The prevalence and associated factors of Helicobacter pylori infection among asymptomatic adolescent schoolchildren in Sudan: a cross-sectional study

Background Only few data have been published on Helicobacter pylori infection in adolescents in Sub-Saharan Africa, including Sudan. The aim of the present study was to investigate the prevalence and associated factors of H. pylori infection in asymptomatic adolescents schoolchildren (aged 10–19 years) in Sudan. Methods A cross-sectional study was conducted from October to November 2022. The participants’ sociodemographic and clinical characteristics were assessed using a questionnaire. The participants underwent a rapid H. pylori antibody test for the detection of H. pylori antibodies. Multivariate regression analyses were performed. Results Of the 368 enrolled adolescents, 155 (42.1%) and 213 (57.9%) were boys and girls, respectively. The median (interquartile range [IQR]) age of the total sample was 15.2 years (14.0‒16.4 years). The overall prevalence of H. pylori infection was 8.4%. In the multivariable regression analyses, only the female adolescents (adjusted odds ratio [AOR], 3.04; 95% confidence interval [CI], 1.24‒7.44) were associated with H. pylori infection. Age, parental education and occupation, and body mass index were not associated with contracting H. pylori infection. Conclusion H. pylori infection was detected in one of 10 adolescents in Northern Sudan. Female adolescents were at a higher risk of contracting H. pylori infection. The introduction of interventional health programs such as awareness campaigns and improving personal hygiene could lead to the reduction of the risk of H. pylori infection at early ages, especially in girls, and ensure that adolescents are healthy in their present and later lives.


Introduction
The widespread global prevalence of Helicobacter pylori infection has conferred a heavy burden on health systems, especially in fragile health systems such as those in Africa [1,2].According to a recent estimation, Africa had the highest pooled prevalence of H. pylori infection (70.1%) compared with other regions [2].H. pylori infection is still highly prevalent in children and adolescents globally [3].Despite the descending trend in the prevalence of H. pylori infection in children worldwide, its overall prevalence in Africa remains very high (70%) [4].Knowledge of the trend of the prevalence of H. pylori infection in children and adolescents is crucial in predicting its related diseases, including gastric cancer, in later life [4,5].H. pylori infection in children and adolescents has been associated with various extragastric pathologies such as iron deficiency anemia [6][7][8], growth retardation, and diabetes [8].In addition, H. pylori is listed as a group 1 carcinogen in the most recent medical literature and is one of the most significant infectious drivers of cancer worldwide, accounting for 8 of 10 stomach cancer cases in adults [9].H. pylori is a gram-negative bacterium with a helical shape [10].
The World Health Organization (WHO) defines adolescence as the phase of life between childhood and adulthood, from the ages of 10 to 19 years [11].It is a unique stage of human development and an important time for laying the foundations of good health [11].
Increased awareness, appropriate screening, early identification, and individualized treatment approaches for H. pylori infection at early ages (children and adolescents) provide opportunities to avoid its complications [5].These preventive approaches are needed in Africa, especially Sudan, where resources are limited.According to the WHO's estimate, more than 20% of the population in Sudan are adolescents [20].
To attain good health, adolescents' health must be addressed at all levels and by all involved parties.The health burden of H. pylori infection in adolescents requires urgent public health action.Therefore, the practical steps to address H. pylori infection and its associated factors in adolescents on a global scale require a thorough understanding of the local context.To achieve this, first, the prevalence of H. pylori infection in adolescents in the community and its associated factors must be investigated.On the basis of community-based data, appropriate health-care measures can then be applied accordingly to maintain good health.There is a paucity of studies on the prevalence of H. pylori infection and its associated factors in adolescents in Sudan in general [12], and no such studies have been conducted in the proposed area (Northern Sudan).Thus, the aim of the present study was to investigate the prevalence and associated factors of H. Pylori infection in asymptomatic adolescents in Northern Sudan.

Study area
This cross-sectional study was conducted in 368 asymptomatic adolescents (aged 10-19 years) who were attending public schools in the locality of Almatamah in Northern Sudan during the study period from October to November 2022.Almatamah, located in the River Nile State, Northern Sudan, is approximately 130 km from Khartoum, the capital of Sudan.Public schools for both boys and girls are available in this locality.A list of students between the ages of 10 and 19 years was obtained from the local authority, from which participants for the study were randomly selected.

