Environ. Sci. Technol. 2010, 44, 5256–5262
Significantly Higher Polybrominated Diphenyl Ether Levels in Young U.S. Children than in Their Mothers SONYA LUNDER,† LOTTA HOVANDER,‡ IOANNIS ATHANASSIADIS,‡ AND Å K E B E R G M A N * ,‡ Environmental Working Group, 1436 U Street, NW, Suite 100, Washington, DC 20009, and Environmental Chemistry Unit, Department of Materials and Environmental Chemistry, Stockholm University, SE-10691 Stockholm, Sweden
Received March 24, 2010. Revised manuscript received May 28, 2010. Accepted June 2, 2010.
While young children are rarely included in biomonitoring studies, they are presumed to be at greater risk of ingesting environmental contaminantssparticularly those that accumulate in foods or shed from consumer products. The widely used fire retardants polybrominated diphenyl ethers (PBDEs) are ubiquitous contaminants in the indoor environment and arewidelydetectedathigherlevelsinAmericansthaninindividuals from other countries. However, there are only three studies of PBDEs in U.S. children. We hypothesized that PBDEs are present in higher concentrations in young children than their mothers. PBDEs were assessed in blood samples collected concurrently from 20 mothers and their children, ages 1.5 to 4 years. The chemical analyses were performed by GC/MS applying selected ion monitoring. The samples were analyzed for 20 PBDE congeners; 11 were detected. ΣPBDEs for children were typically 2.8 times higher than for mothers, with median child:mother ratios varying from 2 to 4 for individual congeners. In 19 of 20 families studied, children had higher ΣPBDE concentrations than their mothers with significant (p < 0.01) concentration differences for five of the PBDE congeners. Decabromodiphenyl ether (BDE-209) was quantitated in 13 children and 9 mothers. Other studies indicate PBDEs are not elevated at birth, suggesting that early life is an intense period of PBDE intake. Children’s increased hand-to-mouth activity, dietary preferences, and exposures from breast milk may result in greater ingestion of PBDEs than adults. These findings suggest that measurements from adults likely do not reflect exposures to young children despite sharing homes and similar diets.
Introduction The epidemic of childhood lead poisoning caused by exposure to lead from old paint alerted researchers to the fact that young children can be at greater risk of exposure than adults to contaminants that originate from indoor sources. Due to the logistical challenges associated with including young children, the Centers for Disease Control and Prevention’s (CDC’s) National Health and Nutrition * Corresponding author phone: 46-816-3997; fax: 46-816-3979; e-mail:
[email protected]. † Environmental Working Group. ‡ Stockholm University. 5256
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Examination Survey (NHANES) biomonitoring studies typically include only older children. In contrast to traditional persistent organic pollutants, like polychlorinated biphenyls (PCBs) or dioxins, NHANES studies report higher concentration of contaminants that originate indoors or from dietary sources in the youngest age groups studied. These include elevated body concentrations of most phthalates (plasticizers) (1) and bisphenol A (2) in 6 to 12 year olds; and lead and tobacco metabolite cotinine in 4 to 11 year olds (3); and polybrominated diphenyl ethers (PBDEs) and perchlorate in teens (4, 5). In each case no data exist for younger age groups. Young children’s tendency to play on the ground and place their hands or other objects in their mouths leads to greater ingestion of many contaminants (6), including those shed from indoor sources and adsorbed to dust, toys, or other items. In addition to lead, home-use pesticides, plasticizers, fire retardants, and other chemicals are widely detected in house dust (7). Children younger than age 6 are likely to ingest these indoor pollutants, but little information exists about the concentrations of these chemicals in their bodies, nor the potential effects of these early life exposures. Paired testing of parents and children is of value because it controls for some of the variability in diet, genes, and environmental exposures. Should