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RESEARCH AND PRACTICE |
At the time of the study, Margaret A. Handley, Kaitie Drace, Robert Wilson, and Mary Croughan were with the Department of Family Medicine and Community Medicine, University of California, San Francisco. Celeste Hall and Evie Diaz were with the Monterey County Health Department, Salinas, Calif, and the Department of Family and Community Medicine, University of California, San Francisco. Eric Sanford was with the Monterey County Health Department, Salinas, and the Department of Family Medicine Collaborative Research Network, University of California, San Francisco. Enrique Gonzalez-Mendez was with the Southwest Community Health Clinic in Sonoma County, Santa Rosa, Calif, and the Department of Family Medicine Collaborative Research Network, University of California, San Francisco. Mario Villalobos was with la Universidad Nacional Autonoma de Mexico, Mexico City.
Correspondence: Requests for reprints should be sent to Margaret A. Handley, PhD, Assistant Professor, Department of Family and Community Medicine, University of California, San Francisco, San Francisco General Hospital, 995 Potrero Ave, Ward 83, San Francisco, CA 94110 (e-mail: handleym{at}fcm.ucsf.edu).
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ABSTRACT |
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Objectives. Although the burden of lead poisoning has decreased across developed countries, it remains the most prevalent environmental poison worldwide. Our objective was to investigate the sources of an outbreak of lead poisoning in Monterey County, California.
Methods. An investigation in 3 county health department clinics in Monterey County, California, was conducted between 2001 and 2003 to identify risk factors for elevated blood lead levels (
10 µg/dL) among children and pregnant women.
Results. The prevalence of elevated blood lead levels was significantly higher in 1 of the 3 clinics (6% among screened children and 13% among prenatal patients). Risk factors included eating imported foods (relative risk [RR]=3.4; 95% confidence interval [CI]=1.2, 9.5) and having originated from the Zimatlan area of Oaxaca, Mexico, compared with other areas of Oaxaca (RR=4.0; 95% CI=1.7, 9.5). Home-prepared dried grasshoppers (chapulines) sent from Oaxaca were found to contain significant amounts of lead.
Conclusions. Consumption of foods imported from Oaxaca was identified as a risk factor for elevated blood lead levels in Monterey County, California. Lead-contaminated imported chapulines were identified as 1 source of lead poisoning, although other sources may also contribute to the observed findings. Food transport between binational communities presents a unique risk for the importation
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONReferences |
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Despite these gains, lead exposure continues to be one of the most prevalent and harmful sources of environmental poisoning in much of the world. Recent estimates by the World Health Organization indicate that the percentage of children aged younger than 6 years with elevated BLLs, defined as 10 or more micrograms of lead per deciliter of blood [µg/dL],4,6 is well over 20% in several regions, including Latin America.4 The World Health Organization emphasizes that the risk of lead toxicity remains as high as in previous centuries for children in many countries. The insidious attack of lead on the developing nervous system significantly limits the ability of children worldwide to climb out of the poverty in which so many grow up.
Globalization and the regular transnational movement of capital, goods, and people allow migrants to maintain strong ties with their communities of origin. In California, thousands of migrants travel back and forth to small communities in Mexico and other parts of Latin America. This connectedness enables families to communicate regularly, eat and transport foods prepared in their hometowns, and preserve language and customs while living in separate countries, all of which creates binational communities.7–8 Unfortunately, the same conditions that allow for strong cultural ties to be maintained over vast distances can also lead to the importation of environmental hazards. We investigated an outbreak of lead poisoning in Monterey County, California, in which a localized problem of lead poisoning was found to be associated with contaminated imported foods among community residents from the southern Mexican state of Oaxaca (Figure 1
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METHODS |
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Food testing was conducted by West Coast Analytic Service, the State of California Food and Drug Administration (State of California, Food and Drug Administration 2003; sample 030675), and by M. V.
