Extragastrointestinal manifestations of Helicobacter pylori infection: Facts or myth? A critical review

Journal of Digestive Diseases

Volumn 13, Issue 7, 2012, Pages 342-349

  Tan, Huck Joo ^a   Goh, Khean Lee ^b  

^a Sunway Medical Centre   (Malaysia)

^b UNIVERSITY OF MALAYA   (Malaysia)

Author keywords

Helicobacter pylori; Idiopathic thrombocytopenic purpura; Iron deficiency anemia

Indexed keywords

GHRELIN; LEPTIN;

ALZHEIMER DISEASE; CORONARY ARTERY DISEASE; DISEASE ASSOCIATION; EPILEPSY; HEART MUSCLE ISCHEMIA; HELICOBACTER INFECTION; HORMONE BLOOD LEVEL; HUMAN; IDIOPATHIC THROMBOCYTOPENIC PURPURA; IRON DEFICIENCY ANEMIA; OBESITY; PARKINSON DISEASE; PRIORITY JOURNAL; REVIEW; SKIN DISEASE; STROKE; URTICARIA;

ANEMIA, IRON-DEFICIENCY; CARDIOVASCULAR DISEASES; GHRELIN; HELICOBACTER INFECTIONS; HELICOBACTER PYLORI; HUMANS; LEPTIN; NERVOUS SYSTEM DISEASES; OBESITY; PURPURA, THROMBOCYTOPENIC, IDIOPATHIC;

EID: 84862650263     PISSN: 17512972     EISSN: 17512980     Source Type: Journal    
DOI: 10.1111/j.1751-2980.2012.00599.x     Document Type: Review

References (99)

