Polycyclic Aromatic Hydrocarbon Residues in Human Milk, Placenta

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Polycyclic Aromatic Hydrocarbon Residues in Human Milk, Placenta, and Umbilical Cord Blood in Beijing, China Yanxin Yu,† Xilong Wang,† Bin Wang,† Shu Tao,*,† Wenxin Liu,† Xuejun Wang,† Jun Cao,† Bengang Li,† Xiaoxia Lu,† and Ming H. Wong‡ † ‡

Laboratory for Earth Surface Processes, College of Urban and Environmental Science, Peking University, Beijing, 100871, China Croucher Institute for Environmental Sciences and Department of Biology, Hong Kong Baptist University, Kowloon Tong, Hong Kong, China

bS Supporting Information ABSTRACT: This paper provides the results of an investigation on dietary intakes and internal doses of polycyclic aromatic hydrocarbons (PAHs) for nonsmoking women from Beijing, China. Concentrations of PAHs were measured by gas chromatography/mass spectrometry (GC/MS) for human milk, placenta, and umbilical cord blood samples from 40 nonsmoking women and for 144 composite food samples covering major food categories. Information on food consumption and estimated ingestion doses of PAHs by the cohort was also collected individually. Relationship among the studied human samples and relative importance of breastfeeding to the total exposure dose of infants were addressed. The median (mean and standard deviation) total concentrations of 15 PAHs in human milk, placenta, and umbilical cord blood with (or without) fat normalization were 278 (9.30 ( 5.75), 819 (35.9 ( 15.4), and 1370 (5.521 ( 3.71) ng/g of fat, respectively, and the corresponding levels of benzo[a]pyrene equivalent (B[a]Pequiv) were 11.2 (0.473 ( 0.605), 16.2 (0.717 ( 0.318), and 13.1 (0.140 ( 0.225) ng/g of fat, respectively. The calculated intake of B[a]Pequiv by Beijing cohort varied from 0.609 to 4.69 ng 3 kg1 3 day1 with a median value of 1.93 (2.09 ( 0.921 mean ( standard deviation) ng 3 kg1 3 day1. Significant correlations were found among human milk, placenta, and umbilical cord blood (p < 0.05) for low-molecular-weight PAHs, indicating selective transfer potential of individual PAHs from mother to fetus. Internal dose of PAHs was not in proportion to amounts of food ingestion, daily dietary intake, lifestyle, and social-demographic characteristics of the participants (p > 0.05). Ingested doses of PAHs (3.00102 ng 3 kg1 3 day1), which were much higher than the inhaled doses (0.1528.50 ng 3 kg1 3 day1), were 34 orders of magnitude lower than the recommended reference doses, unlikely to impose any obvious risk based on current knowledge.

’ INTRODUCTION Polycyclic aromatic hydrocarbons (PAHs) are of public health concern in China due to their high emission density, wide occurrence in the environment, toxicity, and carcinogenicity.1,2 The general population is exposed to PAHs through food ingestion, air inhalation, and dermal contact, among which food ingestion was identified as the primary pathway.3 Although there were a few studies focusing on PAH concentrations in food,4,5 the rather limited data reported thus far can hardly provide a general picture of food contamination in China. Human milk is believed to be a good marker for monitoring human burdens of various persistent organic pollutants.6,7 Umbilical cord blood and placenta were also used as such indicators.8 In addition to being a marker of the mother’s body burden of pollutants, these human tissues can also serve as indicators to potential exposure of embryo and infants. There was clear evidence suggesting that cancer risks increased following childhood exposure to carcinogens as compared with exposure occurring at a mature age.9 In addition, a number of health impacts including r 2011 American Chemical Society

low birth weight, endocrine-disrupting effects, and cytogenetic damage also may be associated with in utero PAH exposure.1012 Most of these studies focused on persistent organic pollutants like organochlorine pesticides and polychlorinated biphenyls.68 Unlike other persistent organic pollutants, PAHs metabolize relatively quickly in the human body, leading to different distributions.13 PAH concentrations in human milk have also been measured in several countries outside of China,1,1315 and there were also a few reports on the residual levels of PAHs in placenta and umbilical cord blood.16,17 To the best of our knowledge, however, such information is not available for Chinese women, although China is one of the most PAH-contaminated countries in the world.18 These data are critical for assessing risks of PAH exposure to mothers and infants. Received: August 13, 2011 Accepted: October 27, 2011 Revised: October 21, 2011 Published: October 27, 2011 10235

dx.doi.org/10.1021/es202827g | Environ. Sci. Technol. 2011, 45, 10235–10242

Environmental Science & Technology The objectives of this study were as follows: (1) Gather firsthand evidence on possible causal relationship between food consumption, dietary intake, and human sample residuals of PAHs. The target population consisted of one subset of mothers from Beijing, which is one of the most polluted cities in China. The potential health threat associated with PAH exposure is a noticeable issue. We determined the dietary intake by the population on the basis of dietary frequencies of all the individuals participating and measured PAHs in major foodstuffs. Human samples were collected and measured for PAHs. (2) Demonstrate, for the first time, the transfer potential of PAHs from mother to fetus. (3) Estimate the milk ingestion doses of PAHs for infants and examine the relative importance of breastfeeding for total internal doses.

