Journal of Toxicology and Environmental Health

ISSN: 0098-4108 (Print) (Online) Journal homepage: http://www.tandfonline.com/loi/uteh19

Use of lead‐glazed ceramics is the main factor

associated to high lead in blood levels in two
Mexican rural communities

Magdalena Rojas‐López , Carlos Santos‐Burgoa , Camilo Ríos , Mauricio

Hernández‐Avila & Isabelle Romieu

To cite this article: Magdalena Rojas‐López , Carlos Santos‐Burgoa , Camilo Ríos , Mauricio
Hernández‐Avila & Isabelle Romieu (1994) Use of lead‐glazed ceramics is the main factor
associated to high lead in blood levels in two Mexican rural communities, Journal of Toxicology
and Environmental Health, 42:1, 45-52, DOI: 10.1080/15287399409531862

To link to this article: http://dx.doi.org/10.1080/15287399409531862

Published online: 15 Oct 2009.

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 USE OF LEAD-GLAZED CERAMICS
IS THE MAIN FACTOR ASSOCIATED
TO HIGH LEAD IN BLOOD LEVELS
IN TWO MEXICAN RURAL COMMUNITIES

Magdalena Rojas-López, Carlos Santos-Burgoa

Instituto Nacional de Salúd Pública, SSA, Cuernavaca, Mexico
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Camilo Ríos
Instituto Nacional de Neurología y Neurocirugía Manuel Velasco Suárez,
SSA, Mexico City, Mexico

Mauricio Hernández-Avila
Instituto Nacional de Salud Pública, SSA, Cuernavaca, Mexico

Isabelle Romieu
Centra Panamericano de Ecología Humana y Salud, Organización
Panamericana de la Salud, Metepec, Mexico

Two isolated rural communities of Mexico were studied to assess the possible relationship
between lead-glazed ceramics use and lead exposure. Women from these communities (n =
98) were asked to participate by filling out a general-purpose and exposure questionnaire
in order to assess the individual contribution of ceramics to lead exposure. Blood samples
were withdrawn to measure lead in blood and erythrocytic zinc protoporphyrin levels.
Results were analyzed by multiple regression in order to find predictors of the dependent
variables. Significant association between lead in blood and erythrocytic zinc protopor-
phyrin levels was identified with the following variables: storage in lead-glazed ceramics,
cooking in lead-glazed ceramics, and meat and cheese consumption. The adjusted regres-
sion models explained 20-23% of the variance of the dependent variables (lead in blood
and erythrocytic zinc protoporphyrin). A significant association (r2 = .38) was observed
between lead in blood and lead in food prepared in lead-glazed ceramics in a sub-
sample of 28 women. Results indicate that lead-glazed ceramics use may be the main
predictor of lead in blood and erythrocytic zinc protoporphyrin levels in the rural com-
munities studied.

Received 4 July 1993; accepted 8 October 1993.

We thank Dr. Manuel Velasco Sua'rez for his valuable contribution to this study. We also thank Dr.
Daniel Paschal for providing reference material for quality control. This work was supported by the
Mexican Health Ministry and by funding from the National Center for Environmental Health, Centers for
Disease Control, Atlanta, Georgia.
Address correspondence to Camilo Ríos, Instituto Nacional de Neurología y Neurocirugía Manuel
Velasco Suárez, SSA, Insurgentes Sur No. 3877, México 14269, D.F., México.

45

Journal of Toxicology and Environmental Health, 42:45-52,1994

Copyright © 1994 Taylor & Francis
0098-4108/94 $10.00 + .00
 46 M. ROJAS-L6PEZ ET AL.

Environmental lead exposure of human population is a world-wide prob-

lem with health hazard implications (Coyer, 1990). In Mdxico, there is a
long history of human exposure to this pollutant (Ruiz-Sandoval, 1878);
however, only recent studies have identified the potential sources of expo-
sure to lead that could have some adverse impact on human health (Albert &
Badillo, 1991). Among these potential sources, lead-glazed ceramics is
thought to be the major contributor to increased lead body burdens in the
urban population (Hernandez-Avila et al., 1991). Lead-glazed pottery is
used amply in Mexico for food preparation and storage, as well as to serve
meals and beverages in the rural areas, as a result of its inexpensive cost.
Isolated rural communities in Mexico are far away from potential industrial
sources of lead such as, for example, lead-exhaust fumes from leaded gaso-
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line combustion, or lead-based battery production factories, which may con-

tribute to a high lead exposure of the inhabitants.
Two isolated rural communities of Mexico were studied to determine the
magnitude of the contribution of lead-glazed pottery use on blood lead and
erythrocytic zinc protoporphyrin (ZPP) levels.

METHOD
Study Population
Two communities (communities A and B) were chosen with a size of less
than 200 families each. One community was located in central Mexico (B)

FIGURE 1. Geographic location of the two communities studied.

