Helicobacter pylori (H. pylori) was first discovered in 1983 by Warren and Marshall [1]. It is well-known as a pathogenic bacteria that causes gastric-related diseases such as gastritis and peptic ulcers [2, 3]. H. pylori is also recognized as bacterial carcinogen that contributes to the development of gastric cancer later in life [4]. Numerous studies have also reported a strong relationship between H. pylori infection and development of gastric cancer [3, 5, 6]. Furthermore, its role in extra-gastroduodenal disorders including iron deficiency anemia, and idiopathic thrombocytopenic purpura is also well documented in recent reports [3, 7]. These H. pylori-related gastric diseases and other-related disorders together cause over a million deaths each year, making H. pylori infection one of the most severe issues to public health worldwide.

H. pylori infection is mainly acquired during childhood and colonizes human gastric mucosa lifelong if not treated [3, 8]. School-going children are at high risk of infection and many infected pupils do not show any gastroduodenal symptoms up to adulthood [3, 9, 10]. According to a recent systematic review, the worldwide prevalence of H. pylori among children was found to be 32.3% [11]. It also reported that the incidence rate of H. pylori was significantly higher in low-income and middle-income countries than in high-income countries (43.2% vs. 21.7%) and in older children than in younger children (41.6% in 13–18 years old vs. 33.9% in 7–12 years old vs. 26.0% in 0–6 years old). Furthermore, several evidences indicated that H. pylori can be transmitted from person to person through possible routes, including oral-oral, and fecal-oral [3, 10]. Therefore, the bacteria can silently spread from asymptomatic infected individuals to others within family or in communities for an extended period of time, which might lead to high burden of H. pylori infection in community with a great impact on the public health system. However, the transmission patterns of H. pylori in children, compared to adults, remain scarce. Given that providing further insights on transmission modes and possible risk factors of H. pylori infection in asymptomatic children are essential for public health sector to build optimal prevention and reduction H. pylori programs.

H. pylori affects over 50% of the global population and its distribution dramatically varies both between and within countries [12]. The prevalence of H. pylori infection greatly decreased in developed countries, but it is still prevalent in developing countries—particularly in Asia with some countries reporting a prevalence of up to 90% [12]. Some recent studies pointed out that this different trend probably reflects the level of urbanization, sanitation, access to clean water, and varied socioeconomic status, but the exact reasons for this variation are not fully discovered yet [3, 12]. Like other developing countries in South-Eastern Asia, H. pylori infection in Vietnam remains high [12, 13]. A study conducted in Ha Noi city, the largest city in the North of VietNam, showed a sero-prevalence of H. pylori infection of 76.8% [14]. It was also reported that poor socioeconomic status, improper hygiene practices, and overcrowding living conditions were risk factors for getting H. pylori infection. A recent paper reporting on prevalence of H. pylori in school-aged children of Ho Chi Minh city (HCMC) showed the prevalence in the range of 80.2% in girls aged 12–15 years to 93.3% in boys aged 9–11 years [19]. There was no available community-based study focused on the mode of transmission and potential risk factors for acquiring H. pylori infection in HCMC, despite it is the biggest city in the South of VietNam. All previous studies on risk factors of H. pylori conducted in VietNam had small sample sizes and used serological tests which are known to have low accuracy in children [14–16]. In addition, there are big socio-economic and geographic disparities between HCMC and other investigated regions in VietNam. Therefore, identifying the route of transmission and associated risk factors for H. pylori infection in a large sample of school-aged children population of HCMC by using reliable tests are needed to develop preventive strategies in specific setting of HCMC.

We therefore conducted a community-based study of a large sample of school-aged children who were assessed for H. pylori infection by stool antigen test, to investigate possible risk factors and the route of transmission that may be associated with H. pylori infection in school-aged children in HCMC.

A total of 1,476 school-aged children were enrolled in this study. Out of these pupils, 13 were excluded due to failure to meet inclusion criteria or not performing the stool test. Observations with missing child age, child sex, number of people, number of children in household, parent’s education, parent’s occupation, types of toilet, and methods to treat water were also excluded from the analysis. Ultimately, the remaining 1,409 pupils were included in the final analysis (Figure 1).

Overall, the prevalence of H. pylori infection among school-aged children in HCMC was 87.7%. Younger age, living in crowded areas (super-urban area, urban area, peri-urban area), larger family size, infrequency of handwashing with soap after toilet, using only water or both water and paper to clean after toilet were independently associated with an increased prevalence of paediatric H. pylori infection.

