biomonitoring of lead and cadmium in the hair and fingernails of elderly korean subjects

Biomonitoring of Lead and Cadmium in the Hairand Fingernails of Elderly Korean Subjects

Minjeong Kim & Kisok Kim

Received: 10 April 2010 /Accepted: 20 December 2010 /Published online: 8 January 2011# Springer Science+Business Media, LLC 2011

Abstract Lead and cadmium are toxic to humans at excessive levels, and monitoring thehuman body burden of these metals is important in preventing adverse health effects. In thisstudy, we assessed the exposure to lead and cadmium among an elderly population 60 yearsof age or older. Based on data from 115 participants, we found that the geometric mean leadconcentrations in hair and fingernails were 1.11 μg/g [95% confidence interval (CI) 0.78–1.58] and 1.11 μg/g (95% CI 0.81–1.51), respectively. The lead concentrations in hair andfingernails were significantly related to cigarette smoking. The geometric mean cadmiumconcentrations in hair and fingernails were 52.6 ng/g (95% CI 42.0–65.9) and 40.1 ng/g(95% CI 29.9–53.9), respectively. Cadmium concentrations in hair were significantlyrelated to body mass index and cigarette smoking, whereas higher fingernail cadmiumconcentrations were related to alcohol drinking. Correlations between hair and fingernailconcentrations of lead and of cadmium were slightly positive. Our findings suggest that thebody burden of lead and cadmium varies according to demographic factors, and hair andfingernails could be used differentially as a biological medium for metal exposure.

Keywords Lead . Cadmium . Elderly . Hair . Nail . Body burden

Introduction

Heavy metals are ubiquitous in natural environments, and some metals are extremely toxicto humans [1]. The toxic heavy metals of greatest concern include lead and cadmium [2].Lead and cadmium are dispersed widely in the environment, and exposure to these metalsmay be increased by human activities that release them into the air, soil, water, and food[3]. Because excessive and/or chronic exposure to lead or cadmium is known to be highlytoxic to humans, the control of environmental levels of and human exposure to these metalsto prevent adverse health effects is an important public health issue.

Biol Trace Elem Res (2011) 143:794–802DOI 10.1007/s12011-010-8942-4

M. Kim : K. Kim (*)Department of Public Health, Keimyung University, 1000 Shindang-dong, Daegu 704-701,Republic of Koreae-mail: [email protected]

The general population is exposed to lead from air and food in roughly equalproportions, and lead emissions to ambient air have increased dramatically during the lastcentury [4]. Exposure to high lead levels can severely damage many organ systems,including the renal, immune, reproductive, and nervous systems [5–11]. Moreover, chronicexposure to lead may have adverse effects on infant behavior [12].

Cadmium is a ubiquitous environmental pollutant, and exposure to cadmium occursprimarily through cigarette smoking and the consumption of contaminated foodstuffs orwater [13]. The International Agency for Research on Cancer has classified cadmium as ahuman carcinogen (group I) on the basis of sufficient evidence in both humans andexperimental animals [14]. In occupational studies, cadmium exposure has been associatedwith increased cancer mortality, including lung, prostate, and renal cancers [15–18].Population-based studies conducted in heavily polluted areas have shown that cadmiumis related to increased risk of cancer, renal tubular dysfunction, and all-cause mortality[19–21].

Because the adverse effects of exposure to these metals are related to the metalconcentrations in the body, human biomonitoring can provide information about the bodyburden and therefore indicate potential health effects. Human biomonitoring reflects anindividual’s exposure to toxic substances by measuring substances or their metabolitesin blood, urine, hair, nail, or other specimens. Hair and nails are biological specimensthat have some advantages as biomarkers for metal exposure, especially because thesample collection is simple and noninvasive, and the samples are very stable duringstorage [22, 23]. Furthermore, trace elements in hair and nails reflect rather long-termexposure because these biological samples remain isolated from other metabolic activitiesin the body [24, 25].

