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Am. J. Trop. Med. Hyg., 75(3), 2006, pp. 509-512
Copyright © 2006 by The American Society of Tropical Medicine and Hygiene

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HELICOBACTER PYLORI INFECTION IN CHILDREN OF LOW AND HIGH SOCIOECONOMIC STATUS IN NORTHEASTERN BRAZIL

JOSÉ MIGUEL L. PARENTE*, BENEDITO BORGES DA SILVA, MÍRIAN P. S. PALHA-DIAS, SCHLIOMA ZATERKA, NANCY F. NISHIMURA, AND JOSÉ MURILO ZEITUNE
Department of Gastroenterology and Department of Pediatrics and Gynecology, Federal University of Piaui, Piaui, Brazil; Department of Public Health, Federal University of Ceará, Ceará, Brazil; Gastrocenter, State University of Campinas, Sao Paulo, Brazil


ABSTRACT
TOP
 ABSTRACT
METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
This survey was designed to evaluate the prevalence of Helicobacter pylori infection in asymptomatic children from families of low and high socioeconomic status living in two neighboring communities in Teresina in northeastern Brazil. The study included 303 children, 163 (53.8%) males and 140 (46.2%) females, ranging in age from 6 months to 12 years. Helicobacter pylori status was determined by the H. pylori stool antigens test, in which sensitivity and specificity values for Brazilian children were 96.9% and 100%, respectively. The prevalence rates were 55.0% (93 of 169) and 16.4% (22 of 134) for children of low and high socioeconomic status, respectively (P < 0.001). Infection with H. pylori occurred early in life (before 2 years of age) in both groups (22.9% versus 14.3%; P = 0.061) and increased as the children became older. The rate of infection in children 11–12 years of age living in the poor area was as high as the levels found in Brazilian adults. An improved standard of living is followed by a sharp decrease in the prevalence rates in children, even in a developing country such as Brazil.

Helicobacter pylori is one of the most common bacterial infections of humans worldwide.1 Infection in humans is usually acquired during childhood and probably lasts throughout life if the person is not treated.2 There have been numerous reports of a strong correlation between socioeconomic status and prevalence of infection.3,4 Low prevalence occurs in industrialized countries and higher prevalence rates have been observed in underdeveloped and developing countries.5 Previous studies have suggested that the high prevalence observed in these countries is related to crowded households, habits (e.g., food preparation, hand washing), and lack of sanitary facilities.6,7 However, few studies have characterized the differences between H. pylori infection rates in person with high and low socioeconomic status in developing countries.8,9 To the best of our knowledge, this is the first report on the prevalence of H. pylori infection in children in two neighboring urban communities in Brazil, one with families with a high economic status and the other with families with a low socioeconomic status.


METHODS
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 ABSTRACT
 METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
Study design and subjects. This cross-sectional study was reviewed and approved by the Institutional Review Board of the Federal University of Piauí, Brazil. All parents or legal guardians of minors gave their written consent prior to participation in the study.

The study was carried out between September 2001 and February 2002 in Teresina, the capital of Piauí, which is one of the least economically developed states in Brazil.10 Persons were enrolled from neighboring communities. Participants included families living in the richest area of the city and those from the poorer area. One street separated these areas. Household conditions in the high-income area were more than adequate, but in the low-income area, typical shanty houses consisted of only a living room and a bedroom, without bathrooms, and rustic outhouses without pits. Children in the neighborhood had close contact with filth and human feces from accumulation of trash from nearby residences and open sewers along unpaved roads.

Two groups of children were included in the study: group A from the impoverished area (200 dwellings) and group B from the high-income area (250 dwellings). Houses in both communities had been previously numbered and households to be surveyed were chosen by means of a table of random number. Forty-six houses were excluded because there were no children within the previously defined age range or the guardian did not give consent. A questionnaire was used to obtain information regarding monthly family income, water supply, garbage collection, sewage system, and household sanitary and family lifestyle. Interviews were conducted and stool samples were collected in households by one of the authors.

Asymptomatic children ranging in age from 6 months to 12 years were enrolled prospectively. Only one child from each house was enrolled, and the index child was randomly chosen. Children were excluded from the study if they had gastric symptoms, acute or chronic diarrhea, mental deficiencies, or if they had taken antibiotics, bismuth salts, nitroimidazoles compounds, or proton pump inhibitors within the previous four weeks. One child from the impoverished area was excluded because a H. pylori stool test result was equivocal.

Sample collection and H. pylori stool test. An H. pylori specific stool antigens (HpSA) test (Premier-Platinum HpSA; Meridian Diagnostics, Cincinnati, OH) Ohio, USA) was used according to the manufacturer’s recommendations. Stool samples were stored at –20°C for up to one year before testing in the Gastrocenter at the State University of Campinas. The period in which samples were frozen did not affect the accuracy and reproducibility of the diagnostic assay and samples can be stored at this temperature indefinitely.11 All procedures with stool samples included appropriate safety measures to avoid risk of contamination of the specimen during collection, storage, and processing.

