ARTICLE IN PRESS

Environmental Research 99 (2005) 235–242

www.elsevier.com/locate/envres

Predictors of elevated blood lead levels among 3-year-old Ukrainian

children: A nested case-control study$
L.S. Friedmana,, O.M. Lukyanovab, Y.I. Kundievc, Z.A. Shkiryak-Nizhnykb,
N.V. Chislovskab, A. Muchaa, A.V. Zvinchukd, I. Oliynyka, D. Hryhorczuka
a
University of Illinois, School of Public Health, Division of Environmental and Occupational Health Sciences, Chicago, IL 60612, USA
b
Institute of Pediatrics, Obstetrics, and Gynecology at the Academy of Medical Sciences of Ukraine, Ukraine
c
Institute of Occupational Medicine at the Academy of Medical Sciences of Ukraine, Ukraine
d
Kyiv University of Illinois Data Management Center, IL, USA
Received 13 August 2004; received in revised form 29 November 2004; accepted 6 December 2004
Available online 21 January 2005

Abstract

Objectives: Lead is common in the general population. However, data are lacking for the Ukraine and many other countries from
the former Soviet Union (FSU). In this study we evaluate the level of blood lead among 212 Ukrainian children and determine
predictors of elevated lead levels. We also describe the health effects associated with elevated blood lead.
Methods: A nested case-control study from a prospective cohort of Ukrainian 3-year-old children was conducted in March 1998.
Blood assays were analyzed for lead by labs at the Centers for Disease Control and using portable examination kits. We evaluated
predictors of elevated blood lead (blood levels in the upper quartile 44.65 mg/dL) using a multivariable logistic regression model.
The model included socioeconomic status, parent occupation, environmental tobacco smoke, hygiene, diet, and health status.
Results: The geometric mean lead level was 3.15 mg/dL (range, 0.7–22.7). In our adjusted model, we observed a strong association
between lead levels in the upper quartile and children whose fathers worked manual labor jobs in industries associated with lead
exposures [adjusted odds ratio (OR) ¼ 2.25; P ¼ 0:025] and mothers who smoke indoors (adjusted OR ¼ 2.87; P ¼ 0:047). Daily
hygiene and dietary habits were not associated with elevated lead levels. No increased risks of overall morbidity or lead-associated
illness were observed (anemia, dental caries, renal disease, cardiovascular diseases, and musculoskeletal complaints).
Conclusion: This is the first study to describe lead levels and associated variables among Ukrainian children in the peer-reviewed
literature. Elevated lead levels in these children were associated with paternal occupation and mothers smoking indoors. At age 3 no
adverse health effects were observed. More data are needed to determine the level of heavy metal contamination in children from the
Ukraine and many other former Soviet nation-states.
r 2004 Elsevier Inc. All rights reserved.

Keywords: Lead; Blood assay; Heavy metals; Adverse effects/children; Occupation; Smoking

$
This work was funded in part by a cooperative agreement from
USEPA and USAID. This project was supported in part by NIH
Research Grant No. D43 TW00653 funded by the Fogarty Interna-
tional Center, National Institutes of Environmental Health Sciences,
National Institute for Occupational Safety and Health, and the Agency
for Toxic Substances and Disease Registry. The US Centers for
Disease Control and Prevention Center for Environmental Health
Laboratory provided us the human tissue heavy metal analysis.
Corresponding author. The Social Policy Research Institute, 8423
Monticello Avenue, Skokie, IL 60076, USA. Fax: +1 8475307926.
E-mail address: spri@sbcglobal.net (L.S. Friedman).
1. Introduction
Lead is common in the general population and has
been well documented around the world. However, data
from the new nation-states of the former Soviet Union
(FSU), including the Ukraine, are lacking. Various
social and economic pressures have contributed to the
declining health status of the Ukrainian population.
During the 1990s, there was a 3.8% drop in life
expectancy and the standardized mortality rate for all