Biomonitoring studies can provide the mean exposure level of a population group for thepurpose of identifying high-risk groups and describing geographical differences. Furthermore,biomonitoring studies can provide information about the relationships between metal bodyburden and demographic or dietary factors [26]. In the determination of the body burden ofmetals, many contributing factors including sex, age, body mass index (BMI), education, anddietary pattern are involved. Therefore, in the present report, we describe the lead andcadmium concentrations in hair and fingernails by demographic and dietary factors based onsurvey data of Koreans aged 60 years or older. We also examined the correlations betweenhair and fingernail levels of lead and of cadmium.

Materials and Methods

Study Group

Healthy volunteers aged 60 years or older were recruited from eight census blocks in theRepublic of Korea. The total number of participants for the hair and fingernail analysis was115 (mean age 73.9 years).

Data Collection

Selected subjects were invited to a public health center in the census block for an interviewand sample collection. Using a face-to-face personal interview, participants were askedabout their sex, age, education, cigarette smoking status, alcohol drinking status, anddietary pattern. Height and weight were measured, and BMI was calculated as weight

Pb and Cd in Elderly Koreans 795

(kilogram) divided by height (square meter). The study protocol was approved by theKorean Ministry of Environment and was conducted in accordance with the EthicalPrinciples for Medical Research Involving Human Subjects, as defined by the HelsinkiDeclaration.

Sample Analysis

Scalp hair and fingernail specimens were collected from the occipital area of the head andall fingers, respectively, using supplies prepared specifically for trace metal measurements.All samples were stored in clean vials at room temperature. For the measurement of metalconcentrations, the hair and fingernail samples were washed once with acetone then twicewith deionized water for 5 min each on an orbital shaker. Subsequently, all samples weredried in an oven at 70°C for 12 h. Aliquots of 40 mg of hair and 30 mg of fingernailsamples were taken for digestion. The digestion procedure was carried out using 10 ml ofconcentrated HNO3 and 30% H2O2 (2:1) for 15 min in a microwave acid digestion system(MARS5, CEM, Matthews, NC, USA). The digests were made up to 10 ml in a volumetricflask with deionized water, and then the total lead and cadmium contents were measuredusing an inductively coupled plasma-mass spectrometer (ELAN 9000, Perkin Elmer,Waltham, MA, USA).

Analytical performance is assessed periodically through participation in external qualityassessment schemes, including the National Institute of Environmental Research’sproficiency testing program for trace elements. Internal quality control was performedusing a rhodium standard solution (36518-1B, Kanto Chemicals, Tokyo, Japan) as aninternal standard material. Moreover, the digestion and analysis methods for the hairsamples were validated using a human hair certified reference material (CRM, GBW 07601human hair, National Research Centre for CRM, Beijing, China). The values attainedthrough the analysis of CRM were 8.15±0.74 and 0.09±0.009 mg/kg for lead andcadmium, respectively, whereas the certified values for lead and cadmium were 8.80±1.10and 0.11±0.03 mg/kg, respectively. However, due to no certified fingernail referencematerial for total lead or cadmium content is commercially available, standard additionmethod was performed with several fingernail samples. Satisfactory recovery rates of 75–96% were obtained for the elements.

Variable Definitions

All variables were dichotomized for further analyses. Age was dichotomized at ≥70 yearsold, and BMI was dichotomized at ≥23. Education was categorized as less than elementaryschool graduation and elementary school or higher. Cigarette smoking status and alcoholdrinking status were categorized as yes or no; smokers (yes) included current smokers orpassive smokers, and drinkers (yes) included current drinkers. Dietary pattern was dividedinto vegetables (eating mainly vegetables every day) and others based on self-reportedeating habits. Tea or coffee consumption was divided by drinking <1 cup per day anddrinking more.

Statistical Analysis

We calculated geometric means (GM) with 95% confidence intervals (CIs) for lead andcadmium concentrations by taking the antilog of the mean of the natural log-transformedvalues. Based on a normal probability plot and other studies, geometric means were used to

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improve the approximation of a normal distribution. We fitted multiple linear regressions ofthe log-metal concentrations on the predictor variables. The exponentiated modelcoefficients represent the proportional change in the arithmetic mean associated with eachlevel of the predictor relative to a referent level, adjusting for the other predictors in themodel. A result was considered to be statistically significant if the 95% CI did not includeone (p<0.05). The log10-transformed concentrations of lead or cadmium were comparedbetween hair and fingernails by regression analysis. All statistical analyses were conductedusing SAS 9.1 computer software (SAS Institute, Inc., Cary, NC, USA).

