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A survey on the current status of Helicobacter pylori infection in households in Hainan Province, China

BMC Gastroenterology volume 23, Article number: 426 (2023) Cite this article

Abstract

Objective

This study aims to assess the prevalence of Helicobacter pylori (Hp) infection at the household level in Hainan Province in China and identify the factors that contribute to its spread. The findings of this study have significant implications for public health prevention strategies in the Hainan region.

Methods

A total of 421 families, comprising 1355 individuals, were tested for Hp infection across five cities in Hainan Province between July 2021 and April 2022. The study utilized questionnaires that included questions about personal characteristics, household shared lifestyle and dietary habits, and potential pathways of Hp infection in children to identify potential factors linked to household Hp infection and transmission patterns.

Results

The prevalence of Hp infection on an individual basis was 46.72% (629/1355), with age ≥ 20 years, being married and having junior secondary education and above as risk factors for Hp infection. The prevalence of Hp infection in households was 80.29% (338/421), household size of 5, 6 and above were risk factors for Hp infection with Odds Ratios (ORs) of 4.09 (1.17–14.33) and 15.19 (2.01–114.73), respectively, household income ≥ 100,000 yuan and drinking boiled water from a tap source were protective factors for Hp infection with ORs of 0.52 (0.31–0.89) and 0.51 (0.28–0.95), respectively. The prevalence of Hp infection among minors in the household was 24.89% (58/233), with paternal infection and maternal infection as risk factors for child infection, with ORs of 2.93 (1.29–6.62) and 2.51 (1.07–5.89), respectively.

Conclusion

Hp infection was prevalent among Hainan families, and interaction with infected family members may be the primary cause of transmission.

Peer Review reports

Introduction

Helicobacter pylori (Hp) is a gram-negative bacterium that colonizes the gastric mucosa and is clearly certified as a class I carcinogen for gastric cancer [1]. In 2015, there were approximately 4.4 billion persons worldwide infected with Hp, with the rate of infection in China ranging from 20.6% to 81.8% due to the enormous territory and varied levels of development in different regions [2, 3]. Hp is transmitted from person to person, particularly between family members, and an infected family member can be a serious source of infection, putting other family members at risk [4]. Hainan Province is located in the southernmost part of China and only surveys of Hp infection in specific populations are available. There are no large-scale surveys of household Hp infection status in the population of Hainan Province. Moreover, the patterns of intra-household transmission of Hp and factors associated with pathogenicity are not known. The aim of this study is to evaluate the prevalence of Hp infection, related risk factors, and possible channels of transmission in the average household in Hainan Province. The findings will contribute to gather evidence on the familial aggregation of Hp infection in the Hainan region.

Methods and materials

Study population

Based on a 50% Hp prevalence rate in China and a relative error of 5% (α = 0.05), the required sample size was calculated to be 1536. The study was conducted from July 2021 to April 2022 in five prefecture-level cities in Hainan Province, specifically Haikou, Danzhou, Dongfang, Wenchang, and Changjiang Li Autonomous County, where study participants were recruited. A total of 1,454 people participated in the questionnaire and test, with a response rate of 94.7%. Based on the results of the questionnaire, 421 households (1355 persons) were finally screened out after excluding unqualified questionnaires. The study conducted by the researchers excluded certain sensitive groups such as pregnant women and breastfeeding mothers, as well as individuals taking proton pump inhibitors, antibiotics, bismuth or herbs with antibacterial effects within a month. Additionally, households with only one resident were also excluded from the study. Participants were recruited based on their actual co-residence, rather than their household registration. Co-residence was defined as living together for more than 10 months per year over the last 5 years, as determined by at least 2 permanent co-residents. All subjects in the study completed questionnaires and were tested for Hp.

Questionnaire

With the assistance of uniformly trained researchers, the questionnaire was completed by all participants or their guardians through scanning a QR code to access a small app on the WeChat platform. The researchers carefully collected data and excluded any invalid questionnaires. The questionnaire consisted of questions regarding personal characteristics, lifestyle and dietary habits, potential routes of Hp infection in children within the family, et al.