1. Hill AB. The environment and disease: association or causation? Proc R Soc Med 1965; 58: 295-300.
2. Gasbarrini A, Franceschi F, Tartaglione R, Landolfi R, Pola P, Gasbarrini G. Regression of autoimmune thrombocytopenia after eradication of Helicobacter pylori. Lancet 1998; 352: 878.
3. Kohda K, Kuga T, Kogawa K etal. Effect of Helicobacter pylori eradication on platelet recovery in Japanese patients with chronic idiopathic thrombocytopenic purpura and secondary autoimmune thrombocytopenic purpura. Br J Haematol 2002; 118: 584-8.
4. Sivapathasingam V, Harvey MP, Wilson RB. Helicobacter pylori eradication: a novel therapeutic option in chronic immune thrombocytopenic purpura. Med J Aust 2008; 189: 367-70.
5. Campuzano-Maya G. Proof of an association between Helicobacter pylori and idiopathic thrombocytopenic purpura in Latin America. Helicobacter 2007; 12: 265-73.
6. Emilia G, Longo G, Luppi M etal. Helicobacter pylori eradication can induce platelet recovery in idiopathic thrombocytopenic purpura. Blood 2001; 97: 812-4.
7. Hashino S, Mori A, Suzuki S etal. Platelet recovery in patients with idiopathic thrombocytopenic purpura after eradication of Helicobacter pylori. Int J Hematol 2003; 77: 188-91.
8. Michel M, Khellaf M, Desforges L etal. Antoimmune thrombocytopenic purpura and Helicobacter pylori infection. Arch Intern Med 2002; 162: 1033-6.
9. Kurtoglu E, Kayacetin E, Ugur A. Helicobacter pylori infection in patients with autoimmune thrombocytopenic purpura. World J Gastroenterol 2004; 10: 2113-5.
10. Ishiyama M, Teramura M, Iwabe K, Kato T, Motoji T. Clonally expanded T-cells in the peripheral blood of patients with idiopathic thrombocytopenic purpura and Helicobacter pylori infection. Int J Hematol 2006; 83: 147-51.
11. Takahashi T, Yujiri T, Shinohara K etal. Molecular mimicry by Helicobacter pylori CagA protein may be involved in the pathogenesis of H. pylori-associated chronic idiopathic thrombocytopenic purpura. Br J Haematol 2004; 124: 91-6.
12. Veneri D, Gottardi M, Guizzardi E, Zanuso C, Krampera M, Franchini M. Idiopathic thrombocytopenic purpura, Helicobacter pylori infection, and HLA class II alleles. Blood 2002; 100: 1925-6; author reply 1926-7.
13. Suzuki T, Matsushima M, Masui A etal. Effect of Helicobacter pylori eradication in patients with chronic idiopathic thrombocytopenic purpura - a randomized controlled trial. Am J Gastroenterol 2005; 100: 1265-70.
14. Russo G, Miraglia V, Branciforte F etal; AIEOP-ITP Study Group. Effect of eradication of Helicobacter pylori in children with chronic immune thrombocytopenia: a prospective, controlled, multicenter study. Pediatr Blood Cancer 2011; 56: 273-8.
15. Treepongkaruna S, Sirachainan N, Kanjanapongkul S etal. Absence of platelet recovery following Helicobacter pylori eradication in childhood chronic idiopathic thrombocytopenic purpura: a multi-center randomized controlled trial. Pediatr Blood Cancer 2009; 53: 72-7.
16. Stasi R, Sarpatwari A, Segal JB etal. Effects of eradication of Helicobacter pylori infection in patients with immune thrombocytopenic purpura: a systematic review. Blood 2009; 113: 1231-40.
17. Arnold DM, Bernotas A, Nazi I etal. Platelet count response to H. pylori treatment in patients with immune thrombocytopenic purpura with and without H. pylori infection: a systematic review. Haematologica 2009; 94: 850-6.
18. Franchini M, Cruciani M, Mengoli C, Pizzolo G, Veneri D. Effect of Helicobacter pylori eradication on platelet count in idiopathic thrombocytopenic purpura: a systematic review and meta-analysis. J Antimicrob Chemother 2007; 60: 237-46.
19. Tsumoto C, Tominaga K, Okazaki H etal. Long-term efficacy of Helicobacter pylori eradication in patients with idiopathic thrombocytopenic purpura: 7-year follow-up prospective study. Ann Hematol 2009; 88: 789-93.