 LEAD-GLAZED CERAMICS A N D BLOOD LEAD LEVELS 47

and the other in a southern state (A), as observed in Figure 1. A simple ran-
dom sample of ~50 women from each community was taken. From the total
sample, only 92 women from both communities accepted to participate in
the study.
Blood from adult women was obtained by venous puncture using lead-
free tubes containing EDTA as anticoagulant. Blood samples were stored at
4°C until analysis.
All women filled out a general-purpose and lead exposure questionnaire.
The lead exposure questionnaire recorded the use of lead-glazed ceramics to
prepare, keep, or serve food, the frequency of consumption of such food,
the consumption of canned food, and other types of potential exposure to
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lead. For proper identification of the lead-glazed ceramics, a photograph of

this kind of pottery was shown to the participants before asking about lead-
glazed ceramics-related items. Demographic variables such as type of floor
in house, number of subjects living in house, and the use of lead-based
paint for walls were also examined by the questionnaire. The questionnaire
was a modification of one previously used by our group to study an urban
population in Mexico City (Hernandez-Avila et al., 1991).
Blood and Water Lead Analysis
Lead in blood was analyzed by graphite furnace atomic absorption
spectrophotometry (GFAAS), according to Miller et al. (1987). A Perkin-Elmer
360 atomic absorption spectrophotometer and an HGA-2200 graphite fur-
nace, P-E lead hollow cathode lamp, deuterium arc background corrector,
and 056 strip-chart recorder were used. Calibration curves were constructed
for lead using an aqueous lead reference standard (NBS-3128, National
Bureau of Standards, Gaithersburg, Md.). Quality control of the lead in blood
analysis was assessed by our current participation in the lead in blood profi-
ciency program of the Centers for Disease Control, Atlanta, Ga.
Water lead was analyzed as recommended by Hunt and Winnard
(1986), using GFAAS.
Erythrocytic Zinc Protoporphyrin Measurement
Zinc protoporphyrin measurements were made by the direct procedure
described by Lamola et al. (1975). We used a Perkin-Elmer MPF-44A fluo-
rescence spectrophotometer for zinc protoporphyrin measurement. A zinc
protoporphyrin standard (Sigma Chemical Co., St. Louis, Mo.) was used to
express the results as micrograms of ZPP. Results were corrected for blood
hemoglobin content (Stanton et al., 1989) analyzed spectrophotometrically
in order to prevent interference of the nutritional status with the levels of
zinc protoporphyrin.
Analysis
Analysis of
or Lead
Leaa in
in Diet
uiei
Some of the participants in the study (n = 28) were able to provide a
;ample of food prepared in lead-glazed ceramics. Such opportunistic food
 48 M. ROJAS-LC»PEZ ET A L

samples were stored in polypropylene containers that were previously

washed with 3% (v/v) HNO3, rinsed with deionized water, and nitrogen gas-
dried to prevent external lead contamination. The content of lead in diet was
determined according to Vahter and Slorach (1986). The food was homoge-
nized with a food processor with a stainless steel grinder. A sample of ~1 g
was carefully weighed and submitted to acid digestion using Suprapur
(E. Merck) HNO3 in a water bath at 60°C for 30 min. The clear solution was
diluted with deionized water, and lead was analyzed by CFAAS.
Data Management
Both lead in blood and erythrocytic ZPP levels were natural log-trans-
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formed in order to achieve symmetric distribution of these variables to allow

us to perform statistical analysis. The statistical significance of the mean dif-
ferences between dependent variables (lead in blood and ZPP) according to
specific characteristics of the population was assessed using Student's t-tests.
Odds ratios were estimated from contingency tables with a chi-squared test
to determine the significance of the univariate predictors of blood lead and
erythrocytic ZPP levels. For these contingency tables, results of both lead in
blood and ZPP were considered high if they were greater than the median of
the whole data. Multivariate regression analysis was used to examine the
independent effects of specific variables with simultaneous adjustment for
other predictors of both blood lead and ZPP levels. All statistical analysis
were performed using SAS software (Dilorio, 1991).

RESULTS
Table 1 summarizes the relevant characteristics of the sample studied.
Fifty percent of the women had values of blood lead higher than 10 /ig/ml,
suggesting significant exposure to lead. Contingency tables univariate analysis
indicated that the exposure variables cooked food in lead-glazed ceramics;
stored food in lead-glazed ceramics, cheese consumption, and meat con-
sumption were associated with high lead in blood levels, as shown in Table
2. When multiple regression analysis was performed on the data using all
the variables as contributors, the same group of variables were found associ-
ated to lead exposure (see Table 2). Our model explained 2 1 % of the vari-
ability of blood lead levels (Table 2). The effect of these variables on the

TABLE 1 . Relevant Characteristics of the Sample

Variable Mean Median SD Range

Age (yr) 31 30 12.4 15-62

Blood lead (^g/dl) 12 10 7.2 1.6-39
ZPP/Hba U'g/g Hb) 9 8 5.1 2.5-30

a
ZPP, zinc protoporphyrin; Hb, hemoglobin.
 LEAD-GLAZED CERAMICS AND BLOOD LEAD LEVELS 49

