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Original article| Volume 21, 101294, May 2023

Prevalence of and risk factors for Helicobacter pylori infection in rural areas of Northwest China: A cross-sectional study in two villages of Yan'an city

Open AccessPublished:March 29, 2023DOI:https://doi.org/10.1016/j.cegh.2023.101294

      Abstract

      Background

      Helicobacter pylori infection is related to the occurrence of various diseases, and its influencing factors have been studied worldwide. Research on the current status of H. pylori infection in underdeveloped rural areas in China is limited.

      Aim

      This research aimed to understand the status of H. pylori infection and its risk factors in rural Yan'an city, Northwest China.

      Methods

      This cross-sectional study was implemented in two villages in Yan'an city in 2018, and 226 individuals underwent the Carbon-14 urea breath test to detect H. pylori infection. Participants' demographic characteristics, socioeconomic status, dietary habits, and lifestyle were collected through structured questionnaires.

      Results

      In this research, the overall infection rate of H. pylori was 32.7% (74/226). Multivariate logistic regression analysis showed that people with a body mass index (BMI)≥24 kg/m2 (OR = 3.03; 95% CI = 1.65–5.57) and people who frequently dined out (OR = 8.87; 95% CI = 1.43–54.97) were more likely to be infected H. pylori. Conversely, the H. pylori infection risk was reduced among people over 60 years of age (OR = 0.32; 95% CI = 0.17–0.62) as well as among those who ate sweet potatoes more than 7 times a week (OR = 0.23; 95% CI = 0.07–0.75).

      Conclusion

      A BMI≥24 kg/m2 and frequent eating out were risk factors for H. pylori infection among the village inhabitants of Yan'an city. The consumption of sweet potatoes was related to a low risk of H. pylori infection.

      Keywords

      1. Introduction

      Helicobacter pylori is a microaerophilic gram-negative spirochete,
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      Helicobacter pylori sero-prevalence in asthma.
      and Warren and Marshall were the first to isolate it in 1983.
      • Warren J.R.
      • Marshall B.
      Unidentified curved bacilli on gastric epithelium in active chronic gastritis.
      H. pylori infection is related to various diseases, including stomach cancer. In line with GLOBOCAN 2020 data, stomach cancer ranks fourth in the global ranking of cancer deaths, after lung cancer, colorectal cancer and liver cancer.
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      • Ferlay J.
      • Siegel R.L.
      • et al.
      Global cancer statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries.
      Gastric cancer is a preventable cancer and greatly affected by life.
      • Rawla P.
      • Barsouk A.
      Epidemiology of gastric cancer: global trends, risk factors and prevention.
      The latest 15th edition of the carcinogen report published by the US Department of Health and Human Services clearly lists H. pylori (chronic infection) as a human carcinogen.
      NTP (National Toxicology Program)
      Report on Carcinogens.
      The eradication of H. pylori is an important measure to prevent stomach cancer.
      The Infection rate of H. pylori varies between countries and regions. The infection rate in developing countries is 50.8%, while that in developed countries is only 34.7%.
      • Zamani M.
      • Ebrahimtabar F.
      • Zamani V.
      • et al.
      Systematic review with meta-analysis: the worldwide prevalence of Helicobacter pylori infection.
      In the last two decades, the infection rate of H. pylori has declined in China.
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      • Zhang J.-M.
      • Li S.-R.
      • Chen C.-W.
      Spatial-temporal distribution and influencing factors of Helicobacter pylori infection in Chinese mainland, 2001-2020: a systematic review and meta-analysis.
      In recent years, the infection rate of H. pylori in different regions of China ranges from 35.0% to 54.27%
      • Li C.
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      Prevalence and predictors of infection in asymptomatic individuals: a hospital-based cross-sectional study in Shenzhen, China.
      ,
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      • et al.
      Family-based infection status and transmission pattern in central China, and its clinical implications for related disease prevention.
      H. pylori infection is associated with multifarious factors. A comprehensive analysis that covered multiple regions in mainland China for nearly 20 years showed that eating meat, milk, vegetable oil, and aquatic product consumption, per capita gross domestic product (GDP) and annual average humidity were related to H. pylori infection.
      • Lu T.-L.
      • Zhang J.-M.
      • Li S.-R.
      • Chen C.-W.
      Spatial-temporal distribution and influencing factors of Helicobacter pylori infection in Chinese mainland, 2001-2020: a systematic review and meta-analysis.
      In Wuwei city, Gansu Province, a high-incidence region of stomach cancer in China, researchers found that age, consumption of yogurt, and household income were the influencing factors of H. pylori infection among the local residents.
      • Wang X.
      • Shu X.
      • Li Q.
      • et al.
      Prevalence and risk factors of Helicobacter pylori infection in Wuwei, a high-risk area for gastric cancer in northwest China: an all-ages population-based cross-sectional study.
      A survey in the rural population of Linqu city, Shandong Province, another high-risk area for stomach cancer in China, found that infrequent hand washing before meals, crowded housing, low education levels, and water source were correlated with H. pylori infection.
      • Brown L.M.
      • Thomas T.L.
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      • et al.
      Helicobacter pylori infection in rural China: demographic, lifestyle and environmental factors.
      Eating more grains and vegetables can reduce the chance of H. pylori infection among Chinese adults, while a high-salt diet has the opposite effect.
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      • Zhang X.-Y.
      • Feng Y.-L.
      Dietary patterns and Helicobacter pylori infection in a group of Chinese adults ages between 45 and 59 years old: an observational study.
      China is a large agricultural country, and few studies have been conducted on H. pylori infection in the Chinese countryside. Because the northwestern region, including northern Shaanxi, is a relatively underdeveloped region against China's contemporary economic development, considering the regional differences in dietary habits and lifestyles, it is crucial to survey the influencing factors of H. pylori infection among rural residents in northern Shaanxi, China.
      Thus, the objective of this study was to investigate the prevalence of H. pylori among adult residents in two villages in northern Shaanxi, China, and to evaluate the potential factors of local H. pylori infection to provide well-founded guidance for the local prevention of H. pylori infection.

