Abstract
Background:
Lead exposure from lead-glazed ceramics (LGCs) and traditional folk remedies have been identified as significant sources of elevated blood lead levels in Mexico and the United States. This study took place from 2005 to 2012 in a rural community in Baja California, Mexico.
Objectives:
1) Investigate the knowledge, attitudes, and practices related to lead and lead exposures from LGCs and two lead-based folk remedies (azarcon and greta); and 2) evaluate a pilot intervention to provide alternative lead-safe cookware.
Methods:
A baseline household survey was conducted in 2005, followed by the pilot intervention in 2006, and follow-up surveys in 2007 and 2012. For the pilot intervention, families who reported using LGCs were given lead-safe alternative cookware to try and its acceptance was evaluated in the following year.
Results:
The community was mostly of indigenous background from Oaxaca and a high proportion of households had young children. In 2006, all participants using traditional ceramic ware at the time (n = 48) accepted lead-safe alternative cookware to try, and 97% reported that they were willing to exchange traditional ceramic ware for lead-safe alternatives. The use of ceramic cookware decreased from over 90% during respondents’ childhood household use in Oaxaca to 47% in 2006 among households in Baja California, and further reduced to 16.8% in 2012. While empacho, a folk illness, was widely recognized as an intestinal disorder, there was almost universal unfamiliarity with the use and knowledge of azarcon and greta for its treatment.
Conclusion:
This pilot evaluation provides evidence 1) for an effective and innovative strategy to reduce lead exposure from LGCs and 2) of the feasibility of substituting lead-free alternative cookware for traditional ceramic ware in a rural indigenous community, when delivered in a culturally appropriate manner with health education. This strategy could complement other approaches to reduce exposure to lead from LGCs.
Introduction
Lead poisoning is a significant environmental hazard which is often insidious, with multi-organ involvement. Young children are most vulnerable, both due to their neuro-behavioral development and their increased likelihood of exposure, primarily through ingestion. Elevated blood lead levels (BLLs) in children have been associated with neurological harm, such as decrement of IQ performance, attention deficit hyperactivity disorder, hearing impairment, and impaired peripheral nerve function (1). Environmental exposures to lead remains a public health hazard of global dimensions. The most common environmental sources of lead include lead mining, smelting, battery factories, lead-based paints, leaded petrol (in a few remaining countries), lead-glazed ceramics (LGCs), and lead-based traditional (folk) remedies (1–3). The frequency of specific sources varies by country and by regions within countries (2).
Background
LGCs and lead-based folk medicines have more widespread use in less-developed countries, but have also been reported as atypical lead poisoning sources in more developed ones, affecting primarily immigrant populations (4,5). In addition to Mexico, LGCs have been found to have been produced in many European and Asian countries (6), and lead-based remedies have been found in India, Middle Eastern countries, and West Asian countries (7). Lead glazes have been used for pottery manufacturing for centuries (8). When the leaded glaze has been improperly prepared, applied, or fired, it can release large amounts of lead into food that has been cooked or stored in it (8–10). Lead in ceramic glaze can also leach into stored beverages, especially acidic juices. Although the amount of lead that might be ingested after leaching into food may generally be small, the regular use of these dishes can produce a steady dose of lead that can accumulate in the body and lead to lead poisoning (11). There is no evidence of reduced lead exposure over time, especially because pottery that has chipped or cracked can accelerate the leeching process (12–16).
In Mexico, multiple studies, as early as 1878 (17), have identified the production (18,19) and use (20–24) of LGC cookware as a major determinant of BLLs among women and children. National laws have been passed to limit the legal levels of lead in commercial products (25). Additionally, governmental agencies have collaborated with private organizations to pursue research and outreach to expand the number of lead-safe producers and retailers (26).
Though most of Mexico’s ceramic ware is industrially produced and safe, there is a sector of the market provided for by small-scale family-operated businesses. These producers cannot afford industrial-type kilns and instead use lead-based glazes, which allow the cookware to be fired and cured at much lower temperatures, enhancing the ceramic appearance, and, consequently, its marketability. Regions of Oaxaca, Mexico City, and Guadalajara are major producers of LGCs (10,20).
Two lead-based folk remedies, azarcon and greta, have been reported to be used in certain regions of Mexico to treat empacho, a folk illness not recognized by the biomedical system, but commonly recognized throughout Latin America and Mexican American communities in the United States (25,26). Empacho is commonly believed to be an intestinal malady caused by eating improperly cooked foods. The most frequently reported symptoms are gastrointestinal bloating, constipation, indigestion, diarrhea, vomiting, and lethargy (27). Azarcon (lead tetroxide) and greta (lead oxide) are both colorful powders that may contain up to 90% pure lead (27,28).
