Helicobacter pylori infection and inflammatory bowel diseases

Cover Page


Cite item

Full Text

Abstract

Helicobacter pylori is detected in the human intestine on average in 35% of clinical cases, but the question about its etiopathogenetic role in intestinal diseases has not been fully investigated. Many scientists study a relationship between the H. pylori persistence and development of various bowel diseases. Diverse viewpoints have been proposed regarding a potential link between H. pylori and inflammatory bowel diseases (IBD). Here we review the data from domestic and foreign studies aimed at examining potential role of H. pylori both as a trigger and protector resulting in the pathogenetic alterations leading to developing Crohn‘s disease and ulcerative colitis. The former is favored by the hypothesis wherein H. pylori may trigger IBD due to potential connection between extragastric infection and its direct damaging action as well as indirect effects contributing to the initiation of oxidative stress, autoimmune aggression and development of intestinal dysbiosis. In addition, the effects of enterohepatic Helicobacter spp. promoting IBD pathogenesis are discussed. The mechanisms underlying the protective role of H. pylori infection may be driven via differentially expressed acute and/or chronic local inflammatory mucosal response able to downmodulate systemic immune responses and suppress autoimmune reactions, as well as skewing host immune response from a pro-inflammatory Th1/Th17 cell-mediated towards regulatory T-cell response. Moreover, it was found that H. pylori may induce production of antibacterial peptides counteracting potentially pathogenic bacteria involved in IBD pathogenesis. In particular, it was found that IBD patients are dominated with moderate active antral gastritis coupled to atrophy, with the peak intensity observed in patients under 30 years of age. Intensity of intestinal metaplasia in the gastric mucosa of IBD patients accounted for by the duration of the disease course. Basal IBD therapy with 5-aminosalicylic acid lowers severity and activity of gastritis, degree of atrophy as well as magnitude H. pylori invasion in the gastric mucosa. There is evidence that 5-aminosalicylic acid-containing drugs may result in a so-called “spontaneous eradication” of H. pylori infection. Extended investigations are required to examine a role of H. pylori in IBD pathogenesis.

About the authors

Yu. P. Uspenskiy

St. Petersburg State Pediatric Medical University; Pavlov First St. Petersburg State Medical University

Email: baryshnikova_nv@mail.ru

Uspenskiy Yu.P., PhD, MD (Medicine), Head of the Department of Faculty Therapy named after professor V.A. Valdman St. Petersburg State PMU; professor of the Department of Internal Medicine, Stomatological Faculty Pavlov First St. Petersburg SMU.

St. Petersburg

Russian Federation

N. V. Baryshnikova

Pavlov First St. Petersburg State Medical University; Institute of Experimental Medicine

Email: baryshnikova_nv@mail.ru

PhD (Medicine), Associate Professor of the Department of Internal Diseases Pavlov First St. Petersburg SMU; Researcher of the Department of Molecular Microbiology IEM.

St. Petersburg

Russian Federation

A. N. Suvorov

St. Petersburg State University; Institute of Experimental Medicine

Email: suvorov.an@iemspb.ru

RAS Corresponding Member, PhD, MD (Medicine), Head of the Department of Fundamental Problems of Medicine and Medical Technologies, Faculty of Stomatology and Medical Technologies St. Petersburg SU; Head of the Department of Molecular Microbiology IEM.

St. Petersburg Russian Federation

A. V. Svarval

St. Petersburg Pasteur Institute

Author for correspondence.
Email: alenasvar@rambler.ru

Alena V. Svarval - PhD (Medicine), Senior Researcher, Laboratory of Pathogenes Identification.

197348, St. Petersburg, Mira str., 14, Phone: +7 (911) 223-14-11 (mobile)

