Skip to main content

Advertisement

Log in

Immunopathology and Th1/Th2 immune response of Campylobacter jejuni-induced paralysis resembling Guillain–Barré syndrome in chicken

  • Original Investigation
  • Published:
Medical Microbiology and Immunology Aims and scope Submit manuscript

Abstract

Immunopathogenesis of Campylobacter jejuni-associated Guillain–Barré syndrome (GBS) is not yet well established probably due to lack of experimental model. Therefore, we studied the Th1/Th2 immune response and pathological changes in C. jejuni-induced chicken model for GBS. C. jejuni (5 × 109 CFU/ml) and placebo were fed to 30 chickens each. Stools of all birds were negative for C. jejuni by culture and PCR before experiment. The birds were regularly assessed for disease symptoms up to 30 days. Sciatic nerves from all chickens were examined at 5 days intervals by histopathology and immunohistochemistry, and also for the expression of Th1/Th2 cytokines. Twenty-two chickens (73.3%) developed diarrhea after C. jejuni infection; 18 (60.0%) experimental chickens developed GBS-like paralytic neuropathy. Pathology in the sciatic nerves of these chickens included perinodal and/or patchy demyelination, perivascular focal lymphocytic infiltration, myelin swelling and presence of macrophages within the nerve fibers on 10th–20th post-infection day (PID). Cytokines (IFN-γ, IL-1β, TNF-α, IL-6 and IL-2) were elevated in early phase (5th–15th PID) and TGF-β2, IL-10 and IL-4 in the recovery phase (25th–30th PID) of the disease. The study provides evidence that C. jejuni infection in the chicken can provide an experimental animal model of GBS.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  1. Linton D, Lawson AJ, Owen RJ, Stanley J (1997) PCR detection, identification to species level, and fingerprinting of Campylobacter jejuni and Campylobacter coli direct from diarrheic samples. J Clin Microbiol 35:2568–2572

    PubMed  CAS  Google Scholar 

  2. Oberhelman RA, Taylor DN (2000) Campylobacter infections in developing countries, 2nd edn. ASM Press, Washington, DC

    Google Scholar 

  3. Nachamkin I, Allos BM, Ho T (1998) Campylobacter species and Guillain–Barré syndrome. Clin Microbiol Rev 11:555–567

    PubMed  CAS  Google Scholar 

  4. Thomas PK (1992) The Guillain–Barré syndrome: no longer a simple concept. J Neurol 239:361–362

    PubMed  CAS  Google Scholar 

  5. Hughes RA (1995) The concept and classification of Guillain–Barré syndrome and related disorders. Rev Neurol (Paris) 151:291–294

    CAS  Google Scholar 

  6. Islam Z, Jacobs BC, van Belkum A, Mohammad QD, Islam MB, Herbrink P, Diorditsa S, Luby SP, Talukder KA, Endtz HP (2010) Axonal variant of Guillain–Barré syndrome associated with Campylobacter infection in Bangladesh. Neurology 74:581–587

    Article  PubMed  CAS  Google Scholar 

  7. Hadden RD, Karch H, Hartung HP, Zielasek J, Weissbrich B, Schubert J, Weishaupt A, Cornblath DR, Swan AV, Hughes RA, Toyka KV (2001) Preceding infections, immune factors, and outcome in Guillain–Barré syndrome. Neurology 56:758–765

    PubMed  CAS  Google Scholar 

  8. Ogawara K, Kuwabara S, Mori M, Hattori T, Koga M, Yuki N (2000) Axonal Guillain–Barré syndrome: relation to anti-ganglioside antibodies and Campylobacter jejuni infection in Japan. Ann Neurol 48:624–631

    Article  PubMed  CAS  Google Scholar 

  9. Ho TW, Mishu B, Li CY, Gao CY, Cornblath DR, Griffin JW, Asbury AK, Blaser MJ, McKhann GM (1995) Guillain–Barré syndrome in northern China. Relationship to Campylobacter jejuni infection and anti-glycolipid antibodies. Brain 118:597–605

    Article  PubMed  Google Scholar 

  10. Koski CL (1997) Mechanisms of Schwann cell damage in inflammatory neuropathy. J Infect Dis 176:S169–S172

    Article  PubMed  CAS  Google Scholar 

  11. Ekerfelt C, Dahle C, Weissert R, Kvarnstrom M, Olsson T, Ernerudh J (2001) Transfer of myelin-specific cells deviated in vitro towards IL-4 production ameliorates ongoing experimental allergic neuritis. Clin Exp Immunol 123:112–118

    Article  PubMed  CAS  Google Scholar 

  12. Nyati KK, Prasad KN, Rizwan A, Verma A, Paliwal VK (2011) Th1 and Th2 response to Campylobacter jejuni antigen in Guillain–Barré syndrome. Arch Neurol 68:445–452

