Prevalence and associated risk factors for Helicobacter pylori infection using stool antigen test among children presenting to the outpatient clinic of a tertiary hospital in Nigeria

INTRODUCTION

Helicobacter pylori is a ubiquitous Gram-negative spiral, flagellate bacillus organism infecting about 50% of individuals globally.^[1,2] The distribution of H. pylori infection is influenced by age, sex, geographical location, ethnicity, and socioeconomic factors.^[3-5] The geographical distribution of H. pylori shows higher prevalence in developing countries of Africa, South America, and South-east Asia when compared to the developed countries, ranging from 5% in developed countries to 80% in developing countries.^[6-13] Li et al.,^[14] in a systematic review and meta-analysis, showed a declining trend in the pooled prevalence of H. pylori infection, particularly in the 2011–2022 period to 43.1% compared to 58.2% in 1980–1990 period globally, with the largest decline seen in the World Health Organization African region with a prevalence of 58.3%, this region still had the second highest prevalence following the Eastern Mediterranean region with a prevalence of 59.1%. In Nigeria, the prevalence of H. pylori infection ranges from 20% to 69%. The variation in the prevalence rate depends on the geographic region, location of studies such as hospital or community-based studies, type of diagnostic method used for the study, and socioeconomic and environmental factors ^{[8,9,12,15-21]} Infection with H. pylori occurs mostly through the faeco-oral or oro-oral routes and the risk factors includes poor socioeconomic status, overcrowding in household, poor personal and environmental hygiene, infection among household members, poor water supply, and fecal waste disposal method.^[22-24]

Most infections occurring in early childhood are asymptomatic and may persist for life if left untreated.^[2] However, some may present with gastrointestinal (GI) symptoms, including abdominal pain, diarrhea, gastric reflux, and peptic ulcer disease.^[9,25,26] Chronic infections could lead to chronic gastritis, mucosa-associated lymphoid tissue lymphoma, gastric cancer, and gastric adenocarcinoma.^[26,27]

H. pylori can be isolated using invasive and non-invasive methods.^[25] The type of diagnostic method used to isolate H. pylori contributes to variable infection rates in children.^[28] The invasive methods include an upper GI endoscopy with biopsies taken using modalities such as rapid urease test, culture, and histology.^[25] In developing countries, upper GI endoscopy is expensive, the expertise and cost of the procedure is not within the reach of many.

Non-invasive methods have gained wider acceptability, and these include serology tests, urea breath tests, fecal antigen tests, and fecal polymerase chain reaction assay.^[29] The sensitivities of the invasive and non-invasive tests are relevant and comparable in clinical practice.^[29,30] The H. pylori stool antigen (HpSAg) test has high sensitivity and specificity, has gained popularity, and is almost readily available in all hospitals.

Due to the geographic variations, which include intra-country variations and different epidemiologic factors associated with infections with H. pylori, local studies are imperative to assess for the prevalence and risk factors of H. pylori as this could assist in marking out preventive measures for the locality. There were no studies on H. pylori infection in children using faecal antigen test presenting to the University of Calabar Teaching Hospital (UCTH), Calabar, South-south Nigeria. This study aimed to determine the prevalence and associated factors of H. pylori infection in Nigerian children aged 3–18 years of age using the fecal antigen test.

MATERIAL AND METHODS

RESULTS

DISCUSSION

Our study showed an overall prevalence of 27.2% for H. pylori infection among children presenting to UCTH, Calabar. This finding was comparable to those reported among children in other hospital-based studies in South-south^[8] and neighboring South-east^[20] Nigeria, with prevalence of 30.9% and 20%, respectively. However, the prevalence rate in this study was lower than the 65.7% and 69% reported in South-west^[9] and North-east^[21] Nigeria, respectively. The wide variation in prevalence rates reported from studies in different regions of Nigeria could be explained by the sociodemographic, environmental, and cultural factors in different parts of Nigeria. The use of serology tests in some of these studies may also account for the higher prevalence rates, as serological methods give higher false rates compared to stool antigen tests, as the antibodies to H. pylori can persist for several months after eradication.^[14]

The prevalence of H. pylori in this study was comparable to the 24.3% reported in a hospital-based study in Ugandan children aged 1–15 years using a similar stool antigen test.^[11] It was, however, lower than the prevalence of 60.4% reported among 3–10-year-old children in Benin Republic^[33] or the 65.7% among 10–19-year-old adolescents in Ethiopia.^[34] The variations in H. pylori prevalence rates worldwide are thought to be due to differences in levels of urbanization, access to good water, sanitation and hygiene services, and socioeconomic status.