Russian Federation

References

  1. Белоусова Е.И. Терапия воспалительных заболеваний кишечника: настоящее и будущее // Врач. 2002. № 2. С. 36—39.
  2. Румянцев В.Г. Хеликобактерная инфекция и воспалительные заболевания кишечника // Экспериментальная и клиническая гастроэнтерология. 2006. № 1. С. 72—77.
  3. Успенский Ю.П., Суворов А.Н., Барышникова Н.В. Инфекция Helicobacter pylori в клинической практике. СПб.: ИнформМед, 2011. 572 с.
  4. Ando T., Watanabe O., Ishiguro K., Maeda O., Ishikawa D., Minami M., Hasegawa M., Kondo S., Goto Y., Ohmiya N., Niwa Y., Goto H. Relationships between Helicobacter pylori infection status, endoscopic, histopathological findings, and cytokine production in the duodenum of Crohn’s disease patients. J. Gastroenterol. Hepatol., 2008, vol. 23, no. S2, pp. S193-S197. doi: 10.1111/j.1440-1746.2008.05438.x
  5. Basset C., Holton J., Bazeos A., Vaira D., Bloom S. Are Helicobacter species and enterotoxigenic Bacteroides fragilis involved in inflammatory bowel disease? Dig. Dis. Sci., 2004, vol. 49, pp. 1425—1432. doi: 10.1023/b:ddas.0000042241
  6. Bell S.J., Chisholm S.A., Owen R.J., Borriello S.P., Kamm M.A. Evaluation of Helicobacter species in inflammatory bowel disease. Aliment. Pharmacol. Ther., 2003, vol. 18, no. 5,pp. 481-486. doi: 10.1046/j.1365-2036.2003.01703.x
  7. Bohr U.R., Glasbrenner B., Primus A., Zagoura A., Wex T., Malfertheiner P. Identification of enterohepatic Helicobacter species in patients suffering from inflammatory bowel disease. J. Clin. Microbiol., 2004, vol. 42, pp. 2766-2768. doi: 10.1128/jcm.42.6.2766-2768.2004
  8. Caner S., Altinhas A., Yesil Y., Beyazit Y., Yilmaz B., Yuksel O. The relation between Helicobacter pylori and ulcerative colitis. Turk. J. Med. Sci., 2014, vo. 44, no. 5, pp. 820-823. doi: 10.3906/sag-1305-39
  9. Castano-Rodriguez N., Kaakoush N.O., Lee W.S., Mitchell H.M. Dual role of Helicobacter and Campylobacter species in IBD: a systematic review and meta-analysis. Gut, 2017, vol. 66, no. 2, pp. 235-249. doi: 10.1136/gutjnl-2015-310545
  10. Chiba M., Tsuji T., Takahashi K., Komatsu M., Sugawara T., Ono I. Onset of ulcerative colitis after Helicobacter pylori eradication therapy: a case report. Perm. J., 2016, vol. 20, no. 2, pp. e115-e118. doi: 10.7812/TPP/15-085
  11. D’Inca R., Sturniolo G., Cassaro M., di Pace C., Longo G., Callegari I., Rugge M. Prevalence of upper gastrointestinal lesions and Helicobacter pylori infection in Crohn’s disease. Dig. Dis. Sci., 1998, vol. 43, pp. 988-992. doi: 10.1023/A:1018870415898
  12. Di Tommaso A., Xiang Z., Bugnoli M., Pileri P., Figura N., Bayeli P.F., Rappuoli R., Abrignani S., De Magistris M.T. Helicobacter pylori-specific CD4+ T-cell clones from peripheral blood and gastric biopsies. Infect. Immun., 1995, vol. 63, pp. 1102-1106.
  13. Duchmann R., Marker-Hermann E., Meyer zum Buschenfelde K.H. Bacteria-specific T-cell clones are selective in their reactivity towards different enterobacteria or H. pylori and increased in inflammatory bowel disease. Scand. J. Immunol., 1996, vol. 44, pp. 71-79. doi: 10.1046/j.1365-3083.1996.d01-273.x
  14. Elizalde J.I., Gomez J., Panes J., Lozano M., Casadevall M., Ramirez J., Pizcueta P., Marco F., Rojas F.D., Granger D.N., Pique J.M. Platelet activation in mice and human Helicobacter pylori infection. J. Clin. Invest., 1997, vol. 100, pp. 996-1005. doi: 10.1172/jci119650