      2. Subjects and methods

      2.1 Study population and design

      This research was carried out in April 2018 in two villages in Ansai County, Yan'an city, Shaanxi Province, China. We recruited 289 villagers who volunteered to participate. All participants completed an epidemiological questionnaire, and we assessed the participants' demographic characteristics, socioeconomic status, dietary habits, and lifestyle. To detect H. pylori infection, we collected breath samples from participants. This study excluded: 1. Participants with a history of antibiotic use within one month before enrollment or the history of taking proton pump inhibitor, bismuth or H2 receptor blockers use within the first two weeks; 2. Participants with partial or complete gastrectomy; 3. Participants who suffered from mental illness and could not cooperate; and 4. Those under 18 years of age. All subjects gave informed consent before being accepted into this study. The Ethics Committee of the Second Affiliated Hospital of Xi'an Jiaotong University approved this study.

      2.2 Description of the research site

      Baitai Village and Xigou Village involved in this study are located in Yan'an city, Shaanxi Province, Northwest China. These villages have a typical continental arid climate. For a long time, the cultivation of grains has been the dominant industry here. Production and living conditions are poor. Only in 2018 were all poor households lifted out of poverty in both villages.

      2.3 Questionnaire

      All participants answered the questionnaire under the guidance of trained investigators. The questionnaire included questions on demographic characteristics (e.g., age, sex, body mass index (BMI), ethnicity, and occupation), socioeconomic status (e.g., annual household revenue and educational background), dietary habits (e.g., frequency of eating fruits, vegetables, milk, and soy product consumption), lifestyle (e.g., drinking water sources and household crowding), and behavioral characteristics (e.g., hand hygiene and sharing of cups and utensils). All results were managed and entered by EpiData 3.1, and the data were double-checked to reduce errors.

      2.4 H. Pylori detection

      The carbon-14 urea breath test (14C-UBT) was used to evaluate H. pylori infection. The test subjects were tested on an empty stomach or after fasting for 4 h. The participants swallowed a capsule of urea C-14 with drinking water, rested, and fasted and avoided strenuous exercise. The breath samples were collected after 30 min. We used the cassette method (Anhui Yanghe Medical Equipment Co., Ltd., China) to analyze the samples, and the C-14 radioactive signal was gauged by an H. pylori detector (model: YH04E). According to the instructions of the manufacturing company, the sample was positive when the C-14 disintegrations per minute (DPM) were >149. All tests were executed strictly in accordance with the manufacturer's instructions, and we validated against known sample gas concentrations using the manufacturer's instrumentation prior to the start of the study.

