Our results show that many of these potential hormonally-active agents, most of which have been little studied previously in children of this age, were detectable in a large proportion of young girls, some at relatively high levels. Concentrations of many, most consistently the PBDEs, varied by geographic location with higher levels found in the California site. There were variations by race, with Blacks having the highest mean PBDE levels, but about 50% lower mean PCB levels and slightly lower pesticide levels, than Whites, even after adjustment for other factors. Hispanics had significantly lower levels of PCBs as well, but higher levels of p,p’-DDE. Asians had similar levels to Whites of all compounds except p,p’-DDE, for which they had the highest GM. As compared to the other compounds, patterns for PBDE levels by the other descriptors differed, including for BMI, SES (as measured by care-giver education), maternal age at delivery and history of being breast-fed. The girls who provided serum specimens were similar demographically to those who did not, so our results for these characteristics should be generalizable to the entire sample.
This is the first study to examine individual PBDE levels in elementary school-aged children in the U.S., reporting mean and median values generally 2–10 times greater than earlier published data (Hites 2004
; Petreas et al. 2002
; Thomsen et al. 2002
). Sjodin et al (2004a)
reported increasing PBDE concentrations in pooled U.S. serum samples from 1985 to 2002 and Hites (2004)
estimated an exponential increase by a factor of 100 in the last 30 years, or a doubling every 4–6 years. Furthermore, studies from the U.S. generally report higher levels than those from Japan and Europe, particularly for BDE-47. Our GM for BDE-47 (42.8 ng/g lipid) is 50 percent higher than that of recent (2003–2004) NHANES data for 12–19 year olds, with differences of a similar magnitude for BDEs- 99, 100, and 153 ( and CDC 2009
). The lack of detection of some congeners in a large proportion of girls should not be interpreted to suggest absence of the compound, but is dependent on assay sensitivity and sample volume available.
The higher PBDE levels in CA than OH suggest greater exposure, as the difference was not explained by other co-variates examined. A recent study of dust samples taken from homes in California and Massachusetts found PBDE levels were 3–9 times higher in CA (Zota et al. 2007). Unlike other states, California has a history of stringent regulations (CA 2000
) regarding flammability of upholstered furniture that can only be met by the addition of flame retardants, such as PBDEs. The primary commercial BDE mixture used to meet the polyurethane standard has been pentaBDE, which contains mainly BDE-47 and BDE-99, but also BDE-100, BDE-153, and BDE-154; the congeners we detected most frequently.
House dust and diet are considered the primary sources of PBDE exposure and young children are more likely to have higher dust exposure due to mouthing and playing activities, as well as to be exposed via breast milk (Lorber 2008
). Our generally higher levels may therefore also indicate young children at greater risk of exposure, as with some other environmental chemicals and supported by exposure pathway modeling (Lorber 2008
). Confirming this likelihood, the youngest age group in the NHANES data (12–19y) generally had higher mean PBDE levels than those of older age groups (Sjodin et al. 2008
) and in pooled serum samples, recent data from Australia showed children 7–12y had higher PBDE levels than adults over 30y, but lower than children 2–6y (Toms et al. 2009
). An increase in levels from newborn to early childhood (up to age 3 or 4y) has been attributed to breast-feeding (Carrizo and Grimalt, 2007
; Toms et al. 2009
). However, we did not find significant differences by whether or duration girls were breastfed, nor by mother’s age at delivery or child’s age within our relatively narrow range. Thus by age 6 and older, differences in PBDE body burdens may be most reflective of post-natal environmental exposures that are continuing, including from dust and diet.
By race, we found significantly higher PBDE levels in Black than in White girls, with intermediate levels in Hispanics before adjustment, suggesting possible differences in exposure. There are few comparison data available; NHANES data are for all ages combined and are not adjusted, but do indicate that Mexican and African Americans had higher GMs than non-Hispanic Whites for BDE-47 and BDE-99, and the 95th
percentile levels were particularly high for African Americans (Sjodin et al. 2008
). A study of cord blood levels in Baltimore found Asians had lower mean BDE-47 and BDE-153 levels than non-Hispanic Whites, and African Americans initially had higher PBDE levels, but not after adjustment (Herbstman et al. 2007
). The reasons for potentially higher levels in Blacks should be explored further, perhaps including differences in metabolism and environmental conditions, such as condition of housing and furniture, or take-home exposures from parental occupations.
Examining the organo-chlorine compounds, the median we report for p,p’-DDE (101.5 ng/g lipid) is similar to that reported in NHANES for 12–19 year olds during 1999–2002 and 2003–04 and that for hexachlorobenzene is slightly less (CDC 2009
). For the other pesticides we examined, the majority (75–90%) of 12–19 year olds in NHANES data had levels below the detection limit, so GMs were not calculated. We thus had higher detection rates for trans-nonachlor (69%), B-hexachlorocyclohexane (36%), and p,p’-DDT (30%). The mean and maximum p,p’-DDE levels we report are higher than recently reported in pregnant women (88 and 622 ng/g respectively) in Sweden (Glynn et al. 2007
), but as expected are much lower than in earlier cohorts of pregnant women (Hertz-Picciotto et al. 2005
) and do not represent a comparable population.