Results

The lead concentrations in hair and fingernails are presented in Table 1. The geometricmean lead concentrations in hair and fingernails were 1.11 μg/g (95% CI 0.78–1.58) and1.11 μg/g (95% CI 0.81–1.51), respectively. The geometric mean hair lead concentrationswere the highest among cigarette smokers (2.13 μg/g), followed by those with a low BMI(1.66 μg/g) and the 60–70-year age group (1.48 μg/g). The patterns of hair leadconcentrations across population subgroups were similar after having adjusted forpredictors simultaneously in a log-linear regression. Cigarette smoking was significantlyrelated to hair lead concentrations after the adjustment of covariates, and it remained thestrongest predictor of hair lead concentration.

Lead concentrations in fingernails showed results similar to those of hair samples, i.e.,cigarette smokingwas themost important factor for increased lead concentrations in fingernails.Moreover, these changes were statistically significant after adjustment for covariates.

The geometric mean hair and fingernail cadmium concentrations among the elderlypopulation were 52.6 ng/g (95% CI 42.0–65.9) and 40.1 ng/g (95% CI 29.9–53.9),respectively, as shown in Table 2. Low BMI (GM=77.2 ng/g; 95% CI 53.9–110.7) andcigarette smoking (GM=76.7 ng/g; 95% CI 52.4–112.1) were strongly associated withincreased hair cadmium levels, whereas sex, education, alcohol drinking, and tea/coffeeconsumption were not strongly related to the cadmium concentrations in hair. Theseinfluences also existed after adjustment for potential covariates, and associations with a lowBMI remained significantly higher after adjustment.

However, the geometric mean cadmium concentration in fingernails was strongly relatedto alcohol drinking status, such that drinkers showed twice the geometric mean cadmiumlevel in fingernails compared with non-drinkers. Moreover, the mean concentration ofcadmium in fingernails was higher in drinkers (95% CI 1.19–3.71) compared with thereference groups after adjustment for potential confounding variables.

A linear regression analysis was used to explore whether the log-transformedconcentrations of lead or cadmium in fingernails changed as a function of the hairconcentrations of the same metal (Fig. 1). Although the correlations observed betweenthe hair and the fingernail concentrations of lead (r=0.20, p=0.06) and of cadmium (r=0.17,p=0.10) were not statistically significant, positive associations were observed between theconcentrations measured from hair and fingernails.

Discussion

Due to the importance of monitoring toxic metal exposure to human health, the appropriateselection and measurement of biomarkers of internal toxic metal doses is critical. Owing to


their many advantages, hair and nail samples have been used widely to assess humanexposure to various toxic substances [27]. In this study, we demonstrated the variability inbody burdens of lead and cadmium across demographic variables using hair and fingernailsamples as biomarkers. Our results revealed a geometric mean hair lead concentration of1.11 μg/g among elderly Koreans. Previous studies on adults have reported geometric meanhair levels in the range of 1.3–4.4 μg/g [28] and 1.72 μg/g [29], which are slightly higherthan our results. Moreover, one report has indicated a geometric mean hair lead level of1.7 μg/g (95% CI 0.1–10.2) among adult women [30]. Even though racial/ethnicdifferences and environmental pollution are important factors in determining the hair leadlevels in a population subgroup, another possible explanation for these differences is thatthe hair lead levels could decline with age. In the present study, hair lead concentrations

Table 1 Lead concentrations in elderly by population subgroups

Variable No. Hair Fingernail

Geometric meanconcentration[μg/g (95% CI)]

Adjusted proportionalchange in meanconcentration[μg/g (95% CI)]a

Geometric meanconcentration[μg/g (95% CI)]

Adjusted proportionalchange in meanconcentration[μg/g (95% CI)]a

Total 115 1.11 (0.78–1.58) – 1.11 (0.81–1.51) –

Sex

Male 29 1.24 (0.61–2.52) 1.00 (reference) 1.28 (0.70–2.33) 1.00 (reference)

