Helicobacter pylori Infection in Different Generations of Hispanics in the San Francisco Bay Area

Chiaojung J. Tsai1,2, Sharon Perry2, Luz Sanchez2 and Julie Parsonnet1,2

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.


    ABSTRACT
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 References
 
To quantify the contributions of household and environmental factors to Helicobacter pylori infection, the authors examined H. pylori infection among several generations of Hispanics in the San Francisco Bay Area. Between 2000 and 2004, household members were tested for H. pylori and interviewed about demographic factors and household pedigree. An immigrant was defined as someone born in Latin America with at least one Latin America-born parent; a first-generation US-born Hispanic was defined as someone born in the United States with at least one Latin America-born parent; and a second-generation US-born Hispanic was defined as someone born in the United States with at least one US-born parent. Prevalences of H. pylori in immigrants and first- and second-generation US-born Hispanics were 31.4% (102/325), 9.1% (98/1,076), and 3.1% (2/64), respectively. Compared with second-generation US-born Hispanics, the age-adjusted odds ratios for H. pylori were 9.70 (95% confidence interval (CI): 1.57, 60.00) for immigrants and 4.32 (95% CI: 0.69, 26.96) for first-generation US-born Hispanics (ptrend < 0.001). These odds ratios decreased to 6.19 (95% CI: 1.13, 33.77) and 3.24 (95% CI: 0.59, 17.82), respectively, after adjustment for parental infection (odds ratio (OR) = 2.94, 95% CI: 1.59, 4.38), low education (OR = 1.76, 95% CI: 1.20, 2.68), and crowding (OR = 1.23, 95% CI: 0.84, 1.79). Both the household and birth-country environments probably contributed to declining H. pylori prevalence among successive generations of Hispanics.

disease transmission; Helicobacter pylori; Hispanic Americans; immigrants; infection; prevalence; social class


Abbreviations: CI, confidence interval; SIFT, Stanford Infection and Familial Transmission


    INTRODUCTION
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 References
 
The prevalence of Helicobacter pylori infection varies across different regions and racial/ethnic groups. H. pylori infection during childhood is now rare in developed countries, and the worldwide prevalence is decreasing rapidly over time (1Go). In contrast, 20 percent of infants in Mexico are infected by age 1 year, and 50 percent of Mexican children are infected by age 10 years (2Go). Approximately 66 percent of the adult population in Mexico harbors H. pylori (2Go).

More than 10 percent of the current US population is foreign-born, and an additional 10 percent is born of immigrant parents (3Go, 4Go). The majority of immigrants in the United States are from Latin America (3Go), with Mexico being the most common country of origin (4Go). Replogle et al. (5Go) 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 (6Go). 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 (7Go). 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. (8Go) 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.


    MATERIALS AND METHODS
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 References
 
Study design and population
The study population was derived from the Stanford Infection and Familial Transmission (SIFT) Study, a prospective cohort study designed to investigate means of H. pylori transmission within San Francisco Bay Area households (9Go). Index cases with gastroenteritis were identified from 17 public health clinics and emergency rooms in Santa Clara and San Mateo counties. The index cases and their households were then invited to participate in this study. A visit was scheduled for each eligible household. During the household visit, information about the household's pedigree structure, each member's race/ethnicity and country of birth, the highest educational attainment in the household, household socioeconomic status, and issues related to the index case's gastroenteritis was obtained. Persons who participated in the study also donated blood samples for H. pylori testing. For children under age 2 years, stool samples were also requested. Biologic samples collected at the home visits were transported directly back to the laboratory and stored at –20°C until they were tested. In instances where stool was unavailable from the household visit, shipping supplies were left with the subjects for them to send samples by overnight mail. Informed consent was obtained from all subjects or their guardians in accordance with guidelines for the conduct of clinical research issued by Stanford University and the US Department of Health and Human Services.

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 (5Go, 9Go). The assay had an average 88.5 percent sensitivity and 99 percent specificity in both children and adults, as described elsewhere (9Go). 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 (10Go) 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.


