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Association of Helicobacter pylori Infection and Height of Mexican Children of Low Socioeconomic Level Attending Boarding Schools

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  • 1 Infectious Diseases Research Unit, Gastroenterology Research Laboratory, Mexican Institute of Social Security, Mexico City, Mexico; GlaxoSmithKline, Research Triangle Park, North Carolina; Nutrition and Health Research Center, Research Center in Health Systems, National Institute of Public Health, Cuernavaca, Morelos, Mexico; Division of Gastroenterology, Hepatology and Nutrition, Vanderbilt University Medical Center, Nashville, Tennessee

This study evaluated the association between Helicobacter pylori infection and height in a population of schoolchildren of a low socioeconomic level regarding growth-related micronutrient status. It was a cross-sectional study of 685 children 5–13 years of age. Height and weight were recorded, a 13C urea breath test was performed for detection of H. pylori, and a blood sample was obtained for determination of micronutrient status. Helicobacter pylori infection was found to be associated with the height of children. Children with H. pylori infection are, on average, 1.32 cm lower (95% confidence interval [CI] = −2.22 to −0.42) in height than children without infection. There was an effect modification by age: for every one-year increase in age, height was 0.66 cm less (95% CI = −1.17 to −0.15) in children with H. pylori infection. This finding suggests that H. pylori infection has a negative effect on the growth of children.

INTRODUCTION

Helicobacter pylori infection is one of the most common bacterial infections in humans and is present in more than 50% of the population worldwide.1 In Mexico, the prevalence of antibodies against H. pylori was estimated to be 42.5% in 5–9-year-old children and 55.5% in 10–14-year-old children, according to the 1998 National Serologic Survey.2

A decrease in height-for-age is an indicator of diverse negative factors such as an inadequate diet in either quantity or quality, the effect of repeated infectious disease episodes, poor sanitary conditions, and difficulty getting access to health services. According to the 2006 National Health and Nutrition Survey, in Mexico, the prevalence of low height-forage in children 5–11 years of age was 10.4% in boys and 9.5% in girls.3

Helicobacter pylori infection has been associated with several diseases in adults, particularly chronic gastritis, duodenal or gastric peptic ulcer, and gastric carcinoma. Even when the infection is acquired during the first years of life, its consequences on children’s health are not known.4 In this group, H. pylori infection has been associated with iron deficiency and anemia. A greater frequency of H. pylori has also been reported in short-stature children and adolescents,57 and children who acquire the infection during follow-up have been shown to have a decreased growth rate.4 However, these studies have not considered other factors that may affect child’s growth such as zinc and vitamin A status.8

Therefore, the aim of this study was to evaluate the association between H. pylori and height in a school-age, low socioeconomic population, and consider the micronutrient status related to growth.

MATERIALS AND METHODS

Study population.

A cross-sectional study was conducted from June 2005 through September 2006. Eight hundred nine schoolchildren of the 945 eligible schoolchildren participate in this study. The participates were 5–13 years of age and of low socioeconomic status. The children at any of three public boarding schools in Mexico City participated. Their parents or tutors signed an informed consent form; in addition, schoolchildren more than seven years of age were asked to give their assent to participate in a research study. The protocol was reviewed and approved by the Research and Ethic Committees of the Mexican Institute of Social Security and the National Institute of Public Health. The study was authorized by the Secretariat of Public Education.

Anthropometric measurements.

Weight and height were measured. According to the technique suggested by Lohman and others,9 height and weight were recorded for children without shoes and wearing light clothes, standing straight, with their weight uniformly distributed on both feet and their arms hanging freely on the sides. The height measurement was performed by two independent observers. If the difference between them was ≥ 0.5 cm, the measurement was made again. The average measurement was used. Before starting each work session, the stature meter was checked for calibration using a standard 60-cm stick. An Easy Glide Bearing wall stadiometer (Perspective Enterprises, Portage, MI) with a reading precision of 1 mm was used. The height measurements were reported in centimeters, approximating the reading to the nearest 0.1 cm. For weight measurement, a digital scale (model 881; Seca, Hamburg, Germany) with a reading precision of 50 g for weights up to 50 kg and of 100 g for greater weights was used. Accuracy of the scale was maintained by using calibration weights. These measurements were made by dieticians who participated in the standardization process.

