An assessment of lead leachability from lead-glazed ceramic cooking vessels.

Introduction

A number of efforts have been made by the U.S. government to reduce lead exposure in the environment such as the banning of lead in paint produced for residential uses in 1978 and the banning of lead additives in gasoline in 1986 (Centers for Disease Control and Prevention [CDC], 2003; Gavaghan, 2002); the Clean Air Act Amendments of 1990, which banned the sale of leaded gasoline (CDC, 2003); and the cessation of the use of lead-containing solders in food cans in 1991 (Farley, 1998). These efforts have been very successful in reducing the prevalence of elevated blood lead levels (BLLs) in the U.S. population, which dropped from 88.2 percent in the 1976-1980 NHANES survey to 2.2 percent in the 1999-2000 survey, although rates remained higher in blacks (8.7 percent) and Hispanics (5.6 percent) (Meyer et al., 2003). Data more recently gathered by CDC demonstrate that the prevalence of elevated BLLs had dropped to 1.59 percent by 2005 (CDC, 2007). Despite these regulatory successes and the accompanying reduction in the prevalence of childhood lead poisoning, lead poisoning remains a serious public health issue, with over 45,000 new cases occurring in 2005. Some specific populations, such as children living along the U.S./Mexico border, have particularly elevated BLLs (Cowan et al., 2006). It has been estimated that as many as 35 percent of elevated BLLs are associated with items made of lead or decorated with lead such as toys, eating/drinking utensils, cosmetics, and traditional medicines (CDC, 2005). The FDA Blue Book requires that nothing from food-contact articles should impart flavor, color, odor, toxicity or other undesirable characteristics to food (FDA, 2000c). It also notes that house-ware items are not exempt from FDAs general safety provisions and that regulatory action has been taken against ceramics containing leachable lead or cadmium.

Ceramic vessels are widely used as cookware in Hispanic communities in both the United States and Mexico. In Mexico, there is a centuries-old tradition of making and using low-temperature-fired lead-glazed ceramic (LGC) ware, which is primarily manufactured by small family businesses (Azcona, Rothenberg, Schnaas, Zamora, & Romero, 2000; Fernandez, Martinez, Fortoul, & Palazuelos, 1997; Flores & Albert, 2004; Johnson, 1997). Several epidemiologic studies have reported LGC as a risk factor for elevated BLLs and have quantified the use of LGC among study participants. The following levels of use have been reported:

* 69.7 percent (Hernandez-Avila, Romieu, Rios, Rivero, & Palazuelos, 1991);

* 64.8 percent (Lopez-Carillo et al., 1996);

* 67.2 percent (Olaiz et al., 1996);

* 74.3 percent (Fernandez et al., 1997);

* 50.0 percent (Brown et al., 2000);

* 40.5 percent (Lacasana, Romieu, Sanin, Palazuelos, & Hernandez-Avila, 2000);

* 67.8 percent (Cifuentes, Villaneuva, & Sanin, 2000);

* 38.2 percent (Hung-Yi et al., 2001);

* 39.9 percent (Schnaas et al., 2002); and

* 81.4 percent (Hernandez-Serrato et al., 2003).

The primary glaze used in the manufacture of these vessels is lead oxide (also known as greta), which is added as a flux to reduce firing temperatures and to add a shiny glaze (Tunstall & Amarasiriwardena, 2002). The vessels are fired at a temperature lower than is needed to permanently fix the lead to the pottery, which allows the lead to leach into foods cooked in the vessels. Increased food volume, which increases the size of the food contact surface; fluid temperatures; cooking times; and food acidity also influence lead leachate levels (Farley, 1998; Foulke, 1997; Hernandez et al., 1991; Johnson, 1997; Tunstall & Amarasiriwardena, 2002). Romieu and co-authors (1995) found that leachate from 84 percent of LGC vessels tested exceeded the Mexican standard of 7 mg/L. Several studies have shown a clear correlation between the use of lead-glazed ceramic ware for cooking or food preparation and elevated BLLs (Azcona et al., 2000; Brown et al., 2000; Cifuentes, et al., 2000; Fernandez et al., 1997; Gonzalez de Mejia & Craigmill, 1996; Hernandez-Serrato et al., 2006; Hemandez-Serrato et al., 2003; Hibbert, Bai, Navia, Kammen, & Zhang, 1999; Lacasana et al., 2000; Lopez-Carillo et al., 1996; Hung-Yi et al., 2001; Olaiz et al., 1996; Rojas-Lopez, Santos-Burgoa, Rios, Hernandez-Avila, & Romieu, 1994; Romieu et al., 1994; Rothenberg, Schnaas, Perroni, Hernandez, & Karchmer, 1998; Rothenberg, Schnaas, Perroni, Hernandez, & Flores-Ortega, 2000).

