• 1. Wiethoelter AK, Beltrán-Alcrudo D, Kock R, et al. Global trends in infectious diseases at the wildlife-livestock interface. Proc Natl Acad Sci U S A 2015;112:96629667.

    • Search Google Scholar
    • Export Citation
  • 2. Barling KS, Sherman M, Peterson MJ, et al. Spatial associations among density of cattle, abundance of wild canids, and seroprevalence to Neospora caninum in a population of beef calves. J Am Vet Med Assoc 2000;217:13611365.

    • Search Google Scholar
    • Export Citation
  • 3. Bevins S, Blizzard E, Bazan L, et al. Neospora caninum exposure in overlapping populations of coyotes (Canis latrans) and feral swine (Sus scrofa). J Wildl Dis 2013;49:10281032.

    • Search Google Scholar
    • Export Citation
  • 4. Gondim LFP, McAllister MM, Pitt WC, et al. Coyotes (Canis latrans) are definitive hosts of Neospora caninum. Int J Parasitol 2004;34:159161.

    • Search Google Scholar
    • Export Citation
  • 5. Bekoff M, Gese EM. Coyote (Canis latrans) In: Feldhamer GA, Thompson BC, Chapman JA, eds. Wild mammals of North America: biology, management, and conservation. Baltimore: Johns Hopkins University Press, 2003;467481.

    • Search Google Scholar
    • Export Citation
  • 6. Moore GC, Parker GR. Colonization by the eastern coyote (Canis latrans). In: Boer AH, ed. Ecology and management of the eastern coyote. Fredericton, NB, Canada: Wildlife Research Unit, University of New Brunswick, 1992;2337.

    • Search Google Scholar
    • Export Citation
  • 7. USDA. Cattle and calves predator death loss in the United States. Fort Collins, Colo: USDA-APHIS-VS-CEAH, National Animal Health Monitoring System, 2005.

    • Search Google Scholar
    • Export Citation
  • 8. USDA. Cattle death loss. Fort Collins, Colo: National Agricultural Statistics Service, Agricultural Statistics Board, USDA, 2011.

  • 9. USDA. Cattle and calves death loss. Fort Collins, Colo: USDA, APHIS, National Agricultural Statistics Service, 1995.

  • 10. ODNR. Coyote relative abundance 1990–2011. Columbus, Ohio: ODNR Division of Wildlife, 2012.

  • 11. Gehrt SD. Urban coyote ecology and management: the Cook county, Illinois, coyote project. OSU Extension Bulletin 929, 2006.

  • 12. Sacks BN, Neale JCC. Coyote abundance, sheep predation, and wild prey correlates illuminate Mediterranean trophic dynamics. J Wildl Manage 2007;71:24042411.

    • Search Google Scholar
    • Export Citation
  • 13. Bapodra P, Wolfe BA. Investigation of Neospora caninum seroprevalence and potential impact on reproductive success in semi-free-ranging Père David's deer (Elaphurus davidianus). Vet Rec Open 2015;2:e000123.

    • Search Google Scholar
    • Export Citation
  • 14. Moreno-Torres K, Wolfe B, Saville W, et al. Estimating Neospora caninum prevalence in wildlife populations using bayesian inference. Ecol Evol 2016;6:22162225.

    • Search Google Scholar
    • Export Citation
  • 15. Bekoff M, Gese EM. Coyote (Canis latrans). Fort Collins, Colo: USDA National Wildlife Research Center, 2003;224.

  • 16. Gese EM. Monitoring of terrestrial carnivore populations. In: Gittleman JL, Funk SM, Macdonald DW, et al, eds. Carnivore conservation. Cambridge, England: Cambridge University Press, 2001;372396.

    • Search Google Scholar
    • Export Citation
  • 17. Wapenaar W, Jenkins MC, O'Handley RM, et al. Neospora caninum-like oocysts observed in feces of free-ranging red foxes (Vulpes vulpes) and coyotes (Canis latrans). J Parasitol 2006;92:12701274.

    • Search Google Scholar
    • Export Citation
  • 18. Halfpenny J. Scats and tracks of the Midwest: a field guide to the signs of seventy wildlife species: Guilford, Conn: Globe Pequot Press, 2006;7681.

    • Search Google Scholar
    • Export Citation
  • 19. Wallace DM. Precipitation of nucleic acids. Methods Enzymol 1987;152:4148.

  • 20. Adams JR, Kelly BT, Waits LP. Using faecal DNA sampling and GIS to monitor hybridization between red wolves (Canis rufus) and coyotes (Canis latrans). Mol Ecol 2003;12:21752186.