      2.5 Statistical analysis

      All statistical analyses were performed using the statistical package R (http://www.R-project. org; version 4.2.0 2022-04-22) and EmpowerStats (http://www.EmpowerStats.com, X&Y Solutions, Inc.). Continuous variables are represented as the means±standard deviations (SDs), and categorical variables are represented as frequencies and percentages. Moreover, the t-test was used for continuous variables, and the chi-square test was used for categorical variables. Univariate analysis was then performed, and if a variable was significantly related to H. pylori infection (p < 0.05), it was selected to enter the logistic regression model. The odds ratio (OR) and 95% confidence interval (CI) between H. pylori infection and possible influencing factors were evaluated by a multivariate logistic regression model, and a P value < 0.05 was considered statistically significant.

      3. Results

      3.1 Sociodemographic characteristics of the respondents

      The 289 subjects invited to participate ranged in age from 30 to 88 years. Sixty-three subjects were excluded because their questionnaires were incomplete or their breath tests were not completed, and 226 eligible subjects were included in the final analysis (Fig. 1). These 226 respondents included 97 males and 129 females, with an average age of 62.6 ± 12.1 years for men and 59.9 ± 11.8 years for women. A total of 67.3% of the subjects had no education, 90% were farmers, 92.9% engaged in manual labor all the year round, and more than half (58%) had a per capita monthly household income of less than 200 yuan.
      Fig. 1
      Fig. 1Study flowchart (n, number; 14C- UBT, carbon- 14 urea breath test).

      3.2 Prevalence of H. pylori infection

      In this study, the total H. pylori infection rate of the individuals included from Baitai Village and Xigou Village, Ansai County, Yan'an city was 32.7% (74/226). The infection rate for females was 31.0% (40/129), and the infection rate for males was 35.0% (34/97), with no significant difference (p = 0.52).

      3.3 Economic and demographic factors of H. pylori infection

      The economic and demographic factors related to H. pylori infection are shown in Table 1. Age and BMI were notably correlated with the H. pylori infection (p < 0.05). Nevertheless, the research showed that factors such as ethnicity, blood type, occupation, education level, marital status and income were not related to H. pylori infection.
      Table 1Correlation between the Helicobacter pylori infection and sociodemographic–economic.
      VariablesStudy population n (%)H.pylori-negative n (%)H.pylori-positive n (%)P-value
      Age years, mean (±SD)59.5 ± 11.961.8 ± 11.654.8 ± 11.3<0.001
      Gender0.521
       Male97 (42.9)63 (64.9)34 (35.1)
       Female129 (57.1)89 (69.0)40 (31.0)
      Nation0.601
       Han224 (99.1)151 (67.4)73 (32.6)
       Minority2 (0.9)1 (50)1 (50)
      BMI, kg/m223.4 ± 3.922.9 ± 3.324.5 ± 4.80.004
      Blood type0.757
       A type11 (4.9)6 (54.5)5 (45.5)
       B type19 (8.4)14 (73.7)5 (26.3)
       AB type6 (2.7)5 (83.3)1 (16.7)
       O type15 (6.6)10 (66.7)5 (33.3)
       Unknown175 (77.4)117 (66.9)58 (33.1)
      Occupation0.535
       Worker5 (2.2)2 (40.0)3 (60.0)
       Farmer204 (90.3)139 (68.1)65 (31.9)
       Businessman3 (1.3)3 (100.0)0 (0.0)
       Intellectual2 (0.9)1 (50.0)1 (50.0)
       Cadre5 (2.2)2 (40.0)3 (60.0)
       Retirement1 (0.4)1 (100.0)0 (0.0)
       Unemployed2 (0.9)1 (50.0)1 (50.0)
       Other4 (1.8)3 (75.0)1 (25.0)
      Education level0.171
       Illiterate152 (67.3)110 (72.4)42 (27.6)
       Primary school32 (14.2)17 (53.1)15 (46.9)
       Junior high school21 (9.3)13 (61.9)8 (38.1)
       Senior high school11 (4.9)7 (63.6)4 (36.4)
       University or above10 (4.4)5 (50.0)5 (50.0)
      Marriage0.933
       Married211 (93.4)142 (67.3)69 (32.7)
       Unmarried8 (3.5)5 (62.5)3 (37.5)
       Loss of spouse7 (3.1)5 (71.4)2 (28.6)
      Per capita monthly income (¥)0.125
       <200131 (58.0)94 (71.8)37 (28.2)
       200-50043 (19.0)30 (69.8)13 (30.2)
       500-100024 (10.6)15 (62.5)9 (37.5)
       1000-300016 (7.1)7 (43.8)9 (56.2)
       >300012 (5.3)6 (50.0)6 (50.0)
      Type of labor0.674
       Mental labor16 (7.1)10 (62.5)6 (37.5)
       Physical labor210 (92.9)142 (67.6)68 (32.4)
      Abbreviations: BMI, body mass index; SD, standard deviation.