There is limited current published literature on the risk awareness and frequency use of LGCs and traditional folk remedies in Mexico. The main objectives of this study were to: 1) investigate the knowledge, attitudes, and practices related to lead and lead exposures from LGCs and two lead-based folk remedies (azarcon and greta); and 2) evaluate a pilot intervention to provide alternative cookware in a community in Mexico.
Methods
This study is part of an ongoing collaboration between San Diego State University (SDSU), University of California San Diego (UCSD), and the Universidad Autónoma de Baja California (UABC) in Mexico. Since 1998, faculty, students, and volunteers from both countries travel to underserved communities in Baja California twice a year, for three days, to provide health care services, health education, and conduct community-based research.
The study took place in Colonia Lomas de San Ramón, a rural farming community with an established history of successful collaboration with the Viajes Interinstitucional de Integración Docente, Asistencial y de Investigación (VIIDAI) project. The community’s indigenous background makes it an ideal setting to study LGC use and lead-based traditional medicines. The community is located in San Quintín, Baja California, about 200 miles south of the US–Mexico border, with approximately 3500 residents. Data were collected during four three-day periods in 2005, 2006, 2007, and 2012. In 2005, all community households were mapped and a systematic random sample of households was selected for a socio-demographic survey. For a total population of 671 inhabited households (29), with 95% confidence level, 80% power, confidence limits of ±5%, and an estimated 50% prevalence use of LGCs, we needed to survey 132 households. In order to ensure the validity and reliability of the survey instruments the surveys were pilot tested with community leaders, and during each visit indigenous language translators were available if needed. Each year, 7–9 teams of 2–3 interviewers conducted the surveys. In 2006, all participating households from 2005 were revisited to collect information on knowledge, attitudes, and practices related to lead, ceramic ware, and folk remedies. The survey included pictures of different types of traditional ceramic ware (for cooking or storing food) and of lead-based folk remedies. Those who reported using ceramic ware at that time were offered to choose one lead-safe cookware alternative: a lead-safe ceramic olla (bean pot) or cazuela (casserole dish), or a stainless steel pot of varying sizes. After the interview, materials conveying lead risk and source information through pictures were provided to all participants.
In 2007, all the households that were given lead-safe cookware were revisited to assess their level of acceptance of the new cookware. Each survey year, selected households were visited up to three times (at different hours and days) to attempt completion of the interview. In 2012, a question on the use of ceramic cookware was included in a systematic random sample anemia survey of the whole community.
In-person interviews (30–40 minutes long) in Spanish were administered to the adult (18 years or older) caregiver at the household, usually the mother. In one case, where a respondent was unable to or uncomfortable about conversing in Spanish, indigenous language translators were available, provided by the community. Prior to the interviews, all participants provided informed consent. Participants were presented with incentives of educational materials and household products of minimal value upon conclusion of the interview. All project activities were approved beforehand by community leaders. The study was approved by the Institutional Review Boards at SDSU and UABC. Responses were coded and analysis using descriptive statistics was performed using SAS 9.3 (SAS Institute, Cary, NC).
Results
Socio-demographic characteristics
In 2005, 134 questionnaires were administered at systematically selected households. Socio-demographic characteristics of the participants are reported in Table 1. The mean length of time living in the colonia was 92 months and in many households (41%) one or more household members had traveled to the United States in the previous five years to live or work. Twenty-seven percent of the respondents had no formal education and 46% had not completed primary education.
Socio-demographic characteristics of respondents and households: Colonia Lomas San Ramon, Mexico, 2005 (N = 134).
Participants could choose more than one language.
Most (87%) respondents were females and 72% were born in Oaxaca, followed by Baja California (7%), Guerrero (6%), and other Mexican States (15%). Sixty-two percent reported an indigenous background. Forty-nine percent were illiterate or had difficulty reading, and 21% of households had at least one child under six years old. Seventy-nine percent of households spoke Spanish at home, 22% Mixteco, 10% Triqui, and 1% spoke another indigenous language.
In 2006, 103 (77%) of the 2005 participating households were available for a second interview. Most common reasons for nonresponse included address not found (29%), a vacant home (19%), respondent moved (19%), or respondent not at home (13%); only one household refused to participate. Ninety-one percent (n = 93) of respondents grew up in a household that used ceramic ware for cooking, serving, or storing food when they were children, and 9% of respondents had a member of their household that worked in a ceramics manufacturing trade. Seventy-two percent of respondents were aware that lead could cause disease and 66% knew that some ceramic ware contained lead. Forty-seven percent of the households currently used ceramic ware for cooking and 33% used ceramics for storing or serving foods.
