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Prevalence, associated factors, and clinical outcomes of Helicobacter pylori infection in pediatric populations in a war-torn urban environment in Eastern Democratic Republic of Congo: a mixed methods study

BMC Pediatrics volume 25, Article number: 257 (2025) Cite this article

Abstract

Background

Helicobacter pylori (H. pylori) infection remains a significant public health concern in developing countries, especially among pediatric populations where data are limited. In war-torn regions like the Eastern Democratic Republic of Congo, the impact of H. pylori infection on children's health may be exacerbated due to disrupted healthcare systems and limited resources.

Methods

This mixed-methods study, incorporating both cross-sectional and prospective cohort designs, was conducted at Samaritan Doctor's Pediatric Centre between January 2020 and December 2022. The study enrolled 323 children aged 0 to 15 years presenting with gastrointestinal symptoms. Sociodemographic and clinical characteristics were assessed via questionnaire, and H. pylori stool antigen rapid tests were performed. Multivariate regression analyses were conducted. Participants were followed up and outcomes recorded after 30 days.

Results

Of the 323 participants, 119 (36.80%) tested positive for H. pylori infection. Independent factors associated with H. pylori infection included age between 37 and 59 months (aOR: 9.76, 95% CI: 2.62–36.40, p = 0.001), caretaker’s occupation (aOR: 2.58, 95% CI: 1.19–5.54, p = 0.016), presence of pets at home (aOR: 0.371, 95% CI: 0.18–0.74, p = 0.005), drinking unsafe water (aOR: 0.13, 95% CI: 0.04–0.42, p = 0.001), anemia (aOR: 4.80, 95% CI: 1.12–20.53, p = 0.034), and presence of red blood cells in stool (aOR: 30.84, 95% CI: 13.97–68.10, p < 0.0001). Thirty days post-initial treatment with first-line medications (omeprazole, clarithromycin, and amoxicillin), 19.30% of patients remained positive for H. pylori.

Conclusion

Children with occult blood in stool and microcytic anemia should be tested for H. pylori using stool antigen tests. Treatment with clarithromycin should be guided by local antibiotic resistance data. Hygiene education, including safe water practices and managing pet contact, is crucial due to their association with H. pylori infection.

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Background

Introduction

Helicobacter pylori (H. pylori) is a microaerophilic, spiral-shaped, Gram-negative bacterium that infects the stomach lining. It is commonly associated with various gastrointestinal issues, presenting symptoms such as abdominal pain, nausea, and bloating [1]. This bacterium causes chronic inflammation of the stomach mucosa, leading to peptic ulcers and, if left untreated, more severe consequences like chronic active gastritis and gastric adenocarcinoma. Although H. pylori -related gastric cancer is rare in children, the infection itself remains clinically significant in the pediatric population due to its association with other gastrointestinal disorders. Globally, H. pylori infects approximately 50% of the population, making it one of the most widespread infections [2, 3].

While the prevalence of this infection has decreased in developed countries over the twenty-first century, H. pylori remains a significant health concern in low-income countries, often contributing to disability-adjusted life years (DALYs) [4]. H. pylori infection, although less likely to cause gastric cancer in children, still poses a significant health risk due to its potential to cause other severe gastrointestinal conditions [5]. In a review of data from population-based and clinical cancer registries, it was concluded that while gastric carcinoma is rare in children, a combination of H. pylori infection, tumour predisposition, and/or immunodeficiency appears to contribute significantly to the risk of developing gastric carcinoma at a young age [5]. Globally, approximately half of the population is affected by H. pylori infection, with prevalence rates ranging from 35 to 90% depending on factors like population diversity and geographic location [3]. The prevalence of this infection is not consistent across different societies; it varies based on geographic location, age, sex, and other socioeconomic factors, including ethnic group [6, 7]. In Japan, the prevalence of H. pylori infection among children ranged from 3.8% to 9.5%, whereas in Nigeria, it varied between 6.0% in the North-Central region and 28% in the South-Western region [8].

In African countries, where the prevalence of H. pylori generally exceeds 50%, it is crucial to understand the infection's impact on the pediatric population, especially in areas with limited healthcare resources. The highest prevalence rates have been reported in the Republic of the Congo (93.1%), the Democratic Republic of Congo (89.0%), Ethiopia (88.9%), Rwanda (75%), Cameroon (73.2%), and Burundi (70.8%)[8]. The association between H. pylori infection and gastric cancer is well established in adults. Evidence suggests that prolonged H. pylori infection, in conjunction with gastric atrophy and intestinal metaplasia, is associated with the development of intestinal-type and undifferentiated adenocarcinomas in adults[9].

In African nations, the incidence of gastric cancer is notably lower in pediatric populations compared to adults [5]. However, for children with H. pylori-associated gastric malignancies, there have been a few occurrences of gastric MALT lymphoma, but no cases of adenocarcinoma have been reported[10]. Nevertheless, regions with higher H. pylori prevalence demonstrate a more substantial disease burden, frequently exacerbated by insufficient healthcare infrastructure[5].

H. pylori infection in children is a significant public health concern influenced by a variety of factors. Age is a notable determinant, with older children frequently exhibiting higher infection rates[11, 12]. The educational level of the child's caretaker can also play a critical role, particularly in environments with varied levels of education and socioeconomic status[11, 13]. Environmental factors such as the presence of pets and consumption of unsafe water, along with familial elements like family size and bed-sharing practices, further contribute to the transmission within households [13, 14]. Abdominal symptoms including nausea, vomiting, and diarrhea, as well as associated complications like anemia characterized by hypochromia and macrocytosis, and gastrointestinal bleeding, as indicated by the presence of red blood cells in stool, are some clinical manifestations of H. pylori infection [9]. A family history of peptic ulcer disease (PUD) can indicate a genetic predisposition or shared environmental risk factors [10, 15]. Understanding these determinants is vital for developing targeted prevention strategies and improving diagnostic approaches for H. pylori infection in children.

The infection may occur in infancy and early childhood; if left untreated, the H. pylori infection generally persists throughout the individual's lifetime [3]. In comparison to adults, the understanding of H. pylori infection in children remains incomplete due to the prevalence of asymptomatic cases and limited research studies, which may contribute to an underestimation of the true prevalence [11]. However, childhood represents a critical period in the natural history of the infection [12]. Symptomatic children present with nonspecific symptoms such as abdominal pain, vomiting, or diarrhea[16]. Numerous studies concur on the interpersonal transmission of H. pylori infection within families as the primary route of contamination, with mother-to-child transmission being the most predominant mode. Oral-to-oral and oral-fecal transmission have been postulated through numerous papers as the principal routes of contamination[11]. In developing countries, H. pylori transmission is influenced by several factors, including low socioeconomic conditions, substandard drinking water, overcrowded living conditions, insufficient personal and environmental hygiene, and food contamination [17].