Female 86 1.07 (0.70–1.62) 0.98 (0.41–2.30) 1.05 (0.73–1.53) 1.09 (0.55–2.13)

Age (years)

60–70 44 1.48 (0.90–2.44) 1.43 (0.68–3.05) 1.13 (0.65–1.98) 0.75 (0.39–1.44)

>70 71 0.93 (0.57–1.51) 1.00 (reference) 1.09 (0.75–1.60) 1.00 (reference)

BMI

<23 54 1.66 (1.02–2.68) 1.93 (0.98–3.81) 1.48 (0.96–2.28) 1.73 (0.96–3.14)

≥23 61 0.78 (0.47–1.30) 1.00 (reference) 0.85 (0.54–1.34) 1.00 (reference)

Education

< Elementaryschool

67 1.08 (0.67–1.72) 0.75 (0.33–1.69) 1.27 (0.85–1.88) 1.43 (0.76–2.70)

≥ Elementaryschool

48 1.15 (0.66–2.03) 1.00 (reference) 0.92 (0.55–1.55) 1.00 (reference)

Cigarette smoking status

No 80 0.83 (0.53–1.31) 1.00 (reference) 0.92 (0.61–1.39) 1.00 (reference)

Yes 35 2.13 (1.30–3.49) 2.18 (1.13–4.21) 1.67 (1.08–2.58) 1.82 (1.02–3.26)

Alcohol drinking status


Yes 32 1.11 (0.66–1.84) 0.91 (0.48–1.73) 0.73 (0.35–1.49) 0.55 (0.27–1.14)

Dietary patterns

Vegetables 68 1.36 (0.92–2.01) 1.60 (0.78–3.26) 1.35 (0.90–2.01) 1.50 (0.81–2.78)

Others 47 0.83 (0.42–1.62) 1.00 (reference) 0.84 (0.50–1.39) 1.00 (reference)

Tea/coffee consumption

<1 cup/day 46 1.02 (0.56–1.88) 1.00 (reference) 1.18 (0.69–2.01) 1.00 (reference)

≥1 cup/day 69 1.17 (0.75–1.82) 1.26 (0.64–2.49) 1.06 (0.71–1.57) 0.91 (0.48–1.71)

a The exponentiated b-coefficient from a log-linear multiple regression that includes all covariates in the table

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were most strongly related to cigarette smoking: the geometric mean hair lead level forelderly Koreans was 2.13 μg/g (95% CI 1.30–3.49) for smokers and 0.83 μg/g (95% CI0.53–1.31) for non-smokers, which is consistent with a previous report on an adultpopulation [31] that showed positive associations between hair lead and smoking. Similarly,the lead levels in fingernails were similar to those of hair and increased with cigarettesmoking. These results indicate that hair and fingernails accumulate nearly the same levelsof lead and are influenced similarly by demographic and dietary factors.

With respect to cadmium, the geometric mean hair cadmium level for Korean elderlysubjects was 52.6 ng/g, which is similar to that found in other studies. Previous studies havereported geometric mean hair cadmium levels of 48–88 ng/g for male adults [28] and85.1 ng/g in scalp hair [29]. Similar to the lead concentrations, cigarette smoking was also

Table 2 Cadmium concentrations in elderly by population subgroups

Variable No. Hair Fingernail

Geometric meanconcentration[ng/g (95% CI)]

Adjusted proportionalchange in meanconcentration[ng/g (95% CI)]a

Geometric meanconcentration[ng/g (95% CI)]

Adjusted proportionalchange in meanconcentration[ng/g (95% CI)]a

Total 115 52.6 (42.0–65.9) – 40.1 (29.9–53.9) –

Sex

Male 29 53.5 (31.3–91.4) 1.00 (reference) 46.4 (33.8–63.7) 1.00 (reference)

Female 86 52.3 (40.8–67.1) 1.15 (0.66–2.02) 26.0 (12.7–52.9) 1.82 (0.82–4.03)

Age (years)

60–70 44 61.2 (42.0–89.2) 1.15 (0.71–1.85) 41.8 (24.9–70.2) 1.21 (0.65–2.25)