0013-9351/$ - see front matter r 2004 Elsevier Inc. All rights reserved.
doi:10.1016/j.envres.2004.12.006
 ARTICLE IN PRESS
236 L.S. Friedman et al. / Environmental Research 99 (2005) 235–242
causes of death increased by 18.2%, and the incidence of
both tuberculosis and AIDS has risen three- to five-fold
since 1990 (WHO, 2000).
Ukraine is a heavily industrialized nation. Forty-two
percent of Ukraine’s gross domestic product is derived
from industry, compared to 18% in the USA. Approxi-
mately 32% of the Ukrainian work force is employed in
industrial occupations—in the USA this figure is around
24.1% (CIA, 2004). However, governmental regulations
of industrial emissions are poorly enforced. Both
occupational and environmental exposures from indus-
trial sources pose a significant risk to the health of
Ukrainians. Because of the problematic situation in the
Ukraine as well as in many other FSU states, there exists
a need for quality data that can assist public health
officials in prioritizing national health issues and high-
light areas of concern. Heavy metal contamination and
associated health effects in children from Ukraine may
be an important public health issue that needs to be
evaluated within the context of a national public health
program.
Among children, lead has been associated with
reduced hematocrit volume (420 mg/dL; Schwartz et
al., 1990), elevated N-acetyl-X-D-glucosaminidase en-
zyme in urine, indicating proximal renal tubular damage
(mean of 34.2 mg/dL; Verberk et al., 1996), mild
increases in blood pressure (mean of 37.3 mg/dL;
Factor-Litvak et al., 1996), reversible electrocardiogram
abnormalities (range of 6–20 mg/dL; Silver and Rodri-
quez-Torres, 1968), lower intelligence (o10 mg/dL and
410 mg/dL; Canfield et al., 2003; Bellinger et al.,1991),
mild behavioral disorders (range of 10–20 mg/dL;
Wasserman et al., 1998), reduced neural conduction
velocity (range of 13–97 mg/dL; Landrigan et al., 1976),
and peripheral neuropathy (range of 60–136 mg/dL;
Erenberg et al., 1974).
Ukrainian children are probably exposed to multiple
lead sources, including contaminated soil, local industry,
parent’s work clothes, cigarettes, and food. In this study
we evaluate the level of blood lead among 212 three-
year-old Ukrainian children, describe potential sources
of exposure, and determine predictors of elevated lead
levels. We also describe the health effects associated with
elevated blood lead.
2. Methods
The Children of Ukraine cohort is a longitudinal,
geographically based study that follows children from
birth through 7 years of age. To date, data have been
collected at the following periods of development: time
of delivery and ages 6 months, 18 months, 3 years, and 7
years.
The Children of Ukraine cohort was initiated through
the coordination of the World Health Organization
(WHO), the Institute of Pediatrics, Obstetrics, and
Gynecology at the Academy of Medical Sciences of
Ukraine, and the University of Illinois at Chicago
School of Public Health. The European Longitudinal
Study of Pregnancy and Childhood (ELSPAC) Coordi-
nating Center in the Department of Child Health,
University of Bristol, England supervised all aspects of
data handling, management, and analysis in order to
ensure quality control.
Approval for the study’s confidentiality, ethics, and
safety standards was granted by the institutional review
boards at the University of Illinois at Chicago and the
Ukrainian Institute for Pediatrics, Obstetrics, and
Gynecology, as well as by local ethical committees in
Kyiv, Dniprodzerzhynsk, and Mariupol.
2.1. Study population
The Children of Ukraine cohort consists of subjects
born between August 1993 and July 1996 in the
following three cities: Kyiv, Dniprodzerzhynsk, and
Mariupol. The three cities were selected because they
represent regions with suspected higher-than-average
levels of exposure to environmental toxins and adverse
health outcomes compared to other regions in the
Ukraine.
The potential offspring of pregnant women who were
(1) permanent residents of Kyiv, Dniprodzerzhynsk, and
Mariupol and (2) planning on carrying the child to term
were considered eligible for inclusion. Both singleton
and multiple pregnancies were included. The centralized
medical system in Ukraine allowed for systematic
identification of eligible subjects in the three cities and
nearby regions during the inclusion period.
Children in the present study were taking part in a
substudy of the Children of Ukraine cohort. We
recruited children from Kiev and Mariupol in March
1998 who were between the ages of 212 and 312 years. We
contacted the parents of 295 eligible children, of which
244 children were enrolled (N ¼ 171; Mariupol; N ¼ 73;
Kiev; 82.7% response rate). Interviews and assessments
occurred between the 16th and 26th of March 1998.
Among the 244 enrolled children, 32 were not included
in this analysis because insufficient blood was drawn to
determine lead levels (N ¼ 28) or records were incom-
plete (N ¼ 4) as of January 2004.
The parents of the children were given a reimburse-
ment of approximately US$5 for travel and other costs
associated with participating in the study.
2.2. Questionnaires
Data regarding the socioeconomic and health status
of each child were collected from several sources.
Socioeconomic and hygiene practices were ascer-
tained from self-administered questionnaires completed
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L.S. Friedman et al. / Environmental Research 99 (2005) 235–242
by a legal guardian. The questionnaires were based on
