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Am. J. Trop. Med. Hyg., 74(4), 2006, pp. 536-539
Copyright © 2006 by The American Society of Tropical Medicine and Hygiene

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PREVALENCE OF AND FACTORS ASSOCIATED WITH HELICOBACTER PYLORI INFECTION IN CHILDREN IN THE NORTH OF VIETNAM

BANG V. NGUYEN*, KHANH G. NGUYEN, CAM D. PHUNG, ODILE KREMP, NICOLAS KALACH, CHRISTOPHE DUPONT, JOSETTE RAYMOND, AND GWENAËLLE VIDAL-TRECAN
Pediatric Department, Hanoi Medical University, Hanoi, Vietnam; Digestive Disease Division, National Institute of Epidemiology and Hygiene, Hanoi, Vietnam; Pediatric Department of Saint Antoine, Saint Vincent de Paul Hospital, Catholic University, Lille, France; Neonatology and Gastroenterology Department, Cochin–Saint Vincent de Paul Hospital Group, Faculty of Medicine, Descartes University, Paris, France; Microbiology Department, Cochin–Saint Vincent de Paul Hospital Group, Faculty of Medicine, Descartes University, Paris, France; Public Health Department, Cochin–Saint Vincent de Paul Hospital Group, Faculty of Medicine, Descartes University, Paris, France


ABSTRACT
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
The study aimed at evaluating the seroprevalence of and sociodemographic, health, lifestyle, and environmental hygiene conditions associated with Helicobacter pylori infection in Vietnamese children. Data from 824 children, aged from 6 months to 15 years and gastrointestinal symptom free when consulted, admitted to a university hospital, were collected using a structured questionnaire and ELISA test for H. pylori infection. The data were examined using univariate and multivariate analyses. H. pylori seroprevalence was 34.0%. Age groups from 3 to 6 years and older than 6, and number of offspring were positively and independently associated with H. pylori seropositivity [adjusted OR (95% CI): 2.9 (1.5–5.5); 1.9 (1.1–3.1) and 1.8 (1.1–2.6), respectively]. Breastfeeding more than 6 months was negatively and independently associated with H. pylori seropositivity [adjusted OR (95% CI): 0.5 (0.3–0.9)]. Mother’s age, history of allergy, gastro-duodenal disease history in the past, initiating collective life before 6 years, sharing bed with parents and time of bed sharing with parents > 24 months were positively but not independently associated with H. pylori seropositivity. None of the other environmental or lifestyle conditions examined was associated with H. pylori infection. Our results support person-to-person transmission and the role of sociodemographic factors in H. pylori infection.


INTRODUCTION
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Helicobacter pylori (H. pylori) is one of the most frequent etiologic agents of peptic ulcer, gastritis, and gastric cancer. The prevalence of these entities might then be reduced by controlling H. pylori infection. H. pylori infection is acquired during the early childhood period.1 In Asia, the prevalence of H. pylori infection in children has been examined in many countries.17 In Vietnam, two studies conducted in small-size pediatric populations found H. pylori seroprevalence globally at 34.5% in children,8,9 at 64.0% in urban and 41.2% in rural children, respectively.10 Moreover, the results of studies trying to identify factors associated with H. pylori infection in Asia either are controversial or lack consistency.1,4,7 This makes difficult the prevention of this infection in Asiatic countries.5,6 The objectives of this study were to evaluate the prevalence of H. pylori infection in Vietnamese children and to identify factors associated with H. pylori infection.


MATERIALS AND METHODS
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
We conducted a cross-sectional survey (April 2001 to August 2002) using a structured questionnaire in a population of children from all provinces in the northern Vietnam. Every consecutive outpatient aged more than 6 months and less than 15 years presenting every Wednesday at the pediatric department of a university hospital was included. However, children with acute diarrhea, ulcer disease, and repeated abdominal pain or immunocompromised status were excluded to avoid selection or measure biases. Informed parental consent was obtained for 824 of 1,062 eligible children (77.6%). The protocol had been submitted and approved by the ethics committee of Hanoi Medical University.

Information on sociodemographic characteristics of the family, health status, and potential exposure (environmental and lifestyle conditions) of children was collected from their parents by investigators during an interview. Concerning health status, answers had to be evidenced by individual health booklet or physician’s prescription or main caregiver’s interview. Venous blood samples were obtained from children to determine their H. pylori infection status. An in-house ELISA, validated in the Microbiology Department, Karolinska Institute, Stockholm11 (sensitivity: 99.6%, specificity: 97.8%), was performed for dosage of H. pylori IgG antibody against specific H. pylori antigen in the Microbiology Division of Digestive Diseases (National Institute of Epidemiology and Hygiene). The cutoff value for seropositivity was taken at 0.18 optical density units.