Inclusion and exclusion criteria
All adolescents between the ages of 10 and 19 years were included in the study, and those younger or older than these ages were excluded.Those who did not give their consent to participate in the study were also excluded.All the participants recruited were apparently healthy, and those who were sick, pregnant, and nursing were excluded from the study.

Data collection
After the participants and their guardians signed an informed consent form, the selected students were approached.Data on the participants' sociodemographic characteristics, including age in years, sex, parental educational level (< secondary or ≥ secondary), mother's occupational status (housewife or employed), and father's education (laborer or skilled worker), were collected using a questionnaire.Anthropometric measurements (i.e., weight and height) were performed using standard procedures.

Weight and height measurements
The participants' weights were measured in kilograms using standard procedures (well-calibrated scales adjusted to zero before each measurement).Weight was measured to the nearest 100 g.During the measurement, the participants stood with minimal movement, with their hands at their sides.Moreover, shoes and excess clothing were removed.Height was measured to the nearest 0.1 cm, with the participant standing straight, with their back against the wall and feet together.BMI was determined in accordance with the participant's age, sex, weight, and height.

Processing of blood samples
Each participant provided 3-5 ml of blood sample for H. pylori serological testing.The blood samples were centrifuged at 1,500 rpm for 15 min, and an H. pylori antibody rapid test was performed in accordance with the manufacturer's instructions (Hangzhou Alltest Biotech Co., Ltd.; Hangzhou, China).A H. pylori antibody rapid test is a rapid visual immunoassay for the qualitative detection of IgM and IgG antibodies specific to H. pylori.It is widely used and has high sensitivity and specificity [17].In this work, we defined our results as positive and negative for H. pylori infection.

Sample size calculation
A total of 368 adolescents were enrolled in the study.We assumed that 40.0% of the adolescents had H. pylori infection.This assumption was based on a previous study in our neighboring country of Ethiopia [17].The sample size of 368 adolescents was calculated to detect a difference of 5% at α = with a power of 80%.We assumed that 10% of the participants would not respond or would have incomplete data.

Statistical analysis
The data collected were entered into a computer using the IBM Statistical Package for the Social Sciences (SPSS) for Windows (version 22.0; SPSS Inc., New York, NY).The proportions were expressed as frequencies (%).The continuous data (age and BMI) were evaluated for normality using the Shapiro-Wilk test and were found to be non-normally distributed and expressed as median (interquartile range [IQR]).A univariate analysis was performed with H. pylori infection as the dependent variable and age, sex, parental educational level and occupation, and BMI as independent variables.Thereafter, all the variables were entered into a multivariable logistic regression model with backward elimination to adjust for covariates.The adjusted odds ratios (AORs) and 95% confidence intervals (CIs) were calculated as necessary.A two-sided P value of < 0.05 was considered statistically significant.
In the univariate analysis, age, parental education and occupation, and BMI were not associated with H. pylori infection (Table 1).In the multivariable regression analysis, only the female adolescents (AOR, 3.04; 95% CI, 1.24-7.44)were associated with H. pylori infection (Table 2).

