Helicobacter pylori (H. pylori) colonization of the stomach is the most common of the chronic bacterial infections in humans.1 It is considered one of the main findings in gastroenterology and is one of the microorganisms of greatest interest in human pathology.2,3 Its origin dates back some 58,000 years.4 Between 1985-89, Warren and Marshall5 associated the presence of the bacterium with chronic gastritis and ulcer, and since then, much work has been carried out in that field. The genesis of chronic gastritis, duodenal and gastric ulcer in children and adults, and both gastric adenocarcinoma and gastric mucosa-associated lymphoid tissue (MALT) lymphoma have been attributed to it. Once acquired, the infection persists, and the majority of infected individuals remain asymptomatic.

Calculations suggest that approximately half of the world’s population is colonized by H. pylori, with wide variability between different populations, possibly related to different factors, such as the virulence of the microorganism, host susceptibility, antibiotic use, and environmental conditions that include socioeconomic level. Genetic, racial, and cultural factors are less clearly involved.6,7 Transmission via the digestive route is well-accepted.6 Prevalence ranges from 1-2% in studies conducted on asymptomatic children in the Netherlands, to over 90% in Bangladesh.6 In developing countries, children are infected mainly before 10 years of age, and the highest prevalence peak in adults (80%) is before 50 years of age. In developed countries, studies show that infection is rarely produced before 10 years of age. It increases to 10% between 18 and 30 years of age and to 50% above 60 years of age.8

The prevalence of H. pylori infection in Cuba has not been widely analyzed. The majority of studies have been conducted on pediatric and adult populations with gastrointestinal symptoms. A high rate of H. pylori infection has been identified in adult patients with gastric ulcer (91%), duodenal ulcer (99%), and chronic gastritis (94%), with an elevated expression of the cagA+ gene.9–12 There are fewer studies on children, but a relation to anemia in school children (79%)13 and to diagnoses of antral chronic gastritis (67.7%) has been observed.14 Opportune preventive measures for stopping H. pylori transmission will reduce the incidence of those diseases and will depend on knowledge of the history of H. pylori infection. Therefore, the aim of the present study was to identify the prevalence of H. pylori infection and the associated socioeconomic, environmental, and lifestyle factors in the pediatric population of 3-year-old children in the province of Havana.

Of the 1,274 three-year-old children enrolled in the study, 100% of their parents or guardians correctly completed the questionnaire applied by the family physicians. The characteristics of the study participants are shown in Table 1. The prevalence of H. pylori infection was 5%.

Table 2 shows the bivariate associations with H. pylori and Table 3 shows the factors associated with H. pylori infection, after the confounding factor adjustment. The risk factor found for H. pylori infection was sleeping together (PR 1.27; 95% CI: 1.03-1.50), and the protective factors were married/living with a partner (PR 0.94; 95% CI: 0.85-0.99) and drinking water delivered by a water truck (PR 0.16; 95% CI: 0.04-0.72).

To the best of our knowledge, the present analysis is the first population-based study investigating the prevalence of and factors associated with H. pylori infection in a population of healthy 3-year-old children in the capital city of Havana, Cuba. The prevalence of bacterial infection in the study population was the result of environmental and lifestyle conditions. The cross-sectional analysis conducted on the 3-year-old children appearing in a database of the longitudinal HINASIC cohort provided the knowledge of the magnitude of the infection at that age. Sleeping accompanied was an important risk factor and the civil status of married/living with a partner and drinking water from a water-delivery truck were protective factors.

From the total number of 3-year-old children surveyed, 83% provided the stool samples needed for H. pylori testing, which enabled the prevalence of the infection to be calculated. The strengths of our study were the fact that the questionnaires were correctly formulated and applied by qualified medical personnel that had been following the children for several years, the majority of questionnaires were answered by the children’s parents (90%), and an internationally validated H. pylori test recommended for epidemiologic studies on that age group was employed.18 In addition, highly qualified technical personnel from the Instituto Nacional de Higiene, Epidemiología y Microbiología de Cuba (INHEM) carried out the external control of the results of the parasitology tests performed at the parasitology laboratories of the health areas involved, guaranteeing the reliability of the stool test results. The following two limitations of our study were identified: a history of ulcers or gastritis in the parents or guardians of the participating children was not determined and thus could not be analyzed as an associated factor, and the low prevalence of H. pylori Ag made it difficult to analyze the possible associated factors. Nevertheless, the results are valuable.