Testing for Helicobacter pylori

The 13C-Urea Breath Test (13C-UBT) is the most extensively researched and highly recommended non-invasive method for detecting Hp infection [5]. In this study, participants including adults, adolescents, and select children underwent the 13C-UBT using a uniform kit (Shenzhen Zhonghe Headway Bio-Sci & Tech Co., Ltd, Shenzhen, China). The participants were instructed to fast for at least two hours prior to the test in the morning. The first respiratory sample, labeled as sample 1, was collected in a blue exhalation collection bag. Following this, participants were instructed to take a urea 13C capsule with 80-100ml of drinking water and remain seated for 30 min. Afterwards, they were asked to exhale again, and this second sample was collected in a green exhalation collection bag labeled as sample 2. Testers analyzed samples 1 and 2 by using the 13C breath detector (HCBT-01, Shenzhen Zhonghe Headway Bio-Sci & Tech Co., Ltd, Shenzhen, China). If the delta over baseline value ≥ 4.0, the result was positive for Hp infection. The stool antigen test (SAT) is an alternative detection method with high specificity and sensitivity [6]. As part of the study, children primarily under the age of 4 or those unable to cooperate in the 13C-UBT underwent SAT. Fresh fecal samples were collected from participants and tested using the Hp antigen test kit (Huagen tailai Biotechnology Co., Ltd, Jiangsu, China). In a clinical trial in Xiamen, China, the sensitivity of the SAT reached 93.8% and the specificity reached 96.6% [7]. A positive result for Hp is indicated by a red T line on the test. If at least one member of a family is infected with Hp, the entire family is considered Hp-infected. Conversely, if no members of a family are infected with Hp, the family is considered Hp-uninfected.

Statistical analysis

This study used SPSS statistical software version 26.0 (IBM Corporation, Armonk, NY, USA) to analyze data. The count data was presented using frequencies and rates (%), and statistical comparisons between groups were conducted using the chi-square test, Fisher's exact probability method, and the continuity correction test. The measurement data was presented as mean ± standard deviation, and group comparisons were conducted using t-tests. Statistical significance was determined at a bilateral p-value < 0.05. In this study, logistic regression analysis was utilized to evaluate the potential factors affecting Hp transmission. The findings were reported as an Odds Ratio (OR) along with its corresponding 95% Confidence Interval (CI).

Result

Helicobacter pylori infection in individuals

A total of 1355 individuals were tested for Hp infection, with 629 (46.42%) testing positive and 726 (53.58%) testing negative. The prevalence rate varied by age group, with the lowest rate of 21.17% (29/137) found in the 0–9 years age group and the highest rate of 57.58% (95/165) found in the ≥ 60 years age group. The prevalence of Hp infection generally increased with age, particularly in the 0–40 years age group, and decreased in the 40–60 years age group. However, it reached its highest point in individuals aged 60 years or older (Fig. 1).

Fig. 1
figure 1

Helicobacter pylori infection status in patients of different age groups 

Note: Hp Helicobacter pylori 

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In a univariate analysis, we screened for significant effects of age, education level, and marital status (p < 0.05) on an individual's Hp infection status. Subsequently, a multifactorial analysis revealed that only age had a greater effect on Hp infection in the population. With the age range of 0–9 years as the reference, the risk of Hp infection was higher in those aged 20 years and older, with the highest risk of infection in those aged 60 years and older with an OR of 4.01 (1.83–8.79). Considering that the population included in this study was all-age, and that age actually had a greater influence on marriage and education level, we excluded the age factor and found that married, middle school and education above high school and college were risk factors for Hp infection, with ORs of 1.64 (1.27–2.13), 1.64 (1.18–2.29) and 1.65 (1.22- 2.22) (Table 1). Of the five prefecture-level cities in Hainan Province, Danzhou had the highest rate of Hp infection at 52.14%, while Wenchang had the lowest rate at 43.57%. However, there was no significant difference in the positive infection rate between different regions (p > 0.05) as shown in Fig. 2. Other factors such as gender, ethnicity, some lifestyle habits such as drinking raw water, washing hands before and after meals, location and frequency of eating out, and history of gastrointestinal symptoms or diseases were found to have no significant effect on Hp infection (Table 1).

Table 1 Prevalence of Helicobacter pylori infection and general information of the individual
Full size table
Fig. 2
figure 2

Distribution of Helicobacter pylori positive infection rate in each involved municipal area in Hainan

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Helicobacter pylori infection in households

Out of the 1355 people, there were a total of 421 households with more than 2 members per household. Among these households, 80.29% (338/421) had at least 1 family member infected with Hp, while 19.71% (83/421) had no household members infected with Hp. Additionally, the infection rate tended to increase as the size of the household increased (Fig. 3).