a correlation be detected between observations in parents and children, this could permit extrapolation from relatively abundant adult exposure data to children. Chemicals like PBDEs are good candidates for exploring the relationship between exposures to young children and adults living in the same household. Widely used as fire retardants in home furnishings, PBDEs are also detected in the environment and found in blood samples of more than 95% of Americans age 12 and older tested (4). PBDE use was also concentrated in the United States, suggesting that North American children may be one of the highest-risk subgroups for PBDE exposure (8). Mothers’ milk is a source of PBDEs for an infant, and tetra- to hexabrominated congeners in American house dust are positively correlated with concentrations in the occupant’s breast milk (9). Yet PBDE levels in Australian children peak at the postweaning stage (age 2.6 to 3) (10). There is limited information about PBDE levels in children, with elevated levels reported in the three studies of U.S. children (11-13). Studies performed in Norway, China, and Australia find elevated concentrations in children relative to adults (10, 14, 15) (Table 1). However, almost every study analyzes pooled samples and/or unrelated individuals, making it impossible to pinpoint the relative difference between adults and children in the same local environment. PBDEs are a class of brominated fire retardants (BFRs) sold in three commercial mixtures: PentaBDE (primarily BDE47, -99, -100, and -153), OctaBDE a mixture of hexa- to octaBDE congeners), and DecaBDE (principally BDE-209) (16). The use of PBDE products became increasingly popular in the 1970s as the price of bromine made it less expensive to produce these compounds. The high efficiency of bromine radicals to reduce flammability, combined with stricter fire retardancy standards around the world and increased number of foam and electronic products, were all drivers for greater use of brominated fire retardants (17). California requires chemical fire retardants be added to home furnishings, particularly children’s products, which appears to have resulted in elevated PBDE exposures in Californians relative to residents of other states (8). In the laboratory, PBDEs disrupt neurodevelopment, thyroid hormone, and androgen synthesis (18). Preliminary 10.1021/es1009357
2010 American Chemical Society
Published on Web 06/11/2010
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2006-2007
Australia
NA ) not available.
2006
United States
a
2004
California, U.S.
20 mothers
4 age groups
cord blood and 12 age groups for 60 years)
4 pools, containing blood from 100 children 0 to 4 years, 15 pools each from 24-100 children 5 to 15 years
United States
60 adults in 3 pooled samples grouped by age
49 children in 2 pooled samples grouped by age
2002
Norway
42 children age 7
adult population
57 maternal serum samples collected during pregnancy
child population
1994-1995 (mothers) 2001-2002 (children)
year of sample collection
Faroe Island
study location
TABLE 1. Summary of Studies Reporting on PBDE Levels in Young Children and Mothers around the World
no
yes
yes
yes
no
no
yes
individual samples?
NAa
yes
yes
no
no
NAa
yes
paired samples
Younger group had highest concentrations of all congeners, and lower concentrations of BB-153. Children’s concentrations were 2 to 7 times higher for tetra- to hexa-congeners and 2 to 10 times higher for BDE-209. Children significantly higher for major tetra-, to hexa- congeners, average 3-fold elevation in children. PBDE concentrations increased from birth through 2.6-3 years and then decreased through adulthood. Levels in the 2 to 5 year old age groups were roughly double those from 13-30 years old and 4 times higher than older adults.
Highest concentrations in 0 to 4 year olds. PBDEs 2.6 to 4 times higher than older age groups.
No association found between individual moms and children. Total PBDE concentrations are similar for both groups, but congener profile is different with BDE-153 dominant in children. 0 to 4 year old pool highest for every congener except BDE-209 (Σ7PBDE ) 9.7 ng/g lw) vs ∼6 ng/g lw in 5 to 14 years old, and e3.6 ng/g lw in older age groups.
