Dual role of Helicobacter and Campylobacter species in IBD: A systematic review and meta-analysis

Gut

Volumn 66, Issue 2, 2017, Pages 235-249

  Castanõ Rodríguez, Natalia ^a   Kaakoush, Nadeem O ^a   Lee, Way Seah ^b,c   Mitchell, Hazel M ^a  

^a UNIVERSITY OF NEW SOUTH WALES   (Australia)

^b UNIVERSITY MALAYA MEDICAL CENTRE   (Malaysia)

^c UNIVERSITY OF MALAYA   (Malaysia)

Author keywords

[No Author keywords available]

Indexed keywords

RNA 16S; ANTIINFECTIVE AGENT;

16SRRNA GENE; AGE; ARTICLE; BACTERIAL STRAIN; CAMPYLOBACTER; CAMPYLOBACTER COLI; CAMPYLOBACTER CONCISUS; CAMPYLOBACTER CURVUS; CAMPYLOBACTER GRACILIS; CAMPYLOBACTER HOMINIS; CAMPYLOBACTER HYOINTESTINALIS; CAMPYLOBACTER JEJUNI; CAMPYLOBACTER LARI; CAMPYLOBACTER RECTUS; CAMPYLOBACTER SHOWAE; CAMPYLOBACTER UPSALIENSIS; CAMPYLOBACTER UREOLYTICUS; CAMPYLOBACTERIOSIS; CASE CONTROL STUDY; COHORT ANALYSIS; CROHN DISEASE; DISEASE ASSOCIATION; DNA SEQUENCE; ETHNICITY; HELICOBACTER; HELICOBACTER BILIS; HELICOBACTER BRANTAE; HELICOBACTER CANADIENSIS; HELICOBACTER CANIS; HELICOBACTER CHOLECYSTUS; HELICOBACTER CINAEDI; HELICOBACTER FENNELLIAE; HELICOBACTER GANMANI; HELICOBACTER HEPATICUS; HELICOBACTER INFECTION; HELICOBACTER MURIDARUM; HELICOBACTER MUSTELAE; HELICOBACTER PULLORUM; HELICOBACTER RAPPINI; HELICOBACTER TROGONTUM; HUMAN; INTESTINE BIOPSY; NONHUMAN; PATHOGENESIS; POLYMERASE CHAIN REACTION; POPULATION RESEARCH; SYSTEMATIC REVIEW; ULCERATIVE COLITIS; CAMPYLOBACTER INFECTIONS; COLITIS, ULCERATIVE; COMPLICATION; HELICOBACTER INFECTIONS; HELICOBACTER PYLORI; META ANALYSIS; MICROBIOLOGY; PROTECTION; RISK FACTOR; STOMACH DISEASES;

ANTI-BACTERIAL AGENTS; CAMPYLOBACTER; CAMPYLOBACTER INFECTIONS; COLITIS, ULCERATIVE; CROHN DISEASE; HELICOBACTER INFECTIONS; HELICOBACTER PYLORI; HUMANS; PROTECTIVE FACTORS; RISK FACTORS; STOMACH DISEASES;

EID: 84946888159     PISSN: 00175749     EISSN: 14683288     Source Type: Journal    
DOI: 10.1136/gutjnl-2015-310545     Document Type: Article

References (126)