The body mass index was obtained (weight in kg/height in m2) and the schoolchildren were classified by using the cut-off points of Cole and others. 10,11 Schoolchildren were classified by age and sex as being thin, normal, and overweight or obese.

13C urea breath test.

The test to detect H. pylori consisted of collecting two samples of expired air. The basal sample was obtained 10 minutes after a child had ingested a beverage containing 2 g of citric acid (Citra-LP; San Miguel Proyectos Agropecuarios S.P.R., Hidalgo, Mexico) to delay gastric emptying. Immediately afterward, children were given 50 mg of 13C-labeled urea dissolved in 150 mL of water, and the final sample was collected after 30 minutes. 12 The 13 CO2: 12 CO2 ratio was calculated for the samples before and after the ingestion of 13 C urea. A change of ≥ 5 parts/1,000 was considered positive. 13,14 Samples were measured on a mass spectrometer (Breath-MAT plus; Finningan, Breman, Germany). The sensitivity and specificity of the test in children are > 90%. 15

Micronutrient nutritional status.

A venous blood sample (4.7 mL) was taken from each child to determine hemoglobin, ferritin, zinc, and retinol serum concentrations. Hematic cytometry was automatically performed by using the cyanometahemoglobin method (Beckman Coulter, Fullerton, CA). Hemoglobin concentrations were adjusted according to altitude above the sea level. 16 Ferritin was measured by radio-immunoassay (Inmunotech SA, Marseille, France). Retinol concentration was determined by high-performance liquid chromatography and zinc concentration was determined by atomic absorption spectrometry (Perkin Elmer, Wiesbaden, Germany). A moderate/severe iron deficiency was a ferritin level < 18 μg/L, and a normal/mild deficiency was a ferritin level ≥ 18 μg/L. 17 Hemoglobin, zinc, and vitamin A concentrations were grouped by tertile.

Socioeconomic status.

The study population consisted of children attending public boarding schools, a program offered by the Secretariat of Public Education for low-income families. However, to obtain more detailed information on possible differences because of the degree of socioeconomic exclusion, a questionnaire was also administered asking about housing conditions, ownership of goods (radio, television, videotape recorder, refrigerator, washing machine, store, oven, heater, telephone, computer, motorcycle, or car).

Goods possessed in each home were added. Homes were grouped under the corresponding quintile according to the obtained score and were further classified into two categories: the most marginal socially corresponded to the lowest two quintiles, and the least marginal socially corresponded to the highest three quintiles.

Overcrowding.

When the number of persons living in the house divided by the number of sleeping rooms was ≥ 3, the house was considered overcrowded.

Statistical analysis.

The demographic characteristics of the studied population were summarized using descriptive statistics. The schoolchildren’s height in cm was the dependent variable. An initial analysis assessed the mean difference of the height adjusted for age and sex according to socioeconomics and health study population’s characteristics. The variables related to the micronutrient concentration were assessed either as continuous or as categorical values. Socioeconomic status analysis was performed by principal components. 18

In the evaluation of the association between H. pylori and the schoolchildren’s height, we computed adjusted coefficients of height through use of a linear regression model with a Gaussian-link function. We used generalized estimating equations to account for correlations between participants in the same school boarding with an exchangeable correlation structure. This analysis considered the possible confounding effect of age, sex, degree of socioeconomic marginality, overcrowding, and iron nutritional status (hemoglobin concentration and iron deficiency according to ferritin concentration). Possible interactions between H. pylori and hemoglobin concentration, age, and degree of socioeconomic marginality were also considered.

The most parsimonious model included H. pylori infection, age (centered at nine years of age, which corresponds to the mean age of the studied population), sex, H. pylori interaction with age, degree of socioeconomic marginality, and hemoglobin concentration adjusted for altitude and centered on the lower level within the normal range (11.5 g/dL for schoolchildren < 12 years of age and 12.0 g/dL for children ≥ 12 years of age).