finding
(10)
this study
(11)
(4)
(40)
(14)
(42)
ref
TABLE 2. Sociodemographic Factors for Participants in the Present Paired Mother-Child PBDE Exposure Study Mothers: age (years: average, range) BMI (average, range) multiparous duration of exclusive breastfeeding all children (range of months)
35.3 (28.9 - 44.4) 22 (19 - 27) 9 of 20 0-6
Children: age (years: average, range) BMI (average, range)a sex of child, male/female (%) a
3.0 (1.5 - 3.9) 16.3 (12.9-20.6) 40/60
BMI is unavailable for two children.
studies of PBDE exposures in people find an association between PBDE levels and both thyroid (19) and reproductive hormones (20). Epidemiological studies link maternal exposures to reduced fecundability (21) as well as cryptorchidism (22, 23) and neurodevelopmental disruption in offspring (24, 25), underscoring the need for accurate information about children’s exposures to these compounds. PBDEs have been restricted in the United States first as actions by individual states and then by voluntary agreements with U.S. manufacturers and importers. PentaBDE and OctaBDE were withdrawn from production by 2005 (26), and DecaBDE will be phased-out by 2013 in the U.S (27). Despite these actions, PBDE exposure continues, as evidenced by the continued detection of PBDEs in household products and people (4, 28).
Experimental Section Study Group. We collected paired serum samples from sampling of 20 U.S. mothers and their firstborn children, whose ages ranged from 1.5 to 4 years. We excluded participants who had not lived continuously in the United States since the child’s birth. All adult participants gave informed consent prior to study enrollment, with both custodial parents giving consent for child participants. The study received institutional review board approval (Independent Review Consulting, Inc., Corte Madera, CA, USA). Adult participants provided information on their and their child’s birthplace, height, weight, parity, duration of lactation for first and any subsequent children, typical diet, presence of foam and electronic items in the home, and other factors that could potentially lead to unusual PBDE exposure for mother or child. Demographic data are presented in Table 2. Participating families were drawn from 16 U.S. cities in 11 states. As a group, adult participants were generally older, with higher socioeconomic status than typical for American mothers. Average age for mothers was mid-thirties. Our study population was 80% Caucasian. Eight of 20 mothers were multiparous, and three more were pregnant with their second child at the time of testing. Body mass indices (BMI) were calculated based on self-reported weights (using prepregnancy weights where applicable). All study children had been breastfed, and solid foods were not typically introduced until five to six months of age. Most children were not weaned until after a year of age. The blood samples were collected between September 2006 and January 2007, at 16 commercial laboratories. Phlebotomists were instructed to fill an evacuated plain tube (Vacutainer, Rutherford, NJ) as completely as possible from the child and then collect two similar-sized duplicate samples from the mother. Samples were centrifuged, and the serum was transferred to acetone-washed glass bottles and shipped 5258
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overnight to a central study site on ice. Once frozen, samples were kept at -20 °C until they were chemically analyzed in Stockholm, Sweden. Similar amounts of serum were collected from children and their mothers in each tube. Chemicals and Instruments. The authentic reference standards, instruments, and detailed running conditions are presented as the Supporting Information (SI). Analytical Procedure. All samples were assessed for their lipid content through an enzymatic procedure at a hospital (Karolinska sjukhuset) and calculated according to Rylander et al. (29). The general method used for extraction and clean up is described elsewhere (30) applying some minor modifications (31). No separation of neutral and phenolic compounds was performed in this study. All samples were adjusted to 5 g of weight with 1% potassium chloride solution prior to extraction and the addition of surrogate standards, 13 C-BDE-209 (1 ng) and BDE-77 (0.5 ng). For recovery purposes 4′-MeO-BDE-121 (0.5 ng) was added as an injection standard. PBDE concentrations were reported on lipid weight basis, and when duplicate samples were analyzed, the average value was reported. In the case where one sample was quantified and the other was below limit of quantification (LOQ), 1/2 the LOQ for that particular sample was used to calculate the average maternal value. Quality Assurance and Data Analysis. Four laboratory reference material samples of plasma, six field blanks, and 11 procedural solvent blanks covering the procedure were extracted and analyzed in parallel with the samples. Standard calibration solvent solutions of the BDE-mixture were run for nine levels (0.1 ng/mL-44 ng/mL) on two occasions, controlling linearity and response of the analytes, and for BDE-209 individually (0.4 ng/mL-160 ng/mL). PBDE concentrations were calculated by using average response factors determined from two calibration standard levels and two quality controls for each series run. BDE-209 was quantitated by the isotope dilution method (32). Every sixth sample was randomly chosen for GC/MS reruns. Duplicate samples were run at the same occasion. The mean recovery of the surrogate standard BDE-77 was 99% with a coefficient of variation (CV) of 15%. Data on limit of detection (LOD) and LOQ are given in Table SI-3. Statistics. Each one of the PBDE congener concentrations in the 20 mother-child pairs were tested using the nonparametric paired Wilcoxon Signed-Rank test. The variance was assessed as described by Snedecor and Cochran (33).