1. Suerbaum S, Michetti P. Helicobacter pylori infection. N Engl J Med 2002;347:1175-86.
2. Bewtra M, Kaiser LM, TenHave T, et al. Crohn's disease and ulcerative colitis are associated with elevated standardized mortality ratios: a meta-analysis. Inflamm Bowel Dis 2013;19:599-613.
3. Baumgart DC, Bernstein CN, Abbas Z, et al. IBD around the world: comparing the epidemiology, diagnosis, and treatment: proceedings of the World Digestive Health Day 2010-Inflammatory Bowel Disease Task Force meeting. Inflamm Bowel Dis 2011;17:639-44.
4. Molodecky NA, Soon IS, Rabi DM, et al. Increasing incidence and prevalence of the inflammatory bowel diseases with time, based on systematic review. Gastroenterology 2012;142:46-54.e42; quiz e30.
5. Ananthakrishnan AN. Epidemiology and risk factors for IBD. Nat Rev Gastroenterol Hepatol 2015;12:205-17.
6. Peleteiro B, Bastos A, Ferro A, et al. Prevalence of Helicobacter pylori infection worldwide: a systematic review of studies with national coverage. Dig Dis Sci 2014;59:1698-709.
7. Satsangi J, Silverberg MS, Vermeire S, et al. The Montreal classification of inflammatory bowel disease: controversies, consensus, and implications. Gut 2006;55:749-53.
8. Kaakoush NO, Castano-Rodriguez N, Mitchell HM, et al. Global epidemiology of Campylobacter infection. Clin Microbiol Rev 2015;28:687-720.
9. Putsep K, Branden CI, Boman HG, et al. Antibacterial peptide from H. pylori. Nature 1999;398:671-2.
10. Van Limbergen J, Radford-Smith G, Satsangi J. Advances in IBD genetics. Nat Rev Gastroenterol Hepatol 2014;11:372-85.
11. Hansen R, Thomson JM, Fox JG, et al. Could Helicobacter organisms cause inflammatory bowel disease? FEMS Immunol Med Microbiol 2011;61:1-14.
12. Blaser MJ, Hoverson D, Ely IG, et al. Studies of Campylobacter jejuni in patients with inflammatory bowel disease. Gastroenterology 1984;86:33-8.
13. Boyanova L, Gergova G, Spassova Z, et al. Campylobacter infection in 682 Bulgarian patients with acute enterocolitis, inflammatory bowel disease, and other chronic intestinal diseases. Diagn Microbiol Infect Dis 2004;49:71-4.
14. Weber P, Koch M, Heizmann WR, et al. Microbic superinfection in relapse of inflammatory bowel disease. J Clin Gastroenterol 1992;14:302-8.
15. Gradel KO, Nielsen HL, Schonheyder HC, et al. Increased short-and long-term risk of inflammatory bowel disease after salmonella or Campylobacter gastroenteritis. Gastroenterology 2009;137:495-501.
16. Moher D, Liberati A, Tetzlaff J, et al. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. BMJ 2009;339:b2535.
17. Higgins JP, Thompson SG. Quantifying heterogeneity in a meta-analysis. Stat Med 2002;21:1539-58.
18. Ando T, Watanabe O, Ishiguro K, et al. Relationships between Helicobacter pylori infection status, endoscopic, histopathological findings, and cytokine production in the duodenum of Crohn's disease patients. J Gastroenterol Hepatol 2008;23(Suppl 2):S193-7.
19. Corrado G, Luzzi I, Lucarelli S, et al. Positive association between Helicobacter pylori infection and food allergy in children. Scand J Gastroenterol 1998;33:1135-9.
20. D'Inca R, Sturniolo G, Cassaro M, et al. Prevalence of upper gastrointestinal lesions and Helicobacter pylori infection in Crohn's disease. Dig Dis Sci 1998;43:988-92.
21. Duggan AE, Usmani I, Neal KR, et al. Appendicectomy, childhood hygiene, Helicobacter pylori status, and risk of inflammatory bowel disease: a case control study. Gut 1998;43:494-8.
22. El-Omar E, Penman I, Cruikshank G, et al. Low prevalence of Helicobacter pylori in inflammatory bowel disease: association with sulphasalazine. Gut 1994;35:1385-8.