’ MATERIALS AND METHODS Sample Collection. Human milk, placenta, and umbilical cord blood samples were collected from 40 nonsmoking mothers in Beijing. Recruitment and collection procedures were described in detail elsewhere.19 In brief, the samples were collected from those who delivering during a period from 2005 to 2006 in Tiantan Hospital, Southeast Beijing. They were all local residents living there for at least 6 years. Social-demographic characteristics of the target population can be found in the Supporting Information of our previous work.19 Approximately 50 mL of human milk was collected by each individual at hospital or home after the delivery using manual expression within 75 days after childbirth. Placenta (100300 g) and umbilical cord blood (30100 mL) were collected from each participant at the time of delivery. These samples were stored at hospital or home freezer until shipping to our laboratory and storage at 18 °C. Each participant finished a written informed consent and filled out two questionnaires: a nondietary determinant questionnaire covering information on lifestyle and social-demographic characteristics and a dietary questionnaire addressing food consumption frequencies during a 1-year period prior to childbirth and the average amount of food consumed on each occasion. The Committee on the Use of Human and Animal Subjects in Teaching and Research (HASC) of Hong Kong approved the project, which was partially supported by Hong Kong Research Grants Council. Food consumption information was taken from our previous study.19 Briefly, 33 kinds of foods, including fruits (apple, banana, pear, grape, and orange), vegetables (Chinese cabbage, cabbage, spinach, cucumber, carrot, green pepper, eggplant, lettuce, potato, and bean), cereals (rice and flour), fish (carp, grass carp, crucian, and bighead), meat (pork, chicken, beef, and mutton), eggs (two brands), and milk (five brands), were collected in local markets based on food consumption patterns of the Chinese population.20,21 For each food item, two composite samples with at least four subsamples were prepared. PAHs in foods were analyzed in a total of 144 composite samples, which included 576 individual samples. Only edible parts of each food item were included in the composites. Fruit, vegetables, cereals, egg, and milk samples were analyzed as soon as possible, while fish and meat samples were freeze-dried (Eyela-FDU-830, Tokyo Rikakikai, Japan) prior to analysis. Reagents. The reagents used in analysis were all purified before usage. Granular anhydrous sodium sulfate (Beijing Reagent) was heated at 600 °C for 6 h. Florisil (6080 mesh, Dikma Technologies) was precleaned for 6 h at 650 °C and dried in an oven at 130 °C for at least 16 h before use. Silica gel

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(100200 mesh, Beijing Reagent) was heated at 450 °C for 4 h and reactivated at 130 °C for 16 h immediately prior to use. Acetonitrile, n-hexane, and dichloromethane were analyticalgrade (Beijing Reagent) and were distilled before use. 2-Fluoro-1, 10 -biphenyl and p-terphenyl-d14 (internal standard), deuterated PAHs (acenaphthylene-d10, anthracene-d10, chrysene-d12, and perylene-d12), surrogates, and mixed standard of PAHs were purchased from J&K Chemical Co. All glassware was cleaned in an ultrasonic cleaner (KQ-500B, Kunshan Ultrasonic Instrument, China) and heated at 400 °C for 6 h. Extraction and Cleanup. The extraction and cleanup procedures of PAHs were similar to those of organochlorine pesticides described in our previous publication.19 Briefly, the extraction of PAHs from human milk, umbilical cord blood, dairy and egg samples followed a slightly modified U.S. EPA 600/8-80-038 procedure.22 A 5 mL sample was extracted three times with 12 mL of acetonitrile, for 5 min each time, then shaken with 120 mL of 12% sodium sulfate solution for 5 min, and finally extracted with 30 mL of n-hexane for 15 min. U.S. EPA 3630 method with slight modification was applied for placenta, fish, and meat samples.23 Briefly, samples (3 g) were homogenized with 5 g of anhydrous sodium sulfate and then Soxhlet-extracted for 24 h at 55 °C with a mixture of n-hexane (20 mL) and dichloromethane (80 mL). The extracts were further successively extracted twice with acetonitrile (30 mL each time, n-hexanesaturated); then 300 mL of 5% sodium sulfate solution was added and the mixture was extracted twice with n-hexane (30 mL each time). Fruit (40 g), vegetables (40 g), and cereals (10 g) samples were extracted by the FDA 2905a (6/92) method.24 Briefly, pulverized samples were extracted with acetonitrile (80 mL for vegetable or fruit, 25 mL for cereals) for 30 min, and then the filtered solution, after being shaken for 10 min with 300 mL (for vegetable or fruit) or 100 mL ( for cereal) of 12% sodium sulfate solution, was extracted twice with 40 mL of n-hexane for 15 min each time. For all the animal-origin and human samples, the extracts were concentrated to 1 mL in a rotary evaporator and transferred with 1 mL of n-hexane to a chromatography column (30 cm 10 mm i.d.) filled with the silica gel and eluted with 20 mL of n-hexane (discarded) and 35 mL of dichloromethane in sequence at a rate of 2 mL/min. For vegetation-origin samples, the extracts were eluted with n-hexane (50 mL) and with a mixture of n-hexane and dichloromethane (50 mL, 3:7 v/v) in sequence on a chromatography column (30 cm 10 mm i.d.) filled with both Florisil (4 g) and silica gel (6 g). For all samples, the eluate was concentrated to a final volume of 0.8 mL and spiked with 125 μL of the internal standard (2 mg/L). Sample Analysis. An Agilent gas chromatograph 6890 coupled with a HP-5 column (30 m 0.32 mm i.d. 0.25 μm film thickness) coupled with a HP 5973 mass-selective detector (MSD) was used for analysis of PAHs. The samples (1 μL) were injected in splitless mode with a venting time of 0.75 min. GC temperature was programmed from an initial 60 °C before commencing at 5 °C/min up to 280 °C, with a final holding time of 20 min. Helium was used as the carrier gas at a flow rate of 1 mL/min. The head column pressure was 30 kPa. The mass spectrometer was operated in SIM mode with an electron impact ionization of 70 eV, an electron multiplier voltage of 1288 V, and an ion source temperature of 280 °C. PAHs were quantified by the internal standard method with 2-fluoro-1,10 -biphenyl and p-terphenyl-d14 (J&K Chemical Co., 2.0 μg/mL). The 15 PAHs include acenaphthylene (ACY), acenaphthene (ACE), fluorine (FLO), phenanthrene (PHE), anthracene (ANT), fluoranthene (FLA), pyrene (PYR), 10236