Recognizing that the use of LCG pottery is prominent in Hispanic families and is one of the major causes of lead poisoning, the Oklahoma Institute for Child Advocacy (OICA) and the Latino Community Development Agency (LCDA) conducted a Lead Poisoning Prevention Project (LPPP) that included addressing the dangers associated with cooking food in LGC. One part of their efforts consisted of a bean pot exchange targeting the Hispanic community in which LGC vessels were collected in exchange for stainless steel cookware. Between 2003 and 2005, over 150 ceramic items from the exchange events, including cups, serving dishes, and cookware, were collected and donated to the authors. Given what is generally known about the prevalence of LGC, we were confident that some of the locally collected vessels would contain lead. Our initial goal was to determine the prevalence of LGC among locally collected ceramic vessels that were used for preparation of food. In addition, we wanted to quantify the amount of lead present and to determine if the lead would leach into prepared foods commonly consumed by the Hispanic community.

Methods

A subset of the donated ceramic items was chosen for testing. We selected items according to the following criteria: large enough for cooking, fully intact, and showing evidence of prior use as cooking ware (e.g., scorch marks on the bottom). We also attempted to select vessels that were similar in size, shape, and color, although there was considerable variability among the 25 vessels that were selected for study. Each selected vessel was initially tested with a Niton Model 703A X-ray fluorescence (XRF) analyzer for determination of lead content. Reported values represent the mean of three consecutive readings.

We performed a 24-hour acetic-acid extraction assay on all vessels to test for lead leachate (FDA, 2000a). The FDA action level for leachate is 1.0 [micro]g/mL for one of six identical large (>1.0-L) ceramic hollowware items other than pitchers (FDA, 2000a, 2000b). Action levels represent a limit at or above which legal action, such as removal of products from the market, can be taken. Canned tomatoes (pH 4.1), canned black beans (pH 6.0), and canned yellow hominy (pH 6.3) were individually cooked in each of the 25 vessels. These foods were selected because they are commonly used ingredients and represent a pH range of many typically consumed foods. Two cans of food (900 mL) and 450 mL of reverse-osmosis-treated (RO) water were cooked in each vessel. Each vessel was heated to a boil for 5 minutes, during which it was covered with a glass lid to minimize evaporation. Uncooked food was tested to ensure that it did not contain lead before being cooked. After cooking, food samples were homogenized in a blender. Homogenate samples of 2 1/2 grams were placed in 50-mL plastic centrifuge tubes, to which was added 15 mL of RO water and 5 mL of trace metal grade nitric acid. Samples were subsequently digested in a laboratory microwave following manufacturer's recommendation. The samples were initially analyzed by the inductively coupled plasma atomic emission spectrometry (ICP) method with a detection limit of 0.020 mg/L. Samples in which lead levels were below the ICP limit of detection were analyzed by graphite furnace atomic absorption spectrophotometer (GFAA) for quantification of lead to a detection limit of 0.002 mg/L.

U.S. EPA's Continuing Survey of Food II (CSFII) Analysis of Food Intake Distributions was used to establish the average serving sizes of tomatoes, black beans, and hominy that children normally consume (U.S. EPA, 2003). Both per-consumer consumption and per-capita consumption values were used. We used per-consumer values to compare lead-in-food values to FDAs provisional tolerable total intake of lead (PTTIL), and we used per-capita consumption values to estimate population effects according to U.S. EPA Integrated Exposure Uptake Biokinetic (IEUBK) model (U.S. EPA, 2002). Lima bean and corn data were used in place of black bean and hominy data since data on the latter two vegetables were not included in the CSFII. This substitution was based on our view that consumption amounts of the substituted vegetables would be similar. We used average-body-weight data for children (male and female) to estimate serving sizes. Relevant body weight data is located in U.S. EPA's Exposure Factors Handbook, Table 7-6 and Table 7-7 (U.S. EPA, 1997).

We combined lead concentrations from analyzed foods with food intake values and mean body weight by age group to estimate the daily dietary lead intake for children 6 to <84 months, 84 months to 18 years, and >18 to 75 years. The two sets of data used to estimate food consumption (U.S. EPA CSFII and the Exposure Factors Handbook) use different age categories to classify children. To calculate corresponding consumption values for each year of age and desired cutoff levels (84 months, 18 years), we developed a regression equation using average weights for age categories and food consumption values by age category for children 0.5 to 18 years for each food. Estimated daily dietary lead intake values were compared with FDA's PTTIL of 6 [micro]g/day for children 6 years of age and younger, 15 [micro]g/day for children 7 to 18 years of age, and 75 [micro]g/day for adults 18 to 75 years of age (FDA, 1993). The U.S. EPA IEUBK model (U.S. EPA, 2002) was used to model the effects of lead leaked from vessels into foods as a dietary source of lead for children between 6 and 84 months of age. Median lead values based on per-capita consumption were entered into the Alternative Source category with an assumption that any lead ingested would be 50 percent bioavailable.