Results and Discussion Our study found consistent elevations in U.S. children’s PBDE levels relative to their mothers. The analysis included 20 PBDE congeners in the samples, but only 11 were detected in participants, as summarized in Table 3. In only 9% of all paired measurements did the mothers have a higher level of any PBDE congener than their child. Children’s levels were higher in 83% of paired measurements, and the remaining 8% were non-detects for both mother and child. Detailed results of the individual PBDE congener concentrations, lipid adjusted, in each pair mother/child are presented on mass basis (nanograms/gram lipid - ng/g lw) values in Table SI-1 and on molar basis (picomoles per gram lipid - pmol/g lw) values in Table SI-2. The sums of six common congeners (Σ(6)PBDE -BDE-28, -47, -99, -100, -153, -197) ranged from 9.6 to 77 ng/g lw (17.7 to 134 pmol/g lw) in the mothers’ serum and from 12.0 to 111 ng/g lw (47.8 to 210 pmol/g lw) in children’s serum, with median values of 17 and 62 ng/g lw, respectively (32.6 and 115 pmol/g lw), as presented in Table 3. In this analysis, BDE-154 coeluted with 2,2′,4,4′,5,5′-hexabromobiphenyl (BB153), another persistent contaminant commonly detected in American adults at concentrations similar to PBDEs (4).
TABLE 3. Mean, Median, and Range PBDE Congener Concentrations in Serum from Mothers and Their Children (ng/g lipid) children (n ) 20) congener
a
BDE-28 BDE-47 BDE-85 BDE-99 BDE-100 BDE-138 BDE-153 BDE-154 + BB-153 BDE-183 BDE-197 BDE-209
mothers (n ) 20) b
median
mean
range
Q
1.0 31 n.c.c 6.2 6.2 n.c.c 13 3.2 n.c.c 0.49 1.7
1.1 31 n.c.c 6.8 6.6 n.c.c 14 6.0 n.c.c 0.65 3.5
0.3-2.2 11-65 n.d.d-2.2 1.8-15 2.1-14 n.d.d -0.33 3.4-32 0.45-38 n.d.d -1.7 0.13-2.0 [0.90]e-19
20 20 15 20 20 7 20 20 6 20 13
median
mean
range
Qb
0.44 8.8 n.c.c 1.4 1.2 n.c.c 5.8 1.8 n.c.c 0.30 1.4
0.72 12 n.c.c 1.7 1.8 n.c.c 7.6 4.4 n.c.c 0.33 1.7
0.2-2.5 3.1-40 n.d.d -0.4 0.4-5.2 0.4-7.0 n.d.d -0.5 1.4-32 0.75-41 n.d.d -0.5 0.11-0.82 [0.94]e-3.2
20 20 2 20 20 1 20 20 5 20 9
a BDE-17, BDE-66, BDE-71, BDE-196, BDE-201, BDE-203, BDE-206, BDE-207, and BDE-208 were not detected in any participants. b Number of quantitated samples. c Not calculated due to few measurements above LOQ. d Not detected. e Denotes 1/2LOQ.
