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Analysis of the health risk of exposure to breast milk

mercury in infants in Taiwan

Ling-Chu Chien

a

, Bor-Cheng Han

a

, Chun-Sen Hsu

b

, Cheun-Bin Jiang

c

,

Hung-Jiun You

a

, Ming-Jer Shieh

d

, Ching-Ying Yeh

a,*

aSchool of Public Health, Taipei Medical University, 250 Wu-Hsing Street, Taipei 110, Taiwan, ROC bTaipei Medical University-Wan Fang Hospital, Taipei, Taiwan, ROC

cDepartment of Pediatrics, HsinChu Mackay Memorial Hospital, HsinChu, Taiwan, ROC dSchool of Nutrition and Health Sciences, Taipei Medical University, Taipei, Taiwan, ROC

Received 23 August 2005; received in revised form 8 November 2005; accepted 10 November 2005 Available online 25 January 2006

Abstract

The aim of this study was to assess the total concentration and health risk to infants of breast milk mercury in urban mothers and mothers married to fishermen in relation to fish intake in Taiwan. A total of sixty-eight healthy mothers were recruited for the study. The breast milk mercury geometric mean concentration was 2.02 lg l1(n = 56, range: 0.24–9.45 lg l1) for the city group and 2.04 lg l1 (n = 12, range: 0.26–8.62 lg l1) for the fishermen’s group. Of the three sources of mercury exposure (i.e., ingestion (breast milk), inha-lation (ambient air), and dermal exposure (shower)), breast-feeding was found to be the largest (96.3–99.6% of the total). From a Monte Carlo simulation, in which methyl mercury accounted for about 50% of total mercury, the hazard quotient (exposure estimate/oral imal risk level or target organ toxicity dose) exceeded 1.0 for 12.9% of urban babies and 18.8% of fishermen’s babies (chronic oral min-imal risk level and target organ toxicity dose: 3· 104mg kg1d1). The calculated mercury exposure was 3.02· 101lg kg1d1for a

3.49 kg urban baby boy and 3.06· 101lg kg1d1for a 3.44 kg urban baby girl. These results suggest the life style of mothers (eating raw fish and shellfish such as used in ‘‘Sashimi’’ and ‘‘Sushi,’’ and vitamin supplementation) may influence the mercury concentration in breast milk.

 2005 Elsevier Ltd. All rights reserved.

Keywords: Mercury; Breast milk; Monte Carlo simulation; Hazard quotient

1. Introduction

Mercury and its compounds are a significant threat to human health, particularly to pregnant women, women of childbearing age, developing fetuses, and breast-fed infants. The US Food and Drug Administration (USFDA) and the US Environmental Protection Agency (USEPA) are advising these women, nursing mothers, and young children to avoid eating fish that contain high levels of mer-cury such as shark, swordfish, king mackerel, and tilefish,

and to eat instead up to three hundred forty grams a week of a variety of fish and shellfish that are lower in mercury (USEPA, 2004). Previous studies have shown that a fish diet is the primary pathway of human exposure to methyl-mercury (MeHg), and that statistical differences in MeHg intake exist between high and low fish consumption groups (Oskarsson et al., 1995; Foo and Tan, 1998). Moreover, more than 90% of the total mercury in certain fish tissues has been found to be in MeHg form (Bloom, 1992; Kim,

1995; USEPA, 2001). MeHg is neurotoxic, readily

absorbed by the gut, and effectively crosses the blood-brain barrier and placenta (JECFA, 2003). The children of preg-nant women with MeHg intakes higher than the provi-sional tolerable weekly dietary intake (PTWI) level 0045-6535/$ - see front matter  2005 Elsevier Ltd. All rights reserved.

doi:10.1016/j.chemosphere.2005.11.059

*

Corresponding author. Tel.: +886 2 27361661x6515; fax: +886 2 27384831.

E-mail address:yehcy@tmu.edu.tw(C.-Y. Yeh).

