Helicobacter ISSN 1523-5378 doi: 10.1111/hel.12153

Prevalence of Helicobacter pylori Infection and its Relation with Body Mass Index in a Chinese Population Chengfu Xu,*,†,‡,1 Ming Yan,†,‡,1 Yan Sun,†,‡ Jungsoo Joo,†,‡ Xingyong Wan,* Chaohui Yu,* Qunyan Wang,* Chao Shen,§ Peng Chen,§ Youming Li* and William G. Coleman Jr† *Department of Gastroenterology, the First Affiliated Hospital, College of Medicine, Zhejiang University, Hangzhou, China, †Cancer Cluster, National Institute on Minority Health and Health Disparities, National Institutes of Health, Bethesda, MD, USA, ‡Laboratory of Biochemistry and Genetics, National Institute of Diabetes and Digestive and Kidney Diseases, National Institutes of Health, Bethesda, MD, USA, §International Health Care Center, the First Affiliated Hospital, College of Medicine, Zhejiang University, Hangzhou, China

Keywords Helicobacter pylori, prevalence, body mass index. Reprint requests to: Youming Li, Department of Gastroenterology, the First Affiliated Hospital, College of Medicine, Zhejiang University, 79 Qingchun Road, Hangzhou 310003, China. E-mail: [email protected] or William G. Coleman Jr., Cancer Cluster, National Institute on Minority Health and Health Disparities, National Institutes of Health, Bldg. 3, Room 5E08, 3 Center Drive, Bethesda, Maryland 20892, USA. E-mail: [email protected]. 1

These authors contributed equally to this work.

Abstract Background: Helicobacter pylori infection is highly prevalent worldwide. The association between obesity and H. pylori infection is controversial in the literature. This study aims to investigate the prevalence of H. pylori infection and its relation with body mass index (BMI) in a Chinese population. Materials and methods: A cross-sectional study was performed among adults who underwent health checkups at the First Affiliated Hospital, College of Medicine, Zhejiang University in 2013. The prevalence of H. pylori infection was examined by 13C urea breath tests, and the association between prevalence of H. pylori infection and BMI was analyzed. Results: Of the 8820 participants enrolled, 3859 (43.8%) were positive for H. pylori infection. H. pylori-positive participants had a more unfavorable metabolic profile than H. pylori-negative participants. Overweight/obese participants showed a higher prevalence of H. pylori infection than that of lean participants, and a positive linear correlation between BMI and prevalence of H. pylori infection was observed. Both unadjusted and adjusted analysis revealed that BMI was significantly associated with risk factors of H. pylori infection. Conclusions: Our results showed that BMI was significantly and positively associated with H. pylori infection, and a high BMI was associated with an increased risk of the infection.

Helicobacter pylori (H. pylori) is a gram-negative, spiralshaped pathogenic bacterium that infects approximately half of the world’s population [1]. Helicobacter pylori infection is a well-established risk factor for gastric diseases, for example chronic gastritis, peptic ulcer, gastric cancer, and mucosa-associated lymphoid tissue (MALT) lymphoma [2–4]. The role of H. pylori on extragastric diseases, such as cardiovascular, neurological, hematological, and metabolic diseases, has also been studied in recent years [5–7]. Factors associated with H. pylori infection have not been firmly established. Socioeconomic status is an important determinant that inversely correlates with H. pylori infection [8]. The prevalence of H. pylori infection has decreased significantly in developed countries such as the United States and those in Western Europe. Previous studies reported that the prevalence of

© 2014 John Wiley & Sons Ltd, Helicobacter 19: 437–442

H. pylori infection was higher than 60% in some parts of China [9,10]. With rapid economic growth and development in recent decades, it is not clear whether there has been a decline in H. pylori infection in China. However, with diverse regional economies in different geographic areas of China, we have an opportunity to assess regional prevalence of H. pylori infection in a natural experiment. A potential association between obesity and H. pylori infection has been proposed by recent studies. It was observed that obese individuals tended to have a higher prevalence of H. pylori infection than that in general patients undergoing gastroscopy examination [11]. Another study reported that overweight/obese individuals showed a significantly lower eradication rate of H. pylori infection than controls [12]. The positive association between obesity and H. pylori infection was

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further supported by a recent systematic review that insulin resistance, a characteristic feature of obesity, was observed to be positively related to H. pylori infection [13]. On the contrary, a study performed by Ioannou et al. did not observe any association between body mass index (BMI), an assessment of whether an adult is overweight or not as it measures weight versus height, and H. pylori infection [14]. Some other studies even reported an inverse association between morbid obesity and H. pylori seropositivity [15], and eradication of H. pylori may lead to a significant net increase of BMI [16,17]. These seemingly contradictory reports point to the need for further studies to characterize the correlation between obesity and H. pylori infection as both are becoming more prevalent worldwide. In this study, we performed a large sample, cross-sectional survey to analyze the prevalence of H. pylori infection and its relation with BMI in a Chinese population.