Results

The amount of lead contained in the vessels and the amount leachate into acid and foods varied considerably (Table 1). Lead content as measured by XRF showed that all vessels contained measurable amounts of lead, with a mean value of 19,231 mg/kg and a maximum of 260,000 mg/kg (26 percent lead). Thirteen out of 25 vessels tested (52 percent) with the acetic-acid leachate procedure exceeded the FDA action level for ceramic hollowware items; however, this evaluation does not provide an adequate assessment of the risk posed by cooking foods in these vessels. The calculations show that consumption of tomatoes cooked in all of these 13 vessels would exceed the PTTIL; however, consumption of tomatoes from 10 of the remaining 12 vessels would also exceed the PTTIL (indicating that the standard acid-based leachate test may not provide an adequate indication of consumption risk). The cooked-food results were both pH and consumption-mass dependent. Of the vessels containing the more acidic product (tomatoes), 23 of 25 (92 percent) produced food that would exceed the PTTIL for children 7 to 18 years of age, and 18 (72 percent) produced food that would exceed the PTTIL for adults. The results for the higher-pH beans and hominy were much lower; only 20 and 24 percent (5 of 25 and 6 of 25) of lima bean samples and 12 percent (3 of 25) of hominy samples exceeded the PTTIL. Since the average estimated consumption rates for these three foods varies from 1.25 to 1.62 to 2.65 g/kg per day for lima beans, tomatoes, and corn, respectively consumption rates also have an important role in the assessment of adherence to the PTTIL.

To model the population effects (elevated BLL) of consumption of foods cooked in the vessels, we entered the median daily dietary lead intake values into the IEUBK model for each of the three foods. The model predicted an increase from the default of 1.1 percent elevated BLLs (>10 [micro]g/dL) to 44.5 percent for a population consuming tomatoes (or a food with similar pH) cooked in these vessels, while the bean and hominy lead leachate concentrations would cause only a negligible increase in the percentage of elevated BLLs. For a population consuming tomatoes, the geometric mean BLL was also predicted to rise substantially, from 3.4 to 9.4 [micro]g/L.

Discussion

The data produced from this analysis clearly demonstrate that the LGC vessels still in use in the middle part of this decade represent a serious risk of lead poisoning to children. Furthermore, LGC vessels seem to be in fairly widespread use in the local Hispanic community Given the 15-year record of data indicating that the use of these vessels represents a high risk and the frequent public warnings issued about their use, it is apparent that much remains to be done to address this public health problem. A significant problem is that the risk assessment questionnaire used to evaluate exposure to lead sources does not typically contain information about the risk from these vessels; therefore, it can mis-evaluate the risks to some children (Erdem, Hernandez, Kyono, Chan-Nishina, & Iwaishi, 2004).

From the data produced in our study, it appears that the lead compounds used in glazes are absorbed into the clay body of the vessels rather than remaining strictly on the surface. It is also obvious that manufacturing techniques for these vessels vary greatly, which is not surprising in light of the fact that their manufacture is largely a cottage industry and occurs in different regions. It should be noted that the vessels tested in our study had been previously used (and to varying degrees); therefore, some lead, and perhaps a significant portion, may have already leached. Given some previous level of lead loss, it is likely that all values in this assessment under-represent the exposures that may have occurred with initial use of the vessels.

The data clearly demonstrate an increase in lead concentrations as food acidity increases. Although less acidic foods leached far less lead, they would still contribute lead to the diet, adding to the overall lead exposure; therefore, their use cannot be condoned for any foods. It is also not practical to restrict use of the vessels to neutral or less acidic foods, as it is highly unlikely that the pH of various recipes would be considered or measured before cooking. The ideal solution would be to educate consumers about the dangers of cooking and storing food in vessels of this type.

