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Sex differences in Helicobacter pylori infection and recurrence rate among 81,754 Chinese adults: a cross-sectional study

BMC Gastroenterology volume 24, Article number: 305 (2024) Cite this article

Abstract

Objective

To compare the sex differences of Helicobacter pylori (HP) infection rate and 1-year recurrence rate.

Methods

A cross-sectional study was conducted on the prevalence of HP infection in 81,754 people who underwent physical examination in physical examination centers and outpatient clinics of the Affiliated Hospital of Gansu University of Traditional Chinese Medicine, the Second People’s Hospital of Zhangye City, Tianshui City Hospital of Integrated Chinese and Western Medicine, the First and Second Department of The First Hospital of Lanzhou University Physical Examination Center, from March 2010 to December 2019. Among them, 53,771 (65.77%) were males (18–91 years old) and 27,983 (34.23%) were females (18–94 years old). According to age, they were divided into young group, middle-aged group and old group. 1448 asymptomatic infected patients were selected and treated with bismuth-containing quadruple drug eradication therapy for 2 weeks. The eradication rate and recurrence rate after 1 year were compared between males and females.

Results

The overall infection rate was 49.59%, including 49.74% in males and 49.3% in females. The risk of infection in young women was lower than that in men (OR = 0.908, 95%CI: 0.868–0.95, P < 0.01), the risk of infection in older women was higher than that in men (OR = 1.137, 95%CI: 1.041–1.243, P < 0.01). The female infection rate was positively correlated with age from 18 to 60, and Spearman’s correlation coefficient was 0.825 (P < 0.01). The overall eradication rate was 84.67% in intention-to-treat analysis (ITT) and 88.46% in protocol analysis (PP). The eradication rates of ITT and PP in the older group were 78.38% and 82.27%, respectively, which were lower than 87.25% and 89.39% in the male group (P < 0.05). The 1-year overall recurrence rate was 3.86%, including 2.82% in males and 5.44% in females (P < 0.05), female was a risk factor for recurrence after eradication after controlling for age (OR = 2.177, 95%CI 1.166–4.066, P < 0.05). There were no obvious adverse reactions during the treatment.

Conclusion

There is a positive linear correlation between HP infection rate and age increase in women. Older women have the characteristics of high HP infection rate, low eradication rate and high recurrence rate.

Peer Review reports

Introduction

Helicobacter pylori (HP) is a risk factor for gastric cancer (GC) and has been classified as a Class I carcinogen [1]. China is a country with a high infection rate of HP, which is the leading cause of GC in China [2]. Guidelines and consensus have pointed out that eradicating HP is the most important means of preventing GC, and it is recommended to detect and eradicate HP in high-risk areas and populations [2,3,4]. HP’s infection rate differs in different age groups [2]. It is generally believed that the prevalence of HP infection increases with age [4]. However, whether there are sex differences in the infection rate, eradication rate and recurrence rate with the increase of age remains to be determined. The aim of this study was to assess the prevalence of Helicobacter pylori in Gansu Province, China, an area characterized by a high burden of gastric cancer, and to compare the differences in HP infection rate, eradication rate, and recurrence rate after 1 year between males and females of different ages who received health checkups to provide a reference for improving public awareness, preventing HP infection, and health management.

Methods

Study subjects

We conducted this study from March 2010 to December 2019 in Gansu Province, China, people among participants ≥ 18 years who underwent 14C-urea (Headquarter: Shenzhen China) breath test (14C-UBT) in physical examination centers and outpatient clinics of the Affiliated Hospital of Gansu University of Traditional Chinese Medicine, the Second People’s Hospital of Zhangye City, Tianshui City Hospital of Integrated Chinese and Western Medicine, the First and Second Department of The First Hospital of Lanzhou University Physical Examination Center, which included 5 different health service stations from 3 cities (Lanzhou, Tianshui and Zhangye) were analyzed. Males and females were divided by age into youth groups (18–24, 25–29, 30–34, and 35–39 years), middle-aged group (40–44, 45–49, 50–54, and 55–59 years) and older group (60–64, 65–69, 70–74, and ≥ 75 years). Asymptomatic infected persons with eradication intention were selected as the research objects for eradication treatment. This study was approved by the Ethics Committee of the First Hospital of Lanzhou University (No. LDYYLL2022-02), in line with the principles of the Declaration of Helsinki. Informed consent was not obtained for cross-sectional studies, but personal information in this study was kept confidential. Informed consent was obtained and signed from the patients and/or guardians for case-control studies.