dx.doi.org/10.1021/es202827g |Environ. Sci. Technol. 2011, 45, 10235–10242

Environmental Science & Technology benz[a]anthracene (BaA), chrysene (CHR), benzo[b]fluoranthene (BbF), benzo[k]fluoranthene (BkF), benzo[a]pyrene (BaP), dibenz[a,h]anthracene (DahA), indeno[l,2,3-cd]pyrene (IcdP), and benzo[g,h,i]perylene (BghiP). Quality Control. Routine quality control procedures were followed. Detection limits based on fresh weight (fw) for four groups of the samples (1, fruits and vegetables; 2, cereals; 3, placenta, meat, and fish; 4, human milk, umbilical cord blood, dairy, and eggs) were 0.0040.007 ng/g(fw), 0.0080.014 ng/g(fw), 0.0290.061 ng/g(fw), and 0.0120.025 ng/g(fw) for the 15 individual PAH compounds (Table S1 in Supporting Information). Recoveries of the surrogates were 94%, 94%, 93%, and 71% for the four sample groups, respectively. The mean and standard deviation of coefficient of variation of the duplicate measurement for the surrogates were 9.2% ( 6.3%. Average recoveries of the individual compounds in the standard solution spiked samples varied from 73.3% to 121% (Table S2 in Supporting Information). At least two procedural blanks and a standard solution were run simultaneously with every set of the sample analysis. The sample measurements were blank-corrected. Two or three replicates were measured for the majority of samples. Data Analysis. Medians, arithmetic means, standard deviations, minima, and maxima are reported. For samples below the detection limit, 0 was assigned. Both fat-content-normalized and fresh-weight- (fw-) based concentrations were provided for comparison with those reported in the literature, even though the latter might not be appropriate as measures of levels of PAHs in human samples. PAH levels were converted into benzo[a]pyrene equivalents (B[a]Pequiv) by use of equivalency factors (Table S3 in Supporting Information) in order to evaluate exposure risk of human body to the measured compounds.25 Daily dietary intakes were estimated from B[a]Pequiv concentrations; as a comparison, inhalation doses of PAH were also estimated on the basis of atmospheric concentrations reported in the literature (Table S4 in Supporting Information). The ingested amounts of various foodstuffs by Beijing mothers were obtained from dietary questionnaires,19 and inhalation rates (i.e., 15 m3/day) were selected on the basis of Suzuki and Yoshinaga’s report.26 On the basis of PAH concentrations in milk and air, the ingestion rate (800 ( 80 mL/day) and inhalation rate (4.5 m3/day) adopted from the literature, and body weight (6.63 kg),19,26,27 the infants’ body-weight-adjusted average daily PAH dose (nanograms per kilogram per day) from ingestion and inhalation were calculated. In all cases, a significant level of 0.05 was applied for all significance tests. Conventional and forward stepwise multivariate regressions were carried out to evaluate the dependence of PAH in human samples on the consumption of various foods and on lifestyle factors. Correlation analysis on the relationship between residuals in the human samples and dietary intake of PAH was performed. Monte Carlo simulation was performed with Matlab (v.13.0, The MathWorks, Inc.) for uncertainty analysis.

