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doi:10.1111/jgh.12617

GASTROENTEROLOGY

Gastric Helicobacter pylori infection associated with risk of diabetes mellitus, but not prediabetes Gi-Hua Yang,* Jin-Shang Wu,*,† Yi-Ching Yang,*,† Ying-Hsiang Huang,* Feng-Hwa Lu*,† and Chih-Jen Chang*,† *Department of Family Medicine, National Cheng Kung University Hospital, and †Department of Family Medicine, College of Medicine, National Cheng Kung University, Tainan, Taiwan

Key words diabetes mellitus, Helicobacter pylori, prediabetic state. Accepted for publication 29 March 2014. Correspondence Chih-Jen Chang, Department of Family Medicine, National Cheng Kung University Hospital, 138, Sheng Li Road, Tainan 70403, Taiwan. Email: [email protected] Conflict of interest: The authors declare that there are no conflicts of interest.

Abstract Backgrounds and Aim: The association between Helicobacter pylori infection and diabetes was inconsistent in previous studies. Moreover, there are no studies on the relationship between H. pylori infection and prediabetes in the literature. The aim of this study is thus to assess the association of Helicobacter infection, diagnosed by pathology from gastric biopsy, with diabetes and prediabetes. Methods: This cross-sectional study included 1285 subjects aged 19–85 who underwent esophagogastroduodenoscopy and gastric biopsy during health examinations at National Cheng Kung University Hospital from 2000 to 2009. Subjects were divided into three groups, including normal glucose tolerance, prediabetes, and diabetes. Diabetes and prediabetes were assessed according to the American Diabetes Association diagnostic criteria. Gastric Helicobacter infection was an independent variable. Chi-square tests, analysis of variance, and multinomial logistic regression models were used to analyze the effects of Helicobacter infection on the risk of diabetes and prediabetes while controlling for age, lifestyle, pathological conditions, and laboratory variables. Results: There were significant differences in the prevalence of gastric Helicobacter infection among the three groups. The results of multivariate analysis showed that age, obesity, family history of diabetes, hypertension, and hypertriglyceridemia were significantly related to both prediabetes and diabetes. Helicobacter pylori infection was positively associated with diabetes (odds ratio [OR] 1.42, 95% confidence interval [CI] 1.01– 2.01), but not prediabetes (OR 1.02, 95% CI 0.77–1.36), in addition to male gender, education level (≤ 9 vs > 12 years), pre-hypertension, and low high-density lipoprotein cholesterol. Conclusions: Gastric H. pylori infection is associated with diabetes, but not prediabetes.

Introduction The incidence of diabetes mellitus is rising globally, with the condition being more prevalent among the poor.1 Smoking, physical inactivity, and poor food quality have been shown to contribute to the low socioeconomic status–diabetes relationship, but they provided only partial explanations for this,2 and chronic infections, which have higher prevalence in such populations, may be another contributing factor. Previous studies3,4 revealed that seropositivity of Helicobacter pylori, cytomegalovirus, herpes simplex virus and Chlamydia pneumoniae are associated with cardiovascular disease and metabolic syndrome. A more recent study5 found that H. pylori infection plays a role in extra-gastric diseases, including cardiometabolic disorders, hematologic disorders, neurologic diseases, and hepatobiliary diseases. 1794

Although some studies demonstrated a higher risk of H. pylori infection in diabetic subjects than non-diabetic ones,6–9 others found an insignificant10–14 and even reverse association between H. pylori infection and diabetes.15,16 These inconsistent results may be related to the relatively small sample size used in some studies, the presence of confounding factors, and different diagnostic methods of H. pylori infection, such as histology, rapid urease tests, 13C urea breath tests, stool antigen tests, or serological approaches. Because serological tests for the H. pylori IgG antibody resulted in a false positive rate of 32% in a native Alaskan population,17 gastric biopsy and histology were used as diagnostic methods for H. pylori infection in the current study. Furthermore, the literature contains no studies on the relationship between H. pylori infection and prediabetes. The aim of this study was thus to investigate the association of H. pylori infection, as revealed by

Journal of Gastroenterology and Hepatology 29 (2014) 1794–1799 © 2014 Journal of Gastroenterology and Hepatology Foundation and Wiley Publishing Asia Pty Ltd

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pathology from gastric biopsy, with diabetes and prediabetes in a Taiwanese population.