H. pylori treatment in children presents significant challenges, particularly in low- and middle-income countries[11]. The lack of routine culture and sensitivity testing in these regions complicates the selection of appropriate antibiotics, potentially leading to suboptimal treatment outcomes[16]. Healthcare providers in these regions often rely on empirical treatment strategies, which may inadvertently contribute to the spread of antibiotic resistance if ineffective regimens are used. This issue is further exacerbated by the rising global trend of clarithromycin resistance, which poses a threat to the efficacy of first-line treatment regimens [18]. Clarithromycin-based triple therapy has long been considered the standard first-line treatment for H. pylori infection in children. However, its effectiveness is increasingly questioned due to the growing prevalence of antibiotic resistance[16, 19]. Given these challenges, it is critical to evaluate the continued effectiveness of clarithromycin-based first-line treatments in pediatric populations, especially in areas where resistance patterns are poorly understood. The absence of culture and sensitivity testing in resource-limited settings creates a significant barrier to tailoring treatment approaches.

Over the past two decades, the eastern region of the Democratic Republic of Congo (DRC) has experienced armed conflicts, resulting in substantial population displacement toward more secure urban centres such as Goma city. Consequently, numerous families reside in overcrowded conditions, with suboptimal personal and environmental hygiene[20]. In Eastern DRC, data regarding the prevalence of H. pylori infection is limited, with research specifically focusing on children being particularly scarce. In this region, few studies have been conducted exclusively among adults or the general population in Bukavu, in the province of South-Kivu, and none among children [13, 14]. In conflict-affected areas, the impact of H. pylori infection on children's health may be exacerbated due to compromised healthcare systems and limited resources. However, specific data on H. pylori infection in children in war-affected regions are insufficient, necessitating further research to elucidate its prevalence, associated factors, and management outcomes in such contexts. To the best of our knowledge, there are no published data regarding H. pylori infection in children in North Kivu, particularly in Goma city. The primary objective of this research is to determine the prevalence, identify the associated factors, and investigate the treatment outcomes of H. pylori infection among children attending Samaritan Doctor's Pediatric Centre in Goma, Eastern DRC.

Methods

Study design and setting

A mixed study design was conducted at Samaritan Doctor’s pediatric centre between January 2020 and December 2022. Initially, a cross-sectional study design was used to assess the prevalence of H. pylori infection and its associated factors among study participants. Subsequently, a prospective cohort study was carried out to follow patients who tested positive for H. pylori. The Samaritan Doctor’s pediatric centre is located in Goma city, North Kivu province, in Eastern DRC. This clinic run from Monday to Monday, (24 h) and serves an average of 15–20 patients daily.

Study population

All study participant aged between 0 and 15 years with at least one of the following nonspecific abdominal symptoms: abdominal pain, nausea, vomiting, diarrhea, bloating, and burping, were enrolled. Children who had been treated with any combinations of medicines used to treat of H. pylori infection including metronidazole, clarithromycin amoxicillin, bismuth subsalicylate, omeprazole or any other proton pump inhibitor in less than two weeks prior to the clinic visit were not enrolled in the study. Children with any cognitive impairments secondary to neurologic problems such as cerebral palsy or any other causes, were also excluded from the study because they couldn’t effectively describe abdominal symptoms.

Sample size determination and sampling technique

The sample size was calculated using Daniel’s formula: \(n=\frac{{Z}^{2}* P*(1-P)}{{d}^{2}}\). Using findings from a study in Mbarara, in the Western Region of Uganda, where the proportion of H. pylori infection was 24.3% [17], P = 0.243. For 95% level of confidence, Z = 1.96 and d = 0.05. On substation, n = 283. After adding 14% to cater for loss of follow up, the required sample size was 323.

A total of 387 children with gastrointestinal symptoms and attending Samaritan Doctor’s pediatric centre were tested for enrolment into the study. Of these children, 64 were excluded from the study. Amongst them; 12 because having neurologic disabilities and 27 children were excluded because of having used a proton pomp inhibiter (omeprazole or Pantoprazole) or any combination of medications employed for the treatment or eradication of H. pylori (metronidazole, clarithromycin amoxicillin and bismuth subsalicylate). 348 children meet the inclusion criteria, however, 25 were excluded because they were accompanied by their caretakers, rather than parents/ legals guardians and we were unable to joined their parents to seek for consent. Finally, 323 children who the parents/ legal guardian consented were enrolled the study.

Data collection method and procedures

Caretakers of all children provided informed consent. They received consent forms to review and had the opportunity to ask questions. An assent form was provided for all study participant aged between seven and fifteen years. Depending on their reading ability, the forms were either read to them or read together. Both the children and their caretakers had the chance to seek clarification, and any unclear information was addressed by the investigator or research assistants. Subsequently, parental permission was obtained from the attender to allow the child’s participation in this research.

Privacy of participants was ensured during data collection. The interview was conducted in a separate room with limited access to their personal information to ensure participants’ privacy. In addition, no names were used on data collection tools, and data records were password-protected. Completed questionnaires were kept under lock and key and were accessible only by the principal investigator.

The investigators administered questionnaires in either French or the local languages (Swahili or Lingala) with the assistance of parents/caretakers for each child. Demographic information, including the child’s age, sex, residential address, parental occupation, access to drinking water, and exposure to various animals (such as dogs, cats, parrots, pigs, goats, ducks, and chickens) were collected.

The medical assessment included evaluating the presence of any of the following symptoms: abdominal pain, nausea, vomiting, diarrhea, bloating, burping, and weight loss. Additionally, the study considered the presence of family members or other individuals living with the child who had a history of peptic ulcer disease. Regarding clinical signs, the investigators assessed the following signs: pallor, jaundice, hepatomegaly, splenomegaly, and epigastric tenderness. Anthropometric measurements (weight and height) were also recorded during the interview (Figs. 1 and 2).

Fig. 1
figure 1

Study procedure

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Fig. 2
figure 2

Helicobacter pylori antigen detection test from stool amongst children included in the study

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H. pylori diagnostic test

H. pylori antigens detection in a sample of fresh stools was carried out for infection diagnosis. Stool samples were obtained either immediately after clinical assessment or later in the day for participant who were not able to provide fecal specimen immediately. The sample was analyzed immediately after collection using H pylori Ag Rapid Test Cassette (feces), manufactured in China, which have a relative sensitivity of 98.8% and a relative specificity of 100%. If not tested within 6 h, the specimen collected was stored for 3 days at a temperature between 2–8 °C. A stool sample of approximately 1 to 2 ml (1–2 g) was collected in a clean, dry specimen collection container to maximize antigen detection.

Process fecal specimens

The procedure was carried out in accordance with the test manufacturer's instructions. For solid specimens, the cap of collection tube was unscrewed, and then the stool collection applicator was stabbed randomly into the fecal specimen in 3 different sites to collect approximately 50 mg of feces. For liquid specimens, following aspiration of the specimens, 2 drops were transferred into the sample tube containing the dilution buffer. After securely tightening the cap onto the sample tube, the specimen was vigorously shaken to thoroughly mix the sample with the dilution buffer. The tube was left to stand for 2 min and 2 drops of the sample solution were squeezed in the sample well of the cassette; the test was read after 10 min. The test device was discarded after interpreting the result to avoid any confusion. A result was considered positive in the presence of two lines, even if the test line exhibited less intensity than the control line. A result was considered negative when only the control line appears solely.