The HpSA test has been shown to be highly accurate in diagnosis11 and in epidemiologic studies on pediatric populations.12 It was previously validated for diagnosis of H. pylori infection in Brazilian children. When this test was compared with culture, histologic analysis, and a urease test, the sensitivity, specificity, positive predictive value, and negative predictive value were 96.9%, 100%, 100%, and 98.0%, respectively.13 Moreover, the population in this study had demographic features similar to the persons enrolled in the present study. Plates were evaluated by direct visual reading (yellow = positive, white = negative) and read at 450 nm using a spectrophotometer. The cut-off values used were ≥ 0.160 = positive, < 0.140 = negative, and 0.140–0.159 = equivocal. Samples with equivocal results were retested.

Statistical analysis. Student’s t-test was used to compare the different household aspects of both socioeconomic groups. The univariate Pearson’s chi-square test with Yates’ correction was used to measure the differences in the overall prevalence of the outcomes and the association of each variable with H. pylori infection. The linear tendency of the proportions of positivity of the H. pylori test for different age ranges was analyzed by the chi-square test for trend. A multivariate analysis was used to describe the independent association of monthly family income, household aspects, and living conditions (independent variables) with H. pylori infection status (dependent variable). P values < 0.05 were statistically significant. Data were analyzed with the Statistics Package of SPSS version 9.0 software (SPSS, Inc., Chicago, IL).


RESULTS
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 ABSTRACT
 METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
Socioeconomic groups. Three hundred three children were enrolled: 169 (55.8%) in group A (89 males and 80 females, mean ± SD age = 6.0 ± 3.374 years) and 134 (44.2%) in group B (74 males and 60 females, mean ± SD age = 6.4 ± 3.435 years). The median monthly family income was < US$ 300.00 (range = US$ 15.00–260.00, mean ± SD = US$ 233.53 ± $107.96) in group A and > US$ 1,800.00 (range = US$ 1,900.00–9,500.00, mean ± SD = US$ 3,570.33 ± $4,346.96) in group B. The household crowding index, which was obtained by dividing the number of people living in the household by the number of rooms, was 1.9 occupants/room in the impoverished area, which indicated overcrowding, and 0.9 occupants/room in the affluent area (P = 0.003).

Prevalence of H. pylori. One hundred fifteen children were positive for H. pylori; the overall prevalence was 38.0% (95% confidence interval [CI] = 1.31–4.12). A higher prevalence was observed in children from the slum area (55.0%, 95% CI = 2.39–6.71) compared with those from the high socioeconomic status area (16.4%, 95% CI = 1.67–3.82), (P < 0.001). No statistically significant difference was observed between males (54.8%) and females (45.2%) (odds ratio [OR] = 3.35, 95% CI = 1.94–5.82, P < 0.001).

Infection with H. pylori occurred early in life in both socioeconomic status groups (Table 1Go). In the area with low socioeconomic status, 22.9% of those less than two years of age were positive for H. pylori. Positivity rates increased sharply with age: 46.9% by 3–4 years of age, 70.0% by 5–6 years of age, and 71.4% by 11–12 years of age (P < 0.001). In the area with high socioeconomic status, 14.3% were infected before two years of age. However, positivity rates were similar in older age groups: 15.4% by 3–4 years of age, 17.4% by 5–6 years of age, and 21.7% by 11–12 years of age (Figure 1Go). None of these differences were statistically significant (P = 0.52).


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TABLE 1
Overall results for the Helicobacter pylori stool test in 303 Brazilian children according to age ranges and socioeconomic status (SES) groups
 

Figure 1
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  		    FIGURE 1. Prevalence rates of Helicobacter pylori infection in children from northeastern Brazil according to age and socioeconomic status (SES).

 
Housing and sanitary facilities were different in the impoverished and the high income areas (Table 2Go): garbage collection (20.7% versus 100%), sewage system (21.9% versus 100%), and plumbing (2.4% versus 100%), respectively (P < 0.001). Analysis of these independent variables was done to evaluate risk factors for acquisition of infection (Table 3Go). Among the H. pylori-positive children in both groups, 75 (65.2%) of 115 had no sewage system or private outhouses, 40 (34.8%) of 115 had these facilities, 76 (66.1%) of 115 had no municipal garbage collection, and 39 (33.9%) of 115 had this public service. These results showed an association between H. pylori status and absence of a sewage system (P < 0.001) and garbage collection (P < 0.001).


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TABLE 2
Household aspects according to socioeconomic status (SES) groups
 

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TABLE 3
Association between household aspects and prevalence of Helicobacter pylori infection in 303 Brazilian children
 
All dwellings in both communities were supplied with the same treated water. However, 165 (97.6%) of 169 households in the slum area transported water to the home from the nearby community faucets in buckets and five-gallon tins. Comparison of this data with all H. pylori-positive children indicated that only 24 (20.9%) of 115 households with H. pylori-infected children had indoor plumbing and 91 (79.1%) of 115 had no plumbing facilities. Univariate analysis showed a direct association between H. pylori status and the absence of proper water supply in the dwellings (P < 0.001).