the ELSPAC questionnaires. For quality assurance
purposes, all questionnaires were translated into Ukrai-
nian and then reverse-translated into English. All of the
final questionnaires were approved by the Coordinating
Committee in Bristol, England. For this study, data
regarding the child and parent were collected at the
following developmental ages: antenatal (mother’s
socioeconomic background), delivery, 6 months, 18
months, and 3 years. These questionnaires included
demographic data, descriptions of environment, and
hygiene practices. No specific data on monetary income
were available. Only self-rated descriptions of income
were available (poor, middle, rich). Although, most
parents rated themselves in the middle-income tier, by
US standards many were living under conditions that
most US researchers would classify as poor.
Data regarding the health status of each child was
taken from medical records. Record abstraction was
completed by Ukrainian physicians trained in ELSPAC
data-collection protocols, and the physicians used a
structured form. Diseases were classified using the Ninth
Edition of the International Classification of Diseases
(ICD-9).
We gathered data regarding family smoking habits
and parental occupation and place of employment from
the Immune System and Respiratory System Question-
naire. The questionnaire was administered by a trained
interviewer to the attending child’s guardian. The
immune questionnaire was an adaptation of the
Immune Function Test Battery for Environmental
Studies prepared by the US Agency for Toxic Sub-
stances and Disease Registry (ATSDR) (Straight et al.,
1994).
Parent occupation was coded following the Interna-
tional Standard Classification of Occupations
(ISCO-88) as developed by the International Labor
Organization. The category of manual labor used in our
analysis included all occupations coded under skilled
agricultural and fishermen, craft and related trades
workers, plant and machine operators/assemblers,
and elementary occupations (International Labor
Organization, 2002).
A food frequency questionnaire was self-administered
by the parent and reviewed by a trained nurse on the day
that blood was drawn. The questionnaire was based on
the modified 1992 version of the Block–NCI–HHHQ
Dietary Food Frequency Survey, which is also used for
National Health and Nutrition Examination Survey III
dietary assessment (NCI, 1992). The questionnaire was
modified to include foods that were culturally appro-
priate to Ukrainians. We evaluated variables regarding
dietary habits for shellfish (1+/month), other fish,
cabbage, green salads, raw spinach, cooked spinach,
homegrown vegetables, milk not purchased at a store,
and daily tap water consumption.
237
The height and weight of the child was evaluated on-
site by a trained nurse prior to assessment. The
measuring procedures followed the operational manual
entitled ‘‘How to Weigh and Measure Children’’ issued
by the United Nations Statistical Office in collaboration
with the World Health Organization.
All data were prepared for analysis at the Kyiv
University of Illinois Data Management Center. Data
files were provided to the Institute of Pediatrics,
Obstetrics, and Gynecology at the Academy of Medical
Sciences of Ukraine and to the University Of Illinois
School Of Public Health for statistical analysis.
2.3. Bioassays
Trained phlebotomists from Ukrainian polyclinics
performed all blood collections by venipuncture and
finger prick. Blood lead was analyzed using two portable
ESA LeadCare instruments (ESA Inc, Chelmsfold, MA,
USA) that had an analytic range of 1.4–65 mg/dL blood
lead. Children washed their hands in the presence of an
adult to limit lead contamination on the skin. The
child’s finger was pricked with a single-use lancet and
blood was drawn into a 50-mL tube after the first drop of
blood was discarded. Blood lead measurements and
daily quality control measures were performed accord-
ing to the ESA LeadCare manual. Among the 242
children who agreed to have blood drawn, only 216 had
a sufficient amount to provide an accurate reading. Four
were later excluded because they had incomplete records
(mean Pb, 3.75 mg/dL). Fifteen children (7.1%) had
blood lead levels below the detection limit of 1.4 mg/dL.
In the analysis, values below the detection limit of
1.4 mg/dL were treated as blood lead levels of 0.7 mg/dL.
Of the 212 children assessed using the ESA LeadCare
manual, blood from 78 children was transported to the
US Centers for Disease Control and Prevention (CDC)
Center for Environmental Health Laboratory for heavy
metal analysis (N ¼ 59 for Mariupol; N ¼ 19 for Kiev)
in order to assess test method bias and agreement.
Venipuncture was conducted using butterfly needles and
color-coded vacutainers. Lidocaine cream, a topical
local anesthetic, was used at the site of venipuncture.
Whole blood lead was determined using a Perkin-Elmer
Model 6000 SIMAA atomic-absorption spectrometer,
with aqueous calibrators prepared to National Institute
of Standards and Technology (NIST) standards. Meth-
od was dilution (1+9) with an ammonium phosphate/
nitric acid/Triton X-100 matrix modifier. Quality con-
trol was evaluated with duplicate determination of two
bench pools and a ‘‘new’’ NIST SRM (Standard
Reference Materials) (SRM 966) with values that were
determined by this method. None of the reported blood
lead levels were below the lower limit of detection for the
Perkin spectrometer (0.6 mg/dL).
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238 L.S. Friedman et al. / Environmental Research 99 (2005) 235–242