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(1.6 lg kg1week1) have an increased risk of developmen-tal abnormalities (JECFA, 2003).

The World Health Organization (WHO, 2002) recom-mends breast-feeding infants exclusively during the first six months of life to achieve optimal growth, development, and health. Breast milk (the first food during this period) may contain toxic chemicals, such as polychlorinated biphenyls, DDT and its metabolites, polychlorinated di-benzo-p-dioxin, polychlorinated dibenzofuran, polybromi-nated diphenyl ethers, and heavy metals (Senawane, 1995; Hooper and McDonald, 2000). The amount of fish consumed during pregnancy can influence the maternal exposure to MeHg. MeHg can be stored and accumulated over time in body fat and then be mobilized into milk dur-ing lactation. Therefore breast-feeddur-ing constitutes a major source of exposure to bioaccumulated contaminant for infants.

However, little is known about fish consumption during pregnancy in Taiwan in relation to the mercury concentra-tion of breast milk. The purposes of this study were to assess the total breast milk mercury concentration of urban mothers and mothers married to fishermen in relation to fish intake and to assess the health risks of MeHg exposure in their infants. To assess MeHg exposure in breast-feeding infants, and to assess uncertainty in risk assessment and the impact of these uncertainties on the estimation of expected risk, we used the Monte Carlo technique. Then, we calcu-lated and validated a hazard quotient to evaluate the impact of fish intake on infants in Taiwan.

2. Methods

2.1. Collection and digestion of milk samples

A total of sixty-eight healthy mothers were recruited for the study. The subjects were separated into two groups: urban mothers (who lived in Taipei city, n = 56) and moth-ers married to fishermen (who lived in Lykang, Dongshih, and Budai, n = 12). Breast milk samples were collected from the subjects during the period from December 2002 to May 2004. All of the mothers provided colostrum sam-ples once early in the postpartum period. Fifty milliliters of breast milk were collected each time using clean poly-ethylene bottles. Collected samples were shipped back to the laboratory immediately, freeze-dried, and then stored until analysis. Approximately one gram of each sample was microwave-digested (CEM, Model MDS-2000, Mat-thews, NC, USA) with 4 ml of nitric acid (Suprapur, Merck, Darmstadt, Germany), 2 ml of hydrogen peroxide (Suprapur, Merck) and 2 ml of distilled water in closed polyfluorotetraethylene (PFTE) vessels. After cooling, the residue fluid was diluted to 10 ml with distilled water. 2.2. Mercury determinations

Mercury concentration was analyzed by a mercury ana-lyzer (HG-200, Hiranuma, Mito, Japan). Certified

refer-ence material (CRM) BCR No. 151 milk powder was used to perform a standard material test to ensure the pre-cision and accuracy of the milk analyses. The prepre-cision was 5.14% and the accuracy was 103.9%. The ratio of wet weight to dry weight for breast milk was 6.17 ± 0.88 (Chien et al., 2006). We divided the dry weight (lg1) by 6.17 to calculate its corresponding wet weight (lg l1).

2.3. Total average daily mercury exposure dose

To better evaluate the total average daily mercury expo-sure dose of infants, we considered the three sources of mercury bioaccumulation in infants: ingestion (breast milk), inhalation (ambient air), and dermal exposure (shower). The equation used for calculating total average daily exposure dose was

Etotal¼ Eingestionþ Einhalationþ Edermal ð1Þ

Ingestion exposure (breast milk):

Eingestion¼

Cmilk IRmilk

BW ð2Þ

where Cmilk: mercury concentration in colostrum (lg l1);

IRmilk: ingestion rate (l d1); and BW: body weight (kg, WHO, 1994).

Inhalation exposure (ambient air):

Einhalation¼

Cair IRinhalation 103

BW ð3Þ

where Cair: mercury concentration in air (urban area: 0.42–

8.44 ng m3, Tsai et al., 2003; coastal area: 1.82– 7.72 ng m3, Kim et al., 2002), IRinhalation: inhalation

volume (4.5 m3d1;USEPA, 2002), and BW: body weight (kg, WHO, 1994).