  15. El-Omar E., Penman I., Cruikshank G., Dover S., Banerjee S., Williams C., McColl K.E. Low prevalence of Helicobacter pylori in inflammatory bowel disease: association with sulphasalazine. Gut, 1994, vol. 35, pp. 1385-1388. doi: 10.1136/gut.35.10.1385
  16. Feeney M.A., Murphy F., Clegg A.J., Trebble T.M., Sharer N.M., Snook J.A. A case-control study of childhood environmental risk factors for the development of inflammatory bowel disease. Eur. J. Gastroenterol. Hepatol., 2002, vol. 14, pp. 529-534. doi: 10.1097/00042737-200205000-00010
  17. Fox J.G., Boutin S.R., Handt L.K., Taylor N.S., Xu S., Rickman B., Marini R.P., Dewhirst F.E., Paster B.J., Motzel S., Klein H.J. Isolation and characterization of a novel helicobacter species, “Helicobacter Macacae,” from rhesus monkeys with and without chronic idiopathic colitis. J. Clin. Microbiol., 2007, vol. 45, pp. 4061-4063. doi: 10.1128/JCM.01100-07
  18. Garza-Gonzalez E., Perez-Perez G.I., Mendoza-Ibarra S.I., Flores-Gutierrez J.P., Bosques-Padilla F.J. Genetic risk factors for inflammatory bowel disease in a North-Eastern mexican population. Int. J. Immunogenet., 2010, vol. 37, pp. 355-359. doi: 10.1111/j.1744-313X.2010.00932.x
  19. Grehan M., Danon S., Lee A., Daskalopoulos G., Mitchell H. Absence of mucosa-associated colonic Helicobacters in an Australian urban population. J. Clin. Microbiol., 2004, vol. 42, pp. 874-876. doi: 10.1128/JCM.42.2.874-876.2004
  20. Halme L., Karkkainen P., Rautelin H., Kosunen T.U., Sipponen P. High frequency of Helicobacter negative gastritis in patients with Crohn’s disease. Gut, 1996, vol. 38, pp. 379-383. doi: 10.1136/gut.38.3.379
  21. Halme L., Rautelin H., Leidenius M., Kosunen T.U. Inverse correlation between Helicobacter pylori infection and inflammatory bowel disease. J. Clin. Pathol., 1996, vol. 49, pp. 65-67. doi: 10.1136/jcp.49.1.65
  22. Hansen R., Thomson J.M., Fox J.G., El-Omar E.M., Hold G.L. Could Helicobacter organisms cause inflammatory bowel disease? FEMS Immunol. Med. Microbiol., 2011, vol. 61, pp. 1-14. doi: 10.1111/j.1574-695X.2010.00744
  23. Hong C.H., Park D.I., Choi W.H., Park J.H., Kim H.J., Cho Y.K., Sohn C.I., Jeon W.K., Kim B.I., Kim D.H., Kim M.K., Chae S.W., Lee K.B., Sohn J.H., Oh S.J. The clinical usefulness of focally enhanced gastritis in Korean patients with Crohn’s disease. Korean. J. Gastroenterol., 2009, vol. 53, pp. 23-28
  24. Huijsdens X.W., Linskens R.K., Koppes J., Tang Y.L., Meuwissen S.G., Vandenbroucke-Grauls C.M., Savelkoul P.H. Detection of Helicobacter species DNA by quantitative PCR in the gastrointestinal tract of healthy individuals and of patients with inflammatory bowel disease. FEMS Immunol. Med. Microbiol., 2004, vol. 41, pp. 79-84. doi: 10.1016/j.femsim.2004.01.007
  25. Jergens A.E., Wilson-Welder J.H., Dorn A., Henderson A., Liu Z., Evans R.B., Hostetter J., Wannemuehler M.J. Helicobacter bilis triggers persistent immune reactivity to antigens derived from the commensal bacteria in gnotobiotic C3H/HeN mice. Gut, 2007, vol. 56, pp. 934-940. doi: 10.1136/gut.2006.099242
  26. Jiang H.Q., Kushnir N., Thurnheer M.C., Bos N.A., Cebra J.J. Monoassociation of SCID mice with Helicobacter muridarum, but not four other enterics, provokes IBD upon receipt of T cells. Gastroenterology, 2002, vol. 122, pp. 1346—1354. doi: 10.1053/gast.2002.32959
  27. Jin X., Chen Y.P., Chen S.H., Xiang Z. Association between Helicobacter Pylori infection and ulcerative colitis — a case control study from China. Int. J. Med. Sci., 2013, vol. 10, no. 11,pp. 1479—1484. doi: 10.7150/ijms.6934