    RESULTS
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 References
 
Household characteristics
Between January 2000 and September 2004, a total of 1,303 SIFT households (43 percent of the eligible referrals) participated in this study. Of the 1,303 households, 1,073 included participants who had at least one parent with information on H. pylori infection, race/ethnicity, and country of birth. Of these, 979 (91.2 percent) were Hispanic families, 44 (4.1 percent) were non-Hispanic White families, and the remaining 50 families (4.7 percent) were of other races/ethnicities. The 979 Hispanic households included 1,465 subjects with participating parents, and the 44 non-Hispanic White families included 72 subjects with participating parents. Thus, we included the above-mentioned 1,537 persons as our study subjects in the subsequent analyses. Among the 1,465 Hispanic subjects, 325 (22.2 percent) were immigrants, 1,076 (73.4 percent) were first-generation US-born Hispanics, and 64 (4.4 percent) were second-generation US-born Hispanics. All of the 72 non-Hispanic White subjects were US-born with US-born parents. The median ages at interview were 9.1 years (range, 0.3–45.4) for immigrants, 2.2 years (range, 0.01–26.2) for first-generation US-born Hispanics, 1.9 years (range, 0.1–46.5) for second-generation US-born Hispanics, and 5.1 years (range, 0.1–43.1) for non-Hispanic Whites.

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, 3–20) for immigrants, six (range, 2–20) for first-generation US-born Hispanics, six (range, 2–10) for second-generation US-born Hispanics, and four (range, 2–11) 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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TABLE 1. Characteristics of subjects and their households, Stanford Infection and Familial Transmission Study, 2000–2004

 
A total of 38 subjects (2.5 percent) did not provide information on the highest educational attainment in their households. Based on the 1,499 subjects with available information on household educational level, the percentages of households with at least one high school graduate were similar between immigrants (48.9 percent) and first-generation US-born Hispanics (49.7 percent) (p = 0.81). A total of 73.0 percent of the households of second-generation US-born Hispanics contained at least one high school graduate—a percentage that was significantly higher than that of immigrant and first-generation US-born Hispanic households. Households of non-Hispanic White subjects had higher levels of education (88.9 percent with at least one high school graduate) than households of second-generation US-born Hispanics (p = 0.02).

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 (0–5, 6–15, and ≥16 years) and household size and income as ordinal variables produced similar results (data not shown).


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TABLE 2. Age-adjusted odds ratios for subjects with Helicobacter pylori infection, Stanford Infection and Familial Transmission Study, 2000–2004*

 
Multivariate analysis.
The multivariate analysis was based on 1,499 study subjects with data on household educational level. Results were mutually adjusted for immigrant generation, subject's age, subject's sex, parental H. pylori infection, household size, and highest household education. In the multivariate analysis using non-Hispanic Whites as the reference group, the odds ratios for H. pylori infection decreased to 4.50 (95 percent CI: 0.71, 28.41), 2.11 (95 percent CI: 0.33, 13.30), and 0.68 (95 percent CI: 0.07, 6.98) for immigrants and first- and second-generation US-born Hispanics, respectively (ptrend < 0.001) (table 3). When second-generation Hispanics were used as the reference group, the multivariate odds ratios for H. pylori infection decreased to 6.19 (95 percent CI: 1.13, 33.77) and 3.24 (95 percent CI: 0.59, 17.82) for immigrants and first-generation US-born Hispanics, respectively. Greater age, having at least one infected parent, and being from a household with no high school graduates remained independently associated with higher risk of H. pylori infection in the multivariate analysis. Further adjustment for combined household income yielded similar results (data not shown).


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TABLE 3. Multivariate odds ratios for subjects with Helicobacter pylori infection, Stanford Infection and Familial Transmission Study, 2000–2004*

 

    DISCUSSION
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 References
 
This study of H. pylori infection among predominately low-income Hispanic immigrants in the San Francisco Bay Area showed that the risk of H. pylori infection in Hispanics declined with increasing generations in the United States. According to the age-adjusted analysis, first-generation US-born Hispanics had a risk lower than that of immigrants but 3.6 times higher (with borderline significance) than that of non-Hispanic Whites. The risk of H. pylori infection in second-generation US-born Hispanics became very similar to that of non-Hispanic Whites. Within the Hispanic population, first-generation US-born Hispanics also had higher risk of H. pylori infection than second-generation US-born Hispanics, although the difference was not statistically significant. In the multivariate analysis, the trend of decreasing risk of H. pylori infection with increasing generations of Hispanics remained significant. Having at least one infected parent and low educational attainment in the household were independently associated with higher risks of H. pylori infection. Thus, these factors probably contributed to the decrease in H. pylori prevalence among successive generations of Hispanics.

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. (11Go, 12Go) 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 (13Go).

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 (14Go–18Go). For example, Moreira et al. (15Go) 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 20–39 years, Replogle et al. (5Go) 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. (19Go) 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 (20Go–23Go).

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 (24Go). Birth order and sibling's infection status could also affect a subject's risk of acquiring H. pylori (25Go). 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.


    ACKNOWLEDGMENTS
 
This study was supported by US Public Health Service grant R01 AI42801-05 from the National Institutes of Health.

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.


    References
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 References
 

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