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High Postnatal Exposures to Polybrominated Diphenyl Ethers (PBDEs) and Polychlorinated Biphenyls (PCBs) via Breast Milk in California: Does BDE-209 Transfer to Breast Milk? June-soo Park,*,† Jianwen She,‡ Arthur Holden,† Margaret Sharp,† Rosanne Gephart,§ Ginger Souders-Mason,|| Vickie Zhang,† Joan Chow,† Bernice Leslie,† and Kim Hooper† †
Department of Toxic Substances Control, California Environmental Protection Agency, Berkeley, California 94710, United States Environmental Health Laboratory, California Department of Public Health, Richmond, California 94804, United States § Woman’s Health and Birth Center, Santa Rosa, California 95405, United States Marin Breast Cancer Watch, San Rafael, California 94901, United States
)
‡
bS Supporting Information ABSTRACT: Breast milk samples collected during 20032005 from 82 first-time mothers in 24 communities located throughout California contained levels of polybrominated diphenyl ethers (∑tri-hexa (8)PBDEs; median = 53.3 ng/g lw, range = 9.601291) and polychlorinated biphenyls (∑12PCBs; median = 73.4 ng/g lw, range = 22.2433) that are among the highest in the world. PBDE levels varied 100-fold. BDE-47 was the dominant PBDE congener, with levels exceeding the U.S.EPA Reference Dose (RfD) for neurodevelopmental toxicity (100 ng/kg/day) in most (60%) breast milk samples. In some samples, BDE-209 (2/82) and/or BDE-153 (5/82) were the dominant congeners, suggesting that BDE-209 can transfer to breast milk and/or break down in the mother and transfer to the nursing infant as the lower-brominated PBDEs associated with adverse effects. PBDE levels in California breast milk are approaching those of PCBs, and the trend PBDEs > PCBs may continue as PBDEs migrate from products to the indoor and outdoor environments.
’ INTRODUCTION Polybrominated diphenyl ethers (PBDEs) are flame retardant additives used in a variety of consumer products and electronics and are widely dispersed in both indoor and outdoor abiotic and biotic environments.1,2 As endocrine-disrupting chemicals that perturb thyroid homeostasis, PBDEs have toxicological effects in lab animals, wildlife, and humans that are similar to those of the polychlorinated biphenyls (PCBs). These effects include neurodevelopmental deficits; irreversible motor and behavior effects that worsen with age; altered reproductive function; immunotoxicity; impaired growth; and fetal toxicity/teratogenicity.28 Production and use of the commercial penta- and octa-BDE mixtures have been restricted in the European Union (EU) and U.S. However, continued biomonitoring of these chemicals in California is warranted for several reasons: 1) flame retardant standards in California for upholstered furniture are stringent (Technical Bulletin 117), and PBDE use has been extensive; 2) PBDE levels in the U.S. population are much higher (12 orders of magnitude) than in Europe, China, and Japan,911 and California’s are among the highest in the world;1214 3) PBDE commercial mixtures continue r 2011 American Chemical Society
to be produced in developing countries and exported to the U.S. as additives in manufactured products; 4) PBDE levels in wildlife and humans have been increasing for several decades,1416 with some data suggesting a leveling off;17 5) use of the deca-BDE commercial mixture in the U.S. continues (except for Washington and Maine), although U.S. EPA plans to prohibit production of the deca-BDE after 2012;18 and 6) a large reservoir of the deca-mixture remains in the environment, likely breaking down over the next several decades to lower brominated BDEs.16,19 Because of its high fat content, breast milk is a useful means of monitoring levels of lipophilic, persistent, environmental contaminants (e.g., PBDEs) in young mothers. Data from such studies can be used to estimate postnatal exposures in young infants via breast feeding.2022 These infant exposures may exceed the adult intake of PBDEs via diet/dust:23 studies show infants, toddlers, and Received: November 18, 2010 Accepted: March 27, 2011 Revised: March 15, 2011 Published: April 15, 2011 4579
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Environmental Science & Technology young children have higher PBDE levels than their parents.2427 To better assess the levels and extent of infant postnatal exposures to these chemicals, we measured PBDE and PCB levels in breast milk samples collected during 20032005 from California firsttime mothers (n = 82) with singleton infants 28 weeks of age. We compare these levels with those measured in samples from the U.S. Pacific Northwest, Texas, Massachusetts, Asia, and Europe and estimate postnatal exposures via breast milk to PBDEs in 6-mo-old infants in California.