Dermal exposure (shower): Table 1defines the parame-ters used in the equation below

Edermal¼

Cw SA  ABS  F  ST  P

BW ð4Þ

2.4. Infant health risk characterization

Previous studies evaluating the health risk of MeHg in nursing infants demonstrated that about 7–50% of the total mercury was in the MeHg form (Abadin et al., 1997). The non-cancer risk was estimated using the hazard quotient (HQ) approach, which involved calculating a specific end-point, such as occurrence of a neurological development, immunological, or reproductive effect. HQ is the ratio of the exposure estimate to the appropriate oral minimal risk level (MRL) or target organ toxicity dose (TTD). The chronic oral MRL of 3· 104mg kg1d1 is recom-mended for use to assess neurological development effect of MeHg exposure and the TTD for immunological effects is 3· 104mg kg1d1(ATSDR, 1999).

For example, an HQ for neurological development effect is calculated as follows:

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HQneurodevelop¼

Cm IR

MRLneurodevelop BW  103

where IR: ingestion rate (l d1); Cm: MeHg concentration in colostrum (lg l1, 7–50% of total mercury); MRL: min-imal risk level (3· 104mg kg1d1); and BW: body weight (kg, WHO, 1994).

2.5. Uncertainty and Monte Carlo analysis

The chi-square and Kolmogorov–Smirnov (K–S) statis-tics were used to optimize the goodness of fit of the distri-butions of mercury concentrations in the breast milk of urban mothers and mothers married to fishermen. Distri-bution of the body weight was fitted to data obtained from the WHO (WHO, 1994).Chien et al.’s (2006) estimate of 400–500 ml of breast milk intake was used in our calcula-tions. The implemented parameter probability distribu-tions are summarized inTable 2. To assess uncertainty in risk assessment and its impact on the estimation of expected risk, we used the Monte Carlo technique. This involved inputting individual distributions of exposure variables to generate output probability distributions of the health risk estimates (USEPA, 1997). The Monte Carlo simulation and estimation of sensitivity were performed using Crystal Ball software (version 2000.2, Decisioneering, Denver, CO, USA). The health risk was calculated from 10,000 iterations of the risk model using randomly selected

values derived from each probability distribution of the model parameters.

2.6. Statistics

The distributions of continuous variables were expressed as mean ± standard deviation (SD). Between-group differ-ences in age, height, weight, and body mass index were evaluated by the Mann–Whitney U test. The chi-square test was used to assess the independence of two categorical variables. All statistical analyses were conducted using STATISTICA version for Windows. Results were consid-ered significant in a two-sided test if p < 0.05.

3. Results and discussion

Demographic characteristics of the sixty-eight mothers and their frequency of fish and shellfish consumption dur-ing pregnancy are summarized inTable 3. The age was sig-nificantly higher in the city group (31.1 ± 4.0 years) than the fishermen’s group (24.8 ± 2.7 years) (p < 0.001). Fish consumption was 1–2 meals per week in 44.6% of the city group and more than seven meals per week in 75% of the fishermen’s group. The frequency of fish consumption (p < 0.001) but not the consumption of shellfish was signif-icantly different between the two groups. None of the mothers had occupational exposure to mercury and in the city group only one mother smoked cigarettes and six mothers drank alcohol (10.7%) during pregnancy.

