IJE Advance Access originally published online on August 2, 2005
International Journal of Epidemiology 2005 34(6):1348-1355; doi:10.1093/ije/dyi152
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Article |
Dynamics of Helicobacter pylori infection in a US–Mexico cohort during the first two years of life
1 University of Texas Health Science Center, School of Public Health, Houston, TX, USA
2 University of Alberta, Faculty of Medicine and Dentistry, Edmonton, Alberta, Canada
3 Lawton and Rhea Chiles Institute, University of South Florida, Tampa, FL, USA
4 Mexican Social Security Institute, Juarez, Chihuahua, Mexico
5 Texas Tech University Health Sciences Center—School of Medicine, El Paso, TX, USA
* Corresponding author. Division of Gastroenterology, University of Alberta, Zeidler Ledcor Centre, 130 University Campus, Edmonton, AB T6G 2X8, Canada. E-mail: karen.goodman{at}ualberta.ca
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Background The Pasitos Cohort Study has followed children in El Paso, Texas and Ciudad Juarez, Mexico since 1998 to identify determinants of Helicobacter pylori infection. This paper describes patterns of acquisition and elimination of H. pylori infection in 468 children from birth to 24 months.
Methods Mothers were recruited during pregnancy at maternal-child clinics; children were targeted for follow-up examinations every 6 months after birth. H. pylori infection was detected using the 13C-urea breath test, corrected for age-dependent variation in CO2 production.
Results Test results were available for 359, 341, 269, and 215 children around target ages of 6, 12, 18, and 24 months, respectively. The person-time at risk of a first detectable infection was 7742 person-months; 128 first infections were detected, thus the incidence rate was 1.7% per month (95% confidence interval 1.4–2.0%). Rates were similar in boys and girls and on both sides of the border; evidence suggests, however, that this similarity could be due to selection bias. Among children with follow-up after a positive test, 77% tested negative at a later visit.
Conclusions The initial acquisition of detectable H. pylori infection occurred at a rate of 20% per year among Pasitos Cohort children from birth to 24 months of age. A key finding, with implications for clinical, community health, and research settings, is that most of these infections did not persist. The transient nature of early H. pylori infection should be considered when designing research or contemplating therapeutic intervention for this age group.
Keywords Child, cohort studies, Helicobacter pylori, infant, infection, Mexican Americans, Mexico, Texas, United States
Accepted 5 July 2005
Helicobacter pylori infection is a bacterial infection of the stomach, affecting half or more of the world population. Persistent H. pylori colonization causes chronic gastritis and peptic ulcer, digestive diseases of major impact, and evidence supports a causal role in gastric cancer, one of the most common cancers worldwide.1–3 The public health burden of this infection, in terms of morbidity, mortality, and health care costs, is considerable.4,5
This infection is associated with poor socioeconomic conditions, and, in particular, residential crowding.6 The usual portals of entry and exit to and from the human host remain unclear, thus the precise modes of transmission have not been identified, though direct person-to-person transmission is likely.6,7 Age-specific patterns of occurrence show that most H. pylori infections are acquired in early childhood, thus the infection is most dynamic during the first few years of life.8 Effective prevention measures have not been identified owing to inadequate knowledge of the natural history and determinants.
Although H. pylori prevalence is highest in developing countries, the National Health and Nutrition Examination Survey showed that, around 1990, 25% of US children aged 6–19 years had this infection, with a disproportionate distribution across racial/ethnic groups.9 The prevalence was 17% in non-Hispanic whites, 40% in non-Hispanic blacks, and 42% in Mexican-Americans (58% in those not born in the US or Canada).
The Pasitos Cohort Study aims to estimate rates of incidence and spontaneous elimination of H. pylori infection in children, starting at birth, on both sides of the US/Mexico border at El Paso, Texas and Ciudad Juarez, Chihuahua and to estimate the effect of socioeconomic indicators, hygiene and diet on H. pylori incidence, persistence, and recurrence in early childhood. This paper presents a description of the dynamics of H. pylori infection from birth to 24 months of age in Pasitos Cohort children, focusing on the rate of first detectable infection, patterns of persistence, and frequencies of elimination and recurrence.