’ EXPERIMENTAL SECTION Sample Collection, Preparation, and Analysis. We followed the WHO protocol for breast milk studies (first-time mothers, healthy singleton infants 28 weeks of age, collection by handexpression).28 The study was approved by the Committee for the Protection of Human Subjects, California Department of Health Services. Participants signed an informed consent form. Eighty-two mothers from birthing and lactation centers in 24 California communities collected samples during the period March, 2003October, 2005. Each participant collected two milk samples (∼100 mL each) over a 23 day period. Collection, preparation, and analysis of samples followed the protocols used in our U.S. Pacific Northwest breast milk study,29 and details are given in the Supporting Information. In brief, lyophilized samples were extracted by ASE, cleaned-up by silica gel column and GPC, and analyzed using HRGC/HRMS (Agilent 6890 coupled to a ThermoFinngan MAT95) and isotope dilution. For PBDE and PCB analysis, a DB-5MS column (15 m 0.25 mm i.d., 0.1 μm film thickness, J&W Scientific, USA) and a DB-5MS column (60 m 0.25 mm i.d., 0.25 μm film thickness, J&W Scientific, USA) were used, respectively. Recoveries of PCB and PBDE internal standards (spiked after lyophilization) ranged from 42.9 ( 1.4% for 13 C12PCB-28 to 82.8 ( 1.5% for 13C12 PCB-105 and from 59.6 ( 4.3% for 13C12BDE-209 to 90.7 ( 3.4% for 13C12BDE-153. Based on analyses of identical samples (37 duplicate pairs and 8 concurrent QCP samples) for BDE-47 and PCB-153, respectively, mean duplicate RPDs were 5.3% and 3.9%, and RSDs for 8 QCP samples were 3.5% and 3.9%.30 The concentrations of PCBs and PBDEs were log-transformed to make the data more symmetrical, as the PCB and PBDE data were skewed (ShapiroWilk normality test, p < 0.05). Parametric tests for the logged-PCB and PBDE data were conducted to determine differences between two populations and to determine the strength and direction of a linear relationship between the PBDEs and PCBs congeners. All statistical tests were conducted by using STATA Software (Version 11). Demographic information and data on individual California milk samples are provided in the Supporting Information (Tables S1S3). To assess possible risks to the 6-mo-old nursing infant in California from consumption of PBDE-contaminated breast milk, we estimated the average daily PBDE intake (ng/kg b.w./day) by the breast-fed infant using our PBDE data and standard estimates of median infant body weight (7.5 kg) 31 and mean milk consumption (769 g/day) at 6 months of age.20,32
’ RESULTS AND DISCUSSION Demographic Characteristics of Study Population. Sociodemographic characteristics of the California study population (79 out of 82 participants) as well as the Pacific Northwest population (n = 40) from our earlier breast milk study29 are
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shown in Table S1 and were reasonably similar. Participants in our California study were mainly Caucasian (71%), with some college education (89%). These characteristics are not representative of the California population. Consequently, our data may underestimate the true PBDE levels for all California first-time breast-feeding first-time mothers, as higher levels of environmental contaminants are reported for nonwhite populations and/or those with lower education levels.33,34 High Levels of PBDEs Found in California Human Milk. ∑PBDE levels (ng/g lw, ppb; with and without BDE-209) in California breast milk samples are compared with levels from the Pacific Northwest study in Table 1. Mean and median levels of ∑(tri-hexa)PBDEs in 82 breast