Screening Children for Lead in Monterey County
We analyzed laboratory data for children aged from birth to 6 years to estimate the prevalence of elevated BLLs among screened children. State and county policies require all children to be screened for lead at 12 and 36 months (with all children to be screened at least once by age 72 months), in accordance with California’s Child Health and Disability Prevention Program guidelines.6,11 Children are tested for lead through either a venous or capillary blood sample.12
Case–Control Study Examining Risk Factors in Seaside
We reviewed charts of pediatric elevated BLL cases and a sample of controls (with BLLs < 10 µg/dL) identified from the laboratory database as Seaside clinic patients screened between January 1997 and June 2001. Abstracted information included sex, race/ethnicity, birthplace, BLL, and answers to lead-risk screening questions. We matched subjects on age at first lead screening (3 groups: 0 to < 1 years; 1 to 
3 years; and 4 to 6 years) to remove the possible confounding for children who were tested outside the 12- to 36-month screening window. We also abstracted prenatal and primary care charts of mothers of cases and controls to determine whether children were either born in or had families from Oaxaca, Mexico.
Prenatal Lead Testing and Assessment of Risk Factors
In August 2002 the Monterey County Health Department Clinics instituted a policy of prenatal blood lead testing during the routine prenatal testing done at the first visit. Between November 2002 and August 2003, a subset of the women at the Seaside and Salinas clinics who were screened for lead was also interviewed about risk factors for lead poisoning. Together, these clinics saw more than 95% of all prenatal patients who attended county clinics for prenatal care. Women were asked during a routine visit with a trained comprehensive perinatal services coordinator if they were interested in the study, and those who gave written informed consent were interviewed about risk factors for lead poisoning. Women approached for the study were those who could return for a scheduled visit. All women who received the lead testing were counseled about their test result and given prevention education that was tailored to their literacy and language background. Risk factors included area of birth, consumption of imported foods, use of lead-glazed ceramics, and occupational and environmental exposures to lead. Because we were interested in examining whether women from different areas of Oaxaca had different risk profiles for elevated BLLs, we examined as risk factors both town of birth and the town where the family of the woman or her partner lived.
We next began a prospective investigation of women receiving prenatal care. We believed that if we found a similar prevalence of elevated BLLs and similar risk factors, we would be able to identify some of the potentially preventable exposures occurring in this community. Also, because we were beginning to suspect a food-borne source of lead, we wanted to understand food preparation and importation practices to better develop lead poisoning prevention messages.14–16
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RESULTS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONReferences |
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Case–Control Study Examining Risk Factors in Seaside
The results of the case–control analysis are summarized in Table 1. More than 70% (90/126) of pediatric cases were born in the United States, although the majority of cases born in Mexico were from Oaxaca. Almost all cases (95%) were Latino, compared with 70% of controls. Close to 40% of cases had chart documentation of 1 or more venous-confirmed BLLs equal or greater than 20 µg/dL. We believed that the high proportion of pediatric cases with a BLL of 20 µg/dL or higher suggested an acute exposure, which was consistent with our understanding of the unique foods and importation practices that were taking place between vendors from Seaside and family members living in Oaxaca.
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The prevalence of elevated BLLs in the pre-natal patients study population was 12%; 18% of the women screened in Seaside and 1% of the women screened in Salinas had elevated BLLs. Table 2 presents demographic and risk factor characteristics of women in the study, by BLL, and associated relative risk (RR) estimates and 95% confidence intervals (CI). Women with elevated BLLs were more likely to be Oaxacan born (96%) (compared with women born elsewhere in Mexico) and from Seaside (96%); more likely to eat imported foods from Mexico, including foods produced locally or home-grown by family members, such as pumpkin seeds, tortillas, chocolate, and chapulines (home-prepared dried grasshoppers; 84%); and more likely to report having a friend or relative "with lead in their blood" (28%). In an analysis restricted to the 66 women from Oaxaca, the RR for women born in the Zimatlan area compared with other areas of Oaxaca was 4.0 (95% CI=1.7, 9.5). Women from the Zimatlan area reported similar patterns of imported food consumption as women from other areas of Oaxaca.
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5 years compared with 6 or more years), prepare food in lead-glazed ceramics or to have used lead-glazed ceramics growing up, live in older housing, live in remodeled houses, live with someone who uses lead in their job, or to have been out of the United States in the previous year. In an analysis restricted to the 54 Oaxacan-born women screened at Seaside, almost half (n = 23; 44%) had elevated BLLs. Among Oaxacan-born women, women from the Zimatlan area were more likely to have elevated BLLs than women from other parts of Oaxaca. Nineteen of the 32 Zimatlan-born women had elevated BLLs (59%), compared with 4 of the 22 women (18%) from other areas of Oaxaca screened at the Seaside clinic (RR = 3.3; 95% CI = 1.3, 8.3). By comparison, the prevalence of elevated BLLs among women from other parts of Mexico who participated in the study and were screened at Seaside was less than 1% (1/161)—this woman reported that she was not born in Oaxaca but that her family lived in Zimatlan. In Salinas, no women screened for lead were from Zimatlan, but the 1 woman with an elevated BLL was from another area of Oaxaca.
