Tropical Animal Health and Production

, Volume 46, Issue 6, pp 1051–1058 | Cite as

Detection of enteric pathogens in Turkey flocks affected with severe enteritis, in Brazil

  • Joelma Moura-Alvarez
  • Luis F. N. Nuñez
  • Claudete S. Astolfi-Ferreira
  • Terezinha Knöbl
  • Jorge L. Chacón
  • Andrea M. Moreno
  • Richard C. Jones
  • Antonio J. Piantino Ferreira
Regular Articles
First Online:
Accepted:

Abstract

Twenty-two flocks of turkeys affected by enteric problems, with ages between 10 and 104 days and located in the Southern region of Brazil, were surveyed for turkey by PCR for turkey astrovirus type 2 (TAstV-2), turkey coronavirus (TCoV), hemorrhagic enteritis virus (HEV), rotavirus, reovirus, Salmonella spp., and Lawsonia intracellularis (Li) infections. Eleven profiles of pathogen combination were observed. The most frequently encountered pathogen combinations were TCoV-Li, followed by TCoV-TAstV-2-Li, TCoV-TastV-2. Only TCoV was detected as the sole pathogen in three flocks. Eight and 19 flocks of the 22 were positive for TAstV-2 and TCoV, respectively. Six were positive for Salmonella spp. and L. intracellularis was detected in 12 turkey flocks. Reovirus and HEV were not detected in this survey. These results throw new light on the multiple etiology of enteritis in turkeys. The implications of these findings and their correlation with the clinical signs are comprehensively discussed, illustrating the complexity of the enteric diseases.

Keywords

Enteric virus Bacteria Enteritis Turkey 
This is a preview of subscription content, log in to check access.

Notes

Acknowledgments

This work was supported by grants from FAPESP (Fundação de Amparo à Pesquisa do Estado de São Paulo—Grant No. 2006/59332-9), CAPES (Coordenação de Aperfeiçoamento de Pessoal de Nível Superior), and CNPq (Conselho Nacional de Desenvolvimento Científico e Tecnológico). A. J. P. Ferreira is recipient of CNPq fellowships.

Conflict of interest

The authors declare that there is no any conflict of interest regarding the publication of this paper.