The geometric means of the matched pairs (N ¼ 78)
for the CDC-analyzed samples and the subset of the
LeadCare samples did not significantly differ (pooled t
test; P ¼ 0:58) and were as follows: CDC, 3.09 (range of
1.1–11.6) and LeadCare, 2.99 (range of 0.7–11.5). We
further tested the degree of agreement between the
LeadCare and CDC lab results (‘‘gold standard’’) using
the methods described by Bland and Altman (1986). The
untransformed LeadCare results were on average
0.25 mg/dL higher (mean difference; 95% CI, 0.13,
0.63) than those reported by the CDC labs. The limits of
agreement ranged from 3.06 to 3.56 mg/dL. The limits
of agreement reflect the degree of discrepancy between
the two measures. Based on the Bland and Altman
method, the overall agreement appears to be adequate,
but the limits of agreement indicate a potential for
misclassification when using the LeadCare results, given
our low overall blood lead levels.
2.4. Statistical analysis
Statistical analyses were performed using SPSS
(v.11.5) and SAS (v.8.2). The analysis of categorical
variables includes a presentation of frequency distribu-
tions, proportions, and statistical comparisons using
Pearson’s hlc chii2 tests. Geometric means are presented
for blood lead levels. The data were transformed to
correct for skewness (the Kolgomorov statistic of data
prior to transformation was D ¼ 0:136; P ¼ 0:01). We
used the Student t test for the analysis of continuous
variables.
Crude and adjusted odds ratios for children with
blood lead levels in the upper quartile were determined
(N ¼ 53; Pb44.65 mg/dL). Predictor variables from
Table 4 with a level of significance less than or equal
to 10% for the unadjusted odds ratios were included in a
multiple logistic regression model. The final multi-
variable logistic regression model included the following
potential predictors of elevated blood lead levels: city,
mother’s education level (412 years), father who
worked in manual labor in industries associated with
lead exposures, and mother who smoked indoors. All
predictors were dichotomous. Confidence intervals of
95% are provided. A two-sided P value of less than 0.05
is considered statistically significant.
3. Results
Table 1 shows the general characteristics of the child
participants. Sixty-one children from the city of Kiev
and 151 children from the city of Mariupol participated
in the study. The mean age for all 212 children was 36.4
months (SD, 1.9) at the time of the study. The Children
from Kiev compared to those from Mariupol were on
average older, more likely to be girls, more likely to have
mother’s with university degrees, and less likely to
attend kindergarten. We observed a statistically sig-
nificant difference in body mass index (BMI) between
the two cities. Only 1 (1.6%) child had a BMI score less
than 14.5 in Kiev compared to 14 (9.3%) from
Mariupol. More than one-third (39.6%) of the children
had at least one family member who smoked within the
home, but there were no significant differences in
smoking patterns between the two cities.
3.1. Lead levels
In both cities combined, the geometric mean lead level
based on the ESA LeadCare units on-site diagnostic test
(N ¼ 212) was 3.15 mg/dL (range of 0.7–22.7 mg/dL) and
based on the smaller sample of blood (N ¼ 78) sent to
the CDC labs was 3.09 mg/dL (range of 1.1–11.6 mg/dL).
More children from Mariupol had lead levels in the