Fig. 3
figure 3

The general status of Helicobacter pylori infection in the family Note: Infected family: At least one family member infected with Helicobacter pylori

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In households infected with Hp, more than half of them consisted of 2–3 persons. Among all infected households, 1 and 2 persons were the most commonly infected with Hp, accounting for 40.53% and 36.39% respectively. When the household size was 5 or more people, 2–3 people were more likely to be concurrently infected with Hp (Table 2). Figure 4 displayed the distribution of Hp-uninfected households and Hp-infected persons, indicating that larger households had a lower distribution of Hp-uninfected individuals.

Table 2 Distribution of Helicobacter pylori infection among family members
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Fig. 4
figure 4

Distribution of Helicobacter pylori infection in the household

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The risk of Hp infection was higher in households with 5, 6, or more persons, with ORs of 4.09 (1.17–14.33) and 15.19 (2.01–114.73), respectively. Conversely, households with an income of ≥ 100,000 yuan and those that drank boiled water from tap sources were found to be protective factors against Hp infection, with ORs of 0.52 (0.31–0.89) and 0.51 (0.28–0.95), respectively. Other factors such as living area, family history of disease, domestic animals, and family habits such as meal gatherings, use of communal chopsticks, and sharing of objects did not have a significant effect on household Hp infection (Table 3).

Table 3 Prevalence of Helicobacter pylori infection and general information of the family
Full size table

Helicobacter pylori infection in minors

A total of 233 minors, consisting of 119 boys and 114 girls, were included in the study. Of these minors, 24.89% (58/233) were infected with Hp and 75.11% (175/233) were not infected. The minors were divided into six age groups, with the highest infection rate of 34.78% (8/37) occurring in the 16–18 years old group. As shown in Fig. 5, there was a tendency for the infection rate to increase with age. However, the rate of Hp positivity did not show a significant difference among the age groups (p > 0.05).

Fig. 5
figure 5

Helicobacter pylori infection status in children of different age groups

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In the study examining the factors contributing to Hp infection in minors, it was found that father's infection and mother's infection were risk factors for children's infection, with ORs of 2.93 (1.29–6.62) and 2.51 (1.07–5.89) respectively in the multivariable logistic regression analysis. Lifestyle habits such as drinking raw water, washing hands before and after meals, and close interaction with parents (including mouth-to-mouth kissing) did not have a significant effect on Hp infection in minors, even when infected by other elders (Table 4).

Table 4 Prevalence of Helicobacter pylori infection and the lifestyle of children in the family
Full size table

Discussion

According to recent studies, approximately 589 million people in mainland China have been infected with Hp. While the rate of infection has decreased compared to 20 years ago, the burden of infection remains high. While the traditional "screen and treat" approach has been recommended for treating individuals infected Hp, in 2021 China proposed a new family unit-based treatment strategy to prevent further transmission of Hp among family members by systematically following up and screening for the Hp status of other family members of those infected with Hp, as well as evaluating and treating them [8]. On top of this, exploring potential modes of Helicobacter pylori transmission within families can aid in mitigating the risk of both initial infection and reinfection.

This study investigated the Hp infection status of 1355 individuals from 421 households on Hainan Island and analyzed the factors influencing Hp infection using a questionnaire. The findings revealed that 80.29% (338/421) of households had at least one person infected with Hp. These results suggested that a significant proportion of households on Hainan Island were at risk of Hp infection. In the analysis of factors influencing household Hp infection, it was found that family size of more than five people was a risk factor. Since each person in the household was susceptible to Hp, having more people in the household meant more individuals were at risk and therefore increased the likelihood of exposure to Hp infection. In contrast, high income (≥ 100,000 yuan) and consumption of boiled tap water were found to be protective factors against the transmission of Hp. This finding was consistent with previous studies that have identified factors influencing Hp transmission [9, 10]. Hp can be transmitted through various water sources, including bottled water, tap water, and well water. Additionally, Hp can adhere to different materials and coexist with other bacteria in pipes and on water surfaces [11, 12]. Hp can withstand challenging conditions such as micro-oxygenation and pH levels ranging from 4.5 to 9.0. It can even survive for up to two weeks at a temperature of 4°C [13, 14]. The prevalence of Hp in drinking water was high, with a global average of 15.7%, and drinking such water can lead to Hp infection [15]. To prevent this, it is recommended to follow good hygiene practices, such as drinking boiled and professionally disinfected tap water.