’ RESULTS AND DISCUSSION Concentrations of PAHs in Human Milk, Placenta, and Umbilical Cord Blood. According to Table 1, the median values

(with means and standard deviations shown in parentheses) of fat-normalized total concentrations of the 15 PAHs (PAH15) in human milk, placenta, and umbilical cord blood were 278 (383 ( 310), 819 (890 ( 330), and 1372 (2560 ( 2708) ng/g of fat,

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respectively. These were converted into tissue or fluid fresh weight average concentrations of 8.35, 35.8, and 5.52 ng/g(fw) (Table 1). The median values (and means and standard deviations) of fat-adjusted and fresh weight levels of B[a]Pequiv were 11.2 ng/g of fat [0.473 ( 0.605 ng/g (fw)], 16.2 ng/g of fat [0.717 ( 0.318 ng/g (fw)], and 13.1 ng/g of fat [0.140 ( 0.225 ng/g (fw)] in human milk, placenta, and umbilical cord blood, respectively. The observed PAH15 concentrations in human milk were much lower than those in Hong Kong measured in 2005 (1981 ng/g of fat),17 but almost 1 order of magnitude higher than those in Japan monitored in 2003 [0.75 ng/g(fw)]28 and in the United States detected in 2005 [17.5 ng/g of fat, 0.60 ng/g(fw)].15 As for umbilical cord blood, levels of total PAHs were similar to that in Hong Kong (1158 ng/g of fat) observed in 2005.17 Compared with placenta PAH concentrations determined in India in 20052006 (1052 ng/g of fat),29 our results were also comparable. As a whole, our measurements were higher than those reported in developed countries, suggesting that the Beijing cohort had much higher internal doses of PAHs than those in developed countries. The predominant PAHs in human milk, placenta, and umbilical cord blood were all low-molecular-weight compounds, including ACY, ACE, FLO, ANT, FLA, PYR, and PHE, while higher-molecular-weight PAHs showed relatively low levels. The PAH ranked in the order PHE > FLA > FLO > PYR in human milk, which was similar to that (PHE > FLO > FLA > PYR) reported in an American study15 but somewhat different from that (PHE > PYR > FLO > FLA) observed in Hong Kong.17 The pattern of PAH ranking for placenta in India, PHE > PYR > FLA > ACY > ANT,29 was very different from what we had observed (PHE > FLO > FLA > PYR > ANT). Similarly, there was also significant difference in rank order of PAH in umbilical cord blood between Beijing (PHE > FLO > FLA > ACY > PYR > ACE > CHR) and Hong Kong (PHE > PYR > FLO, FLA, CHR > ANT > ACY). With the information currently available, we are not able to identify the reason causing such differences. More study is need for a better understanding. Comparison of PAHs in Human Milk, Placenta, and Umbilical Cord Blood. Based on the total fat-content-normalized concentrations of low-molecular-weight PAHs including ACY, ACE, FLO, PHE, ANT, FLA, PYR, BaA, and CHR, the three kinds of human samples ranked in the order umbilical cord blood > placenta > human milk, which was very different from the sample rank based on fresh weight concentrations, that is, placenta > human milk > umbilical cord blood. The reason was that the median value of fat content in umbilical cord blood (0.50%) was much lower than those of human milk (2.92%) and of placenta (4.0%). Concentration of B[a]Pequiv also presented a very different rank order (placenta > umbilical cord blood > human milk) when compared with that based on fat-contentnormalized concentrations. The reason was that placenta contained more high-molecular-weight PAHs with higher equivalency factors than human milk and umbilical cord blood (Table S3 in Supporting Information). It was not surprising that fatcontent-normalized levels of low-molecular-weight members in human milk were the lowest among them when it is considered that these compounds are more readily metabolized and eliminated and therefore do not bioaccumulate significantly. It was reported that the half-life of PYR was between 6 and 35 h or between 16 and 20 h in the human body.13,30 An early work by Berenblum and Schoental31 demonstrated rapid elimination of BaP from mice (t1/2 of 48 h). N€af et al.32 examined the 10237


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Table 1. Statistics of PAHs in Human Milk, Placenta, and Umbilical Cord Blood in Beijinga fat-adjusted levels, ng/g of fat n

