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Year : 2021  |  Volume : 34  |  Issue : 1  |  Page : 354-359

Epidemiology of Helicobacter pylori infection among children (6–12 years) in Menoufia Governorate

Public Health and Community Medicine Department, Faculty of Medicine, Menoufia University, Menoufia, Egypt

Date of Submission28-Apr-2019
Date of Decision19-May-2019
Date of Acceptance20-May-2019
Date of Web Publication27-Mar-2021

Correspondence Address:
Sally A Mehesin
El-Bagour, Menoufia
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Source of Support: None, Conflict of Interest: None

DOI: 10.4103/mmj.mmj_171_19

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To study the prevalence of Helicobacter pylori infection and to assess potential risk factors and possible complications among children aged 6–12 years.
H. pylori infection is said to be associated with growth delay in children, resistant iron-deficiency anemia, chronic antral gastritis that is related to duodenal ulcer, gastric ulcer, and probably gastric adenocarcinoma.
Participants and methods
A cross-sectional study included randomly selected 384 apparently healthy children from whom blood samples were collected after obtaining their parents' written consent. The study included 179 males and 205 females, and their age ranged from 6 to 12 years. Sociodemographic data and history of risk factors were obtained through a questionnaire. For every child, H. pylori antibody in serum was tested using H. pylori Antibody Rapid Test Cassette to detect the overexposure of H. pylori.
Results of this study showed that prevalence of the overexposure to H. pylori was 45.1%. A significant association was found between each of previous usage of municipal tap water drinking, lack of personal hygiene, and contact with domestic animals and H. pylori infection, whereas there was no significant association between age, sex, or socioeconomic level and H. pylori infection.
In Menoufia Governorate, the seroprevalence of H. pylori was 45.1%. Tap water, lack of personal hygiene, and contact with domestic animal were major risk factors.

Keywords: epidemiology, Helicobacter pylori, prevalence, serum antibodies

How to cite this article:
Mehesin SA, Badr SA, El Shazli HA, Ghoneim YA, Soliman SS, Al Bahnasy RE. Epidemiology of Helicobacter pylori infection among children (6–12 years) in Menoufia Governorate. Menoufia Med J 2021;34:354-9

How to cite this URL:
Mehesin SA, Badr SA, El Shazli HA, Ghoneim YA, Soliman SS, Al Bahnasy RE. Epidemiology of Helicobacter pylori infection among children (6–12 years) in Menoufia Governorate. Menoufia Med J [serial online] 2021 [cited 2023 Dec 4];34:354-9. Available from: http://www.mmj.eg.net/text.asp?2021/34/1/354/312004

  Introduction Top

Helicobacter pylori infection is predominant in developing world, where socioeconomic status is associated with increased prevalence of the infection [1]. Though the type and way of acquiring H. pylori infection is still controversial, it is thought to be transmitted from person to person by mouth, fecal, or oral route [2]. It also seems that the pathogenesis of H. pylori infection is related to the virulence factors of the bacteria as well as environmental (dietary habits, hygiene, and stress) and host factors (age, sex, and blood type) [3]. The infectious rate with H. pylori varies greatly between and within populations. This suggests that cultural and socioeconomic-related environmental factors may have a role in acquiring it [3],[4],[5].

The aim of this work was to study the prevalence of H. pylori infection and to assess potential risk factors and possible complications among children aged 6–12 years.

  Patients and methods Top

A cross-sectional study was carried out in Menoufia Governorate from 1 May 2017 to 30 April 2019. The study was approved by local ethical committee in Menoufia faculty of medicine. All procedures performed in this this study were in accordance with the 1964 Helsinki Declaration and its later amendments.

The total studied participants were 384 children selected randomly from primary schools of two districts by multistage random sample technique. After receiving a written consent from parents, blood samples were collected. The history of the patients was taken in a predesigned data questionnaire, which included demographic data like age, sex, and residence. Household crowding was determined according to American crowding index, which is calculated by dividing the number of family members on the number of rooms, and it is defined to be crowded if more than 1. Risk factors like child housing condition, personal hygiene, contact with domestic animals, and feeding pattern were also included in the questionnaire.