milk samples from California firsttime mothers collected during 20032005 are among the highest in the world (mean = 130, median = 53.3, range = 9.601291). The California levels were higher than those reported for Chinese women exposed to a PBDE-contaminated e-waste site (mean and median ∑7PBDE = 71.2 and 29.3, range = 4.99273).20 The California levels were also higher than those measured in breast milk samples collected elsewhere in North America during a similar (20022007) period: Pacific Northwest = mean and median 93.9 and 49.3;29 Texas = medians 34.0, 39.7 (6.2580);11,35 Massachusetts = mean 75.0 (0.061910);36 New Hampshire = median 29.7 (6.5167);37 Pennsylvania = median 33.5;38 a U.S. population = median 28 (n.d.-1430).10 PBDE levels in California were more than an order of magnitude higher than those (mean = 0.423.7) reported for four Asian countries (Vietnam, China, Korea, and Japan)39,40 and Europe (median = 2.03.0)21,4143 during 20062008. Such comparisons we believe are useful even though samples in the cited studies were collected at different weeks of lactation and/or in different calendar years, as studies of U.S. populations indicate that PBDE levels change little during lactation,30,38 and changed little over these calendar years (this study and ref 11). Comparison between PBDEs and PCBs. Consistent with results from our Pacific Northwest breast milk study,29 levels of ∑8(major)PBDEs were greater than levels of Σ12(major)PCBs in nearly 50% (40/82) of the samples, although ΣPBDEs and ΣPCBs were not significantly different (p > 0.05). Thus, PBDE levels in breast milk samples from the western U.S. are approaching those of the legacy PCBs. This contrasts with results from studies of California wildlife (fish, shorebird, and peregrine eggs) and the outdoor environment, where PCBs still greatly exceed PBDEs.14,44 No significant correlations existed between PBDEs and PCBs in either the California or Pacific Northwest breast milk samples, when comparing either ∑8(major)PBDEs vs Σ12(major)PCBs or BDE-47 vs PCB-153. This contrasts with results from our studies of California marine wildlife (fish, harbor seals, shorebird eggs), where PBDE and PCB levels were correlated (e.g., shorebird eggs (R2 = 0.65).12,44,45 Such correlations may be limited to marine animals, where exposures to PBDEs and PCBs occur via a common source/pathway, the marine food chain. In our studies of peregrine falcon eggs from urban California,14 PBDE and PCB levels did not correlate, suggesting different exposure pathways. We hypothesized that urban peregrines were exposed to PBDEs via ingestion of PBDE-contaminated urban dusts, either via feather preening or consumption of dust-bearing urban prey birds.46,47 The lack of correlation between PBDE and PCB levels in breast milk samples is consistent with earlier suggestions that the sources and pathways for PBDE exposures in humans differ significantly from those for PCBs.1,29,48 If food ingestion is the major source/pathway for human exposures to PCBs, and 4580
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Table 1. Levels of PBDEs and PCBs in Breast Milk Samples from California (2003-2005) (This Study) and the U.S. Pacific Northwest (2003-2004)29 California mothers (n = 82)
Washington mothers (n = 40)
U.S. West Coast mothers (N = 122)
min
med
max
mean
stdev
min
med
max
mean
stdev
min
med
max
mean
stdev
fat%
1.75
3.83
6.80
4.04
1.26
1.43
4.06
6.12
3.99
1.01
1.43
3.96
6.80
4.03
1.18
PBDE-28/33 PBDE-47
0.01 4.35
2.44 29.7
26.1 723
4.20 72.6
4.81 116
0.26 2.63
3.59 50.1
4.03 52.1
0.01 2.63
2.23 29.1
26.1 723
4.00 65.2
4.56 99.8
PBDE-85
0.00
0.44
28.8
1.89
4.27
0.00