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Methods |
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The Pasitos Cohort Study recruited pregnant women from Women, Infant and Child (WIC) clinics in Socorro and San Elizario, El Paso County, Texas and maternal-child clinics of the Mexican Social Security Institute (IMSS) in Ciudad Juarez, Mexico from April 1998 to October 2000. At baseline, prior to the birth of the enrolled cohort children, staff interviewed mothers regarding the household environment. In this ongoing cohort study, we target follow-up exams at 6-month intervals beginning at age 6 months. At each follow-up visit, conducted at the clinic or participants' homes, we take measurements of weight and height, collect blood and breath samples for H. pylori testing, and interview the child's caretaker to ascertain information about selected exposures. Details regarding study methods and recruitment have been published.10
Owing to difficulties in following a low income, border population, exams do not always occur at target ages. When an exam does not occur at the target age, it is conducted as soon as possible thereafter. Some exams take place before the target age to coordinate with clinic visits for the convenience of participants. To account for gaps in follow-up, we designate target ages of 6, 12, 18, and 24 months as visits 1, 2, 3, and 4, respectively. If a visit does not occur approximately within 3 months before or after a given target age, the child is considered to have missed the corresponding visit. This descriptive analysis of infection dynamics presents data for target ages of 6, 12, 18, and 24 months, collected from October 1998 to December 2002.
For the present analysis, we classify H. pylori infection status based on the 13C-urea breath test. For this test, harmless 13C-labelled urea is ingested and the exhaled CO2 is analysed for excess 13C.11 If the infection is present in the stomach, urease secreted by H. pylori hydrolyses the 13C-labelled urea into ammonia and CO2, leading to an increase in 13C relative to other carbon isotopes in the exhaled CO2. We use the IRIS system (Infrared-13C-Stable Isotope Analyser, Wagner Analysen Technik, Germany), a non-dispersive isotope-selective infrared spectrometer, to measure the 13C/12C ratio in breath samples for the urea breath test.12–14 Breath samples are collected in aluminium bags through a rubber mouthpiece with a one-way valve. The bags attach to the IRIS for analysis. For children <24 months of age, who are often unable to blow air into a bag, a mask is attached to the mouthpiece to capture the exhaled breath. For breath tests administered through 24 months of age, we collected a baseline breath sample before having the child drink 150 ml of fruit juice with a 75 mg dose of 13C-urea, and a second breath sample 20 min later. Breath samples were transported to the lab for analysis. Protocols such as this have shown excellent accuracy in validation studies,15 although such studies include few preschool children.16
The test value is the change (delta-over-baseline) in the 13C/12C ratio comparing the second breath sample to the baseline sample. Evidence suggests that validity of breath test results in young children can be improved by correcting for variation in body-mass-dependent CO2 production, as proposed by Klein;17 therefore, we applied this correction. There has been little validation of either the uncorrected or corrected breath test results among infants and toddlers.16 This is because biopsy-based evaluation, generally used for the gold standard diagnosis, is not frequently justifiable in this age group.
A few reports present estimates of breath test accuracy in preschool children;18–24 some show reduced accuracy relative to older age groups whereas others show comparable accuracy. In some studies, higher delta-over-baseline cut-off values improved accuracy for younger children.19,24 Our experience shows that Klein's correction, in effect, increases the delta-over-baseline cut-off value with decreasing age: for ages 6, 12, 18, and 24 months, the corrected results corresponded to delta-over-baseline cut-off values of 9.5, 7.3, 6.5, and 6.0
, respectively. Among subjects within 1 month of those ages, we had 120 positive and 781 negative corrected results, with only four results, at varied ages, that did not correspond to these age-specific cut-off values, though all were very close. Hence, it appears that the correction classifies as positive those with a high probability of being truly positive. Therefore, the specificity of this method is likely to be near perfect. The degree of sensitivity is less certain, but this limitation cannot be avoided because no other detection method has revealed greater accuracy for detecting H. pylori infection in this age group.
Given that H. pylori infection is frequently asymptomatic and not usually detected at onset, cases must be detected by screening. Because infection is not generally present at birth,6 we consider all children to be uninfected at birth. We define incident cases as those detected in children who screen positive the first time they are tested or after a previous negative test. Owing to the possibility that infections may come and go between intervals, we refer to the observable infection frequency as the frequency of detectable infection. For person-time calculations, the precise time of onset of incident cases must be estimated, given that our observations reveal only the interval during which onsets occur. We define time of onset as the mid-point of the interval since the previous negative test or, when the first test is positive, the mid-point of the interval between birth and the first test. To estimate the incidence rate, we counted in the numerator only the first positive breath test result and we estimated the person-time at risk by counting the time between birth and the estimated onset time of the first detectable infection. For children who missed visit 4 (target age 24 months) but had a breath test result beyond the time period of this analysis, our protocol used the subsequent test result to classify the subject's status through 24 months. Children who did not have an infection onset during the study period contributed 24 person-months at risk; if visit 4 took place after 24 months of age, no person-time beyond 24 months was counted. Stata 8.1 (Stata Corporation, College Station, TX) was used for statistical analyses.
The Pasitos Cohort Study was approved by the Committee for the Protection of Human Subjects of the University of Texas Health Science Center at Houston and internal review boards of the University of Texas at El Paso, the Texas Department of Health, and the Mexican Social Security Institute. Staff read parental permission forms to mothers in their preferred language (English or Spanish), and obtained signed consent for participation at the time of enrolment.