Inclusion and exclusion criteria

A retrospective cross-sectional analysis was carried out among people who received health checkups. Inclusion criteria: (1) Han Chinese people ≥ 18 years; (2) people with long-term residence in local district; (3) people who received 14C-UBT for the first time. Exclusion criteria: (1) people with missing data of medical history, physical examination, and routine laboratory tests; (2) people combined with hypertension, diabetes, and other chronic diseases, and tumors; (3) people who had a history of abdominal surgery; (4) people with liver and kidney function indicators, triglyceride (TG), high-density lipoprotein cholesterol (HDL-C), low-density lipoprotein cholesterol (LDL-C), total cholesterol (TC), fasting blood glucose (FBG), and blood uric acid (UA) lower or higher than the normal reference range; (5) people with long- term drinking, smoking, and various types of medications; (6) people who have taken various types of antibiotics, H2 receptor antagonists, or proton pump inhibitors in the last 2 months; (7) people with various gastrointestinal symptoms such as nausea, abdominal distension, and abdominal pain; (8) pregnant and lactating females.

Data collection

The general clinical data including sex, age, smoking and drinking history, combined underlying diseases, surgical history and medication history, physical examination, and clinical laboratory data including blood routine, blood biochemistry, body mass index (BMI), 14C-UBT, and abdominal B-ultrasonography were collected.

Diagnosis of HP infection

HP is defined as the delta over baseline (DOB) value of the 14C-UBT count per minute>100dpm/mmol. If the value is close to 100dpm/mmol, the test should be performed again after 2 weeks.

Eradication schemes and efficacy evaluation

The patients were given Esomeprazole magnesium enteric-coated tablets (20 mg each time, twice a day, taken before breakfast and dinner), Bismuth potassium citrate (220 mg each time, twice a day, taken on an empty stomach half an hour before breakfast, and dinner), clarithromycin (0.25 g each time, twice a day, taken after breakfast and dinner), and tinidazole tablets (0.5 g each time, twice a day, taken after breakfast and dinner). The course of administration of these drugs was 2 weeks. 14C-UBT was performed 1 month and 1 year after eradication therapy at the same standard as before. The HP eradication rate and recurrence rate were calculated, respectively. During the telephone follow-up, patients were urged to take medication regularly and record adverse reactions.

Statistical analysis

SPSS 26.0 statistical software was used. Continuous variables conforming to normal distribution were represented by mean ± standard deviation (SD) and a t-test was adopted. Continuous variables not conforming to normal distribution were represented by M (Q1, Q3), and a non-parametric test was adopted. Categorical variables were expressed as (%) and the χ2 test was used for comparison. The variables that were statistically significant (or nearly statistically significant) by univariate analysis were included in the multivariate logistic regression analysis. The risk factors of HP were determined by the positive method. The study population was divided by sex, and a stratified Chi-square test was used to verify whether there were sex differences in the HP infection rate in different age groups. Correlation analysis was conducted between age groups and male and female infection rates, and the Spearman correlation coefficient was compared. Logistic regression analysis was used to determine the effects of age, BMI, TG, HDL-C, LDL-C, TG, FBG, and UA on the correlation between HP infection and recurrence and sex. P < 0.05 was considered statistically significant.

Results

Changes in HP infection in the past 10 years

A total of 81,754 participants who underwent HP testing from 2010 to 2019 were included, with an average infection rate of 49.59%. The infection rate, the number of infected (+) and uninfected (-) males and females, and the infection rate in males and females are shown in Fig. 1.

Fig. 1
figure 1

HP infection in participants who received health checkups from 2010 to 2019

HP: Helicobacter pylori

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The correlation between infection rate and the year was analyzed by Spearman’s rank correlation, with a coefficient of the annual infection rate, the infection rate in males and females was − 0.479, -0.49, and − 0.358, respectively, and P of 0.162, 0.150, and 0.310, respectively (all P > 0.05). The infection rate of HP decreased gradually from 2010 to 2019, but there was no statistical significance.