Another part of the stool specimen was used to look for evidence of red blood cell using Immunochemical Fecal Occult Blood Test (iFOBT). In Nigeria, when assessing patients with peptic ulcer and gastric disturbances, 71.4% of patients who tested positive for either H. pylori infection or fecal occult blood test were positive for both tests [21]. While false negatives may occur with FOBT alone, the combination of FOBT and H. pylori stool antigen tests enhances detection rates for upper gastrointestinal lesions. This approach provides a more comprehensive diagnostic tool, improving clinical management of H. pylori-related conditions and their complications.

Two ml of whole blood were also sampled from a peripheral vein of each study participant and immediately put into Ethylenediaminetetraacetic acid (EDTA) containing tube. This sample was used to evaluated the level of anemia amongst study participants. Full blood count was used to assess the level of anemia by providing valuable information on the levels of red blood cells, haemoglobin, haematocrit, mean corpuscular volume, mean corpuscular Haemoglobin and red cell distribution width and Mentzer index. Laboratory quality was observed by having inbuilt positive controls, double checking with previously established positive controls. Furthermore, two technicians independently performed the analysis they reached a consensus regarding the conclusive outcomes for each sample following discussions about challenging-to-interpret test results from the specimens.

Treatment

All patients diagnosed as positive for H. pylori were treated with a 14-day regimen. Follow-up testing was performed 4 weeks after completing the treatment using a non-invasive stool antigen assay. Patients who tested positive for H. pylori by fecal antigen testing were offered standard triple therapy, which included omeprazole (2 mg/kg twice a day), clarithromycin (15 mg/kg twice a day), and amoxicillin (50 mg twice a day).

The standard triple therapy was selected based on clinical guidelines for pediatric H. pylori eradication. Omeprazole, a proton pump inhibitor, reduces gastric acid secretion, creating a more favourable environment for the antibiotics to work effectively. Clarithromycin, a macrolide antibiotic, inhibits bacterial protein synthesis, while amoxicillin, a beta-lactam antibiotic, disrupts bacterial cell wall synthesis. This combination targets the bacteria directly and enhances the likelihood of successful eradication.

Thirty days post-treatment, all participants completed a post-treatment survey, and an H. pylori stool antigen test was repeated.

Participants who remained positive after initial therapy received an additional 14 days of quadruple therapy, consisting of bismuth subsalicylate (262 mg for children under 10 years and 524 mg for children over 10 years) four times a day, metronidazole (30 mg/kg four times a day), amoxicillin (50 mg/kg twice a day), and omeprazole (2 mg/kg twice a day). The quadruple therapy was chosen as second-line treatment due to its ability to address potential antibiotic resistance and provide a broader spectrum of antibacterial activity. Bismuth subsalicylate provides additional antimicrobial effects and helps protect the stomach lining, metronidazole is effective against anaerobic bacteria, and the combination of amoxicillin and omeprazole continues to target and suppress the H. pylori bacteria.

Follow-up of study participant

All children receiving H. pylori treatment were monitored for side effects and adherence. The follow-up was conducted through phone calls made every 5 days throughout the treatment course. This approach allowed healthcare providers to maintain regular contact with patients and their caregivers, enabling timely identification of any adverse reactions or compliance issues. During these calls, healthcare professionals inquired about the child's well-being, any experienced side effects, (nausea, abdominal discomfort, diarrhea, taste disturbances.) and adherence to the prescribed medication regimen. This proactive monitoring strategy facilitated early intervention, when necessary, potentially improving treatment outcomes and patient safety. Additionally, the frequent phone contact provided an opportunity to address any concerns or questions from parents or guardians, thereby enhancing overall treatment support and potentially increasing adherence rates.

Data management and analysis

Before concluding the interviews, all questionnaires were thoroughly reviewed to ensure they were fully completed. After the data was collected, no new information was added to the surveys. IBM SPSS 27.0 statistics for Windows (Armonk, NY: IBM Corp.) was used to organize, summarize, and analyse the data retrieved from completed questionnaires. H. pylori infection prevalence was calculated as proportion of patient with positive stool test among all participant enrolled in the study (from January 2020 to December 2022). Binary logistic regression was used to assess the factors associated with H. pylori infection both at bivariable and multivariable level. The crude and adjusted odds ratios (OR) with accompanying 95% confidence intervals (CI) were reported. A p-value of 0.05 or lower was regarded as statistically significant.

Respect of individual persons

The study participants’ legal guardians had the unrestricted right to withdraw their children from the study at any time, without the obligation to justify their decision. Importantly, the withdrawal from the study was not affecting the right of their children to receive medical care.

Benefits and risks

All investigations were free of charge aimed to improve patients care. The findings were shared with parents or caregivers. Participants who were tested positive received appropriate treatment. There were no major risks except some pain during phlebotomy or mild discomfort when moving the patient for physical examination or anthropometric measurement. Strict aseptic techniques were observed, and no infection occurred.

Justice

All eligible patients were given the opportunity to participate in the study regardless of their religious, racial, social or financial background. There was no any form of discrimination or preferential treatment.

Results

Baseline characteristic of study participants

Sociodemographic characteristic of study participants

Sociodemographic characteristics of study participants are presented in Table 1. The majority of children were aged between 5 and 15 years, 55.10% were female and most of caregivers had a level of education beyond the primary school.

Table 1 Baseline sociodemographic characteristic of study participants
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Clinical and laboratory characteristics of study participants

Baseline clinical and laboratory characteristics of study participants are summarized in the Table 2. Abdominal pain was the major presenting complain of children. Almost half of study participant has red blood cell in the stool and 89.50% had a safe source of drinking water.

Table 2 Baseline clinical and laboratory characteristic of study participants
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Prevalence of H. pylori

Of the 323 participants enrolled in the study, 119 (36.80%) was screened positive for H. pylori infection.

Treatment

Tables 3 and 4 are related to the treatment of H. pylori infection among study participant.

Table 3 First line therapy regimen with amoxicillin + clarithromycin + Omeprazole
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Table 4 Second line therapy Regimen with bismuth subsalicylate + metronidazole + amoxicillin + omeprazole
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The Table 3 present a follow-up conducted 30 days post-treatment. Out of the 119 children who were administered the first-line regimen—comprising of Amoxicillin, Clarithromycin, and Omeprazole—approximately one-fifth of study participant were tested positive for the infection 30 days after completing the treatment.

Table 4, as shown below, illustrates the second-line therapy regimen. This regimen, which includes Bismuth Subsalicylate, Metronidazole, Amoxicillin, and Omeprazole, was administered to patients who did not respond to the first-line treatment. Thirty days after completion of the treatment, all were tested negatives.