Fig. 1 shows box-and-whisker plots of colostrum mer-cury concentrations. The geometric mean of mermer-cury con-centration in all colostrum samples (n = 68) was 2.03 lg l1 (range: 0.24–9.45 lg l1). The breast milk mercury concen-tration was 2.02 lg l1(range: 0.24–9.45 lg l1) for the city group and 2.04 lg l1(range: 0.26–8.62 lg l1) for the fish-ermen’s group. These were not significantly different between the two groups. The three most popular fish (in descending order of intake) were cod, salmon, and anchovy for the city group and milkfish, tilapia, and hairtail for the fishermen’s group. In our previous study, the mercury concentrations in fish increased in the following order: milkfish (0.04 ± 0.04 mg kg1wet wt.) < hairtail (0.05 ± 0.01 mg kg1wet wt.) < salmon (0.06 ± 0.07 mg kg1wet Table 2

Input variables/parameter values used to define distributions for Monte Carlo simulation

Input variable Symbol Distribution Mean SD Hg concentration

in breast milka

Cm(lg l1)

City group Lognormal 2.03 2.48

Fishermen’s group Lognormal 2.04 3.10

Body weight BW (kg)

Baby boy Normal 3.49 0.40

Baby girl Normal 3.44 0.37

Breast milk ingestion rate for baby

IR (l d1) Normal 0.45 0.03

a

MeHg forms accounted for about 7–50% of total mercury (Abadin et al., 1997).

Table 1

Physiological parameters for estimating infants body burden

Parameter Symbol Values Reference

Hg concentration in water Cw(mg l1) 0.002 Taipei Water

Department (2005)

Surface area SA (m2) SA = 0.02350H0.42246W0.51456

baby boy: 0.243 m2

baby girl: 0.239 m2

USEPA (2002)

Dermal contact fraction F 80% USEPA (2002)

Showering time ST (min d1) 10 USEPA (2002)

Dermal absorption fraction ABS (mg mg1) 0.01 USEPA (1997)

Dermal penetration constant P (cm h1) 1.67· 103 USEPA (1997)

Body weight BW (kg) Baby boy: 3.49 kg

baby girl: 3.44 kg

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wt.) < cod (0.11 ± 0.08 mg kg1wet wt.) < tilapia (0.12 ± 0.06 mg kg1wet wt.) (Chien, 2005). Interestingly, some mothers in the city group ate raw fish and shellfish as used in ‘‘Sashimi’’ and ‘‘Sushi.’’ The three fish species most fre-quently used in ‘‘Sashimi’’ in Taiwan are swordfish, tuna, and salmon. Approximately 34.7% of the swordfish

mer-cury concentrations exceeded the Codex guideline level of 1 mg kg1(FAO/WHO, 1991; Chien, 2005).

Mercury concentrations in breast milk in our study are comparable to those found in other studies. Mercury con-centrations in breast milk in Brazil are 5.8 lg l1 in high-fish eaters (Barbosa et al., 1998) and 3.3 lg l1in non-fish eaters living near gold fields (Nunes-Junior and Sote´rio, 2000). A study in Saudi Arabia reported that mercury con-centrations in breast milk were 4.15 lg l1 and 2.19 lg l1 for Riyadh and Al-Ehssa residents, respectively (Al-Saleh et al., 2003). In Taiwan, the geometric mean in our study is slightly higher than the value (1.0 lg l1) published by

Ding et al. (1993).

Table 4shows the average daily mercury exposure dose in infants. There was not significantly different between the city group infants and fishermen’s group infants. Accord-ing to our findAccord-ings, inhalation and dermal contact with mercury are not the major source of exposure. Breast-feed-ing was estimated to represent 96.3–99.6% of the total mer-cury exposure in infants. Thus, breast milk is the major source of mercury exposure for infants. In our study, the calculated mercury exposure was 3.02· 101lg kg1d1 and 3.06· 101lg kg1d1 for an urban baby boy and baby girl (based on assumed weights of 3.49 kg and 3.44 kg and exposures of 1.04 lg d1 and 1.04 lg d1, respec-tively). The total estimated mercury exposure for Canadi-ans consuming various types of foods is 3.3 lg d1 for toddlers, 5.6 lg d1 for children, 6.7 lg d1 for teens, 9.4 lg d1for adults, and 6.8 lg d1for seniors ( Richard-son et al., 1995).

