Pathogenicity of an emergent, ovine abortifacient Campylobacter jejuni clone orally inoculated into pregnant guinea pigs

Eric R. Burrough Department of Veterinary Pathology, College of Veterinary Medicine, Iowa State University, Ames, IA 50011.

Search for other papers by Eric R. Burrough in
Current site
Google Scholar
PubMed
Close
 DVM
,
Orhan Sahin Department of Veterinary Microbiology and Preventive Medicine, College of Veterinary Medicine, Iowa State University, Ames, IA 50011.

Search for other papers by Orhan Sahin in
Current site
Google Scholar
PubMed
Close
 DVM, PhD
,
Paul J. Plummer Department of Veterinary Microbiology and Preventive Medicine, College of Veterinary Medicine, Iowa State University, Ames, IA 50011.

Search for other papers by Paul J. Plummer in
Current site
Google Scholar
PubMed
Close
 DVM
,
Qijing Zhang Department of Veterinary Microbiology and Preventive Medicine, College of Veterinary Medicine, Iowa State University, Ames, IA 50011.

Search for other papers by Qijing Zhang in
Current site
Google Scholar
PubMed
Close
 BVSc, PhD
, and
Michael J. Yaeger Department of Veterinary Pathology, College of Veterinary Medicine, Iowa State University, Ames, IA 50011.

Search for other papers by Michael J. Yaeger in
Current site
Google Scholar
PubMed
Close
 DVM, PhD

Abstract

Objective—To compare pathogenicity of an emergent abortifacient Campylobacter jejuni (IA 3902) with that of reference strains after oral inoculation in pregnant guinea pigs.

Animals—58 pregnant guinea pigs.

Procedures—12 animals were challenged IP with C jejuni IA 3902 along with 5 sham-inoculated control animals to confirm abortifacient potential. Once pathogenicity was confirmed, challenge via oral inoculation was performed whereby 12 guinea pigs received IA 3902, 12 received C jejuni isolated from ovine feces (OF48), 12 received a fully sequenced human C jejuni isolate (NCTC 11168), and 5 were sham-inoculated control animals. After abortions, guinea pigs were euthanized; samples were collected for microbial culture, histologic examination, and immunohistochemical analysis.

ResultsC jejuni IA 3902 induced abortion in all 12 animals following IP inoculation and 6 of 10 animals challenged orally. All 3 isolates colonized the intestines after oral inoculation, but only IA 3902 induced abortion. Evidence of infection existed for both IA 3902 and NCTC 11168; however, C jejuni was only recovered from fetoplacental units of animals inoculated with IA 3902. Immunohistochemical analysis localized C jejuni IA 3902 infection to subplacental trophoblasts, perivascular tissues, and phagocytes in the placental transitional zone.

Conclusions and Clinical Relevance—This study revealed that C jejuni IA 3902 was a unique, highly abortifacient strain with the ability to colonize the intestines, induce systemic infection, and cause abortion because of its affinity for the fetoplacental unit. Guinea pigs could be effectively used in the study of septic abortion after oral inoculation with this Campylobacter strain.

Abstract

Objective—To compare pathogenicity of an emergent abortifacient Campylobacter jejuni (IA 3902) with that of reference strains after oral inoculation in pregnant guinea pigs.

Animals—58 pregnant guinea pigs.

Procedures—12 animals were challenged IP with C jejuni IA 3902 along with 5 sham-inoculated control animals to confirm abortifacient potential. Once pathogenicity was confirmed, challenge via oral inoculation was performed whereby 12 guinea pigs received IA 3902, 12 received C jejuni isolated from ovine feces (OF48), 12 received a fully sequenced human C jejuni isolate (NCTC 11168), and 5 were sham-inoculated control animals. After abortions, guinea pigs were euthanized; samples were collected for microbial culture, histologic examination, and immunohistochemical analysis.

ResultsC jejuni IA 3902 induced abortion in all 12 animals following IP inoculation and 6 of 10 animals challenged orally. All 3 isolates colonized the intestines after oral inoculation, but only IA 3902 induced abortion. Evidence of infection existed for both IA 3902 and NCTC 11168; however, C jejuni was only recovered from fetoplacental units of animals inoculated with IA 3902. Immunohistochemical analysis localized C jejuni IA 3902 infection to subplacental trophoblasts, perivascular tissues, and phagocytes in the placental transitional zone.