Follow-up of study participant

The treatment was generally well-tolerated by the majority of patients. Common side effects reported included taste disturbances in 7/119 (5.90%) patients, nausea in 13/119 (10.90%), and mild diarrhea in 8/119 (6.70%). The adherence rate was high, with 110/119 (92.40%) patients following the treatment regimen as prescribed. Only a small proportion, 9/119 (7.60%), required additional support to complete the course.

Factors associated with H. pylori infection amongst study participants

Bivariate analysis of Factors associated with H. pylori infection

The Table 5 below show the bivariate analysis of factors associated with H. pylori infection amongst study participants. The following factors were associated with H. pylori infections at bivariate binary logistic regression analysis: the age between 37 and 59 months (cOR 3.01, 95% C.I: 1.30–6.92,p = 0.01), Parent occupations (cOR 2.35, 95% CI:1.38–3.99, p = 0.002), parent’s level of education (At most primary: cOR 2.45 95% CI: (1.14–5.24, p = 0.02) presence of pet at the compound (cOR 2.01, 95% CI: 1.48–2.74, p = 0.001), positive family history of PUD (cOR 1.76, 95% CI: 1.10–2.79, p = 0.02), drinking unsafe water (cOR 4.9, 95% CI: 2.95–8.15, p = 0.001), weight loss (cOR 0.59, 95% CI: 0.37–0.95, p = 0.03) anemia (cOR 3.75, 95% CI:1.46 −9.58, p = 0.006) and presence of RBC in the stool ( cOR 26.5, 95% CI: 13.68 −51.3, p = < 0.0001).

Table 5 Bivariate analysis of Factors associated with H pylori infection
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Multivariate analysis of factors associated with H. pylori infection

The Table 6 below show the multivariate analysis of factors associated with H. pylori infection amongst study participants. The following factors were significantly and independently associated with H. pylori infections: the age between 37 and 59 months (aOR 9.76, 95% C.I: 2.62–36.40, p = 0.001), parent’s occupations (aOR 2.58, 95% C.I:1.19–5.54, p = 0.016), presence of pet at the compound (aOR = 2.43, 95% CI: 1.17–5.06; p = 0.02); drinking unsafe water (aOR = 8.7, 95% CI: 2.49–30.41, p = 0.001) anemia (aOR 4.804, 95% C.I: 1.12–20.53 p = 0.034) and presence of red blood cells in the stool (aOR 30.84, 95% C.I:13,97–68,10, p = < 0.0001).The odds of H. pylori infection were 30.84 times higher among children with red blood cells in the stool compared to those who didn’t. The odds H. pylori infection was higher by 9.76 amongst children aged between 37 and 59 moths compare to others age group. Anemia increases the odd of H. pylori infection by 4.8. Others characteristics is showed in the Table 6 below.

Table 6 Multivariate analysis of Factors associated with H. pylori infection
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Discussion

Prevalence of H. pylori infection amongst children aged 0 to 15 years

This study conducted a longitudinal investigation of H. pylori infection in a cohort of children aged 0 to 15 years in Goma, North Kivu province, Eastern Democratic Republic of Congo (DRC). The findings revealed a prevalence of 36.80% among children attending the Samaritan Doctor's pediatric centre. This rate suggests that H. pylori infection is endemic among children in Goma City, a region affected by protracted conflict and population displacement. These results have significant implications for public health in the area and contribute to the understanding of the global distribution of this infection.

These results align with a recent systematic review suggesting that nearly half of the world’s population is infected with H. pylori, highlighting its global prevalence [22]. Our findings are consistence with some researches undertaken in surrounding countries. A comprehensive review and meta-analysis from 2011 to 2016 found that the global childhood prevalence of H. pylori infection was 33% [23]. In Kasese district, Uganda, the prevalence of H. pylori infection among children was 37.4% evaluated with the immunochromatographic rapid test (IRT) [24]. Similarly, a retrospective study conducted over five years in Kampala observed a prevalence of 35.7% in patients with gastrointestinal symptoms [25].

On the other hand, the prevalence observed in our study was lower than the 79.1% expected in African countries [22]. This prevalence is also lower compared to a study conducted on Ethiopian school children, which reported a H. pylori prevalence rate of 65.7% [26]. Higher prevalence rates were also reported in Ugandan children with sickle cell anemia (49%) [1] and in Cameroon (51.5%) [27]. Our study’s prevalence was higher compared to the prevalence reported in Mbarara, western Uganda (24.3%) [17] and in Havana, Cuba (5%) [28]. The prevalence of H. pylori infection varies from region to region worldwide, and among different population groups, study settings and type of diagnosis tests. Goma city, unlike Mbarara and Havana which reported low prevalence rates, is located in a war-torn area with massive population movement, overcrowding, and water supply problems. Thus, may partially explain the difference in the prevalence of H. pylori infection. The variation in prevalence rates across different studies highlights the importance of standardized diagnostic methods in epidemiological research. The use of serologic tests in some studies, which cannot distinguish between active and past infections, may lead to overestimation of prevalence rates. This emphasizes the need for more accurate, non-invasive diagnostic tools for large-scale screening, especially in resource-limited settings. The unique conditions in Goma, including prolonged conflict, overcrowding, and water supply issues, likely contribute to the observed prevalence. These findings underscore the need for a multifaceted approach to addressing H. pylori infection, encompassing improvements in sanitation, water quality, and living conditions, alongside medical interventions.

Factors associated to H. pylori infection among study participant

In this study, several factors were found to be significantly and independently associated with H. pylori infection among children aged 0 to 15 years. These factors included age between 37 and 59 months, caretaker’s occupation, presence of a pet in the compound, consumption of unsafe drinking water, anemia, and the presence of red blood cells (RBC) in the stool.

Children aged 37–59 months were 9.76 times more likely to be infected, aligning with previous studies reporting H. pylori acquisition between the second and third year of life [29]. The findings are consistent with research from other developing countries, which have reported high infection rates in children under 5 years. For instance, studies in Gambia [30], Uganda [17], Vietnam, Mexico, Egypt, and Bangladesh, all demonstrated early acquisition of H. pylori infection, with prevalence rates ranging from 22.6% to 80% in children under 5 years. [15, 31,32,33]. The period below 5 years of age represents a critical window for H. pylori infection in childhood due to multiple factors. During this developmental stage, children are establishing hygiene habits and may experience increased exposure to infection sources [34]. Their immune systems are still in the process of maturation, rendering them more susceptible to colonization [11]. This period frequently coincides with entry into preschool or daycare environments, facilitating close contact with other children[13]. Environmental conditions such as high-density living areas and inadequate sanitation, in conjunction with dietary habits and exposure to contaminated food and water sources, contribute to the elevated prevalence [11, 35]. These findings emphasize the necessity for targeted public health interventions to mitigate H. pylori transmission in early childhood.