Cuba is a country that has medium and low resource settings. Despite those conditions and the strong economic blockade imposed by the United States for more than 50 years, unlike other countries with the same level of development, its health and education indicators are similar to those of the developed world. That situation, the fact that our study was conducted in an urban zone, and the high rate of antibiotic use in the pediatric population most likely were contributing factors to our study results.19–22 The prevalence of H. pylori in the 3-year-old children analyzed places us in an intermediate prevalence pattern in the international context, but we are close to the pattern of industrialized countries, if we take into account that early childhood prevalence is approximately 1.2% in Western Europe.6 In the Latin American countries of Ecuador, Chile, Brazil, and Mexico, an important percentage of children are already infected (63%, 25%, 31.1% and 10%, respectively).21,23–26 On the African continent, studies by Amberbir et al. describe a prevalence of 41% in children 3 years of age in an Ethiopian population, and in Uganda, 28.7% in 1-year-old children, 46% of children between 1 and 2 years of age, and 51.7% of children between 3 and 5 years old are already infected.27,28 In a recent meta-analysis conducted by Zabala Torres et al., those authors report prevalence of 20% in children under 6 years of age (95% CI: 14%-25%), among other results.29

Children sleeping together with other persons was the risk factor identified in the present study. Regardless of not having determined a history of infection in the adults living with the children, a high prevalence of infection detected in the adult Cuban population (75-90%)8–12,14 and evidence of infection transmission between couples suggest an increased risk for transmission to children living with infected individuals.24,25,29–32 Family has been found to play a fundamental role in the transmission of the H. pylori bacterium, especially within the first years of life, during which the most probable cause is oral-oral transmission from the mother to the child.24,29,32

It appears that living in a stable nuclear family unit is a protective factor against bacterial infection. Greater care given to the children is most likely an important factor and a plausible explanation is the presence of better personal and environmental hygiene habits related to a higher educational level of the study population. In addition, the greater antibiotic use detected in the study participants was relevant, which could lend important weight to that result.24,31

The consumption of potable water delivered by water truck (tankers) was another factor that contributed to the protection against H. pylori infection. The technical condition of the water supply system is not good in all parts of Havana and therefore the distribution of water by tankers is necessary. Despite the inconvenience of that type of public service, it appears that water is safer for drinking, if it does not flow through the water pipeline network, where it can become cross-contaminated due to structural deficiencies. In their 1997 study, Johnson et al. showed that chlorinated water was a factor that inactivated the bacterium, interfering with its transmission by water.33 A recent review revalidated contaminated water as a source of H. pylori, but insists on the need for further detailed study on that route of transmission.34 Eichelberger et al. presented information on the association between environmental risk factors and H. pylori infection in the United States based on data from the National Health and Nutrition Examination Survey (NHANES), indicating that environmental exposure (incorrect water use and occupational contact with soil) play an important role in the transmission of H. pylori (adjusted odds ratio [OR] 2.7, 95% CI: 1.3-5.6).35

In conclusion, the estimated prevalence of H. pylori infection in early childhood places Havana in an intermediate position in the international context. Socioeconomic conditions appear to be important factors in the presence of the infection. Opportune interventions should be implemented to reduce future complications.

The present study was funded by the Wellcome Trust (090375), the Nottingham University Hospital Charitable Trust, the Nottingham Respiratory Biomedical Research Unit, and the Instituto Nacional de Higiene, Epidemiología y Microbiología, Havana, Cuba.

The authors declare that there is no conflict of interest.