0.57
4.73
1.17
1.35
0.00
0.46
28.8
1.65
3.59
PBDE-99
1.03
6.40
364
24.2
55.3
0.79
5.36
49.2
10.3
11.4
0.79
6.16
364
19.7
46.2
PBDE-100
0.63
5.65
97.5
12.8
18.9
0.50
5.25
76.5
11.7
14.7
0.50
5.45
97.5
12.5
17.6
PBDE-153
0.52
6.34
107
13.0
17.7
0.84
4.79
169
16.3
30.9
0.52
5.58
169
14.1
22.8
PBDE-154
0.01
0.32
21.5
1.22
2.89
0.03
0.40
3.94
0.81
0.87
0.01
0.33
21.5
1.08
2.42
PBDE-209
0.28
1.41
55.3
3.67
8.56
0.05
0.43
4.26
0.80
0.97
0.05
1.15
55.3
2.73
7.16
∑(no BDE-209)PBDE ∑PBDE
9.60 9.93
53.3 54.5
1291 1295
130 134
206 208
5.35 6.81
49.3 51.7
319 320
93.9 94.7
92.7 92.6
5.35 6.81
52.1 53.7
1291 1295
118 121
177 179
PCB-28
0.78
2.21
6.32
2.43
1.00
0.90
2.83
10.6
3.84
2.59
0.78
2.52
10.6
2.89
1.81
PCB-74
1.99
6.35
44.1
8.29
7.04
0.66
2.24
106
7.36
17.1
0.66
5.54
106
7.98
11.3
PCB-99/113
0.76
3.54
28.8
5.00
4.91
1.49
5.41
33.8
7.43
6.17
0.76
4.16
33.8
5.80
5.45
PCB-118
1.84
6.10
18.9
7.03
3.96
2.17
6.69
125
11.8
19.8
1.84
6.39
125
8.59
11.9
PBDEs (ng/g lipid) 1.72 27.8
17.4 201
PCBs (ng/g lipid)
PCB-132/153
4.36
20.6
144
26.5
25.6
5.54
19.8
370
29.9
56.5
4.36
20.2
370
27.6
38.3
PCB-138
1.32
12.3
110
16.2
15.8
2.31
11.4
338
21.9
52.2
1.32
12.1
338
18.1
32.5
PCB-156 PCB-180
0.32 1.71
2.13 10.6
38.6 82.2
3.56 15.2
4.83 15.5
1.79 3.29
5.33 9.46
12.7 75.2
5.76 12.6
2.61 11.9
0.32 1.71
3.51 10.3
38.6 82.2
4.28 14.4
4.35 14.4
PCB-170/190
1.03
4.78
36.3
6.70
7.12
0.98
4.32
62.7
8.35
11.3
0.98
4.58
62.7
7.24
8.69
∑PCB
22.2
73.4
433
90.9
74.5
28.5
73.5
1121
109
170
22.2
73.4
1121
96.8
114
ingestion of house/office dusts a significant source/pathway for exposures to PBDEs, the ratio PBDEs:PCBs in breast milk may continue to increase in the future as PBDEs continue to migrate from products into the indoor and outdoor environments. However, recent reports of PCBs in construction materials and paints may affect this.49 PBDE Congener Patterns. BDE-47 was the dominant congener in California milk samples, followed by BDE-99, -100, and -153, with the latter congeners showing no significant differences among themselves in levels or proportions (p > 0.05) (Figure 1). The general PBDE congener pattern (BDE-47 > BDE-99 = BDE100 = BDE-153) was similar to patterns found in other breast milk studies in the U.S.,29,35,36 Europe, 21,4143 and Asia.20,39,40 These results may indicate that the lower brominated PBDEs (e.g., BDE47) preferentially transfer to breast milk compared to the higher brominated congeners. BDE-209: Evidence for Transfer to Breast Milk? Debromination? Transfer of the higher (hexa-deca) brominated BDEs to breast milk may be less favored than transfer of the lower (tri-penta) brominated BDEs due to their larger molecular size and lower lipophillicity.50 In our California milk samples, levels of BDE-209 were generally low (median 1.41 ng/g lw), similar to levels reported in milk samples from the U.S. and Europe (median range = n.d.-5.9 ng/g lw).21,36,42,43 However, a few samples (5 out of 82) had higher levels of BDE-209 (10.755.3 ng/g lw), with BDE-209 exceeding BDE-47 in two samples, and the maximum BDE-209 value among the highest reported in the world for breast milk (Figure 1). At first we discounted these results to be artifacts of BDE-209