20. Malfertheiner P, Megraud F, O'Morain C etal. Current concepts in the management of Helicobacter pylori infection: the Maastricht III Consensus Report. Gut 2007; 56: 772-81.
21. Fock KM, Katelaris P, Sugano K etal; Second Asia-Pacific Conference. Second Asia-Pacific Consensus Guidelines for Helicobacter pylori infection. J Gastroenterol Hepatol 2009; 24: 1587-600.
22. Dufour C, Brisigotti M, Fabretti G, Luxardo P, Mori PG, Barabino A. Helicobacter pylori gastric infection and sideropenic refractory anemia. J Pediatr Gastroenterol Nutr 1993; 17: 225-7.
23. Cardenas VM, Mulla ZD, Ortiz M, Graham DY. Iron deficiency and Helicobacter pylori infection in the United States. Am J Epidemiol 2006; 163: 127-34.
24. Milman N, Rosenstock S, Andersen L, Jørgensen T, Bonnevie O. Serum ferritin, hemoglobin, and Helicobacter pylori infection: a seroepidemiological survey comprising 2794 Danish adults. Gastroenterology 1998; 115: 268-74.
25. Choe YH, Kim SK, Hong YC. The relationship between Helicobacter pylori infection and iron deficiency: seroprevalence study in 937 pubescent children. Arch Dis Child 2003; 88: 178.
26. Muhsen K, Cohen D. Helicobacter pylori infection and iron stores: a systematic review and meta-analysis. Helicobacter 2008; 13: 323-40.
27. Choi JW. Does Helicobacter pylori infection relate to iron deficiency anaemia in prepubescent children under 12 years of age? Acta Paediatr 2003; 92: 970-2.
28. Collett JA, Burt MJ, Frampton CM etal. Seroprevalence of Helicobacter pylori in the adult population of Christchurch: risk factors and relationship to dyspeptic symptoms and iron studies. N Z Med J 1999; 112: 292-5.
29. Chen LH, Luo HS. Effects of H pylori therapy on erythrocytic and iron parameters in iron deficiency anemia patients with H pylori-positive chronic gastritis. World J Gastroenterol 2007; 13: 5380-3.
30. Annibale B, Marignani M, Monarca B etal. Reversal of iron deficiency anemia after Helicobacter pylori eradication in patients with asymptomatic gastritis. Ann Intern Med 1999; 131: 668-72.
31. Qu XH, Huang XL, Xiong P etal. Does Helicobacter pylori infection play a role in iron deficiency anemia? A meta-analysis. World J Gastroenterol 2010; 16: 886-96.
32. Huang X, Qu X, Yan W etal. Iron deficiency anaemia can be improved after eradication of Helicobacter pylori. Postgrad Med J 2010; 86: 272-8.
33. Yuan W, Li Y, Yang K etal. Iron deficiency anemia in Helicobacter pylori infection: meta-analysis of randomized controlled trials. Scand J Gastroenterol 2010; 45: 665-76.
34. Ciacci C, Sabbatini F, Cavallaro R etal. Helicobacter pylori impairs iron absorption in infected individuals. Dig Liver Dis 2004; 36: 455-60.
35. Lombard M, Chua E, O'Toole P. Regulation of intestinal non-haem iron absorption. Gut 1997; 40: 435-9.
36. Patel P, Mendall MA, Carrington D etal. Association of Helicobacter pylori and Chlamydia pneumoniae infections with coronary heart disease and cardiovascular risk factors. BMJ 1995; 311: 711-4.
37. Kinjo K, Sato H, Sato H etal; Osaka Acute Coronary Insufficiency Study (OACIS) Group. Prevalence of Helicobacter pylori infection and its link to coronary risk factors in Japanese patients with acute myocardial infarction. Circ J 2002; 66: 805-10.
38. Folsom AR, Nieto FJ, Sorlie P, Chambless LE, Graham DY. Helicobacter pylori seropositivity and coronary heart disease incidence. Atherosclerosis Risk In Communities (ARIC) Study Investigators. Circulation 1998; 98: 845-50.
39. McDonagh TA, Woodward M, Morrison CE etal. Helicobacter pylori infection and coronary heart disease in the North Glasgow MONICA population. Eur Heart J 1997; 18: 1257-60.
40. Danesh J, Peto R. Risk factors for coronary heart disease and infection with Helicobacter pylori: meta-analysis of 18 studies. BMJ 1998; 316: 1130-2.