      3.4 Dietary influencing factors of H. pylori infection

      The eating habits associated with H. pylori infection are shown in Table 2. An increased risk of H. pylori infection was significantly correlated with the frequency of sweet potato consumption (p < 0.05). However, the consumption of bean products, seafood, sweets, fried foods, pickled foods, animal blood, milk, eggs, garlic, and coarse grains was not related to H. pylori infection. In addition, the different proportions of staple foods or fruits and vegetables and the saltiness of the foods were not found to be correlated with H. pylori infection.
      Table 2Correlation between the prevalence of Helicobacter pylori infection and dietary-related factors.
      VariablesStudy population n (%)H.pylori-negative n (%)H.pylori-positive n (%)P-value
      Frequency of eating fruits (times/week)0.926
       Never or hardly ever106 (46.9)70 (66.0)36 (34.0)
       1-697 (42.9)66 (68.0)31 (32.0)
       ≥723 (10.2)16 (69.6)7 (30.4)
      Frequency of eating vegetables (times/week)0.701
       Never or hardly ever29 (12.8)21 (72.4)8 (27.6)
       1-6114 (50.4)74 (64.9)40 (35.1)
       ≥783 (36.7)57 (68.7)26 (31.3)
      Frequency of eating beans (times/week)0.088
       Never or hardly ever85 (37.6)62 (72.9)23 (27.1)
       1-6111 (49.1)67 (60.4)44 (39.6)
       ≥730 (13.3)23 (76.7)7 (23.3)
      Frequency of eating seafood (times/week)0.713
       Never or hardly ever183 (81.0)124 (67.8)59 (32.2)
       1-642 (18.6)27 (64.3)15 (35.7)
       ≥71 (0.4)1 (100.0)0 (0.0)
      Frequency of eating sweets (times/week)0.488
       Never or hardly ever161 (71.2)112 (69.6)49 (30.4)
       1-659 (26.1)36 (61.0)23 (39.0)
       ≥76 (2.7)4 (66.7)2 (33.3)
      Frequency of eating fried foods (times/week)0.314
       Never or hardly ever113 (50.0)81 (71.7)32 (28.3)
       1-6109 (48.2)69 (63.3)40 (36.7)
       ≥74 (1.8)2 (50.0)2 (50.0)
      Frequency of eating pickled foods (times/week)0.927
       Never or hardly ever46 (20.4)32 (69.6)14 (30.4)
       1-6101 (44.7)67 (66.3)34 (33.7)
       ≥779 (35.0)53 (67.1)26 (32.9)
      Frequency of eating animal blood (times/week)0.113
       Never or hardly ever195 (86.3)135 (69.2)60 (30.8)
       1-631 (13.7)17 (54.8)14 (45.2)
      Frequency of drinking milk (times/week)0.659
       Never or hardly ever179 (79.2)122 (68.2)57 (31.8)
       1-636 (15.9)22 (61.1)14 (38.9)
       ≥711 (4.9)8 (72.7)3 (27.3)
      Frequency of eating eggs (times/week)0.363
       Never or hardly ever80 (35.4)55 (68.8)25 (41.2)
       1-6132 (58.4)90 (68.2)42 (31.8)
       ≥714 (6.2)7 (50.0)7 (50.0)
      Frequency of eating sweet potatoes (times/week)0.025
       Never or hardly ever108 (47.8)66 (61.1)42 (38.9)
       1-687 (38.5)59 (67.8)28 (32.2)
       ≥731 (13.7)27 (87.1)4 (12.9)
      Amount of eating food per week0.640
       staple food>vegetables and fruit184 (81.4)124 (67.4)60 (32.6)
       staple food=vegetables and fruit36 (15.9)23 (63.9)13 (36.1)
       staple food<vegetables and fruit6 (2.7)5 (83.3)1 (16.7)
      Salt status of dishes0.788
       Salty59 (26.1)38 (64.4)21 (35.6)
       Medium86 (38.1)60 (69.8)26 (30.2)
       Light81 (35.8)54 (66.7)27 (33.3)
      Frequency of eating garlic (times/week)0.154
       Never or hardly ever102 (45.1)75 (73.5)27 (26.5)
       1-691 (40.3)58 (63.7)33 (36.3)
       ≥733 (14.6)19 (57.6)14 (42.4)
      Frequency of eating coarse grains (times/week)0.085
       Never or hardly ever25 (11.1)13 (52.0)12 (48.0)Never or hardly ever
       1-673 (32.3)46 (63.0)27 (37.0)1–6
       ≥7128 (56.6)93 (72.7)35 (27.3)≥7

