792) obtained during Trichinella inspections. Parasite 2011; 18: 271275.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 18. Esite Z, Deksae G, Bagrade G. Overview of Alaria alata distribution in different host animals in Latvia, in Proceedings. Anim Health Food Hyg Conf 2012;36.

    • Search Google Scholar
    • Export Citation
  • 19. Riehn K, Lalkovski N, Hamedy A, et al. First detection of Alaria alata mesocercariae in wild boars (Sus scrofa, Linnaeus, 1758) from Bulgaria. J Helminthol 2014; 88: 247249.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 20. Duscher GG, Leschnik M, Fuehrer HP, et al. Wildlife reservoirs for vector-borne canine, feline and zoonotic infections in Austria. Int J Parasitol Parasites Wildl 2014; 4: 8896.

    • Search Google Scholar
    • Export Citation
  • 21. Gamble HR. Trichinae. Available at: www.aphis.usda.gov/vs/trichinae/docs/fact_sheet.htm. Accessed Jan 28, 2015.

  • 22. USDA National Agricultural Library. Wild boar. Available at: www.invasivespeciesinfo.gov/animals/wildboar.shtml. Accessed Sep 29, 2015.

    • Search Google Scholar
    • Export Citation
  • 23. Stevens RL. Current status and distribution. In: The feral hog in Oklahoma: Ardmore, Oklahoma. Ardmore, Okla: The Samuel Roberts Noble Foundation, 2010;119.

    • Search Google Scholar
    • Export Citation
  • 24. Meng XJ, Lindsay DS, Sriranganathan N. Wild boars as sources for infectious diseases in livestock and humans. Parasite 2011; 18: 271275.

    • Search Google Scholar
    • Export Citation
  • 25. Széll Z, Tolnai Z, Sreter T. Environmental determinants of the spatial distribution of Alaria alata in Hungary. Vet Parasitol 2013; 198: 116121.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 26. Blagburn BL, Schenker R, Gagne F, et al. Prevalence of intestinal parasites in companion animals in Ontario and Quebec, Canada during the winter months. Vet Ther 2008; 9: 169175.

    • Search Google Scholar
    • Export Citation
  • 27. Hiestand SJ, Nielsen CK, Jimenez FA. Epizootic and zoonotic helminths of the bobcat (Lynx rufus) in Illinois and a comparison of its helminth component communities across the American midwest. Parasite 2014; 21: 4.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 28. Foster GW, Main MB, Kinsella JM, et al. Parasitic helminths and arthropods of coyotes (Canis latrans) from Florida, USA. Comp Parasitol 2003; 70: 162166.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 29. Rausch R, Williamson FS. Studies on the helminth fauna of Alaska. XXXIV. The parasites of wolves, Canis lupus. J Parasitol 1959; 45: 395403.

  • 30. Samuel WM, Ramalingam S, Carbyn LN. Helminths in coyotes (Canis latrans Say), wolves (Canis lupus L.), and red foxes (Vulpes vulpes L.) of southwestern Manitoba. Can J Zool 1978; 56: 26142617.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 31. Unruh DHA, King JE, Eaton RDP, et al. Parasites of dogs from Indian settlements in northwestern Canada: a survey with public health implications. Can J Comp Med 1973; 37: 2532.

    • Search Google Scholar
    • Export Citation
  • 32. Lucio-Forster A, Bowman DD. Prevalence of fecal-borne parasites detected by centrifugal flotation in feline samples from two shelters in upstate New York. J Feline Med Surg 2011; 13: 300303.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 33. Jordan HE, Mullens ST, Stebbins ME. Endoparasitism in dogs: 21,584 cases (1981–1990). J Am Vet Med Assoc 1993; 203: 547549.

  • 34. Zajac AM, Conboy GA, eds. Fecal examination for the diagnosis of parasitism. In: Veterinary clinical parasitology. 7th ed. Ames, Iowa: Blackwell Publishing, 2006;38.

    • Search Google Scholar
    • Export Citation
  • 35. Schell SC. Key to families and genera of subclass digenea. In: Handbook of trematodes of North America. Moscow: University Press of Idaho, 1985;7885, 90–94.

    • Search Google Scholar
    • Export Citation
  • 36. Riehn K, Hamedy A, Saffaf J, et al. First interlaboratory test for the detection of Alaria spp. mesocercariae in meat samples using the Alaria spp. mesocercariae migration (AMT). Parasitol Res 2013; 112: 26532660.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 37. Riehn K, Hamedy A, Alter T, et al. Development of a PCR approach for differentiation of Alaria spp. mesocercariae. Parasitol Res 2011; 108: 13271332.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 38. Sokal RR, Rohlf FJ. 1997. The chi-square distribution. In: Biometry. 3rd ed. New York: WH Freeman and Co, 1997;152–154.

  • 39. González-Fuentes H, Riehn K, Koethe M, et al. Effects of in vitro conditions on the survival of Alaria alata mesocercariae. Parasitol Res 2014; 113: 29832989.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 40. González-Fuentes H, Hamedy A, von Borell E, et al. Tenacity of Alaria alata mesocercariae in homemade German meat products. Int J Food Microbiol 2014; 176: 914.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 41. González-Fuentes H, Hamedy A, Koethe M, et al. Effect of temperature on the survival of Alaria alata mesocercariae. Parasitol Res 2015; 114: 11791187.

    • Crossref
    • Search Google Scholar
    • Export Citation

Advertisement