In this study, children with parents having informal occupations were 2.58 times more likely to be infected with H. pylori compared to those with parents in formal occupations. This finding aligns with recent research indicating that socioeconomic factors, including parental occupation, can influence H. pylori infection rates in children[36]. Informal occupations often correlate with lower income and less stable living conditions, which may contribute to increased exposure to H. pylori through contaminated water and poor sanitation[34, 37]. Further studies are needed to explore the mechanisms underlying this association and to develop targeted interventions to reduce H. pylori infection in vulnerable populations.

Children consuming unsafe water were 8.7 times more likely to have H. pylori compared to those who did not. This finding underscores the critical role of water quality in the transmission of H. pylori. Goma city and its surrounding areas face a severe drinking water shortage, exacerbated by persistent insecurity, massive population displacement, and a lack of investment in water infrastructure[20]. Numerous studies indicate that various types of water, including drinking water, wastewater, surface water, and groundwater, can be potential reservoirs for H. pylori infection[38, 39]. Unsafe drinking water can harbour the bacterium, leading to infection through ingestion, and children are infected through consumption of contaminated water[39]. The bacterium can survive in contaminated water sources, and upon consumption, it colonizes the stomach lining, causing infection[11]. Recent studies, have also demonstrated a strong association between drinking unsafe water and H. pylori infection [35, 40]. In Istanbul, Turkey, low socio-economic status, dinking unsafe water, and consumption of uncooked vegetable was reported as important source of this infection [15]. In Havana, Cuba, drinking potable water was protective against H. pylori infection [28]. This reinforces the necessity for targeted interventions to ensure access to safe drinking water, thereby reducing the risk of H. pylori infection and improving public health outcomes.

In our study, children who had pets at home were 2.43 times more likely to be infected with H. pylori compared to those who did not. The association between H. pylori infection in children and the presence of pets in the household is a subject of ongoing research and debate within the medical community. Some studies suggest that pet ownership, particularly of dogs, and cat may be associated with an increased risk of H. pylori infection in children[41]. Pets may serve as potential reservoirs or vectors for the bacteria, facilitating transmission through close contact or contaminated environments[42]. However, other studies have found no significant correlation between pet ownership and H. pylori infection rates in children. Machine learning algorithms were employed to identify risk factors for H. pylori infection among school children in Ethiopia. While several risk factors were identified, pet ownership was not found to be a significant predictor of H. pylori infection[35]. Similarly, various risk factors for H. pylori infection in children were examined but did not establish a significant correlation between pet ownership and infection rates[11]. These conflicting findings underscore the complexity of H. pylori transmission and the necessity for further investigation.

Children with red blood cells (RBCs) in their stool were 30.84 times more likely to be infected by H. pylori compared to those without RBCs. Fecal occult bleeding is well-documented in H. pylori infection. An increased risk of occult gastrointestinal bleeding in H. pylori-positive children was reported in 2018 [43]. In Nigeria, 36.67% of patients with non-specific abdominal symptoms tested positive for both H. pylori and fecal occult blood [21]. In India, 20.7% of the patients with upper gastrointestinal bleeding were H. pylori positive [44]. and in Egypt, 65.4% of such children were infected. [45]. Gastric mucosal inflammation often chronic-active or nodular gastritis—is common in H. pylori-infected children [46]. Antral gastritis and duodenal ulcers are recognized causes of fecal occult bleeding in childhood[10]. These findings highlight the importance of early detection and treatment of H. pylori infection in children, especially when blood is detected in stool samples.

Children with anemia were 4.8 times more likely to be infected by H. pylori compared to those without anemia. H. pylori infection can lead to anemia by impairing the absorption of essential micronutrients and elevating the production of hepcidin in liver cells[47]. Additionally, H. pylori cause chronic gastritis, which impairs iron absorption and can lead to gastric ulcers, resulting in chronic blood loss. The infection can also interfere with the absorption of vitamin B12, leading to megaloblastic anemia. Furthermore, H. pylori induces systemic inflammation, disrupting red blood cell production and contributing to anemia[48]. This finding aligns with Asiimwe et al. (2023), who reported a significant association between H. pylori infection and anemia in dyspeptic patients in Uganda[40]. In a population-based survey conducted in Alaska, the prevalence of anemia and iron deficiency among children with H. pylori infection was 17% and 15%, respectively [49]. A recent systematic review revealed that children with H. pylori infection were at a higher risk of developing anemia compared to non-infected children [47]. Additionally, a retrospective case–control study in Saudi Arabia assessed the association between H. pylori infection and anemia across all age groups, finding that the prevalence of anemia, iron deficiency anemia (IDA), and microcytic anemia was higher among the infected group compared to uninfected children [50]. These findings underscore the importance of considering H. pylori infection in pediatric patients with anemia.

Treatment of H. pylori infection amongst children aged 0 to 15 years with H. pylori

In our study, 19.3% of patients treated with first-line drugs, including omeprazole, clarithromycin, and amoxicillin, remained positive for H. pylori 30 days after completing their initial treatment, indicating an eradication rate of 80.7%. In contrast, 100% of patients who did not respond to the first-line regimen were successfully treated with quadruple therapy consisting of bismuth subsalicylate, metronidazole, amoxicillin, and omeprazole.

This finding underscores the importance of considering alternative treatment strategies for patients who do not respond to initial therapy. Quadruple therapy has shown to be highly effective in such cases, providing a viable option for achieving complete eradication of H. pylori.

Our results align closely with a study carried out in Swedish children from 2005 to 2016, where 21% of cases showed resistance to clarithromycin[51]. This result is also consistent with a prospective, open, comparative, and cross-sectional study involving 228 Chinese children aged between 6 and 18 years, where the eradication rate was as low as 74.1% for standard triple therapy; however, in their study, the eradication rate with bismuth-based quadruple therapy was 89.9%[19]. In another study conducted in Portugal, the resistance rates were 6.7% for amoxicillin, 3.3% for metronidazole, and 23.3% for clarithromycin [52]. The eradication rates following a standard triple therapy of 7 to 14 days fall below 90% if clarithromycin resistance rates exceed 5%[18].

The current recommendation of international consensuses on H. pylori eradication therapy suggests that only regimens that reliably produce eradication rates of more than 90% should be used for empirical treatment[18]. In areas where the eradication rate of H. pylori infection exceeds 90%, most guidelines recommend a treatment course lasting 7 to 14 days, consisting of the standard triple therapy as the first-line approach[18]. A culture and sensitivity test are recommended if there is either unknown clarithromycin resistance or if the resistance level is more than 5% before initiating patients on clarithromycin-based triple therapy regimens [52]. In our study area, the prevalence of clarithromycin resistance and other drugs used as first-line therapy is unknown; this may explain the low rate of eradication compared to other studies conducted worldwide. Additionally, we did not perform culture and antibiotic susceptibility testing, so this result may be explained by poor adherence to therapy and other uncontrolled factors.