HP infection in males and females of different ages

There were 53,771 (65.77%) males, aged 18–91 years, with an average infection rate of 49.74%. There were 27,983 (34.23%) females, aged 18–94 years, with an average infection rate of 49.3%. No statistical significance was found (χ2 = 1.431, P = 0.232).

The standardized infection rate in males and females was 49.73% and 49.29%, respectively. The sex composition of different age groups did not affect the infection rate of HP.

Before the age of 70, the infection rate in males and females showed an increasing trend with the increase in age, and after the age of 70, it showed a decreasing trend.

The infection rate was statistically significant among different age groups (male: χ2 = 121.958, female: χ2 = 105.249, P < 0.01). The correlation between infection rate and age was analyzed by Spearman’s rank correlation, with a coefficient in males of 0.441 (P > 0.05) and females of 0.825 (P < 0.01). There was a positive linear correlation between infection rate in females age from 18 to 60.

In the youth group, the infection rate in females of all ages was lower than in males, with statistical significance in 25–29 years and 30–34 years (χ2 = 15.485, 8.805, P < 0.01). In the middle-aged group, the infection rate in females and males of all ages was close, and the comparison was not statistically significant. In the older group, the infection rate in females was higher than that in males of all ages, but there was no statistical significance.

HP infection in males and females of different age groups

Age group was used as a stratification factor for the stratification χ2 test. The risk of infection in young females was lower than that in males [odds ratio (OR) = 0.908, 95% confidence interval (CI): 0.868–0.95, χ2 = 17.572, P < 0.01)]. The risk of infection was similar in middle-aged females and males (OR = 0.989, 95%CI: 0.948–1.031, χ2 = 0.27, P > 0.05). The risk of infection in older females was higher than that in males (OR = 1.137, 95%CI: 1.041–1.243, χ2 = 8.162, P < 0.01) (Table 1; Fig. 2).

Table 1 HP infection in males and females of different ages
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Fig. 2
figure 2

HP infection rate in males and females of different ages

HP: Helicobacter pylori

Full size image

Risk factors for HP infection

Excluding 40,003 participants with missing general data and examination data and participants combined with various chronic diseases, the remaining 41,751 participants were selected, including 30,729 (73.6%) males aged 18–92 years and 11,022 (26.4%) females aged 18–94 years. 20,387 (48.83%) cases were in the infection group (+), and 21,364 (51.17%) cases were in the non-infection group (-).

Univariate analysis showed that there was no statistical significance in sex (χ2 = 1.336, P = 0.248), but age, BMI, TG, HDL-C, LDL-C, TG, FBG, and UA were statistically significant (Table 2).

Table 2 Characteristics of included participants
Full size table

Age, BMI, TG, HDL-C, LDL-C, TG, FBG, and UA were included in multivariate logistic regression analysis, showing that age and BMI were risk factors for HP infection. The risk of HP infection increased with age (OR = 1.010, 95%CI:1.008–1.011, P < 0.01) and BMI (OR = 1.018, 95%CI:1.013–1.024, P < 0.01).

Association between HP infection and sex difference in different age groups

In the youth group, the infection rate in males and females was lower than the average level with the infection rate in females lower than in males (43.21% vs. 46.26%), and the difference was statistically significant (OR = 0.884, 95%CI:0.825–0.947, P < 0.01).

In the middle-aged group, the infection rates in males and females were 51.1% and 50.73% respectively, with no significant difference (OR = 0.985, 95%CI:0.927–1.047, P = 0.628, P > 0.05).

In the older person group, the infection rate in males and females was 51.42% and 56.52% respectively, and the difference was statistically significant (OR = 1.228, 95%CI:1.052–1.435, P < 0.01).

After adjusting for age, BMI, TG, HDL-C, LDL-C, TG, FBG, and UA, the OR values of the youth group were 0.884 and 0.913, respectively, and this difference still existed (all P < 0.05). The risk of HP infection in females was lower than that in males in youth group. There was no significant change in OR values in the older person group (1.257 vs. 1.214, both P < 0.05). The risk of HP infection in females was higher than that in males, and older female was an independent risk factor for HP infection. The OR values of the middle-aged group before and after adjustment were 0.985 and 1.026, respectively (both P > 0.05), and the infection risk of females and males was similar (Table 3).