DR, %

mean

SD

median

ACY ACE FLO PHE ANT FLA PYR BaA CHR BbF BkF BaP DahA IcdP BghiP PAH15

27 39 38 39 40 40 40 35 31 37 34 30 31 21 21

67.5 97.5 95.0 97.5 100 100 100 87.5 77.5 92.5 85.0 75.0 77.5 52.5 52.5

5.27 36.6 53.5 133 14.4 50.9 36.5 3.97 7.42 20.5 8.62 1.77 6.39 2.50 1.26 383

8.09 33.6 55.7 124 15.2 40.2 26.8 3.88 10.2 22.1 9.6 1.76 13.9 4.08 1.45 310

2.10 25.0 31.4 85.7 9.39 35.5 28.4 3.17 5.06 12.2 3.92 1.49 2.31 0.655 0.529 278


40 27 40 40 32 40 39 40 38 40 36 28 40 19 33

100 67.5 100 100 80.0 100 97.5 100 95.0 100 90.0 70.0 100 47.5 82.5

70.4 22.5 170 336 23.4 106 67.9 16.9 25.1 24.2 8.98 6.86 8.36 1.01 2.65 890

56.3 19.9 65.4 144 24.7 39.1 27.4 13.1 17.8 14.2 6.59 7.63 13.4 0.826 1.65 330

73.6 26.0 166 291 17.6 100 68.8 17.1 22.2 22.0 7.40 4.23 2.26 0.64 2.79 819


32 30 31 37 40 36 40 36 38 21 19 12 9 3 7

80.0 75.0 77.5 92.5 100 90.0 100 90.0 95.0 52.5 47.5 30.0 22.5 7.50 17.5

169 86.8 367 763 117 283 236 73.4 116 214 85.5 16.2 16.7 4.73 10.3 2560

min

fresh weight levels, ng/g(fw) max

mean

SD

median

min

max

29.4 143 252 591 84.6 212 151 17.5 58.1 84.6 35.3 8.13 87.0 19.3 5.09 1668

0.132 0.845 1.22 3.25 0.367 1.23 0.97 0.113 0.238 0.476 0.190 0.047 0.129 0.064 0.030 8.35

0.169 0.421 1.09 2.49 0.306 0.684 0.744 0.150 0.505 0.429 0.183 0.054 0.210 0.103 0.033 9.29

0.055 0.808 0.976 2.57 0.299 1.14 0.861 0.096 0.147 0.289 0.114 0.040 0.087 0.024 0.019 5.77

ND ND ND ND 0.066 0.296 0.232 ND ND ND ND ND ND ND ND 1.21

0.535 2.15 5.77 11.8 1.27 3.18 4.71 0.958 3.18 1.52 0.635 0.314 1.30 0.576 0.135 25.0

165 67.3 370 657 100 249 141 47.4 82.8 50.2 23.1 28.3 50.7 3.75 6.04 1780

3.06 0.824 6.94 13.5 0.918 4.22 2.71 0.720 1.03 0.972 0.364 0.228 0.277 0.041 0.098 35.9

2.51 0.763 3.09 6.40 0.985 1.68 1.19 0.579 0.738 0.637 0.298 0.234 0.398 0.033 0.056 15.4

3.92 0.906 6.23 10.4 0.572 3.96 2.61 0.802 1.04 0.895 0.261 0.169 0.086 0.028 0.118 32.6

0.296 ND 2.60 5.04 ND 2.031 ND 0.037 ND 0.061 ND ND 0.035 ND ND 13.6

7.37 2.92 12.3 26.8 3.79 8.42 5.42 2.21 2.76 2.31 1.06 0.899 1.35 0.137 0.244 71.1

0.350 0.229 0.874 1.88 0.297 0.549 0.491 0.131 0.230 0.302 0.119 0.022 0.024 0.010 0.014 5.52

0.234 0.216 0.873 1.63 0.255 0.392 0.258 0.126 0.175 0.568 0.208 0.047 0.060 0.036 0.036 3.71

0.381 0.230 0.603 1.95 0.241 0.587 0.474 0.096 0.147 0.040 ND ND ND ND ND 5.60

ND ND ND ND 0.029 ND 0.096 ND ND ND ND ND ND ND ND 0.448

1.12 1.03 3.41 8.93 1.59 1.18 1.18 0.549 0.738 2.08 0.791 0.206 0.270 0.225 0.170 19.1

Human Milk ND ND ND ND 2.32 6.91 4.93 ND ND ND ND ND ND ND ND 47.2 Placenta 10.0 ND 62.7 136 ND 49.6 ND 0.995 ND 1.31 ND ND 0.830 ND ND 329

Umbilical Cord Blood

a

196 108 469 819 104 355 271 120 155 450 181 39.3 45.9 17.9 27.9 2710

81.7 52.8 219 468 84.5 141 112 27.6 64.2 7.03 ND ND ND ND ND 1370

ND ND ND ND 4.86 ND 18.2 ND ND ND ND ND ND ND ND 78.5

684 426 1747 3040 398 1176 1182 549 738 1922 791 206 228 112 127 9620

DR, detectable rate; ND, not detectable; SD, standard deviation; min and max, minimum and maximum. 10238



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Figure 1. Correlations between paired human milkumbilical cord blood, placentaumbilical cord blood, and milkplacenta samples for the sum of 10 individual PAH compounds: ACY, ACE, FLO, PHE, ANT, FLA, PYR, BaA, CHR, and BbF.