References

  1. Barnes, H.J. and Guy, J.S., 2003. Poult enteritis-mortality syndrome. In: Saif, Y.M., Barnes, H.J., Glisson, J.R., Fadly, A.M., McDougald, L.R. and Swayne, D.E. (eds), Diseases of Poultry. 11st Edition. (Iowa State University Press, Ames), 320--326Google Scholar
  2. Behling-Kelly, E., Schultz-Cherry, S., Koci, M., Kelley, L., Larsen, D. and Brown, C., 2002. Localization of astrovirus in experimentally infected turkeys as determined by In Situ hybridization. Veterinary Pathology, 39, 595–598PubMedCrossRefGoogle Scholar
  3. Bezerra, D.A., da Silva, R.R., Kaiano, J.H., Silvestre, R.V., de Souza Oliveira, D., Linhares, A.C., Gabbay, Y.B. and Mascarenhas, J.D., 2012. Detection of avian group D rotavirus using the polymerase chain reaction for the VP6 gene. Journal of Virological Methods, 185, 189–192PubMedCrossRefGoogle Scholar
  4. Boom, R., Sol, C.J.A., Salimans, M.M., Jansen, C.L., Dillen, P.M.E.W. and Noordaa, J.V.D., 1990. Rapid and simple method for purification of nucleic acids. Journal of Clinical Microbiology, 28, 495–503PubMedCentralPubMedGoogle Scholar
  5. Bunger, A.N.D., Chacón, J.L., Jones, R.C. and Ferreira, A.J.P., 2009. Detection and molecular characterization of gene 3 and 5 of turkey coronavirus from turkeys with severe enteritis in Brazil. Avian Diseases, 53, 356–362PubMedCrossRefGoogle Scholar
  6. Cavanagh, D., Mawditt, K., Welchman, D.B., Britton, P. and Gough, R.E., 2002. Coronaviruses from pheasants (Phasianus colchicus) are genetically closely related to coronaviruses of domestic fowl (infectious bronchitis virus) and turkeys. Avian Pathology, 31, 81–93PubMedCrossRefGoogle Scholar
  7. Cooper, D.M., Swanson, D.L., Barns, S.M. and Gebhart, C.J., 1997. Comparison of the 16S Ribosomal DNA Sequences from the Intracellular Agents of Proliferative Enteritis in a Hamster, Deer, and Ostrich with the Sequence of a Porcine Isolate of Lawsonia intracellularis. International Journal of Systematic Bacteriology, 47, 635–639PubMedCrossRefGoogle Scholar
  8. Day, J.M., Spackman, E. and Pantin-Jackwood, M., 2007. A multiplex RT-PCR test for the differential identification of turkey astrovirus type 1, turkey astrovirus type 2, chicken astrovirus, avian nephritis virus, and rotavirus. Avian Diseases, 51, 681–684PubMedCrossRefGoogle Scholar
  9. Dea, S., Marsolais, G., Beaubien, J. and Ruppaner, R., 1986. Coronavirus associated with outbreaks of transmissible enteritis of turkeys in Quebec: Hemagglutination properties and cell cultivation. Avian Diseases, 30, 319–326PubMedCrossRefGoogle Scholar
  10. Estes, M.K., 1990. Rotaviruses and their replication. In: Fields, B.N. and Knipe, D.M. (eds), Fields Virology, 2nd Edition. (Raven Press, New York), 1329–1352Google Scholar
  11. Gast, R.K., 2003. Salmonella infections. In: Saif, Y.M., Barnes, H.J., Glisson, J.R., Fadly, A.M., McDougald, L.R. and Swayne, D.E. (eds), Diseases of Poultry, 11st Edition. (Iowa State University Press, Ames), 567–568Google Scholar
  12. Gouvea, V., Santos, N. and Timenetsky, M.C., 1994. VP4 typing of bovine and porcine group A rotaviruses by PCR. Journal of Clinical Microbiology, 32, 1333–1337PubMedCentralPubMedGoogle Scholar
  13. Grimont, P.A.D. and Weill, F.X., 2007. Antigenic formulae of the Salmonella serovars, 9th ed. WHO Collaborating Centre for Reference and Research on Salmonella. Institute Pasteur, Paris, 166Google Scholar
  14. Guy, J.S., Levy, M.G., Ley, D.H., Barnes, H.J. and Gerig, T.M., 1987. Experimental reproduction of enteritis in bobwhite quail (Colinus virginianus) with Cryptosporidium and reovirus. Avian Diseases, 31, 713–722PubMedCrossRefGoogle Scholar
  15. Heggen-Peay, C.L., Qureshi, M.A., Edens, F.W., Sherry, B., Wakenell, P.S., O’Connell, P.H. and Schat, K.A., 2002. Isolation of Reovirus from poult enteritis and mortality syndrome and its pathogenicity in turkey poults. Avian Diseases, 46, 32–47PubMedCrossRefGoogle Scholar