Table 3 Association between HP infection and sex difference in different age groups
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Eradication status

A total of 1,448 eradicated patients were selected, and except for age, there was no statistical significance in sex, BMI, and biochemical indexes among all age groups.

A total of 62 cases were lost to follow-up (the rate of loss was 4.28%, among which 27 cases stopped treatment due to a few scattered rashes and cutaneous pruritus, 34 cases did not take medicine regularly, and 1 case went out), 1,386 cases finally completed eradication treatment, and 1,226 cases were successfully eradicated, with the overall eradication rate of 84.67% (1226/1448) according to per-protocol (PP) and 88.46% (1226/1386) according to intention-to-treat (ITT). There was no significant difference among the three groups.

There was no significant difference in the eradication rate between males and females in the youth group and middle-aged group (both P > 0.05). The PP and ITT of females in the older group were 78.38% (116/148) and 82.27% (116/141), respectively, lower than 87.25% (219/251) and 89.39% (219/245) in males (χ2 = 5.442 vs. 3.955, respectively, P < 0.05) (Table 4).

Table 4 Eradication status of males and females in different age groups
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Recurrence in different age groups after 1 year of eradication

The overall recurrence rate was 3.86%, with 2.82% in males and 5.44% in females, and the difference was statistically significant (χ2 = 5.625, P < 0.05).

In the older person group, the recurrence rate of females was higher than that of males, which was 9.4% and 3.86%, respectively, and the difference was statistically significant (χ2 = 2.581, P < 0.05) (Table 5).

Table 5 Recurrence of males and females in different age groups after 1 year of eradication
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When stratified by age group, the OR values among strata were homogeneous (P > 0.05). Female sex was a risk factor for recurrence after eradication (pooled OR = 2.177, 95%CI: 1.166–4.066, χ2 = 5.458, P = 0.019).

After adjusting for age, BMI, TG, HDL-C, LDL-C, TG, FBG, and UA, the OR values of the older person group were 2.117 and 2.162 respectively, and this difference still existed (all P < 0.05). The risk of HP recurrence in females was higher than that in males, and older female was an independent risk factor for HP recurrence. (Table 6).

Table 6 Association between HP recurrence and sex difference in different age groups
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Adverse reactions

The main adverse reactions included constipation or aggravation of constipation symptoms, abdominal distension, and bad breath, but there was no significant difference among the three groups.

Discussion

There are great differences in the infection rate of HP among different populations [1]. A latest systematic review and meta-analysis showed that the prevalence of HP infection in the world decreased from 58.2% in 1980–1990 to 43.1% in 2011–2022 [2]. A multi-center study in Korea also showed that the HP infection rate showed a significant downward trend for 13 consecutive years [3]. The results of this study showed that the infection rate of people ≥ 18 years in Gansu Province was 49.59%, basically consistent with a domestic report [1]. By comparing annual infection rates for 10 consecutive years, we did not find a downward trend.

Age is one of the main risk factors for HP infection [3, 4]. A study suggested that the infection rate increased with age, about 1% per year [4]. A meta-analysis of 16 studies carried out by Wang et al. [5] showed that age was one of the main risk factors for HP infection. The EUROGAST research group investigated the prevalence of HP in Europe, North Africa, North America, and Japan, finding that the infection rates of the 25–34 age group and the 55–64 age group were 34.9% and 61.4%, respectively [6, 7]. We also found that the HP infection rate increased with age. The infection rate was the lowest in the age group of 18–24 years (39.71%), and reached 54.75% in the age group of 65–69 years. Although it showed a downward trend in the age group of over 70 years, it was still higher than the average level.

The reasons why H. pylori infection rates decrease in younger generation is unclear. Lim [3] et al. believed that it was related to the birth cohort effect. HP infection mostly occurs in childhood and adolescence and is most acquired by the age of 10 years. Without intervention, infection can last a lifetime [7, 8]. Infection will not resolve on its own unless proactive interventions [3]. HP infection can also occur in adulthood, but relatively infrequently [8]. However, some studies have suggested that the increase in infection was due to the persistent risk of infection in adults, rather than a cohort effect [9].