Standard descriptive statistics were used to examine the seroprevalence. Associations between sociodemographic characteristics, health status, and variables of potential exposure (environmental and lifestyle conditions), and H. pylori seropositivity of children were examined using univariate analysis. Backward stepwise procedures were used for multivariate analysis building a final model only including variables that were statistically significant in univariate analysis. Associations were expressed as odds ratio (OR) with their confidence intervals (95% CI). Data were analyzed using SPSS software (SPSS for Windows version 10.1 Copyright SPSS Inc., 1998).


RESULTS
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Among 824 children without gastrointestinal symptoms on admission, 280 (34.0%) were H. pylori positive. The association between H. pylori seropositivity in children and 1) the sociodemographic and health status variables and 2) the environmental and lifestyle conditions is shown in Tables 1Go and 2Go, respectively. Table 3Go shows the variables independently associated with H. pylori seropositivity in children.


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TABLE 1
Sociodemographic and health factors associated with H. pylori seropositivity in a hospital-based population of 824 Vietnamese children aged 6 months to 15 years
 

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TABLE 2
Environmental hygiene and lifestyle conditions associated with H. pylori seropositivity in a hospital-based population of 824 Vietnamese children aged 6 months to 15 years
 

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TABLE 3
Sociodemographic characteristics variables, environmental hygiene, and lifestyle conditions associated with H. pylori seropositivity in a hospital-based population of Vietnamese children aged 6 months to 15 years (N = 529): final results of logistic regression model
 

DISCUSSION
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Our study was the first epidemiologic study in Vietnam designed both to assess H. pylori seroprevalence in a hospital-based population of children without gastrointestinal symptoms on admission and to identify associations of this infection with sociodemographic characteristics, health status, lifestyle, and environmental conditions. H. pylori seroprevalence was 34.0% in this population. Age of children and number of offspring were identified as positively and independently associated while breastfeeding more than 6 months was negatively associated with H. pylori infection. Mother’s age at child’s birth, initiating collective life before school age, allergy history, children’s gastro-duodenal disease history in the past, sharing bed with parents and the time of sharing bed with parents more than 24 months were also positively associated with H. pylori seropositivity but not independently of other variables.

The H. pylori seroprevalence found in our study was similar to that of 34.5% observed on 104 Vietnamese children in the 1990s.8 However, it was much lower than that of 64.0% from an urban group and 41.2% from a rural group of children in a recent study performed in 308 Vietnamese children,10 but children in the latter study were defined as up to 18 years old and not selected on their absence of digestive symptoms. It was higher than that observed in children from Taiwan (8.1% in 3- to 6-year-old children) and from South Korea (22.0%).6,7 These neighboring countries though also developing have a higher mean income per inhabitant than Vietnam that might indirectly explain the difference in H. pylori seroprevalence. However, H. pylori prevalence in Vietnamese children was lower than those observed in China (42.2% in southern China,1 69% in Shandong12), in Thailand (50%),3 and in India (60%)2 where the mean income per inhabitant was somewhat similar to Vietnam. However, differences in the population selected and in the kits used for ELISA especially render difficult comparison between these results.

As reported in some previous studies,1,13,14 we noted a high seroprevalence in children under 3, with a sharp increase between 3 and 6 years of age.

Some of the variables associated with the infection in Vietnam support directly or indirectly the hypothesis of person-to-person pathway transmission due to promiscuity: being a child in a family with more than one child and also, though not independently, sharing the same bed with parents, time of bed sharing with parents longer than 24 months, and initiating collective life earlier than school age. A very strong body of evidence exists showing that promiscuity, particularly family overcrowding (large number of offspring and bed sharing), is associated with H. pylori infection in children.2,4,7,1517 Currently, to our knowledge, the association of lower risk of H. pylori seroprevalence in children of young mothers found in our study had never been reported. However, it may only reflect a smaller number of offspring in young families. This argument issues from the fact that among 217 unique children, 41 of 181 born by mothers younger than or equal to 30 years were H. pylori seropositive (22.8%), while 17 of 38 born by mothers older than 30 years were seropositive (44.7%) (P = 0.007); in contrast, among 516 children from families with more than 1 child, 119 of 326 (36.5%) born to mothers younger or equal to 30 years were seropositive, while 75 of 117 (38.4%) were born to mothers older than 30 years (P = 0.706).

We also found that breastfeeding longer than 6 months may be protective against H. pylori infection as noted in some previous studies.16,18,19 This might be due to passive immunity by anti–H. pylori antibodies from breast milk, but further investigation is needed to confirm this finding although still controversial.