In the 6 months after the introduction of prenatal lead testing by the county health department, we estimated the prevalence of elevated BLLs among all new prenatal patients seen in the Salinas and Seaside clinics. This was done to determine how representative the subset of interviewed study participants was of all women entering care in the clinics during this period. Between August 2003 and February 2004, we conducted a chart review of all women who entered prenatal care at these 2 clinics. Demographic information, including birthplace and lead test results, were abstracted for 420 of the 450 women (93%) entering prenatal care. In this sample, 402 women had complete lead test results and demographic data. The prevalence of elevated BLLs was 13% in Seaside and 0% in Salinas. All 27 cases were from Oaxaca, although the town or area of origin was not recorded in the charts. Women in the chart review study were similar to women in the interview study with regard to age, ethnicity, and time in the United States.
Confirmation of Food-Borne Lead Contamination
In September 2003, a 2-year-old boy screened as part of his Child Health and Disability Prevention Program visit in Seaside had a BLL of 36 µg/dL, after having a much lower lead test result the preceding November (4 µg/dL). The child was born in the United States, but his parents had previously immigrated from San Pablo Huixtepec in Oaxaca. The child’s mother provided samples of foods received from her family in Oaxaca for testing. Tortillas and a bag of chapulines that she had received 2 weeks previously, through an importer that relayed foods directly from families living in Oaxaca to families in Seaside, were tested. The mother reported that the child had consumed about a small baby food jar’s worth of chapulines in the previous few days (about 4 ounces). Food analyses indicated that the chapulines contained 2300 ppm of lead, and the tortillas contained less than 0.1 ppm. The mother was counseled to remove the food source, and a state-wide health alert was issued by the California Department of Health Services with regard to imported chapulines.17 The investigation of the child’s home by the Monterey County Childhood Lead Prevention Program did not find common lead-containing sources such as home health remedies, lead-glazed pottery, or food sources known to have lead such as tamarind candy (Donna Staunton, Public Health Nurse, written communication, May 2005).
Between August 2003 and June 2005 we collected and tested several samples of chapulines obtained from vendors in Seaside who reported that the samples were from Zimatlan, from vendors in the marketplace in Zimatlan, and from fields in the Zimatlan area (Table 3). Products were not labeled and had no indication that they were produced commercially. Several chapulin samples had extremely high amounts of lead. Additional chapulin samples that were boiled but not seasoned contained 580 ppm and 3 ppm of lead. Eating foods with lead levels like these would result in daily intake levels that exceeded the Food and Drug Administration’s provisional tolerable intake level for children of 6 µg of lead per day by many orders of magnitude (based on an estimate of 5 to 15 ounces consumed daily).18 Additional samples of pumpkin seeds and tortillas had no detectable lead (less than 1 ppm), and 1 sample of mole (a prepared and condensed sauce) contained 40 ppm.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONReferences |
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Although there is strong evidence that the origins of the elevated BLLs in Seaside are associated with lead contamination of food in Oaxaca, there are also 3 lines of evidence showing that the exposures are occurring in Seaside: (1) the high proportion of pediatric lead cases that were born in the United States (70%); (2) the data that indicate that recent immigration or recent travel outside the United States were not associated with elevated BLLs among prenatal women studied; and (3) the food test results (from foods obtained in Seaside) and the case report of the child who had an initially low BLL followed by an extremely high one after eating lead-contaminated foods in Seaside that were sent by his family in Oaxaca. We believe that the lead exposures in the Seaside community result from both ongoing exposures from imported foods that contain lead and from past exposures that may have resulted in the storage of lead in bone and other organs that is later released into the blood, including during pregnancy.19
That elevated BLLs were not strongly associated with current or past use of lead-glazed clay ceramics among prenatal patients is surprising because their use has been associated with higher mean BLLs in studies in Mexico.20–21 Our outbreak investigation was focused on risk factors for elevated BLL (rather than for mean BLL), which might partially account for this difference. However, our focus group interviews confirm that women do not widely use Mexican pottery in the United States, and our finding of past use of lead-glazed ceramics among women in our study is consistent with studies in Mexico.22