Methods The Human Experiment and Ethics Committee of National Cheng Kung University Medical Center approved the study, which was conducted in accordance with the Helsinki human investigations guidelines. From January 2000 to August 2009, 19 694 participants were enrolled during health examinations. All subjects completed a structured questionnaire, which included demographic information, year of education, lifestyle habits, medical or surgical history, medication history, and family history of type 2 diabetes mellitus in first or second-degree relatives.18 The education level was divided into ≤ 9, > 9–≤ 12, and > 12 years. Current smoking was defined as at least 20 cigarettes per month for more than 6 months. Regular exercise was defined as a minimum of 20 min at least three times per week. Oral contraceptive pill use was defined as previous use for at least 1 month at any time in their lives. Hormone replacement therapy was defined as previous oral medication or injection for at least 1 month. All participants underwent body weight, body height, and blood pressure measurements by well-trained nurses. Body weight (to the nearest 0.1 kg) and height (to the nearest 0.1 cm) were measured using a certified machine, when subjects wore light clothing and without shoes. The body mass index (BMI) was calculated by the formula of body weight (kg)/body height squared (m2). Obesity was defined as BMI ≥ 27 kg/m2 according to the criteria used by the Department of Health, Executive Yuan, Taiwan. Right brachial artery blood pressure was measured using a blood pressure monitor (model 1846SX; Critikon Inc., Irvine, CA, USA) with the subjects in a supine position and after at least 15 min of rest. Hypertension was defined as systolic blood pressure (SBP) ≥ 140 mmHg, diastolic blood pressure (DBP) ≥ 90 mmHg or a positive hypertension history. Pre-hypertension was defined as SBP of 120–139 mmHg or DBP of 80–89 mmHg without a history of hypertension. Normal blood pressure was defined as SBP < 120 mmHg and DBP < 80 mmHg without a history of hypertension. Various forms of examination, including esophagogastroduodenoscopy (EGD), fasting plasma glucose (FPG), post-load 2-h glucose (2 h-PG), creatinine, C-reactive protein (CRP), triglyceride (TG), high-density lipoprotein cholesterol (HDL-C), and antihepatitis C virus antibody were performed. EGD was performed by experienced gastroenterologists using LUCERA gastroscopes (GIF-XQ260; Olympus, Tokyo, Japan). Biopsy and histopathology were performed on 1866 out of 11 653 subjects who underwent EGD. H. pylori infection was defined as H. pylori present in samples of gastric biopsy. Finally, 1285 subjects were available for analysis after the following exclusion criteria were applied: age < 18 years old, past history of type 1 diabetes mellitus, biopsy of esophagus or duodenum, endoscopic diagnosis of cancer proven by histopathological examination, prior upper gastrointestinal tract surgery, prior Helicobacter eradication therapy, use of nonsteroid anti-inflammatory drugs, and incomplete data. A standard 75-gram oral glucose tolerance test was performed in subjects without pregnancy or a history of diabetes. FPG and 2 h-PG were measured by a hexokinase method (Roche Diagnostic GmbH, Mannheim, Germany). The intra-assay and inter-

Helicobacter, diabetes, and prediabetes

assay coefficients of variation were 1.5% and 1.7%, respectively. Diabetes mellitus was defined as FPG ≥ 7.0 mmol/L, 2 hPG ≥ 11.1 mmol/L, or a positive history of type 2 diabetes mellitus. Prediabetes was defined as FPG of 5.6–6.9 mmol/L or 2 h-PG of 7.8–11.0 mmol/L without a history of diabetes. Normal blood glucose was defined as FPG < 5.6 mmol/L and 2 hPG < 7.8 mmol/L without a history of diabetes. Serum TG and HDL-C levels were determined in the central laboratory of National Cheng Kung University Hospital with an autoanalyzer (Hitachi 747E; Hitachi, Tokyo, Japan). Hypertriglyceridemia was defined as TG > 1.69 mmol/L. Low HDL-C was defined as < 1.03 mmol/L in men or < 1.29 mmol/L in women. CRP level was determined via VITROS 5.1 FS Chemistry System (Johnson & Johnson, Raritan, New Jersey, USA). CRP was divided into ≤ 8 mg/L and > 8 mgl/L according to the criteria used by the central laboratory of National Cheng Kung University Hospital. Anti-hepatitis C virus antibody was measured with chemiluminescence microparticle immunoassay (Architect i2000, Abbott Laboratories. Abbott Park, Illinois, USA). Hepatitis C infection was defined as signal-to-cut-off ratio ≥ 1. Statistical analysis was performed using the Windows version of the Statistical Package for the Social Sciences software (SPSS, version 17.0; Chicago, Illinois, USA). Continuous variables were summarized as mean ± standard deviation and categorical variables using number (percentage). Continuous variables among subjects with normal blood glucose, prediabetes and diabetes were compared using anova. Categorical variables among groups were compared using chi-square tests. Multinomial logistic regression models were used for analyzing the relationship between different glycemic statuses and H. pylori infection with adjustment for the following variables: age, male gender, education level (≤ 9 years vs > 12 years, 9–12 years vs > 12 years), family history of type 2 diabetes mellitus, obesity, current smoking, regular exercise, oral contraceptive pill use, hormone replacement therapy, blood pressure status (hypertension vs normal blood pressure, prehypertension vs normal blood pressure), hypertriglyceridemia, low HDL-C, CRP > 8 mg/L, creatinine and hepatitis C infection.

