Skip to main content

Advertisement

SpringerLink
Log in

Coccoid Helicobacter pylori exists in the palatine tonsils of patients with IgA nephropathy

  • Original Article—Alimentary Tract
  • Published:
Journal of Gastroenterology Aims and scope Submit manuscript

Abstract

Purpose

Helicobacter pylori infection is acquired by oral ingestion. H. pylori has been reported to be present in the palatine tonsils. To clarify the route and mode of infection, the prevalence of tonsillar H. pylori was evaluated, and an attempt was made to culture tonsillar H. pylori.

Methods

In a prospective study, 55 patients with recurrent pharyngotonsillitis or IgA nephropathy underwent a tonsillectomy. The carbon 13-urea breath test and enzyme-linked immunosorbent assay for the detection of H. pylori IgG antibodies in the serum were performed. Tonsillar H. pylori was cultured under conventional culture conditions for gastric H. pylori with or without the following shock methods; heat shock, hydrogen-peroxide-degrading compounds, or parasitizing amoebae. Immunofluorescence and immunoelectron microscopy using antibodies against H. pylori and cytotoxin-associated antigen A were used to identify tonsillar H. pylori.

Results

H. pylori in the coccoid form was present in tonsillar crypts. Of 55 patients, 43 (78.2%) had tonsillar H. pylori, and 15 (27.3%) were infected with gastric H. pylori. All patients with gastric H. pylori also had tonsillar H. pylori (p < 0.01). Cytotoxin-associated antigen A was observed in 38 (88.4%) of 43 tonsillar H. pylori. Tonsillar H. pylori could not be cultured in any culture conditions. All patients with IgA nephropathy had tonsillar H. pylori (p < 0.01).

Conclusions

The present research might provide some insight into clarifying the route and mode of H. pylori infection. Our findings may indicate that tonsillar H. pylori is one of the antigens causative of IgAN.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  1. Mendall MA, Northfield TC. Transmission of Helicobacter pylori infection. Gut. 1995;37:1–3.

    Article  CAS  PubMed  Google Scholar 

  2. Nguyen AM, el Zaatari FA, Graham DY. Helicobacter pylori in the oral cavity. A critical review of the literature. Oral Surg Oral Med Oral Pathol Oral Radiol Endod. 1995;79:705–9.

    Article  CAS  PubMed  Google Scholar 

  3. Cave DR. How is Helicobacter pylori transmitted? Gastroenterology. 1997;113:S9–14.

    CAS  PubMed  Google Scholar 

  4. Song Q, Spahr A, Schmid RM, Adler G, Bode G. Helicobacter pylori in the oral cavity: high prevalence and great DNA diversity. Dig Dis Sci. 2000;45:2162–7.

    Article  CAS  PubMed  Google Scholar 

  5. Shimada T, Ogura K, Ota S, Terano A, Takahashi M, Hamada E, et al. Identification of Helicobacter pylori in gastric specimens, gastric juice, saliva, and faeces of Japanese patients. Lancet. 1994;343:1636–7.

    Article  CAS  PubMed  Google Scholar 

  6. Cirak MY, Ozdek A, Yilmaz D, Bayiz U, Samim E, Turet S. Detection of Helicobacter pylori and its CagA gene in tonsil and adenoid tissues by PCR. Arch Otolaryngol Head Neck Surg. 2003;129:1225–9.

    Article  PubMed  Google Scholar 

  7. Ishihara K, Miura T, Kimizuka R, Ebihara Y, Mizuno Y, Okuda K. Oral bacteria inhibit Helicobacter pylori growth. FEMS Microbiol Lett. 1997;152:355–61.

    Article  CAS  PubMed  Google Scholar 

  8. Allaker RP, Young KA, Hardie JM, Domizio P, Meadows NJ. Prevalence of Helicobacter pylori at oral and gastrointestinal sites in children: evidence for possible oral-to-oral transmission. J Med Microbiol. 2002;51:312–7.