These findings highlight the necessity for further research into the prevalence of antibiotic resistance in our study area and the importance of adherence to therapy. Future research should focus on conducting culture and sensitivity tests to tailor treatment plans more effectively and explore additional strategies to improve adherence to H. pylori treatment regimens. By addressing these challenges, we can enhance the overall effectiveness of H. pylori eradication therapies and reduce the incidence of treatment failure.

Study limitations and strength

This study presents several limitations that may have influenced the observed prevalence. The focus on children in healthcare settings potentially introduces selection bias, as the sample may not be representative of the overall population of Goma City. Consequently, the prevalence observed in this study may not accurately reflect the true prevalence in the broader population.

The utilization of the stool antigen test, despite its high sensitivity and specificity, has inherent limitations. The inability to perform endoscopy and gastric biopsy, which are considered the gold standard for H. pylori infection diagnosis, represents a significant constraint. Furthermore, the absence of culture and susceptibility testing limits the capacity to detect antibiotic resistance.

The reliance on self-reported data from patients and caregivers regarding treatment adherence and side effects introduces potential reporting bias. The accuracy of such self-reported information can be influenced by factors such as recall bias and the willingness of participants to report accurately.

Despite these limitations, our study has significant strengths. To our knowledge, this is the first study conducted in eastern DRC, a war zone with a crowded population, to evaluate the rate of treatment failure after using clarithromycin-based therapy as the first line. Our study provides important baseline data on the prevalence of H. pylori and its resistance to antibiotics in this region, which can inform future research and treatment strategies.

Conclusion

This was, at our knowledge at the time, the first study in eastern DRC, specifically Goma city. The prevalence of H. pylori amongst children aged 0 to 15 years attending Samaritan Doctors pediatric centre was low than expected in African countries. Factors independently associated to H. pylori infection, identified through a multivariate binary logistic regression, included the age of the child, caretaker’s occupations, presence of pet at the compound, drinking unsafe water, anemia and presence of red blood cells in the stool. The eradication rate of H. pylori infection using standard clarithromycin based triple therapy was lower than the recommended of most current guidelines. Children presenting with, occult blood in the stool and microcytic anemia should be systematically screened for H. pylori infection using stool antigen test, which provides evidence of an active infection.

The use of clarithromycin-based therapy as first line of treatment to eradicate H. pylori infection should be guided by local data on antibiotic resistance. Patients and caretakers should be counselled about hygienic measures, including drinking potable safe water, and risk of close contact with pet at home, which is a real risk factor for H. pylori infection.

Data availability

Data is available upon request to the primary investigator.

Abbreviations

aOR:

Adjusted odd ratio

CI:

Confident interval

cOR:

Crude odd ratio

DALYs:

Disability Adjusted Life Years

DRC:

Democratic Republic of Congo

EDTA:

Ethylenediamine tetraacetic acid

GIT:

Gastrointestinal tract

IDA:

Iron deficiency anemia

iFOBT:

Immunochemical Fecal Occult Blood Test

IRT:

Immunochromatographic rapid test

RBC:

Red Blood Cells

UN:

United Nations

References

  1. Mubiru IS, Kasirye PG, Ndeezi G, et al. Prevalence and factors associated with Helicobacter Pylori infection among children with sickle cell anemia attending Mulago hospital, in Uganda. Afr Health Sci. 2022;22(2):135–145.https://doiorg.publicaciones.saludcastillayleon.es/10.4314/ahs.v22i2.16.

  2. Brown LM. Helicobacter pylori: Epidemiology and routes of transmission. Epidemiol Rev. 2000;22(2):283–97. https://doiorg.publicaciones.saludcastillayleon.es/10.1093/oxfordjournals.epirev.a018040.

    Article  CAS  PubMed  Google Scholar 

  3. Park JS, Jun JS, Seo JH, et al. Changing prevalence of Helicobacter pylori infection in children and adolescents. Clin. Exp. Pediatr. 2021;64(1):21–25. https://doiorg.publicaciones.saludcastillayleon.es/10.3345/cep.2019.01543.

  4. Lee YJ, et al. Community prevalence of Helicobacter pylori and dyspepsia and efficacy of triple therapy in a rural district of eastern Uganda. Heliyon. 2022;8(12). https://doiorg.publicaciones.saludcastillayleon.es/10.1016/j.heliyon.2022.e12612.

  5. Abele M, et al. Epidemiology and Characteristics of Gastric Carcinoma in Childhood—An Analysis of Data from Population-Based and Clinical Cancer Registries. Cancers (Basel). 2023;15(1). https://doiorg.publicaciones.saludcastillayleon.es/10.3390/cancers15010317.

  6. Miranda ACP, Machado RS, da Silva EMK. at al, “Seroprevalence of Helicobacter pylori infection among children of low socioeconomic level in São Paulo.” Sao Paulo Med J. 2010;128(4):187–91. https://doiorg.publicaciones.saludcastillayleon.es/10.1590/s1516-31802010000400002.

    Article  PubMed  PubMed Central  Google Scholar 

  7. Hunt RH, et al. World gastroenterology organisation global guideline: Helicobacter pylori in developing countries. J Clin Gastroenterol. 2011;45(5):383–8. https://doiorg.publicaciones.saludcastillayleon.es/10.1097/MCG.0b013e31820fb8f6.

    Article  Google Scholar 

  8. Alfaray RI, Saruuljavkhlan B, Ansari S, Fauzia KA, Yamaoka Y. Review: epidemiology of helicobacter pylori infection. Microbial Health Dis. 2022;4(3):e733. https://doiorg.publicaciones.saludcastillayleon.es/10.26355/mhd_20229_733.

  9. Suerbaum S, Michetti P. Helicobacter pylori infection. N Eng J Med. 2002;347(15):1175–86. https://doiorg.publicaciones.saludcastillayleon.es/10.1056/NEJMra020542.

  10. Pacifico L, et al. Consequences of Helicobacter pylori infection in children. 2010;16(41):5181–5194. https://doiorg.publicaciones.saludcastillayleon.es/10.3748/wjg.v16.i41.5181.

  11. Aguilera Matos I, Diaz Oliva SE, Escobedo AA, at al. Helicobacter pylori infection in children. BMJ Paediatr. Open. 2020;4(1):1–7. https://doiorg.publicaciones.saludcastillayleon.es/10.1136/bmjpo-2020-000679.

  12. Rowland M, Daly L, Vaughan M, et al. Age-specific incidence of Helicobacter pylori. Gastroenterology. 2006;130(1):65–72.https://doiorg.publicaciones.saludcastillayleon.es/10.1053/j.gastro.2005.11.004.

  13. Ozbey G, Hanafiah A. Epidemiology, Diagnosis, and Risk Factors of Helicobacter pylori Infection in Children. Euroasian J Hepato-Gastroenterology. 2017;7(1):34–9. https://doiorg.publicaciones.saludcastillayleon.es/10.5005/jp-journals-10018-1208.