contamination, either during sample collection (house dust or hair falling into the milk while the mother was hand-expressing a breast milk sample) or during sample preparation or analysis (contamination from laboratory dust). However, extensive data from our Pacific Northwest and California studies on quality control samples and multiple samples from the same mothers29,30 made contamination unlikely. In brief, >60 quality control samples and 140 multiple samples or separate measurements from mothers showed no unusual BDE-209 levels. These and other data supported this, as follows: 1) ∑(tri-hexa)PBDE levels in California breast milk samples varied 100-fold (9.601291 ng/g lw). This wide range of lowerbrominated PBDE levels suggests that California mothers can have great interindividual variability in exposures and/or uptake and transfer of PBDEs. This may include BDE-209. 2) Some California samples with high BDE-209 also had high BDE-153. Among the 5 California breast milk samples with high BDE-209 levels, 2 samples had BDE-209 as the dominant congener (35.1 ng/g lw, 47% of ΣPBDEs; and 55.3 ng/g lw, 39%), with BDE-153 as the second major congener (20% and 25%: levels close to, or exceeding, BDE-47; Figure 1). BDE-153 was the dominant congener in 5 other samples. High levels of BDE-209 and high proportions of BDE-153 are unusual. In our studies of over 250 samples of California marine wildlife (harbor seals, fish, shorebird eggs), BDE-209 levels were minimal and BDE-153 never exceeded BDE-47.12,44,45 However, in eggs from California urban peregrines (N = 31), BDE-209 was a major congener, and BDE-153 > BDE-47 in all 4581
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Figure 1. PBDE congener patterns in California breast milk samples.
3)
4)
Figure 2. Inverse correlation between proportions of BDE-153 and ΣBDE-47 þ 99 in California breast milk samples.
5)
samples.14 In contrast, BDE-209 levels were low in eggs from coastal peregrines, as were proportions of BDE-153. Thus, BDE-153 was the dominant congener only in eggs with high levels of BDE-209. Urban peregrine eggs had high levels of unusual nona- and octa-BDE congeners that are not in the deca-commercial mixtures, whose structures could arise from the stepwise (meta, meta) metabolic debromination of BDE209. That BDE-153, not BDE-47, was the dominant congener in urban eggs suggested that the BDE-153 was a further product of BDE-209 stepwise debromination.14,16 The same
6)
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may be true for the 5 samples of California breast milk with BDE-153 > BDE-47 (Figure 1). BDE-153 was inversely correlated with BDE-47 and -99. Our California results, and our previous Pacific Northwest data, are consistent with enzymatic debromination of BDE-153 to BDE-99 and -47. In California samples, the % fractions of BDE-153 were inversely correlated with the % fractions of 1) BDE-47 (r = 0.82); 2) BDE-99 (r = 0.46); or 3) BDE-47 plus -99 (r = 0.88) (Figure 2). A similar inverse correlation (BDE-153 vs BDE-47 plus -99: r = 0.94) was found in our Pacific Northwest breast milk study.29 No high BDE-209 levels were found in breast milk samples from Pacific Northwest (She et al. 2007). The Pacific Northwest study (n = 40) used the same collection protocols, sample preparation methods, and analytical instrumentation as the California study (n = 82), yet no anomalous BDE-209 levels were found. If the high BDE-209 levels in the California samples were artifacts of contamination during sample collection or in the laboratory, we might expect to find at least one high BDE-209 level in the Pacific Northwest samples. No high BDE-209 levels were found in any of multiple breast milk samples analyzed from the same California mothers: two samples each were analyzed from 38 mothers, and 7 samples each were analyzed from 9 mothers. The reproducibility of results seen here, and with lab duplicates and quality control data, argued against contamination occurring either during sample collection or analysis. High levels of BDE-209 were reported in breast milk samples from Belgium (max 34.7 ng/g lw)21 and Spain (max 52.0 ng/g lw).43 It was suggested that transfer of BDE209 to breast milk occurs when BDE-209 body burdens are high, possibly from ingestion of BDE-209-contaminated food and/or house dust.43 dx.doi.org/10.1021/es103881n |Environ. Sci. Technol. 2011, 45, 4579–4585