If lead-glazed ceramics had been a strong risk factor for elevated BLLs in the women in the prenatal study, it would have been likely to affect all Oaxacan-born women, rather than primarily those from the Zimatlan area. There is no known local production of lead-glazed ceramics in this area, with the majority of lead-glazed ceramics produced in eastern Oaxaca and distributed to other parts of Oaxaca and Mexico.23 Lead-glazed ceramics are available, however, in local markets in Monterey County and some women did report using them for preparing certain types of foods. We suspect that use of lead-glazed ceramics does contribute to the elevated BLLs in this population but that it is not the primary source of lead exposure. It is possible that lead-glazed ceramics are being used in Zimatlan in a manner that is increasing the amount of lead in food, and it is also possible that ingredients themselves are contaminated with lead, through food preparation practices (such as the drying of ingredients or grinding and milling practices).24
Environmental contamination is also a possible source of lead because the Zimatlan Valley has a history of silver mining,25 in which lead-contaminated mine tailings have been dispersed throughout the area. One study that examined soil, plant, and invertebrate samples in an area of Wales contaminated with mine tailings found similar lead levels in local species of grasshopper to those found in the chapulin samples collected in this study, which raises the possibility that lead could be bioaccumulated in locally harvested foods, including chapulines, in Oaxaca.26 These potential routes of exposure will be examined in future studies we are developing with relatives of case families in Zimatlan.
We are not aware of any studies that have previously identified an outbreak of lead poisoning from home-prepared and locally produced foods. Clearly, there is an extensive system of transporting foods between binational communities that remains outside the international surveillance systems designed to identify food contamination in imported products. These epidemiological findings highlight the importance of the collection of community-level data that is disaggregated both geographically and within ethnic groups,27,28 because without them, the elevated BLLs in Seaside among Oaxacans would have been diluted in county-level prevalence assessments. They also demonstrate the importance of community-oriented primary care that is engaged with binational communities,29,30 and of the increasing relevance of globalization in the examination of health outcomes. We were able to identify the lead problem in Seaside as a result of the insightfulness of the clinicians who noticed the cases with high lead levels and were aware of the binational nature of the lives of Oaxacans living in Monterey County. An understanding of the different indigenous groups, towns of origin, the fluidity of migration patterns, and of the importance of food importation in this community was critical to the development of the outbreak investigation. The problem of elevated BLLs in Monterey County reflects a binational problem. It is our hope that by determining the origins of the lead exposure in this community, many more cases of lead poisoning will be averted, both among migrant communities and among their communities of origin.
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Acknowledgments |
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We acknowledge the contributions of the Monterey County Health Department and the staff at Seaside Family Health Center, Alisal Health Center, and Marina Health Center, in Monterey County, Calif.
We also acknowledge the personal contributions of the following individuals: Susan McNelly, who at the time of the study was with the Monterey County Health Department; Dean Schillinger, University of California, San Francisco, Division of General Internal Medicine, San Francisco General Hospital; and Pilar Fernández-Lomelín from Laboratorio de Análisis Físicos y Químicos del Ambiente, Instituto de Geographia, for the digestions and analyses of samples and her guidance in the analytic work of the undergraduate chemistry students at la Universidad Nacional Autonoma de Mexico—Belen Ramírez, Pedro Bazán, and Claudia Merino; and Raul Aguirre Gomes, Instituto de Geographia.
Note. The findings and conclusions are those of the authors and do not necessarily represent the views of the funding agencies.
Human Participant Protection
This study was approved by the institutional review board at the University of California, San Francisco, and the Monterey County Division of Primary Care.
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Footnotes |
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Contributors
M. A. Handley originated the study, supervised all aspects of its implementation and data analysis, and led the writing. C. Hall and E. Sanford originated the study, conducted data collection, and provided writing support. E. Diaz and K. Drace conducted data collection. E. Gonzalez-Mendez and M. Croughan originated the study and provided writing support. R. Wilson conducted data analysis. M. Villalobos conducted sample analyses.
Accepted for publication December 20, 2005.
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References |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONReferences |
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19. Tellez-Rojo MM, Hernandez-Avila M, Lamadrid-Figueroa H, et al. Impact of bone lead and bone resorption on plasma and whole blood lead levels during pregnancy. Am J Epidemiol. 2004;160:668–678.
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