41. Singh RK, McMahon AD, Patel H, Packard CJ, Rathbone BJ, Samani NJ. Prospective analysis of the association of infection with CagA bearing strains of Helicobacter pylori and coronary heart disease. Heart 2002; 88: 43-6.
42. Khodaii Z, Vakili H, Ghaderian SM, Najar RA, Panah AS. Association of Helicobacter pylori infection with acute myocardial infarction. Coron Artery Dis 2011; 22: 6-11.
43. Figura N, Palazzuoli A, Faglia S etal. Infection by CagA-positive Helicobacter pylori strains in patients with ischemic heart disease: prevalence and association with exercise-induced electrocardiographic abnormalities. Dig Dis Sci 2002; 47: 831-6.
44. Kowalski M. Helicobacter pylori (H. pylori) infection in coronary artery disease: influence of H. pylori eradication on coronary artery lumen after percutaneous transluminal coronary angioplasty. The detection of H. pylori specific DNA in human coronary atherosclerotic plaque. J Physiol Pharmacol 2001; 52: 3-31.
45. Pellicano R, Parravicini PP, Bigi R etal. Infection by Helicobacter pylori and acute myocardial infarction. Do cytotoxic strains make a difference? New Microbiol 2002; 25: 315-21.
46. Franceschi F, Niccoli G, Ferrante G etal. CagA antigen of Helicobacter pylori and coronary instability: insight from a clinico-pathological study and a meta-analysis of 4241 cases. Atherosclerosis 2009; 202: 535-42.
47. Huang B, Chen Y, Xie Q etal. CagA-positive Helicobacter pylori strains enhanced coronary atherosclerosis by increasing serum OxLDL and HsCRP in patients with coronary heart disease. Dig Dis Sci 2011; 56: 109-14.
48. Jia EZ, Zhao FJ, Hao B etal. Helicobacter pylori infection is associated with decreased serum levels of high density lipoprotein, but not with the severity of coronary atherosclerosis. Lipids Health Dis 2009; 8: 59.
49. Tamer GS, Tengiz I, Ercan E, Duman C, Alioglu E, Turk UO. Helicobacter pylori seropositivity in patients with acute coronary syndromes. Dig Dis Sci 2009; 54: 1253-6.
50. Szklo M, Ding J, Tsai MY etal. Individual pathogens, pathogen burden and markers of subclinical atherosclerosis: the Multi-Ethnic Study of Atherosclerosis. J Cardiovasc Med (Hagerstown) 2009; 10: 747-51.
51. Kucukazman M, Yavuz B, Sacikara M etal. The relationship between updated Sydney System score and LDL cholesterol levels in patients infected with Helicobacter pylori. Dig Dis Sci 2009; 54: 604-7.
52. Ayada K, Yokota K, Kobayashi K, Shoenfeld Y, Matsuura E, Oguma K. Chronic infections and atherosclerosis. Clin Rev Allergy Immunol 2009; 37: 44-8.
53. Lenzi C, Palazzuoli A, Giordano N etal. H pylori infection and systemic antibodies to CagA and heat shock protein 60 in patients with coronary heart disease. World J Gastroenterol 2006; 12: 7815-20.
54. Birnie DH, Holme ER, McKay IC, Hood S, McColl KE, Hillis WS. Association between antibodies to heat shock protein 65 and coronary atherosclerosis. Possible mechanism of action of Helicobacter pylori and other bacterial infections in increasing cardiovascular risk. Eur Heart J 1998; 19: 387-94.
55. Zhu J, Katz RJ, Quyyumi AA etal. Association of serum antibodies to heat-shock protein 65 with coronary calcification levels: suggestion of pathogen-triggered autoimmunity in early atherosclerosis. Circulation 2004; 109: 36-41.
56. De Bastiani R, Gabrielli M, Ubaldi E etal. High prevalence of Cag-A positive H. pylori strains in ischemic stroke: a primary care multicenter study. Helicobacter 2008; 13: 274-7.
57. Pietroiusti A, Diomedi M, Silvestrini M etal. Cytotoxin-associated gene-A-positive Helicobacter pylori strains are associated with atherosclerotic stroke. Circulation 2002; 106: 580-4.
58. Diomedi M, Pietroiusti A, Silvestrini M etal. CagA-positive Helicobacter pylori strains may influence the natural history of atherosclerotic stroke. Neurology 2004; 63: 800-4.