Using this model, we calculated the intersection value to determine the precise value for the effect modify variable (age) in which the estimated effect of H. pylori infection was different for the child’s height. 19 Models were checked to comply with the assumptions for linear generalized models. 20 The analysis was performed using the STATA version 8.2 statistical software (Stata Corp., College Station, TX).

RESULTS

Information was collected on 809 schoolchildren of the 945 who were invited to participate in this study. One hundred twenty-one children (15%) were excluded because of lack of information on their socioeconomic questionnaire. Another three were excluded because they had diseases related to growth. Thus, the statistical analysis was performed on the data collected for 685 schoolchildren. No statistically significant differences were found in the height adjusted to age and sex among the children who remained in the analysis and those who were excluded. Because of an insufficient amount of serum, the measurement of vitamin A and zinc was only feasible in 52.3% (n = 358) and 69.6% (n = 477) of the studied children, respectively. The general characteristics of the studied population are summarized in Table 1.

The mean ± SD age was 9.2 ± 1.8 years; 62.6% of the participants were female. Low height for age (stunting) was present in the 6.0% of schoolchildren; 22.3% of the children were overweight or obese. The mean ± SD hemoglobin level was 13.9 ± 1.0 g/dL, and 30.6% of the children had moderate or severe iron deficiency according to the ferritin concentration. Almost 35% had H. pylori infection.

Height means adjusted for age and sex according to the sociodemographic and health characteristics of the studied population are summarized in Table 2. Schoolchildren with H. pylori infection were shorter than children who were not infected (P = 0.002). With respect to the iron nutritional status and to the tertile of hemoglobin concentration, the mean height was greater in children in the second and third tertiles than in those in the first tertile. Schoolchildren with severe or moderate iron deficiency were shorter than children with mild or no iron deficiency, according to the ferritin concentrations (P = 0.040). Schoolchildren with a higher degree of socioeconomic marginality were shorter, on average, than children with a lower degree of socioeconomic marginality (P = 0.0001). No significant differences on height were found among schoolchildren according to home overcrowding and among the vitamin A and zinc tertiles.

The multivariate analysis showed a negative, age-dependent association between H. pylori infection and the schoolchildren’s height, adjusting by sex, degree of socioeconomic marginality and hemoglobin concentration. Because the H. pylori effect on height was modified by age, the effect increases as children get older. Nine-year-old H. pylori-infected schoolchildren measured an average −1.98 cm (95% confidence interval [CI] = −2.97 to −0.99, P = 0.0001) (Tables 3 and 4) less than same-age, uninfected children. For each one-year increment in age greater than seven years, children with H. pylori infection had an average height difference of −0.66 cm (95% CI = −1.17 to −0.15) (P = 0.012) compared with same-age, noninfected children (Table 3).

Additionally, the results of this model (Table 3) show that for each increment in hemoglobin g/dL, the height increases 1.08 cm (95% CI = 0.84–1.32, P = 0.0001). The association between H. pylori infection status and schoolchildren’s height did not depend on the hemoglobin concentration, i.e., the hemoglobin concentrations did not modify the effect of H. pylori status on the schoolchildren’s height.

Although the children in this study were at a low socioeconomic level, a difference in height could still be detected among the schoolchildren with the highest degree of socioeconomic marginality versus those with the lowest degree of socioeconomic marginality. Schoolchildren coming from the lowest income homes were −1.38 cm (95% CI = −2.28 to −0.48, P = 0.003) shorter than children from homes that were not of the lowest income, adjusting for other variables included in the model.

According to the results obtained by this model, Table 4 shows an estimated effect of H. pylori infection on the height per year, per age of the studied children.

DISCUSSION

This study found an association between H. pylori infection and a decreased height in schoolchildren. This association was modified by age, with older children showing greater effects.

Some cross-sectional studies have reported results similar to ours regarding the existence of this association, as well as its dependence on age. Perri and others found a significant association only for children more than 8.5 years of age: 25.8% of children this age and infected by H. pylori were under the 25th percentile of height-for-age, compared with 8.3% of children not infected. 22 In Scotland, Patel and others found a 1.1-cm difference in the height increment during a follow-up after four years, favoring the preadolescents not infected by H. pylori when compared with those infected.6 Fialho and others found significant differences in Brazilian children 3–14 years of age in the percentage of children who were allocated under the 25th percentile of height-for-age in accordance with the infection of H. pylori. These differences were significant only in children more than eight years of age. 23

Our results suggest that the effect of H. pylori on the schoolchildren’s height is cumulative, worsening with every year of age. This finding could occur because older children have been exposed longer to the infection, which is acquired in early childhood in developing countries.

