Advertisement

Parasitology Research

, Volume 115, Issue 5, pp 1767–1772 | Cite as

Toxoplasmosis in geese and detection of two new atypical Toxoplasma gondii strains from naturally infected Canada geese (Branta canadensis)

  • Shiv Kumar Verma
  • Rafael Calero-Bernal
  • Camila K. Cerqueira-Cézar
  • Oliver C. H. Kwok
  • Mike Dudley
  • Tiantian Jiang
  • Chunlei Su
  • Dolores Hill
  • Jitender P. Dubey
Original Paper

Abstract

Wild birds are important in the epidemiology of toxoplasmosis because they can serve as reservoir hosts, and vectors of zoonotic pathogens including Toxoplasma gondii. Canada goose (Branta canadensis) is the most widespread geese in North America. Little is known concerning T. gondii infection in both migratory, and local resident populations of Canada geese. Here, we evaluated the seroprevalence, isolation, and genetic characterization of viable T. gondii isolates from a migratory population of Canada geese. Antibodies against T. gondii were detected in 12 of 169 Canada geese using the modified agglutination test (MAT, cutoff 1:25). The hearts of 12 seropositive geese were bioassayed in mice for isolation of T. gondii. Viable parasites were isolated from eight. One isolate was obtained from a seropositive goose by both bioassays in mice, and in a cat; the cat fed infected heart excreted T. gondii oocysts. Additionally, one isolate was obtained from a pool of four seronegative (<1:25) geese by bioassay in a cat. The T. gondii isolates were further propagated in cell culture, and DNA extracted from cell culture-derived tachyzoites were characterized using 10 polymerase chain reaction-restriction fragment length polymorphism (PCR-RFLP) genetic markers (SAG1, 5′ and 3′SAG2, alt.SAG2, SAG3, BTUB, GRA6, c22-8, c29-2, L358, PK1, and Apico). The results revealed five different genotypes. ToxoDB PCR-RFLP genotype #1 (type II) in one isolate, genotype #2 (type III) in four isolates, genotype #4 in two isolates, and two new genotypes (ToxoDB PCR-RFLP genotype #266 in one isolate and #267 in one isolate) were identified. These results indicate genetic diversity of T. gondii strains in the Canada geese, and this migratory bird might provide a mechanism of T. gondii transmission at great distances from where an infection was acquired.

Keywords

Canada geese Toxoplasma gondii Bioassay Genotype 

Notes

Acknowledgments

We would like to thank Jamie Houchens, Stewart Kerr, Jason Evans, and Clifton Thomas for their help in procuring the geese.

Compliance with ethical standards

All investigations reported here were approved by the institutional animal care and use protocol committee of the US Department of Agriculture.