In our analysis, the prevalence of H. pylori significantly increased when the level of parent education decreased in univariate analysis, but this significant association was not observed in multiple analysis. This was explained by a correlation between level of education and living area. In fact, families with high level of education usually tend to live in central areas, where people can easily access most of commercial, educational, or business centers within a short distance. This inverse association was also comparable to a study of Nguyet et al. conducted in the North of Vietnam, which indicated low parental education as a risk factor of acquiring H. pylori [22]. This finding was also consistent with other reports from China [23], Pakistan [24], Iran [25] which also pointed that children whose parents had a lower education level were significantly at a higher risk of H. pylori infection. In addition, our study found that pupils with parents who completed only primary school had a higher prevalence than those with parents who completed a higher educational degree. A lower level of education can make harder to understand health message. A lower income level leads to live in smaller and more crowdy spaces, and so increased the chances to contract a H. pylori infection.

H. pylori infection was not significantly associated with the wealth status of a household, which was inconsistent with previous studies [26–28]. A possible reason for these conflicting findings might be the different methods used to assess the wealth status. Most previous studies used family monthly income and expenditure, or a combination of multiple indicators such as education level, occupation, and monthly earnings to categorize the wealth index. However, data on income and expenditure were not available in our study. We therefore built the household wealth index based on the ownership of 28 household assets following the DHS guidelines for Vietnam [21]. These items were easy to collect and to measure for researchers compared to using monetary indicators. However, the guideline was published several years ago and might be less appropriate at the time that our study was conducted. Therefore, further analyses are needed to discover and verify an appropriate method for evaluating the wealth index of Vietnamese population.

H. pylori could spread from person to person through two main routes: the oral-to-oral route, and the fecal-oral route. The second route was identified to be the predominant mode for H. pylori transmission in several studies [10, 29]. In addition, the pathogen in feces can spread by the fecal-oral route from one person to another’s oral cavity through contaminated food, surfaces, or water, which is mainly caused by a lack of adequate sanitation and poor hygiene practices [3, 9, 29]. In our findings, the prevalence of H. pylori infection was significantly higher in pupils who infrequently washed their hands with soap after toilet, and it was significantly lower in participants who used only paper to clean after toilet. Interestingly, when carefully assessing the two hygiene factors, results showed that there was an increasing trend in prevalence of H. pylori infection: lowest in participants who always washed their hands with soap and used only paper to clean after toilet usage (81.5%), followed by pupils who always washed their hands with soap and did not use paper to clean after toilet usage (88.9%), and highest in individuals who rarely or sometimes washed hands with soap whatever using or not using paper to clean after toilet (91.5%). These evidences support that unhygienic toilet conditions, particularly poor handwashing behavior, increase the possibility of contact with fecal material, which can create an infection vehicle of H. pylori and cause the spread of the bacterium both within the family and within the community. In addition, sharing cups or dishes or sauces or foods was not associated with H. pylori infection in our findings, suggesting that the oral-oral transmission might not play a main route in spreading H. pylori in children in HCMC. Based on these findings, the fecal-oral route appears to be the most likely mode of transmission for H. pylori infection among school-aged children in HCMC. Therefore, educating and improving hygiene practices are essential to control the transmission of H. pylori and reduce the burden of this infection in the community.

Waterborne infection can be an important route of H. pylori infection, particularly in developing countries with a high prevalence of acquiring H. pylori [9]. Several studies pointed to a positive association between H. pylori infection and the consumption of well water [10, 30]. Other reports also found a strong correlation between H. pylori infection and the source of drinking water [27, 31]. However, water-related variables (source of drinking water or cooking water or methods of water treatment) were not correlated with H. pylori prevalence in our study, supporting that the water supply may not act as a reservoir for the transmission of H. pylori in the population of HCMC. Indeed, HCMC replaced, developed, and installed new water distribution systems over the past 10 years to ensure treated water for 100% population of the city from 2015 [32]. However, some households are still using well water instead of treated water from the government.

Our study is the first to use a random, so representative sample of school-aged children of HCMC to investigate the pathway of H. pylori transmission. Our results point the oral-fecal route as an important - but not isolated - pathway for H. pylori spread. Other routes of transmission such as oral-oral are not well documented yet.

Our study has several limitations. Firstly, we relied on the DHS guidelines to build a wealth index based on 28 household assets, but this approach may not be the most suitable way for assessing the wealth status of the family. Several studies showed that a combination of multiple indicators, including education level, occupation, and monetary indicators such as monthly income and expenditure, provides a more comprehensive wealth index compared to solely replying on house assets [26–28]. However, our study lacked data on monthly income and expenditure, which limited our ability to use those measures to evaluate the wealth status. Secondly, we did not examine the school environmental fators as availability of soap and water at handwashing sites, food-borne factors, sleeping conditions, that could potentially have a significant impact on the prevalence of H. pylori infection.