Use and beliefs of ceramic ware
Of those currently using ceramic ware in 2006 (Table 2), most (63%) had used it within the last week and 41% had been using it for over 10 years. No significant differences were found in ceramic use by knowledge of the potential for lead in ceramics causing disease (p = 0.56), or by years living in the community (p = 0.59). Out of the 48 households using ceramics, 40% believed their household ceramic ware contained lead, and the remaining households responded “no” or “do not know”. All respondents who reported using ceramic ware were offered, and all accepted, to try alternative lead-safe cookware. Sixty-seven percent chose a stainless steel pot and 33% choose a lead-safe ceramic pot or dish.
Use of and beliefs about ceramic ware among community members using ceramic ware: Colonia Lomas San Ramon, Mexico, 2006 (N = 48).
Respondents can reply using more than one type.
Mug (3), plate (2), mortar and pestle (2), and pan (2).
Lead-safe cookware intervention evaluation
In 2007, 34 of the 48 (74%) households that had accepted an alternate lead-safe cookware in 2006 were available for the interview. Non-participation was mostly due to the respondent not being home at the time of the visits; there were no refusals. Table 3 describes the alternative lead-safe cookware intervention evaluation. In 2007, of those that had received lead-safe cookware, 58% reported having used it at least one time in the last week. A similar percentage (57%) also continued to use their old ceramic ware at least once in the last week. Most (97%) respondents were willing to give up or trade their old ceramic ware for a lead-safe alternative. Overall (96%), food taste (76%), and heating (92%) satisfaction on the new lead-safe cookware was reported. The remaining responses were either neutral or missing. In 2012, of 149 participating households, 16.8% reported using ceramic cookware.
Lead-safe cookware intervention evaluation: Colonia Lomas San Ramon, Mexico, 2007 (N = 34).
Knowledge and use of lead-based folk remedies
The community’s knowledge and practices related to empacho and use of lead-based folk remedies in 2006 are presented in Table 4. Of the 103 respondents, 75% knew of empacho and described it universally as an intestinal or stomach illness. Thirty percent reported having had a case of empacho in their house in the last year, with the majority (71%) of cases being in children under 10 years or younger. None of the households had reportedly used azarcon or greta to treat empacho. In fact, almost none of the respondents recognized these remedies by name or picture.
Knowledge and use of lead-based folk remedies for empacho: Colonia Lomas San Ramon, Mexico, 2006 (N = 103).
All respondents described empacho as an intestinal or stomach illness.
Asked only to those who knew what empacho was.
One family had two cases of empacho in the last 12 months.
Asked only of respondents who reported empacho in their house in the last 12 months (N = 23).
Discussion
Baja California is a major migration destination from other Mexican states, primarily Oaxaca, a traditional ceramic-ware-producing region. Although most households in our study appear to have settled in the community, the region is also an intermediate migration stage to the United States for some household members. Most community members are of indigenous background from Oaxaca, community members are young, and a high proportion of households have young children, therefore, especially susceptible to lead poisoning.
The results of this alternate lead-safe cookware intervention pilot provides initial evidence for an effective and innovative strategy to reduce lead exposure from LGCs. The design of the pilot intervention was sensitive to the profound cultural bonds the community had to using traditional ceramic ware. For that reason, instead of trying to remove their current ceramic ware we decided to explore their acceptance of a lead-safe alternative. The community was not only willing to use alternate lead-safe cookware, but also willing to exchange their LGCs. To the best of the authors’ knowledge, this is the first published evaluation of a ceramic ware exchange strategy for lead poisoning prevention. This strategy could be used to complement other approaches to reduce exposure to lead from LGCs.
Our study found an almost 50% decrease in the use of ceramic ware between participants’ household use at childhood and use in 2006 as adults in Baja California, and an approximately 90% decrease in 2012. In addition to this project’s pilot intervention and education activities, this decrease might also be associated with better economic status and availability of modern cookware by the community in Baja California or a loss of traditions from their region of origin, among other reasons. Although the majority in the community was aware of the dangers of lead and the exposure from ceramic ware, many were not. Secondary analysis showed no significant differences in awareness of the dangers of lead from ceramic ware between those who did and did not report using it. Resistance to cooking with lead-safe alternative cookware may persist beyond education and knowledge of dangers, due to cultural bonds or cooking preferences (such as flavor or heating) associated with LGCs. Therefore, there is a need for expanded community education on this topic.