23. Feeney MA, Murphy F, Clegg AJ, et al. A case-control study of childhood environmental risk factors for the development of inflammatory bowel disease. Eur J Gastroenterol Hepatol 2002;14:529-34.
24. Furusu H, Murase K, Nishida Y, et al. Accumulation of mast cells and macrophages in focal active gastritis of patients with Crohn's disease. Hepatogastroenterology 2002;49:639-43.
25. Garza-Gonzalez E, Perez-Perez GI, Mendoza-Ibarra SI, et al. Genetic risk factors for inflammatory bowel disease in a North-eastern Mexican population. Int J Immunogenet 2010;37:355-9.
26. Genta RM, Sonnenberg A. Non-Helicobacter pylori gastritis is common among paediatric patients with inflammatory bowel disease. Aliment Pharmacol Ther 2012;35:1310-16.
27. Guslandi M, Fanti L, Testoni PA. Helicobacter pylori seroprevalence in Crohn's disease: lack of influence by pharmacological treatment. Hepatogastroenterology 2002;49:1296-7.
28. Halme L, Rautelin H, Leidenius M, et al. Inverse correlation between Helicobacter pylori infection and inflammatory bowel disease. J Clin Pathol 1996;49:65-7.
29. Hansen R, Berry SH, Mukhopadhya I, et al. The microaerophilic microbiota of de-novo paediatric inflammatory bowel disease: the BISCUIT study. PLoS ONE 2013;8:e58825.
30. Hong CH, Park DI, Choi WH, et al. [The clinical usefulness of focally enhanced gastritis in Korean patients with Crohn's disease]. Korean J Gastroenterol 2009;53:23-8.
31. Lidar M, Langevitz P, Barzilai O, et al. Infectious serologies and autoantibodies in inflammatory bowel disease: insinuations at a true pathogenic role. Ann N Y Acad Sci 2009;1173:640-8.
32. Matsumura M, Matsui T, Hatakeyama S, et al. 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;36:740-7.
33. Meining A, Bayerdorffer E, Bastlein E, et al. Focal inflammatory infiltrations in gastric biopsy specimens are suggestive of Crohn's disease. Crohn's Disease Study Group, Germany. Scand J Gastroenterol 1997;32:813-8.
34. Moriyama T, Matsumoto T, Jo Y, et al. Mucosal proinflammatory cytokine and chemokine expression of gastroduodenal lesions in Crohn's disease. Aliment Pharmacol Ther 2005;21(Suppl 2):85-91.
35. Oberhuber G, Puspok A, Oesterreicher C, et al. Focally enhanced gastritis: a frequent type of gastritis in patients with Crohn's disease. Gastroenterology 1997;112:698-706.
36. Oliveira AG, Rocha GA, Rocha AM, et al. Isolation of Helicobacter pylori from the intestinal mucosa of patients with Crohn's disease. Helicobacter 2006;11: 2-9.
37. Ormand JE, Talley NJ, Shorter RG, et al. Prevalence of Helicobacter pylori in specific forms of gastritis. Further evidence supporting a pathogenic role for H. pylori in chronic nonspecific gastritis. Dig Dis Sci 1991;36:142-5.
38. Parente F, Cucino C, Bollani S, et al. Focal gastric inflammatory infiltrates in inflammatory bowel diseases: prevalence, immunohistochemical characteristics, and diagnostic role. Am J Gastroenterol 2000;95:705-11.
39. Parente F, Molteni P, Bollani S, et al. Prevalence of Helicobacter pylori infection and related upper gastrointestinal lesions in patients with inflammatory bowel diseases. A cross-sectional study with matching. Scand J Gastroenterol 1997;32:1140-6.
40. Parlak E, Ulker A, Disibeyaz S, et al. There is no significant increase in the incidence of Helicobacter pylori infection in patients with inflammatory bowel disease in Turkey. J Clin Gastroenterol 2001;33:87-8.
41. Pearce CB, Duncan HD, Timmis L, et al. Assessment of the prevalence of infection with Helicobacter pylori in patients with inflammatory bowel disease. Eur J Gastroenterol Hepatol 2000;12:439-43.
42. Pellicano R, Bresso F, Demarchi B, et al. Prevalence of Helicobacter pylori infection in patients with inflammatory bowel disease: pilot study. Rev Esp Enferm Dig 2010;102:675-6; author reply 6.