Methods Subjects The study population was recruited from adults who underwent health checkups at the First Affiliated Hospital, College of Medicine, Zhejiang University in 2013. The analyses were limited to the participants who had complete records of anthropometric, biochemical data and had results of H. pylori test. A total of 8820 individuals (5262 men and 3558 women) with a medium (interquartile ranges) age of 46.0 (39.0–53.0) years were included in the final analysis. The study was approved by the Ethics Committee of the First Affiliated Hospital, College of Medicine, Zhejiang University. All participants were verbally informed about the study. Written informed consent was not required for this study because of observational nature of the study. The participant’s personal information was anonymized at collection and anonymized prior to analysis.

Clinical Examination Clinical examination including anthropometric and laboratory measurements was performed using standard methods as previously described [18,19]. Height and weight were measured without shoes and with light clothing. BMI was calculated by dividing weight in kilograms by the square of height in meters. Waist circumference was measured at the minimum circumference between the iliac crest and the rib cage using a nonstretchable standard tape. Blood pressure was recorded using an automated sphygmomanometer.

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An overnight fasting blood samples were obtained from an antecubital vein, and serum samples were separated for biochemical analysis without freezing. The biochemical variables included serum lipids, glucose, liver enzymes, creatinine, blood urea nitrogen, and uric acid. All the biochemical variables were measured with a Hitachi 7600 autoanalyzer (Hitachi, Tokyo, Japan) using standard methods.

Helicobacter pylori Infection Test The diagnosis of H. pylori infection was based on the results of fasting 13C urea breath test (13C-UBT), which is one of the most important and reliable noninvasive approaches for detection of H. pylori infection. Since it was first described more than 20 years ago by Graham et al.[20], 13C-UBT has been extensively applied for the detection of H. pylori infection [21–23]. The 13C-UBT was carried out according to standard procedures described previously [24]. In brief, a baseline breath sample was collected by asking each subject to blow through a straw into a 10-mL plastic container. Then, the subject was asked to take a tablet containing 75 mg of 13C-urea (Beijing Boran Pharmaceutical Co., Ltd., Beijing, China) with 100 mL water. A second breath sample was collected 30 minutes later. The breath samples were analyzed by an infrared heterodyne radiometer (Beijing Huaheng Anbang Science and Technology Co., Ltd, Beijing, China). H. pylori infection was considered to be positive if the 30-minutes value showed a greater than 4.0& difference over the baseline value.

Statistics Analysis Statistical analyses were carried out using SAS 9.1 (SAS Institute, Cary, NC, USA). Continuous variables were expressed as median and interquartile ranges as not all variables were normally distributed. Mann–Whitney U-test and chi-square test were used for comparisons between the groups. Unadjusted and adjusted relative risks of H. pylori infection was analyzed using PROC GENMOD with binomial distribution in SAS. p < .05 (2-tailed) was considered to be statistically significant.

Results Prevalence of H. pylori Infection of the Study Population Of the 8820 participants enrolled in this study, 3859 (43.8%) were positive for H. pylori infection. The H. pylori-positive participants had higher BMI, waist circumference, and diastolic and systolic blood pressure

© 2014 John Wiley & Sons Ltd, Helicobacter 19: 437–442

H. pylori and BMI

Xu et al.

than H. pylori-negative participants (Table 1). The H. pylori-positive participants also had higher serum levels of alanine aminotransferase, c-glutamyltransferase, triglyceride, total cholesterol, and LDL cholesterol, while lower serum HDL cholesterol levels than H. pylori-negative participants (all with p < .05; Table 1). Serum uric acid level appeared to trend higher in the H. pylori-positive participants, but did not reach statistical significance (p = .08). These results suggested that H. pylori-positive participants were associated with a more unfavorable metabolic profile than H. pylori-negative participants.