    Article  PubMed  Google Scholar 

  13. Griffin JW, Li CY, Ho TW, Tian M, Gao CY, Xue P, Mishu B, Cornblath DR, Macko C, McKhann GM, Asbury AK (1996) Pathology of the motor-sensory axonal Guillain–Barré syndrome. Ann Neurol 39:17–28

    Article  PubMed  CAS  Google Scholar 

  14. Griffin JW, Li CY, Ho TW, Xue P, Macko C, Gao CY, Yang C, Tian M, Mishu B, Cornblath DR (1995) Guillain–Barré syndrome in northern China. The spectrum of neuropathological changes in clinically defined cases. Brain 118:577–595

    Article  PubMed  Google Scholar 

  15. Feasby TE, Hahn AF, Brown WF, Bolton CF, Gilbert JJ, Koopman WJ (1993) Severe axonal degeneration in acute Guillain–Barré syndrome: evidence of two different mechanisms? J Neurol Sci 116:185–192

    Article  PubMed  CAS  Google Scholar 

  16. Berciano J, Coria F, Monton F, Calleja J, Figols J, LaFarga M (1993) Axonal form of Guillain–Barré syndrome: evidence for macrophage-associated demyelination. Muscle Nerve 16:744–751

    Article  PubMed  CAS  Google Scholar 

  17. Kaldor J, Speed BR (1984) Guillain–Barré syndrome and Campylobacter jejuni: a serological study. Br Med J (Clin Res Ed) 288:1867–1870

    Article  CAS  Google Scholar 

  18. Kuroki S, Saida T, Nukina M, Haruta T, Yoshioka M, Kobayashi Y, Nakanishi H (1993) Campylobacter jejuni strains from patients with Guillain–Barré syndrome belong mostly to penner serogroup 19 and contain beta-N-acetylglucosamine residues. Ann Neurol 33:243–247

    Article  PubMed  CAS  Google Scholar 

  19. Li CY, Xue P, Tian WQ, Liu RC, Yang C (1996) Experimental Campylobacter jejuni infection in the chicken: an animal model of axonal Guillain–Barré syndrome. J Neurol Neurosurg Psychiatry 61:279–284

    Article  PubMed  CAS  Google Scholar 

  20. Nyati KK, Prasad KN, Rizwan A, Verma A, Paliwal VK, Pradhan S (2010) Lymphocyte transformation test detects a response to Campylobacter jejuni antigens in patients with Guillain–Barré syndrome. Med Microbiol Immunol 199:109–116

    Article  PubMed  Google Scholar 

  21. Sinha S, Prasad KN, Pradhan S, Jain D, Jha S (2004) Detection of preceding Campylobacter jejuni infection by polymerase chain reaction in patients with Guillain–Barré syndrome. Trans R Soc Trop Med Hyg 98:342–346

    Article  PubMed  CAS  Google Scholar 

  22. Jain D, Prasad KN, Sinha S, Husain N (2008) Differences in virulence attributes between cytolethal distending toxin positive and negative Campylobacter jejuni strains. J Med Microbiol 57:267–272

    Article  PubMed  CAS  Google Scholar 

  23. Bader SR, Kothlow S, Trapp S, Schwarz SC, Philipp HC, Weigend S, Sharifi AR, Preisinger R, Schmahl W, Kaspers B, Matiasek K (2010) Acute paretic syndrome in juvenile white leghorn chickens resembles late stages of acute inflammatory demyelinating polyneuropathies in humans. J Neuroinflamm 7:7

    Article  Google Scholar 

  24. Maurer M, Toyka KV, Gold R (2002) Immune mechanisms in acquired demyelinating neuropathies: lessons from animal models. Neuromuscul Disord 12:405–414

    Article  PubMed  Google Scholar 

  25. Maier H, Schmidbauer M, Pfausler B, Schmutzhard E, Budka H (1997) Central nervous system pathology in patients with the Guillain–Barre syndrome. Brain 120:451–464

    Article  PubMed  Google Scholar 

  26. Shahrizaila N, Yuki N (2011) Guillain–barre syndrome animal model: the first proof of molecular mimicry in human autoimmune disorder. J Biomed Biotechnol 2011:1–5

    Article  Google Scholar 

  27. Chowdhury D, Arora A (2001) Axonal Guillain–Barré syndrome: a critical review. Acta Neurol Scand 103:267–277

    Article  PubMed  CAS  Google Scholar 

  28. Honavar M, Tharakan JK, Hughes RA, Leibowitz S, Winer JB (1991) A clinicopathological study of the Guillain–Barré syndrome. Nine cases and literature review. Brain 114:1245–1269

    Article  PubMed  Google Scholar 

  29. Kahl KG, Kruse N, Toyka KV, Rieckmann P (2002) Serial analysis of cytokine mRNA profiles in whole blood samples from patients with early multiple sclerosis. J Neurol Sci 200:53–55

