Is Helicobacter pylori infection associated with glycemic control in diabetics?

World Journal of Gastroenterology

Volumn 21, Issue 17, 2015, Pages 5407-5416

  Dai, Yi Ning ^a   Yu, Wei Lai ^a   Zhu, Hua Tuo ^a   Ding, Jie Xia ^a   Yu, Chao Hui ^a   Li, You Ming ^a  

^a ZHEJIANG UNIVERSITY   (China)

Author keywords

Diabetes mellitus; Eradication; Glycemic control; Helicobacter pylori; Meta analysis; Reinfection

Indexed keywords

AMOXICILLIN; AZITHROMYCIN; BISMUTH CITRATE; C PEPTIDE; CLARITHROMYCIN; GLUCOSE; GLYCOSYLATED HEMOGLOBIN; HEMOGLOBIN A1C; INSULIN; METRONIDAZOLE; OMEPRAZOLE; ANTIDIABETIC AGENT; ANTIINFECTIVE AGENT; BIOLOGICAL MARKER; GLUCOSE BLOOD LEVEL; HEMOGLOBIN A1C PROTEIN, HUMAN; PROTON PUMP INHIBITOR;

ARTICLE; BACTERIAL CLEARANCE; COHORT ANALYSIS; DIABETES MELLITUS; DISEASE ASSOCIATION; DISEASE DURATION; ERADICATION THERAPY; FOLLOW UP; GASTROINTESTINAL SYMPTOM; GLUCOSE BLOOD LEVEL; GLYCEMIC CONTROL; HELICOBACTER INFECTION; HEMOGLOBIN BLOOD LEVEL; HUMAN; INSULIN BLOOD LEVEL; INSULIN DEPENDENT DIABETES MELLITUS; META ANALYSIS; NON INSULIN DEPENDENT DIABETES MELLITUS; OBSERVATIONAL STUDY; PROTEIN BLOOD LEVEL; RANDOMIZED CONTROLLED TRIAL (TOPIC); REINFECTION; SCORING SYSTEM; SYSTEMATIC REVIEW; TREATMENT OUTCOME; TREATMENT RESPONSE; ADOLESCENT; ADULT; BLOOD; CHI SQUARE DISTRIBUTION; CHILD; COMBINATION DRUG THERAPY; DIABETES MELLITUS, TYPE 1; DIABETES MELLITUS, TYPE 2; DRUG EFFECTS; FEMALE; HELICOBACTER INFECTIONS; HELICOBACTER PYLORI; MALE; METABOLISM; MICROBIOLOGY; MIDDLE AGED; ODDS RATIO; PATHOGENICITY; RISK FACTOR;

ADOLESCENT; ADULT; ANTI-BACTERIAL AGENTS; BIOMARKERS; BLOOD GLUCOSE; CHI-SQUARE DISTRIBUTION; CHILD; DIABETES MELLITUS, TYPE 1; DIABETES MELLITUS, TYPE 2; DRUG THERAPY, COMBINATION; FEMALE; HELICOBACTER INFECTIONS; HELICOBACTER PYLORI; HEMOGLOBIN A, GLYCOSYLATED; HUMANS; HYPOGLYCEMIC AGENTS; MALE; MIDDLE AGED; ODDS RATIO; PROTON PUMP INHIBITORS; RISK FACTORS; TREATMENT OUTCOME;

EID: 84929001355     PISSN: 10079327     EISSN: 22192840     Source Type: Journal    
DOI: 10.3748/wjg.v21.i17.5407     Document Type: Article

References (51)

