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Chemosphere
PBDEs and PBBs in human serum and breast milk from cohabiting UK couples
Lindsay Bramwella'*, Alwyn Fernandes b, Martin Rose b, Stuart Harradc, Tanja Pless-Mullolia
a Institute of Health and Society, Medical Faculty, Newcastle University, Newcastle upon Tyne NE2 4AX, UK b Food and Environment Research Agency, Sand Hutton, York YO41 1LZ, UK
c Birmingham University, School of Geography, Earth & Environmental Sciences, Birmingham B15 2TT, UK
HIGHLIGHTS
• UK body burdens of tri to deca PBDE and PBB are reported.
• Paired male and female serum, and female serum and breast milk were measured.
• These are the first UK serum data since EU restrictions on PBDEs.
• A small reduction in median J^PBDE3-7 UK serum levels are indicated.
• Estimated infant intakes are amongst the highest in the EU for BDEs-47 and -99.
ARTICLE INFO ABSTRACT
Concentrations of PBDEs and PBBs were measured in matched blood and breast milk samples from 10 UK couples collected in 2011-12. These data are the first measurements in human serum from the UK since the 2004 EU ban on all uses of the penta-and octa-BDE formulations and the 2008 ban on the use of the deca-BDE formulation in some applications. Serum J^PBDE tri-hepta concentrations ranging from 1.0 to 16 ng g 1 lipid weight, with median 4.0 ng g 1 lw were measured. Breast milk J^PBDE tri-hepta concentrations ranged from 1.3 to 21 ng g 1 lw, with median 5.7 ng g 1 lw. Couples had similar serum congener concentrations unless one of them frequently stayed away from home for work (different diet and dust exposures) or one had occupational exposure to foams and furnishings or electronics. BB-153 were measured above LOD in 40% of sera and 100% of breast milks samples, with median concentrations of 0.04 and 0.06, and maximums of 0.91 and 0.79 ngg 1 lw respectively. Concentrations in this study indicated a modest decrease from pre-ban levels reported for the UK. BDE-209 was detected above the limit of detection (LOD) in 15% of sera and 83% of breast milks, with ranges <1.2-20 and <0.2-1.0 ngg 1 lw respectively. Average daily infant intakes were estimated at 17, 5, 5 and 3 ng kg 1 bw for BDE-47,-99,-153 and -209 respectively, all well below relevant US-EPA threshold reference dose values (RfDs). © 2014 The Authors. Published by Elsevier Ltd. This is an open access article under the CC BY license (http://
creativecommons.org/licenses/by/3.0/).
Article history:
Received 14 November 2013 Received in revised form 10 March 2014 Accepted 12 March 2014 Available online xxxx
Handling Editor: H. Fiedler
Keywords:
1. Introduction
Polybrominated diphenyl ethers (PBDEs) and polybrominated biphenyls (PBBs) are classes of flame retardant that have been used to meet fire safety regulations for fabrics, furnishings, electronics and vehicles since the 1970s. PBDEs are additive flame retardants that are mixed into plastics or foam, or sprayed onto fabrics, without forming chemical bonds with the material. During the use and lifetime of the product, PBDEs may migrate from the material (Sjodin et al., 2003). PBDEs are now ubiquitous in indoor air and
* Corresponding author. Tel.: +44 191 208 5673. E-mail address: lindsay.bramwell@ncl.ac.uk (L. Bramwell).
dusts (Harrad et al., 2010) and transfer into the wider environment and food chains (Harrad and Diamond, 2006).
PBBs are another group of brominated flame retardants similar in structure, use, manufacture, contamination pathways and toxi-cological impact to PCBs. Production in the USA ceased following the Michigan Firemaster incident of 1973 where PBB was accidentally introduced into animal feed. Their use as flame retardants in textiles was banned in the EU where they have not been used or manufactured since 1996.
In 1999, Merionyte et al. noted a marked increase in concentrations of PBDEs in the breast milk of Swedish women with levels doubling approximately every four years (Meironyte et al., 1999).This triggered a global interest in human body burden and
http://dx.doi.org/10.1016/j.chemosphere.2014.03.060 0045-6535/© 2014 The Authors. Published by Elsevier Ltd.
This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/3.0/).
L. Bramwell et al. /Chemosphere xxx (2014) xxx-xxx
exposure to PBDEs and investigations into their persistence in humans and the environment. Inhalation and ingestion of indoor dust and food are potential pathways of exposure to PBDEs. Mother to child transfer of PBDEs occurs during breast feeding (Guvenius et al., 2003; Carrizo et al., 2007). Potential adverse human health effects of PBDE exposure and body burden are reproductive toxicity, neurotoxicity and immune effects (Darnerud et al., 2001; Meeker et al., 2009; Gascon et al., 2012; Eskenazi et al., 2013). Evidence of PBDE concentrations in indoor dusts and air in the UK has grown in recent years (Santillo et al., 2003; Harrad et al., 2004, 2006, 2008a,b,c; Harrad and Hunter, 2006; Sjodin et al., 2008a; Harrad and Abdallah, 2011) but few data are available regarding resultant UK human body burdens. It is widely accepted that PBDEs have long half-lives in humans but, even for the same congener, estimates of these values vary widely. There is a general trend of shorter half-lives for the more brominated compounds. Penta- and octa-BDE were banned from use in the EU in 2004 (EU, 2004) with use of deca-BDE in electronics and electrical goods also banned in 2008 (EU, 2008).
1.1. Aim
The aims of this study were to investigate (a) levels of PBDE and PBBs in the sera of co-habiting UK couples, and (b) paired sera and breast milk samples for nursing female partners. Measurements were compared with previous UK data collected prior to the implementation of EU restrictions on the manufacture and use of PBDEs (EU, 2004, 2008). Concentrations of PBDEs in human milk were used to derive estimated infant intakes of tri- to deca-PBDEs.