Sample size calculation was done as follows: according to the obtained number (440 000) of the total population of children aged from 6 to 12 years in Menoufia Governorate, which was taken from civil registry, and based on past review of literature of Deeb et al. [4], the calculated sample size was 384 children at 95% confidence level which gave 80% as power of the study. The serum was analyzed for IgG antibody using Acon H. pylori antibody rapid test cassette (Acon Laboratories Inc., San Diego, California, USA). Hemoglobin level and anthropometric measurement (weight and height) were also assessed as indicators for H. pylori infection complications. Weight and height were classified according to WHO z score tables. Hemoglobin% was measured through hemoglobin assay using Drabkin reagent.

Statistical analysis

Results were collected, tabulated, and statistically analyzed by an IBM compatible personal computer with SPSS, version 20 (released 2011; SPSS Inc., Chicago, Illinois, USA; IBM SPSS statistics for Windows, version 20.0; IBM Corp., Armonk, New York, USA). Normality of the data was tested by Kolmogorov–Smirnov and Shapiro–Wilk tests. Then quantitative data were analyzed using Student t-test or Mann–Whitney test, and qualitative data were analyzed using the χ2 or Fisher exact test. Two-sided P value of less than 0.05 was considered statistically significant.

  Results Top

The mean age of the 384 children was 9.6 ± 1.7 years. There were 179 (46.6%) male and 205 (53.4%) female. A total of 138 (35.9%) children were from urban areas and 246 (64.1%) from rural areas. The seroprevalence of H. pylori infection was 45.1% (95% confidence interval: 39.8–50.0) [Figure 1]. There were no statistically significant differences between positive and negative children regarding age, sex, residence, or socioeconomic level (P = 0.727, 0.454, 0.213, and 0.320, respectively), whereas seropositive children had significantly higher usage of municipal tap water as a main source of drinking water, household crowding, and contact with domestic animals (P value = <0.001, 0.038, and <0.001, respectively; [Table 1]). There was no statistically significant difference between both groups regarding history or duration of breastfeeding, whereas seropositive children had significantly higher positive family history of H. pylori infection (P = 0.913, 0.962, and 0.004, respectively; [Table 2]). Seronegative children had significantly higher consumption of fruits and vegetables and following personal hygiene standards, whereas there was no significant difference between both groups regarding intake of salted snacks or soft drink (P = 0.010, 0.031, 0.003, 0.506, and 0.156, respectively; [Table 3]). Seropositive children had significantly higher gastrointestinal tract complaint (P = 0.002), whereas they had significantly lower weight, height, and blood hemoglobin level (P = 0.022, 0.017, and 0.030, respectively; [Table 4] and [Table 5]). A logistic regression was done to ascertain the effect of age, sex, residence, source of drinking water, contact with pets, and general hygiene on the likelihood that the participants have positive serum H. pylori antibodies. Tap water, contact with domestic animals, and general hygiene were found to be significant predictors (P = 0.025, 0.027, and 0.045, respectively). Tap water and contact with domestic animals were found to be significant risk factors for infection with H. pylori, whereas general hygiene was found to be a significant protective factor.
Figure 1: Seroprevalence of Helicobacter pylori among the children.

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Table 1: Relationship between socioeconomic characteristic of the participants and serum antibodies of Helicobacter pylori (n=384)

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Table 2: Relationship between the child past and family history and presence of serum antibodies of Helicobacter pylori (n=384)

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Table 3: Relationship between the feeding pattern and personal hygiene of the children and presence of serum antibodies of Helicobacter pylori (n=384)

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Table 4: Relationship between potential complications of Helicobacter pylori and presence of Helicobacter pylori serum antibodies (n=384)

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Table 5: Logistic regression for potential risk factors of Helicobacter pylori infection