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Results |
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Of the 803 children enrolled prenatally, 472 returned for follow-up (details about cohort recruitment have been published).10 Those who returned for follow-up included notably higher proportions of girls, living in the US, in family-owned, uncrowded homes with telephones and better-educated mothers; however, they were similar to those without follow-up on the number of siblings, the father's presence in the home, and the family's residential stability (Table 1). Most families without telephones lived in Juarez and this may largely explain the poor follow-up there.
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The numbers of children returning at target ages of 6, 12, 18, and 24 months were 383, 347, 274, and 235, respectively. For visits 1, 2, 3, and 4, respectively, 90% of attendees were 5.0–7.9 months old (91% were <8.0 months), 92% were 11.0–13.9 months old (95% were <14.0 months), 90% were 17.0–19.9 months old (91% were <20.0 months), and 85% were 23.0–25.9 months old (92% were <26.0 months). Table 2 shows the follow-up patterns for target ages of 6–24 months; 140 children had all four follow-up exams, 124 had just three, 99 had just two, and 109 had just one. The factors associated with completing all four targeted exams were the same as those associated with not returning for any follow-up exams (Table 1).
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This analysis includes data from 468 children (467 of whom had one or more breath tests during the study period and one who had an initial breath test later and so provided information about infection status during the 0–24 month age period); four children who had follow-up visits either provided no breath sample or provided insufficient samples. Classifiable breath tests were available for 359 children at the 6-month visit, and 341, 269, and 215 children at target ages of 12, 18, and 24 months, respectively. Table 3 shows the age-specific prevalence, which was 7% at 6 months, doubled to 14% at 12 months and then increased gradually to 19% at 24 months.
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Table 4 shows the frequency of first detectable infections, of which there were 128 (27% of the 468 children) during the 2-year study period (three of these were detected at a visit subsequent to visit 4 but had an estimated onset before 24 months of age). Of these, the first positive result was detected at the 6-month visit in 30 children, at the 12-month visit in 46 children, at the 18-month visit in 26 children, and at the 24-month visit in 26 children. The total person-time at risk of a first detectable infection was 7742 person-months and the incidence rate of first detectable infection was 1.7% per month (95% confidence interval (CI) 1.4–2.0% per month). The rate per month was 1.1% during the interval from birth to 6 months, 2.1% from 6–12 months, 1.6% from 12–18 months, and 2.1% from 18–24 months. The average rate per month was 1.6% (95% CI 1.2–1.9%) during the first year and 1.8% (95% CI 1.4–2.4%) during the second year. Incidence rates were similar in children living on the US and Mexico sides of the border, as were the rates in boys and girls (Table 5). Among children who completed all four visits during the study period, rates were notably higher across all age intervals, except the first 6 months (Table 4). In this group, rates were similarly elevated on both sides of the border, though somewhat more in Juarez children; the excess, however, was restricted to boys, as the rate in girls did not vary across those with and without complete follow-up.
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Of the 125 children with one or more positive breath test results detected at visits 1–4, 99 had one positive result, 21 had two positive results, five had three positive results, and none were positive at all four visits. Table 6 shows the patterns of infection across target ages. Only 20 children had infections that persisted across more than one time point: 15 were positive at two consecutive visits and five were positive at three consecutive visits.
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Table 7 shows frequencies of spontaneous elimination, which could be estimated among children who tested positive and had a subsequent test. Of the 19 children who tested positive at visit 1 and were tested at visit 2, 15 (79%) were negative at visit 2; in all, of the 19 children who tested positive at visit 1 and were tested at any later visit, 18 (95%) subsequently tested negative. Of the 38 children who tested positive at visit 2 and were tested at visit 3, 26 (68%) were negative at visit 3. In all, 41 children who tested positive at visit 2 were tested at a later visit and 32 (78%) subsequently tested negative. Of the 24 children who tested positive at visit 3 and were tested at visit 4, 15 (63%) were negative at visit 4.
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Evidence of reinfection during the 2-year follow-up required a positive test at target ages of 6 or 12 months to allow sufficient follow-up. A total of 41 children who were positive at either visit 1 or visit 2 subsequently lost their infection, as documented by a negative test at a later exam, and 26 of these children were tested subsequently. Of these 26 children, five showed evidence of reinfection; thus the reinfection frequency was 19%.