2. Materials and methods
Paired serum and breast milk samples were obtained from volunteer couples living in the north east of England as part of a wider in-depth study into potential human exposure sources and uptake of PBDE and emerging brominated contaminants. The wider study matches indoor dust and 24 h duplicate diet samples with these serum and breast milks as well as room surveys, diaries and exposure questionnaires, the results of which will be reported later. Sampling was undertaken between April 2011 and February 2012. Ten couples took part in the study and women from six of the couples provided breast milk samples.
2.1. Volunteer recruitment
We aimed to recruit individuals with a range of occupations and diets to reflect low, medium and high exposure to PBDEs, such as workers in electronics, soft furnishings or transport and outdoor workers, oily fish eaters and vegetarians. A short pre-screening questionnaire identified volunteers that would provide the optimum range of exposures. Recruitment was via local universities, local authorities, hospitals, playgroups and breast feeding groups. 79 couples completed the pre-screening questionnaires in 2011. 10 couples were invited, and agreed, to participate in the full study week. Of these 10 couples, two repeated the sampling week as a validation of the method. Inclusion in the study required the participants to be over 18 years of age and to have six months or more of domestic and occupational stability. Volunteers gave written informed consent prior to participation. Ethical approval for the study was provided by the NHS National Research Ethics Committee North East, Durham and Tees Valley, the Newcastle upon Tyne Hospitals NHS Foundation Trust, Newcastle University's Research Ethics Committee and the Food and Environment Research Agency's Ethics Committee.
2.2. Sample collection
Volunteers visited the Clinical Research Facility (CRF) at the Royal Victoria Infirmary at Newcastle to provide 60 mL fasted blood, sampled in the morning of the 8th day of the wider study. Physical measurements, such as body mass index (BMI), were also recorded at the CRF. Where a breast milk sample was provided, P50 mL milk was collected by the volunteer by either pump or manual expression up to 12 h before and 24 h after provision of the blood sample. Blood samples were collected in 6 x 10 mL redtop vacutainers, allowed to coagulate for 20 min, then centrifuged at 1000 rpm to separate the serum which was frozen to -18 °C and stored at the CRF laboratory until analysis. Breast milk samples were collected in Nalgene bottles and stored at -18 °C until transport with the sera samples to the Food and Environment Research Agency (Fera) Laboratories, York, UK for analysis. A set of unused sampling equipment was collected as field blanks in case sample results indicated a potential contamination source, however this was not required. Two couples repeated the sampling week, with sampling points 6.5 and 7.5 months apart. This provided a longitudinal element to the study.
2.3. Laboratory analyses
Details of the methods used for sample preparation, extraction, clean up and analysis of PBDEs and PBBs by high resolution GC MS are described elsewhere (Fernandes et al., 2004 and Fernandes et al., 2008). The performance characteristics of the methodology, including QA parameters such as limits of detection (LODs), precision, linear range of measurement, recoveries etc. have been reported earlier (Fernandes et al., 2008). Further confidence in the data is provided by regular and successful participation in inter-comparison schemes such as POPs in Food 2012 (Bruun Bremnes et al., 2012). The following congeners were measured: BDEs-17, -28, -47, -49, -66, -71, -77, -85, -99, -100, -119, -126, -138, -153, -154, -183 and -209 and PBBs -49, -52, -80, -101, -153 and -209. Lipid determination was carried out by West Yorkshire Analytical Services, Leeds, using the IS017025 accredited Werner-Schmidt method; acid hydrolysis and solvent extraction.
2.4. Data analysis
Data were normalised to ng g-1 lipid for serum and breast milk to enable comparison between matrices and with previous studies. Descriptive statistics were calculated for both lower bound (LB) and upper bound (UB) data, where concentrations <L0D are treated as 0 and the LOD respectively.
2.5. Statistical analysis
Due to the small sample size statistical analyses were mostly descriptive. Statistical analyses were carried out using lower bound data, in keeping with previous UK serum data (Thomas et al., 2006). The analyses used IBM SPSS Statistics for Windows, Version 21.0. Armonk, NY: IBM Corp. Spearman's correlation coefficients were determined between individual and sum congeners and age, BMI, waist-hip ratio, total months breast feeding and parity. The Mann Whitney U test was used to determine any serum differences between males and females, urban and rural inhabitants and different diets.
2.6. Infant intake estimations
Nursing infants' intakes of PBDEs were estimated by multiplying age-appropriate estimated mean daily lipid intakes per kg bodyweight by the lipid weight concentrations of PBDE congeners
L. Bramwell et al. /Chemosphere xxx (2014) xxx-xxx
for each breast milk sample. The EFSA mean daily intake scenarios used were for a three months old infant (body weight 6.1 kg) with average intake of 800 mL and higher intake 1200 mL. Whole weight PBDE and PBB concentrations were used for the calculations.
2.7. Risk assessment
Estimated BDE-47, -99 and -153 exposures were compared with the corresponding threshold reference dose (RfD) suggested by the US-EPA to determine whether the PBDE infant intakes estimated for this study might be associated with any toxicological endpoints. RfDs are an estimate of oral daily human exposure to a chemical at no-observed-adverse, non-carcinogenic effects levels (NOAEL). For these PBDEs the endpoints considered by the US-EPA are neurodevelopmental toxicological effects. The daily exposures considered were BDE-47 (100ngkg-1) (US-EPA, 2006b), BDE-99 (100ngkg-1) (US-EPA, 2006a) and BDE-153 (200 ng kg-1) (US-EPA, 2006c).