43. Piodi LP, Bardella M, Rocchia C, et al. Possible protective effect of 5-aminosalicylic acid on Helicobacter pylori infection in patients with inflammatory bowel disease. J Clin Gastroenterol 2003;36:22-5.
44. Pronai L, Schandl L, Orosz Z, et al. 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;9:278-83.
45. Roka K, Roubani A, Stefanaki K, et al. The prevalence of Helicobacter pylori gastritis in newly diagnosed children with inflammatory bowel disease. Helicobacter 2014;19:400-5.
46. Sladek M, Jedynak-Wasowicz U, Wedrychowicz A, et al. [The low prevalence of Helicobacter pylori gastritis in newly diagnosed inflammatory bowel disease children and adolescent]. Przegl Lek 2007;64(Suppl 3):65-7.
47. Song MJ, Park DI, Hwang SJ, et al. [The prevalence of Helicobacter pylori infection in Korean patients with inflammatory bowel disease, a multicenter study]. Korean J Gastroenterol 2009;53:341-7.
48. Sonnenberg A, Genta RM. Low prevalence of Helicobacter pylori infection among patients with inflammatory bowel disease. Aliment Pharmacol Ther 2012;35:469-76.
49. Triantafillidis JK, Gikas A, Apostolidiss N, et al. The low prevalence of Helicobacter infection in patients with inflammatory bowel disease could be attributed to previous antibiotic treatment. Am J Gastroenterol 2003;98:1213-4.
50. Varas-Lorenzo MJ, Munoz-Agel F. [Is Helicobacter pylori active infection increased or decreased in Crohn's disease?]. Rev Esp Enferm Dig 2010;102:509-10.
51. Vare PO, Heikius B, Silvennoinen JA, et al. Seroprevalence of Helicobacter pylori infection in inflammatory bowel disease: is Helicobacter pylori infection a protective factor? Scand J Gastroenterol 2001;36:1295-300.
52. Wagtmans MJ, Witte AM, Taylor DR, et al. Low seroprevalence of Helicobacter pylori antibodies in historical sera of patients with Crohn's disease. Scand J Gastroenterol 1997;32:712-8.
53. Xiang Z, Chen YP, Ye YF, et al. Helicobacter pylori and Crohn's disease: a retrospective single-center study from China. World J Gastroenterol 2013;19:4576-81.
54. Zhang S, Zhong B, Chao K, et al. Role of Helicobacter species in Chinese patients with inflammatory bowel disease. J Clin Microbiol 2011;49:1987-9.
55. Jin X, Chen YP, Chen SH, et al. Association between Helicobacter pylori infection and ulcerative colitis-a case control study from China. Int J Med Sci 2013;10:1479-84.
56. Mantzaris GJ, Archavlis E, Zografos C, et al. Low prevalence of Helicobacter pylori in inflammatory bowel disease: association with sulfasalazine. Am J Gastroenterol 1995;90:1900.
57. Oliveira AG, das Gracas Pimenta Sanna M, Rocha GA, et al. Helicobacter species in the intestinal mucosa of patients with ulcerative colitis. J Clin Microbiol 2004;42:384-6.
58. Basset C, Holton J, Bazeos A, et al. Are Helicobacter species and enterotoxigenic Bacteroides fragilis involved in inflammatory bowel disease? Dig Dis Sci 2004;49:1425-32.
59. Bohr UR, Glasbrenner B, Primus A, et al. Identification of enterohepatic Helicobacter species in patients suffering from inflammatory bowel disease. J Clin Microbiol 2004;42:2766-8.
60. Kaakoush NO, Holmes J, Octavia S, et al. Detection of Helicobacteraceae in intestinal biopsies of children with Crohn's disease. Helicobacter 2010;15:549-57.
61. Keenan JI, Beaugie CR, Jasmann B, et al. Helicobacter species in the human colon. Colorectal Dis 2010;12:48-53.
62. Laharie D, Asencio C, Asselineau J, et al. Association between entero-hepatic Helicobacter species and Crohn's disease: a prospective cross-sectional study. Aliment Pharmacol Ther 2009;30:283-93.