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Discussion |
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In this cohort, H. pylori infection occurred with similar frequency among children on both sides of the Rio Grande, with incidence rates of the first detectable infection from birth to 24 months of age
20% per year in both sexes. These rates were 1% per month during the first 6 months of life and fluctuated 2% per month from 6 to 24 months of age. Most of the infections detected in this study did not persist from one 6-month follow-up exam to the next and 20% of the children who lost infections showed evidence of reinfection within the 2-year study period. Thus, although the age-specific prevalence increased little from 12 to 24 months, the group that tested positive at each target age included mostly different individuals; for this reason, estimates of incidence based solely on increases in age-specific prevalence would be grossly underestimated. Future analyses will aim to differentiate determinants of acquisition and persistence of H. pylori infection in early life. Studies such as ours were undertaken when it became clear that H. pylori infection is most dynamic early in life and that a complete description of its natural history required following children from birth. Since we began this study, evidence of the limitations of methods for accurately detecting H. pylori infection in young children has emerged. It has become clear that serology is particularly problematic because young children with this infection often do not have detectable antibodies.25,26 Stool antigen tests were introduced more recently, but there is little information specific to infants and toddlers on test accuracy,27 and the collection and proper handling of stool samples presents logistic challenges for population-based research.28 Some reports suggest that the urea breath test has reduced specificity in young children,18,19 although other reports show comparably good specificity in younger age groups.20,29–31 Complicating matters is the lack of a true gold standard for validating non-invasive diagnostic tests for H. pylori infection, because biopsy-based diagnosis, commonly used as a gold standard, may miss colonized areas of the stomach owing to the typical patchy distribution.32
Given that the corrected breath test values maximize specificity, the most likely impact of test error is that the infection frequencies are underestimated. Similarly, missing infections that resolve between examinations would underestimate infection frequencies. The higher infection rates observed in children with complete follow-up suggest that infections were indeed missed between visits, by showing that shorter screening intervals increase the probability of detecting H. pylori infection. An alternate explanation is that the compliant children had a higher risk of acquiring H. pylori infection. However, H. pylori infection risk factors were more common in children lost to follow-up. Further, it appears that the incidence rates in Juarez children and in boys were particularly underestimated given poorer compliance with follow-up and higher rates among those with complete follow-up. Thus the observed lack of difference in rates by sex and country may be due to selective loss-to-follow-up. Despite the limitations, our examination of patterns of infection in the same children over time illustrates the observable dynamics of H. pylori infection during the 0–24-month age period.
A thorough literature review identified 21 studies that used follow-up data to track H. pylori status in children over time. Of these studies, eight were conducted with other aims and used stored sera to track seroprevalence.33–40 Another 13 studies were prospective: six tracked antibody levels;41–46 five tracked active infection using the urea breath test;47–51 and two tracked infection using the stool antigen test.52,53 It is difficult to judge the success with follow-up of many of these studies, particularly the retrospective ones, because few present details regarding loss-to-follow-up. Of the prospective studies, the targeted follow-up duration was 1 year or less in seven studies and 2–2.5 years in six studies. Among these studies, the cohort sizes ranged from 48 to 347, the average being 135; just two followed >200 children, while seven followed fewer than 100. Of the nine prospective studies with information on mean follow-up, the average was 1.2 years (range 0.33–1.9 years).
Three reports presented information on acquisition and loss of active infection in early childhood;48,50,52 all three showed frequent acquisition and loss of infection, though rates varied widely. These studies had relatively small amounts of person-time from quite distinct community-based samples of children (Peruvian, Gambian, and German), so wide variation would be expected. It has been argued that observed loss of infection in such studies may be attributable to improved breath-test specificity as children get older rather than actual infection loss;27 however, one of these three studies used stool antigen testing,52 which does not appear vulnerable to reduced specificity at younger ages.27 Furthermore, we corrected breath test results for the age-related factors believed to influence test accuracy and still observed frequent loss of infection. Additionally, other studies show evidence of relatively frequent seroreversion as children get older.34–36,38,40
Of the 21 studies, six examined multiple potential determinants of childhood H. pylori infection.39,43,45,46,53,54 Just one of these studies, which followed 50 Canadian First Nations children, tracked active infection rather than antibodies.53 None of the 21 studies attempted to distinguish factors that influence acquisition from those that determine persistence. It is apparent, then, that the Pasitos Cohort Study offers unique information for examining the natural history of H. pylori infection and (to be presented in future reports) factors that influence its acquisition and persistence.
The key finding, with implications for clinical, community health, and research settings, is that most detectable H. pylori infections in Pasitos Cohort children during the first 2 years of life did not persist. The evidence of frequent spontaneous elimination of H. pylori infection in this age group should be considered when designing research, interpreting data, or contemplating therapeutic interventions.
KEY MESSAGES
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Acknowledgments |
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The Pasitos Cohort Study is funded by the United States National Institute of Diabetes & Digestive & Kidney Diseases (grant R01-DK053664). The authors acknowledge the devoted effort of the Pasitos Cohort staff: Lupe Garcia, Flor Puentes, Patricia Juarez, Salina Torres, Julie Sanchez, and Cheryl Broussard and thank the reviewers for their constructive comments.
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