Fig. 2 shows the probability density distribution of the predicted hazard quotient in the city and fishermen’s groups for a baby boy exposed to different amounts of MeHg. The Monte Carlo simulation showed that if MeHg is about 50% of total mercury, then 12.9% and 18.8% of the hazard quotient estimates exceed 1.0 for the city and the fisherman’s babies, respectively, whereas if it is about 7% of total mercury, none of the hazard quotient exceeds 1.0. Note that a hazard quotient exceeding 1.0 indicates that breast milk consumption by infants is a potential health risk, such as risk of neurological development and immunological problems.

A multiple regression model for breast milk mercury concentration as function of age, supplementation with vitamins, mercury intake from fish, and selenium intake from fish is shown inTable 5. Breast milk mercury concen-tration increased with age and with mercury intake from fish, though the increases did not reach statistical signifi-cance. Breast milk mercury concentration was significantly lower in those who took vitamins than those who did not during pregnancy (p = 0.06). Interestingly, breast milk mercury concentration decreased with selenium intake from fish.Oskarsson et al. (1995, 1996)observed a positive association between breast milk mercury concentration and fish consumption in mature milk. Barbosa et al. (1998)

demonstrated that infant MeHg exposure during the fetal and breast-feeding periods is strongly related to maternal Table 3

Demographic characteristics and frequency of fish and shellfish consump-tion during the pregnancy of urban mothers and mothers married to fishermen

Characteristic City group

(n = 56) Fishermen’s group (n = 12) p-Value Age (years) 31.1 ± 4.0 24.8 ± 2.7 <0.001 Height (cm) 160 ± 4.0 158 ± 4.2 0.434 Weight (kg) Before pregnancy 53.4 ± 8.0 50.3 ± 7.3 0.178 After pregnancy 66.4 ± 9.6 63.0 ± 8.4 0.253 Body mass index (kg m2)

Before pregnancy 21.0 ± 2.9 20.1 ± 2.6 0.190 After pregnancy 26.0 ± 3.4 25.2 ± 3.4 0.389

Drinking during pregnancy 0.235

Yes 6 (10.7%) 0 (0%)

No 50 (89.3%) 12 (100%)

Smoking during pregnancy 0.641

Yes 1 (1.8%) 0 (0%) No 55 (98.2%) 12 (100%) Fish consumption <0.001 <3 meals/month 12 (21.4%) 0 (0%) 1–2 meals/week 25 (44.6%) 1 (8.3%) 3–6 meals/week 16 (28.6%) 2 (16.7%) >7 meals/week 3 (5.4%) 9 (75.0%) Shellfish consumption 0.256 <3 meals/month 40 (71.4%) 7 (58.3%) 4–8 meals/month 12 (21.4%) 5 (41.7%) >12 meals/month 4 (7.2%) 0 (0%) Values are given as mean ± standard deviation or n (%).

Hg concentration in colostrum ( μ g/l) 0 5 10 15 20 25 City Fishermen

Fig. 1. Box and whisker plots display the distributions of the mercury concentrations of colostrum in the city (n = 56) and fishermen’s groups (n = 12); median (horizontal line in the box), minimum, and maximum are shown. The box includes 50% of the values and is limited by the 25% and 75% percentiles.

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mercury body burden. In Austria, a significant positive relation was found between breast milk mercury concentra-tion and vitamin supplementaconcentra-tion (p < 0.05) (Gundacker et al., 2002). The exogenous application of the vitamin E (a-tocopherol) decreased mercury toxicity in rats (Welsh, 1979), and B-complex and E vitamins were found to mobi-lize a significant amount of mercury from brain, spinal cord, liver, and kidneys in rats (Bapu et al., 1994). Simi-larly, a study in rats found that selenium may protect against the acute neurotoxicity of MeHg (Ohi et al.,

1980). The possible mechanisms of protection include redistribution of mercury (Mengel and Karlog, 1980), competition for binding sites (Lucu and Skreblin, 1981; Leonzio et al., 1982), formation of a mercury-selenium complex (Naganuma and Imura, 1981; Magos et al., 1987), and prevention of oxidative damage (Cuvin-Aralar and Furness, 1991; Imura and Naganuma, 1991; Nylander and Weiner, 1991). In addition to vitamin supplementation and fish selenium consumption, the life style of mothers may influence mercury concentration in breast milk.