Since the 1990s the Mexican government has been developing programs to eliminate the use of lead-based glazes among traditional ceramists, including pioneering work in developing lead-safe glaze alternatives, but with limited success to date. In Mexico, the use of greta (or lead oxide) by ceramicists is regulated by law and pottery containing certain levels (>1–2 mg/L) of soluble lead should be labeled ‘not for human use’ or perforated to prevent it from being used in food preparation (29). However, this regulation is rarely enforced and greta remains widely available to artisans (30). Of an estimated 50,000 traditional ceramicists in Mexico, less than 3% use lead-safe glazes (31). In addition to higher costs associated with lead-safe glazes, several factors can be attributed to the limited success. Among the ceramic cookware producers there is limited awareness, scarce availability, and lead-safe glazes require more expensive kilns that can fire at much higher temperatures than those available to artisans. Recent efforts have focused on the development of a safe low-temperature ceramic flux, with some reportedly initial success (30).
In addition to Mexico, LGCs are still widely available in several Latin American and Caribbean countries, the Middle East, North Africa, China, Europe, and other regions (32–34). Lead poisoning from LGCs has also been reported in Europe (35) and in the United States among immigrant communities (4,5,36–38). This may be due to exposure to LGCs while in their country of origin and/or continued use of LGCs after migration. For that reason, it is important that immigrant populations are targeted for lead prevention and education outreach.
Cases of child lead poisoning associated with azarcon and greta have been reported in Mexico (39), but most published reports have come from the United States, mostly among Hispanic Mexican populations (27,28,40–43). In the United States, traditional folk remedies from Mexico and other countries have been described as the most common atypical (i.e. not from lead-based paint ingestion, exposure to leaded gasoline, lead-soldered pipes, or occupational exposure) source of childhood lead poisoning in the country (44).
The lack of awareness and use of azarcon and greta in the community may be an indication of regional variation in the use of these products across Mexico. Available data on the use of lead-based folk remedies in Mexico and the United States is mostly based on case reports and decades-old surveys in limited geographic areas. Trotter reported that there is also a considerable variation in the remedies to treat empacho, but it is most commonly treated with massage or with herbal teas, like in our study community (27). In the first published population-based study in Mexico, Baer et al. (1998) found that 71% of households in Guadalajara have treated empacho and 16% had used a lead-based remedy (26). A previous study showed that the risk from use of lead-based remedies was lower in indigenous Oaxaca (5%) compared to mestizo Guadalajara (35%) (25). The authors are not aware of more current published studies. Though respondents may be reluctant to admit using these folk remedies (40) or fail to mention them (27), one study reported that approximately 10% of Hispanic families treating empacho use greta or azarcon in some US neighborhoods (27,40) reserving its use for the most serious cases of empacho (25). Much remains to be known about the current prevalence and risk factors for the use of lead-based folk remedies, which are generally considered a frequent source of lead poising in Mexico and among Mexican communities in the United States.
Though the outcomes of the study indicate that the risks of lead exposure due to LGCs persist in the community and suggest a successful intervention strategy, interpretation of the results should be cautious of the fact that this study was limited to one small community and the sample size was constrained to the three days of data collection during each trip to the community. Thus, results may not be generalizable beyond other similar communities in the region, given the extreme ethnic and cultural diversity in Mexico (45). On the other hand, the trust built between the project and the community by ensuring the support from community leaders and through years of providing health care, and other interventions to improve the lives of residents, give us some assurance that the information provided by participants accurately reflects the reality in the community. Our investigation did not confirm that the ceramic ware used in the community was lead glazed, though because of the traditional use of LGCs and the limited availability of lead-safe ceramic cookware in the area, we assumed it was LGCs. This pilot intervention likely could have been improved by directly observing the use of the lead-safe alternate cookware and surveying lead-safe cookware preferences (size and material) that maximize their adoption. Unfortunately, this would have increased the duration of the interview, decreasing our sample size, and required entry into the participants’ house, which may have been considered culturally inappropriate in the community.
Conclusion
Future larger representative studies are needed in different areas of Mexico, and among Mexican immigrants in the United States, to assess the risk of exposure from LGCs and folk remedies. Our successful pilot intervention offers guidance on a feasible strategy that substitutes lead-safe alternative cookware for traditional LGCs in a culturally appropriate manner. For LGCs, it is important that any potential interventions acknowledge and respect the cultural and economic value of traditional ceramics for this community. A major challenge to the adoption of lead-safe cookware that needs to be considered is the lower cost of traditional leaded ceramic ware compared to lead-safe products. In addition to expanded community education, a continuing focus on the development and adoption strategies of sustainable lead-safe ceramic-ware production alternatives for traditional artisans is also recommended.
Footnotes
Acknowledgements
We would like to thank the community members in Colonia Lomas de San Ramón who were integral to this project and the overall success of the VIIDAI project. We would also like to thank Rotary International, the medical students at UCSD and UABC, and the public health students at SDSU.
Conflict of interest
None declared.
Funding
This research received no specific grant from any funding agency in the public, commercial, or not-for-profit sectors.