Table 1
General characteristics of 3-year-old children and their parents, Kiev and Mariupol, Ukraine

Characteristics Kiev Mariupol Total P valuea

Number of participants 61 151 212 

Age at lead screening (months) 37.2 (SD ¼ 1.4) 36.1 (SD ¼ 2.0) 36.4 (SD ¼ 1.9) 0.010
Female 33 (54.1%) 68 (45.0%) 101 (47.6%) 0.232
Family income: poor/low income 2 (3.3%) 7 (4.6%) 9 (4.3%) 0.657
Mother’s education 412 years 17 (27.9%) 29 (19.2%) 46 (21.7%) 0.166
Attends kindergarten 26 (42.6%) 86 (57%) 112 (52.8%) 0.059
Mean weight (kg) at age 3 15.5 (SD ¼ 2.03) 14.8 (SD ¼ 1.58) 15.0 (SD ¼ 1.74) 0.029
Mean height (cm) at age 3 96.2 (SD ¼ 4.15) 95.6 (SD ¼ 3.57) 95.8 (SD ¼ 3.74) 0.364
Mean BMI (kg/m2) 16.8 (SD ¼ 1.48) 16.2 (SD ¼ 1.29) 16.4 (SD ¼ 1.36) 0.010
Low BMI (o14.5) 1 (1.6%) 14 (9.3%) 15 (7.1%) 0.048
Any family member smokes indoors 22 (36.1%) 62 (41.1%) 84 (39.6%) 0.501
Mother smokes indoors 4 (6.6%) 14 (9.3%) 18 (8.5%) 0.521
Father smokes indoors 21 (34.4%) 51 (33.8%) 72 (34.0%) 0.928
a
Continuous variables; we used Student’s t test, a two-sided means test between Kiev and Mariupol; Levenne’s test was used to determine
homogeneity of variance; for categorical variables we used Pearson’s hlc chii2 test.
 ARTICLE IN PRESS
L.S. Friedman et al. / Environmental Research 99 (2005) 235–242
Table 2
Geometric mean lead (Pb) levels in 3-year-old children, Kiev and Mariupol, Ukraine
Lead diagnostic test Kiev
a
Lead finger prick (mg/dL) 2.83 (r ¼ 0:7; 9.7)
Upper 25% of both cities combined (44.65 mg/dL)b N ¼ 9 (14.8%)
Upper 10% of both cities combined (46.20 mg/dL)b N ¼ 3 (4.9%)
a
N ¼ 212 children had available blood lead levels from the finger-prick method (N ¼ 151; Mariupol; N ¼ 61; Kiev). N ¼ 78 children also had
blood lead levels from CDC laboratories (N ¼ 59; Mariupol; N ¼ 19;Kiev).
b
Student’s t test, two-sided means test between Kiev and Mariupol; Levenne’s test was used to determine equivariance.
c
Mantel-Haenszel hlc chii2 test by city by number of children above and below the cut-off point.
upper quartile (greater than 4.65 mg/dL) compared to
children in Kiev (Table 2).
Geometric mean lead levels were significantly higher
among children whose fathers worked in manual labor
jobs (P ¼ 0:004) and among those whose mothers
smoked indoors (P ¼ 0:014). We did not observe any
hygiene or diet variables associated with elevated blood
lead in our group of children (Table 3).
3.2. Predictors of elevated lead levels
Table 4 presents unadjusted odds ratios for children
with blood lead levels in the upper quartile (elevated
blood lead levels above 4.65 mg/dL). Elevated blood lead
levels (ESA LeadCare units) were associated with
residence in Mariupol (unadjusted OR ¼ 2.38;
P ¼ 0:032), mother’s education (unadjusted
OR ¼ 0.47; P ¼ 0:089), and maternal indoor smoking
(unadjusted OR ¼ 2.65; P ¼ 0:053). Measures of hy-
giene and diet were not significantly associated with lead
levels in these children.
Children had an increased likelihood of blood lead
levels greater than 4.65 mg/dL if their fathers worked in
manual labor occupations (unadjusted OR ¼ 2.97;
P ¼ 0:001) or industries associated with lead exposures