TABLE 2. Predictors of Lead in Blood

Multiple regression
Odds Ratio
Variable (95% CD 8 P

Cooking in LGC 7.91 (1.8-25.8) 0.0464 0.0482

Storage in LGC 3.33(0.8-13.0) 0.1644 0.043
Meat consumption 6.37(1.6-26.5) 0.1190 0.103
Cheese consumption 3.64(1.1-11.6) 0.2228 0.030

Note. LGC, lead-glazed ceramics; Cl, confidence interval; 6 is the estimated coeffi-
cient of the variable in the regression, and p is the significance.
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mean of lead in blood levels is depicted in Figure 2. As is clearly seen, those

persons who answered yes to the question of lead-glazed ceramics use pre-
sented significantly higher levels of lead in blood. Cooking or storing in
lead-glazed ceramics produced a 71-72% increase in blood lead as com-
pared to non-use levels. The association between high lead in blood levels
and meat or cheese consumption observed in Table 2 could be the result of
the processing of such food in lead-glazed ceramics, since these nutritional
variables are not independent of lead-glazed ceramics use (p < .05, chi-
squared independence test).
The frequency of lead-glazed ceramics use was also correlated to high
lead in blood levels, as observed in Figure 3. Storage in lead-glazed ceramics
presented a similar trend.
Water lead content and consumption of canned food were not signifi-
cantly correlated with blood lead levels (p < .31 and p < .26, respectively).
Predictors for erythrocytic ZPP were the same as those already described

Blood lead (ug/dl)

Cook In IOC Start In LGC Ch««t« consumption M««t eontumpllon

I YES 3 NO

FIGURE 2. Lead in blood levels according to food intake habits. Results are expressed as mean ± SEM.
LGC, lead-glazed ceramics. Asterisks indicates statistically different by t-test from the respective negative
answer: *p < .05, **p < .01.
 50 M. ROJAS-L6PEZ ET AL.

Blood lead (ug/dt)

14

12

10

0
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0 1 2
Frequency of lead-glazed ceramics use
FIGURE 3. Lead in blood levels according to the frequency of lead-glazed ceramics use. Results are
expressed as mean ± SEM; 0, never; 1, rarely; 2, frequently.

for lead in blood (see Table 3). In this case, the multiple regression model
explained 20% of the variance of erythrocytic ZPP. As in the case of lead in
blood levels, lead-glazed ceramics-related variables were statistically associ-
ated to high erythrocytic ZPP. This could be the result of the close and
unique correlation between lead in blood levels and erythrocytic ZPP found
(r2 = .59). A significant association was also found between lead in blood
levels and lead content in food (r2 = .38) in the subsample of 28 subjects
who donated samples of their diet. Lead in water was not significantly asso-
ciated with lead in blood levels (r2 = .06).

DISCUSSION A N D CONCLUSIONS
In our study, lead-glazed ceramics-related variables were the only sources
of exposure associated with high lead in blood and erythrocytic ZPP contents.
This association was observed in a sample of women living in isolated com-
munities not exposed to other potential sources. Such a design strengthened

TABLE 3. Predictors of Erythrocytic ZPP

Multiple regression

Variable Odds ratio (95% CD B

Cooking in LCC 7.17(2.14-24.01) 0.0240 0.189

Storage in LCC 7.47(2.25-24.81) 0.1289 0.043
Meat consumption 3.47 (1.47-3.23) 0.1271 0.027
Cheese consumption 2.78(1.15-6.76) 0.0730 0.204

Note. LCC, lead-glazed ceramics; ZPP, zinc protoporphyrin; Cl, confidence interval; B
is the estimated coefficient of the variable in the regression, and p is the significance.
 LEAD-GLAZED CERAMICS A N D BLOOD LEAD LEVELS 51

the validity of the association. The fact that lead-glazed ceramics use was
associated with high ZPP levels suggests that lead-glazed ceramics might be
a health risk factor for the inhabitants of the two rural communities, using
ZPP as a biomarker of lead adverse effects (Hastka et al., 1992). The associa-
tion between high lead in blood levels and meat and cheese consumption
was unexpected as these products are calcium-rich, and calcium has been
reported to reduce lead absorption (Sorrell et al., 1977). However, the associ-
ation observed in the present work may be explained by the use of lead-
glazed ceramics to prepare cheese and meat meals. This is further supported
by the significant association between lead in blood and lead in food
observed.
Both water lead and consumption of canned food were not associated
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with high lead levels in blood. This is in agreement with our previous study
in the urban Mexican population (HernaYidez-Avila et al., 1991), indicating
that these potential sources of the metal are not important determinants of
blood lead in Mexico. One explanation for these findings is that drinking
water is rather "hard" in Mexico (pH > 7), tending to precipitate lead. On
the other hand, the use of lead solder for canned foods in Mexico was
banned some years ago, eliminating this possible source of lead.
To our knowledge, this is the first report on potential lead sources in iso-
lated rural communities. These results indicate that even people in isolated
communities are exposed to lead. Data support the need for regulations in
our country and many others that go beyond the urban pollution issues to
reduce the availability of daily use products with high content of lead. It also
calls for the development of new technology for pottery that can be used for
traditional cooking.

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