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  Discussion Top

H. pylori has been detected worldwide in individuals of all ages. Infection rates are falling in the developed and developing countries; however, H. pylori is still widespread in the world. Approximately half of the world's population are affected [5]. The prevalence of H. pylori varies greatly whether between or within countries. Estimated prevalence is ∼70% in developing countries [6], and 30–40% in the developed countries [5]. In this study, of the studied 384 children 173 (45.1%) were seropostive for H. pylori antibody. Same results have been shown by El Shafie et al. [7], who studied 407 children aging between 1 month and 13 years old in Menoufia governorate through serum antibodies and found H. pylori antibody in more than half (51%) of them. Naji et al. [8] in Yemen had tested 100 serum and stool specimens for H. pylori antibodies and antigen correspondingly. The age of the patients ranged from 10 to 80 years. Antibody was positive in 72 of the 100 samples tested (72%), whereas stool antigen was detected in 49 (49%) of 100 samples tested, which indicate higher exposure of H. pylori. In Turkey, ∼64.4% of children ageing 6–17 years old were infected [9]. School children in London had a prevalence rate of 16.7% according to O'Donohoe et al. [10]. In our study, analysis showed that there was no significant relationship between age of the children and prevalence of infection (P = 0.727). This could be explained by the fact that infection can happen in any age owing to the continuous presence of organism in the environment and susceptibility at any age. This finding was the same to that reported by Mahmud et al. [11] and Naji et al. [8] who stated that the prevalence of H. pylori is not influenced by age. They hypothesized that possible frequent antibiotics usage in this age might lead to un-intended clearance of infection. On the contrary, this finding was contrary to that reported by Balci et al. [12], which showed that the prevalence of H. pylori infection steadily increases with age among children. When we compared the prevalence of infection among males and females, there was no significant difference between them (P = 0.454). This can be explained by the fact that children at this age are exposed to nearly the same risk of infection in both sexes. This was in agreement with serological studies done by El Shafie et al. [7] and Castro et al. [13]; however, Naji et al. [9] had found a significant difference regarding sex, being more prevalent among female than male. They gave no clear explanation for this. Regarding socioeconomic level and residential area as other epidemiologic factors in H. pylori infection, analysis did not show any significant difference between positive and negative cases (P = 0.320). This is in line with Xin-Hua et al. [14] who stated that prevalence did not differ according to socioeconomic status and residence area. On the contrary, studies done by El Shafie et al. [7] and Braga et al. [15] found a significant difference regarding socioeconomic status and residence area. Positivity was significantly associated with overcrowdings (P = 0.038). This agrees with Ding et al. [16] who found that seropositivity was lower in children with family members less than four. Moreover, Ahmed et al. [17] found the most crowded homes are more risky for infection. However, Awuku et al. [18] found no association between H. pylori infection and household crowding. There was a relationship between prevalence of H. pylori and the main source of water supply. We found a significant difference (P < 0.001), as tap water was more risky than other sources. These results agree with Awuku et al. [18] and Naji et al. [8] who found that the prevalence of infection among participants who usually consumed tap water or well water during livelihood was 73.7% compared with 47.9% among those who usually consumed filtered water. Breastfeeding and its duration was not significantly related to the prevalence of H. pylori (P = 0.913). These results agree with Dore et al. [19] who found no association between breastfeeding and presence of infection. This contradicts with Bhuiyan et al. [20] and El Shafie et al. [7] who stated that breastfeeding is a potential protective factor against H. pylori, whereas Rothenbacher and Guenter [21] stated that breastfeeding does not protect against H. pylori infection. On the contrary, they found that the duration of breastfeeding is positively associated with the H. pylori prevalence especially for children breastfed for 6 month or more due to potential close contact with infected mother. In this work, we found a significant difference in infection (P = 0.004), being more among those who had positive family history of infection. These results agree with Yokota et al. [22]. This was mentioned at a Japanese study that highlighted the relationship between prevalence of H. pylori infection in children and their mothers. Their data showed that the prevalence of infection was 6 and 38% in mothers of negative and positive children (P = 0.04), respectively, and 12 (3 of 25) and 50% (8 of 16) (P = 0.01), respectively, in fathers [23]. These results disagree with Queiroz et al. [24] who stated that negative association remained between infection with H. pylori and family history of infection. Contact with domestic animals is another mode of transmission of H. pylori infection. In this study, there was a significant association between contact with domestic animals and presence of infection. These results agree with El Shafie et al. [7]. However this contradicts with Awuku et al. [18] who stated that epidemiological data have not been able to identify any major importance of any house animals as a vector in H. pylori transmission. A significant inverse relationship between good personal hygiene and presence of infection was clear in this work. This correlates with study of Nouraie et al. [25] but is contrary to the findings of Hoda et al. [26], who stated that childhood acquisition of H. pylori infection is not linked to hygienic practices. Regarding the relationship between the presence of H. pylori and dietary factors, there was no statistically significant association between eating salted snacks, soft drinks, and street food and the presence of H. pylori infection (P = 0.506, 0.156, and 0.593, respectively). This agrees with Assaad et al. [27]; however, the result was significantly different regarding eating fruit and vegetables which appeared to be protective. This agrees with results of Begue et al. [28]. Our results demonstrated a significant decrease in weight and height of positive children (P = 0.022 and 0.017, respectively). These results agree with El Shafie et al. [7] who found that H. pylori infection affects weight and stature. On the contrary, Cherian et al. [29] found no relationship between H. pylori infection and child anthropometric measurements. We found that there was a significant association between H. pylori infection and low blood hemoglobin level (P = 0.030). This agrees with Ali et al. [30], whereas it contradicts Pellicano and Rizzetto [31], who found that anemia was not increased in those with H. pylori infection. They suggested that such a phenomenon is uncommon in African children who have a high prevalence of both iron-deficiency anemia and H. pylori infection, but they showed no relationship between the two diagnoses.