The IEUBK model predicts an increase in elevated BLLs of more than 45 percent for a population of children consuming tomatoes cooked in these vessels. It should be noted that the IEUBK and PTTIL values may be conservative since the foods were cooked only for 5 minutes and it seems likely that lead concentrations would increase with longer cooking times. In addition to predicting an effect on the prevalence of elevated BLL levels, the IEUBK model also estimated a dramatic increase in the mean BLL of a hypothetical population. Although the use of this model is based on a number of assumptions (eating low-pH foods cooked in LGC every day), the high rates of use (range = 39.9-81.8 percent, mean = 63.6 percent) reported in several of the studies cited earlier make this number seem more plausible. Each of the foods tested would exceed the PTTIL comparison to varying degrees ranging from 92 percent for tomatoes to 12 percent for hominy Of particular note is that acidic foods leached enough lead to exceed adult PTTIL for 75 percent of tested vessels. Since both the IEUBK model and the PTTIL indicate a potential for excessive dietary lead ingestion, strong support should be given to the recommendation to discourage the use of LGC vessels for cooking or storing any food or beverage.

The study had several limitations. Since the vessels tested were not identical, generalizations about rates of leaching based on averages may not be representative of any group of identical vessels. A more appropriate experimental design would have been to develop average values based on the testing of several different sets of identical vessels. We also used surrogate values for hominy and black bean consumption, which may have mis-estimated the true amount of product consumed. Indeed, none of the consumption values used may be indicative of true values in any given population. Finally, we are unsure if the pH of the foods that we tested is representative of foods in normal use.

Conclusion

The results of our study indicate that the amount of lead that migrates into food from LGC vessels constitutes a significant public health concern. Furthermore, our work demonstrates that vessels of this type are commonly available and in use in the local community despite years of accumulated knowledge about the risks they pose. There is clearly a disconnect between academic and community knowledge with respect to the hazards of LGC.

The vessels tested in our study were used for cooking in homes located in the local Hispanic community. While similar vessels can be purchased locally, the vessels could also have been brought into the United States from Mexico during family visits. A warning in English is printed on three of the vessels, stating: "NOT FOR FOOD USE, Food Consumed From This Vessel May Be Harmful." Since the warning label is printed in English, it is not particularly helpful to people who read in Spanish. The probable foreign origin of the examined vessels reduces the efficacy of federal agency intervention, as it is difficult to regulate manufacturing practices outside U.S. borders. Removal of unsafe products from store shelves is an incomplete solution for elimination of unsafe consumer products from U.S. markets. In addition to the regulatory efforts made by federal, state, and local agencies, public health professionals, health care providers, public schools, and universities must provide education in their communities so that consumers can make safe and informed decisions for themselves. The project that collected the vessels used in our study is a good example of an education effort that targets adults and community leaders.

Corresponding author: Robert Lynch, Associate Professor, University of Oklahoma Health Sciences Center, Department of Occupational and Environmental Health, 801 N.E. 13th Street, Oklahoma City, OK 73104. [e-mail].

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Robert Lynch, R.S., Ph.D.

Brenda Elledge, Dr.PH.

Christopher Peters, M.S.

TABLE 1 Lead Content Data for Lead-Glazed Ceramic Cooking Ware, Acetic
Acid Leachate, and Food Leachate

                                           Acetic-Acid   Food Tested
                                           Leachate      Tomatoes
Parameter                    LCG* (mg/kg)  ([micro]g/L)  ([micro]g/L)

Minimum                          170           170          112
Maximum                      126,000       260,000       36,000
Mean                          19,231        26,764        5,007
Median                         8,164         1,030        2,000
Number of vessels exceeding       --            13 (52)      --
  FDA action level (%)

Number of foods exceeding PTTIL**, by age of consumer

6 to <84 months                                              23
>84 months to <18 years                                      23
18 to 75 years                                               18

Median per capita lead consumption ([micro]g/day), by age (years)

0-1                                                          16.9
1-2                                                          35.1
2-3                                                          42.2
3-4                                                          49.3
4-5                                                          56.4
5-6                                                          63.5
6-7                                                          70.7

                                     Food Tested
                             Beans         Hominy
Parameter                    ([micro]g/L)  ([micro]g/L)

Minimum                          8           8
Maximum                      1,280         416
Mean                           200          70
Median                          51          38
Number of vessels exceeding     --          --
  FDA action level (%)

Number of foods exceeding PTTIL**, by age of consumer

6 to <84 months                  5           3
>84 months to <18 years          6           1
18 to 75 years                   1           0

Median per capita lead consumption ([micro]g/day), by age (years)

0-1                              0.0005      0.121
1-2                              0.010       0.181
2-3                              0.011       0.196
3-4                              0.012       0.211
4-5                              0.013       0.223
5-6                              0.015       0.241
6-7                              0.016       0.256

* Determined by XRF.
** PTTIL = provisional tolerable total intake of level.