For PCBs, our median levels tended to be similar, but slightly higher than, those in the recent NHANES data for 12–19 year olds (, CDC 2009
). Comparing studies of neurodevelopment in children, Longnecker et al. (2003)
reported much higher median CB-153 levels in maternal serum ranging from about 30–140 ng/g in the U.S. and up to 450 ng/g in the Faroe Islands. Most of these samples are from much earlier cohorts or have established exposure sources.
GM levels were higher in CA than OH for the three pesticides most frequently detected and four of the six frequently detected PCB congeners, similar to PBDEs. Consistent with these results, in the Nurses Health Study, Laden et al. (1999)
reported that mean DDE levels were higher in participants from the West than the Midwest. Our results were not explained by race or SES, but race categories do not describe immigrant status. Pesticide exposure patterns differ in countries outside the U.S. (Bradman et al. 2007b
, Smith 1999
), hence a larger influx of immigrants (e.g. the parents) to CA from developing countries in Latin American and Southeast Asia, where some of these pesticides are still used, may explain higher levels of persistent pesticides in their offspring, via placental transport or breast-feeding.
In NHANES data combining all ages (CDC 2009
), levels of p,p’-DDE were higher among Mexican Americans than Blacks or Whites, consistent with our findings for Hispanic girls. As noted above, the higher DDE levels we find in Asians and Hispanics may reflect a higher proportion of immigrants. Also similar to our results, some of the PCB congener levels in NHANES were lower among Mexican Americans. In contrast to the PBDEs, we found lower PCB levels in Blacks, as well as lower pesticide levels, which were not evident in NHANES data. Other studies have suggested lower PCB levels in Black than in White gravidas, but results were inconsistent by adjustment and these are not comparable populations (Herbstman et al. 2007
, Wolff et al. 2007b
). Nor are the NHANES data, which are for all ages (>12) and genders combined, and Asians are not separated, so our data thus add important detail to the literature.
Our finding of an inverse relationship between BMI and several pesticides or PCBs is difficult to interpret as either a contributor to or consequence of chemical levels. We examined BMI because of changing growth and fat stores in children of this age (Wolff and Landrigan, 2002
). Exposure to some of the compounds occurs through breast-feeding, which may affect later BMI. We observed a slight trend towards lower BMI among breast-fed girls, which was, however, not statistically significant. Furthermore, in models that control for breast-feeding, the inverse association of the chemicals with BMI persisted. To explore this further, we examined the relationship between height and the pesticides or the PCBsum (adjusting for the other co-variates) and also found an inverse relationship. Similarly, a study from Germany found that girls with higher DDE levels during childhood had reduced growth at age 10 and shorter height at age 8, but reported no associations with PCBs (Karmaus et al. 2001
). Levels of these persistent chemicals in girls primarily represent in utero and lactational exposures from the mother, as well as possibly later childhood exposure from diet and other sources. Studies with data on maternal or early childhood PCB levels show inconsistent results with later childhood anthropometric measures (Blank et al. 2000; Hertz-Picciotto et al. 2005
, Gladen et al. 2000; Guo et al. 1995
), likely further complicated by pubertal status at the time of anthropometric measurement.
In adults, a complex pharmacokinetic model has been proposed to explain interaction between BMI, time since exposure and organochlorine concentrations in adipose tissue (Wolff and Anderson 1999), which may also explain some of the findings in girls. DDE levels were inversely related to BMI in nulliparous Chinese women (Perry MJ et al. 2005
), but varied in other studies. PCB levels were also lower in obese women in at least one study (Herbstman et al. 2007
), but not in another (Wolff et al. 2007b
). These observations seem less likely to support an effect on growth in children and perhaps suggest a “dilution” effect, which we can examine further when the longitudinal data collection is complete. Unlike typical findings in adults and with maternal age in our study, we found that some of the PCBs and pesticide levels were lower in older children, likely reflecting tapering effects of exposure occurring trans-placentally or through breast-feeding.
In summary, our study provides data that was previously lacking on body burdens of HAAs in young children from a large, racially diverse population using the most sensitive assays now available. Similar to some studies (Bradman et al. 2007a
, Herbstman et al. 2007
), but not all, we did not see strong correlations between PBDEs and PCBs, nor were their descriptors consistent. The variation we found by race and BMI, which are both relevant to puberty, as well as by site, warrant further investigation, both with respect to puberty and to identify factors contributing to exposure.