In addition to external factors, such as contaminated water or food, that can lead to family-based Hp infection, it is important to also consider the oral-oral route of transmission. This survey found no correlation between household members' use of public utensils and household products and Hp infection. It is important to note that Hp must pass through the mouth before colonizing the stomach and can be detected in various oral sources such as plaque, saliva, tongue, and dental pulp [16]. The oral cavity, as the first reservoir of Hp outside the stomach, was closely related to Hp infection in the stomach [17]. In China, it is common for family members to use their own cutlery, such as chopsticks and spoons, to obtain and share food during meals. However, an Australian study has shown that the use of chopsticks may promote Hp infection due to the possibility of cross-contamination during this process [18]. However, this study on Hp detection was based on a serological test and did not directly prove the presence of these microorganisms on the chopsticks. A subsequent trial in Hong Kong detected Hp by PCR in the saliva of 15 (33%) Hp-infected subjects and in the chopsticks of one (2%), indicating a high likelihood of direct transmission of the bacteria through infected saliva. Although the detection rate of Hp on chopsticks is low, it is still infectious, and communal utensils should be used with caution during meals [19].

This study also analyzed Hp infection on an individual unit basis and the factors influencing Hp infection. The results showed that 46.72% of the participants were infected with Hp, which is consistent with the medium prevalence of Hp in Hainan Province, relative to other provinces in China. The study investigated the prevalence of Hp-positive infections across different age groups. The results showed that the prevalence increased with age, particularly in the 0–40 age group, which is consistent with previous studies [10, 20]. It seemed that the risk of Hp infection in the population was concentrated in children and young adults, thus, the study focused on analyzing Hp infection in minors.

The survey found that the prevalence of Hp infection among infants and children aged 0–3 years was as high as 23.54%. The prevalence of infection varied between countries and regions. Studies in Norway showed almost no infection in children aged 0–11 years (0.6%), while Turkey had 10.71% infection in children aged 0–5 years. In Wuwei, Gansu Province, China, 12.6% of infants aged 0–3 years had infection, while in Hong Kong, 9.3% of children aged 6–9 years were infected [10, 21,22,23]. The results suggested a correlation between the economic status of an area and the prevalence of Hp infection in children, with more economically developed areas having lower rates of infection. However, further validation through normative studies with larger samples and a wider range of areas is necessary due to variations in sample size, testing protocols, and survey time across studies. This study confirmed that the majority of Hp infections occurred during early childhood, as evidenced by the high prevalence of infection among children aged 0–3 years. A previous study of 231 Israeli children found that Hp infection typically occurred around 14 months of age, and identified low income, low-education parents and poor hygiene practices (such as infrequent sterilization of bottles and teats) as important risk factors for Hp infection during infancy [24]. Breastfeeding has been found to reduce the risk of Hp infection in infants [25]. Additionally, a study has shown that specific immunoglobulin A antibodies found in breast milk can delay Hp fixation in infants [26]. However, children attending day-care facilities have been found to be at an increased risk of infection. The risk of infection was observed to increase significantly with the cumulative time spent in day-care centers (p < 0.001) [27].

The study found that the prevalence of Hp infection increased with the age of the child, particularly in those who were 10 years or older, with rates exceeding 25%. The risk of infection in children was also found to be higher when family members, especially fathers (OR: 2.93, 95% CI: 1.29–6.62) and mothers (OR: 2.51, 95% CI: 1.07–5.89), were infected, which was in line with previous cross-sectional studies [28, 29]. Most studies have confirmed that parents play an important role in the transmission of Hp within the family, especially as mothers, whether based on genetic analysis or 13C-UBT [30,31,32]. Studies from Germany showed that paternal Hp infection was a risk factor with a crude OR of 7.8 (95% CI, 2.5–24.2) and an OR of 3.8 (95% CI, 0.8–19.1) after adjusting for potential confounders (except maternal infection) [33]. This indicates that the role of fathers in spreading hp within the family cannot be ignored. At the same time, the longer the exposure time of HP-positive parents caring for their children, the greater the risk of infection of the child. In this study, fathers had a more significant OR value, and it cannot be ruled out that fathers were the main caregivers in the convenient sample population for this study.

A study conducted in Japan found that the strains of Hp isolated from children were similar to those of their siblings [34]. Similarly, a Swedish study that compared strains isolated from Hp-infected children aged 10–12 years in school and their infected family members arrived at similar conclusions [4]. The transmission of Hp was found to be stronger from mother to child than between father and son or siblings. This mode of transmission played a key role in the spread of Hp [35]. According to data released by the Hainan Provincial Bureau of Statistics in 2021, the average number of persons per household in Hainan Province decreased from 4.86 in 1982 to 3.06 in 2021. Due to the one child per household family planning policy encouraged from 2002 to 2016, it was even less likely that most families had children with Hp infection had originated from their siblings [36].