3. Results
Serum PBDE tri-hepta concentrations ranged from 1.0 to 16 ngg-1 lipid weight (lw), with a median concentration of 4.0 ng g-1 lw. BDE-209 was detected above the LOD in 15% of samples, with a maximum of 19.8 ngg-1 lw. Breast milk ]TPBDE tri-hepta concentrations ranged from 1.3 to 21 ng g-1 lw, with a median concentration of 5.7 ng g-1 lw. BDE-209 was detected in 83% of breast milk samples with a maximum of 1.04 ngg-1 lw. BDE-47 was usually the most abundant congener present in sera in this study, making up 40% (median) of the PBDE tri-hepta. This was followed by BDE-99 (20%), BDE-153 (9%), BDE-66 (6.5%) then BDE-100 (3.7%) and BDE-49 (2.9%). In samples where BDE-209 was measured above LOD (15% detection rate) this congener comprised 40% (median) of the PBDE. Results for PBDE congener concentrations in individual serum samples from couples 1 to 10 are presented in Fig. 1. Repeat samples for couples 1 and 2 are also depicted. A summary of the serum data (not including repeat samples for couples 1 and 2) and breast milk data is presented in Table 1, including sums of all BDEs measured ( PBDE), all BDEs measured excluding BDE-209 (pPBDE tri-hepta), BDE-47, -99, -100, -153, -154 and -183 (PPBDE(6)), BDEs-47, -99 and -153 (PPBDE(3)). Individual concentrations are provided in supplementary data (Tables S-1 and S-2). BB-153 was the only PBB detected above the LOD in sera in this study (40% detection rate). BB-153 was
detected in 100% of breast milk samples and BB-101 in one sample. PBB measurements are included in Table 1 and both supplementary data Tables S1 and S2.
A significant negative association was found between ]TPBDE in serum and age (Spearman's rho r = -0.55, p = 0.01), but the association with breast milk and age was not significant (r = 0.09, p = 0.87). The associations between ]TPBDE in serum and BMI (r = -0.03, p = 0.89) or body fat mass (r = -0.07, p = 0.78) were not found to be significant and neither were PBDE in breast milk and BMI (r = 0.09, p = 0.87). For both congeners BDE-49 and BDE-66 in breast milk, the same significant positive association was noted with BMI (r = 0.845, p = 0.03). Significant negative associations were found for individual congeners in serum with waist-hip ratio (WHR); BDE-28 (r = -0.46, p = 0.04); BDE-153 (r = -0.47, p = 0.04). Parity was found to have a significant negative association with PBDE in females' serum (r = -0.67, p = 0.04) and serum BDE-153 (r = -0.69, p = 0.03). Associations between pPBDE in breast milk and parity (r = -0.29, p = 0.57) or total months breastfeeding (r = -0.26, p = 0.62) were weaker. However, significant negative associations were found between total months breastfeeding and serum BDE-49 (r = -0.67, p = 0.04). Lipid normalised pPBDE data indicated that males had higher PBDE body burdens than their corresponding female partners (7/10 cases). The median concentration of £PBDE tri-hepta in males (4.6 ng g-1 lipid) was higher than that for females (3.5 ng g-1 lipid). However, the difference was only significant for BDE-153 (p = 0.03), with a weaker association with BDE-209 (p = 0.7). A weak association was found between sera PBDE and having a home in an urban or rural environment (p = 0.32). For the two couples who provided two serum samples, differences between PBDE or PBB congener concentrations from the first and second samples were not generally significant, except for increases in BDE-28 (p = 0.02) and BDE-47 (p = 0.04).
4. Discussion
This 2011/12 study documents UK serum and breast milk data for PBDEs and PBBs. A modest decrease in UK serum PBDE concentrations since the EU bans was found. Compared to earlier studies, participants were recruited from as wide a pool of socio-economic class, occupation, diet and location as possible, with great focus on the detail of information collected for each individual. The small number of participants and the focus on breastfeeding mothers means, however, that results are not representative of all UK residents' exposures.
FFMM FFMM FM FM FM FM FM FM FM FM Fig. 1. Individual UK serum PBDE concentrations (ngg-1 lw) for congeners with detection rate p50%: BDE-47, -99, -100, -153, -183.
Table 1
Summary of selecteda PBDE and PBB body burden concentrations for all study participants (ng g-1 lw).
Congener Serum (n = 20) Breast milk (n = 6)
Median Range % > LOD Median Range % > LOD
LBh ÜB1 Min Max LBh ub' Min Max
BDE-28 0.04 0.12 <0.03 0.55 55 0.09. 0.091.92 0.02 0.31 100
BDE-47 0.63 1.582 <0.36 4.87 60 1.92 1.92 0.32 13.09 100
BDE-49 0.06 0.12 <0.03 0.65 60 0.03 0.03 <0.02 <0.11 67
BDE-66 0.05 0.26 <0.03 0.79 55 0.03 0.03 <0.03 0.13 67
BDE-85 0.02 0.05 <0.02 0.26 50 0.04 0.04 <0.01 0.35 83
BDE-99 0.79 0.79 <0.26 5.61 70 0.88 0.88 0.12 3.74 100
BDE-100 0.15 0.15 <0.03 0.57 80 0.64 0.64 0.07 2.19 100
BDE-153 0.37 0.37 0.12 4.05 100 1.01 1.01 0.70 1.68 100
BDE-138 <LOD 0.07 0.03 0.19 5 0.02 0.02 <0.01 0.04 67
BDE-154 <LOD 0.06 <0.02 0.38 35 0.07 0.07 0.01 0.18 100
BDE-183 0.05 0.07 <0.03 0.33 60 0.05 0.05 0.02 0.23 100
BDE-209 <LOD 3.27 <1.24 19.80 15 0.52 0.54 <0.20 1.04 83
BB-153 <LOD 0.04 <0.01 0.91 40 0.08 0.08 0.06 0.79 100
pPBDEsb 2.41 8.32 2.25 35.41 5.59 5.67 1.28 22.02
X]PBDEtri-heptac 2.41 4.03 1.01 15.61 4.76 4.84 1.28 21.03
pPBDE(6)d 2.23 3.12 0.80 12.82 4.59 4.59 1.25 20.09
£PBDEme 1.98 2.85 0.73 11.53 3.88 3.88 1.14 5.89
X]PBBtri-hepta <LOD 0.37 <0.04 1.60 0.08 0.17 0.06 0.81
pPBBg <LOD 0.74 <0.09 2.27 0.08 0.22 0.06 0.86
Sample fat % 0.43 0.43 0.25 0.93 2.61 2.61 0.97 4.56
a Where % > LOD is over 15% for either serum or breast milk (BDE-17, -71, -77, -119, -126, and PBB-15, -49, -52, -80, -101, 209 measured but not reported here). b Sum of all PBDE congeners measured. c Sum of all PBDE congeners measured except BDE-209. d Sum of BDE-47, -99, -100, -153, -154 and -183. e Sum of BDE-47, -99 and -153. f Sum of all PBB congeners measured except BB-209. g Sum of all PBB congeners measured. h Lower bound data. i Upper bound data.