Multivariate analysis was used to identify potential risk factors for infection with H. pylori (Table 4Go). The final model confirmed the high risk of three living aspects: lower family income (OR = 2.0, 95% CI = 1.43–2.80, P < 0.001), dwellings without a sewage system (OR = 2.94, 95% CI = 1.78–4.15, P < 0.001), and houses without garbage collection (OR = 2.31, 95% CI = 1.03–3.02, P < 0.001). Although univariate analysis showed an association between water supply and a positive stool test result, the multivariate model did not confirm this association as a risk for H. pylori infection in childhood (OR = 1.01, 95% CI = 0.70–3.23, P = 0.293).


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TABLE 4
Multivariate analysis of childhood risk factors associated with Helicobacter pylori infection in children from northeastern Brazil*
 

DISCUSSION
TOP
 ABSTRACT
 METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
The present study indicated that the overall prevalence of H. pylori infection in children from the slum area was high. Our results were similar to those of another study that included Brazilian children living in an impoverished area5 and to those observed in underdeveloped nations.14,15 In this area, we also observed a considerable number of infected children before two years of age, with a tendency to increase quickly in the first few years of life. Thus, the rate by 5–6 years of age was as high as those observed in adults in impoverished urban16 and rural17 populations in Brazil and Africa.18 Conversely, the overall prevalence observed in the area with high socioeconomic status was low, similar to those encountered in Swedish19 and German20 children. Children less than two years of age also were infected, although there was only a slight, non-significant increased risk in the older age ranges. The highest rate observed in children 11–12 years of age in the affluent group was similar to the lowest rate observed in children 0.5–2 years of age living in the poor area. We speculate that the low prevalence of H. pylori infection in children with high socioeconomic status may be a reflection of living standards and improvements in personal habits.

If one considers family composition and household aspects, this study also showed an association between a positive H. pylori stool test result and household overcrowding. These findings were observed mainly in the impoverished area, where rustic dwellings were small and the number of persons living in these houses was high, with close contact among children and adults. As previously reported, these results suggest that household overcrowding, close contact, and inadequate hygiene often promotes the person-to-person transmission of H. pylori infection by oral-oral or fecal-oral routes.21 However, since other routes of H. pylori acquisition were not evaluated in the present study, mother-infant and sibling-sibling transmission may have a major role in the primary transmission pathways of H. pylori within families.22,23 Such a limitation may require future studies regarding the routes of H. pylori acquisition and transmission.

Univariate analysis showed a positive association between H. pylori infection and the absence of a sewage system, garbage collection service, and indoor plumbing. These factors were confirmed in the multivariate model as risk factors for H. pylori infection; water supply was not a risk factor. However, we observed during the interviews that water could be easily contaminated by inadequate hygiene practices in the slum area when it was transported to the houses in large cans. It was evident that close contact of children, especially during early life, with a filthy environment increased the risk of H. pylori infection transmission through the fecal-oral route. This finding is consistent with an epidemiologic study carried out in Peru in which environmental factors, such as unhygienic food preparation, were incriminated as a probable mechanism of transmission of H. pylori infection in developing countries.24 Thus, additional studies are needed to clarify these findings regarding H. pylori transmission by water contamination, either at the source or in the home during water storage.25

Our study shows that early childhood is a critical period for H. pylori acquisition, mainly for the population with a low socioeconomic status, as reported by others.26 This infection also occurred at other times during infancy, even among children with a higher standard of living in Brazil, as observed in developed nations.27,28 The prevalence of H. pylori infection in both communities was not related to the country, but to the healthy standard of living of the population. Improvements in hygiene practices and lifestyle, which would decrease acquisition of this infection, are regarded as the most important reason for differences in rates of infection, as observed in industrialized countries.3,29

Received August 27, 2005. Accepted for publication March 29, 2006.

Acknowledgments: We thank Professor Dr. Dulciene Maria Magalhães Queiroz (Laboratory of Research in Bacteriology, Federal University of Minas Gerais, Belo Horizonte, Brazil) for reviewing the manuscript.

Financial support: This study was supported by grants from the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior/Ministério da Educação e Cultura, Brazil, and Núcleo Brasileiro para Pesquisa do Helicobacter pylori.

* Address correspondence to José Miguel L. Parente, Rua Professora Julieta Neiva Nunes No. 5821, Bairro Uruguai, Teresina, Piauí, Brazil 64057-085. E-mail: parentepalha{at}uol.com.br Back

Author’s addresses: José Miguel L. Parente, Rua Professora Julieta Neiva Nunes No. 5821, Bairro Uruguai, Teresina, Piauí, Brazil 64057-085, E-mail: parentepalha{at}uol.com.br. Benedito Borges da Silva, Avenida Elias João Tajra No. 1600, Teresina, Piauí, Brazil 64049-300. Mírian P. S. Palha-Dias, Rua Rio Grande do Sul No. 940, Teresina, Piauí, Brazil 64014-100. Schlioma Zaterka, Nancy F. Nishimura and José Murilo R. Zeitune, Rua Carlos Chagas No. 420, Bairro Barão Geraldo, Campinas, São Paulo, Brazil 13081-970.


REFERENCES
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