    Article  Google Scholar 

  14. Dore MP, Malaty HM, Graham DY, et al. Risk factors associated with Helicobacter pylori infection among children in a defined geographic area. Clin Infect Dis. 2002;35(3):240–245. https://doiorg.publicaciones.saludcastillayleon.es/10.1086/341415.

  15. Salih B. Helicobacter pylori infection in developing countries: The burden for how long? Saudi J Gastroenterol. 2009;15(3):201–7. https://doiorg.publicaciones.saludcastillayleon.es/10.4103/1319-3767.54743.

    Article  PubMed  PubMed Central  Google Scholar 

  16. Kalach N, Bontems P, Raymond J. Helicobacter pylori infection in children. Helicobacter. 2017;22:1–7. https://doiorg.publicaciones.saludcastillayleon.es/10.1111/hel.12414.

    Article  Google Scholar 

  17. Aitila P, et al. Prevalence and Risk Factors of Helicobacter pylori Infection among Children Aged 1 to 15 Years at Holy Innocents Children’s Hospital, Mbarara, South Western Uganda. J Trop Med. 2019;2019:1–6. https://doiorg.publicaciones.saludcastillayleon.es/10.1155/2019/9303072.

    Article  Google Scholar 

  18. Shih C, Shie C, Hsu P. Update on the first-line treatment of Helicobacter pylori infection in areas with high and low clarithromycin resistances. 2022. pp. 1–13. https://doiorg.publicaciones.saludcastillayleon.es/10.1177/17562848221138168.

  19. Zhou Y, et al. Comparison of four different regimens against Helicobacter pylori as a first-line treatment: A prospective, cross-sectional, comparative, open trial in Chinese children. Helicobacter. 2020;25(2):1–9. https://doiorg.publicaciones.saludcastillayleon.es/10.1111/hel.12679.

    Article  Google Scholar 

  20. United Nations Security Council. Resolutions adopted by the Security Council in 2023. United Nations Digital Library. 2023;64724:1–3: https://main.un.org/securitycouncil/en/content/resolutions-adopted-security-council-2023.

  21. Umeh S, Enwuru CP. Faecal Occult Blood Test in Helicobacter pylori Positive Patients With Peptic and Gastric Disturbances. J Microbiol Health Sci. 2019:1–10.

  22. Hooi JKY, et al. Systematic Review and Meta-Analysis. Gastroenterology. 2017;153(2):420–9. https://doiorg.publicaciones.saludcastillayleon.es/10.1053/j.gastro.2017.04.022.

    Article  PubMed  Google Scholar 

  23. Torrres BZ, Lucero Y, Lagomarcino AJ, et al. Prevalence and dynamics of Helicobacter pylori infection during childhood. 2017;1130561:1–18. https://doiorg.publicaciones.saludcastillayleon.es/10.1111/hel.12399.

  24. Tsongo L, Nakavuma J, Mugasa C, et al. Helicobacter pylori among patients with symptoms of gastroduodenal ulcer disease in rural Uganda. Infect Ecol Epidemiol. 2015;5(1):26785. https://doiorg.publicaciones.saludcastillayleon.es/10.3402/iee.v5.26785.

  25. Namyalo E, et al. Prevalence of Helicobacter pylori among Patients with Gastrointestinal Tract (GIT) Symptoms: A Retrospective Study at Selected Africa Air Rescue (AAR) Clinics in Kampala, Uganda, from 2015 to 2019. J Trop Med. 2021;2021. https://doiorg.publicaciones.saludcastillayleon.es/10.1155/2021/9935142.

  26. Schacher K, et al. Individual and household correlates of Helicobacter pylori infection among Young Ethiopian children in Ziway, Central Ethiopia. BMC Infect Dis. 2020;20(1):1–10. https://doiorg.publicaciones.saludcastillayleon.es/10.1186/s12879-020-05043-1.

    Article  Google Scholar 

  27. Aminde JA, Dedino GA, Ngwasiri CA, et al. Helicobacter pylori infection among patients presenting with dyspepsia at a primary care setting in Cameroon : seroprevalence, five-year trend and predictors. 2019. pp. 1–9.

  28. Venero-Fernández SJ, et al. Prevalence of and factors associated with Helicobacter pylori infection in preschoolers in Havana, Cuba: A population-based study. Rev Gastroenterol Mex. 2020;85(2):151–9. https://doiorg.publicaciones.saludcastillayleon.es/10.1016/j.rgmx.2019.03.010.

    Article  Google Scholar 

  29. Kienesberger S, et al. When is Helicobacter pylori acquired in populations in developing countries? A birth-cohort study in Bangladeshi children. Gut Microbes. 2018;9(3):252–63. https://doiorg.publicaciones.saludcastillayleon.es/10.1080/19490976.2017.1421887.

    Article  PubMed  PubMed Central  Google Scholar 

  30. Weyermann M, Rothenbacher D, Brenner H. Acquisition of helicobacter pylori infection in early childhood: Independent contributions of infected mothers, fathers, and siblings. Am J Gastroenterol. 2009;104(1):182–9. https://doiorg.publicaciones.saludcastillayleon.es/10.1038/ajg.2008.61.

    Article  PubMed  Google Scholar 

  31. Nguyen BV, et al. Prevalence of and factors associated with Helicobacter pylori infection in children in the North of Vietnam. Am J Trop Med Hyg. 2006;74(4):536–9. https://doiorg.publicaciones.saludcastillayleon.es/10.4269/ajtmh.2006.74.536.

    Article  PubMed  Google Scholar 

  32. Frenck RW. et al. Sensitivity and specificity of various tests for the diagnosis of Helicobacter pylori in Egyptian children. Pediatrics. 2006;118(4). https://doiorg.publicaciones.saludcastillayleon.es/10.1542/peds.2005-2925.

  33. Ahmad MM, et al. Long-term re-infection rate after Helicobacter pylori eradication in Bangladeshi adults. Digestion. 2007;75(4):173–6. https://doiorg.publicaciones.saludcastillayleon.es/10.1159/000107046.

    Article  PubMed  Google Scholar 

  34. Bashir SK, Khan MB. Overview of Helicobacter pylori Infection, Prevalence, Risk Factors, and Its Prevention. Adv Gut Microbiome Res. 2023;2023:1–9. https://doiorg.publicaciones.saludcastillayleon.es/10.1155/2023/9747027.

    Article  Google Scholar 

  35. Tran V, et al. Helicobacter pylori (H. pylori) risk factor analysis and prevalence prediction: a machine learning-based approach. BMC Infect Dis. 2022;22(1):1–14. https://doiorg.publicaciones.saludcastillayleon.es/10.1186/s12879-022-07625-7.

    Article  Google Scholar 

  36. Borka Balas R, Meliț LE, Mărginean CO. Worldwide Prevalence and Risk Factors of Helicobacter pylori Infection in Children. Children. 2022;9(9). https://doiorg.publicaciones.saludcastillayleon.es/10.3390/children9091359.