Environmental Science & Technology California Breast Milk: PBDE Levels of Concern? PBDE levels in California breast milk (median 53.3 ng/g lw) are much higher than levels (few ng/g lw) associated with congenital cryptorchidism in a DanishFinnish population22 and adverse birth outcomes (e.g., decreased birth weight)51 and irregular menstruation periods52 in a Taiwan population. Chao et al.52 reported that higher brominated PBDEs (e.g., BDE-209) in breast milk were associated with irregular menstruation periods. From our estimates of average daily PBDE intakes (ng/kg b.w./ day) by our breast-fed infants, we found that about 60% (48/82) of the California infants (median intake BDE-47 = 274 ng/kg b.w./ day; range 21.62039) exceeded U.S.EPA’s RfD for BDE-47 (100 ng/kg/day) for neurodevelopmental toxicity.53 Moreover, 7% of the California breast-fed infants ingested ∑tri-hexaPBDEs (20403559 ng/kg b.w./day) at levels exceeding the chronic oral reference dose (RfD) for liver toxicity (2000 ng/kg/day)54 for the commercial penta-BDE mixture (mainly composed of tetra-, penta-, hexaBDEs). Thus, infant exposure to PBDEs via breast milk consumption raises legitimate concerns about health outcomes for these breast-fed infants in the U.S. Pacific Northwest area and California. In summary, we found levels of PBDE contaminants in California samples to be among the highest in the world for breast milk. These levels are cause for concern, as most (60%) breast milk samples exceeded U.S. EPA’s RfD for BDE-47 (100 ng/kg/day) for neurodevelopmental toxicity. We confirmed that PBDEs levels in breast milk are approaching the levels of the legacy PCBs and suggest that the trend PBDE > PCB may increase as PBDEs continue to migrate from product to indoor and outdoor environments. Our data suggest that BDE-209 may transfer to breast milk and may break down in the mother and transfer to breast milk and the nursing infant as the lower-brominated PBDEs associated with adverse effects (e.g., neurodevelopmental deficits). Our results also send a cautionary note for the PBDE-replacement brominated flame retardants (e.g., BTBPE, DBDPE). Presently unregulated, these have chemical structures similar to BDE-209 and may transfer to the newborn via breast milk consumption. Although breastfeeding should be encouraged because of the well-documented beneficial effects,55,56 we must continue efforts to characterize contaminants in breast milk so that protective measures may be initiated, if necessary, to avoid potential harmful effects to the newborn. Further studies are underway to better understand the transfer pathways, temporal changes, and breakdown products of BDE-209 and the new alternative brominated flame retardants (BFRs). To this end, we are measuring BFRs in concurrently collected paired samples of breast milk and blood from California first-time mothers.
’ ASSOCIATED CONTENT
bS
Supporting Information. Experimental Section, Table S1 contains demographic characteristics of California and U.S. Pacific Northwest study populations, and Tables S2 and S3 list concentrations of PBDEs and PCBs (ng/g lipid wt) in California breast milk samples (n = 82). This material is available free of charge via the Internet at http://pubs.acs.org.
’ AUTHOR INFORMATION Corresponding Author
*Phone: (510)540-2441. Fax: (510)540-2305. E-mail: jpark@ dtsc.ca.gov.