1. Marshall BJ, Warren JR. Unidentified curved bacilli in the stomach of patients with gastritis and peptic ulceration. Lancet 1984; 1: 1311-1315 [PMID: 6145023 DOI: 10.1016/S0140-6736(84)91816-6]
2. Suerbaum S, Michetti P. Helicobacter pylori infection. N Engl J Med 2002; 347: 1175-1186 [PMID: 12374879 DOI: 10.1056/NEJMra020542]
3. Peek RM, Blaser MJ. Helicobacter pylori and gastrointestinal tract adenocarcinomas. Nat Rev Cancer 2002; 2: 28-37 [PMID: 11902583 DOI: 10.1038/nrc703]
4. Malfertheiner P, Megraud F, O'Morain CA, Atherton J, Axon AT, Bazzoli F, Gensini GF, Gisbert JP, Graham DY, Rokkas T, El-Omar EM, Kuipers EJ. Management of Helicobacter pylori infection - the Maastricht IV/Florence Consensus Report. Gut 2012; 61: 646-664 [PMID: 22491499 DOI: 10.1136/gutjnl-2012-302084]
5. Moyaert H, Franceschi F, Roccarina D, Ducatelle R, Haesebrouck F, Gasbarrini A. Extragastric manifestations of Helicobacter pylori infection: other Helicobacters. Helicobacter 2008; 13 Suppl 1: 47-57 [PMID: 18783522 DOI: 10.1111/j.1523-5378.2008.00634.x]
6. Shin DW, Kwon HT, Kang JM, Park JH, Choi HC, Park MS, Park SM, Son KY, Cho B. Association between metabolic syndrome and Helicobacter pylori infection diagnosed by histologic status and serological status. J Clin Gastroenterol 2012; 46: 840-845 [PMID: 23064216 DOI: 10.1097/MCG.0b013e3182522477]
7. Roubaud Baudron C, Franceschi F, Salles N, Gasbarrini A. Extragastric diseases and Helicobacter pylori. Helicobacter 2013; 18 Suppl 1: 44-51 [PMID: 24011245 DOI: 10.1111/hel.12077]
8. Albaker WI. Helicobacter pylori infection and its relationship to metabolic syndrome: is it a myth or fact? Saudi J Gastroenterol 2011; 17: 165-169 [PMID: 21546717]
9. Li M, Shen Z, Li YM. Potential role of Helicobacter pylori infection in nonalcoholic fatty liver disease. World J Gastroenterol 2013; 19: 7024-7031 [PMID: 24222944 DOI: 10.3748/wjg.v19.i41.7024]
10. Zhou X, Zhang C, Wu J, Zhang G. Association between Helicobacter pylori infection and diabetes mellitus: a meta-analysis of observational studies. Diabetes Res Clin Pract 2013; 99: 200-208 [PMID: 23395214 DOI: 10.1016/j.diabres.2012.11.012]
11. Jeon CY, Haan MN, Cheng C, Clayton ER, Mayeda ER, Miller JW, Aiello AE. Helicobacter pylori infection is associated with an increased rate of diabetes. Diabetes Care 2012; 35: 520-525 [PMID: 22279028 DOI: 10.2337/dc11-1043]
12. Ojetti V, Pellicano R, Fagoonee S, Migneco A, Berrutti M, Gasbarrini A. Helicobacter pylori infection and diabetes. Minerva Med 2010; 101: 115-119 [PMID: 20467410]
13. Marietti M, Gasbarrini A, Saracco G, Pellicano R. Helicobacter pylori infection and diabetes mellitus: the 2013 state of art. Panminerva Med 2013; 55: 277-281 [PMID: 24088801]
14. Ojetti V, Pitocco D, Ghirlanda G, Gasbarrini G, Gasbarrini A. [Role of Helicobacter pylori infection in insulin-dependent diabetes mellitus]. Minerva Med 2001; 92: 137-144 [PMID: 11404721]
15. Gasbarrini A, Ojetti V, Pitocco D, Franceschi F, Candelli M, Torre ES, Gabrielli M, Cammarota G, Armuzzi A, Pola R, Pola P, Ghirlanda G, Gasbarrini G. Insulin-dependent diabetes mellitus affects eradication rate of Helicobacter pylori infection. Eur J Gastroenterol Hepatol 1999; 11: 713-716 [PMID: 10445788]
16. Gasbarrini A, Ojetti V, Pitocco D, Armuzzi A, Silveri NG, Pola P, Ghirlanda G, Gasbarrini G. Efficacy of different Helicobacter pylori eradication regimens in patients affected by insulin-dependent diabetes mellitus. Scand J Gastroenterol 2000; 35: 260-263 [PMID: 10766318]
17. Candelli M, Rigante D, Schiavino A, Gabrielli M, Crea F, Minguell Del Lungo L, Pignataro G, Sacco E, Monaco S, Gentiloni Silveri N, Gasbarrini A. High reinfection rate of Helicobacter pylori in young type 1 diabetic patients: a three-year follow-up study. Eur Rev Med Pharmacol Sci 2012; 16: 1468-1472 [PMID: 23111958]