    CAS  PubMed  Google Scholar 

  9. Kusano K, Tokunaga O, Ando T, Inokuchi A. Helicobacter pylori in the palatine tonsils of patients with IgA nephropathy compared with those of patients with recurrent pharyngotonsillitis. Hum Pathol. 2007;38:1788–97.

    Article  PubMed  Google Scholar 

  10. Wai SN, Moriya T, Kondo K, Misumi H, Amako K. Resuscitation of Vibrio cholerae O1 strain TSI-4 from a viable but nonculturable state by heat shock. FEMS Microbiol Lett. 1996;136:187–91.

    Article  CAS  PubMed  Google Scholar 

  11. Mizunoe Y, Wai SN, Takade A, Yoshida S. Restoration of culturability of starvation-stressed and low-temperature-stressed Escherichia coli O157 cells by using H2O2-degrading compounds. Arch Microbiol. 1999;172:63–7.

    Article  CAS  PubMed  Google Scholar 

  12. Steinert M, Emody L, Amann R, Hacker J. Resuscitation of viable but nonculturable Legionella pneumophila Philadelphia JR32 by Acanthamoeba castellanii. Appl Environ Microbiol. 1997;63:2047–53.

    CAS  PubMed  Google Scholar 

  13. Adams BL, Bates TC, Oliver JD. Survival of Helicobacter pylori in a natural freshwater environment. Appl Environ Microbiol. 2003;69:7462–6.

    Article  CAS  PubMed  Google Scholar 

  14. Cellini L, Robuffo I, Di Campli E, Di Bartolomeo S, Taraborelli T, Dainelli B. Recovery of Helicobacter pylori ATCC43504 from a viable but not culturable state: regrowth or resuscitation? APMIS. 1998;106:571–9.

    Article  CAS  PubMed  Google Scholar 

  15. Segal ED, Cha J, Lo J, Falkow S, Tompkins LS. Altered states: involvement of phosphorylated CagA in the induction of host cellular growth changes by Helicobacter pylori. Proc Natl Acad Sci USA. 1999;96:14559–64.

    Article  CAS  PubMed  Google Scholar 

  16. Basso D, Zambon CF, Letley DP, Stranges A, Marchet A, Rhead JL, et al. Clinical relevance of Helicobacter pylori cagA and vacA gene polymorphisms. Gastroenterology. 2008;135:91–9.

    Article  CAS  PubMed  Google Scholar 

  17. van Doorn LJ, Schneeberger PM, Nouhan N, Plaisier AP, Quint WG, de Boer WA. Importance of Helicobacter pylori cagA and vacA status for the efficacy of antibiotic treatment. Gut. 2000;46:321–6.

    Article  PubMed  Google Scholar 

  18. Azuma T, Ohtani M, Yamazaki Y, Higashi H, Hatakeyama M. Meta-analysis of the relationship between CagA seropositivity and gastric cancer. Gastroenterology. 2004;126:1926–7.

    Article  PubMed  Google Scholar 

  19. Maeda S, Ogura K, Yoshida H, Kanai F, Ikenoue T, Kato N, et al. Major virulence factors, VacA and CagA, are commonly positive in Helicobacter pylori isolates in Japan. Gut. 1998;42:338–43.

    Article  CAS  PubMed  Google Scholar 

  20. Amieva MR, Vogelmann R, Covacci A, Tompkins LS, Nelson WJ, Falkow S. Disruption of the epithelial apical-junctional complex by Helicobacter pylori CagA. Science. 2003;300:1430–4.

    Article  CAS  PubMed  Google Scholar 

  21. Saadat I, Higashi H, Obuse C, Umeda M, Murata Kamiya N, Saito Y, et al. Helicobacter pylori CagA targets PAR1/MARK kinase to disrupt epithelial cell polarity. Nature. 2007;447:330–3.

    Article  CAS  PubMed  Google Scholar 

  22. Necchi V, Candusso ME, Tava F, Luinetti O, Ventura U, Fiocca R, et al. Intracellular, intercellular, and stromal invasion of gastric mucosa, preneoplastic lesions, and cancer by Helicobacter pylori. Gastroenterology. 2007;132:1009–23.