The finding of a significant negative association of ]TPBDE in serum and age was in line with some previous studies with greater age range of adult participants (Fromme et al., 2009; Gari and Gri-malt, 2013; Shi et al., 2013). A non-significant negative association was found with PBDE in serum and BMI in keeping with Jain who found PBDE-153 and PBB-153 to be negatively associated, (Jain, 2013) and in contrast to Fitzgerald et al. who found a significant positive association (Fitzgerald et al., 2010). The present finding that serum BDE-153 was significantly higher for males was in contrast to the two earlier studies of cohabiting couples where gender differences were found not to be significant (Gomara et al., 2007; Fromme et al., 2009).
To the authors' knowledge, the only previous published UK PBDE study is provided by Thomas et al., from samples collected in 2003. This study had 154 participants from thirteen locations across the mainland, including some from the general area of this study. Thomas et al. suggested that their 154 volunteers were not representative of the general UK population as they had a higher proportion of women (68%) and vegetarians (12%) and that
sampling on weekdays might select against people in work. They noted that the majority of mothers in their cohort breastfed, which was also found in this study. This study had only one vegetarian (5%). The median age was 37 years (range 26-43), Thomas et al.'s being 41 (range 22-80). The median BMI was 26 (range 22-33) for this study, Thomas et al.'s being 23 (18-43). Technological advances have reduced the LOD for analyses since 2003, most significantly for BDE-209. By considering ratios of data provided by Thomas et al. and the equivalents from this study, indicators of potential changes in UK body burdens were gauged. The data and ratios are presented in Table 2. All median congener concentrations for this study were lower than those reported by Thomas et al. except for BDE-99, where the measurements were very similar. It is likely that significant reductions would take time to manifest due to the long life of PBDE-containing items such as household and office soft furnishings and electronics. The maximum concentrations for individual congeners in 2003 were considerably higher (~50 times) than those in our study (2011/12). The absence of similar high maximum values in this study may indicate a downward shift
Table 2
Comparison of serum PBDE content between UK studies (ng g_1 lw).
Thomas et al. (2006) 2003 data This study, 2011 data Ratio medians 2003/2011
Median LB (ng g_1 lw) Range (ng g_1 lw) % Detects Median LB (ng g_1 lw) Range (ng g_1 lw) % Detects
BDE 28 <0.14 <0.14-10 27 0.04 <0.03-0.55 55
BDE 47 0.82 <0.30-180 68 0.63 <0.36-4.87 60 1.26
BDE 99 0.76 <0.16-150 41 0.79 <0.26-5.61 70 0.96
BDE 100 <0.16 <0.17-390 92 0.15 <0.03-0.57 80
BDE 153 1.7 <0.26-87 99 0.37 0.12-4.05 100 4.72
BDE 154 0.6 <0.15-4.4 86 <LOD <0.12-0.38 35 5.45
BDE 183 0.3 <0.14-1.8 55 0.05 <0.03-0.33 60 2.73
BDE 209 <15 <15-240 7 <LOD <1.24-19.8 15
pPBDE 5.6 0.63-420 100 2.408 2.25-35.41 100 3.13
% Fat 0.426 0.25-0.93
L. Bramwell et al. /Chemosphere xxx (2014) xxx-xxx
in the distribution of exposure within the UK population, but a more representative study is needed to fully evaluate this hypothesis.
Medians and ranges for BDE-47, -99, -100 and -153 in sera for this study are presented alongside examples from Europe, Asia and North America in Fig. 2. These examples are for studies that include data for men and women together, and where occupational exposure was not targeted. Human body burdens in North America are approximately one to two orders of magnitude higher than those found elsewhere in the developed world. This may be explained by the history of flame retardant regulations in the USA and California in particular (Shaw et al., 2010). The UK has more stringent flame retardant furnishings regulations than mainland Europe (EFRA, 2011) and the highest reported indoor dust BDE-209 concentrations in Europe (Harrad et al., 2008a). However, there is currently no evidence to suggest that penta- BDE use has been any higher in the UK than in mainland Europe. Median results for this study and previous UK figures indicate that BDE-209 and BDEtri to hepta levels sit at the mid to lower end of European data (Thomas et al., 2006; Gomara et al., 2007; Antignac et al., 2009; Frederiksen et al., 2009; Fromme et al., 2009; Roosens et al., 2009). Maximum UK values reported by Thomas et al. are similar to those from the USA, indicating that some UK individuals have had higher PBDE exposure.
To the authors' knowledge, data presented here are the first UK PBB data for both human sera and breast milk. Previous studies with such PBB measurements have often been focused around the Michigan incident and its legacy. General population exposures were sought for comparison with the present results and are shown in Table 3. The median serum BB-153 concentration of 0.04 ngg-1 lw (range< 0.01-0.9) for this study, is almost two
Table 3
Median concentrations of BB-153 (ng g-1 lw) in human serum samples from different countries.