  28. Kaakoush N.O., Holmes J., Octavia S., Man S.M., Zhang L., Castano-Rodriguez N., Day A.S., Leach S.T., Lemberg D.A., Dutt S., Stormon M., O’Loughlin E.V., Magoffin A., Mitchell H. Detection of Helicobacteraceae in intestinal biopsies of children with Crohn’s disease. Helicobacter, 2010, vol. 15, pp. 549-557. doi: 10.1111/j.1523-5378.2010.00792.x
  29. Kabir S. Detection of Helicobacter pylori DNA in feces and saliva by polymerase chain reaction: a review. Helicobacter, 2004, vol. 9, pp. 115-123. doi: 10.1111/j.1083-4389.2004.00207.x
  30. Kabir S. Detection of Helicobacter pylori in faeces by culture, PCR and enzyme immunoassay. J. Med. Microbiol., 2001, vol. 50, pp. 1021-1029. doi: 10.1099/0022-1317-50-12-1021
  31. Keenan J.I., Beaugie C.R., Jasmann B., Potter H.C., Collett J.A., Frizelle F.A. Helicobacter species in the human colon. Colorectal Dis., 2010, vol. 12, pp. 48-53. doi: 10.1111/j.1463-1318.2008.01672.x
  32. Kelly S.M., Pitcher M.C., Farmery S.M., Gibson G.R. Isolation of Helicobacter pylori from feces of patients with dyspepsia in the United Kingdom. Gastroenterology, 1994, vol. 107, pp. 1671-1674. doi: 10.1016/0016-5085(94)90806-0
  33. Krause I., Anaya J.M., Fraser A., Barzilai O., Ram M., Abad V., Arango A., Garcia J., Shoenfeld Y. Anti-infectious antibodies and autoimmune-associated autoantibodies in patients with type I diabetes mellitus and their close family members. Ann. NY Acad. Sci., 2009, vol. 1173, pp. 633-639. doi: 10.1111/j.1749-6632.2009.04619.x
  34. Kullberg M.C., Ward J.M., Gorelick P.L., Caspar P., Hieny S., Cheever A., Jankovic D., Sher A. Helicobacter hepaticus triggers colitis in specific-pathogen-free interleukin-10 (IL-10)-deficient mice through an IL-12- and gamma interferon-dependent mechanism. Infect. Immun., 1998, vol. 66, pp. 5157-5166.
  35. Laharie D., Asencio C., Asselineau J., Bulois P., Bourreille A., Moreau J., Bonjean P., Lamarque D., Pariente A., Soule J.C., Charachon A., Coffin B., Perez P., Megraud F., Zerbib F. Association between entero-hepatic Helicobacter species and Crohn’s disease: a prospective cross-sectional study. Aliment Pharmacol. Ther., 2009, vol. 30, pp. 283-293. doi: 10.1111/j.1365-2036.2009.04034.x
  36. Lidar M., Langevitz P., Barzilai O., Ram M., Porat-Katz B.S., Bizzaro N., Tonutti E., Maieron R., Chowers Y., Bar-Meir S., Shoenfeld Y. Infectious serologies and autoantibodies in inflammatory bowel disease: insinuations at a true pathogenic role. Ann. NY Acad. Sci., 2009, vol. 1173, pp. 640-648. doi: 10.1111/j.1749-6632.2009.04673.x
  37. Lundgren A., Stromberg E., Sjoling A., Lindholm C., Enarsson K., Edebo A., Johnsson E., Suri-Payer E., Larsson P., Rudin A., Svennerholm A.M., Lundin B.S. Mucosal FOXP3-expressing CD4+CD25high regulatory T cells in Helicobacter pylori-infected patients. Infect. Immun., 2005, vol. 73, pp. 523-531. doi: 10.1128/IAI.73.1.523-531.2005
  38. Luther J., Dave M., Higgins P.D., Kao J.Y. Association between Helicobacter pylori infection and inflammatory bowel disease: a meta-analysis and systematic review of the literature. Inflamm. Bowel. Dis., 2010, vol. 16, 1077-1084. doi: 10.1002/ibd.21116
  39. Man S.M., Zhang L., Day A.S., Leach S., Mitchell H. Detection of enterohepatic and gastric helicobacter species in fecal specimens of children with Crohn’s disease. Helicobacter, 2008, vol. 13, pp. 234-238. doi: 10.1111/j.1523-5378.2008.00607.x
