© 2007 American Public Health Association DOI: 10.2105/AJPH.2005.074138
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).
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 ( 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
In the past 25 years, the United States and many other countries have witnessed dramatic decreases in environmental exposure to lead, largely resulting from environmental policies that mandated that lead be removed from gas, paint, and other manufactured products, and through the modification of mining and other extraction processes.14 The success of these programs is evidenced by studies that have reported substantial declines in blood lead levels (BLLs) in population samples of children in the United States over the past 10 years.5 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.78 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
In 2000, one of the community doctors (E. S.) affiliated with the Department of Family and Community Medicine at the University of California, San Francisco, asked for help in investigating a large number of lead poisoning cases where he worked. The clinic, in Seaside, Calif, is one of Monterey County Health Departments 3 community-based primary care clinics. There were no epidemiological data from the County or State Health Department that could answer the questions of the doctor and nurse at the Seaside clinic who were seeing "way too many cases of lead poisoning" among their patients who were from Oaxaca. Although there had been prior lead case investigations conducted by the Monterey County Health Department, the more common sources of lead exposure in California, such as lead-contaminated water from old pipes, peeling lead-based paint, lead-contaminated soil, occupational sources, lead-glazed ceramics, or home health remedies containing lead, had not been identified in the majority of these investigations (Donna Staunton, Public Health Nurse, written communication, May 2005).
We used epidemiological methods common in outbreak investigations, which incorporated casecontrol and cohort designs. Qualitative methods, including focus groups, were used to complement and inform the epidemiological findings.9,10 Initial steps focused on estimating the prevalence of elevated BLLs among children screened for lead in Monterey County Health Department Primary Care Clinics, including the clinic in Seaside and 2 others in the neighboring communities of Salinas and Marina. A casecontrol study in Seaside to determine if pediatric lead cases were concentrated among the families from Oaxaca, Mexico, followed. Focus groups with families of lead-poisoned children, Oaxacan community healers (curanderas), and pregnant women with elevated BLLs were then conducted in Seaside, to better understand community perceptions about lead poisoning and to inform the next study design. The next study examined risk factors for lead among pregnant women who entered care at 2 of the primary care clinics in Monterey County that saw the majority of prenatal patients in the clinic system. 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
CaseControl Study Examining Risk Factors in Seaside
Prenatal Lead Testing and Assessment of Risk Factors 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.1416
Prevalence of Elevated Blood Lead Levels For children tested between January 1997 and June 2001, with 1 observation per child per year, the prevalence of elevated BLLs at Seaside was 3 times that of the clinics in Salinas and Marina (6.0% compared with 1.7% each) and significantly higher than population-based estimates in the United States over the same period (2.2%).5 Seaside accounted for 47% of pediatric lead tests but 80% of the pediatric lead cases in Monterey County. Lead screening rates for children in this target age group exceeded 97% in each of the 3 clinics.13 These findings suggested that the lead problem in Monterey County was concentrated in Seaside, so the investigation was focused there.
CaseControl Study Examining Risk Factors in Seaside
Prenatal Testing and Assessment of Risk Factors A total of 214 women enrolled in the study between November 2002 and August 2003. All women approached for the study participated. The study population was almost entirely Latina (95%) and born in Mexico (87%). Sixty-six women were from the state of Oaxaca: 32 were from the Zimatlan area (12 from Santa Ynez Yatzeche, 15 from San Pablo Huixtepec, and 5 from Zimatlan) in the western central valley of Oaxaca, and 34 were from towns in the eastern central valley or from the Pacific coast of Oaxaca. These 2 areas of Oaxaca represent culturally distinct communitiesthe Zimatlan-area Oaxacans are Zapotecans, and the Oaxacans from the eastern valley are primarily Miztecans.7
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
Women with elevated BLLs were not significantly more likely than women with normal BLLs to be younger, more recently arrived immigrants (immigration within 1 year compared with more than 1 year or 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
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
We found a significant public health problem of lead poisoning among a group of immigrants who have come to Seaside, Calif, from Oaxaca, Mexico. The high prevalence of elevated BLLs in both children and pregnant women over several years, as well as the association between elevated BLLs and at least 1 food that is widely eaten within this community, suggests an even greater problem among the Oaxacan community in Seaside, and possibly among other communities that have not yet been identified. The majority of Oaxacans who live in Seaside are from indigenous Zapotecan communities that are distinct from other Oaxacans who live in Monterey County, and it is possible that they may have unique sources of lead exposure that have not been determined. The fact that reports of eating imported foods, including tortillas (with a RR higher than 9), were associated with elevated BLLs among prenatal patients needs to be substantiated with wider testing of imported foods. That several chapulin samples obtained in Seaside and in Zimatlan contained high levels of lead suggests that the home community in Oaxaca has significant ongoing lead exposure. There have been no studies of this area to date to determine the extent of lead poisoning or to pinpoint the lead sources so that widespread lead poisoning can be prevented. 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.2021 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.
The authors were supported by grants from the University of California Institute for Mexico and the United States, the Monterey Commission on Families and Children, the California Academy of Family Physicians, and la Universidad Nacional Autonoma de Mexico (grant UNAM-PAPIIT 0113905). 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 MexicoBelen 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
Peer Reviewed
Contributors Accepted for publication December 20, 2005.
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