Embryonic and Placental Development
Human pregnancies are usually divided into two stages of development—
embryonic and fetal (38). During the embryonic period, or the first 14 weeks
of gestation, gross development of the fetal anatomical features and placental formation
occur. The remaining 26 weeks of gestation are devoted to completing fetal
growth and development. Prior to implantation, the blastocyst becomes polarized,
with one part becoming the embryo and another part forming the placenta. As the
cells destined to become the placenta proliferate, they invade the uterine lining and
establish contact with maternal blood vessels so that the growing embryo can be
nourished (38).
Embryonic and placental development is a very complex process; cells divide
and redivide, migrate, differentiate, and undergo apoptosis. Prior to implantation,
the embryo is nourished by oviductal and then uterine secretions (13). After implantation
and establishment of the placenta, nourishment is provided via exchanges
between maternal and fetal circulation. This circulatory exchange is not established
until about eight weeks of gestation (13). Thus, the embryo is nourished
primarily by maternal uterine gland secretions that are taken up by placental villi.
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274 KING
There is evidence that embryonic development and organogenesis during the first
eight weeks is particularly vulnerable to perturbation by free radicals. To reduce
the risk of free radical–mediated damage, uterine nutrients are taken up by the
placental villi under a low oxygen concentration.
Uterine secretions during the first weeks of gestation are also a rich source of
growth factors, such as tumor necrosis factor-a and epidermal growth factor (13).
These growth factors influence placental villous development and the subsequent
form and function of the mature placenta. This may explain how the maternal
environment in early gestation affects pregnancy outcome. Studies in sheep and
experimental animals show that poor maternal nutrition during the embryonic
period alters health of the offspring. In rats, for example, poor nutrition during
embryonic development produces offspring with a high risk of hypertension (38).
Sheep fed nutritionally restricted diets during the embryonic period produced
offspring with higher amounts of fat than that in lambs born to ewes adequately
nourished throughout gestation (75). Evidence is accumulating in humans showing
that early maternal undernutrition increases the risk of obesity in the child. For
example, children born to women who experienced severe nutritional restriction
in early gestation during the five-month Dutch famine in World War II tended to
become obese adults (87). Thus, maternal undernutrition early in gestation, when
the nutritional demand is low, alters embryonic and placental development in such
a way as to influence lifelong health of the offspring. As discussed below, maternal
overnutrition also affects the postnatal health of the child.
Aberrations in Embryonic and Placental Development
Infants born to obese women have a higher prevalence of congenital anomalies
than do the offspring of normal-weight women, a finding that implies that maternal
adiposity alters development during the sensitive embryonic period (18, 29, 37).
Adipose tissue is a highly active endocrine organ secreting a number of hormones
that alter the circulation of metabolites, cytokines, and growth factors (40, 42).
Women who are obese at conception enter the period of embryonic development
with metabolic deviations in place that likely contribute to the increased prevalence
of congenital malformations.
Data from a large study of 56,857 U.S.women between 1959 and 1966 showed a
1.4-fold increase in major congenital anomalies among infants born to overweight
or obesewomen (64). Case-control studies report that the prevalence of neural tube
defects (NTDs) is twice as high among obese women as that in normal-weight or
thin women (89). Those studies are subject to the errors of self-reported maternal
heights and weights, however. But the relationship persisted in two large cohort
studies without the potential flaws in reports of maternal weight (89). Spina bifida is
more common than anencephaly, which suggests that these two birth defects have
different etiologies (89). NTDs are not the only type of birth defects more common
in obese women; other defects include oral clefts, heart anomalies, hydrocephaly,
and abdominal wall abnormalities (89).
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MATERNAL OBESITY 275
It is not known why obese women tend to have more birth defects, but evidence
is accumulating that the underlying mechanism may be similar to that causing
increased anomalies in diabetic mothers. Hyperinsulinemia and poor glycemic
control due to insulin resistance are common among the obese, even if they do
not have diabetes (40). Studies in diabetic women show that good glucose control
in the periconceptional period reduces the risk of birth defects (89). For example,
consuming a diet high in sucrose and other high-glycemic foods increased the risk
of NTDs approximately twofold among all women (81); the risk was increased to
fourfold among women with a body mass index (BMI) >29. The specific mechanism
whereby poor glycemic control alters early development is unknown, but
studies in experimental animals show that an increase in free radicals alters the
expression of transcription factors and contributes to embryopathology (88). Poor
folic acid nutrition has also been proposed as a factor increasing the incidence of
NTDs in obese women (57, 89). But in a number of epidemiological studies, the
relationship between maternal obesity and NTDs persisted after controlling for
self-reported folic acid intakes (37). Also, a recent study in Canada showed that
the risk of an NTD tended to be more pronounced (p < 0.09) in obese women
after folic acid supplementation than before (73); the relative risk increased from
1.4 to 2.8. It does not appear, therefore, that poor folic acid nutrition increases the
risk of NTDs among obese women. Instead, poor glycemic control seems to be a
more likely explanation.
Placental development also appears to be affected by maternal obesity. Delivery
of overgrown LGA infants occurs more frequently among obese than normalweight
women (18). Obese women are more likely to have larger placentas as well
as bigger babies (94). Recent studies show that a high placental weight relative to
birth weight predicts adult-onset diseases such as hypertension (3), coronary heart
disease (2), and diabetes (76). Larger placental-to-birth weight ratios are more
common in women with high BMIs (56), a finding that implies that an imbalance
between placental and birth weight is a risk factor for chronic disease later in life in
children of obese women. The presence of maternal hypertension among obese
women may be a factor influencing the relationship between placental size and
birth weight (90).
Preeclampsia, a problem affecting about 3% of all pregnancies, originates in the
placenta (74). Preeclampsia is more common among women with high BMIs. A
meta-analysis of maternalBMIand preeclampsia showed that the risk doubled with
each 5–7 kg/m2 increase in BMI (66). There are two broad categories of preeclampsia:
(a) placental preeclampsia arising from hypoxic state and poor development of
the placenta and its maternal blood supply, and (b) maternal preeclampsia arising
from an interaction between a normal placenta and a maternal low-grade inflammatory
response such as obesity, hypertension, or diabetes. In placental preeclampsia,
invasion of the trophoblast cells is inhibited by the hypoxic state, the arteries
are poorly remodeled, and uteroplacental circulation is inadequate. The hypoxic,
dysfunctional placenta releases what is called trophoblast debris into maternal circulation,
which causes a generalized systemic inflammatory response. Thus, an
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276 KING
inflammatory response is the outcome of both placental and maternal preeclampsia,
but the etiology differs. Placental preeclampsia, or abnormal placentation, has
its origins early in gestation; maternal preeclampsia, or maternal subclinical inflammatory
response, reflects the metabolic milieu of the mother at conception.
Clinically, it is impossible to differentiate the two forms of preeclampsia since the
outcome of both is an inflammatory state.
Obese women are more likely than normal-weight women to enter pregnancy
in a subclinical inflammatory state since increases in body fat are associated with
elevated cytokine levels and subclinical inflammation (39a). Alternatively, maternal
adiposity could also produce a hypoxic state if glycosylated hemoglobin levels
are increased and affinity for oxygen is reduced, decreasing oxygen transfer to the
uterus and impairing normal placentation. Several studies of dietary antioxidants
and preeclampsia have been done to prevent or treat the disorder. The results are
mixed (86); in some cases, the maternal inflammatory response is improved, but
symptoms of preeclampsia are unchanged (74). This may be because antioxidants
can improve the inflammatory response associated with preeclampsia, but not the
cause.
METABOLISM DURING LATE PREGNANCY
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