1 Department of Health Research and Policy, Stanford University School of Medicine, Stanford, CA
2 Department of Medicine, Stanford University School of Medicine, Stanford, CA
Reprint requests to Dr. Julie Parsonnet, Departments of Medicine and Health Research and Policy, Stanford University School of Medicine, Grant Building, Room S156, 300 Pasteur Drive, Stanford, CA 94305-5107 (e-mail: parsonnt{at}stanford.edu).
Received for publication January 10, 2005. Accepted for publication March 25, 2005.
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ABSTRACT |
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disease transmission; Helicobacter pylori; Hispanic Americans; immigrants; infection; prevalence; social class
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INTRODUCTION |
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More than 10 percent of the current US population is foreign-born, and an additional 10 percent is born of immigrant parents (3, 4
). The majority of immigrants in the United States are from Latin America (3
), with Mexico being the most common country of origin (4
). Replogle et al. (5
) found that Hispanics in the San Francisco Bay Area had 4.40 times the risk (95 percent confidence interval (CI): 2.80, 6.90) of H. pylori infection of non-Hispanic Whites. In studies using data from the Third National Health and Nutritional Examination Survey, persons who were foreign-born had 2.53 times the infection risk (95 percent CI: 1.55, 4.13) of persons who were US-born (6
). In addition, Latin Americans born in the United States or Canada had substantially lower H. pylori prevalence than those born outside the United States or Canada (7
). In both studies, risk of H. pylori infection was positively associated with household crowding, a low level of education, and low income.
Prevalence of H. pylori infection not only varies between racial/ethnic groups but also differs across regions. To identify factors that may help explain geographic variations in H. pylori prevalence in children, O'Rourke et al. (8) examined H. pylori infection status among children under 6 years of age on both sides of the US-Mexico border (El Paso, Texas, and Juarez, Mexico). According to the univariate analysis, Mexican children had 3.9 times the risk of H. pylori infection (95 percent CI: 1.72, 9.06) of US children. The odds ratio decreased to 1.75 (95 percent CI: 0.64, 4.52) after adjustment for socioeconomic variables, indicating that these factors could account for most of the difference in H. pylori prevalence between El Paso and Juarez.
Previous studies demonstrated that risk of H. pylori infection could vary by race/ethnicity, geographic location, and household characteristics. To study the independent effects of the above factors and to estimate the magnitude of their associations with H. pylori infection, we examined the prevalence of H. pylori infection and socioeconomic status in different generations of Hispanics and non-Hispanic Whites using data from a community-based cohort study conducted in the San Francisco Bay Area.
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MATERIALS AND METHODS |
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For this analysis, we restricted our study subjects to the SIFT Study participants (index cases and participating household members) with at least one parent who completed interviews and blood testing. We defined Latin America-born subjects with at least one Latin America-born parent as immigrants, US-born Hispanics with at least one Latin America-born parent as first-generation US-born Hispanics, and US-born Hispanics whose every participating parent was US-born as second-generation US-born Hispanics. The group "second-generation US-born Hispanics" could include third- or later-generation US-born Hispanics. In addition, we included a group of US-born non-Hispanic Whites for comparison.
Laboratory methods
For participants aged 2 years or more, H. pylori infection was diagnosed using serum enzyme-linked immunosorbent assay (5, 9
). The assay had an average 88.5 percent sensitivity and 99 percent specificity in both children and adults, as described elsewhere (9
). For children under age 2 years, we used a commercial stool enzyme-linked immunosorbent assay (HpSA enzyme immunoassay; Meridian Bioscience, Cincinnati, Ohio) to test for H. pylori infection. The assay had 96 percent sensitivity and 91 percent specificity, according to the manufacturer. We excluded subjects with borderline H. pylori results.
Statistical analysis
We defined a dummy variable, "generation," to represent four groups of people with different ethnicities and/or countries of origin: immigrants, first-generation US-born Hispanics, second-generation US-born Hispanics, and US-born non-Hispanic Whites. We assessed differences in baseline distributions of variables across the four groups using a two-sided Kruskal-Wallis test for continuous variables and the chi-squared test (or Fisher's exact test for small cell numbers) for dichotomous variables. A significant p value indicated that at least two of the four groups differed with respect to the distribution of a particular variable.