(unadjusted OR ¼ 2.53; P ¼ 0:005).
After adjusting for all other predictors (Table 5), we
observed a strong association between lead levels in the
upper quartile and children whose fathers worked
manual labor jobs in industries associated with lead
exposures (adjusted OR ¼ 2.25; P ¼ 0:025) and mothers
who smoke indoors (adjusted OR ¼ 2.87; P ¼ 0:047).
3.3. Health outcomes
Forty-nine of the 212 children had an ICD-9
diagnosis registered in their medical records. These 49
children had a geometric mean blood lead level of
3.13 mg/dL, which is nearly equivalent to the overall
geometric mean of 3.15 mg/dL. Only 26 had diagnoses of
lead-related diseases, including anemia (N ¼ 22; geo-
metric mean Pb ¼ 3.14 mg/dL), circulatory diseases
(N ¼ 5; geometric mean Pb ¼ 3.12), and dental caries
(N ¼ 1; Pb ¼ 4.2 mg/dL). Circulatory diseases included
239
Mariupol Total P value
3.29 (r ¼ 0:7; 22.7) 3.15 (r ¼ 0:7; 22.7) 0.075b
N ¼ 44 (29.1%) N ¼ 53 (25.0%) 0.029c
N ¼ 19 (12.6%) N ¼ 22 (10.4%) 0.098c
four cases of cardiac murmurs and one case of
secondary cardiomyopathy. No cases of renal disease,
neuropathy, or encephalopathy were reported. In
addition to the low age of this group of children, the
blood lead levels are well below the levels associated
with acute and chronic illness in both pediatric and
adult populations based on the peer-reviewed literature.
3.4. Outliers
There were eight children with blood lead levels that
were found to be greater than 1.5 times the intraquartile
range (i.e., outliers). The geometric mean blood lead
level among the outliers was 11.88 mg/dL (range of
7.7–22.7). The children with outlying blood lead levels
compared to the remaining children were more likely to
have mothers who smoked (37.5 vs. 7.7%), fathers who
smoked (75 vs. 38%), and mothers who worked in
industries associated with lead exposures (37.5 vs.
21.6%), but not a father who worked in an industry
associated with lead exposure (37.5 vs. 52.4%). In an
adjusted logistic regression model, the eight outlying
children were more likely to have mothers who smoked
compared to the overall group (adjusted OR ¼ 6.15;
P ¼ 0:04; adjusted for father smoking, father with lead-
associated occupation, mother with lead-associated
occupation, and city). Health outcomes associated with
lead exposures were equally common among the outliers
compared to the other children (outliers vs. all other):
overall lead related morbidity was 12.5 vs. 10.1%.
4. Discussion
This is the first study to describe lead levels and
associated variables among Ukrainian children in the
peer-reviewed literature. We found strong associations
between elevated blood lead levels and maternal
smoking and father’s occupation. Among 3-year-old
children with levels almost entirely below 10 mg/dL, we
did not observe any increase in overall morbidity,
anemia, renal dysfunction, neuropathy, or colic.
We did not expect to find any lead-related diseases in
these children because of their young age and relatively
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240 L.S. Friedman et al. / Environmental Research 99 (2005) 235–242