      3.5 Lifestyle-related influencing factors of H. pylori infection

      The lifestyle factors correlated with H. pylori infection are shown in Table 3. The infection rate of H. pylori was notably correlated with whether participants mainly ate at home (p = 0.001). However, family size, the number of indoor rooms, the sharing of tableware and utensils, washing hands before and after meals, the method of eating, the disinfection of tableware, and the water source were not related to H. pylori infection (P > 0.05).
      Table 3Correlation between the prevalence of Helicobacter pylori infection and lifestyle characteristics.
      VariablesStudy population n (%)H.pylori-negative n (%)H.pylori-positive n (%)P-value
      Household population (family size)0.237
       ≤4184 (81.4)127 (69.0)57 (31.0)
       >442 (18.6)25 (59.5)17 (40.5)
      Number of rooms per house0.948
       ≤5202 (89.4)136 (67.3)66 (32.7)
       >524 (10.6)16 (66.7)8 (33.3)
      Frequency of sharing toothbrushes and cups0.975
       Almost always/always6 (2.7)4 (66.7)2 (33.3)
       Sometimes/never220 (97.3)148 (67.3)72 (32.7)
      Frequency of washing hands before meals0.214
       Almost always/always199 (88.1)131 (65.8)68 (34.2)
       Sometimes/never27 (11.9)21 (77.8)6 (22.2)
      Frequency of washing hands after going to the bathroom0.214
       Almost always/always192 (85.0)126 (65.6)66 (34.4)
       Sometimes/never34 (15.0)26 (76.5)8 (23.5)
      Source of drinking water0.301
       Well water52 (23.0)36 (69.2)16 (30.8)
       River or Lake water1 (0.4)0 (0.0)1 (100.0)
       Bottled water3 (1.3)3 (100.0)0 (0.0)
       Tap water170 (75.2)113 (66.5)57 (33.5)
      Frequency of drinking boiled tap water0.288
       Almost always/always197 (87.2)135 (68.5)62 (31.5)
       Sometimes/never29 (12.8)17 (58.6)12 (41.4)
      Way of using tableware0.441
       Alone17 (7.5)10 (58.8)7 (41.2)
       Share209 (92.5)142 (67.9)67 (32.1)
      Way of eating0.975
       Eating separately6 (2.7)4 (66.7)2 (33.3)
       Eating together220 (97.3)148 (67.3)72 (32.7)
      Main Dining place0.001
       Home214 (94.7)149 (69.6)65 (30.4)
       Outside12 (5.3)3 (25.0)9 (75.0)
      Frequency of disinfection of tableware0.807
       Almost always/always14 (6.2)9 (64.3)5 (35.7)
       Sometimes/never212 (93.8)143 (67.5)69 (32.5)
      Rain leaked into the house0.345
       No156 (69.0)108 (69.2)48 (40.8)
       Yes70 (31.0)44 (62.9)26 (37.1)
      Garbage disposal station or sewerage system near the house0.174
       No177 (78.3)123 (69.5)54 (30.5)
       Yes49 (21.7)29 (59.2)20 (40.8)