distribution and metabolism of 16 PAHs injected into the eggs of chickens and found that the concentrations of parent PAHs had reduced by 94% 14 days after the injection, as a result of metabolism by the chicken embryo. As for the observed higher fat-content-normalized levels of low-molecular-weight PAHs in umbilical cord than those in placenta, one important implication was that these compounds passed through placenta freely. This was proved by the findings that there were significant correlations (p < 0.05) between the paired human milkplacenta (r = 0.901), placentaumbilical cord blood (r = 0.977), and human milkumbilical cord blood (r = 0.933) samples for the sum of 10 low-molecular-weight PAHs (Figure 1). Determinations of PAHs in maternal serum and umbilical cord blood from Taiyuan, China, also showed that concentrations of a number of individual compounds in umbilical cord blood were considerably higher than those in maternal serum.33 Madhavan and Naidu16 collected human milk, placenta, and umbilical cord blood samples from 24 Indian women and analyzed the presence of selected PAHs. They found that umbilical cord blood contained relatively high concentrations of CHR. In comparison, sample rank for fat-contentnormalized concentrations of high-molecular-weight PAHs (BbF, BkF, BaP, IcdP, DahA, and BghiP) was rather different from that for low-molecular-weight PAHs. BbF was the only PAH compound found above the detection limit in umbilical cord blood. BkF and BaP showed their highest concentrations in placenta, followed by human milk, implying the influence of the placental barrier on transfer of higher-molecular-weight PAHs from mother to fetus. Concentration ranks for low-molecular-weight PAHs observed in human milk (PHE > FLA > FLO > PYR > ACE > ANT > CHR > BaA > ACY), placenta (PHE > FLO> FLA > PYR > ANT > ACY > CHR > ACE > BaA), and umbilical cord blood (PHE > FLO > FLA > ACY > PYR > ACE > CHR > ANT > BaA) were somewhat different from one another, showing variability in absorption, metabolism, and distribution of individual PAH compounds in different human tissues or fluids. PAH ranks in human samples were inconsistent with those reported for various foodstuffs in Beijing (Table S5 in Supporting Information) and ambient atmospheric particulate matter in North China,34 indicating differential transfer potential of PAHs from food and air to mothers. Cavret et al.35 carried out an in vitro experiment to investigate the mammary barrier role in C-14-labeled PAH transfer from food to human milk, and they found that PHE and PYR, but not BaP, were able to cross mammary cell layers. PHE radioactivity appeared more quickly in apical media, and its level after a 6-h exposure was 1.3 times higher than for PYR and 7.7 times higher than for BaP, indicating the selective transfer of PAH from food to milk.

Daily Dietary Exposure to PAHs. Based on the food consumption of individuals from the Beijing cohort and the B[a]Pequiv concentrations in various foodstuffs from local market, the daily dietary intakes of PAH by the target cohort were calculated. The calculated intakes varied from 0.609 to 4.60 ng 3 kg1 3 day1, with a median (mean ( standard deviation) of 1.93 (2.09 ( 0.921) ng 3 kg1 3 day1. In order to understand the relative importance of dietary intake for the total ingestion PAH dose, we further compared this with the inhalation intake of PAHs by the same group. On the basis of reported atmospheric PAH concentrations in Beijing,34 it was estimated that the inhalation intake was approximately 0.087 ng 3 kg1 3 day1. Obviously, dietary intake was the major pathway of the exposure. Different food categories usually gave differential contributions to the PAH exposure. The greatest contribution originated from vegetables (0.791 ng 3 kg1 3 day1, 37.8%), followed by cereals (0.511 ng 3 kg1 3 day1, 24.4%), because the ingestion amounts of vegetables (517 g/day) and cereals (200 g/day) by the Beijing cohort were larger than those of other food categories (34.6198 g/day) with the exception of fruit (534 g/day) and because concentrations of B[a]Pequiv in both vegetables [0.122 ng/g(fw)] and cereals [0.254 ng/g(fw)] were relatively high compared with those of other food categories. Bartle36 and Philips3 also found that vegetables and cereals were the most important contributors to human burden of PAH. Fruit gave the relatively small contribution of 6.42% in this study because of its lowest B[a]Pequiv value, even though the Beijing cohort ingested the largest amount of fruit. Milk ranked last (0.115 ng 3 kg1 3 day1, 5.49%) among all the local food categories for PAH intake. One important reason was that concentration of B[a]Pequiv in milk was relatively low [0.054 ng/g(fw)], and another reason was that the consumption of milk in Beijing was only 198 g/day. Concentration of B[a]Pequiv in fish was 0.423 ng/g(fw), largest among all the food categories; whereas the ingestion amount of fish was only 34.6 g/day, smallest among those of all the food categories. Consequently, fish accounted for only 8.21% of the total PAH intake in Beijing. Similar results were found for meat and eggs. They contributed 11.8% and 5.80% of the PAH intake, respectively, resulting from their relatively higher B[a]Pequiv concentrations [meat 0.154 and eggs 0.142 ng/g(fw)] and their relatively smaller ingestion amounts (118 and 72.9 g/day) in Beijing. Table 2 presents the shares of major food categories in total food consumption and total PAH intake. Association of Human Body Residual with Intake. Dietary exposure was already identified to be the most important source of PAH in the general population among various exposure pathways.26,37 We also found that daily dietary exposure contributed 96.0% of the total (diet + inhalation) daily exposure 10239