59. Cremonini F, Gabrielli M, Gasbarrini G, Pola P, Gasbarrini A. The relationship between chronic H. pylori infection, CagA seropositivity and stroke: meta-analysis. Atherosclerosis 2004; 173: 253-9.
60. Zhang S, Guo Y, Ma Y, Teng Y. Relationship between the cytotoxin-associated gene-A status of H pylori strains and cerebral infarction in European Caucasians and Chinese Han: a meta-analysis. World J Gastroenterol 2008; 14: 1286-92.
61. Pasceri V, Patti G, Cammarota G, Pristipino C, Richichi G, Di Sciascio G. Virulent strains of Helicobacter pylori and vascular diseases: a meta-analysis. Am Heart J 2006; 151: 1215-22.
62. Gabrielli M, Santoliquido A, Cremonini F etal. CagA-positive cytotoxic H. pylori strains as a link between plaque instability and atherosclerotic stroke. Eur Heart J 2004; 25: 64-8.
63. Xu Q, Willeit J, Marosi M etal. Association of serum antibodies to heat-shock protein 65 with carotid atherosclerosis. Lancet 1993; 341: 255-9.
64. Sung JJ, Sanderson JE. Hyperhomocysteinaemia, Helicobacter pylori, and coronary artery disease. Heart 1996; 76: 305-7.
65. Markus HS, Mendall MA. Helicobacter pylori infection: a risk factor for ischaemic cerebrovascular disease and carotid atheroma. J Neurol Neurosurg Psychiatry 1998; 64: 104-7.
66. Bjarnason IT, Charlett A, Dobbs RJ etal. Role of chronic infection and inflammation in the gastrointestinal tract in the etiology and pathogenesis of idiopathic parkinsonism. Part 2: response of facets of clinical idiopathic parkinsonism to Helicobacter pylori eradication. A randomized, double-blind, placebo-controlled efficacy study. Helicobacter 2005; 10: 276-87.
67. Pierantozzi M, Pietroiusti A, Brusa L etal. Helicobacter pylori eradication and l-dopa absorption in patients with PD and motor fluctuations. Neurology 2006; 66: 1824-9.
68. Dobbs SM, Dobbs RJ, Weller C etal. Differential effect of Helicobacter pylori eradication on time-trends in brady/hypokinesia and rigidity in idiopathic parkinsonism. Helicobacter 2010; 15: 279-94.
69. Honjo K, van Reekum R, Verhoeff NP. Alzheimer's disease and infection: do infectious agents contribute to progression of Alzheimer's disease? Alzheimers Dement 2009; 5: 348-60.
70. Kountouras J, Tsolaki M, Gavalas E etal. Relationship between Helicobacter pylori infection and Alzheimer disease. Neurology 2006; 66: 938-40.
71. Kountouras J, Boziki M, Gavalas E etal. Increased cerebrospinal fluid Helicobacter pylori antibody in Alzheimer's disease. Int J Neurosci 2009; 119: 765-77.
72. Kountouras J, Boziki M, Gavalas E etal. Eradication of Helicobacter pylori may be beneficial in the management of Alzheimer's disease. J Neurol 2009; 256: 758-67.
73. Ozturk A, Ozturk CE, Ozdemirli B, Yucel M, Bahçebaşi T. Helicobacter pylori infection in epileptic patients. Seizure 2007; 16: 147-52.
74. Arslan E, Atilgan H, Yavaşoǧlu I. The prevalence of Helicobacter pylori in obese subjects. Eur J Intern Med 2009; 20: 695-7.
75. Ioannou GN, Weiss NS, Kearney DJ. Is Helicobacter pylori seropositivity related to body mass index in the United States? Aliment Pharmacol Ther 2005; 21: 765-72.
76. Wu MS, Lee WJ, Wang HH, Huang SP, Lin JT. A case-control study of association of Helicobacter pylori infection with morbid obesity in Taiwan. Arch Intern Med 2005; 165: 1552-5.
77. Pacifico L, Anania C, Osborn JF etal. Long-term effects of Helicobacter pylori eradication on circulating ghrelin and leptin concentrations and body composition in prepubertal children. Eur J Endocrinol 2008; 158: 323-32.
78. Azuma T, Suto H, Ito Y etal. Eradication of Helicobacter pylori infection induces an increase in body mass index. Aliment Pharmacol Ther 2002; 16 Suppl 2: 240-4.