Table 3
Geometric mean lead (Pb) levels by characteristics in 3-year-old children, Kiev and Mariupol, Ukraine

Characteristic N Geometric mean blood lead in mg/dL (range) P value

Gender
Male 111 3.06 (0.7–22.7)
Female 101 3.27 (0.7–15.0) 0.365
Income
Poor 9 2.02 (0.7–7.5)
Middle to wealthy 203 3.23 (0.7–22.7) 0.041
Mother’s Education
12 years and less 166 3.26 (0.7–22.7)
412 years 46 2.85 (0.7–13.0) 0.151

Mother’s occupation
Administrative/professional 105 3.24 (0.7–22.7)
Manual labor 107 3.10 (0.7–13.0) 0.570
Father’s occupation
Administrative/professional 103 2.82 (0.7–11.5)
Manual labor 109 3.53 (0.7–22.7) 0.004
Maternal smoking habits
Mother does not smoke indoors 194 3.07 (0.7–22.7)
Mother smokes indoors 18 4.38 (1.6–13.0) 0.014
Paternal smoking habits
Father does not smoke indoors 140 3.10 (0.7–15.0)
Father smokes indoors 72 3.31 (0.7–22.7) 0.490
Body mass index (BMI)
Normal BMI (14.5–22.0) 197 3.15 (0.7–22.7)
Low BMI (o14.5) 15 3.43 (0.7–11.5) 0.424
Hygiene
Eat dirt 8 3.64 (1.6–10.3) 0.524
Does not wash face (1+/day) 10 3.82 (1.6–7.7) 0.346
Does not always wash hands before meal 96 3.37 (0.7–15.0) 0.180
Does not bathe daily 146 3.22 (0.7–22.7) 0.505
Diet
Eats shellfish (1+/month) 35 2.95 (0.7–8.0) 0.479
Fried fish or fish sandwich (weekly+) 83 3.09 (0.7–22.7) 0.727
Eats homegrown vegetables 116 3.32 (0.7–15.0) 0.221
Drinks milk not bought at store 38 3.15 (0.7–13.0) 0.804
Drinks tap water (daily serving 48 oz.) 46 3.50 (0.7–22.7) 0.220

P values were determined by Student’s two-sided t test.

low exposures. The geometric mean blood lead levels in
this group of Ukrainian children were 3–20 times lower
than the mean levels associated with colic (ATSDR,
1999), mild nephropathy (x̄ ¼ 34:2 mg=dL; Verberk et
al., 1996), increased blood pressure (x̄ ¼ 37:3 mg=dL;
Factor-Litvak et al., 1996), mild behavioral disorders
(10–20 mg/dL; Wasserman et al., 1998), and peripheral
neuropathy (60–136 mg/dL; Erenberg et al., 1974).
However, studies have shown that levels below 10 mg/
dL have adverse neurocognitive effects (Canfield et al.,
2003; Wasserman et al., 1998).
The occupation of the parent has been associated with
blood lead levels in children (Paoliello et al., 2002;
Baghurst et al., 1992). In this study, there were 33
children with elevated blood lead levels who had fathers
employed in manual labor jobs in industries associated
with lead exposure. Among the 33, only 1 child was
from Kiev, and the child’s father worked in construc-
tion. Kiev is less industrialized than Mariupol. By
contrast, in Mariupol, there are coke byproduct-
recovery operations, a large steel industry, and a
manufacturing sector that produces heavy machinery.
The fathers of 28 (of the 32) Mariupol children worked
in these three industries.
Researchers have also shown an association between
passive smoking and blood lead levels in children
(Hossny et al., 2001; Baghurst et al., 1992; Willers et
al., 1988). Tobacco contains some lead at concentrations
between 2.5 and 12.2 mg/cigarette (WHO, 1977). In our
group of children, maternal smoking was more strongly
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L.S. Friedman et al. / Environmental Research 99 (2005) 235–242 241

Table 4 Table 5
Socioeconomic status, smoking, hygiene, and diet and their relation- Multivariable logistic regression model predictors associated with lead
ship to children with lead levels in the upper quartile (44.65 mg/dL)a, levels in the upper quartile (44.65 mg/dL blood)a among 3-year-old
Kiev and Mariupol, Ukraine children from Kiev and Mariupol, Ukraine