Location Year Number BB-153 Reference Note
UK 2011- 20 0.04 This study (Range)
12 (<0.01-0.9)
China 2009- 21 0.024 Yang et al. Geometric mean
10 (2013) (gm)
China* 2009- 35 0.52 Yang et al. e waste
10 (2013) dismantlers (gm)
Greenland 2002- 99 1.2 Lenters et al. gm
4 (2013)
Poland and 2002- 200 <LOQ Lenters et al.
Ukraine 4 (2013)
Northwest 2004 2062 3.3 (1.4- Sjödin et al. NHANES
USA 5.5) (2008b)
* Occupationally exposed cohort.
Table 4
Comparison of median (range) PBDE measurements in UK breast milks (ng g-1 lw).
Study Number Year Sum PBDE BDE-209
tri-hepta
2011-12 5.7 (1.3-21.0) 0.5 (0.2-1.0)
2009 5.0(0.2-26.1)a 0.3 (0.1-0.9)
2000-2 6.4 (0.7-19.3)
2001-3 6.6 (0.3-69.0)
a tri-hexa
This study Abdallah and Harrad (2014) D'Silva (2005)
Kalantzi et al. (2004)
10 Pooled
groups
Fig. 2. Median levels and ranges (minimum-maximum) of major PBDE congener concentrations in serum for this and some previous studies of general populations. bKalantzi et al. (2011), cFromme et al. (2009), dZhu et al. (2009), eButtke et al. (2013), 'Sjodin et al. (2008b).
Table 5
Comparison of mean daily infant intake estimations (ng kg-1 bw).
Average daily consumption scenario 800 mL High daily consumption scenario 1200 mL
BDE 47 BDE 99 BDE153 BDE 209 BDE 47 BDE 99 BDE153 BDE209
UK, This study (n = 6) 2012a 17 5 5 3 26 8 8 4
EU, EFSA (24 EU studies)" 0.6-14 <0.1-5 0.5-11 1.0-13 1.0-21 <0.1-8 0.7-17 1.0-20
China, Shi et al. (n = 103) 2013c 64 41 6 13 1109
NZ, Coakley et al. (n = 33) 2013d 11 3 3
UK, Abdallah and Harrad (n = 28) 2009e 19.3 4.2 6.5 1.8
UK, Kalantzi et al. (n = 54) 2003b 14 4 6
a Intakes are calculated for the scenario of a three month old infant weighing 6.1 kg using whole weight breast milk data. b EFSA (2011) Intakes are calculated for the scenario of a three month old infant weighing 6.1 kg and assuming breast milk to contain 3.5% lipid. c Shi et al. (2013) estimated daily maximums and a mean of 64 for BDE-209. d Coakley et al. (2013) estimated daily median exposures.
e Abdallah and Harrad (2014) estimated the mean exposure for a 1 month old infant weighing 4.14 kg and consuming 24.4 g lipid day-1.
orders of magnitude below those found in the North American and Inuit studies.
PBDE concentrations in breast milk samples for this study were very similar to the two previous UK studies and current Birmingham UK study (Abdallah and Harrad, 2014). Data for comparison are presented in Table 4. A slight reduction in the median ]rPBDE3-7 may be indicated by the two most recent studies. BDE-209 was measured in 28 breast milk samples collected from women in Birmingham, UK in 2009 with a median concentration of 0.25 and a range <0.06-0.92 ng g-1 lw (71%>LOQ) (Abdallah and Harrad, 2014). These are broadly consistent with those reported in this study, where the median concentration of BDE-209 was 0.54 ngg-1 lw (range < 0.20-1.04 ng g-1 lw).
Although a significant negative association was found with PBDE in females' serum and parity, the association with breast milk was negative but not significant. Of the six women who provided breast milk samples for this study, three were primiparus and three were feeding their second child. Parity has been reported to have a decreasing association with PBDE levels in breast milk (Kang et al., 2010). For all women in the study, total breastfeeding time prior to blood and breast milk sampling for this study ranged from 0 to 60 months, with a median of 10 months. Although a significant negative association was found between total months breastfeeding and BDEs-49 and -153 in females' serum, the negative associations between PBDEs or PBBs in breast milk and breast feeding were not found to be significant. Significant associations were found between BDE-49 and BDE-66 in breast milk and BMI in contrast with earlier studies that found no significant association between BMI and pPBDE in breast milk (Chao et al., 2010; Thomsen et al., 2010). The positive association found between age and BDE-153 in breast milk was not significant, although earlier studies have reported that the association is significant (Koh et al., 2010; Lignell et al., 2011) and increased PBDE levels in breast milk with age has been reported (Chao et al., 2010). The breast feeding mothers' median age in this study (35 years, range 2739) was older than earlier studies by Koh et al. (30.5 years), Lignell et al. (mean 28.7, range 19-41), Chao et al. (30.1, range 22-42), and Kalantzi et al. (range 24-34). In a study of UK breast milk sampled in 2003, the participants were from Lancaster (a small city in rural north-west UK) and London (Kalantzi et al., 2004). Kalantzi et al.'s London participants were found to have higher PBDE body burdens suggesting higher concentrations in individuals residing in larger cities. This study also noted a positive association between breast milk ]TPBDE and urban living, although the difference was not found to be significant.