    • Search Google Scholar
    • Export Citation
  • 21. Gondim LF, Gao L, McAllister MM. Improved production of Neospora caninum oocysts, cyclical oral transmission between dogs and cattle, and in vitro isolation from oocysts. J Parasitol 2002;88:11591163.

    • Search Google Scholar
    • Export Citation
  • 22. Hill DE, Liddell S, Jenkins MC, et al. Specific detection of Neospora caninum oocysts in fecal samples from experimentally-infected dogs using the polymerase chain reaction. J Parasitol 2001;87:395398.

    • Search Google Scholar
    • Export Citation
  • 23. Sinnott D, Moreno Torres K, Wolfe B, et al. Detection of Hammondia heydorni DNA in feces collected in and around an Ohio wildlife conservation center. Vet Parasitol Reg Stud Reports 2016;6:3134.

    • Search Google Scholar
    • Export Citation
  • 24. Lalonde LF, Gajadhar AA. Detection and differentiation of coccidian oocysts by real-time PCR and melting curve analysis. J Parasitol 2011;97:725730.

    • Search Google Scholar
    • Export Citation
  • 25. Müller N, Zimmermann V, Hentrich B, et al. Diagnosis of Neospora caninum and Toxoplasma gondii infection by PCR and DNA hybridization immunoassay. J Clin Microbiol 1996;34:28502852.

    • Search Google Scholar
    • Export Citation
  • 26. Slapeta JR, Modry D, Kyselova I, et al. Dog shedding oocysts of Neospora caninum: PCR diagnosis and molecular phylogenetic approach. Vet Parasitol 2002;109:157167.

    • Search Google Scholar
    • Export Citation
  • 27. Webbon CC, Baker PJ, Harris S. Faecal density counts for monitoring changes in red fox numbers in rural Britain. J Appl Ecol 2004;41:768779.

    • Search Google Scholar
    • Export Citation
  • 28. Thrusfield M. Veterinary epidemiology. 3rd ed. Oxford, England: Blackwell Science Ltd, 2007;240.

  • 29. Wilson EB. Probable inference, the law of succession, and statistical inference. J Am Stat Assoc 1927;22:209212.

  • 30. Newcombe RG. Two-sided confidence intervals for the single proportion: comparison of seven methods. Stat Med 1998;17:857872.

  • 31. Cohen J. A coefficient of agreement for nominal scales. Educ Psychol Meas 1960;20:3746.

  • 32. Chapanis A. An exact multinomial one-sample test of significance. Psychol Bull 1962;59:306310.

  • 33. Atwood TC, Vercauteren KC, Deliberto TJ, et al. Coyotes as sentinels for monitoring bovine tuberculosis prevalence in white-tailed deer. J Wildl Manage 2007;71:15451554.

    • Search Google Scholar
    • Export Citation
  • 34. Bowman DD, Georgi JR. Georgis' parasitology for veterinarians. 9th ed. St Louis: Elsevier Health Sciences, 2009.

  • 35. Almería S, Ferrer D, Pabón M, et al. Red foxes (Vulpes vulpes) are a natural intermediate host of Neospora caninum. Vet Parasitol 2002;107:287294.

    • Search Google Scholar
    • Export Citation
  • 36. Schares G, Heydorn AO, Cuppers A, et al. In contrast to dogs, red foxes (Vulpes vulpes) did not shed neospora caninum upon feeding of intermediate host tissues. Parasitol Res 2002;88:4452.

    • Search Google Scholar
    • Export Citation
  • 37. Stuart P, Zintl A, Waal TD, et al. Investigating the role of wild carnivores in the epidemiology of bovine neosporosis. Parasitology 2013;140:296302.

    • Search Google Scholar
    • Export Citation
  • 38. Bartley PM, Wright SE, Zimmer IA, et al. Detection of Neospora caninum in wild carnivorans in Great Britain. Vet Parasitol 2013;192:279283.

    • Search Google Scholar
    • Export Citation
  • 39. Ohio Department of Natural Resources. Red fox relative abundance 1990–2011. Columbus, Ohio: Ohio Department of Natural Resources, Division of Wildlife, 2012.

    • Search Google Scholar
    • Export Citation
  • 40. Dubey JP. A review of Sarcocystis of domestic animals and of other coccidia of cats and dogs. J Am Vet Med Assoc 1976;169:10611078.