  40. Mansour L., El-Kalla F., Kobtan A., Abd-Elsalam S., Yousef M., Soliman S., Ali L.A., Elkhalawany W., Amer I., Harras H., Hagras M.M., Elhendawy M. Helicobacter pylori may be an initiating factor in newly diagnosed ulcerative colitis patients: a pilot study. World J. Clin. Cases, 2018, vol. 6, no. 13, pp. 641-649. doi: 10.12998/wjcc.v6.i13.641
  41. Mantzaris G.J., Archavlis E., Zografos C., Zavos K., Petraki K., Triadaphyllou G. Low prevalence of Helicobacter pylori in inflammatory bowel disease: association with sulfasalazine. Am. J. Gastroenterol., 1995, vol. 90: 1900.
  42. Matsumura M., Matsui T., Hatakeyama S., Matake H., Uno H., Sakurai T., Yao T., Oishi T., Iwashita A., Fujioka T. Prevalence of Helicobacter pylori infection and correlation between severity of upper gastrointestinal lesions and H. pylori infection in Japanese patients with Crohn’s disease. J. Gastroenterol., 2001, vol. 36, pp. 740-747. doi: 10.1007/s005350170015
  43. Meining A., Bayerdorffer E., Bastlein E., Raudis N., Thiede C., Cyrus B., Kramer W., Klann H., Labenz J., Stolte M. Focal inflammatory infiltrations in gastric biopsy specimens are suggestive of Crohn’s disease. Crohn’s Disease Study Group, Germany. Scand. J. Gastroenterol., 1997, vol. 32, pp. 813-818. doi: 10.3109/00365529708996539
  44. Meyer F., Wilson K.T., James S.P. Modulation of innate cytokine responses by products of Helicobacter pylori. Infect. Immun., 2000, vol. 68, pp. 6265-6272. doi: 10.1128/IAI.68.11.6265-6272.2000
  45. Monceaux C.P., Testerman T.L., Boktor M., Jordan P., Adegboyega P., McGee D.J., Jennings M.H., Parker C.P., Gupta S., Yi P., Ganta V.C., Galous H., Manas K., Alexander J.S. Helicobacter infection decreases basal colon inflammation, but increases disease activity in experimental IBD. Open J. Gastroenterol., 2013, vol. 3, pp. 177-189. doi: 10.4236/ojgas.2013.33029
  46. Oberhuber G., Puspok A., Oesterreicher C., Novacek G., Zauner C., Burghuber M., Vogelsang H., Potzi R., Stolte M., Wrba F. Focally enhanced gastritis: a frequent type of gastritis in patients with Crohn’s disease. Gastroenterology, 1997, vol. 112, pp. 698706. doi: 10.1053/gast.1997.v112.pm9041230
  47. Oliveira A.G., das Granas Pimenta Sanna M., Rocha G.A., Rocha A.M., Santos A., Dani R., Marinho F.P., Moreira L.S., de Lourdes Abreu Ferrari M., Moura S.B., Castro L.P., Queiroz D.M. Helicobacter species in the intestinal mucosa of patients with ulcerative colitis. J. Clin. Microbiol., 2004, vol. 42, pp. 384-386. doi: 10.1128/jcm.42.1.384-386.2004
  48. Oliveira A.G., Rocha, G.A., Rocha A.M., Sanna M.d., Moura S.B., Dani R., Marinho F.P., Moreira L.S., Ferrari M., Castro L.P., Queiroz D.M. Isolation of Helicobacter pylori from the intestinal mucosa of patients with Crohn’s disease. Helicobacter, vol. 11, no. 1, pp. 2-9. doi: 10.1111/j.0083-8703.2006.00368.x
  49. Papamichael K., Konstantopoulos P., Mantzaris G.J. Helicobacter pylori infection and inflammatory bowel disease: is there a link? World J. Gastroenterol., 2014, vol. 20, pp. 6374-6385. doi: 10.3748/wjg.v20.i21.6374
  50. Papamichael K.X., Papaioannou G., Karga H., Roussos A., Mantzaris G.J. Helicobacter pylori infection and endocrine disorders: is there a link? World J. Gastroenterol., 2009, vol. 15, pp. 2701-2707. doi: 10.3748/wjg.15.2701