  37. Malaty HM, Graham DY. Importance of childhood socioeconomic status on the current prevalence of Helicobacter pylori infection. Gut. 1994;35(6):742–5. https://doiorg.publicaciones.saludcastillayleon.es/10.1136/gut.35.6.742.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Ma C, et al. Quantification and cultivation of Helicobacter pylori (H. pylori) from various urban water environments: A comprehensive analysis of precondition methods and sample characteristics. Environ Int. 2024;187(May):108683. https://doiorg.publicaciones.saludcastillayleon.es/10.1016/j.envint.2024.108683.

  39. Leyton J, Fernández J, Acosta P, et al. Reduction of Helicobacter pylori cells in rural water supply using slow sand filtration. Environ Monit Assess. 2024;196(7):1–12. https://doiorg.publicaciones.saludcastillayleon.es/10.1007/s10661-024-12764-2.

  40. Asiimwe D, et al. Association Between Helicobacter pylori Infection and Anemia Among Adult Dyspeptic Patients Attending Kiryandongo General Hospital, Uganda. J Blood Med. 2023;14:57–66. https://doiorg.publicaciones.saludcastillayleon.es/10.2147/JBM.S392146.

    Article  PubMed  PubMed Central  Google Scholar 

  41. Taillieu E, De Bruyckere S, Van Steenkiste C, et al. Presence of potentially novel Helicobacter pylori-like organisms in gastric samples from cats and dogs. Vet Res. 2023:54(1):93. https://doiorg.publicaciones.saludcastillayleon.es/10.1186/s13567-023-01223-4.

  42. Shaaban SI, et al. An investigative study on the zoonotic potential of Helicobacter pylori. BMC Vet Res. 2023;19(1):1–7. https://doiorg.publicaciones.saludcastillayleon.es/10.1186/s12917-023-03572-w.

    Article  CAS  Google Scholar 

  43. Smith SI, et al. Helicobacter pylori Infection in Africa: Update of the Current Situation and Challenges. Dig Dis. 2022;40(4):535–44. https://doiorg.publicaciones.saludcastillayleon.es/10.1159/000518959.

    Article  PubMed  Google Scholar 

  44. Usta M, Urganci N. Upper gastrointestinal bleeding in children: The role of Helicobacter pylori infection and non-steroidal anti-inflammatory drug use. West Indian Med J. 2015;64(2):113–6. https://doiorg.publicaciones.saludcastillayleon.es/10.7727/wimj.2014.130.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. El-Mazary. Helicobacter Pylori Infection in a Group of Egyptian Children With Upper Gastro-Intestinal Bleeding. Gastroenterol Res. 2013;6(3):95–102. https://doiorg.publicaciones.saludcastillayleon.es/10.4021/gr533e.

  46. Broide E, et al. Lymphoid follicles in children with Helicobacter pylori-negative gastritis. Clin Exp Gastroenterol. 2017;10:195–201. https://doiorg.publicaciones.saludcastillayleon.es/10.2147/CEG.S133421.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Walle M, Tesfaye A, Agidew MM, et al. The association of Helicobacter pylori infection with the risk of anemia in children: systematic review and meta-analysis. BMC Infect Dis. 2025;25(1). https://doiorg.publicaciones.saludcastillayleon.es/10.1186/s12879-024-10427-8.

  48. Motupalli SK, Oroszi TL. The nexus between Helicobacter pylori infection and anemia—a systematic review. Front Hematol. 2024;3(August):1–9. https://doiorg.publicaciones.saludcastillayleon.es/10.3389/frhem.2024.1423494.

    Article  Google Scholar 

  49. Digirolamo AM, Perry GS, Gold BD, at al. Helicobacter pylori. 2007;26(10):927–934, https://doiorg.publicaciones.saludcastillayleon.es/10.1097/INF.0b013e31812e52cd.

  50. Al Mutawa OA, et al. Helicobacter pylori (H. pylori) Infection-Associated Dyslipidemia in the Asir Region, Saudi Arabia. Life. 2023;13(11):2206. https://doiorg.publicaciones.saludcastillayleon.es/10.3390/life13112206.

  51. Jansson L, Agardh D. Prevalence of clarithromycin-resistant Helicobacter pylori in children living in South of Sweden: a 12-year follow-up. Scand J Gastroenterol. 2019;54(7):838–42. https://doiorg.publicaciones.saludcastillayleon.es/10.1080/00365521.2019.1637452.

    Article  CAS  PubMed  Google Scholar 

  52. Silva GM, Moreira H, Joao S, et al. “Helicobacter pylori antimicrobial resistance in a pediatric population,” no. April, pp. 1–6, 2018, https://doiorg.publicaciones.saludcastillayleon.es/10.1111/hel.12528.

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Acknowledgements

We thank all participants for their contributions to this study, and the nursing team of Samaritan doctor’s pediatrics center for the assistance rendered during data collection.

Clinical trial number

Not applicable.

Funding

This research received no external funding.

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Authors and Affiliations

  1. Department of Paediatrics and Child Health, Faculty of Clinical Medicine and Dentistry, Kampala International University, Ishaka-Bushenyi, Uganda

    Patrick Kumbowi Kumbakulu, Gabriel Kakuru Shamavu & Banga Mseza

  2. Department of Paediatrics and Child Health, Université Libre Des Pays Des Grands Lacs, Goma, Democratic Republic of Congo

    Emmanuel Busha Tibasima

  3. Department Of Pediatric and Child Health Samaritan Doctor’S Pediatric Centre, Goma, Democratic Republic of Congo

    Emmanuel Busha Tibasima, Lundula Penge Chirac, Omari Ramazani, Tsumbu Byaruhanga Patrick & Kazembe Kamalo Olga

  4. Departement of Epidemiology, Université Officielle de Ruwenzori, Butembo, Democratic Republic of Congo

    Mitangala Ndeba Prudence

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Contributions

BM, EBT conceptualized and designed the study. TBP, KKO and OR participated to the data collection and interpretation. PKK and BM analyzed the data; BM wrote the original manuscript. EBT, GKS, MNP and PKK reviewed and improved the manuscript. All authors approved the final version of the manuscript for publication.

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Correspondence to Banga Mseza.

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Ethics approval and consent to participate

The ethical review and approval were obtained from “comité d’éthique de la santé CNES” (N° Réf 012/BUR-CNES/NK/2020). Permission to conducted the study was sought in advance from the administration of Samaritan Doctor’s pediatric center.

Written informed consent was obtained from caregivers of children. Study participants were free to withdraw from the study at any point, without any consequences.

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Tibasima, E.B., Kumbakulu, P.K., Chirac, L.P. et al. Prevalence, associated factors, and clinical outcomes of Helicobacter pylori infection in pediatric populations in a war-torn urban environment in Eastern Democratic Republic of Congo: a mixed methods study. BMC Pediatr 25, 257 (2025). https://doiorg.publicaciones.saludcastillayleon.es/10.1186/s12887-025-05588-7

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