63. Man SM, Zhang L, Day AS, et al. Detection of enterohepatic and gastric Helicobacter species in fecal specimens of children with Crohn's disease. Helicobacter 2008;13:234-8.
64. Streutker CJ, Bernstein CN, Chan VL, et al. 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;42:660-4.
65. Sturegard E, Hertervig E, Sjunnesson H, et al. Helicobacter species in human colon biopsies. Aliment Pharmacol Ther 2004;19:613-14.
66. Thomson JM, Hansen R, Berry SH, et al. Enterohepatic Helicobacter in ulcerative colitis: potential pathogenic entities? PLoS ONE 2011;6:e17184.
67. Veijola L, Nilsson I, Halme L, et al. Detection of Helicobacter species in chronic liver disease and chronic inflammatory bowel disease. Ann Med 2007;39:554-60.
68. Zhang L, Day A, McKenzie G, et al. Nongastric Helicobacter species detected in the intestinal tract of children. J Clin Microbiol 2006;44:2276-9.
69. Keenan JI, Salm N, Pearson JF, et al. Campylobacter Seroreactivity in Adults with Recent Onset of Crohn's Disease. J Gastroenterol Hepatol Res 2013;2:468-72.
70. Mahendran V, Riordan SM, Grimm MC, et al. Prevalence of Campylobacter species in adult Crohn's disease and the preferential colonization sites of Campylobacter species in the human intestine. PLoS ONE 2011;6:e25417.
71. Man SM, Zhang L, Day AS, et al. Campylobacter concisus and other Campylobacter species in children with newly diagnosed Crohn's disease. Inflamm Bowel Dis 2010;16:1008-16.
72. Mukhopadhya I, Thomson JM, Hansen R, et al. Detection of Campylobacter concisus and other Campylobacter species in colonic biopsies from adults with ulcerative colitis. PLoS ONE 2011;6:e21490
73. Zautner AE, Johann C, Strubel A, et al. Seroprevalence of campylobacteriosis and relevant post-infectious sequelae. Eur J Clin Microbiol Infect Dis 2014;33:1019-27.
74. Zhang L, Man SM, Day AS, et al. Detection and isolation of Campylobacter species other than C. jejuni from children with Crohn's disease. J Clin Microbiol 2009;47:453-5.
75. Kaakoush NO, Mitchell HM, Man SM. Role of emerging Campylobacter species in inflammatory bowel diseases. Inflamm Bowel Dis 2014;20:2189-97.
76. Sartor RB. Mechanisms of disease: pathogenesis of Crohn's disease and ulcerative colitis. Nat Clin Pract Gastroenterol Hepatol 2006;3:390-407.
77. Blaser MJ, Falkow S. What are the consequences of the disappearing human microbiota? Nat Rev Microbiol 2009;7:887-94.
78. Kaakoush NO, Castano-Rodriguez N, Man SM, et al. Is Campylobacter to esophageal adenocarcinoma as Helicobacter is to gastric adenocarcinoma? Trends Microbiol 2015;23:455-62.
79. Arnold IC, Hitzler I, Muller A. The immunomodulatory properties of Helicobacter pylori confer protection against allergic and chronic inflammatory disorders. Front Cell Infect Microbiol 2012;2:10.
80. Azuma T, Suto H, Ito Y, et al. Gastric leptin and Helicobacter pylori infection. Gut 2001;49:324-9.
81. Nishi Y, Isomoto H, Uotani S, et al. Enhanced production of leptin in gastric fundic mucosa with Helicobacter pylori infection. World J Gastroenterol 2005;11:695-9.
82. Barbier M, Vidal H, Desreumaux P, et al. Overexpression of leptin mRNA in mesenteric adipose tissue in inflammatory bowel diseases. Gastroenterol Clin Biol 2003;27:987-91.
83. Tuzun A, Uygun A, Yesilova Z, et al. Leptin levels in the acute stage of ulcerative colitis. J Gastroenterol Hepatol 2004;19:429-32.
84. Barbier M, Cherbut C, Aube AC, et al. Elevated plasma leptin concentrations in early stages of experimental intestinal inflammation in rats. Gut 1998;43:783-90.
85. Singh UP, Singh NP, Guan H, et al. Leptin antagonist ameliorates chronic colitis in IL-10(-)/(-) mice. Immunobiology 2013;218:1439-51.