Characteristic Unadjustedb OR P value Characteristic Adjusted OR P value

(95% CI) (95% CI)b

City: Mariupol 2.38 (1.08, 5.23) 0.032 City 1.54 (0.65, 3.69) 0.328
Gender: male 1.26 (0.67, 2.35) 0.475 Father works manual labor in 2.25 (1.11, 4.58) 0.025
Income: poor 0.36 (0.04, 2.97) 0.345 industries associated with lead
Attends kindergarten 0.82 (0.44, 1.52) 0.525 exposuresc
Low body mass index (o14.5) 2.13 (0.72, 6.29) 0.172 Mother smokes indoors 2.87 (1.01, 8.12) 0.047
Mother’s education level 412 0.47 (0.20, 1.12) 0.089 Mother’s education level 412 years 0.53 (0.21, 1.30) 0.164
years
Variables included in the adjusted logistic regression model are all
Manual labor in industries those with Pp0:10 in the unadjusted model.
associated with lead exposuresc CI, confidence interval. The global model with the above four variables
Mother 1.53 (0.67, 3.50) 0.315 has a likelihood ratio of G2 ¼ 16.619 (df ¼ 4), P ¼ 0:002: All variables
Father 2.72 (1.43, 5.17) 0.002 in the logistic regression model were dichotomous. Manual labor is
Environmental tobacco smoke defined as those occupations with codes of 611 or higher in the
Any family member smokes 1.37 (0.73, 2.56) 0.332 International Standard Classification of Occupations (not including
indoors housewives or the unemployed).
a
Mother smokes indoors 2.65 (0.99, 7.11) 0.053 N ¼ 53 children in the upper quartile; the upper 25th percentile is
Father smokes indoors 1.12 (0.58, 2.14) 0.738 4.65 mg/dL.
b
Odds ratios for the outcome variable (lead, upper quartile) for each
Hygiene predictor variable, adjusted for all other variables.
c
Eats dirt 1.85 (0.43, 8.01) 0.411 Industries identified with a potential risk for lead exposure within
Washes face (1+/day) 0.48 (0.13, 1.77) 0.271 our sample were metallurgy, power engineering, machinery construc-
Always wash hands before 0.74 (0.40, 1.38) 0.340 tion, radio instrument manufacturing, construction, transportation,
meals farming, vehicle servicing center, and byproduct coking industry.
Diet
Shellfish (4once a month) 0.87 (0.37, 2.05) 0.749
Drinks milk not from store 1.50 (0.69, 3.23) 0.303
Eats homegrown vegetables 1.51 (0.80, 2.86) 0.204 lead level was 5.59 mg/dL (r ¼ 1:87239:36 mg=dL) (Os-
Drinks tap water (daily 1.43 (0.69, 2.94) 0.337 man et al., 1998). In Bulgaria near a nonferrous smelter,
serving 48 oz.) children ages 3–11 had a mean blood lead level of
24.0 mg/dL (r ¼ 7:7263:1 mg=dL) (Fischer et al., 2003).
Manual labor is defined as those occupations with codes of 611 or
higher in the International Standard Classification of Occupations (not A study from the Czech Republic noted a median blood
including housewives or the unemployed). CI, confidence interval. lead level of 3.4 mg/dL in a population-wide survey of
a
N ¼ 53 children in the upper quartile; the upper 25th percentile is children with a mean age of 10 years (Cerna et al., 2001).
4.65 mg/dL. In the USA, a group of 382 children ages 6–35 months
b
Odds ratios for the outcome variable (lead, upper quartile) for each
had a mean blood lead level of 7 mg/dL (SD, 5.2)
predictor variable, unadjusted for any other variable.
c
Industries identified with a potential risk for lead exposure within (Sarasua et al., 2000). These US children were selected
our sample were metallurgy, power engineering, machinery construc- from communities with high lead levels in the soil (the
tion, radio instrument manufacturing, construction, transportation, geometric mean ranged from 300 to 530 mg/kg in soil
farming, vehicle servicing center, byproduct coking industry. samples), and an additional group of children was
selected as controls from communities with low lead soil
levels.
associated with elevated blood lead levels than paternal Based on the findings of this study, 3-year-old
smoking. In fact, the only predictor significantly Ukrainian children in the cities of Kiev and Mariupol
associated with elevated blood lead among the outliers appear to not be severely contaminated with lead.
(geometric mean blood Pb ¼ 11.88 mg/dL) was maternal Health officials should investigate local occupational
smoking. Willers et al. also found that maternal hygiene practices, including on-site showers, the use of
smoking compared to paternal smoking was more overalls, and changing clothes before leaving work,
strongly associated with blood lead levels in their which can limit the transfer of contaminants to the
children (Willers et al., 1988). workers’ homes. Improved occupational hygiene prac-
The blood lead levels found among this group of tices could reduce exposures in children to lead as well as
Ukrainian children were comparable to some of the to many other contaminants. Health-intervention pro-
levels reported in pediatric populations from Eastern grams targeted at smoking mothers may prove useful in
Europe. In a survey of 9-year-old children from the reducing childhood exposure to heavy metals and other
industrial city of Katowice (Poland), the median blood toxics, as well as improving maternal health. Future
 ARTICLE IN PRESS
242 L.S. Friedman et al. / Environmental Research 99 (2005) 235–242
studies should monitor other suspect heavy metals like
mercury and arsenic. There is also a need to follow up
with this group of children to determine how blood lead
levels will change with age.
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