  16. Herring, A.J., Inglis, N.F., Ojeh, C.K., Snodgrass, D.R. and Menzies, J.D., 1982. Rapid diagnosis of rotavirus infection by direct detection of viral nucleic acid in silver-stained poliacrylamide gels. Journal of Clinical Microbiology, 16, 473–477PubMedCentralPubMedGoogle Scholar
  17. Hess, M., Raue, R. and Hafez, H.M., 1999. PCR for specific detection of haemorrhagic enteritis virus of turkeys, an avian adenovirus. Journal of Virological Methods, 81, 199–203PubMedCrossRefGoogle Scholar
  18. Ismail, M.M., Tang, Y. and Saif, Y.M., 2003. Pathogenicity of turkey coronavirus in turkeys and chickens. Avian Diseases, 47, 515–522PubMedCrossRefGoogle Scholar
  19. Jacobson, M., Fellström, C. and Jensen-Waern, M., 2010. Porcine proliferative enteropathy: An important disease with questions remaining to be solved. Veterinary Journal, 184, 264–268CrossRefGoogle Scholar
  20. Jindal, N., Patnayak, D.P., Ziegler, A.F., Lago, A. and Goyal, G.M., 2009. A retrospective study on poult enteritis Syndrome in Minnesota. Avian Diseases, 53, 268–275PubMedCrossRefGoogle Scholar
  21. Jindal, N., Chander, Y., Patnayak, D.P., Mor, S.K., Ziegler, A.F. and Goyal, S.M., 2012. A multiplex RT-PCR for the detection of astrovirus, rotavirus, and reovirus in turkeys. Avian Diseases, 56, 592–596PubMedCrossRefGoogle Scholar
  22. Jones, G.F., Ward, G.E., Murtaugh, M.P., Lin, G. and Gebhart, C.J., 1993. Enhanced detection of intracellular organism of swine proliferative enteritis, ileal symbiont intracellularis, in feces by polymerase chain reaction. Journal of Clinical Microbiology, 31, 2611–2615PubMedCentralPubMedGoogle Scholar
  23. Koci, M. and Schultz-Cherry, S., 2002. Avian astroviruses. Avian Pathology, 31, 213–227PubMedCrossRefGoogle Scholar
  24. Koci, M., Seal, B. and Schultz-Cherry, S., 2000. Molecular characterization of an avian astrovirus. Journal of Virology, 74, 6173–6177PubMedCentralPubMedCrossRefGoogle Scholar
  25. McNulty, M.S., 2003. Rotavirus infections. In: Saif, Y.M., Barnes, H.J., Glisson, J.R., Fadly, A.M., McDougald, L.R. and Swayne, D.E. (eds), Diseases of Poultry, 11st Edition. (Iowa State University Press, Ames), 308–320Google Scholar
  26. Mor, S.K., Sharafeldin, T.A., Abin, M., Kromm, M., Porter, R.E., Goyal, S.M. and Patnayak, D.P., 2013. The occurrence of enteric viruses in Light Turkey Syndrome. Avian Pathology, 42, 497–501PubMedCrossRefGoogle Scholar
  27. Nagaraja, K.V. and Pomeroy, B.S., 1997. Coronaviral enteritis of turkeys (bluecomb disease). In: Calnek, B.W., Barnes, H.J., Beard, C.W., McDougald, L.R. and Saif, Y.M. (eds), Diseases of Poultry, 10th Edition. (Iowa State University Press, Ames). 686–692Google Scholar
  28. Naqi, S.A., Hall, C.F. and Lewis, D.H., 1971. The intestinal microflora of turkeys: comparison of apparently healthy and bluecomb-infected turkey poults. Avian Diseases, 15, 14–21PubMedCrossRefGoogle Scholar
  29. Pantin-Jackwood, M.J., Spackman, E. and Woolcock, P.R., 2006. Molecular characterization and typing of chicken and turkey Astrovirus circulating in the United States: implications for diagnostics. Avian Diseases, 50, 397–404PubMedCrossRefGoogle Scholar
  30. Pantin-Jackwood, M.J., Spackman, E., Day, J.M. and Rives, D., 2007. Periodic monitoring of commercial turkeys for enteric indicates continuous presence of astrovirus and rotavirus on the farms. Avian Diseases, 51, 674–680PubMedCrossRefGoogle Scholar
  31. Pantin-Jackwood, M.J., Day, J.M., Jackwood, M.W. and Spackman, E., 2008. Enteric viruses detected by molecular methods in commercial chicken and turkey flocks in the United States between 2005 and 2006. Avian Diseases, 52, 235–244PubMedCrossRefGoogle Scholar
  32. Pierson, F.W. and Domermuth, C.H., 1997. Hemorrhagic enteritis, marble spleen disease, and related infections. In: Calnek, B.W., Barnes, H.J., Beard, C.W., McDougald, L.R. and Saif, Y.M. (eds), Diseases of Poultry, 10th Edition. (Iowa State University Press, Ames), 624–633Google Scholar