FIGURE 1. Box-Whisker plots on a pmol/gram lipid basis for BDE-28, -47, -99, -100, -138, -153, -154/BB-153, -197, -209, as determined in serum from 20 pairs of children and their mothers. A few of our participants have indication of some BB-153 in their sample, as evidenced by an elevated (BDE-154 + BB153): BDE-153 ratio compared to the findings of CDC’s 2003-2004 NHANES study. Therefore we excluded BDE-154 from our summation of ΣPBDEs (these findings are discussed in detail in the SI). BDE-209 is not included in the summation either due to numerous nondetects, which most likely is due to its short half-life in humans (34). Box-Whisker plots for eight of the PBDE congeners on a molar basis in mothers’ and children’s samples are depicted in Figure 1. Statistical nonparametric paired test analysis of the mother/child concentrations revealed significantly higher concentrations and greater variability in children (p < 0.01) for BDE-47, -99, -100, -153 and BDE-154/BB-153, and (p < 0.05) for BDE-28 and BDE-197 (Figure 1). BDE-209 was detected in more children than mothers, but there was no statistically significantly elevation. All data are presented in Tables SI-1 and SI-2 to show levels and numbers of samples below LOD. Despite consistent elevations of PBDE congeners in children relative to their mothers, there was no systematic relationship between mothers and children. The median child to mother ratio was 2.8, with a 95th percentile of 7.4, when PBDEs are summed on a molar basis (pmol/g lw) (Table SI-4). Design Considerations. Our study employed several techniques to ensure a valid comparison between maternal and child measurements. Phlebotomists were instructed to collect samples concurrently, first drawing blood from
children and then drawing a similar volume from their mothers. This was done in case sample collection was more difficult for young children and enabled phlebotomists to collect a similar volume of blood from the adult. Similar sample sizes were sought to ensure that any trace contamination in glassware or the laboratory would not differentially affect results if smaller samples were systematically collected from children. The duplicate samples analyzed from mothers showed minimal variation in the concentrations determined for each of the congeners: BDE-28, -47, -99, -100, -153 and BDE-154 exhibited CVs between 6.2 and 20.9, while BDE197 and BDE-209 showed CVs of 30 and 20, respectively, confirming the quality of sample analysis. Study Limitations. The small number of families included lack of random selection and bias toward older mothers with higher socioeconomic status may mean that our findings are not representative of the PBDE ratios for other U.S. mothers and young children. Median maternal PBDE levels in our study were similar to or lower than the CDC’s NHANES sampling results for adults age 20 to 39 years (4). Older mothers (>34 years) have been found to have lower PBDE levels in breast milk than women aged 25 to 29 (35). Median values for our children were similar to or greater than median values for the 12-19 year olds in the NHANES cohort (4) but less than PBDE levels in two other studies of U.S. children (12, 13). The Role of Breastfeeding in the Mother-Child Comparison. Comparing maternal and child PBDE exposure can highlight children’s increased vulnerability to contaminants VOL. 44, NO. 13, 2010 / ENVIRONMENTAL SCIENCE & TECHNOLOGY
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in food and household products. However one must also account for chemicals transferred from mother to child during pregnancy and lactation. Studies comparing maternal serum and umbilical cord serum generally find similar PBDE levels (36, 37). Breast milk is a significant source of PBDEs for infants, and all of the children in our study group were breastfed, many of them for much longer than average for American infants. Majorcan four-year-olds who were breastfed (on average 4.5 months) had PBDE levels three times higher than children fed exclusively formula (3.6 vs 1.3 ng/g lw) (38). However these early life elevations may not persist through childhood. In our study neither the duration of exclusive breastfeeding nor the age of weaning correlated with observed PBDE measurements, nor did the younger children (age