These results are consistent with those from a cohort study performed in Colombia, where the longitudinal growth rate in preschool children was assessed. A 0.5 cm/year decrease on the growth rate was found in children who acquired the infection. This slowing down of the growth rate was relatively constant during the follow-up time. No catch-up phenomenon on height during an 8-month follow-up was found in children after they were infected. The authors conclude that the effect of H. pylori on height is significant and irreversible. 4,24

The mechanisms by which H. pylori infection may affect growth have not been identified, but possible mechanisms such as dyspepsia and hypochlorhydria have been proposed. It has been suggested that this infection may reduce food intake because of its association with dyspepsia.6 Nevertheless, most infected subjects remain asymptomatic and the proportion of children with dyspeptic symptoms may be similar among infected and noninfected children. 25 Helicobacter pylori infection causes hypochlorhydria and the loss of the protecting barrier in the stomach, thus facilitating the acquisition of enteral infections, which may, in turn, cause diarrheal diseases. However, results from studies on the incidence of diarrheic episodes in infected and noninfected children are not consistent. 26,27

Passaro and others in a retrospective cohort found that children seropositive for H. pylori had more and lengthier episodes of diarrhea the year after the acquisition of the infection than children who were not infected. This effect was greater in the two months after infection. 27 In Thailand, no difference in the incidence of diarrheal disease according to the H. pylori infection was found among children less than five years of age, either in those who acquired the infection during the study in contrast to the prevalent cases or among these and children who remained negative during the follow-up. 26 In the Colombian cohort study, a positive association was found between the H. pylori-infected children and the days absent from nursery school because of respiratory infections. According to the authors, this association could be explained by respiratory infections being occasional manifestations of gastrointestinal infections during childhood.4

The effect of H. pylori infection on children’s growth may be related to the immune response on infection. Helicobacter pylori infection provokes an increase in some cytokines, therefore inducing chronic inflammation. 28 Infection with H. pylori could produce a systemic immunostimulation and subsequent growth retardation. 29 Infections may also decrease appetite and increase the nutritional requirements because of a catabolic phase relationship with the immune response.

In this study, we found a positive relationship between serum hemoglobin concentration and schoolchildren’s height, despite children exhibiting a normal hemoglobin concentration. To date, we cannot explain this fact, but it has been suggested that a decreased intake of iron-containing food may be related to a reduction on the total caloric intake and protein intake. Furthermore, iron deficiency has been associated with a greater risk of morbidity.8 Studies conducted in Thailand, India, and Kenya have found improvement in growth after anemic children were given iron supplements. 3032

Helicobacter pylori infection has been associated with iron deficiency and iron-deficiency anemia. 3336 In a study that included adolescents in South Korea, Choe and others found that the height-for-age mean was less in those who had H. pylori infection and anemia because of iron deficiency. The authors concluded that infection, together with iron-deficiency anemia, more than infection per se, may affect growth. 5,37 Süoglu and others in a study comprising a population 4–16 years of age found that the mean height-for-age Z score in H. pylori-infected and iron-deficiency anemic patients was lower than that in patients who were non–iron-deficiency anemic and negative for H. pylori infection.35 Yokota and others reported that H. pylori strains in iron-deficiency anemia patients showed a better ferric ion uptake and a fast, iron-dependent growth compared with strains from patients without iron-deficiency anemia. The capability of H. pylori for ferric ion uptake could be a causal factor for the iron-deficiency anemia. 36 Hypochlorhydria has also been proposed as a mechanism by which H. pylori is associated with anemia and iron deficiency because non-heminic iron absorption is decreased in persons with this condition. 22,38 In our study, no effect modification according to the hemoglobin concentrations on the association between H. pylori infection and schoolchildren’s height was found. Nevertheless, we found that the hemoglobin concentration was independently associated with height in these children. This important association should be evaluated in further studies.