The survey also indicated that individuals with education beyond junior high school and those who were married were at higher risk of Hp infection. The transmission of the infection between spouses was also a significant factor to consider, in addition to the transmission from parents to children. A German survey found that the risk of Hp infection increased with the number of years an individual lives with an infected partner, indicating that Hp can be transmitted between spouses [37]. The Swedish study used methods such as random amplified polymorphic DNA markers to validate isolated strains in 23 couples who were both infected with Hp. The results revealed that five of the couples shared the same strain, thereby indicating the likelihood of inter-spousal transmission of Hp [4].

The prevalence of Hp infection in Hainan was still significant, particularly within households. This study served as a valuable resource for identifying the primary sources of household-based Hp infection and its transmission in Hainan. These findings reinforced the need for a family-based approach to Hp eradication treatment. The use of convenience sampling to obtain the sample for this study may have introduced bias in the selection of the population. However, the large sample size likely mitigated this effect. It is important to note that this was a cross-sectional survey study, and as such, the population was not followed up with a before-and-after control to establish causality. Further research is needed to strengthen the conclusion of this study.

Availability of data and materials

Data for this study can be obtained by contacting the corresponding author by email.

Abbreviations

Hp :

Helicobacter pylori

OR:

Odds Ratio

13C-UBT:

13C-Urea Breath Test

CI:

Confidence Interval

SAT:

Stool Antigen Test

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Acknowledgements

Authors would like to thank all the volunteers, researchers and funding support who participated in this study.

Funding

This project was supported by Health Industry Research Projects of Hainan Province (20A200456), Natural Science Foundation of Hainan Province (823RC603) and Health Industry Research Projects of Hainan Province (22A200319).

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Authors and Affiliations

  1. Department of Gastroenterology, Central South University Xiangya School of Medicine Affiliated Haikou Hospital, Haikou, China

    Danni Liu, Jing Pan, Zhengyi Chen, Sailian Li, Jiamei Ma, Yening Xiao & Xiaoxi Huang

  2. Department of Pediatrics, Central South University Xiangya School of Medicine Affiliated Haikou Hospital, Haikou, China

    Danhong Wang

  3. Department of Gastroenterology, Hospital of Wuhan University, Wuhan, China

    Ganggang Mu

  4. Department of Gastroenterology, Tongji Wenchang Hospital of Huazhong University of Science and Technology, Wenchang, China

    Ya Lin

  5. Department of Gastroenterology, Hainan West Central Hospital, Danzhou, China

    Juyuan Li

  6. Digestive Endoscopy Center, Dongfang People’s Hospital, Dongfang, China

    Zhai Chen

Authors
  1. Danni Liu
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  2. Jing Pan
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  3. Zhengyi Chen
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  4. Sailian Li
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  5. Jiamei Ma
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  6. Yening Xiao
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  7. Danhong Wang
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  8. Ganggang Mu
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  9. Ya Lin
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  10. Juyuan Li
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  11. Zhai Chen
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  12. Xiaoxi Huang
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Contributions

Zhengyi Chen, Xiaoxi Huang, Ganggang Mu developed the theoretical formalism of the study. Danni Liu, Jiamei Ma, Danhong Wang, Ganggang Mu, Ya Lin, Juyuan Li, Zhai Chen, Sailian Li conducted surveys and collected data. Jing Pan, Yening Xiao analyzed the data. Danni Liu, Xiaoxi Huang edited the manuscript. Xiaoxi Huang supervised the project. All authors reviewed the manuscript.

Corresponding author

Correspondence to Xiaoxi Huang.

Ethics declarations

Ethics approval and consent to participate

This study was conducted in strict accordance with the Declaration of Helsinki. All subjects received informed consent and signed informed consent forms. Meanwhile, the Ethics Committee of Haikou People's Hospital approved the study. For minors, we have obtained the informed consent of their guardians. This study was registered with the China Clinical Trials Registry (www.chictr.org.cn; registration number: ChiCTR2100051229).

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Not applicable.

Competing interests

The authors declare no competing interests.

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Liu, D., Pan, J., Chen, Z. et al. A survey on the current status of Helicobacter pylori infection in households in Hainan Province, China. BMC Gastroenterol 23, 426 (2023). https://doi.org/10.1186/s12876-023-03010-z

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  • DOI: https://doi.org/10.1186/s12876-023-03010-z

Keywords

BMC Gastroenterology

ISSN: 1471-230X

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