Results Diabetes was diagnosed in 238 (18.5%) and prediabetes in 318 (24.7%) of the 1285 subjects. Table 1 shows that there were significant differences in age, gender, education level, and the prevalence of hypertension, prehypertension, H. pylori infection, hepatitis C infection, hypertriglyceridemia, low HDL-C, CRP > 8 mg/L, and family history of type 2 diabetes mellitus among subjects with normal blood glucose, prediabetes, and diabetes. Based on the multinomial logistic regression, Table 2 reveals the adjusted ORs and 95% CIs of the clinical variables with the regards to the risk of diabetes and prediabetes. Age, obesity, family history of type 2 diabetes mellitus, hypertension, and hypertriglyceridemia were significantly related to both prediabetes and diabetes, after adjusting for current smoking, regular exercise, oral contraceptive pill use, hormone replacement therapy, CRP > 8 mg/L, creatinine, and hepatitis C infection. In addition, male gender, education level (≤ 9 vs > 12 years), prehypertension, low HDL-C, and H. pylori infection (diabetes: OR 1.42, 95% CI

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Table 1

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Clinical characteristics of subjects with normal blood glucose, prediabetes, and diabetes

Age (year) Male gender Education level > 12 years 9∼12 years ≤ 9 years Family history of type 2 DM Body weight (kg) Body height (cm) Body mass index (kg/m2) Obesity Current smoker Regular exercise Oral contraceptive pill use Hormone replacement therapy Blood pressure status Hypertension Prehypertension Normal blood pressure Helicobacter pylori infection Hypertriglyceridemia Low high-density lipoprotein cholesterol C-reactive protein > 8 mg/L Creatinine (μmol/L) Hepatitis C infection

Normal (n = 729)

Pre-DM (n = 318)

DM (n = 238)

P-value

50.3 ± 11.1 415 (56.9)

54.2 ± 10.1 202 (63.5)

59.6 ± 10.0 171 (71.8)

< 0.001 < 0.001* < 0.001*

355 (47.8) 177 (24.3) 197 (27.0) 122 (16.7) 50.3 ± 11.2 163.5 ± 8.4 24.2 ± 3.3 142 (19.5) 103 (14.1) 66 (9.1) 21 (2.9) 26 (3.6)

149 (46.9) 63 (19.8) 106 (33.3) 68 (21.7) 54.2 ± 10.1 163.3 ± 8.2 25.9 ± 3.8 114 (35.8) 46 (14.5) 28 (8.8) 8 (2.5) 7 (2.2)

78 (32.8) 42 (17.6) 118 (49.6) 64 (26.9) 59.6 ± 10.0 162.8 ± 8.0 26.3 ± 3.8 92 (38.7) 36 (15.1) 21 (8.8) 2 (0.8) 5 (2.1)

289 (39.6) 29 (4.0) 411 (56.4) 358 (49.1) 169 (23.2) 272 (37.3) 39 (5.3) 65.6 ± 14.5 29 (4.0)

180 (56.6) 22 (6.9) 116 (36.5) 165 (51.9) 127 (39.9) 157 (49.4) 23 (7.2) 70.2 ± 27.5 18 (5.7)

153 (64.3) 29 (12.2) 56 (23.5) 147 (61.8) 101 (42.4) 132 (55.5) 25 (10.5) 74.0 ± 35.1 24 (10.1)

< 0.001* < 0.001 0.498 < 0.001 < 0.001* 0.707 0.894 0.095 0.171 < 0.001*

0.001* < 0.001* < 0.001* 0.006* < 0.001 0.001*

Data are expressed as mean ± SD or number (%). *P for trend. DM, diabetes mellitus.