Sociodemographic characteristics are widely regarded as being associated with H. pylori infection status. Low socioeconomic class is considered an important risk factor for the acquisition of H. pylori infection. This is due to its attendant consequences of poor hygiene and unsanitary conditions, which strongly predispose toward the acquisition of H. pylori infection. This study showed a significant inverse relationship between socioeconomic status and H. pylori infection. This is consistent with results from studies conducted in Nigeria and other parts of the world. In Owerri, South-east Nigeria, H. pylori prevalence was 14.3% and 50% in upper and lower social classes, respectively.^[20] In Uyo, South-south Nigeria, higher H. pylori seroprevalence was associated with low social class.^[8] In Japan, a cross-sectional study found that the prevalence of H. pylori infection linearly decreased with increasing socioeconomic status.^[35]

The previous studies report conflicting findings on the association between H. pylori infection and diarrhea. This study found an association between H. pylori infectivity and diarrhea, with prevalence higher among children who had diarrhea in the preceding 1 year compared to those who did not. This result is in agreement with several studies which reported a positive association between H. pylori infection and diarrhea. A study among Gambian children found that 53% of infants with chronic diarrhea and malnutrition were infected with H. pylori when compared with 26% of age-matched healthy controls.^[36] Similarly, a multicenter study on the incidence, etiology, and adverse clinical consequences of diarrhea among children in developing countries found a significant association between H. pylori and diarrhea.^[37] These studies may suggest the possibility that H. pylori infection increases susceptibility to other enteropathogens or is simply a comorbid condition since it shares similar routes of transmission and, thus, risk factors with diarrheal pathogens. In contrast, a large population-based study in Germany found a strong inverse association between gastric carriage of H. pylori and the occurrence of diarrhea in children.^[38] The contrast in findings between studies in a developed country like Germany and those in developing countries may be explained by contrasting exposure to enteric pathogens and differing availability of water, sanitation, and hygiene services, and most diarrhea in developed countries are due to chronic inflammatory diseases and not faeco-oral diarrheal microbial agents as is the case in developing countries.^[39] Further studies are required to determine the true relationship between diarrhea and H. pylori infection.

The educational level of a child’s parents, either independently or as a surrogate for socioeconomic status, is associated with H. pylori infection status. Our data showed that the prevalence of H. pylori infection significantly increased with a decrease in parental educational levels. This finding is consistent with data from earlier studies, which found an inverse association between the educational level of parents and H. pylori positivity. In China, a cross-sectional study among children aged 0–12 years found that having parents with a higher educational level was a protective factor against H. pylori infection.^[40] Likewise, a systematic review and meta-analysis of observational population-based studies found that lower education of parents was significantly associated with a higher prevalence of H. pylori infection in children.^[28] A higher educational level is believed to be associated with greater knowledge of good sanitation and personal hygiene practices which act to reduce the risk of H. pylori infection. The significant association between socioeconomic status and parental level of education with H. pylori infection indicates that poverty alleviation, provision of jobs, and improved access to education may be employed as strategies for H. pylori prevention among children in Calabar.

Household-level factors found to be significantly associated with H. pylori infection in this study were the location of residence, the number of rooms in the house, and the method of household waste disposal. Residence in a rural area was significantly associated with a higher prevalence of H. pylori than urban residence. This is in keeping with findings in a recent meta-analysis of global studies that the prevalence of H. pylori infection was higher in rural areas than in urban areas.^[28] The higher prevalence among rural residents may be explained by the lack of access to good healthcare services, lack of potable water supply, poor sanitation and hygiene services, and low levels of education and poverty, which are common in rural areas in Nigeria. Living in a home with less than three rooms was a risk factor for H. pylori infection in children in this study. This may indicate that the relative lack of space in homes with less than three rooms enhances interpersonal contact, thereby facilitating the transmission of H. pylori. Thus, this finding provides further evidence in support of household crowding as a risk factor for H. pylori infection, as reported in earlier studies.^[8,11,40] This study also found that disposal of household waste in open pits was associated with increased H. pylori prevalence compared to waste disposal in the bush or the practice of burning waste. Similarly, Etukudo et al.^[8] found that open space disposal of household waste had a higher risk prediction for H. pylori infection than other waste disposal methods. This finding is presumably because refuse disposal pits are usually close to residential areas and are easily accessible to houseflies, thus increasing vector-borne transmission of H. pylori from fecal matter to food. There was no significant association between H. pylori positivity and other household variables studied, including number of persons in the house, bed-sharing, source of drinking water in the house, and method of home sewage disposal. This could be due to similarities in these characteristics among most of the study participants.

Several studies in the literature have established unclean water as a source of the spread of H. pylori.^[8,11] Source of drinking water in schools was significantly associated with H. pylori infection of study participants. The provision of potable water supply in schools in Calabar would go a long way in reducing the prevalence of H. pylori infection among children. This study showed no association between the type of toilet in the school and H. pylori infection. There was also no association between hygiene-related variables such as washing hands before eating or after defecation and H. pylori infection status of children in Calabar. These findings of no association between some variables assessed and H. pylori infection status may be because most of the children studied had similar characteristics.

After multivariable logistic regression analysis, having less than three rooms in the house, disposal of household waste in the bush, residence in urban areas, and having diarrhea in the past 1 year remained significant as independent predictors of H. pylori infection among children in Calabar. These findings are in keeping with the predisposing factors to H. pylori infection, as demonstrated in other studies.^[9-11]

The limitation of this present study is that the study was hospital-based; therefore, the prevalence may not be a true reflection of the prevalence of the infection in the communities.

CONCLUSION

The study showed a high prevalence of H. pylori infection among children presenting to the UCTH. Living in a house with less than three rooms, poor disposal of household waste, poor source of drinking water in schools, and a past history of diarrhea were risk factors for H. pylori infection. Public health education and the provision of potable water in schools are, therefore, advocated to curb H. pylori infection.