    • Search Google Scholar
    • Export Citation
  • 41. Schares G, Pantchev N, Barutzki D, et al. Oocysts of Neospora caninum, Hammondia heydorni, Toxoplasma gondii and Hammondia hammondi in faeces collected from dogs in Germany. Int J Parasitol 2005;35:15251537.

    • Search Google Scholar
    • Export Citation
  • 42. Palavicini P, Romero JJ, Dolz G, et al. Fecal and serological survey of Neospora caninum in farm dogs in Costa Rica. Vet Parasitol 2007;149:265270.

    • Search Google Scholar
    • Export Citation
  • 43. Razmi G. Fecal and molecular survey of Neospora caninum in farm and household dogs in Mashhad area, Khorasan Province, Iran. Korean J Parasitol 2009;47:417420.

    • Search Google Scholar
    • Export Citation
  • 44. King JS, Brown GK, Jenkins DJ, et al. Oocysts and high seroprevalence of Neospora caninum in dogs living in remote aboriginal communities and wild dogs in Australia. Vet Parasitol 2012;187:8592.

    • Search Google Scholar
    • Export Citation
  • 45. Asmare K, Skjerve E, Bekele J, et al. Molecular identification of Neospora caninum from calf/foetal brain tissue and among oocysts recovered from faeces of naturally infected dogs in southern Ethiopia. Acta Trop 2013;130:8893.

    • Search Google Scholar
    • Export Citation
  • 46. McGarry JW, Stockton CM, Williams DJ, et al. Protracted shedding of oocysts of Neospora caninum by a naturally infected foxhound. J Parasitol 2003;89:628630.

    • Search Google Scholar
    • Export Citation
  • 47. Gondim LF, McAllister MM, Gao L. Effects of host maturity and prior exposure history on the production of Neospora caninum oocysts by dogs. Vet Parasitol 2005;134:3339.

    • Search Google Scholar
    • Export Citation
  • 48. Cypher Brian L. Foxes (Vulpes species, Urocyon species, and Alopex lagopus). In: Feldhamer GA, Thompson BC, Chapman JA, eds. Wild mammals of North America: biology, management, and conservation. Baltimore: Johns Hopkins University Press, 2003;511546.

    • Search Google Scholar
    • Export Citation
  • 49. Sobrino R, Dubey JP, Pabón M, et al. Neospora caninum antibodies in wild carnivores from Spain. Vet Parasitol 2008;155:190197.

  • 50. Dijkstra T, Eysker M, Schares G, et al. Dogs shed Neospora caninum oocysts after ingestion of naturally infected bovine placenta but not after ingestion of colostrum spiked with Neospora caninum tachyzoites. Int J Parasitol 2001;31:747752.

    • Search Google Scholar
    • Export Citation
  • 51. Dubey JP, Hemphill A, Calero-Bernal R, et al. Neosporosis in dogs. In: Neosporosis in animals. Boca Raton, Fla: CRC Press, 2017;261316.

    • Search Google Scholar
    • Export Citation
  • 52. Miller KV, Muller LI, Demarais S. White-tailed deer (Odocoileus virginianus). In: Feldhamer GA, Thompson BC, Chapman JA, eds. Wild mammals of North America: biology, management, and conservation. Baltimore: Johns Hopkins University Press, 2003;906930.

    • Search Google Scholar
    • Export Citation
  • 53. Elmore SA, Lalonde LF, Samelius G, et al. Endoparasites in the feces of arctic foxes in a terrestrial ecosystem in Canada. Int J Parasitol Parasites Wildl 2013;2:9096.

    • Search Google Scholar
    • Export Citation
  • 54. Alves Neto AF, Bandini LA, Nishi SM, et al. Viability of sporulated oocysts of Neospora caninum after exposure to different physical and chemical treatments. J Parasitol 2011;97:135139.

    • Search Google Scholar
    • Export Citation
  • 55. Lélu M, Villena I, Darde ML, et al. Quantitative estimation of the viability of Toxoplasma gondii oocysts in soil. Appl Environ Microbiol 2012;78:51275132.

    • Search Google Scholar
    • Export Citation
  • 56. Dabritz HA, Miller MA, Atwill ER, et al. Detection of Toxoplasma gondii-like oocysts in cat feces and estimates of the environmental oocyst burden. J Am Vet Med Assoc 2007;231:16761684.

    • Search Google Scholar
    • Export Citation
  • 57. Jenkins MC, Parker C, O'Brien C, et al. Differing susceptibilities of Eimeria acervulina, Eimeria maxima, and Eimeria tenella oocysts to desiccation. J Parasitol 2013;99:899902.