To get a better view of the relation between BMI and prevalence of H. pylori infection, all the participants were further classified into quintiles according to their BMI: BMI ≤ 21.15, 21.16–22.96, 22.97–24.63, 24.64– 26.56, and ≥26.57 kg/m2 for quintile 1, 2, 3, 4, and 5, respectively. A linear correlation between BMI quintiles and prevalence of H. pylori infection was observed. The prevalence was 40.1% among the participants with BMI in the first quintile and increased to 41.9%, 43.5%, 45.2%, and 48.1% in quintile 2, 3, 4, and 5, respectively (p for trend < .001; Table 3). These results suggested that individuals with a higher BMI had an increased risk of H. pylori infection.

Association of BMI and Prevalence of H. pylori Infection

Risk Factors Analysis of H. pylori Infection

As illustrated in Table 1, H. Pylori-positive participants had a higher BMI than H. pylori-negative participants, suggesting a potential link between H. pylori infection and BMI. To clarify the association of BMI with prevalence of H. pylori infection, all the participants were classified into three groups according to their BMI: lean (BMI < 25.00 kg/m2), overweight (BMI = 25.00– 29.99 kg/m2), and obese (BMI ≥ 30.00 kg/m2). Compared with the prevalence of H. pylori infection among lean participants (42.3%), the prevalence was significantly higher among overweight participants (46.1%), and the prevalence was the highest among obese participants (48.7%; p for trend = .001) (Table 2).

We further analyzed risk factors for H. pylori infection. Odds ratio may be grossly overestimated due to high prevalence of H. pylori infection. Therefore, we analyzed relative risks instead of odds ratios using PROC GENMOD with binomial distribution in SAS. Unadjusted analysis showed that eight variables, including BMI, waist circumference, systolic and diastolic blood pressure, aspartate aminotransferase, total cholesterol, HDL cholesterol, and LDL cholesterol, were associated with risk factors of H. pylori infection (Table 4). After adjusting for all 17 variables listed in Table 4, only BMI (RR = 1.018; 95% CI: 1.011–1.025) and total cholesterol (RR = 1.026; 95% CI: 1.000–1.052) remained to be statistically significantly associated with risk factors

Table 1 Characteristics of study participants according to Helicobacter pylori infection status Variables

H. pylori positive (n = 3859)

H. pylori negative (n = 4961)

Z value

p value

Age (yr) Gender (male/female, n) Body mass index (kg/m2) Waist circumference (cm) Systolic blood pressure (mmHg) Diastolic blood pressure (mmHg) Alanine aminotransferase (U/L) Aspartate aminotransferase (U/L) c-Glutamyltransferase (U/L) Triglyceride (mmol/L) Total cholesterol (mmol/L) HDL cholesterol (mmol/L) LDL cholesterol (mmol/L) Fasting plasma glucose (mmol/L) Creatinine (lmol/L) Blood urea nitrogen (mmol/L) Serum uric acid level (lmol/L)

46.0 (40.0–53.0) 2330/1529 24.01 (21.77–26.23) 84.0 (77.0–91.0) 126.0 (115.0–138.0) 78.0 (70.0–85.0) 20.0 (14.0–30.0) 21.0 (17.0–25.0) 23.0 (15.0–41.0) 1.29 (0.90–1.89) 4.80 (4.23–5.42) 1.09 (0.93–1.29) 2.55 (2.16–2.98) 4.79 (4.49–5.14) 69.0 (56.0–79.0) 5.20 (4.40–6.10) 335.0 (268.0–399.0)

46.0 (39.0–54.0) 2932/2029 23.63 (21.52–25.81) 83.0 (75.0–90.0) 125.0 (114.0–138.0) 77.0 (69.0–85.0) 19.0 (13.0–28.0) 20.0 (17.0–25.0) 23.0 (15.0–39.0) 1.25 (0.86–1.91) 4.74 (04.16–5.35) 1.12 (0.94–1.32) 2.51 (2.13–2.93) 4.78 (4.48–5.12) 68.0 (56.0–79.0) 5.20 (4.40–6.00) 328.0 (267.0–395.0)

0.927 1.342a 4.929 4.260 2.763 2.405 2.573 1.466 2.919 1.991 3.184 3.554 2.812 0.670 1.411 1.099 1.758

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Prevalence of Helicobacter pylori infection and its relation with body mass index in a Chinese population.

Helicobacter pylori infection is highly prevalent worldwide. The association between obesity and H. pylori infection is controversial in the literatur...
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