    Article  PubMed  CAS  Google Scholar 

  30. Ruddle NH, Bergman CM, McGrath KM, Lingenheld EG, Grunnet ML, Padula SJ, Clark RB (1990) An antibody to lymphotoxin and tumor necrosis factor prevents transfer of experimental allergic encephalomyelitis. J Exp Med 172:1193–1200

    Article  PubMed  CAS  Google Scholar 

  31. Creange A, Belec L, Clair B, Raphael JC, Gherardi RK (1996) Circulating tumor necrosis factor (TNF)-alpha and soluble TNF-alpha receptors in patients with Guillain–Barré syndrome. J Neuroimmunol 68:95–99

    Article  PubMed  CAS  Google Scholar 

  32. Hartung HP, Pollard JD, Harvey GK, Toyka KV (1995) Immunopathogenesis and treatment of the Guillain–Barré syndrome: part I. Muscle Nerve 18:137–153

    Article  PubMed  CAS  Google Scholar 

  33. Jones MA, Totemeyer S, Maskell DJ, Bryant CE, Barrow PA (2003) Induction of proinflammatory responses in the human monocytic cell line THP-1 by Campylobacter jejuni. Infect Immun 71:2626–2633

    Article  PubMed  CAS  Google Scholar 

  34. Hu L, Bray MD, Osorio M, Kopecko DJ (2006) Campylobacter jejuni induces maturation and cytokine production in human dendritic cells. Infect Immun 74:2697–2705

    Article  PubMed  CAS  Google Scholar 

  35. Hickey TE, Majam G, Guerry P (2005) Intracellular survival of Campylobacter jejuni in human monocytic cells and induction of apoptotic death by cytholethal distending toxin. Infect Immun 73:5194–5197

    Article  PubMed  CAS  Google Scholar 

  36. Strierter RM, Standiford TJ, Rolfe MW, Lynch JP III, Metinko AP, Kunkel SL (1992) Cytokines in pulmonary injury. Marcel Dekker, New York

    Google Scholar 

  37. Abbas A, Lichtman A (2003) Cellular and molecular immunology, 5th edn. Saunders, Philadelphia

    Google Scholar 

  38. Baqar S, Pacheco ND, Rollwagen FM (1993) Modulation of mucosal immunity against Campylobacter jejuni by orally administered cytokines. Antimicrob Agents Chemother 37:2688–2692

    PubMed  CAS  Google Scholar 

  39. Al-Banna N, Raghupathy R, Albert MJ (2008) Correlation of proinflammatory and anti-inflammatory cytokine levels with histopathological changes in an adult mouse lung model of Campylobacter jejuni infection. Clin Vaccine Immunol 15:1780–1787

    Article  PubMed  CAS  Google Scholar 

  40. Creange A, Belec L, Clair B, Degos JD, Raphael JC, Gherardi RK (1998) Circulating transforming growth factor beta 1 (TGF-beta1) in Guillain–Barré syndrome: decreased concentrations in the early course and increase with motor function. J Neurol Neurosurg Psychiatry 64:162–165

    Article  PubMed  CAS  Google Scholar 

  41. Zhu J, Mix E, Link H (1998) Cytokine production and the pathogenesis of experimental autoimmune neuritis and Guillain–Barre syndrome. J Neuroimmunol 84:40–52

    Article  PubMed  CAS  Google Scholar 

  42. Koski CL, Chou DK, Jungalwala FB (1989) Anti-peripheral nerve myelin antibodies in Guillain–Barre syndrome bind a neutral glycolipid of peripheral myelin and cross-react with Forssman antigen. J Clin Invest 84:280–287

    Article  PubMed  CAS  Google Scholar 

  43. Fiorentino DF, Bond MW, Mosmann TR (1989) Two types of mouse T helper cell. IV. Th2 clones secrete a factor that inhibits cytokine production by Th1 clones. J Exp Med 170:2081–2095

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

The study was financially supported by the Indian Council of Medical Research (ICMR), Government of India, New Delhi (5/3/3/24/2006-ECD-I). The authors are thankful to Mrs. Madhulika, Department of Pathology, Sanjay Gandhi Postgraduate Institute of Medical Sciences, Lucknow, India for her technical assistance during electron microscopy experiments. The authors KKN (80/569/2007-ECD-I) and NKK (3/1/2/12/Neuro/2010-NCD-I) acknowledge the financial assistance from ICMR, Government of India, New Delhi.

Conflict of interest

The authors declare that they have no conflict of interest.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Kashi N. Prasad.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Nyati, K.K., Prasad, K.N., Kharwar, N.K. et al. Immunopathology and Th1/Th2 immune response of Campylobacter jejuni-induced paralysis resembling Guillain–Barré syndrome in chicken. Med Microbiol Immunol 201, 177–187 (2012). https://doi.org/10.1007/s00430-011-0220-3

Download citation

  • Received:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00430-011-0220-3

Keywords

Navigation