  51. Parente F., Molteni P., Bollani S., Maconi G., Vago L., Duca P.G., Rembacken B., Axon A.T., Bianchi Porro G. Prevalence of Helicobacter pylori infection and related upper gastrointestinal lesions in patients with inflammatory bowel diseases. A crosssectional study with matching. Scand. J. Gastroenterol., 1997, vol. 32, pp. 1140—1146. doi: 10.3109/00365529709002994
  52. Parlak E., Ulker A., Disibeyaz S., Alkim C., Dagli U. There is no significant increase in the incidence of Helicobacter pylori infection in patients with inflammatory bowel disease in Turkey. J. Clin. Gastroenterol., 2001, vol. 33,pp. 87—88. doi: 10.1097/00004836200107000-00025
  53. Pascasio J.M., Hammond S., Qualman S.J. Recognition of Crohn disease on incidental gastric biopsy in childhood. Pediatr. Dev. Pathol., 2003, vol. 6,pp. 209-214. doi: 10.1007/s10024-002-0601-0
  54. Pearce C.B., Duncan H.D., Timmis L., Green J.R. Assessment of the prevalence of infection with Helicobacter pylori in patients with inflammatory bowel disease. Eur. J. Gastroenterol. Hepatol., 2000, vol. 12, pp. 439-443. doi: 10.1097/00042737200012040-00012
  55. Pellicano R., Bresso F., Demarchi B., Bertolusso L., Sapone N., Rizzetto M., Astegiano M. Prevalence of Helicobacter pylori infection in patients with inflammatory bowel disease: pilot study. Rev. Esp. Enferm. Dig., 2010, vol. 102, pp. 675-666. doi: 10.4321/s1130-01082010001100017
  56. Perri F., Clemente R., Festa V., De Ambrosio C.C., Quitadamo M., Fusillo M., Grossi E., Andriulli A. Serum tumour necrosis factor-alpha is increased in patients with Helicobacter pylori infection and CagA antibodies. Ital. J. Gastroenterol. Hepatol., 1999, vol. 31, pp. 290-294.
  57. Piodi L.P., Bardella M., Rocchia C., Cesana B.M., Baldassarri A., Quatrini M. Possible protective effect of 5-aminosalicylic acid on Helicobacter pylori infection in patients with inflammatory bowel disease. J. Clin. Gastroenterol., 2003, vol. 36, pp. 22-25. doi: 10.1097/00004836-200301000-00008
  58. Pronai L., Schandl L., Orosz Z., Magyar P., Tulassay Z. Lower prevalence of Helicobacter pylori infection in patients with inflammatory bowel disease but not with chronic obstructive pulmonary disease — antibiotic use in the history does not play a significant role. Helicobacter, 2004, vol. 9, pp. 278-283. doi: 10.1111/j.1083-4389.2004.00223.x
  59. Rad R., Brenner L., Bauer S., Schwendy S., Layland L., da Costa C.P., Reindl W., Dossumbekova A., Friedrich M., Saur D., Wagner H., Schmid R.M., Prinz C. CD25+/Foxp3+ T cells regulate gastric inflammation and Helicobacter pylori colonization in vivo. Gastroenterology, 2006, vol. 131, pp. 525-537. doi: 10.1053/j.gastro.2006.05.001
  60. Ram M., Barzilai O., Shapira Y., Anaya J.M., Tincani A., Stojanovich L., Bombardieri S., Bizzaro N., Kivity S., Agmon Levin N., Shoenfeld Y. Helicobacter pylori serology in autoimmune diseases — fact or fiction? Clin. Chem. Lab. Med., 2013, vol. 51, pp. 10751082. doi: 10.1515/cclm-2012-0477
  61. Reibman J., Marmor M., Filner J., Fernandez-Beros M.E., Rogers L., Perez-Perez G.I., Blaser M.J. Asthma is inversely associated with Helicobacter pylori status in an urban population. PLoS One, 2008, vol. 3: e4060. doi: 10.1371/journal.pone.0004060
  62. Rosania R., Von Arnim U., Link A., Rajilic-Stojanovic M., Franck C., Canbay A., Malfertheiner P., Venerito M. Helicobacter pylori eradication therapy is not associated with the onset of inflammatory bowel diseases. A case-control study. J. Gastrointestin. Liver Dis., 2018, vol. 27, no. 2, pp. 119-125. doi: 10.15403/jgld.2014.1121.272.hpy