Conclusions and Clinical Relevance—This study revealed that C jejuni IA 3902 was a unique, highly abortifacient strain with the ability to colonize the intestines, induce systemic infection, and cause abortion because of its affinity for the fetoplacental unit. Guinea pigs could be effectively used in the study of septic abortion after oral inoculation with this Campylobacter strain.

Contributor Notes

Supported by a grant from the Iowa Livestock Health Advisory Council.

The authors thank Deborah Moore for assistance with the immunohistochemical analysis.

Address correspondence to Dr. Yaeger (myaeger@iastate.edu).
  • 1.

    Skirrow MB. Diseases due to Campylobacter, Helicobacter and related bacteria. J Comp Pathol 1994;111:113149.

  • 2.

    USDA. Part II: reference of sheep health in the United States. Fort Collins, Colo: USDA, APHIS, Veterinary Services, National Animal Health Monitoring System, 2001.

    • Search Google Scholar
    • Export Citation
  • 3.

    Kirkbride CA. Diagnoses in 1,784 ovine abortions and stillbirths. J Vet Diagn Invest 1993;5:398402.

  • 4.

    Diker KS, Istanbulluoglu E. Ovine abortion associated with Campylobacter jejuni. Vet Rec 1986;118:307.

  • 5.

    Diker KS, Sahal M, Aydin N. Ovine abortion associated with Campylobacter coli. Vet Rec 1988;122:87.

  • 6.

    Varga J, Mézes B, Fodor L, et al. Serogroups of Campylobacter fetus and Campylobacter jejuni isolated in cases of ovine abortion. Zentralbl Veterinarmed B 1990;37:148152.

    • Search Google Scholar
    • Export Citation
  • 7.

    Delong WJ, Jaworski MD, Ward AC. Antigenic and restriction enzyme analysis of Campylobacter spp associated with abortion in sheep. Am J Vet Res 1996;57:163167.

    • Search Google Scholar
    • Export Citation
  • 8.

    Sahin O, Plummer PJ, Jordan DM, et al. Emergence of a tetracycline-resistant Campylobacter jejuni clone associated with outbreaks of ovine abortion in the United States. J Clin Microbiol 2008;46:16631671.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 9.

    Mannering SA, Marchant RM, Middelberg A, et al. Pulsed-field gel electrophoresis typing of Campylobacter fetus subsp. fetus from sheep abortions in the Hawke's Bay region of New Zealand. N Z Vet J 2003;51:3337.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 10.

    Mannering SA, West DM, Fenwick SG, et al. Pulsed-field gel electrophoresis typing of Campylobacter fetus subsp. fetus isolated from sheep abortions in New Zealand. N Z Vet J 2004;52:358363.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 11.

    Mannering SA, West DM, Fenwick SG, et al. Pulsed-field gel electrophoresis of Campylobacter jejuni heep abortion isolates. Vet Microbiol 2006;115:237242.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 12.

    SultanDosa AB, Bryner JH, Foley JW. Pathogenicity of Campylobacter jejuni and Campylobacter coli strains in the pregnant guinea pig model. Am J Vet Res 1983;44:21752178.

    • Search Google Scholar
    • Export Citation
  • 13.

    Taylor DE, Bryner JH. Plasmid content and pathogenicity of Campylobacter jejuni and Campylobacter coli strains in the pregnant guinea pig model. Am J Vet Res 1984;45:22012202.

    • Search Google Scholar
    • Export Citation
  • 14.

    Bryner JH, Foley JW, Hubbert WT, et al. Pregnant guinea pig model for testing efficacy of Campylobacter fetus vaccines. Am J Vet Res 1978;39:119121.

    • Search Google Scholar
    • Export Citation
  • 15.

    Bryner JH, Foley JW, Thompson K. Comparative efficacy of ten commercial Campylobacter fetus vaccines in the pregnant guinea pig: challenge with Campylobacter fetus serotype A. Am J Vet Res 1979;40:433435.

    • Search Google Scholar
    • Export Citation
  • 16.

    Bryner JH, Firehammer BD, Wesley IV. Vaccination of pregnant guinea pigs with Campylobacter fetus: effects of antigen dose, Campylobacter strain, and adjuvant type. Am J Vet Res 1988;49:449455.

    • Search Google Scholar
    • Export Citation
  • 17.

    Coid CR, O'Sullivan AM, Doré CJ. Variations in the virulence, for pregnant guinea pigs, of campylobacters isolated from man. J Med Microbiol 1987;23:187189.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 18.