Discussion
The main finding of the present study was that 8.4% of the enrolled adolescents had H. pylori infection.In this study, the prevalence (8.4%) of H. pylori infection was comparable with the results from Tanzania in children aged 6 months to 17 years, of whom 11.5% had H. pylori infection [16].Moreover, in Ghana, a cross-sectional study that included 240 asymptomatic children aged 7 to 16 years reported a prevalence rate of 14.2% for H. pylori infection [13].The prevalence rate (8.4%) of H. pylori infection in the present study is lower than that reported among 431 schoolchildren (aged 8-18 years) in Eastern Sudan, which showed that 21.8% of them had H. pylori infection [12].
Compared with those in other countries, the prevalence rate of H. pylori infection in our study was lower than that previously reported in Ethiopia (65.7%) [17] and Nigeria (32.8%) [14].Data from a systematic review meta-analysis that included 198 studies with a total of 152,650 children aged ≤ 18 years showed that the overall global prevalence rate of H. pylori infection in children was 32.3%, which was higher in low-and middle-income countries than in high-income countries (43.2% vs. 21.7%)[3].
The low prevalence of H. pylori infection in our study could be explained by the fact that only asymptomatic adolescents were screened in our study.For example, a recent study by Balas et al. showed a low prevalence rate (14.2%) of H. pylori infection in children without gastrointestinal symptoms [4].Moreover, the difference in the sanitation and hygiene practice in the different population could explain the difference in the prevalence of H. pylori infection which was reported in the different studies.
In the present study, the risk of contracting H. pylori infection was three times higher among the female than among the male adolescents.This is in agreement with previous studies [13,21].For example, in Ghana, a study by Awuku et al. that included 240 asymptomatic children revealed that a higher proportion of females than males had H. pylori infection (16.8% vs. 10.7%)[13].Furthermore, Mehata et al. analyzed data from the 2016 Nepal National Micronutrient Status Survey, which included 1,023 adolescents aged 10-19 years, and revealed that 16% of adolescent girls and 14% of adolescent boys had H. pylori infection [21].In Iran, a longitudinal cohort study that included 54 patients diagnosed with gastric cancer reported a significant association between female sex and higher gastric cancer stage [22].It is not clear why females were at higher risk to have H. pylori infection in this study.Perhaps, there was a difference in the hygiene and sanitation practice between males and females in the region of Sudan.
Contrary to our study, a study in Eastern Sudan showed that boys were more likely to have H. pylori infection than girls [12].However, other studies have shown no significant differences in the prevalence of H. pylori infection between boys and girls [18,23].
Similar to our study, other studies have shown that parental educational status is not associated with H. pylori infection in adolescents [13].Wangda et al., reported that the prevalence of H. pylori infection inversely correlated with the mother's educational level [18].The lack of parental education in our study could be explained by the low quality of education and the low impact of education on the workforce in Sudan.
Our study showed no association between H. pylori infection and father's occupation in the enrolled adolescents, similarly to previous studies.By contrast, a study in Tanzania reported that father's occupation was an independent predictor of the presence of H. pylori antibodies [16].
The present study did not show an association between H. pylori infection and BMI.In a recent meta-analysis, H. pylori infection had an adverse impact on growth outcomes in children, mainly children's height-for-age Z (HAZ) scores [19].In Eastern Sudan, where a high prevalence of H. pylori infection was found (21.8%), most children (84%) had BMI scores below the normal range [12].
Our study also showed no association between adolescent age and H. pylori infection, consistent with previous studies [12,18].For example, Abbas et al. revealed that H. pylori infection was prevalent among schoolchildren of all age groups in Eastern Sudan [12].However, in Ethiopia [17], Nigeria [15], and Tanzania [16], older adolescent age was associated with H. pylori infection.
Our results should be cautiously compared with the findings of other studies for the following reasons: First, the inclusion and exclusion criteria used differed between our study and other studies.For example, asymptomatic adolescents were screened in our study, whereas adolescents with gastrointestinal symptoms were included in other studies.Second, whereas our study used the WHO cutoff age (10-19 years), other studies used different ages (early adolescence, late adolescence, or both adolescence and childhood).Third, different tests were used to detect H. pylori infection.Such differences in the prevalence and risk factors of H. pylori infection between and within countries necessitate further research.

Limitations
This study has limitations inherent to its cross-sectional design and the direction of the association can't be ascertained.A longitudinal study will provide more clarification regarding the association between the prevalence of H. pylori infection and its associated factors in later life.In Africa, H. pylori infection occurred in early life and carried-out in the later age.This study was conducted in Northern Sudan, thus limiting the of the findings to adolescents in Sudan.One of the major limitations of the study is the lack of comprehensive risk factors (variables) to look their impact on the prevalence of H. pylori.We have only few socio demographic factors that are not even consider important predicators for H. pylori infection.The impact of WASH (Water, Sanitation, and Hygiene) interventions as potential risk factors for H. pylori are well-known.Moreover, this study uses rapid antibody test which can't differentiate past and current infection.

Conclusion
H. pylori infection was detected in one of 10 adolescents in Northern Sudan.The female adolescents were at a higher risk of contracting H. pylori infection than the male adolescents.The introduction of interventional health programs such as awareness campaigns and improving personal hygiene could lead to the reduction of the risk of H. pylori infection at early ages, especially in females, and ensure that adolescents are healthy in their present and later lives.

Table 1
Univariate analysis of the factors associated with H. pylori infection in adolescents in northern Sudan (n = 368), 2022

Table 2
Multivariate logistic regression analysis of the factors associated with H. pylori infection in adolescents in NorthernSudan (n = 368), 2022