  63. Ruuska T., Vaajalahti P., Arajarvi P., Maki M. Prospective evaluation of upper gastrointestinal mucosal lesions in children with ulcerative colitis and Crohn’s disease. J. Pediatr. Gastroenterol. Nutr., 1994, vol. 19, pp. 181-186. doi: 10.1097/00005176199408000-00007
  64. Shinzaki S., Fujii T., Bamba S., Ogawa M., Kobayashi T., Oshita M., Tanaka H., Ozeki K., Takahashi S., Kitamoto H. Seven days triple therapy for eradication of Helicobacter pylori does not alter the disease activity of patients with inflammatory bowel disease. Intest. Res., 2018, vol. 16, no. 4, pp. 609-618. doi: 10.5217/ir.2018.00044
  65. Shomer N.H., Dangler C.A., Schrenzel M.D., Fox J.G. Helicobacter bilis-induced inflammatory bowel disease in scid mice with defined flora. Infect. Immun., 1997, vol. 65, pp. 4858-4864.
  66. Smoot D.T., Mobley H.L., Chippendale G.R., Lewison J.F., Resau J.H. Helicobacter pylori urease activity is toxic to human gastric epithelial cells. Infect. Immun., 1990, vol. 58, pp. 1992-1994.
  67. Smythies L.E., Waites K.B., Lindsey J.R., Harris P.R., Ghiara P., Smith P.D. Helicobacter pylori-induced mucosal inflammation is Th1 mediated and exacerbated in IL-4, but not IFNgamma, gene-deficient mice. J. Immunol., 2000, vol. 165, pp. 1022-1029.
  68. Song M.J., Park D.I., Hwang S.J., Kim E.R., Kim Y.H., Jang B.I., Lee S.H., Ji J.S., Shin S.J. The prevalence of Helicobacter pylori infection in Korean patients with inflammatory bowel disease, a multicenter study. Korean J. Gastroenterol., 2009, vol. 53, pp. 341-347. doi: 10.4166/kjg.2009.53.6.341
  69. Sonnenberg A. Review article: historic changes of Helicobacter pylori-associated diseases. Aliment. Pharmacol. Ther., 2013, vol. 38, pp. 329-342. doi: 10.1111/apt.12380
  70. Sonnenberg A., Genta R.M. Low prevalence of Helicobacter pylori infection among patients with inflammatory bowel disease. Aliment. Pharmacol. Ther., 2012, vol. 35, pp. 469-476. doi: 10.1111/j.1365-2036.2011.04969.x
  71. Sonnenberg A., Melton S.D., Genta R.M. Frequent occurrence of gastritis and duodenitis in patients with inflammatory bowel disease. Inflamm. Bowel Dis., 2011, vol. 17, pp. 39-44. doi: 10.1002/ibd.21356
  72. Sladek M., Jedynak-Wasowicz U., Wedrychowicz A., Kowalska-Duplaga K., Pieczarkowski S., Fyderek K. The low prevalence of Helicobacter pylori gastritis in newly diagnosed inflammatory bowel disease children and adolescent. Przegl. Lek., 2007, vol. 64, no. 3, pp. 65-67.
  73. Streutker C.J., Bernstein C.N., Chan V.L., Riddell R.H., Croitoru K. Detection of species-specific helicobacter ribosomal DNA in intestinal biopsy samples from a population-based cohort of patients with ulcerative colitis. J. Clin. Microbiol., 2004, vol. 42, pp. 660-664. doi: 10.1128/jcm.42.2.660-664.2004
  74. Sturegard E., Hertervig E., Sjunnesson H., Wadstrom T. Helicobacter species in human colon biopsies. Aliment. Pharmacol. Ther., 2004, vol. 19, pp. 613-614. doi: 10.1111/j.1365-2036.2004.01880.x
  75. Thia K.T., Loftus E.V., Sandborn W.J., Yang S.K. An update on the epidemiology of inflammatory bowel disease in Asia. Am. J. Gastroenterol., 2008, vol. 103, pp. 3167-3182. doi: 10.1111/j.1572-0241.2008.02158.x
  76. Thomson J.M., Hansen R., Berry S.H., Hope M.E., Murray G.I., Mukhopadhya I., McLean M.H., Shen Z., Fox J.G., El-Omar E., Hold G.L. Enterohepatic helicobacter in ulcerative colitis: potential pathogenic entities? PLoS One, 2011, vol. 6: e17184. doi: 10.1371/journal.pone.0017184