  Conclusion Top

Seroprevalence of H. pylori among school children 6–12 years in Menoufia Governorate, Egypt, was 45.1%. Drinking municipal water, contact with domestic animal, and lack of personal hygiene were the major risk factors, in order. H. pylori infection was found to be negatively affecting the health of children, i.e., child growth and blood hemoglobin, to name a few.

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Conflicts of interest

There are no conflicts of interest.

  References Top

Marshall B, Warren J. Unidentified curved bacilli in the stomach of patients with gastritis and peptic ulceration. Lancet 1984; 1311–1314.  Back to cited text no. 1
Ghil H, Yoo J, Jung W, Chung T, Young H, Hwang C. Survey of Helicobacter infection in domestic and feral cats in Korea. J Vet Sci 2009; 10:67–72.  Back to cited text no. 2
Kandulski A, Selgrad M, Malfertheiner P. Helicobacter pylori infection: a clinical overview. Dig Liver Dis 2008; 40:619–626.  Back to cited text no. 3
Deeb M, Bahbah W, Abou-Elela D, Hessen M. Seroprevalence of Helicobacter pylori infection among school children in Al Qulubia governorate. Menoufia Med J 2017; 31:963–969.  Back to cited text no. 4
Raymond J, Bergert M, Kalach N. Helicobacter pylori in children. Presse Med 2008; 37:513–518.  Back to cited text no. 5
Hanafi M, Mohamed A. Helicobacter pylori infection: seroprevalence and predictors among healthy individuals in AL Madinah, Saudi Arabia. J Egypt Public Health Assoc 2013; 88:40–50.  Back to cited text no. 6
El Shafie A, Kandel S, Bahbah M. Seroprevalence of Helicobacter pylori infection among infants and children of Menoufia governorate Bahbah WA, Msc thesis. Menoufia Med J 2004; 31:63–68  Back to cited text no. 7
Naji1 A, Ameri1 G, Alkadasi M. Comparison of stool antigen and blood antibody test methods for detection of Helicobacter pylori infection and the risk factors. Int J Curr Microbiol Appl Sci 2014; 3:118–127.  Back to cited text no. 8
Selimoglu M, Ertekin V, Inandi T. Seroepidemiology of H. pylori infection in children living in eastern Turkey. Pediatr Int 2002; 44:666–669.  Back to cited text no. 9
O'Donohoe J, Sullivan P, Scott R. Recurrent abdominal pain and H. pylori infection in community-based sample of London children. Acta Paediatr 2001; 85:961–964.  Back to cited text no. 10
Mahmud S, Shah S, Ali S. Frequency of Helicobacter pylori (HP) infection in children with recurrent abdominal pain (RAP). Pak Armed Forces Med J 2015; 65:358.  Back to cited text no. 11
Balci Y, Aral Y, Covut I, Polat Y, Turk M, Acimis N. The frequency of Helicobacter pylori infection in Beta Thalassemia major Patients with recurrent abdominal pain. Pak J Med Sci 2011; 27:316–319.  Back to cited text no. 12
Castro L, González C, Muñoz A, Tovar-Ayona B. Prevalence of Helicobacter pylori from the oral cavity of Mexican asymptomatic children under 5 years of age through PCR. Arch Oral Bio 2017; 73:55–59.  Back to cited text no. 13
Xin-Hua Q, Huang X, Xiong P, Zhu C, Zhu CY. Does Helicobacter pylori infection play a role in iron deficiency anemia? A meta-analysis. World J Gastroenterol 2010; 16:886–896.  Back to cited text no. 14
Braga A, Fialho A, Rodrigues M, queiroz D, Braga L. Helicobacter pylori colonization among children up to 6 years: results of a community-based study from northeastern Brazil. J Trop Pediatr 2007; 53:393–397.  Back to cited text no. 15