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Table 2. Relative Contributions of Major Food Categories to Food Consumption and the Human Burden of PAH in Beijing fruits

vegetables

fish

cereals

meat

eggs

milk

food consumption, g/day

534 ( 381

517 ( 364

200 ( 82.0

34.6 ( 32.0

118 ( 94.6

72.9 ( 48.2

198 ( 191

food consumption, %

36.2

35.0

13.6

2.34

7.99

4.94

13.4

total 1674 ( 810

PAH intake, ng 3 kg1 3 day1 0.134 ( 0.109 0.791 ( 0.692 0.511 ( 0.212 0.172 ( 0.167 0.247 ( 0.195 0.121 ( 0.085 0.115 ( 0.107 2.09 ( 0.921 PAH intake, %

6.42

37.8

24.4

8.21

11.8

5.80

5.49

sample size

23

6

25

43

14

6

5

doses of PAH for the nonsmoking Beijing cohort. However, no significant correlation was found between concentrations of PAH in the measured human samples and ingestion amounts of foodstuffs or between measured PAH concentrations in the measured human samples and ingestion doses of PAH. Dependence of PAH concentrations in the human samples on lifestyle and social-demographic characteristics of the participants was not observed either. In contrast, significant correlations were found for organochlorine pesticides for this Beijing cohort in our previous studies (p > 0.1).19,27 For PAHs, inhalation is another important exposure pathway,38,39 and the way the food is prepared may change the PAH concentrations.40 These factors could be part of the reason causing no correlation between the dietary PAH exposure based on market basket analysis and tissue residues. Other factors affecting the possible correlation between intake and accumulation of PAHs include nonstandardized sampling procedures and differences among tested individuals in terms of absorption, translocation, metabolism, and elimination of PAHs in human bodies. Of 40 target women, five individuals ingested almost the same amounts of B[a]Pequiv doses (187194 ng 3 person1 3 day1), but the concentration of B[a]Pequiv ranged from 0.364 to 45.5 ng/g of fat in human milk, from 8.74 to 29.2 ng/g of fat in placenta, and from 2.94 to 86.9 ng/g of fat in umbilical cord blood. One woman ingested the largest amount of B[a]Pequiv dose (345 ng 3 person1 3 day1) but had comparatively lower levels of B[a]Pequiv (12.8, 10.9, and 4.56 ng/g of fat in human milk, placenta, and umbilical cord blood, respectively), while another women ingested the smallest amount of B[a]Pequiv dose (52.3 ng 3 person1 3 day1) but had relatively higher levels of B[a]Pequiv (26.6, 32.4, and 211 ng/g of fat in human milk, placenta, and umbilical cord blood, respectively). The highest level of B[a]Pequiv in human milk (115 ng/g of fat) was found for a woman whose dietary exposure to B[a]Peq was 113 ng 3 person1 3 day1, an intermediate dose among all the calculated dietary exposures. The average coefficient of variation for dietary exposure to B[a]Pequiv was 0.448, whereas the corresponding values for concentration in human milk, placenta, and umbilical cord blood were 1.26, 0.538, and 1.83, respectively, suggesting internal levels of PAH changed greatly among individuals although ingestion PAH dose varied within a narrow range. Tsang et al.17 also pointed out that no significant correlation (p > 0.05) was observed between the consumption frequency of freshwater and marine fish with human milk and serum PAH levels for Hong Kong residents. The absence of correlation between PAH levels in body tissue or fluid with food consumption and dietary exposure is likely attributed to interindividual variability in metabolism of PAH. A variety of PAH metabolites and their conjugates are formed in the body and excreted in urine and bile. For the group of PAH with four or more rings, a large proportion of metabolites formed in the organism was preferentially excreted via bile, while metabolites originating from lower-molecular-weight PAH were