  77. Triantafillidis J.K., Gikas A., Apostolidiss N., Merikas E., Mallass E., Peros G. The low prevalence of helicobacter infection in patients with inflammatory bowel disease could be attributed to previous antibiotic treatment. Am. J. Gastroenterol., 2003, vol. 98, pp. 1213-1214. doi: 10.1111/j.1572-0241.2003.07434.x
  78. Valle J., Kekki M., Sipponen P., Ihamaki T., Siurala M. Longterm course and consequences of Helicobacter pylori gastritis. Results of a 32-year follow-up study. Scand. J. Gastroenterol., 1996, vol. 31, pp. 546-550. doi: 10.3109/0036552960900912
  79. Van Amsterdam K., van Vliet A.H., Kusters J.G., van der Ende A. Of microbe and man: determinants of Helicobacter pylorire-lated diseases. FEMS Microbiol. Rev., 2006, vol. 30, pp. 131-156. doi: 10.1111/j.1574-6976.2005.00006.x
  80. Varas-Lorenzo M.J., Munoz-Agel F. Is Helicobacter pylori active infection increased or decreased in Crohn’s disease? Rev. Esp. Enferm. Dig., 2010, vol. 102, pp. 509-510. doi: 10.4321/s1130-01082010000800013
  81. Vare P.O., Heikius B., Silvennoinen J.A., Karttunen R., Niemela S.E., Lehtola J.K., Karttunen T.J. Seroprevalence of Helicobacter pylori infection in inflammatory bowel disease: is Helicobacter pylori infection a protective factor? Scand. J. Gastroenterol., 2001, vol. 36, pp. 1295-1300. doi: 10.1080/003655201317097155
  82. Wagtmans M.J., Witte A.M., Taylor D.R., Biemond I., Veenendaal R.A., Verspaget H.W., Lamers C.B., van Hogezand R.A. Low seroprevalence of Helicobacter pylori antibodies in historical sera of patients with Crohn’s disease. Scand. J. Gastroenterol., 1997, vol. 32, pp. 712-718. doi: 10.3109/00365529708996523
  83. Wehkamp J., Fellermann K., Herrlinger K.R., Bevins C.L., Stange E.F. Mechanisms of disease: defensins in gastrointestinal diseases. Nat. Clin. Pract. Gastroenterol. Hepatol., 2005, vol. 2, pp. 406-415. doi: 10.1038/ncpgasthep026
  84. Xiang Z., Chen Y.P., Ye Y.F., Ma K.F., Chen S.H., Zheng L., Yang Y.D., Jin X. Helicobacter pylori and Crohn’s disease: a retrospective single-center study from China. World J. Gastroenterol., 2013, vol. 19, pp. 4576-4581. doi: 10.3748/wjg.v19.i28.4576
  85. Zhang L., Danon S.J., Grehan M., Chan V., Lee A., Mitchell H. Natural colonization with Helicobacter species and the development of inflammatory bowel disease in interleukin10-deficient mice. Helicobacter, 2005, vol. 10, pp. 223-230. doi: 10.1111/j.1523-5378.2005.00314.x
  86. Zhang L., Day A., McKenzie G., Mitchell H. Nongastric Helicobacter species detected in the intestinal tract of children. J. Clin. Microbiol., 2006, vol. 44, pp. 2276-2279. doi: 10.1128/jcm.02017-05
  87. Zhang S., Zhong B., Chao K., Xiao Y., Cui Y., Gao X., Chen B., He Y., Hu P., Chen M., Mitchell H.M. Role of Helicobacter species in Chinese patients with inflammatory bowel disease. J. Clin. Microbiol., 2011, vol. 49, pp. 1987-1989. doi: 10.1128/JCM.02630-10

Supplementary files

Supplementary Files
Action
1. JATS XML
Download

Copyright (c) 2021 Uspenskiy Y.P., Baryshnikova N.V., Suvorov A.N., Svarval A.V.

Creative Commons License
This work is licensed under a Creative Commons Attribution 4.0 International License.
СМИ зарегистрировано Федеральной службой по надзору в сфере связи, информационных технологий и массовых коммуникаций (Роскомнадзор).
Регистрационный номер и дата принятия решения о регистрации СМИ: серия ПИ № ФС 77 - 64788 от 02.02.2016.


This website uses cookies

You consent to our cookies if you continue to use our website.

About Cookies