86. De Rosa V, Procaccini C, Cali G, et al. A key role of leptin in the control of regulatory T cell proliferation. Immunity 2007;26:241-55.
87. Codolo G, Mazzi P, Amedei A, et al. The neutrophil-activating protein of Helicobacter pylori down-modulates Th2 inflammation in ovalbumin-induced allergic asthma. Cell Microbiol 2008;10:2355-63.
88. Windle HJ, Ang YS, Athie-Morales V, et al. Human peripheral and gastric lymphocyte responses to Helicobacter pylori NapA and AphC differ in infected and uninfected individuals. Gut 2005;54:25-32.
89. Luther J, Owyang SY, Takeuchi T, et al. Helicobacter pylori DNA decreases pro-inflammatory cytokine production by dendritic cells and attenuates dextran sodium sulphate-induced colitis. Gut 2011;60:1479-86.
90. Arnold IC, Dehzad N, Reuter S, et al. Helicobacter pylori infection prevents allergic asthma in mouse models through the induction of regulatory T cells. J Clin Invest 2011;121:3088-93.
91. Arnold IC, Lee JY, Amieva MR, et al. Tolerance rather than immunity protects from Helicobacter pylori-induced gastric preneoplasia. Gastroenterology 2011;140:199-209.
92. Harris PR, Wright SW, Serrano C, et al. Helicobacter pylori gastritis in children is associated with a regulatory T-cell response. Gastroenterology 2008;134:491-9.
93. Plummer M, van Doorn LJ, Franceschi S, et al. Helicobacter pylori cytotoxinassociated genotype and gastric precancerous lesions. J Natl Cancer Inst 2007;99:1328-34.
94. Lina TT, Pinchuk IV, House J, et al. CagA-dependent downregulation of B7-H2 expression on gastric mucosa and inhibition of Th17 responses during Helicobacter pylori infection. J Immunol 2013;191:3838-46.
95. Cook KW, Letley DP, Ingram RJ, et al. CCL20/CCR6-mediated migration of regulatory T cells to the Helicobacter pylori-infected human gastric mucosa. Gut 2014;63:1550-9.
96. Wroblewski LE, Peek RM Jr, Wilson KT. Helicobacter pylori and gastric cancer: factors that modulate disease risk. Clin Microbiol Rev 2010;23:713-39.
97. Islami F, Kamangar F. Helicobacter pylori and esophageal cancer risk: a meta-analysis. Cancer Prev Res (Phila) 2008;1:329-38.
98. Inoue N, Tamura K, Kinouchi Y, et al. Lack of common NOD2 variants in Japanese patients with Crohn's disease. Gastroenterology 2002;123:86-91.
99. Leong RW, Armuzzi A, Ahmad T, et al. NOD2/CARD15 gene polymorphisms and Crohn's disease in the Chinese population. Aliment Pharmacol Ther 2003;17:1465-70.
100. Castano-Rodriguez N, Kaakoush NO, Goh KL, et al. Autophagy in Helicobacter pylori infection and related gastric cancer. Helicobacter 2015;20:353-69.
101. Umeno J, Asano K, Matsushita T, et al. Meta-analysis of published studies identified eight additional common susceptibility loci for Crohn's disease and ulcerative colitis. Inflamm Bowel Dis 2011;17:2407-15.
102. Yang SK, Ye BD, Song K. ATG16L1 contributes to Crohn's disease susceptibility in Koreans: overmuch concern for ethnic difference? Gut 2015;64:687-8.
103. Zavros Y, Rogler G. Variants in autophagy genes affect susceptibility to both Crohn's disease and Helicobacter pylori infection. Gastroenterology 2012;142:1060-3.
104. Lemke LB, Ge Z, Whary MT, et al. Concurrent Helicobacter bilis infection in C57BL/6 mice attenuates proinflammatory H. pylori-induced gastric pathology. Infect Immun 2009;77:2147-58.
105. Newell DG. Identification of the outer membrane proteins of Campylobacter pyloridis and antigenic cross-reactivity between C. pyloridis and C. jejuni. J Gen Microbiol 1987;133:163-70.
106. Tindberg Y, Bengtsson C, Bergstrom M, et al. The accuracy of serologic diagnosis of Helicobacter pylori infection in school-aged children of mixed ethnicity. Helicobacter 2001;6:24-30.