Ding S, Minohara Y, Fan X. H. pylori infection induces oxidative stress and programmed cell death in human gastric epithelial cells. Infect Immun 2007; 75:4030.  Back to cited text no. 16
Ahmed K, Khan A, Ahmed I, Tiwari SK, Habeeb A, Ahi JD, et al. Impact of household hygiene and water source on the prevalence and transmission of Helicobacter pylori: a South Indian perspective. Singapore Med J 2007; 48:543.  Back to cited text no. 17
Awuku Y, Simpong D, Alhassan I Tuoyire D, Afaa T, Adu P. Prevalence of Helicobacter pylori infection among children living in a rural setting in sub.Saharan Africa. BMC Public Health 2017; 17:360.  Back to cited text no. 18
Dore M, Malaty H, Graham D, Fanciulli G. Risk factors associated with H. pylori infection among children in a Defined Geographic Area. Clin Infect Dis 2002; 35:240–245.  Back to cited text no. 19
Bhuiyan T, Qadri F, Saha A, Svennerholm A. Infection by Helicobacter pylori in Bangladeshi children from birth to two years: Relation to blood group, nutritional status and seasonality. Pediatr Infect Dis J 2009; 28:79–85.  Back to cited text no. 20
Rothenbacher D, Guenter H. History of breastfeeding and H. pylori infection. Int J Epidemiol 2002; 31:632–637.  Back to cited text no. 21
Yokota S, Konno M, Fujiwara S, Toita N, Takahashi M, Yamamoto S, et al. Intrafamilial, Preferentially Mother.to.Child and Intraspousal, Helicobacter pylori Infection in Japan Determined by Mutilocus Sequence Typing and Random Amplified Polymorphic DNA Fingerprinting. Helicobacter 2015; 20:334–342.  Back to cited text no. 22
Okuda M, Kirkuchi S, Osaki T, Ueda J, Maekawa K, Lin. Fukuda prevalence and incidence of Helicobacter pylori infection in Japanese children: a population based study in Japan. Helicobacter. 2015; 20:133-8.  Back to cited text no. 23
Queiroz D, Saito M, Rocha A. H.pylori infection in infant and toddlers in south America: concordance between (13c) urea breath test and monoclonal H-pylori stool antigen test. Helicobacter 2013; 51:3735–3740.  Back to cited text no. 24
Nouraie M, Latifi-Navid S, Rezvan H, Radmard A, Maghsudlu M, Zaer-Rezaii H. Childhood Hygienic Practice and Family Education Status Determine the Prevalence of Helicobacter pylori Infection in Iran. Dig Dis 2009; 14:40–46.  Back to cited text no. 25
Hoda M, Malaty D, Inger G, Nancy E, Pederson L. Co.twin study of the effect of environment and dietary elements on acquisition of Helicobacter pylori Infection. Am J Epidemiol 1998; 148:793–797.  Back to cited text no. 26
Assaad S, Chaaban R, Tannous F, Costanian C. Dietary habits and Helicobacter pylori infection: a cross sectional study at a Lebanese hospital. BMC Gastroenterol 2018; 18:48.  Back to cited text no. 27
Begue J, Gonzales CH Dietary risk factors associated with the transmission of H. pylori in Lima, Peru. Am Jo Trop Med. 2000; 59:637–640.  Back to cited text no. 28
Cherian S, Forbe D, Sanfilippo F, Cook A, Burgner D. Helicobacter pylori, helminth infections and growth: a cross sectional study in a high prevalence population. Acta Paediar 2009; 98:860.  Back to cited text no. 29
Ali M, Muhammad E, Hameed B, Hasoobe H. The impact of Helicobacter pylori infection on iron deficiency anemia in pregnancy. Panminerva Med 2017; 6:60–64.  Back to cited text no. 30
Pellicano R, Rizzetto M. Is hepcidin the bridge linking Helicobacter pylori and anaemia of chronic infection? Panminerva Med 2004; 46:165–169.  Back to cited text no. 31


  [Figure 1]

  [Table 1], [Table 2], [Table 3], [Table 4], [Table 5]

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