18. Ojetti V, Pitocco D, Bartolozzi F, Danese S, Migneco A, Lupascu A, Pola P, Ghirlanda G, Gasbarrini G, Gasbarrini A. High rate of helicobacter pylori re-infection in patients affected by type 1 diabetes. Diabetes Care 2002; 25: 1485 [PMID: 12145262]
19. Ojetti V, Migneco A, Nista EC, Gasbarrini G, Gasbarrini A, Pitocco D, Ghirlanda G. H pylori re-infection in type 1 diabetes: a 5 years follow-up. Dig Liver Dis 2007; 39: 286-287 [PMID: 17275424 DOI: 10.1016/j.dld.2006.11.008]
20. Chen Y, Blaser MJ. Association between gastric Helicobacter pylori colonization and glycated hemoglobin levels. J Infect Dis 2012; 205: 1195-1202 [PMID: 22427676 DOI: 10.1093/infdis/jis106]
21. Rostom A, Dubé C, Cranney A, Saloojee N, Sy R, Garritty C, Sampson M, Zhang L, Yazdi F, Mamaladze V, Pan I, McNeil J, Moher D, Mack D, Patel D. Celiac Disease. Rockville (MD): Agency for Healthcare Research and Quality (US); 2004 Sep. (Evidence Reports/Technology Assessments, No. 104.) Appendix D. Quality Assessment Forms. Available from: URL: http://www.ncbi.nlm.nih.gov/books/NBK35156/
22. Jadad AR, Moore RA, Carroll D, Jenkinson C, Reynolds DJ, Gavaghan DJ, McQuay HJ. Assessing the quality of reports of randomized clinical trials: is blinding necessary? Control Clin Trials 1996; 17: 1-12 [PMID: 8721797 DOI: 10.1016/0197-2456(95)00134-4]
23. Higgins JP, Thompson SG. Quantifying heterogeneity in a metaanalysis. Stat Med 2002; 21: 1539-1558 [PMID: 12111919 DOI: 10.1002/sim.1186]
24. Higgins JP, Thompson SG, Deeks JJ, Altman DG. Measuring inconsistency in meta-analyses. BMJ 2003; 327: 557-560 [PMID: 12958120 DOI: 10.1136/bmj.327.7414.557]
25. Thornton A, Lee P. Publication bias in meta-analysis: its causes and consequences. J Clin Epidemiol 2000; 53: 207-216 [PMID: 10729693 DOI: 10.1016/S0895-4356(99)00161-4]
26. Egger M, Davey Smith G, Schneider M, Minder C. Bias in metaanalysis detected by a simple, graphical test. BMJ 1997; 315: 629-634 [PMID: 9310563 DOI: 10.1136/bmj.315.7109.629]
27. Begg CB, Mazumdar M. Operating characteristics of a rank correlation test for publication bias. Biometrics 1994; 50: 1088-1101 [PMID: 7786990]
28. Arslan D, Kendirci M, Kurtoglu S, Kula M. Helicobacter pylori infection in children with insulin dependent diabetes mellitus. J Pediatr Endocrinol Metab 2000; 13: 553-556 [PMID: 10803874]
29. Ko GT, Chan FK, Chan WB, Sung JJ, Tsoi CL, To KF, Lai CW, Cockram CS. Helicobacter pylori infection in Chinese subjects with type 2 diabetes. Endocr Res 2001; 27: 171-177 [PMID: 11428708]
30. Jones KL, Wishart JM, Berry M, Russo A, Xia HH, Talley NJ, Horowitz M. Helicobacter pylori infection is not associated with delayed gastric emptying or upper gastrointestinal symptoms in diabetes mellitus. Dig Dis Sci 2002; 47: 704-709 [PMID: 11991596]
31. Candelli M, Rigante D, Marietti G, Nista EC, Crea F, Bartolozzi F, Schiavino A, Pignataro G, Silveri NG, Gasbarrini G, Gasbarrini A. Helicobacter pylori, gastrointestinal symptoms, and metabolic control in young type 1 diabetes mellitus patients. Pediatrics 2003; 111: 800-803 [PMID: 12671115]
32. Wang YJ, Zhang X, Yang Y. The study of Helicobacter pylori infection in patients with type 2 diabetes mellitus. Zhonghua Zhongxiyi Zazhi 2003; 4: 2856-2857
33. Candelli M, Rigante D, Marietti G, Nista EC, Crea F, Schiavino A, Cammarota G, Pignataro G, Petrucci S, Gasbarrini G, Gasbarrini A. Helicobacter pylori eradication rate and glycemic control in young patients with type 1 diabetes. J Pediatr Gastroenterol Nutr 2004; 38: 422-425 [PMID: 15085021]
34. Toporowska-Kowalska E, Wasowska-Królikowska K, Szadkowska A, Bodalski J. [Helicobacter pylori infection and its metabolic consequences in children and adolescents with type 1 diabetes mellitus]. Med Wieku Rozwoj 2007; 11: 103-108 [PMID: 17625277]