      3.6 Multivariate analysis of influencing factors related to H. Pylori infection

      The multivariate logistic regression model further evaluated the effects of these variables, as shown in Table 4. A decreased risk of H. Pylori infection significantly with increasing age (≥60 years) (OR = 0.32, 95% CI: 0.17–0.62). In addition, eating more sweet potatoes was associated with a low risk of H. Pylori infection in the local population (OR = 0.23, 95% CI: 0.07–0.75). Risk factors for H. Pylori infection were BMI≥24 kg/m2 (OR = 3.03, 95% CI: 1.65–5.57) and frequent eating out (OR = 8.87, 95% CI: 1.43–54.97).
      Table 4Multivariate analysis of risk factors for Helicobacter pylori infection.
      VariablesUnadjustedadjusted
      OR (95%CI)P-valueOR (95%CI)P-value
      Age (years)
       <60ReferenceReference
       ≥600.32 (0.18–0.58)<0.0010.32 (0.17–0.62)0.001
      BMI,kg/m2
       <24ReferenceReference
       ≥243.08 (1.73–5.50)<0.0013.03 (1.65–5.57)<0.001
      Frequency of eating sweet potatoes (times/week)
       Never or hardly everReferenceReference
       1-60.75 (0.41–1.35)0.3320.77 (0.41–1.44)0.412
       ≥70.23 (0.08–0.71)0.0110.23 (0.07–0.75)0.015
      Main Dining place
       HomeReferenceReference
       Outside6.88 (1.80–26.23)0.0058.87 (1.43–54.97)0.019
      Abbreviations: BMI, body mass index; 95% CI, Confidence Interval; OR, Odds Ratio.