This study was carried out with children from low-income families. All of them attended public boarding schools. However, even in this group, which could be considered economically homogeneous, differences in height could be identified according to the degree of socioeconomic marginality, but no significant differences in average height among schoolchildren according to vitamin A or zinc concentrations could be found. The micronutrient deficiency of zinc or A vitamin has been associated with growth retardation, and supplementation studies with zinc have shown increases in the children’s height.8 Nevertheless, most schoolchildren in this study had normal serum zinc and retinol concentrations.

The results of this study should be interpreted with caution because the study was a cross-sectional study. We should recognize a possible problem of temporal ambiguity. It is possible that schoolchildren who are nutritionally compromised have more susceptibility to initial H. pylori colonization, they could be more susceptible to chronic infection, or the infection influences nutritional status. However, the different effects of infection on the height in relation to age, with the effects increasing as children get older, suggested that this chronic infection influences the schoolchildren’s height. Prospective studies are required to confirm the results of this study. Other possible limitation is residual confounding.

Helicobacter pylori infection and growth restriction have a risk factors relationship with socioeconomic level. We attempted to control for these factors by including only schoolchildren with a low socioeconomic level in our study. Additionally, we include degree of socioeconomic marginality in the analysis. Helicobacter pylori infection was associated with shorter height in schoolchildren. This association is age dependent; i.e., the effect increases as children get older. These results suggest that H. pylori infection has a negative effect on children’s growth. In this study, we also found an association between hemoglobin concentration and height. Additional information is needed to understand the effect of iron on growth.

Table 1

General characteristics of the study population (n = 685), Mexico*

Table 1
Table 2

Mean heights (cm) adjusted for age and sex according to the sociodemographic and health characteristics of the study population (n = 685), Mexico*

Table 2
Table 3

Association between Helicobacter pylori infection and height in schoolchildren, Mexico

Table 3
Table 4

Estimated effect of Helicobacter pylori infection on the schoolchildren’s height by age, Mexico*

Table 4

*

Address correspondence to Ximena Duque, Infectious Diseases Research Unit, Hospital de Pediatria, CMN Siglo XXI, IMSS, Av. Cuauhtemoc No. 330, Col. Doctores, Del. Cuauhtemoc, Mexico City, Distrito Federal, Mexico, CP 06720. E-mail: xduquelo@hotmail.com

Authors’ addresses: Jenny Vilchis, Ximena Duque, Javier Torres, Fabiola Navarro, and María-Eugenia Mendoza, Infectious Diseases Research Unit, CMN Siglo XXI, Instituto Mexicano del Seguro Social, Mexico City, Mexico, E-mails: jennyben17@hotmail.com, xduquelo@hotmail.com, jtorresl57@yahoo.com.mx, fabisnava@hotmail.com, and mendoza_ma13@hotmail.com. Robertino Mera, GlaxoSmithKline, Research Triangle Park, NC 27709, E-mail: robertino.m.mera@gsk.com. Segundo Morán, Gastroenterology Research Laboratory, CMN Siglo XXI, Instituto Mexicano del Seguro Social, Mexico City, Mexico, E-mail: segundomoran@hotmail.com. Teresita González-Cossío, Nutrition and Health Research Center, National Institute of Public Health, Cuernavaca, Morelos, Mexico, E-mail: tgonzale@insp.mx. María de la Luz Kageyama-Escobar, Research Center in Health Systems, National Institute of Public Health, Cuernavaca, Morelos, Mexico, E-mail: kescobar@correo.insp.mx. Pelayo Correa, Division of Gastroenterology, Hepatology and Nutrition, Vanderbilt University Medical Center, Nashville, TN 37232, E-mail: pelayo.correa@vanderbilt.edu.

Acknowledgments: We thank the students, parents, and boarding school staffs where the study was performed for their participation; Berenice Gonzalez, Amelia Hernandez, Angeles Cruz, Victoria Roque and Octavio Rivera for collaborating in the research aspect of this study.

Financial support: This work was supported by the National Council of Science and Technology (SALUD-2004-C01-74/A-1) and the Fund for Research Promotion (2005/1/I/089 and 190).

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