To estimate the association between a risk factor and H. pylori infection, we used generalized estimating equations (10) with an autoregressive correlation matrix to account for within-household correlations. Two different models were used. In the first (age-adjusted) model, the dependent variable was H. pylori infection status (yes vs. no) and the independent variables were subject's age (as a continuous variable) and one of the following variables: immigrant generation (either non-Hispanic Whites or second-generation US-born Hispanics were the reference group), subject's sex (male vs. female), parental H. pylori infection (yes vs. no), number of people in the household (>6 vs.
6), highest household education (no high school graduate vs.
1 high school graduate), and combined household income (<$30,000/year vs.
$30,000/year). In the second (multivariate) model, the dependent variable was H. pylori infection status and the independent variables included all of the following: immigrant generation, subject's sex, parental H. pylori infection, number of people in the household, and highest household education. For the above analyses, dichotomization of household size, education, and income variables was determined using each variable's median value in the study subjects as the cutoff point. To test for a trend in risk across different generations of Hispanics, we treated the variable "generation" as an ordinal variable and tested for significance using generalized estimating equations.
Missing demographic information from some parents had the potential to result in misclassification of first-generation US-born Hispanics as second-generation US-born Hispanics (64 persons). To assess the likelihood of this effect, we compared study characteristics in "possible" second-generation US-born Hispanics (53 subjects with only one participating parent) with those in "definite" second-generation US-born Hispanics (11 subjects with two participating parents) and in first-generation US-born Hispanics. Possible and definite second-generation US-born Hispanics were very similar in terms of their household socioeconomic characteristics and infection status (data not shown). Consequently, we grouped these subjects together in all analyses.
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RESULTS |
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Overall, the Hispanic subjects lived in more populated households than non-Hispanic Whites, and the household size decreased by generation in the United States. The median number of people in each household was eight (range, 320) for immigrants, six (range, 220) for first-generation US-born Hispanics, six (range, 210) for second-generation US-born Hispanics, and four (range, 211) for non-Hispanic Whites. As table 1 shows, 71.7 percent of the immigrants had more than six people in the household, and the percentage decreased to 49.4 percent for first-generation US-born Hispanics, 28.1 percent for second-generation US-born Hispanics, and 13.9 percent for non-Hispanic Whites (ptrend < 0.001).
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Information on household income was available for only one third of the study subjects (200 immigrants, 714 first-generation US-born Hispanics, 46 second-generation US-born Hispanics, and 65 US-born non-Hispanic Whites). Using data from these 1,025 persons, Hispanic households of all generations had a consistently lower combined household income than non-Hispanic White households. The proportions of Hispanic households with less than $30,000 in combined annual income were 79.0 percent, 71.7 percent, and 41.3 percent for immigrants and first- and second-generation US-born Hispanics, respectively (ptrend < 0.001). In contrast, only 15.4 percent of non-Hispanic White families had less than $30,000 in annual household income. Because Hispanic households had more family members than non-Hispanic White households, the annual income per capita in Hispanic households was even lower than that of non-Hispanic Whites.
Prevalence of H. pylori infection in the study subjects
The prevalence of H. pylori infection among Hispanics declined with increasing generations in the United States. Immigrants had the highest prevalence of H. pylori infection (31.4 percent), first-generation US-born Hispanics had an intermediate prevalence (9.1 percent), and second-generation US-born Hispanics had the lowest prevalence (3.1 percent) (ptrend < 0.001). The prevalence of H. pylori infection in non-Hispanic Whites (5.6 percent) was significantly lower than that in immigrants (p < 0.001) but was similar to that of first- and second-generation US-born Hispanics (p = 0.40 and p = 0.68, respectively). Likewise, the prevalence of H. pylori infection was highest in parents of first-generation US-born Hispanics and lowest in parents of US-born non-Hispanic Whites.
Association between immigrant generation and H. pylori infection
Age-adjusted analysis.
Compared with non-Hispanic Whites, the age-adjusted odds ratios for H. pylori infection were 8.60 (95 percent CI: 2.27, 32.58), 3.58 (95 percent CI: 0.90, 14.26), and 0.89 (95 percent CI: 0.11, 7.17) for immigrants and first- and second-generation US-born Hispanics, respectively (ptrend < 0.001) (table 2). Thus, although the first-generation Hispanics were not statistically different from non-Hispanic Whites with regard to H. pylori infection, the second-generation Hispanics were even more similar to non-Hispanic Whites in this respect. When second-generation US-born Hispanics were used as the reference group, the age-adjusted odds ratios for H. pylori infection were 9.70 (95 percent CI: 1.57, 60.00) and 4.32 (95 percent CI: 0.69, 26.96) for immigrants and first-generation US-born Hispanics, respectively (ptrend < 0.001). Among Hispanics, greater age, having at least one infected parent, and not having a high school graduate in the household were positively associated with H. pylori infection. Gender, household size, and combined household income were not significantly associated with H. pylori infection. Analyses treating age as a categorical variable (05, 615, and 16 years) and household size and income as ordinal variables produced similar results (data not shown).