      4. Discussion

      This was a cross-sectional study that assessed the prevalence of H. pylori in villages of Yan'an city, Northwest China. This study used the 14C-UBT to detect present H. Pylori infection. Because of its accuracy, operability, and noninvasiveness, the UBT has become the first choice for many doctors to evaluate H. Pylori infection in patients.
      • Wang X.
      • Zhang S.
      • Chua E.G.
      • et al.
      A re-testing range is recommended for C- and C-urea breath tests for Helicobacter pylori infection in China.
      Our research revealed that the total infection rate of H. Pylori in Baitai and Xigou villages was 32.7%, which was similar to the infection rate in Wuwei, which is also located in Northwest China (35.6%).
      • Wang X.
      • Shu X.
      • Li Q.
      • et al.
      Prevalence and risk factors of Helicobacter pylori infection in Wuwei, a high-risk area for gastric cancer in northwest China: an all-ages population-based cross-sectional study.
      It is worth noting that the rural areas of Yan'an city are remote and inconvenient for transportation, most of the middle-aged and elderly people have lived there here for a long time, and population mobility is poor, which is similar to other underdeveloped rural areas in China.
      Our research found that H. pylori infection was correlated with age, BMI, main eating location, and sweet potatoes consumption. The influencing factors for H. pylori infection have been studied worldwide and include socioeconomic status, sanitation, dietary patterns, etc. However, due to diversities in the features of the research population and the variables used to assess risk factors, this issue remains controversial.
      Consistent with several studies,
      • Zamani M.
      • Ebrahimtabar F.
      • Zamani V.
      • et al.
      Systematic review with meta-analysis: the worldwide prevalence of Helicobacter pylori infection.
      ,
      • Zhang F.
      • Pu K.
      • Wu Z.
      • et al.
      Prevalence and associated risk factors of Helicobacter pylori infection in the Wuwei cohort of north-western China.
      we found that H. pylori infection was not significantly related to sex, and our results revealed that the H. pylori infection rate was slightly higher among males than among females (31.0%). Cheng et al.
      • Cheng H.
      • Hu F.
      • Zhang L.
      • et al.
      Prevalence of Helicobacter pylori infection and identification of risk factors in rural and urban Beijing, China.
      also reported a slightly higher infection rate of H. pylori among men, they believed that in rural settings, men's workplaces often lack clean water sources and toilet facilities, the poor sanitation may increase the chance of men being infected with H. pylori.
      This research revealed that the H. pylori-positive population was relatively young, and the multivariate logistic regression analysis further confirmed that the risk of H. pylori infection was significantly reduced among those aged ≥60 years. The research by Wang et al. also reported that the infection rate of H. pylori peaked at the age of 51–60 years, after which the infection risk gradually decreased.
      • Wang W.
      • Jiang W.
      • Zhu S.
      • et al.
      Assessment of prevalence and risk factors of helicobacter pylori infection in an oilfield Community in Hebei, China.
      The possible mechanisms are as follows: On the one hand, in the elderly population, H. pylori is not detected due to the low number or low activity of H. pylori colonization; on the other hand, with age, the environmental conditions of the human stomach are not conducive to the survival of H. pylori, which tends to disappear.
      • Zhang F.
      • Pu K.
      • Wu Z.
      • et al.
      Prevalence and associated risk factors of Helicobacter pylori infection in the Wuwei cohort of north-western China.
      However, other studies have shown that older individuals have greater risk to infect H. pylori.
      • Tarkhashvili N.
      • Chakvetadze N.
      • Mebonia N.
      • et al.
      Traditional risk factors for Helicobacter pylori infection not found among patients undergoing diagnostic upper endoscopy-Republic of Georgia, 2007-2008.
      The differences in these results may be associated with regional differences in diet, customs, and lifestyle.
      BMI is an indicator that reflects the degree of obesity of the body. The internationally accepted BMI thresholds are as follows: 25–30 kg/m2 is recognized as overweight, and BMI≥30 kg/m2 is recognized as obesity. The China Obesity Working Group proposed that the standard for Chinese individuals is that a BMI of 24–28 kg/m2 is defined as overweight, while a BMI≥28 kg/m2 is defined as obesity.
      • Chen C.
      • Lu F.C.
      The guidelines for prevention and control of overweight and obesity in Chinese adults.
      Our study found that BMI≥24 kg/m2 was a risk factor for H. pylori infection (OR = 3.03, 95% CI: 1.65–5.57). Several studies have shown that high BMI is correlated with an increase in H. pylori infection.
      • Siddiqui B.
      • Yakoob J.
      • Abbas Z.
      • Azmat R.
      • Fatima S.S.
      • Awan S.
      Distribution of Helicobacter pylori infection and abnormal body- mass index (BMI) in a developing country.
      ,
      • Kouitcheu Mabeku L.B.
      • Noundjeu Ngamga M.L.
      • Leundji H.
      Potential risk factors and prevalence of Helicobacter pylori infection among adult patients with dyspepsia symptoms in Cameroon.
      Bacterial infection can interfere with the secretion of leptin and ghrelin in the body, resulting in an increase in the level of ghrelin and a reduction in the level of leptin within plasma.
      • Francois F.
      • Roper J.
      • Joseph N.
      • et al.
      The effect of H. pylori eradication on meal-associated changes in plasma ghrelin and leptin.
      • Pacifico L.
      • Anania C.
      • Osborn J.F.
      • et al.
      Long-term effects of Helicobacter pylori eradication on circulating ghrelin and leptin concentrations and body composition in prepubertal children.
      • Roper J.
      • Francois F.
      • Shue P.L.
      • et al.
      Leptin and ghrelin in relation to Helicobacter pylori status in adult males.
      Ghrelin can increase body weight by reducing energy expenditure,
      • Tschöp M.
      • Smiley D.L.
      • Heiman M.L.
      Ghrelin induces adiposity in rodents.
      while leptin is involved in the regulation of metabolism, which can reduce food intake and increase energy release, resulting in weight loss.
      • Halaas J.L.
      • Gajiwala K.S.
      • Maffei M.
      • et al.
      Weight-reducing effects of the plasma protein encoded by the obese gene.
      The mechanism of transmission of H. pylori is inconclusive, and researchers believe that bacteria are transmitted either directly between people or indirectly via contaminated food and water sources.