107. Kaakoush NO, Day AS, Huinao KD, et al. Microbial dysbiosis in pediatric patients with Crohn's disease. J Clin Microbiol 2012;50:3258-66.
108. Tankovic J, Burghoffer B, Petit JC. Frequent detection by real-time PCR of bacteria from the Helicobacter and Campylobacter genera in stool samples from inflammatory bowel disease patients. 19th European Congress of Clinical Microbiology and Infectious Diseases. Helsinki, 2009:S613.
109. Rajilic-Stojanovic M, Shanahan F, Guarner F, et al. Phylogenetic analysis of dysbiosis in ulcerative colitis during remission. Inflamm Bowel Dis 2013;19:481-8.
110. Kovach Z, Kaakoush NO, Lamb S, et al. Immunoreactive proteins of Campylobacter concisus, an emergent intestinal pathogen. FEMS Immunol Med Microbiol 2011;63:387-96.
111. O'Brien CL, Pavli P, Gordon DM, et al. Detection of bacterial DNA in lymph nodes of Crohn's disease patients using high throughput sequencing. Gut 2014;63:1596-606.
112. Aabenhus R, Permin H, Andersen LP. Characterization and subgrouping of Campylobacter concisus strains using protein profiles, conventional biochemical testing and antibiotic susceptibility. Eur J Gastroenterol Hepatol 2005;17: 1019-24.
113. Aabenhus R, Permin H, On SL, et al. Prevalence of Campylobacter concisus in diarrhoea of immunocompromised patients. Scand J Infect Dis 2002;34:248-52.
114. Engberg J, Bang DD, Aabenhus R, et al. Campylobacter concisus: an evaluation of certain phenotypic and genotypic characteristics. Clin Microbiol Infect 2005;11:288-95.
115. Matsheka MI, Elisha BG, Lastovica AL, et al. Genetic heterogeneity of Campylobacter concisus determined by pulsed field gel electrophoresis-based macrorestriction profiling. FEMS Microbiol Lett 2002;211:17-22.
116. Matsheka MI, Lastovica AJ, Zappe H, et al. The use of (GTG)5 oligonucleotide as an RAPD primer to type Campylobacter concisus. Lett Appl Microbiol 2006;42:600-5.
117. On SL, Harrington CS. Identification of taxonomic and epidemiological relationships among Campylobacter species by numerical analysis of AFLP profiles. FEMS Microbiol Lett 2000;193:161-9.
118. Suzuki J, Sugiyama T, Ito K, et al. Campylobacter showae bacteremia with cholangitis. J Infect Chemother 2013;19:960-3.
119. Harada K, Ozaki S, Kono N, et al. Frequent molecular identification of Campylobacter but not Helicobacter genus in bile and biliary epithelium in hepatolithiasis. J Pathol 2001;193:218-23.
120. Rowland M, Daly L, Vaughan M, et al. Age-specific incidence of Helicobacter pylori. Gastroenterology 2006;130:65-72; quiz 211.
121. Ishikawa N, Fuchigami T, Matsumoto T, et al. Helicobacter pylori infection in rheumatoid arthritis: effect of drugs on prevalence and correlation with gastroduodenal lesions. Rheumatology (Oxford) 2002;41:72-7.
122. Taha AS, Sturrock RD, Russell RI. Helicobacter pylori and peptic ulcers in rheumatoid arthritis patients receiving gold, sulfasalazine, and nonsteroidal anti-inflammatory drugs. Am J Gastroenterol 1992;87:1732-5.
123. Luther J, Dave M, Higgins PD, et al. Association between Helicobacter pylori infection and inflammatory bowel disease: a meta-analysis and systematic review of the literature. Inflamm Bowel Dis 2010;16:1077-84.
124. Wu XW, Ji HZ, Yang MF, et al. Helicobacter pylori infection and inflammatory bowel disease in Asians: a meta-analysis. World J Gastroenterol 2015;21: 4750-6.
125. Rokkas T, Gisbert JP, Niv Y, et al. The association between Helicobacter pylori infection and inflammatory bowel disease based on meta-analysis. United Eur Gastroenterol J 2015. doi: 10.1177/2050640615580889
126. Sterne JA, Sutton AJ, Ioannidis JP, et al. Recommendations for examining and interpreting funnel plot asymmetry in meta-analyses of randomised controlled trials. BMJ 2011;343:d4002.