4.1. Infant intake via breast milk
The infant intake estimations in this study used the average (800 mL) and high (1200 mL) daily consumption scenarios used
by the European Food Safety Authority (EFSA, 2011), and are presented in Table 5. Whole weight breast milk PBDE concentrations were used for calculations. EFSA intakes are calculated for the scenario of a three month old infant weighing 6.1 kg and assuming breast milk to contain 3.5% lipid. Lipid content in breast milk samples for this study ranged from 0.97% to 4.56% (median 2.61%). Estimated mean daily infant exposures of BDE-47,-99, -153 and -209 for earlier UK studies and some comparable data from the Europe, China and New Zealand are also presented in Table 4. The estimates in this study are very similar to the most recent UK estimates (Abdallah and Harrad, 2014). BDE-47 and -99 estimates are towards the top end of the EFSA EU data whilst BDE-153 and -209 are more central. The infant intake estimations for BDE-47, -99 and -153 in this study were compared with corresponding US-EPA RfDs. Maximum values for high infant consumption for this study were well within US-EPA guidelines. A NOAEL range of 18.841.4 ng kg-1 bw for BDE-99 has also been proposed (Bakker et al., 2008). The maximum estimate of daily exposure to BDE-99 (20 ng kg-1 bw) in this study is at the low end of this NOAEL. This limited assessment indicates that BDE-47, -99 and -153 in UK breast milk are unlikely to raise health concerns.
5. Conclusions
Evidence of current UK body burdens of PBDEs and PBBs is reported. Although the study is limited in size, it was found that the EU penta- and octa-BDE bans have yet to translate into substantial reductions in internal exposure of the UK population. Little or no reduction in breast milk levels since 2003 has been found.
Acknowledgements
This study was funded by the UK's Natural Environment Research Council (NERC): CASE studentship NE/F014139/1, the Institute of Health and Society, Newcastle University, UK and the Food and Environment Research Agency (Fera). Thanks are also given to the study participants.
Appendix A. Supplementary material
Supplementary data associated with this article can be found, in the online version, at http://dx.doi.org/10.1016/jj.chemosphere. 2014.03.060.
References
Abdallah, M.A.-E., Harrad, S., 2014. Polybrominated diphenyl ethers in UK human milk: implications for infant exposure and relationship to external exposure. Environ. Int. 63,130-136. Antignac, J.-P., Cariou, R., Zalko, D., Berrebi, A., Cravedi, J.-P., Maume, D., Marchand, P., Monteau, F., Riu, A., Andre, F., Le Bizec, B., 2009. Exposure assessment of
French women and their newborn to brominated flame retardants: determination of tri- to deca-polybromodiphenylethers (PBDE) in maternal adipose tissue, serum, breast milkand cord serum. Environ. Pollut. 157,164-173.
Bakker, M.I., De Winter-Sorkina, R., De Mul, A., Boon, P.E., Van Donkersgoed, G., Van Klaveren, J.D., Baumann, B.A., Hijman, W.C., Van Leeuwen, S.P.J., De Boer, J., Zeilmaker, M.J., 2008. Dietary intake and risk evaluation of polybrominated diphenyl ethers in the Netherlands. Mol. Nutr. Food Res. 52, 204-216.
Bruun Bremnes, N., Smastuen Haug, L., Broadwell, S.L., Becher, G., 2012. Interlaboratory Comparison on POPs in Food 2012. Norwegian Institute of Public Health.
Buttke, D.E., Wolkin, A., Stapleton, H.M., Miranda, M.L., 2013. Associations between serum levels of polybrominated diphenyl ether (PBDE) flame retardants and environmental and behavioral factors in pregnant women. J. Expo. Sci. Environ. Epidemiol. 23, 176-182.
Carrizo, D., Grimalt, J.O., Fito, N.R., Sunyer, J., Torrent, M., 2007. Influence of breastfeeding in the accumulation of polybromodiphenyl ethers during the first years of child growth. Environ. Sci. Technol. 41, 4907-4912.
Chao, H.A., Chen, S.C.C., Chang, C.M., Koh, T.W., Chang-Chien, G.P., Ouyang, E., Lin, S.L., Shy, C.G., Chen, F.A., Chao, H.R., 2010. Concentrations of polybrominated diphenyl ethers in breast milk correlated to maternal age, education level, and occupational exposure. J. Hazard Mater. 175, 492-500.
Coakley, J.D., Harrad, S.J., Goosey, E., Ali, N., Dirtu, A.-C., Van den Eede, N., Covaci, A., Douwes, J., Mannetje, A.t., 2013. Concentrations of polybrominated diphenyl ethers in matched samples of indoor dust and breast milk in New Zealand. Environ. Int. 59, 255-261.
Darnerud, P.O., Eriksen, G.S., Johannesson, T., Larsen, P.B., Viluksela, M., 2001. Polybrominated diphenyl ethers: occurrence, dietary exposure, and toxicology. Environ. Health Perspect. 109, 49-68.
D'Silva, K., 2005. Brominated Organic Micro-pollutants in Food and Environmental Biota. School of Earth and Environment. University of Leeds.
EFRA, 2011. Keeping Fire in Check. European Flame Retardants Association.
EFSA, 2011. Panel on contaminants in the food chain (CONTAM): scientific opinion on polybrominated diphenyl ethers (PBDEs) in food. EFSA J. 9 (5), 2156-2430.
Eskenazi, B., Chevrier, J., Rauch, S.A., Kogut, K., Harley, K.G., Johnson, C., Trujillo, C., Sjodin, A., Bradman, A., 2013. In utero and childhood polybrominated diphenyl ether (PBDE) exposures and neurodevelopment in the CHAMACOS study. Environ. Health Perspect. 121, 257-262.
EU, 2008. Regulation of Hazardous Substances (RoHS) Directive (2002/95/EC) amendment.
EU, 2004. 24th amendment to the marketing and use Directive 76/769/EEC, Chemicals - Market Restrictions. in: EU (Ed.). Directive 76/769/EEC.
Fernandes, A., White, S., D'Silva, K., Rose, M., 2004. Simultaneous determination of PCDDs, PCDFs, PCBs and PBDEs in food. Talanta 63,1147-1155.