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’ ACKNOWLEDGMENT The study was partially supported by U.S.EPA Region IX Pollution Prevention Grant # NP979442010. We thank the California first-time mothers who donated breast milk samples and participated in this study. The views expressed herein are those of the authors and do not necessarily reflect those of the Department of Toxic Substances Control, California Environmental Protection Agency. ’ REFERENCES (1) Harrad, S.; de Wit, C. A.; Abdallah, M. A.; Bergh, C.; Bjorklund, J. A.; Covaci, A.; Darnerud, P. O.; de Boer, J.; Diamond, M.; Huber, S.; Leonards, P.; Mandalakis, M.; Ostman, C.; Haug, L. S.; Thomsen, C.; Webster, T. F. Indoor contamination with hexabromocyclododecanes, polybrominated diphenyl ethers, and perfluoroalkyl compounds: an important exposure pathway for people?. Environ. Sci. Technol. 2010, 44 (9), 3221–31. (2) Vonderheide, A. P.; Mueller, K. E.; Meija, J.; Welsh, G. L. Polybrominated diphenyl ethers: Causes for concern and knowledge gaps regarding environmental distribution, fate and toxicity. Sci. Total Environ. 2008, 400 (13), 425–36. (3) Darnerud, P. O. Toxic effects of brominated flame retardants in man and in wildlife. Environ. Int. 2003, 29 (6), 841–53. (4) Martin, P. A.; Mayne, G. J.; Bursian, F. S.; Tomy, G.; Palace, V.; Pekarik, C.; Smits, J. Immunotoxicity of the commercial polybrominated diphenyl ether mixture DE-71 in ranch mink (Mustela vison). Environ. Toxicol. Chem. 2007, 26 (5), 988–97. (5) Toschik, P. C.; Rattner, B. A.; McGowan, P. C.; Christman, M. C.; Carter, D. B.; Hale, R. C.; Matson, C. W.; Ottinger, M. A. Effects of contaminant exposure on reproductive success of ospreys (Pandion haliaetus) nesting in Delaware River and Bay, USA. Environ. Toxicol. Chem. 2005, 24 (3), 617–28. (6) Viberg, H.; Fredriksson, A.; Eriksson, P. Neonatal exposure to polybrominated diphenyl ether (PBDE 153) disrupts spontaneous behaviour, impairs learning and memory, and decreases hippocampal cholinergic receptors in adult mice. Toxicol. Appl. Pharmacol. 2003, 192 (2), 95–106. (7) Viberg, H.; Johansson, N.; Fredriksson, A.; Eriksson, J.; Marsh, G.; Eriksson, P. Neonatal exposure to higher brominated diphenyl ethers, hepta-, octa-, or nonabromodiphenyl ether, impairs spontaneous behavior and learning and memory functions of adult mice. Toxicol. Sci. 2006, 92 (1), 211–8. (8) Schreiber, T.; Gassmann, K.; Gotz, C.; Hubenthal, U.; Moors, M.; Krause, G.; Merk, H. F.; Nguyen, N. H.; Scanlan, T. S.; Abel, J.; Rose, C. R.; Fritsche, E. Polybrominated diphenyl ethers induce developmental neurotoxicity in a human in vitro model: evidence for endocrine disruption. Environ. Health Perspect. 2010, 118 (4), 572–8. (9) Darnerud, P. O.; Eriksen, G. S.; Johannesson, T.; Larsen, P. B.; Viluksela, M. Polybrominated diphenyl ethers: occurrence, dietary exposure, and toxicology. Environ. Health. Perspect. 2001, 109 (Suppl 1), 49–68. (10) Daniels, J. L.; Pan, I. J.; Jones, R.; Anderson, S.; Patterson, D. G., Jr.; Needham, L. L.; Sjodin, A. Individual characteristics associated with PBDE levels in U.S. human milk samples. Environ. Health Perspect. 2010, 118 (1), 155–60. (11) Schecter, A.; Colacino, J.; Sjodin, A.; Needham, L.; Birnbaum, L. Partitioning of polybrominated diphenyl ethers (PBDEs) in serum and milk from the same mothers. Chemosphere 2010, 78 (10), 1279–84. (12) She, J.; Petreas, M.; Winkler, J.; Visita, P.; McKinney, M.; Kopec, D. PBDEs in the San Francisco Bay Area: measurements in harbor seal blubber and human breast adipose tissue. Chemosphere 2002, 46 (5), 697–707. (13) Petreas, M.; She, J.; Brown, F. R.; Winkler, J.; Windham, G.; Rogers, E.; Zhao, G.; Bhatia, R.; Charles, M. J. High body burdens of 2,20 ,4,40 -tetrabromodiphenyl ether (BDE-47) in California women. Environ. Health Perspect. 2003, 111 (9), 1175–9. 4583
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