  33. Pierson, F.W. and Fitzgerald, S.D., 2008. Hemorrhagic enteritis and related infections. In: Saif, Y.M., Fadly, A.M., Glisson, J.R., McDougald, L.R., Nolan, L.K. and Swayne, D.E. (eds), Diseases of Poultry, 12th Edition. (Iowa State University Press, Ames), 276–286Google Scholar
  34. Qureshi, M.A., Yu, M. and Saif, Y.M., 2000. A novel “small round virus” inducing poult enteritis and mortality syndrome and associated immune alterations. Avian Diseases, 44, 275–283PubMedCrossRefGoogle Scholar
  35. Reynolds, D.L. and Saif, Y.M., 1986. Astrovirus: a cause of an enteric disease in turkey poults. Avian Diseases, 30, 728–735PubMedCrossRefGoogle Scholar
  36. Reynolds, D.L. and Schultz-Cherry, S.L., 2003. Astrovirus infections. Saif, Y.M., Barnes, H.J., Glisson, J.R., Fadly, A.M., McDougald, L.R. and Swayne, D.E. (eds), Diseases of Poultry, 11st Edition. (Iowa State University Press, Ames), 320--326Google Scholar
  37. Reynolds, D.L., Saif, Y.M. and Theil, K.W., 1987a. A survey of enteric viruses of turkey poults. Avian Diseases, 31, 89–98PubMedCrossRefGoogle Scholar
  38. Reynolds, D.L., Saif, Y.M. and Theil, K.W., 1987b. Enteric viral infections of turkey poults: incidence of infection. Avian Diseases, 31, 272–276PubMedCrossRefGoogle Scholar
  39. Rosenberger, J.K., Fries, P.A., Cloud, S.S. and Wilson, R.A., 1986. In vitro and in vivo characterization of Escherichia coli. II. Factors associated with pathogenicity. Avian Diseases, 29, 1094–1107CrossRefGoogle Scholar
  40. Ruff, M.D. and Rosenberger, J.K., 1985. Concurrent infections with reoviruses and coccidian in broilers. Avian Diseases, 29, 465–478PubMedCrossRefGoogle Scholar
  41. Saif, L.J., Saif, Y.M. and Theil, K.W., 1985. Enteric viruses in diarrheic turkey poults. Avian Diseases, 29, 798–811PubMedCrossRefGoogle Scholar
  42. Silva, S.E.L., Bonetti, A.M., Petrocelli, A., Ferrari, H.F., Luvizotto, M.C.R. and Cardoso, T.C. 2009. Epidemiological aspects of Astrovirus and Coronavirus in poults in the south eastern region of Brazil. Brazilian Journal of Microbiology, 40, 248–253PubMedCentralPubMedCrossRefGoogle Scholar
  43. Swamy, S.C., Barnhart, H.M., Lee, M.D. and Dreesen, D.W., 1996. Virulence Determinants invA and spvC in Salmonellae Isolated from Poultry Products, Wastewater, and Human Sources. Applied in Environmental Microbiology, 62, 3768–3771Google Scholar
  44. Villarreal, L.Y.B., Assayag, M.S., Brandão, P.E., Chacón, J.L., Bunger, A.N.D., Astolfi-Ferreira, C.S., Gomes, C.R., Jones, R.C. and Ferreira, A.J.P., 2006. Identification of turkey astrovirus and turkey coronavirus in an outbreak of poult enteritis and mortality syndrome. Brazilian Journal of Poultry Science, 8, 131–135Google Scholar
  45. White, R.G., Mebus, C.A. and Twiehaus, M., 1970. Incidence of herds infected with a Neonatal Calf Diarrhea Virus (NCDV). Veterinary Medicine and Small Animal Clinic, 65, 487–490Google Scholar
  46. Xu, L., Harbour, D. and McCrae, M.A., 1990. The application of polymerase chain reaction to the detection of rotaviruses in faeces. Journal of Virological Methods, 27, 29–37PubMedCrossRefGoogle Scholar
  47. Yu, M., Tang, Y., Guo, M., Zhang, Q. and Saif, Y.M., 2000. Characterization of a small round virus associated with the poult enteritis and mortality syndrome. Avian Diseases, 44, 600–610PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2014

Authors and Affiliations

  • Joelma Moura-Alvarez
    • 1
  • Luis F. N. Nuñez
    • 1
  • Claudete S. Astolfi-Ferreira
    • 1
  • Terezinha Knöbl
    • 1
  • Jorge L. Chacón
    • 1
  • Andrea M. Moreno
    • 2
  • Richard C. Jones
    • 3
  • Antonio J. Piantino Ferreira
    • 1
  1. 1.Department of Pathology, School of Veterinary MedicineUniversity of São PauloSão PauloBrazil
  2. 2.Department of Preventive Veterinary Medicine and Animal Health, School of Veterinary MedicineUniversity of São PauloSão PauloBrazil
  3. 3.Department of Infection Biology, Institute of Global HealthUniversity of Liverpool, Leahurst CampusLiverpoolUK

Personalised recommendations