Fernandes, A., Dicks, P., Mortimer, D., Gem, M., Smith, F., Driffield, M., White, S., Rose, M., 2008. Brominated and chlorinated dioxins, PCBs and brominated flame retardants in Scottish shellfish: methodology, occurrence and human dietary exposure. Mol. Nutr. Food Res. 52, 238-249.
Fitzgerald, E.F., Fletcher, B.A., Belanger, E., Tao, L., Kannan, K., Hwang, S.-A., 2010. Fish consumption and concentrations of polybrominated diphenyl ethers (PBDEs) in the serum of older residents of upper Hudson River communities. Arch. Environ. Occup. H. 65, 183-190.
Frederiksen, M., Vorkamp, K., Thomsen, M., Knudsen, L.E., 2009. Human internal and external exposure to PBDEs - a review of levels and sources. Int. J. Hyg. Environ. Health 212,109-134.
Fromme, H., Korner, W., Shahin, N., Wanner, A., Albrecht, M., Boehmer, S., Parlar, H., Mayer, R., Liebl, B., Bolte, G., 2009. Human exposure to polybrominated diphenyl ethers (PBDE), as evidenced by data from a duplicate diet study, indoor air, house dust, and biomonitoring in Germany. Environ. Int. 35 (8), 1125-1135.
Gari, M., Grimalt, J.O., 2013. Inverse age-dependent accumulation of decabromodiphenyl ether and other PBDEs in serum from a general adult population. Environ. Int. 54,119-127.
Gascon, M., Fort, M., Martinez, D., Carsin, A.E., Forns, J., Grimalt, J.O., Marina, L.S., Lertxundi, N., Sunyer, J., Vrijheid, M., 2012. Polybrominated diphenyl ethers (PBDEs) in breast milk and neuropsychological development in infants. Environ. Health Perspect. 120,1760-1765.
Gomara, B., Herrero, L., Ramos, J.J., Mateo, J.R., Fernandez, M.A., Garcia, J.F., Gonzalez, M.J., 2007. Distribution of polybrominated diphenyl ethers in human umbilical cord serum, paternal serum, maternal serum, placentas, and breast milk from madrid population, Spain. Environ. Sci. Technol. 41, 6961-6968.
Guvenius, D.M., Aronsson, A., Ekman-Ordeberg, G., Bergman, A., Noren, K., 2003. Human prenatal and postnatal exposure to polybrominated diphenyl ethers, polychlorinated biphenyls, polychlorobiphenylols, and pentachlorophenol. Environ. Health Perspect. 111,1235-1241.
Harrad, S., Abdallah, M.A.E., 2011. Brominated flame retardants in dust from UK cars - within-vehicle spatial variability, evidence for degradation and exposure implications. Chemosphere 82,1240-1245.
Harrad, S., Diamond, M., 2006. New directions: exposure to polybrominated diphenyl ethers (PBDEs) and polychlorinated biphenyls (PCBs): current and future scenarios. Atmos. Environ. 40,1187-1188.
Harrad, S., Hunter, S., 2006. Concentrations of polybrominated diphenyl ethers in air and soil on a rural-urban transect across a major UK conurbation. Environ. Sci. Technol. 40, 4548-4553.
Harrad, S., Wijesekera, R., Hunter, S., Halliwell, C., Baker, R., 2004. Preliminary assessment of U.K. human dietary and inhalation exposure to polybrominated diphenyl ethers. Environ. Sci. Technol. 38, 2345-2350.
Harrad, S., Hazrati, S., Ibarra, C., 2006. Concentrations of polychlorinated biphenyls in indoor air and polybrominated diphenyl ethers in indoor air and dust in Birmingham, United Kingdom: implications for human exposure. Environ. Sci. Technol. 40, 4633-4638.
Harrad, S., Ibarra, C., Abdallah, M.A.-E., Boon, R., Neels, H., Covaci, A., 2008a. Concentrations of brominated flame retardants in dust from United Kingdom cars, homes, and offices: causes of variability and implications for human exposure. Environ. Int. 34,1170-1175.
Harrad, S., Ibarra, C., Diamond, M., Melymuk, L., Robson, M., Douwes, J., Roosens, L., Dirtu, A.C., Covaci, A., 2008b. Polybrominated diphenyl ethers in domestic indoor dust from Canada, New Zealand, United Kingdom and United States. Environ. Int. 34, 232-238.
Harrad, S., Ibarra, C., Abdallah, M.A., Boon, R., Neels, H., Covaci, A., 2008c. Concentrations of brominated flame retardants in dust from United Kingdom cars, homes, and offices: causes of variability and implications for human exposure. Environ. Int. 34,1170-1175.
Harrad, S., De Wit, C.A., Abdallah, M.A.E., 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., 2010. Indoor contamination with hexabromocyclododecanes, polybrominated diphenyl ethers, and perfluoroalkyl compounds: an important exposure pathway for people? Environ. Sci. Technol. 44, 3221-3231.
Jain, R.B., 2013. Effect of smoking and caffeine consumption on polybrominated diphenyl ethers (PBDE) and polybrominated biphenyls (PBB). J. Toxicol. Environ. Health A 76, 515-532.
Kalantzi, O.I., Geens, T., Covaci, A., Siskos, P.A., 2011. Distribution of polybrominated diphenyl ethers (PBDEs) and other persistent organic pollutants in human serum from Greece. Environ. Int. 37, 349-353.
Kalantzi, O.I., Martin, F.L., Thomas, G.O., Alcock, R.E., Tang, H.R., Drury, S.C., Carmichael, P.L., Nicholson, J.K., Jones, K.C., 2004. Different levels of polybrominated diphenyl ethers (PBDEs) and chlorinated compounds in breast milk from two U.K. regions. Environ. Health. Persp. 112, 1085-1091.