Table 2 The adjusted odds ratios (OR) and 95% confidence intervals (CI) of the clinical variables on the risk of diabetes and prediabetes based on multinomial logistic regression Variables

Age (year) Gender (male vs female) Education level Education ≤ 9 years versus > 12 years Education 9–12 years versus > 12 years Family history of type 2 diabetes mellitus (yes vs no) Obesity (yes vs no) Current smoker (yes vs no) Regular exercise (yes vs no) Oral contraceptive pill use (yes vs no) Hormone replacement therapy (yes vs no) Blood pressure status Hypertension versus normal blood pressure Prehypertension versus normal blood pressure Helicobacter pylori infection (yes vs no) Hypertriglyceridemia (yes vs no) Low high density lipoprotein cholesterol (yes vs no) C-reactive protein > 8 mg/L (yes vs no) Creatinine (μmol/L) Hepatitis C infection (yes vs no)

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Prediabetes

Diabetes

OR (95% CI)

P value

OR (95% CI)

P-value

1.04 (1.02–1.05) 0.95 (0.66–1.37)

< 0.001 0.783

1.08 (1.06–1.10) 1.66 (1.07–2.56)

< 0.001 0.024

0.92 (0.64–1.32) 0.80 (0.56–1.60) 1.55 (1.09–2.21) 2.02 (1.47–2.77) 0.96 (0.63–1.45) 1.00 (0.61–1.64) 1.37 (0.53–3.51) 0.44 (0.17–1.13)

0.666 0.803 0.015 < 0.001 0.841 0.996 0.516 0.088

1.55 (1.02–2.36) 1.00 (0.63–1.60) 2.76 (1.84–4.15) 2.27 (1.57–3.28) 0.89 (0.54–1.44) 1.08 (0.60–1.91) 0.58 (0.11–3.03) 0.56 (0.18–1.71)

0.042 0.986 < 0.001 < 0.001 0.627 0.807 0.521 0.305

1.54 (1.13–2.09) 1.67 (0.89–3.14) 1.02 (0.77–1.36) 1.83 (1.33–2.53) 1.23 (0.91–1.66) 1.17 (0.66–2.06) 1.43 (0.79–2.59) 1.29 (0.68–2.43)

0.006 0.111 0.892 < 0.001 0.176 0.596 0.238 0.441

1.94 (1.32–2.85) 2.72 (1.41–5.24) 1.42 (1.01–2.01) 1.97 (1.36–2.87) 1.52 (1.06–2.17) 1.45 (0.79–2.67) 1.46 (0.79–2.70) 1.83 (0.96–3.46)

0.001 0.003 0.045 < 0.001 0.022 0.234 0.225 0.065

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1.01–2.01; prediabetes: OR 1.02, 95% CI 0.77–1.36) were positively associated with diabetes, but not prediabetes.

Discussion In this cross-sectional study, the associations among gastric H. pylori infection, diabetes, and prediabetes were examined in a large sample of adult participants in a health examination center in Taiwan. Our results revealed that H. pylori infection was associated with an increased risk of diabetes mellitus in addition to male gender, low education level (< 9 years), pre-hypertension, and low HDL-C. Our findings are in accord with the results from some previous studies,6–8 which revealed a higher prevalence of H. pylori infection in diabetic rather than nondiabetic participants. However, other studies revealed an insignificant10–14 and even reverse association between H. pylori infection and diabetes.15,16 A prospective cohort study also showed an increased rate of diabetes in the elderly with H. pylori infection.9 To the best of our knowledge, this is the first study to investigate the association between H. pylori infection and prediabetes. However, no significant effects of H. pylori infection were found with regard to the risk of prediabetes, after carefully adjusting for current smoking, regular exercise, oral contraceptive pill use, hormone replacement therapy, CRP > 8.0 mg/L, creatinine, and hepatitis C infection. In addition, based on ordinal logistic regression analysis, the trend for the effect of H. pylori infection on diabetes/ prediabetes was not significant (data not shown), and it may infer the existence of a threshold effect between H. pylori infection and hyperglycemia. The mechanisms for the positive association between type 2 diabetes mellitus and H. pylori infection may involve inflammation and decreased ghrelin levels. Gut Gram-negative bacteria, such as H. pylori, has lipopolysaccharide which activates innate inflammatory processes.19 Inflammation inhibits downstream signaling of the insulin receptor, and may lead to insulin resistance.20 Meanwhile, a systemic review21 showed lower circulating ghrelin levels in H. pylori infected people, and a cohort study also revealed that ghrelin levels were negatively associated with type 2 diabetes mellitus.22 However, further investigations are needed to uncover the mechanisms underlying the association between H. pylori infection and diabetes mellitus. As for the relation between H. pylori infection and prediabetes, no significant association was found in the current study. One earlier work showed that prediabetes was not significantly associated with CRP levels after adjustment for age, gender, and BMI,23 although elevated serum CRP levels were found to be associated with prediabetes in another study.24 A case-control study revealed no difference in ghrelin levels between subjects with and without impaired glucose tolerance.25 Furthermore, ghrelin was not associated with the risk of impaired glucose tolerance after adjusting for age, sex, and a homeostasis assessment for insulin resistance and BMI in another prospective study.26 These earlier findings may partially explain the insignificant relationship that was found in this work between H. pylori infection and prediabetes, but other mechanisms need further clarification. In this study, hypertension was significantly associated with prediabetes and diabetes mellitus. Previous cohort studies showed that type 2 diabetes mellitus was 2.5 times more likely to occur in subjects with hypertension than in subjects with normal blood