      • Zamani M.
      • Vahedi A.
      • Maghdouri Z.
      • Shokri-Shirvani J.
      Role of food in environmental transmission of Helicobacter pylori.
      We found that the higher the frequency of fruit and vegetable consumption was, the lower the infection risk of H. pylori, although the difference was not significant in this study. A similar phenomenon was also revealed by Zhang et al.
      • Zhang F.
      • Pu K.
      • Wu Z.
      • et al.
      Prevalence and associated risk factors of Helicobacter pylori infection in the Wuwei cohort of north-western China.
      A diet rich in fruits and vegetables is thought to reduce the risk of H. pylori infection, and vitamin C contained within vegetables and fruits may directly affect the growth of H. pylori by reinforcing the gastric mucosal immune response and neutralizing free radicals.
      • Zhang Z.W.
      • Farthing M.J.G.
      The roles of vitamin C in Helicobacter pylori associated gastric carcinogenesis.
      A study
      • Fox J.G.
      • Dangler C.A.
      • Taylor N.S.
      • King A.
      • Koh T.J.
      • Wang T.C.
      High-salt diet induces gastric epithelial hyperplasia and parietal cell loss, and enhances Helicobacter pylori colonization in C57BL/6 mice.
      reported that salt interferes with the completeness of the gastric mucosa and promotes the colonization of H. pylori, ultimately triggering inflammation and accelerating gastric carcinogenesis. Zhu et al.
      • Chen C.
      • Lu F.C.
      The guidelines for prevention and control of overweight and obesity in Chinese adults.
      reported that eating pickled fish and fried food was positively related to H. pylori infection, and speculated that this result was related to the cooking method and high salt content in the food. According to our results, the H. pylori infection risk tended to decrease as salt consumption decreased. More interestingly, our study concluded that eating more sweet potatoes reduced significantly the risk of H. pylori infection. Considering that Yan'an city is located inland in Northwest China, people mainly live off of the cultivation of grains and root crops. The specific reasons may be associated with the cooking methods of food in various geographical areas, but further investigation is needed.
      Risk factors correlated with H. pylori infection also involve poor sanitation, overcrowding, and cross-infection within households.
      • Chen C.
      • Lu F.C.
      The guidelines for prevention and control of overweight and obesity in Chinese adults.
      In terms of hygiene habits, this study concluded that frequent eating out was a risk factor for H. pylori infection, which is consistent with the study results of Hu et al.
      • Hu J.
      • Wang X.
      • Chua E.G.
      • et al.
      Prevalence and risk factors of infection among children in Kuichong Subdistrict of Shenzhen City, China.
      The thorough disinfection of tableware and the prevention of cross-infection cannot be guaranteed when eating out. In addition, we did not find that variables that represented household crowding were correlated with H. pylori infection.
      Few studies have investigated H. pylori infection in underdeveloped areas of China, and the results of our study contribute to understanding H. pylori prevalence and potential infection risk factors in rural Yan'an city. Furthermore, multivariate logistic regression quantified the independent role of BMI as a risk factor for H. pylori infection.
      Nevertheless, this research has many limitations. First, in our cross-sectional study, the causality between H. pylori infection and various influencing factors could not be conclusively verified. Second, although our study population came from two different rural areas in Yan'an city, the results may still not represent the overall rural population well. We did not recruit subjects between the ages of 18 and 30 because most of this generation of young people study or work in other place, but this is also in line with the demographics of rural underdeveloped areas in China. Third, the sample size of this study was small, and it is crucial to conduct a large-scale prospective epidemiological survey in the local area. Fourth, our study was based on questionnaires, and the questionnaire design only assessed the frequency of intake of the relevant food but not the number or portion size. Research suggests that the difference in the portion size between different subjects is much smaller than the difference in the frequency of intake, so this part of the difference would not have exerted a prominent influence on the results.
      • Samet J.M.
      • Humble C.G.
      • Skipper B.E.
      Alternatives in the collection and analysis of food frequency interview data.
      At last, The effect of blood type on H. pylori infection has attracted attention, and individuals with O blood type have a higher inflammatory response to H. pylori.
      • Alkout A.M.
      • Blackwell C.C.
      • Weir D.M.
      Increased inflammatory responses of persons of blood group O to Helicobacter pylori.
      However, It was not found that the blood type is related to H. pylori infection in our study. Among H. pylori infected individuals, the proportion of individuals with O blood was the same as that of A and B, both are 6.75%, while AB only accounts for 1.4%. Among H. pylori uninfected individuals, only 3.3% of individuals were type AB, 3.9% were type A, 6.6% were type O, and 9.2% were type B. This result was affected by the unknown blood type of 77.7% of the subjects, and it is necessary to add various laboratory tests in the follow-up research.

      5. Conclusions

      In summary, the infection rate of H. pylori in the two rural areas of Yan'an city, China was 32.7%. Our results revealed that BMI≥24 kg/m2 and frequent eating out are independent risk factors for H. pylori infection. Eating sweet potatoes might decrease the risk of H. pylori infection. These findings will certainly help to develop targeted prevention strategies locally to control the H. pylori epidemic and reduce the incidence of related diseases.

      Funding support

      This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.

      Author contributions

      She X, Zhao P, Shi HT and Dong L designed the study. Zhao J collected the data. Cheng S analyzed the data. She X drafted the manuscript. Zhao p and Cheng S revised the manuscript. All authors have agreed the final article.

      Disclosure of interest

      The authors have no competing interests.

      Acknowledgments

      None.

      Appendix A. Supplementary data

      The following is the Supplementary data to this article.

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