    • Search Google Scholar
    • Export Citation
  • 58. Moreno-Torres KI, Pomeroy LW, Moritz M, et al. Host species heterogeneity in the epidemiology of Neospora caninum. PLoS One 2017;12:e0183900.

    • Search Google Scholar
    • Export Citation

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Risk of environmental exposure to small coccidia from wild canid feces in rural Ohio

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  • 1 Department of Veterinary Preventive Medicine, The Ohio State University, Columbus, OH 43210.
  • | 2 College of Veterinary Medicine, The Ohio State University, Columbus, OH 43210.
  • | 3 Department of Veterinary Preventive Medicine, The Ohio State University, Columbus, OH 43210.
  • | 4 Department of Veterinary Preventive Medicine, The Ohio State University, Columbus, OH 43210.
  • | 5 Department of Veterinary Preventive Medicine, The Ohio State University, Columbus, OH 43210.
  • | 6 Department of Anthropology, College of Arts and Sciences, The Ohio State University, Columbus, OH 43210.
  • | 7 Department of Veterinary Preventive Medicine, The Ohio State University, Columbus, OH 43210.

Abstract

OBJECTIVE To determine the extent of environmental exposure to heteroxenous coccidia from wild canid feces in southeastern Ohio.

SAMPLE 285 presumed wild canid fecal samples collected across an ecological system in southeastern Ohio.

PROCEDURES Morphological classification and molecular analysis were used to determine the canid genus for collected fecal samples. Microscopic and molecular analysis were used to detect coccidian oocysts and DNA. Several variables were analyzed for associations with coccidian DNA detection or prevalence.

RESULTS Coccidian DNA was detected in 51 of 285 (17.9%) fecal samples. Of those positive samples, 1% (95% confidence interval, 0.4% to 3%) had positive results for Hammondia heydorni and none had positive results for Neospora caninum, for an estimated environmental N caninum prevalence of 0% (95% confidence interval, 0% to 7%)/1-km2 hexagonal area evaluated. Morphological classification revealed that 78.9% (225/285) of fecal samples were from coyotes and 17.2% (49/285) were from foxes. No difference in proportions of coccidian DNA-positive fecal samples was identified among canid species. Environmental temperature and fecal freshness were associated with coccidian DNA detection. Land use type, relative canid density, and cattle density were not associated with the prevalence of coccidian DNA-positive samples.

CONCLUSIONS AND CLINICAL RELEVANCE The low prevalence of coccidia shed in wild canid feces in this study, including the estimated 0% environmental prevalence of N caninum, suggested that the role of the oocyst environmental phase in coccidia transmission to ruminants is likely minor in rural southeastern Ohio.

Abstract

OBJECTIVE To determine the extent of environmental exposure to heteroxenous coccidia from wild canid feces in southeastern Ohio.

SAMPLE 285 presumed wild canid fecal samples collected across an ecological system in southeastern Ohio.

PROCEDURES Morphological classification and molecular analysis were used to determine the canid genus for collected fecal samples. Microscopic and molecular analysis were used to detect coccidian oocysts and DNA. Several variables were analyzed for associations with coccidian DNA detection or prevalence.

RESULTS Coccidian DNA was detected in 51 of 285 (17.9%) fecal samples. Of those positive samples, 1% (95% confidence interval, 0.4% to 3%) had positive results for Hammondia heydorni and none had positive results for Neospora caninum, for an estimated environmental N caninum prevalence of 0% (95% confidence interval, 0% to 7%)/1-km2 hexagonal area evaluated. Morphological classification revealed that 78.9% (225/285) of fecal samples were from coyotes and 17.2% (49/285) were from foxes. No difference in proportions of coccidian DNA-positive fecal samples was identified among canid species. Environmental temperature and fecal freshness were associated with coccidian DNA detection. Land use type, relative canid density, and cattle density were not associated with the prevalence of coccidian DNA-positive samples.

CONCLUSIONS AND CLINICAL RELEVANCE The low prevalence of coccidia shed in wild canid feces in this study, including the estimated 0% environmental prevalence of N caninum, suggested that the role of the oocyst environmental phase in coccidia transmission to ruminants is likely minor in rural southeastern Ohio.

Supplementary Materials

    • Supplementary Table S1 (PDF 166 kb)

Contributor Notes

Dr. Moreno-Torres’ present address is Center for Epidemiology and Animal Health, Monitoring and Modeling, APHIS, USDA, 2150 Centre Ave, Fort Collins, CO 80526.

Address correspondence to Dr. Garabed (garabed.l@osu.edu).