Kang, C.S., Lee, J.H., Kim, S.K., Lee, K.T., Lee, J.S., Park, P.S., Yun, S.H., Kannan, K., Yoo, Y.W., Ha, J.Y., Lee, S.W., 2010. Polybrominated diphenyl ethers and synthetic musks in umbilical cord Serum, maternal serum, and breast milk from Seoul, South Korea. Chemosphere 80, 116-122.
Koh, T.-W., Chih-Cheng Chen, S., Chang-Chien, G.-P., Lin, D.-Y., Chen, F.-A., Chao, H.-R., 2010. Breast-milk levels of polybrominated diphenyl ether flame retardants in relation to women's age and pre-pregnant body mass index. Int. J. Hyg. Envir. Heal. 213, 59-65.
Lenters, V., Thomsen, C., Smit, L.A.M., Jonsson, B.A.G., Pedersen, H.S., Ludwicki, J.K., Zviezdai, V., Piersma, A.H., Toft, G., Bonde, J.P., Becher, G., Vermeulen, R., Heederik, D., 2013. Serum concentrations of polybrominated diphenyl ethers (PBDEs) and a polybrominated biphenyl (PBB) in men from Greenland, Poland and Ukraine. Environ. Int. 61, 8-16.
Lignell, S., Aune, M., Darnerud, P.O., Soeria-Atmadja, D., Hanberg, A., Larsson, S., Glynn, A., 2011. Large variation in breast milk levels of organohalogenated compounds is dependent on mother's age, changes in body composition and exposures early in life. J. Environ. Monitor. 13, 1607-1616.
Meeker, J.D., Johnson, P.I., Camann, D., Hauser, R., 2009. Polybrominated diphenyl ether (PBDE) concentrations in house dust are related to hormone levels in men. Sci. Total Environ. 407, 3425-3429.
Meironyte, D., Koren, N., Bergman, A., 1999. Analysis of polybrominated diphenyl ethers in Swedish human milk. A time-related trend study, 1972-1997. J. Toxicol. Environ. Health A 58, 329-341.
Roosens, L., Abdallah, M.A.E., Harrad, S., Neels, H., Covaci, A., 2009. Factors influencing concentrations of polybrominated diphenyl ethers (PBDEs) in students from Antwerp, Belgium. Environ. Sci. Technol. 43, 3535-3541.
Santillo, D., Labunska, I., Davidson, H., Johnston, P., Strutt, M., Knowles, O., 2003. Consuming Chemicals - Hazardous Chemicals in House Dust as an Indicator of Chemical Exposure in the Home Greenpeace Research Laboratories.
Shaw, S.D., Blum, A., Weber, R., Kannan, K., Rich, D., Lucas, D., Koshland, C.P., Dobraca, D., Hanson, S., Birnbaum, L.S., 2010. Halogenated flame retardants: do the fire safety benefits justify the risks? Rev. Environ. Health 25, 261-305.
Shi, Z., Jiao, Y., Hu, Y., Sun, Z., Zhou, X., Feng, J., Li, J., Wu, Y., 2013. Levels of tetrabromobisphenol A, hexabromocyclododecanes and polybrominated diphenyl ethers in human milk from the general population in Beijing, China. Sci. Total Environ. 452-453, 10-18.
Sjodin, A., Patterson Jr., D.G., Bergman Ake, A., 2003. A review on human exposure to brominated flame retardants - particularly polybrominated diphenyl ethers. Environ. Int. 29, 829-839.
Sjodin, A., Paepke, O., McGahee, E., Focant, J.F., Jones, R.S., Pless-Mulloli, T., Toms, L.M.L., Herrmann, T., Maeller, J., Needham, L.L., Patterson Jr., D.G., 2008a. Concentration of polybrominated diphenyl ethers (PBDEs) in household dust from various countries. Chemosphere 73, S131-S136.
Sjodin, A., Wong, L.Y., Jones, R.S., Park, A., Zhang, Y., Hodge, C., Dipietro, E., McClure, C., Turner, W., Needham, L.L., Patterson Jr, D.G., 2008b. Serum concentrations of polybrominated diphenyl ethers (PBDEs) and polybrominated biphenyl (PBB) in the United States population: 2003-2004. Environ. Sci. Technol. 42, 13771384.
Thomas, G.O., Wilkinson, M., Hodson, S., Jones, K.C., 2006. Organohalogen chemicals in human blood from the United Kingdom. Environ. Pollut. 141, 30-41.
Thomsen, C., Stigum, H., Froshaug, M., Broadwell, S.L., Becher, G., Eggesbo, M., 2010. Determinants of brominated flame retardants in breast milk from a large scale Norwegian study. Environ. Int. 36, 68-74.
US-EPA, 2006a. Toxicological review of 2,2', 4,4', 5-Pentabromodiphenyl ether (BDE-99). United States Environmental Protection Agency, US Environmental Protection Agency, Washington, DC. <www.epa.gov/iris>.
US-EPA, 2006b. Toxicological review of 2,2',4,4'-Tetrabromodiphenylether (BDE-47). USEPA (United States Environmental Protection Agency), US Environmental Protection Agency, Washington, DC. <www.epa.gov/iris>.
US-EPA, 2006c. Toxicological review of 2,2',4,4',5,5'-Hexabromodiphenylether (BDE-153). in: Agency, U.S.E.P. (Ed.), US Environmental Protection Agency, Washington, DC. <www.epa.gov/iris>.
Yang, Q., Qiu, X., Li, R., Liu, S., Li, K., Wang, F., Zhu, P., Li, G., Zhu, T., 2013. Exposure to typical persistent organic pollutants from an electronic waste recycling site in Northern China. Chemosphere 91, 205-211. Zhu, L., Ma, B., Li, J., Wu, Y., Gong, J., 2009. Distribution of polybrominated diphenyl ethers in breast milk from North China: Implication of exposure pathways. Chemosphere 74,1429-1434.