    Article  CAS  PubMed  Google Scholar 

  23. Sisto F, Brenciaglia MI, Scaltrito MM, Dubini F. Helicobacter pylori: ureA, cagA and vacA expression during conversion to the coccoid form. Int J Antimicrob Agents. 2000;15:277–82.

    Article  CAS  PubMed  Google Scholar 

  24. Crabtree JE, Shallcross TM, Heatley RV, Wyatt JI. Evaluation of a commercial ELISA for serodiagnosis of Helicobacter pylori infection. J Clin Pathol. 1991;44:326–8.

    Article  CAS  PubMed  Google Scholar 

  25. Kato S, Ozawa K, Konno M, Tajiri H, Yoshimura N, Shimizu T, et al. Diagnostic accuracy of the 13C-urea breath test for childhood Helicobacter pylori infection: a multicenter Japanese study. Am J Gastroenterol. 2002;97:1668–73.

    Article  PubMed  Google Scholar 

  26. Covacci A, Censini S, Bugnoli M, Petracca R, Burroni D, Macchia G, et al. Molecular characterization of the 128-kDa immunodominant antigen of Helicobacter pylori associated with cytotoxicity and duodenal ulcer. Proc Natl Acad Sci USA. 1993;90:5791–5.

    Article  CAS  PubMed  Google Scholar 

  27. Jonkers D, Stobberingh E, de Bruine A, Arends JW, Stockbrugger R. Evaluation of immunohistochemistry for the detection of Helicobacter pylori in gastric mucosal biopsies. J Infect. 1997;35:149–54.

    Article  CAS  PubMed  Google Scholar 

  28. Jeong JH, Lee DW, Ryu RA, Lee YS, Lee SH, Kang JO, et al. Bacteriologic comparison of tonsil core in recurrent tonsillitis and tonsillar hypertrophy. Laryngoscope. 2007;117:2146–51.

    Article  PubMed  Google Scholar 

  29. Saito N, Konishi K, Sato F, Kato M, Takeda H, Sugiyama T, et al. Plural transformation-processes from spiral to coccoid Helicobacter pylori and its viability. J Infect. 2003;46:49–55.

    Article  CAS  PubMed  Google Scholar 

  30. Benaissa M, Babin P, Quellard N, Pezennec L, Cenatiempo Y, Fauchere JL. Changes in Helicobacter pylori ultrastructure and antigens during conversion from the bacillary to the coccoid form. Infect Immun. 1996;64:2331–5.

    CAS  PubMed  Google Scholar 

  31. Bode G, Mauch F, Malfertheiner P. The coccoid forms of Helicobacter pylori. Criteria for their viability. Epidemiol Infect. 1993;111:483–90.

    Article  CAS  PubMed  Google Scholar 

  32. Mizoguchi H, Fujioka T, Nasu M. Evidence for viability of coccoid forms of Helicobacter pylori. J Gastroenterol. 1999;34(Suppl 11):32–6.

    PubMed  Google Scholar 

  33. Sato F, Saito N, Konishi K, Shoji E, Kato M, Takeda H, et al. Ultrastructural observation of Helicobacter pylori in glucose-supplemented culture media. J Med Microbiol. 2003;52:675–9.

    Article  PubMed  Google Scholar 

  34. Di Bonaventura G, Catamo G, Neri M, Neri G, Piccolomini R. Absence of Helicobacter pylori in tonsillar swabs from dyspeptic patients. New Microbiol. 2000;23:445–8.

    CAS  PubMed  Google Scholar 

  35. Hotta O, Miyazaki M, Furuta T, Tomioka S, Chiba S, Horigome I, et al. Tonsillectomy and steroid pulse therapy significantly impact on clinical remission in patients with IgA nephropathy. Am J Kidney Dis. 2001;38:736–43.

    Article  CAS  PubMed  Google Scholar 

  36. Xie Y, Nishi S, Ueno M, Imai N, Sakatsume M, Narita I, et al. The efficacy of tonsillectomy on long-term renal survival in patients with IgA nephropathy. Kidney Int. 2003;63:1861–7.