>70 71 48.0 (36.0–63.9) 1.00 (reference) 39.1 (27.1–56.2) 1.00 (reference)

BMI

<23 54 77.2 (53.9–110.7) 2.00 (1.30–3.08) 39.7 (25.1–63.0) 1.04 (0.59–1.85)

≥23 61 37.7 (28.9–49.1) 1.00 (reference) 40.4 (27.3–59.8) 1.00 (reference)

Education

< Elementaryschool

67 51.3 (37.5–70.1) 0.89 (0.55–1.45) 35.2 (23.3–53.2) 0.84 (0.43–1.63)

≥ Elementaryschool

48 54.5 (39.1–76.0) 1.00 (reference) 48.2 (31.7–73.3) 1.00 (reference)

Cigarette smoking status


Yes 35 76.7 (52.4–112.1) 1.53 (0.98–2.38) 38.3 (24.0–61.1) 0.90 (0.51–1.59)

Alcohol drinking status


Yes 32 55.4 (35.5–86.5) 1.03 (0.65–1.63) 66.6 (40.4–109.7) 2.10 (1.19–3.71)

Dietary patterns

Vegetables 68 59.4 (44.7–79.0) 1.34 (0.86–2.07) 44.5 (29.9–66.4) 1.37 (0.76–2.49)

Others 47 44.2 (30.3–64.4) 1.00 (reference) 34.5 (22.1–53.9) 1.00 (reference)

Tea/coffee consumption

<1 cup/day 46 54.1 (38.8–75.5) 1.00 (reference) 35.5 (21.1–59.7) 1.00 (reference)

≥1 cup/day 69 51.6 (37.8–70.4) 0.98 (0.65–1.47) 43.5 (30.4–62.3) 1.23 (0.67–2.27)

a The exponentiated b-coefficient from a log-linear multiple regression that includes all covariates in the table


an important variable influencing hair cadmium: the geometric mean was 76.7 ng/g forsmokers and 44.5 ng/g for non-smokers. These results are almost the same as those in aprevious report [31] showing a geometric mean of 75 ng/g for smokers and 38 ng/g for non-smokers. Additionally, our results indicate that BMI is an important factor in determininghair cadmium levels. Alcohol drinking was the most important factor for elevated cadmiumlevels in fingernails, whereas cigarette smoking and BMI did not exhibit such influence.

The correlations between hair and fingernail concentrations of lead and cadmium werenot strong, in agreement with another study that reported correlation coefficients betweenlog-transformed values of hair and toenail of 0.15 for lead and 0.17 for cadmium [32]. Theweak correlation between these two markers may be attributable to the large variation inaccumulation and the different kinetics of lead and cadmium in hair and fingernails.However, the different kinetics of accumulation enable the use of hair and fingernailsdifferentially as exposure media for the monitoring of metals accumulated over a periodfrom a few weeks to a few months [33].

In summary, our findings suggest that hair and fingernail concentrations of lead weresimilarly affected by demographic factors, whereas those of cadmium were affecteddifferentially. The most significant factor in the bioaccumulation of lead in hair and

Fig. 1 a Correlation betweenlog-transformed concentrationsof hair lead (Pb) and fingernaillead (Pb) among 115 elderlyKorean subjects. Data wereanalyzed by linear correlationwith a 95% confidence interval,with a correlation coefficient (r)=0.20 and p=0.06. b Correlationbetween log-transformed concen-trations of hair cadmium (Cd) andfingernail cadmium (Cd) among115 elderly Korean subjects. Datawere analyzed by linear correla-tion with 95% confidence inter-val, with a correlation coefficient(r)=0.17 and p=0.10

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fingernails is likely to be cigarette smoking, whereas the level of cadmium in hair andfingernails was influenced mostly by cigarette smoking and BMI and by alcohol drinking,respectively. Our results also demonstrated a weak but positive correlation between hair andfingernail concentrations of both lead and cadmium.

Acknowledgments This research was supported by the Basic Science Research Program through theNational Research Foundation of Korea (NRF) funded by the Ministry of Education, Science andTechnology (2009-0072222).

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biomonitoring of lead and cadmium in the hair and fingernails of elderly korean subjects

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