35. Demir M, Gokturk HS, Ozturk NA, Kulaksizoglu M, Serin E, Yilmaz U. Helicobacter pylori prevalence in diabetes mellitus patients with dyspeptic symptoms and its relationship to glycemic control and late complications. Dig Dis Sci 2008; 53: 2646-2649 [PMID: 18320319 DOI: 10.1007/s10620-007-0185-7]
36. Zhou HC, Zhou L, Chen XQ. Influence of Helicobacter pylori infection on insulin resistance in diabetic patient. Guiyang Yixueyuan xuebao 2012; 37: 131-133
37. Peng WP, Wu CS, Ye XL. Clinical study on relationship between Helicobacter pylori infection and type 2 diabetes complications. Zhongguo Yishijinxiu Zazhi 2013; 36: 26-28
38. Agrawal RP, Sharma R, Garg D, Pokharna R, Kochar DK, Kothari RP. Role of Helicobacter pylori in causation of diabetic gastropathies and non-gastrointestinal complications in type 2 diabetes. J Indian Med Assoc 2010; 108: 140-143 [PMID: 21043350]
39. Wei AF. Helicobacter pylori infection and related risk factors in type 2 diabetes research. Zhongguo Shiyong Yiyao 2012; 7: 34-35
40. Lu SC, Yan HJ, Wu BY, Chen L, Zhang Y. HP infection and insulin, C peptic secretion of type 1 diabetes. Medical Research and Education 2010; 27: 26-34
41. Moghimi J, Toussy J, Babaei M, Mousavi S, Tamadon M, Karamai M. Effect of Helicobacter pylori eradication on short-term control of glycemia in patients with type 2 diabetes mellitus. Saudi Med J 2007; 28: 475-476 [PMID: 17334489]
42. Vafaeimanesh J, Rajabzadeh R, Ahmadi A, Moshtaghi M, Banikarim S, Hajiebrahimi S, Seyyedmajidi M. Effect of Helicobacter pylori eradication on glycaemia control in patients with type 2 diabetes mellitus and comparison of two therapeutic regimens. Arab J Gastroenterol 2013; 14: 55-58 [PMID: 23820501 DOI: 10.1016/j.ajg.2013.03.002]
43. de Luis DA, Cordero JM, Caballero C, Boixeda D, Aller R, Cantón R, de la Calle H. Effect of the treatment of Helicobacter pylori infection on gastric emptying and its influence on the glycaemic control in type 1 diabetes mellitus. Diabetes Res Clin Pract 2001; 52: 1-9 [PMID: 11182211]
44. Khalil T, Dorchy H, Scaillon M, Melot C. [Helicobacter pylori infection and eradication are not related to glycosylated hemoglobin levels (HbA1c) in young patients with type 1 diabetes]. Presse Med 2007; 36: 1191-1195 [PMID: 17360147 DOI: 10.1016/j.lpm.2006.12.030]
45. Wada Y, Hamamoto Y, Kawasaki Y, Honjo S, Fujimoto K, Tatsuoka H, Matsuoka A, Ikeda H, Fujikawa J, Koshiyama H. The Eradication of Helicobacter pylori does not Affect Glycemic Control in Japanese Subjects with Type 2 Diabetes. Jpn Clin Med 2013; 4: 41-43 [PMID: 23966817 DOI: 10.4137/JCM.S10828]
46. Horikawa C, Kodama S, Fujihara K, Yachi Y, Tanaka S, Suzuki A, Hanyu O, Shimano H, Sone H. Association of Helicobacter pylori infection with glycemic control in patients with diabetes: a metaanalysis. J Diabetes Res 2014; 2014: 250620 [PMID: 24901007 DOI: 10.1155/2014/250620]
47. Ram M, Barzilai O, Shapira Y, Anaya JM, 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; 51: 1075-1082 [PMID: 23079514 DOI: 10.1515/cclm-2012-0477]
48. Polyzos SA, Kountouras J, Zavos C, Deretzi G. The association between Helicobacter pylori infection and insulin resistance: a systematic review. Helicobacter 2011; 16: 79-88 [PMID: 21435084 DOI: 10.1111/j.1523-5378.2011.00822.x]
49. Ibrahim A, Zaher T, Ghonemy TA, El-Azim SA, El-Azim MA, Ramadan A. Impact of cytotoxin-associated gene A of Helicobacter pylori strains on microalbuminuria in type 2 diabetes. Saudi J Kidney Dis Transpl 2010; 21: 694-700 [PMID: 20587874]
50. Khamaisi M, Leitersdorf E. Severe hypoglycemia from clarithromycin-repaglinide drug interaction. Pharmacotherapy 2008; 28: 682-684 [PMID: 18447665 DOI: 10.1592/phco.28.5.682]
51. Otsuka SH. Severe hypoglycemia from Helicobacter pylori tripledrug therapy and insulin detemir drug interaction. Pharmacotherapy 2013; 33: e45-e49 [PMID: 23471710 DOI: 10.1002/phar.1228]