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DISCUSSION |
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Results from our analysis lend credence to the hypothesis that both household characteristics and birth-country environment contribute to the risk of H. pylori infection among immigrants. Our finding also draws support from other published studies. Since transmission of H. pylori commonly occurs in early childhood, characteristics of the household environment such as parental H. pylori infection may increase the risk of H. pylori infection. In a population-based study of preschool children in southern Germany, Rothenbacher et al. (11, 12
) showed that multivariate odds ratios for H. pylori infection were 3.9 (95 percent CI: 1.4, 10.6) in children with an infected mother and 2.0 (95 percent CI: 0.8, 5.3) in children with an infected father. Similarly, among schoolchildren from high-risk regions in northeastern China, those with at least one infected parent had substantially higher risk of H. pylori infection (odds ratio = 30.4, 95 percent CI: 4.0, 232) than those with uninfected parents (13
).
In this study, lack of a high school diploma in the household remained independently associated with increased risk of H. pylori infection, but household crowding and income were not. Thus, parental education may be a more appropriate indicator of personal and household hygiene practices of the participants in our study, as well as other studies (1418
). For example, Moreira et al. (15
) found that parental education was the only socioeconomic variable that remained significantly associated with H. pylori after multivariate adjustment. The parents' higher educational attainment may be important in protecting children from H. pylori infection regardless of household crowding and socioeconomic conditions.
Aside from household characteristics, country of birth also appeared to be an important risk factor for H. pylori infection. In a study of Northern California adults aged 2039 years, Replogle et al. (5) observed a significant association between birth in a developing country and increased risk of H. pylori infection after adjusting for race/ethnicity, age, education, and income. A similar association was found by Gilboa et al. (19
) among people living in communal settlements in Israel. Factors that contributed to an elevated risk of infection among people born in developing countries may include limited access to clean water and food supplies, poor sanitation, malnutrition, and exposure to infected persons outside of the household (20
23
).
Limitations of our study included possible selection bias in the study participants and misclassification of immigrant generations. Since only 43 percent of the referrals were eligible and participated in the study, those who were not eligible or declined to participate might have differed from those who agreed to participate with regard to H. pylori infection and/or socioeconomic status. However, it is unlikely that the magnitude and direction of the selection bias were systematic across three generations of Hispanics and non-Hispanic Whites. Thus, the relative risk of H. pylori infection in our analysis may not be affected by differential selection bias. In addition, for subjects with only one participating parent, we could not determine the country of birth of the other parent. However, as we mentioned above in the "Statistical analysis" section, we think this potential misclassification is unlikely to have contributed significantly to our findings. Furthermore, several factors not measured in this study could also have contributed to the risk differences in successive generations of Hispanics. For example, a functional polymorphism of the interleukin-1 receptor-1 gene has been linked to increased susceptibility to H. pylori infection (24). Birth order and sibling's infection status could also affect a subject's risk of acquiring H. pylori (25
). Finally, since only a small percentage of the non-Hispanic Whites and the second-generation US-born Hispanics had H. pylori infection, analysis using either of those two groups as the reference group would result in wide confidence intervals.
To our knowledge, this study was the first to examine H. pylori infection in different generations of Hispanics. Our findings lend credence to the hypothesis that both household environment and birth in a developing country are important risk factors for H. pylori infection. It is likely that infection is acquired through person-to-person transmission within the household and through the local environment.
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ACKNOWLEDGMENTS |
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The authors thank Shufang Yang and Thomas Haggerty for technical assistance. Additionally, they gratefully thank Rosario L. Villacorta and the entire SIFT study team for their effort in collecting data and samples in the field. They also thank the following California health-care providers for their invaluable assistance with study recruitment: Santa Clara Valley Health Center emergency department (San Jose), Santa Clara Valley Health Center pediatric clinic (San Jose), East Valley Pediatric and Urgent Care Clinics (San Jose), Santa Clara County Office of Environmental Health (San Jose), Mayview Community Health Center (Palo Alto), Mayview Community Health Center (Mountain View), San Mateo County General Hospital pediatric and primary care clinics (San Mateo), Stanford Hospital emergency department (Stanford), and Willow Clinic (Menlo Park).
Conflict of interest: none declared.
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References |
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