Whether there is a sex difference in the HP infection rate has not been concluded. Graham [4] et al. believed that the infection rate was not related to sex, while some studies [10,11,12] found that HP susceptibility was related to sex. We found that there was no sex difference in the overall HP infection rate, but it was surprising to find that the infection rate of both males and females increased with age, and this trend was more obvious in females: the infection rate of females in 18–24 age group was only 38.62%, while it reached 56.21% in 65–69 age group. Correlation analysis showed that the female infection rate was linearly and positively correlated with age. More interestingly, we also found that the infection rate was lower in females than in males in the young group, equal in the middle-aged group, and higher in females than in males in the older group. The difference still existed after adjusting for BMI, blood lipid, and blood glucose. Therefore, we believed that older female was the main risk factor for HP infection.

There is no reasonable explanation for the difference in infection rate between males and females at different ages. We believed that according to the birth cohort effect theory, there was a sex difference in the infection rate in children and adolescents. However, it is currently believed that the infection rate in childhood also increases with age, and it is close to the adult level by the age of 12 [13]. However, whether there is a sex difference is still lacking in China. Studies in Korea have shown that there was no sex difference in the infection rate of children [14, 15].

The HP infection rate increased with age in both males and females, but the reason for the increase in females was not clear. Some studies suggested that estrogen may play an important role in this process [16, 17]. Our statistics showed that the HP infection rate in middle-aged females was significantly higher than that in young females, but almost the same as that in males, which was highly consistent with that in the menopausal age group. The average age of menopause in Chinese females is 48 to 52 years old, and about 90% of females experience menopause between 45 and 55 years old. Menopause is caused by the decline of estrogen levels caused by ovarian failure [18]. We believed that the higher level of estrogen was the reason why the infection rate of young females was significantly lower than that of males, and the decrease in estrogen level was the reason why the infection rate of older females was significantly higher. In addition, it is well known that HP infection is one of the main risk factors for GC. Sipponen [19] believed that the reason why the delay in the appearance and onset of GC in females compared with males was related to the later acquisition of HP infection in postmenopausal females compared with males. Ohtani [20] et al. showed that estrogen supplementation, but not castration, reduced gastric injury in HP-infected male INS-GAS mice. A large number of studies have shown that autoimmune diseases were related to HP infection, and most autoimmune diseases have an obvious sex difference [21], therefore, we believed that these were evidence that HP infection was related to sex or estrogen.

Whether there were age and sex differences in the eradication rate of HP was not conclusive. It was generally believed that the older people have a high rate of eradication failure due to the high rate of antibiotic resistance [22]. Nguyen [23] et al. suggested that in terms of the risk of emergence of drug-resistant strains of antibiotics related to the eradication of HP treatment, patients > 65 years were at higher risk than patients < 65 years, with females at higher risk than males. Chang [24] et al. found that female sex and clindamycin resistance in Korea were factors affecting the failure of HP eradication in patients with chronic gastritis. A US study showed that metronidazole and clarithromycin resistance was more common in females than in males but there was no regional difference [25]. Cai et al. [26] studied HP eradication in 25 hospitals in five provinces in South China, finding that female gender was one of the factors contributing to the low eradication rate. Our results showed that the eradication rate was lower in females than in males in the older group.

Whether there were age and sex differences in relapse rate after eradication is unknown. Xie [27] reported that the annual reinfection rate was 1.5% after the first eradication among people aged 18–65 years in China. The results of our study were 3.86%, 2.82% in males, and 5.44% in females, which was higher in females than in males. Especially in the older females, the rate was 9.4%. Female Sex was a risk factor for relapse after eradication after controlling for age.

The reasons for the high HP infection rate, low eradication rate, and high recurrence rate in over 60 years old females are still unclear. Sipponen [19] and Ohtani [20] et al. found that females were infected with HP later than males, which was highly consistent with our results. Although there is no direct clinical evidence that HP colonization is related to sex or sex hormones, we believe that because of the protection of estrogen, young females are not susceptible to HP or can clear it spontaneously after infection. However, HP infection is susceptible and difficult to clear for the older people, and it can cause persistent damage to gastric mucosa after infection. Therefore, the change in estrogen level may be the main reason for the high infection rate, low eradication rate, and high recurrence rate of HP in females.

