HJI, FME Slijper, PGH Mulder, and N Weisglas-Kuperus 2002. Effects
of Perinatal Exposure to PCBs and Dioxins on Play Behavior in Dutch
Children at School Age. Environmental
Health Perspectives 110:A593-A598.
this groundbreaking study, Vreugdenhil et al. report that
perinatal exposure to PCBs is associated with changes in play behavior
of children. Boys with higher PCB exposures are less likely
to engage in masculine patterns of play, and girls
with higher exposure are more likely to engage in masculine play.
They also find an association with dioxin: more feminized
behaviors were found in both boys and girls exposed prenatally
to higher levels of dioxin. While this is the first study ever reported
of the effects of contaminant-induced endocrine disruption on gender
differences in child behavior, its results are consistent with animal
should be noted that the PCB levels studied here are not terribly
high, nor a result of occupational exposures. They are background
levels resulting (most likely) from normal consumption
of foods from Dutch markets. The study focused on differences among
the mothers in their PCB body burdens: while some had less, some
had more, none had none nor did any have levels out of the ordinary.
did they do? Vreugdenhil et al. study continues
the work by this team of Dutch scientists on a cohort of children
whose PCB and dioxin exposures have been carefully characterized.
Previously reported findings include adverse impacts on immune
system function and neurological development.
research focused on 207 Dutch infant-mother pairs recruited to the
investigation between 1990 and 1992. Chemical exposure was assessed
at three stages: from mothers' blood drawn during the final month
of pregnancy, from umbilical cord blood obtained at birth, and from
breast milk within two weeks of birth. In the blood samples, they
measured levels of four PCB congeners (118, 138, 153 and 180). Measurements
of breast milk were more extensive: 26 PCBs and 17 dioxins. They
combined the measurements of the individual congeners using the
standard TEQ approach (toxic equivalents).
half of the infants were breast fed; the others received infant
formula. For the breast-fed infants, total post-natal TEQ was estimated
based on the concentrations measured in breast milk and the duration
of breast feeding. In combination with the blood samples, these
data also allowed the investigators to assess the impacts of exposure
characterize play behavior, Vreugdenhil et al. used the
Dutch version of the Pre-School Activities Inventory (PSAI), a standard
method for assessing gender aspects of play behavior in young
to the authors:
PSAI is designed to discriminate play behavior both within
and between the sexes. It consists of 24 questions addressing
three aspects of play behavior: type of toys, activities,
and child characteristics. Answers are given on a 5-point
scale ranging from never to very often. The questions assess
either feminine or masculine play behavior from which 3 scales
are derived: a composite scale, integrating both masculine
and feminine play behavior, and a masculine and a feminine
scale. The composite scale is essentially defined as the difference:
feminine scale minus masculine scale. A negative score on
the composite scale implies masculine play behavior and a
positive score feminine play behavior. A higher score on the
feminine scale indicates more feminine play behavior, whereas
a higher score on the masculine scale indicates more masculine
in their earlier studies, the Dutch scientists used statistical
procedures (multiple regressions) to control for the potential influence
of confounding variables that might affect neurological development,
including education level of parents, verbal IQ of the principal
parent, smoking, alcohol use, age of the mother, etc.
average age of the children at the time of behavioral assessment
was seven and a half years.
did they find? On average, boys measured using the PSAI
method scored higher on the masculine scale than girls and lower
on the feminine scale.
gender differences are all significantly different (p < 0.001)
and are precisely what is expected: on average, boys engage in more
masculine play, girls in more feminine play.
the multiple regression analysis of contaminant effects, Vreugdenhil
et al. found statistically significant relationships between
their measures of masculinity and femininity of play behavior and
PCB and dioxin exposures.
increasing prenatal PCB exposure, boys exhibited less masculine
play behavior. Their composite scale score rose and their
masculine scale score fell. The association was stronger with cord
blood PCB levels (p < 0.011 and p < 0.001, respectively, for
composite and masculine scales) than with maternal blood during
the final month of pregnancy (p < 0.03 for both scales). Girls
scores fell on the composite scale and rose on the masculine scale,
but the trends were not significant statistically. Feminine scale
scores did not change for either boys or girls in relation to prenatal
contrast, prenatal dioxin levels were associated with higher feminine
scale scores in both boys and girls (p = 0.048), "indicating
more feminized play behavior in both sexes."
PCB levels in breast milk were associated with more masculinized
behavior in girls (p=0.028). The trends for boys suggested association
with more feminized behavior but was not significant.
controlling for prenatal exposure, there was no link between total
post-natal exposure via breast milk and trends in play behavior.
does it mean? Vreugdenhil et al. interpret their
results to indicate that prenatal exposure to PCBs and dioxin interfere
with the hormonal signals controlling development of sexual differences
in typical play behavior:
play behavior shows marked sex differences and is likely to
be influenced by the prenatal steroid hormone environment.
We therefore suggest that these results may indicate behavioral
effects of steroid hormone imbalances early in development
related to prenatal exposure to PCBs and dioxins, their metabolites,
and/or related compounds."
acknowledge that their methods do not allow a complete test of this
hypothesis, especially as they have no information on the levels
of natural steroid hormones experienced by the children prenatally,
nor is there full understanding of the (likely multiple) ways that
PCBs and dioxin disrupt steroid hormone action during development.
results nonetheless are consistent with previous
indications that prenatal hormone levels can affect sexual differentiation
of childhood play.
human data, moreover, already implicate contaminants in disrupting
sex-specific behavioral development. Research
with babies born to mothers exposed to PCBs and PCDFs in the
Yucheng rice oil contamination incident found a diminution of spatial
orientation abilities in boys, with no effect in girls. Because
boys typically perform better on tests of spatial orientation than
girls, these results were interpreted as demasculinizing or feminizing
effects caused by disturbances in steroid hormones by prenatal exposure
et al.'s results are important for two reasons.
they clearly implicate hormonally-active contaminants in disruption
of the development of gender-specific human behavior, even if
they fall short of establishing causality.
the affected behaviors, sex-specific childhood play, has been
linked speculatively to later patterns in adult sexual choice.
While highly controversial, at least some research (e.g., Green
1985) suggests that "childhood gender nonconformity"
(e.g., play behavior typical for opposite sex) is a predictor
of same-sex sexual choice in adulthood. Whether or not the observations
reported in by Vreugdenhil et al. are relevant to this
theory remains to be determined.