HQneurodevelop 0.5 1.0 1.5 2.0 2.5 3.0 3.5 Probability 0.00 0.04 0.08 0.12 0.16 0.20 HQneurodevelop 0.5 1.0 1.5 2.0 2.5 3.0 3.5 Probability 0.00 0.04 0.08 0.12 0.16 0.20 (A) (B) HQneurodevelop 0.5 1.0 1.5 2.0 2.5 3.0 3.5 Probability 0.00 0.04 0.08 0.12 0.16 0.20 HQneurodevelop 0.5 1.0 1.5 2.0 2.5 3.0 3.5 Probability 0.00 0.04 0.08 0.12 0.16 0.20 (C) (D)

Fig. 2. Probability density distribution of predicted hazard quotient in the city and fishermen’s groups for a baby boy exposed to different amounts of MeHg. (A) city group, MeHg: 50%; (B) city group, MeHg: 7%; (C) fishermen’s group, MeHg: 50% and (D) fishermen’s group, MeHg: 7%.

Table 4

Average daily mercury exposure dose in infants

Exposure Daily mercury exposure dose (lg kg1d1)

City group Fishermen’s group

Baby boy Baby girl Baby boy Baby girl

Breast milk 2.91· 101 2.95· 101 2.92· 101 2.97· 101

Air 1.09· 102(5.41· 104) 1.10· 102(5.49· 104) 9.95· 103(2.34· 103) 1.01· 102(2.38· 103)

Shower 3.10· 106 3.15· 106 3.10· 106 3.15· 106

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4. Conclusion

Our study explored the association between mothers’ consumption of fish and shellfish and mercury body burden in infants in Taiwan. According to our findings, breast milk mercury concentrations are not significantly different between urban mothers and mothers married to fishermen. The mercury concentration of breast milk may be affected by the life style of mothers, such as supplementation with vitamins, fish mercury consumption, and fish selenium con-sumption. In conclusion, fish have certain nutrients good for health; however, women of childbearing age, to reduce the body burden of mercury in their infants, should be con-cerned about mercury accumulated in fish.

Acknowledgement

This study was sponsored by the Taipei Medical Univer-sity (TMC 90-Y05-A102) and the National Science Coun-cil, ROC (NSC 92-2320-B-038-043).

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Table 5

Multivariate regression analysis of breast milk mercury concentration Coefficient p-Value

Intercept 0.47 0.81

Age 0.13 0.12

Supplementation with vitamins 1.37 0.06

Fish mercury consumptiona 1.23 0.52

Fish selenium consumptionb

1.94 0.35

(n = 68).

a Calculation based on individual consumed fish species, mercury

con-centration, and fish consumption rate divided into four categories (<3 meals/month, 1–2 meals/week, 3–6 meals/week, and >7 meals/week). For example, one mother ate milkfish, hairtail, and salmon <3 meals/month

0:04þ0:05þ0:06

3 Hg mg kg

1

· 1 = 0.05 Hg mg kg1.

bCalculation based on individual consumed fish species, selenium

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數據

Fig. 1 shows box-and-whisker plots of colostrum mer- mer-cury concentrations. The geometric mean of mermer-cury  con-centration in all colostrum samples (n = 68) was 2.03 lg l 1 (range: 0.24–9.45 lg l 1 )
Table 4 shows the average daily mercury exposure dose in infants. There was not significantly different between the city group infants and fishermen’s group infants
Fig. 2. Probability density distribution of predicted hazard quotient in the city and fishermen’s groups for a baby boy exposed to different amounts of MeHg

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