Helicobacter, diabetes, and prediabetes

pressure,27 and hypertensive subjects had a higher prevalence of impaired fasting glucose than the normotensive population in rural China.28 Another cohort of German subjects that had a follow-up period of 12.5 years revealed a 1.8-fold higher incidence of diabetes mellitus in men with prehypertension.29 In this study, prehypertension was significantly associated with type 2 diabetes mellitus, but not prediabetes. Because elevated blood pressure could be a marker for underlying insulin resistance,30 different degrees of insulin resistance between subjects with diabetes and prediabetes31 may be a partial explanation for the different associations with pre-hypertension. Hypertriglyceridemia, low HDL-C, increased age, family history of type 2 diabetes mellitus, and obesity were all associated with diabetes in our study, which is consistent with the literature.18,32,33 In this work, male gender was associated with diabetes, as in a previous epidemiologic study carried out in southern Taiwan.34 However, the ratio of the prevalence of diabetes in males compared to females varies markedly between populations.35 In the current study, hypertriglyceridemia, obesity, family history of type 2 diabetes mellitus, and increased age were all associated with prediabetes. The reason for this might be prediabetes is due to insulin resistance or insufficient insulin secretion, and may share the same risk factors as type 2 diabetes mellitus.18,36,37 Regular exercise was not associated with the risk of type 2 diabetes mellitus in our study, which may be because some subjects with hyperglycemia may change their lifestyles leading to an underestimation of the relationship between regular exercise and hyperglycemia. Based on the result of univariate analysis, our study showed a trend of an increasing prevalence of hepatitis C infection and CRP, based on the degrees of glycemic status. However, the trend became insignificant after adjustment for other clinical factors, and may be due to collinearity with other clinical variables. This study has several limitations. First, it is a cross-sectional observational study which does not allow for causal inferences. Second, there are a variety of methods for diagnosis of H. pylori infection, but there is no single test that can be considered the gold standard.38 However, with properly trained personnel, histopathology detects current H. pylori infection and has greater sensitivity and specificity than serological tests.38 In contrast, serological tests have lower accuracy resulting in a misclassification for detecting current H. pylori infection and therefore inconsistent findings for the relationship between H. pylori infection and DM in previous studies.6–16 In addition, H. pylori infection usually started in childhood, and their serological tests may remain positive even 4 years after successful treatment. Thus, serological tests may not represent current infection status.39 The urea breath test provides a reliable means of identifying active H. pylori infection, but colonization of ureasepositive non-H. pylori bacteria and gastric hypochlorhydric conditions may induce a false-positive result.40 Third, we did not repeat the tests of fasting plasma glucose or oral glucose tolerance tests, which may result in more cases and proportions of prediabetes or diabetes. In conclusion, gastric H. pylori infection was associated with type 2 diabetes mellitus, but not prediabetes in a Taiwanese population. Further prospective studies are warranted to explore whether any causative relation exits between gastric H. pylori infection and diabetes mellitus.

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Acknowledgment This study was funded by the Department of Family Medicine, National Cheng Kung University Hospital, Taiwan (NCKUHFM101-002).

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Journal of Gastroenterology and Hepatology 29 (2014) 1794–1799 © 2014 Journal of Gastroenterology and Hepatology Foundation and Wiley Publishing Asia Pty Ltd

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Gastric Helicobacter pylori infection associated with risk of diabetes mellitus, but not prediabetes.

The association between Helicobacter pylori infection and diabetes was inconsistent in previous studies. Moreover, there are no studies on the relatio...
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