79. Nwokolo CU, Freshwater DA, O'Hare P, Randeva HS. Plasma ghrelin following cure of Helicobacter pylori. Gut 2003; 52: 637-40.
80. Osawa H, Kita H, Ohnishi H etal. Changes in plasma ghrelin levels, gastric ghrelin production, and body weight after Helicobacter pylori cure. J Gastroenterol 2006; 41: 954-61.
81. Shiotani A, Miyanishi T, Uedo N, Iishi H. Helicobacter pylori infection is associated with reduced circulating ghrelin levels independent of body mass index. Helicobacter 2005; 10: 373-8.
82. Jang EJ, Park SW, Park JS etal. The influence of the eradication of Helicobacter pylori on gastric ghrelin, appetite, and body mass index in patients with peptic ulcer disease. J Gastroenterol Hepatol 2008; 23 Suppl 2: S278-85.
83. Méndez-Sánchez N, Pichardo-Bahena R, Vásquez-Fernández F etal. Effect of Helicobacter pylori infection on gastric ghrelin expression and body weight. Rev Gastroenterol Mex 2007; 72: 359-64.
84. Osawa H, Nakazato M, Date Y etal. Impaired production of gastric ghrelin in chronic gastritis associated with Helicobacter pylori. J Clin Endocrinol Metab 2005; 90: 10-6.
85. Roper J, Francois F, Shue PL etal. Leptin and ghrelin in relation to Helicobacter pylori status in adult males. J Clin Endocrinol Metab 2008; 93: 2350-7.
86. Cindoruk M, Yetkin I, Deger SM, Karakan T, Kan E, Unal S. Influence of H pylori on plasma ghrelin in patients without atrophic gastritis. World J Gastroenterol 2007; 13: 1595-8.
87. Nweneka CV, Prentice AM. Helicobacter pylori infection and circulating ghrelin levels - a systematic review. BMC Gastroenterol 2011; 11: 7.
88. Fukuda S, Shimoyama T, Umegaki N, Mikami T, Nakano H, Munakata A. Effect of Helicobacter pylori eradication in the treatment of Japanese patients with chronic idiopathic urticaria. J Gastroenterol 2004; 39: 827-30.
89. Di Campli C, Gasbarrini A, Nucera E etal. Beneficial effects of Helicobacter pylori eradication on idiopathic chronic urticaria. Dig Dis Sci 1998; 43: 1226-9.
90. Hellmig S, Troch K, Ott SJ, Schwarz T, Fölsch UR. Role of Helicobacter pylori infection in the treatment and outcome of chronic urticaria. Helicobacter 2008; 13: 341-5.
91. Pellicano R, Leone N, Berrutti M etal. Helicobacter pylori seroprevalence in hepatitis C virus positive patients with cirrhosis. J Hepatol 2000; 33: 648-50.
92. Queiroz DM, Rocha AM, Rocha GA etal. Association between Helicobacter pylori infection and cirrhosis in patients with chronic hepatitis C virus. Dig Dis Sci 2006; 51: 370-3.
93. Zullo A, Sanchez-Mete L, Hassan C etal. Helicobacter pylori density and CagA status in cirrhotic patients: a case-control study. J Gastroenterol Hepatol 2004; 19: 1174-8.
94. Leone N, Pellicano R, Brunello F etal. Helicobacter pylori seroprevalence in patients with cirrhosis of the liver and hepatocellular carcinoma. Cancer Detect Prev 2003; 27: 494-7.
95. Dasani BM, Sigal SH, Lieber CS. Analysis of risk factors for chronic hepatic encephalopathy: the role of Helicobacter pylori infection. Am J Gastroenterol 1998; 93: 726-31.
96. Chen SJ, Wang LJ, Zhu Q, Cai JT, Chen T, Si JM. Effect of H pylori infection and its eradication on hyperammo-nemia and hepatic encephalopathy in cirrhotic patients. World J Gastroenterol 2008; 14: 1914-8.
97. Miquel J, Barcena R, Boixeda D etal. Role of Helicobacter pylori infection and its eradication in patients with subclinical hepatic encephalopathy. Eur J Gastroenterol Hepatol 2001; 13: 1067-72.
98. Huber M, Rössle M, Siegerstetter V etal. Helicobacter pylori infection does not correlate with plasma ammonia concentration and hepatic encephalopathy in patients with cirrhosis. Hepatogastroenterology 2001; 48: 541-4.
99. Zullo A, Rinaldi V, Meddi P, Hassan C, Winn S, Attili AF. Helicobacter pylori infection, plasma ammonia levels, and psychometric testing in cirrhotic patients. Am J Gastroenterol 1999; 94: 2214-8.