At present, it is believed that HP infection is the most important and controllable risk factor for GC. The eradication of HP can reduce the risk of GC in China and effectively prevent GC [3]. Therefore, we believe that age and sex should also be considered in the detection and eradication of GC in high-risk areas and high-risk populations. Of course, although HP infection is a risk factor for GC, the occurrence of GC is a complex process with multi-factor participation and multi-step evolution, which is the comprehensive result of the interaction between genetic and environmental factors [28].

Since this is a retrospective cross-sectional study, the study population was limited to a multi-center physical examination population in Gansu province, and people with various chronic diseases and long-term medication were excluded, the results need to be confirmed by future studies.

Conclusion

In conclusion, the prevalence of HP infection increased with age in both males and females, but this trend was more significant in females. older females have the characteristics of high infection rate, low eradication rate, and high recurrence rate. Although there was no sex difference in the infection rate of HP in general, the infection rate of HP in different age and age groups was significantly different. The infection rate of females was lower than that of males in the youth group but higher than that of males in the older group. Older female is an independent risk factor for HP infection, and the reason was speculated to be related to estrogen. Therefore, sex and age should be considered in the prevention, eradication, and health management of HP as well as related epidemiological investigation and clinical research.

Data availability

Data is provided within the manuscript or supplementary information files.

Abbreviations

14 C-UBT:

4 C-urea breath test

BMI:

Body mass index

CI:

Confidence interval

DOB:

The delta over baseline

FBG:

Fasting blood glucose

GC:

Gastric cancer

HDL-C:

High-density lipoprotein cholesterol

HP:

Helicobacter pylori

ITT:

Intention-to-treat analysis

LDL-C:

Low-density lipoprotein cholesterol

OR:

Odds ratio

PP:

Protocol analysis

SD:

Standard deviation

TC:

Total cholesterol

TG:

Triglyceride

UA:

Uric acid

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Acknowledgements

All authors contributed to the writing of the paper. The authors appreciate everyone for their support and research assistance.

Funding

This work was supported by Hospital fund of The First Hospital of Lanzhou University (ldyyyyn2023-55); Science and technology Project of Gansu Province (Key Research and Development Program, 21YF5FA120); Gansu Province Health Industry Research Project (GSWSKY2020-12).

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Authors and Affiliations

  1. The First School of Clinical Medicine of Lanzhou University, Lanzhou, 730000, China

    Qiao Yuqin, Zhou Yun & Liu Shixiong

  2. Department of Geriatrics, First Hospital of Lanzhou University, Lanzhou, 730000, China

    Zhou Yun & Liu Shixiong

  3. Department of Medical Ultrasound, Affiliated Hospital of Gansu University of Traditional Chinese Medicine, Lanzhou, 730020, China

    Zhao Li

  4. Intensive Care Unit, Tianshui Combine Traditional Chinese and Western Medicine Hospital, Tianshui, 741020, China

    Yang Shengyi

  5. Intensive Care Unit, ZhangYe Second People’s Hospital, Zhangye, 734000, China

    Zhang Xiaodong

Authors
  1. Qiao Yuqin
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  2. Zhou Yun
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  3. Zhao Li
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  4. Yang Shengyi
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  5. Zhang Xiaodong
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  6. Liu Shixiong
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Contributions

1. Yq Q, YZ involved in the design and implementation of the research; collected and analyzed data, wrote the main manuscript text. 2. L Z, Xd Z, Sy Y provided research work support, data collection. 3. Sx L prepared figures and tables, obtained research funding, and guided experiments.

Corresponding author

Correspondence to Liu Shixiong.

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Ethics approval and consent to participate

This study was approved by the Ethics Committee of the First Hospital of Lanzhou University (No. LDYYLL2022-02), in line with the principles of the Declaration of Helsinki. Informed consent was obtained and signed from the patients and/or guardians and personal information in these studies was kept confidential.

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The authors declare no competing interests.

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Qiao, Y., Zhou, Y., Zhao, L. et al. Sex differences in Helicobacter pylori infection and recurrence rate among 81,754 Chinese adults: a cross-sectional study. BMC Gastroenterol 24, 305 (2024). https://doi.org/10.1186/s12876-024-03404-7

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  • DOI: https://doi.org/10.1186/s12876-024-03404-7

Keywords

BMC Gastroenterology

ISSN: 1471-230X

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