However, we could not confirm directly the results of previous studies in developed16,17 and developing countries3,7,15 showing that deprived household living conditions in childhood were associated with a higher risk of H. pylori infection. As noted previously,20 we found children’s H. pylori infection neither associated with several variables related to environmental exposure4,21 nor with lifestyle conditions, such as sharing utensils and chewed-food feeding reported in some studies.22

The positive but not independent association between H. pylori seropositivity and children’s allergy history in the past found in our study had been observed in some recent studies, although the opinion about the nature of the association stayed largely controversial.23,24 The association between children’s history of treated gastro-duodenal disease in the past and the higher rate of H. pylori seropositivity observed in our study was reported in recent studies.9 It might reflect a more susceptible status of the host to this infection in these children. However, an ongoing or a relapse of H. pylori infection in these children could not be excluded and further investigation is required.

Despite several difficulties, we had tried to reduce selection biases, including a large population not expressing digestive symptoms of children of all age groups from different areas. However, like several hospital-based studies on this infection, our population failed to be representative for a general population, as evidenced by more urban participants (47.5% in our study for a nationwide proportion of 35.0%) and by male predominance (62.4% in our study for a nationwide proportion of 51.5%). Another issue may arise from the lack of accuracy in the answers of parents possibly due to overdiscretion or ignorance when reporting details related to socioeconomic and hygienic variables. This has resulted in missing values or may have led to misclassification of variables and may weaken the the power of statistical methods as seen in Table 3Go where only 64.2% of the study population (529 of 824 children) could be included for analysis.

In conclusion, our study figured a moderately high H. pylori seroprevalence in a pediatric population in northern Vietnam. Age of children and number of offspring were positively associated with H. pylori seropositivity. Breastfeeding longer than 6 months was negatively associated with H. pylori seropositivity. These associations support person-to-person transmission pathways. It seems that in Vietnam, the prevention of H. pylori infection in childhood may lie on family planning and on promoting prolonged breastfeeding.


Received August 6, 2004. Accepted for publication November 14, 2005.

Acknowledgments: We would like to thank Hanoi Medical University and the National Institute of Epidemiology and Hygiene for supporting techniques and materials indispensable for the study; the personnel of the Pediatric Department of Bachmai Teaching Hospital (Hanoi), whose invaluable assistance and primordial involvement in organization and participation makes these findings possible; and our patients and their families participating in the study for their preciously collaborative spirit.

Financial support: This study was supported by the Ministry of Health of Vietnam.

* Address correspondence to Bang V. Nguyen, 299 Giap Bat Street, Hanoi, Vietnam. E-mail: hongbang52{at}yahoo.com Back

Authors’ addresses: Bang V. Nguyen, 299 Giap Bat Street, Hanoi, Vietnam, Telephone: 84 903293212, E-mail: hongbang52{at}yahoo.com. Khanh G. Nguyen, 18 Hang Hom Street, Hanoi, Vietnam, Telephone: 84 4 8289702, E-mail: nguyengiakhanh1945{at}yahoo.com. Cam D. Phung, Digestive Disease Division, National Institute of Epidemiology and Hygiene, 1 Yersin Street, Hanoi, Vietnam, E-mail: cam{at}fpt.vn. Odile Kremp, Pediatric Department of St Antoine, St Vincent de Paul Hospital, Catholic University, Lille, France, Telephone: 33 3 20877618, E-mail: kremp.odile{at}ghicl.net. Nicolas Kalach, Pediatric Department of St Antoine, St Vincent de Paul Hospital, Catholic University, Lille, France, Telephone: 33 3 20877617, E-mail: kalach.nicolas{at}ghicl.net. Christophe Dupont, Neonatology and Gastroenterology Department, University René Descartes, CHU Cochin–Saint Vincent de Paul, Paris, France, Telephone: 33 1 40488060, E-mail: secretariat.dupont{at}svp.ap-hop-paris.fr. Josette Raymond, Microbiology Department, University René Descartes, CHU Cochin–Saint Vincent de Paul, Paris, France, Telephone: 33140487656, E-mail: j.raymond{at}svp.ap-hop-paris.fr. Gwenaëlle Vidal-Trecan, Public Health Service, University René Descartes, CHU Cochin–Saint Vincent de Paul, Paris, France, Telephone: 33 1 58412646, E-mail: gwenaelle.vidal-trecan{at}univ-paris5.fr.

Reprint requests: Bang V. Nguyen, 299 Giap Bat Street, Hanoi, Vietnam, Telephone: 84 903293212, E-mail: hongbang52{at}yahoo.com.


REFERENCES
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 

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