    Article  PubMed  Google Scholar 

  37. Mariotti AJ, Agrawal R, Hotaling AJ. The role of tonsillectomy in pediatric IgA nephropathy. Arch Otolaryngol Head Neck Surg. 2009;135:85–7.

    Article  PubMed  Google Scholar 

  38. Suzuki S, Nakatomi Y, Sato H, Tsukada H, Arakawa M. Haemophilus parainfluenzae antigen and antibody in renal biopsy samples and serum of patients with IgA nephropathy. Lancet. 1994;343:12–6.

    Article  CAS  PubMed  Google Scholar 

  39. Koyama A, Sharmin S, Sakurai H, Shimizu Y, Hirayama K, Usui J, et al. Staphylococcus aureus cell envelope antigen is a new candidate for the induction of IgA nephropathy. Kidney Int. 2004;66:121–32.

    Article  CAS  PubMed  Google Scholar 

  40. Gregory MC, Hammond ME, Brewer ED. Renal deposition of cytomegalovirus antigen in immunoglobulin-A nephropathy. Lancet. 1988;1:11–4.

    Article  CAS  PubMed  Google Scholar 

  41. Iwama H, Horikoshi S, Shirato I, Tomino Y. Epstein-Barr virus detection in kidney biopsy specimens correlates with glomerular mesangial injury. Am J Kidney Dis. 1998;32:785–93.

    Article  CAS  PubMed  Google Scholar 

  42. Barratt J, Bailey EM, Buck KS, Mailley J, Moayyedi P, Feehally J, et al. Exaggerated systemic antibody response to mucosal Helicobacter pylori infection in IgA nephropathy. Am J Kidney Dis. 1999;33:1049–57.

    Article  CAS  PubMed  Google Scholar 

  43. Nagashima R, Maeda K, Yuda F, Kudo K, Saitoh M, Takahashi T. Helicobacter pylori antigen in the glomeruli of patients with membranous nephropathy. Virchows Arch. 1997;431:235–9.

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

We would like to thank Mrs. S. Tanaka, Mr. F. Mutoh, Mr. S. Nakahara, Mr. H. Tanaka, and Mr. M. Hashimoto for their skillful technical assistance. This work was supported by KAKENHI 20791201.

Conflict of interest statement

None.

Author information

Authors and Affiliations

  1. Department of Otolaryngology-Head and Neck Surgery, Faculty of Medicine, Saga University, 5-1-1 Nabeshima, Saga, 849-8501, Japan

    Kenichiro Kusano, Akira Inokuchi, Yuichiro Kuratomi & Rintaro Shimazu

  2. Department of Internal Medicine and Gastrointestinal Endoscopy, Faculty of Medicine, Saga University, Saga, Japan

    Kazuma Fujimoto

  3. Division of Microbiology, Department of Pathology and Microbiology, Faculty of Medicine, Saga University, Saga, Japan

    Hiroshi Miyamoto

  4. Division of Pathology, Department of Pathology and Microbiology, Faculty of Medicine, Saga University, Saga, Japan

    Osamu Tokunaga, Daisuke Mori & Fumio Yamasaki

  5. Department of Otolaryngology-Head and Neck Surgery, Saga Prefectural Hospital Koseikan, Saga, Japan

    Kazuki Kidera, Kyoko Tsunetomi & Junji Miyazaki

Authors
  1. Kenichiro Kusano
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Akira Inokuchi
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Kazuma Fujimoto
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Hiroshi Miyamoto
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Osamu Tokunaga
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Yuichiro Kuratomi
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Rintaro Shimazu
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Daisuke Mori
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Fumio Yamasaki
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Kazuki Kidera
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Kyoko Tsunetomi
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Junji Miyazaki
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Kenichiro Kusano.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Kusano, K., Inokuchi, A., Fujimoto, K. et al. Coccoid Helicobacter pylori exists in the palatine tonsils of patients with IgA nephropathy. J Gastroenterol 45, 406–412 (2010). https://doi.org/10.1007/s00535-009-0169-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00535-009-0169-9

Keywords

Search

Navigation