References

  1. Bártová E, Sedlák K, Literák I (2009) Serologic survey for toxoplasmosis in domestic birds from the Czech Republic. Avian Pathol 38:317–320CrossRefPubMedGoogle Scholar
  2. Dolbeer RA, Seubert JL, Begier MJ (2014) Population trends of resident and migratory Canada geese in relation to strikes with civil aircraft. Hum-Wildl Interact 8:88–99Google Scholar
  3. Dubey JP (1995) Duration of immunity to shedding of Toxoplasma gondii oocysts by cats. J Parasitol 81:410–415CrossRefPubMedGoogle Scholar
  4. Dubey JP (2010) Toxoplasmosis of animals and humans, 2nd edn. CRC, Boca Raton, pp 1–313Google Scholar
  5. Dubey JP, Desmonts G (1987) Serological responses of equids fed Toxoplasma gondii oocysts. Equine Vet J 19:337–339CrossRefPubMedGoogle Scholar
  6. Dubey JP, Garner MM, Willette MM, Batey KL, Gardiner CH (2001) Disseminated toxoplasmosis in magpie geese (Anseranas semipalmata) with large numbers of tissue cysts in livers. J Parasitol 87:219–223CrossRefPubMedGoogle Scholar
  7. Dubey JP, Parnell PG, Sreekumar C, Vianna MCB, de Young RW, Dahl E, Lehmann T (2004) Biologic and molecular characteristics of Toxoplasma gondii isolates from striped skunk (Mephitis mephitis), Canada goose (Branta canadensis), black-winged lory (Eos cyanogenia), and cats (Felis catus). J Parasitol 90:1171–1174CrossRefPubMedGoogle Scholar
  8. Dubey JP, Webb DM, Sundar N, Velmurugan GV, Bandini LA, Kwok OCH, Su C (2007) Endemic avian toxoplasmosis on a farm in Illinois: clinical disease, diagnosis, biologic and genetic characteristics of Toxoplasma gondii isolates from chickens (Gallus domesticus), and a goose (Anser anser). Vet Parasitol 148:207–212CrossRefPubMedGoogle Scholar
  9. Dubey JP, Van Why K, Verma SK, Choudhary S, Kwok OCH, Khan A, Behinke MS, Sibley LD, Ferreira LR, Oliveira S, Weaver M, Stewart R, Su C (2014) Genotyping Toxoplasma gondii from wildlife in Pennsylvania and identification of natural recombinants virulent to mice. Vet Parasitol 200:74–84CrossRefPubMedPubMedCentralGoogle Scholar
  10. Dubey JP, Laurin E, Kwowk OC (2016) Validation of the modified agglutination test for the detection of Toxoplasma gondii in free-range chickens by using cat and mouse bioassay. Parasitology. doi: 10.1017/S0031182015001316
  11. Elmore SA, Huyvaert KP, Bailey LL, Milhous J, Alisauskas RT, Gajadhar AA, Jenkins EJ (2014) Toxoplasma gondii exposure in arctic-nesting geese: a multi-state occupancy framework and comparison of serological assays. Int J Parasitol Parasites Wildl 3:147–153CrossRefPubMedPubMedCentralGoogle Scholar
  12. Elmore SA, Samelius G, Fernando C, Alisauskas RT, Jenkins EJ (2015) Evidence for Toxoplasma gondii in migratory vs. nonmigratory herbivores in a terrestrial arctic ecosystem. Can J Zool 93:671–675CrossRefGoogle Scholar
  13. Literák I, Hejlicek K (1993) Incidence of Toxoplasma gondii in populations of domestic birds in the Czech Republic. Avian Pathol 22:275–281CrossRefPubMedGoogle Scholar
  14. Maksimov P, Buschtöns S, Herrmann DC, Conraths FJ, Görlich K, Tenter AM, Dubey JP, Nagel-Kohl U, Thoms B, Bötcher L, Kühne M, Schares G (2011) Serological survey and risk factors for Toxoplasma gondii in domestic ducks and geese in Lower Saxony, Germany. Vet Parasitol 182:140–149CrossRefPubMedGoogle Scholar
  15. Murao T, Omata Y, Kano R, Murata S, Okada T, Konnai S, Asakawa M, Ohashi K, Onuma M (2008) Serological survey of Toxoplasma gondii in wild waterfowl in Chukotka, Kamchatka, Russia and Hokkaido, Japan. J Parasitol 94:830–833CrossRefPubMedGoogle Scholar
  16. Prestrud KW, Åsbakk K, Fuglei E, Mørk T, Stien A, Ropstad E, Tryland M, Gabrielsen GW, Lydersen C, Kovacs KM, Loonen MJJE, Sagerup K, Oksanen A (2007) Serosurvey for Toxoplasma gondii in arctic foxes and possible sources of infection in the high Arctic of Svalbard. Vet Parasitol 150:6–12CrossRefPubMedGoogle Scholar
  17. Rong G, Zhou HL, Hou GY, Zhao JM, Xu TS, Guan S (2014) Seroprevalence, risk factors and genotyping of Toxoplasma gondii in domestic geese (Anser domestica) in tropical China. Parasit Vectors 7:459PubMedPubMedCentralGoogle Scholar
  18. Sandström CAM, Buma AGJ, Hoye BJ, Prop J, van der Jeugd H, Voslamber B, Madsen J, Loonen MJJE (2013) Latitudinal variability in the seroprevalence of antibodies against Toxoplasma gondii in non-migrant and Arctic migratory geese. Vet Parasitol 194:9–15CrossRefPubMedGoogle Scholar
  19. Shwab EK, Zhu XQ, Majumdar D, Pena HFJ, Gennari SM, Dubey JP, Su C (2014) Geographical patterns of Toxoplasma gondii genetic diversity revealed by multilocus PCR-RFLP genotyping. Parasitology 141:453–461CrossRefPubMedGoogle Scholar
  20. Sibley LD, Ajioka JW (2008) Population structure of Toxoplasma gondii: clonal expansion driven by infrequent recombination and selective sweeps. Ann Rev Microbiol 62:329–351CrossRefGoogle Scholar
  21. Sroka J (2001) Seroepidemiology of toxoplasmosis in the Lublin region. Ann Agric Environ Med 8:25–31PubMedGoogle Scholar
  22. Su C, Shwab EK, Zhou P, Zhu XQ, Dubey JP (2010) Moving towards an integrated approach to molecular detection and identification of Toxoplasma gondii. Parasitology 137:1–11CrossRefPubMedGoogle Scholar
  23. Work TM, Massey JG, Lindsay DS, Dubey JP (2002) Toxoplasmosis in three species of native and introduced Hawaiian birds. J Parasitol 88:1040–1042CrossRefPubMedGoogle Scholar
  24. Work TM, Dagenais J, Rameyer R, Breeden R (2015) Mortality patterns in endangered hawaiian geese (nene; Branta sandvicensis). J Wildl Dis 51:688–695CrossRefPubMedGoogle Scholar
  25. Work TM, Verma SK, Su C, Medeiros J, Kaiakapu T, Dubey JP (2016) Serology and genetics of Toxoplasma gondii in endangered Hawaiian (Nene) geese (Branta sandvicensis). J Wildlife Dis (in press)Google Scholar
  26. Yan C, Yue CL, Zhang H, Yin CC, He Y, Yuan ZG, Lin RQ, Song HQ, Zhang KX, Zhu XQ (2011) Serological survey of Toxoplasma gondii infection in the domestic goose (Anser domestica) in southern China. Zoonoses and Public Health 58:299–302CrossRefPubMedGoogle Scholar
  27. Yang N, Mu MY, Li HK, Long M, He JB (2012) Seroprevalence of Toxoplasma gondii infection in slaughtered chickens, ducks, and geese in Shenyang, northeastern China. Parasit Vectors 5:237–240CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg (outside the USA) 2016

Authors and Affiliations

  • Shiv Kumar Verma
    • 1
  • Rafael Calero-Bernal
    • 1
  • Camila K. Cerqueira-Cézar
    • 1
  • Oliver C. H. Kwok
    • 1
  • Mike Dudley
    • 2
  • Tiantian Jiang
    • 3
  • Chunlei Su
    • 3
  • Dolores Hill
    • 1
  • Jitender P. Dubey
    • 1
  1. 1.United States Department of Agriculture, Agricultural Research ServiceBeltsville Agricultural Research Center, Animal Parasitic Diseases LaboratoryBeltsvilleUSA
  2. 2.United States Department of Agriculture, Agricultural Research ServiceBeltsville Agricultural Research Center, Farm ServicesBeltsvilleUSA
  3. 3.Department of MicrobiologyUniversity of TennesseeKnoxvilleUSA

Personalised recommendations