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easily detected in urine.41 The metabolism of PAH in the human body was possibly influenced by personal factors including age, body fat content, xenobiotic metabolizing enzyme system, physical and constitutional characteristics of an individual, and lifestyle factors including smoking, alcohol consumption, and exercise frequency.42 Viau et al.43 carried out a controlled feeding trial to five Canadian volunteers for five consecutive days and found large interindividual variation in urinary excretion of 1-hydroxypyrene (1-OHP), a metabolite of PYR, as an indicator of PAH exposure, due to interindividual variation in the absorption and metabolism of PYR. In a study performed in America, Kang et al.44 found that there was an 8-fold range of concentration of urinary 1-OHP among 10 subjects 1 day after identical quantities of charbroiled beef were ingested, and this variability was not appreciably altered after adjustment of 1-OHP concentration by urine creatinine concentration or individual body weight. They also found that concentrations of PAHDNA adduct in peripheral white blood cells varied significantly during or after charbroiled beef ingestion. They attributed the observed interindividual variability in both urinary 1-OHP level and concentration of PAHDNA adduct in peripheral white blood cells to individual differences in absorption, metabolism, and/or excretion rate of PAH and presumed that major biological factor(s) responsible for the interindividual differences observed might be common to both biomarkers.44 Another possible reason for the lack of correlation between residual levels of PAH in the human body and dietary exposures is the difference in sampling time. Furthermore, we relied on questionnaire information on food consumption to calculate daily dietary PAH intakes, which might result in uncertainty in the PAH ingestion dose. This factor may also play a role in the lack of association of dietary PAH intakes with PAH residues in human body. Postnatal Exposure of Infants. Like other contaminants, PAHs accumulated in human milk could be readily passed to breastfed infants. Based on the measured PAH concentrations in sampled human milk and the daily ingestion rate, the median intake doses by breastfed infants were calculated as 14.2, 69.6, 112, 287, 33.2, 102, 85.0, 12.7, 36.1, 45.2, 17.9, 4.90, 16.5, 7.90, and 3.00 ng 3 kg1 3 day1 for ACY, ACE, FLO, PHE, ANT, FLA, PYR, BaA, CHR, BbF, BkF, BaP, IcdP, DahA, and BghiP, respectively. Kim et al.15 have reported that the intake doses by American infants were 18.8, 75.8, 9.1, and 6.1 ng 3 kg1 3 day1 for FLU, PHE, FLO, and PYR. It appears that PAH exposure rates of infants in the study area to PAHs via breastfeeding were significantly higher than those of American infants. Such a difference is quite understandable since various environmental media and foodstuffs in Beijing were severely contaminated by PAHs.34,45 Among the three major exposure pathways, dermal contact usually contributed a negligible fraction of total human exposure to PAHs except in occupational environments. To compare the contributions between inhalation and ingestion by breastfed infants in Beijing, the recently measured concentrations of PAHs 10240



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Figure 2. Comparison between ingestion and inhalation exposure doses of infants in Beijing to PAHs as boxwhisker diagrams. The results are presented as the 10th, 25th, 50th, 75th, and 90th percentiles.

in both gases and particulate phases (gas, 204 ng/m3; particulate, 346 ng/m3 for the 15 PAHs) were adopted to calculate the inhalation doses (Table S4 in Supporting Information).34 The results are shown in Figure 2 together with those of ingestion doses as the 10th, 25th, 50th, 75th, and 90th percentiles. The median inhaled doses for the 15 PAH compounds were 6.04, 1.88, 4.51, 8.50, 1.32, 6.69, 5.33, 2.14, 2.58, 1.61, 1.54, 1.85, 1.25, 0.152, and 0.995 ng 3 kg1 3 day1, respectively, which account for only from 0.26029.9% of the total intake of individual compounds from both ingestion and inhalation (Table S6 in Supporting Information). Such ingestion-dominated PAH exposure was also reported by Kim et al.15 for American infants. When B[a]Pequiv were calculated, the inhalation and ingestion intake doses by infants in Beijing were 3.32 and 52.1 ng 3 kg1 3 day1, respectively. In fact, for Chinese adults, the predominant PAH exposure pathway is also ingestion, instead of inhalation. 46 Following the practice of Kim et al.,15 margin of exposure (MOE) was calculated as ratio of reference dose (RfD) to intake dose to evaluate the potential risk of PAH exposure of breastfed infants in Beijing. The calculated MOEs were 9.93 103 for ACY, 8.87 103 for FLO, 9.03 103 for ANT, and 1.96 104 for FLA, which were the only compounds with RfD listed (6 102, 4 102, 3 101, and 2 102, respectively) (http://www.epa.gov/iris). It appears that the daily dietary intakes were remarkably lower than the RfD levels and the exposure is unlikely to impose any obvious risk according to current knowledge.

’ ASSOCIATED CONTENT

bS

Supporting Information. Six tables as described in the text. This material is available free of charge via the Internet at http://pubs.acs.org.

’ AUTHOR INFORMATION Corresponding Author

*Tel: +86 10 62751938; e-mail: [email protected].

’ ACKNOWLEDGMENT This research was supported by grants from the National Natural Science Foundation of China (41130754 and 41101490), Beijing Municipal Government (YB20101000101), and the Research Grants Council of Hong Kong (RGC-ERG-2005-06). We thank the donors who provided the samples and the hospital for the assistance in sample collection.

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