    Parkhill J, Wren BW, Mungall K, et al. The genome sequence of the food-borne pathogen Campylobacter jejuni reveals hypervariable sequences. Nature 2000;403:665668.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 19.

    Bell JA, Manning DD. Reproductive failure in mink and ferrets after intravenous or oral inoculation of Campylobacter jejuni. Can J Vet Res 1990;54:432437.

    • Search Google Scholar
    • Export Citation
  • 20.

    Zhang Q, Meitzler JC, Huang S, et al. Sequence polymorphism, predicted secondary structures, and surface-exposed conformational epitopes of Campylobacter major outer membrane protein. Infect Immun 2000;68:56795689.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 21.

    Coid CR, Fox H. Short review: campylobacters as placental pathogens. Placenta 1983;4:295305.

  • 22.

    Smith JL. Campylobacter jejuni infection during pregnancy: long-term consequences of associated bacteremia, Guillain-Barré syndrome, and reactive arthritist. J Food Prot 2002;65:696708.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 23.

    Simor AE, Karmali MA, Jadavji T, et al. Abortion and perinatal sepsis associated with campylobacter infection. Rev Infect Dis 1986;8:397402.

  • 24.

    Ertaú HB, Özbey G, Kiliç A, et al. Isolation of Campylobacter jejuni and Campylobacter coli from the gall bladder samples of sheep and identification by polymerase chain reaction. J Vet Med B Infect Dis Vet Public Health 2003;50:294297.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 25.

    Açik MN, Çetinkaya B. Heterogeneity of Campylobacter jejuni and Campylobacter coli strains from healthy sheep. Vet Microbiol 2006;115:370375.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 26.

    Poly F, Guerry P. Pathogenesis of Campylobacter. Curr Opin Gastroenterol 2008;24:2731.

  • 27.

    Young KT, Davis LM, Dirita VJ. Campylobacter jejuni: molecular biology and pathogenesis. Nat Rev Microbiol 2007;5:665679.

  • 28.

    Ladrón de Guevara C, Gonzalez J, Peña P. Bacteraemia caused by Campylobacter spp. J Clin Pathol 1994;47:174175.

  • 29.

    Walker RI, Caldwell MB, Lee EC, et al. Pathophysiology of Campylobacter enteritis. Microbiol Rev 1986;50:8194.

  • 30.

    Blaser MJ, Perez GP, Smith PF, et al. Extraintestinal Campylobacter jejuni and Campylobacter coli infections: host factors and strain characteristics. J Infect Dis 1986;153:552559.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 31.

    Skirrow MB, Jones DM, Sutcliffe E, et al. Campylobacter bacteraemia in England and Wales, 1981–91. Epidemiol Infect 1993;110:567573.

  • 32.

    Korman TM, Varley CC, Spelman DW. Acute hepatitis associated with Campylobacter jejuni bacteraemia. Eur J Clin Microbiol Infect Dis 1997;16:678681.

  • 33.

    Reddy KR, Farnum JB, Thomas E. Acute hepatitis associated with campylobacter colitis. J Clin Gastroenterol 1983;5:259262.

  • 34.

    Cullen JM. Liver, biliary system and exocrine pancreas. In: McGavin MD, Zachary JF, eds. Pathologic basis of veterinary disease. 4th ed. St Louis: Elsevier Mosby, 2007;434435.

    • Search Google Scholar
    • Export Citation
  • 35.

    Campero CM, Anderson ML, Walker RL, et al. Immunohistochemical identification of Campylobacter fetus in natural cases of bovine and ovine abortions. J Vet Med B Infect Dis Vet Public Health 2005;52:138141.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 36.

    van Spreeuwel JP, Duursma GC, Meijer CJ, et al. Campylobacter colitis: histological immunohistochemical and ultrastructural findings. Gut 1985;26:945951.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 37.

    Davies J, Dempsey EW, Amoroso EC. The subplacenta of the guinea-pig: development, histology and histochemistry. J Anat 1961;95:457473.

  • 38.

    Mess A. The guinea pig placenta: model of placental growth dynamics. Placenta 2007;28:812815.

  • 39.

    Carter AM. Animal models of human placentation—a review. Placenta 2007;28:S41S47.

  • 40.

    Hedstrom OR, Sonn RJ, Lassen ED, et al. Pathology of Campylobacter jejuni abortion in sheep. Vet Pathol 1987;24:419426.

Advertisement