American Journal of Epidemiology
Copyright O 1997 by The Johns Hopkins University School of Hygiene and Public Health
All rights reserved
Vol. 146, No. 10
Printed In U.S.A
Invited Commentary: An Assessment of Maternal Intergenerational Factors
in Pregnancy Outcome
Irvin Emanuel1
Two articles in this issue (1,2) address an important
but often-overlooked area of investigation: maternal
intergenerational factors in reproductive problems, or
"...those factors, conditions, exposures, and environments experienced by one generation that relate to the
health, growth, and development of the next generation" (3, p. 27).
Coutinho et al. (1) linked infants' birth certificates
to mothers' birth certificates in Illinois. They found a
consistent decreasing trend in the proportion of infants
with low birth weight (<2,500 g) by maternal birth
weight for both whites and African Americans and,
conversely, an increasing trend for mean infant birth
weight. However, at some of the lowest levels of
mother's birth weight, the proportions of infant low
birth weight were not the highest, nor were infant
mean birth weights the lowest. This pattern, in which
the lowest-birth-weight mothers did not have the
smallest infants, has been seen by other investigators
(4-6). One possible explanation is that these mothers
had been preterm but healthy and had not been in utero
long enough to achieve their genetic potential for
prenatal growth.
Coutinho et al.'s finding that mother's birth weight
was more strongly associated with infant birth weight
than was paternal birth weight (1) also sheds light on
the relative contributions of genes and environment to
low birth weight. In general, it appears, as Coutinho et
al. also show, that maternal growth factors—birth
weight and adult stature—have stronger relations with
fetal growth than do paternal growth factors (7-9).
Further support for the greater importance of maternal
factors comes from studies showing that fetal growth
is most strongly related to the birth weights of relatives
in the maternal line (10-13). Furthermore, the association of maternal grandmother's stature to grandchild's fetal growth in two studies (9, 14) indicates a
multigenerational process.
Lumey and Stein (2) report the latest findings from
the Dutch Famine Birth Cohort Study, which takes
advantage of an unfortunate "natural experiment." In
this paper, they identify the mother's own early gestational growth as a critical period for her future reproductive success. The expected between-sibling parity relations of birth weight were disrupted in infants
born to mothers who had experienced intrauterine
exposure to the famine during the first trimester of
pregnancy. Because adequate nutrition was reestablished during the third trimester—the time of large
body mass accumulation—these mothers had higher
birth weights than those mothers exposed in the second and third trimesters. This finding of low correlations between birth weights of mothers and infants is
consistent with studies of mothers who are twins. As a
group, these mothers have babies as large as those of
singleton mothers, even though twins are markedly
small at birth (15, 16). The growth pattern of twins is
similar to that of singletons until late in gestation.
Thus, as in the Lumey and Stein study (2), it is the
mother's early gestational growth retardation which
seems to be related to later suboptimal reproductive
outcomes.
Received for publication May 13,1997, and in final form July 11,
1997.
Abbreviations: AGA, appropriate for gestational age; LGA, large
for gestational age; SGA, small for gestational age.
1
Department of Epidemiology and the Maternal and Child Health
Program, School of Public Health and Community Medicine, University of Washington, Seattle, WA.
2
Department of Pediatrics, School of Medicine, University of
Washington, Seattle, WA.
3
Center on Human Development and Disability, University of
Washington, Seattle, WA.
Reprint requests to Dr. Irvin Emanuel, School of Public Health
and Community Medicine, University of Washington, Box 357236,
Seattle, WA 98195-7236.
UNFOLDING EVIDENCE FOR
INTERGENERATIONAL FACTORS
These two papers are part of a 60-year-old body of
literature documenting the importance of intergenerational factors in pregnancy outcomes. The earliest
such study, a birth cohort analysis of mortality in
Great Britain carried out by Kermack et al. (17) in the
1930s, found that age-specific standardized mortality
ratios improved from one generation to the next. Relative mortality throughout the life span was related to
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Intergenerational Factors in Pregnancy Outcome
the decade of birth, but declines in infant mortality
lagged behind reduced mortality at later ages. The
authors concluded that 1) the health of adults was
largely determined by their health as children and
2) infant mortality fell only when maternal health had
improved.
The Kermack et al. study seems to have stimulated
the socioeconomic and social mobility studies conducted in the 1950s by investigators in Aberdeen,
Scotland (18-22), which found that low birth weight
and perinatal mortality rates were related to the social
class of both the infant's father and the maternal
grandfather. Perinatal mortality and low birth weight
were inversely related to maternal stature within each
class. Infants of women bom into the lowest class who
married men in the highest class (upwardly mobile
women) had lower rates of low birth weight and perinatal mortality than did the babies of women who
married within the lowest class. Upwardly mobile
women tended to come from smaller families, were
better educated, had higher-status occupations, and,
perhaps most importantly, were taller. However, the
perinatal mortality and low birth weight rates of babies
born to these upwardly mobile women still exceeded
those of babies whose mothers were born into and
married into the highest class. These studies indicate
that both the conditions under which a mother is born
and grows up and the conditions under which her
pregnancies occur are important determinants of her
reproductive success. They also suggest that it takes
more than one generation to equalize socioeconomic
disparities.
The association between maternal tallness and favorable pregnancy outcome has long been recognized
by clinicians and seems to be a constant phenomenon
in all human groups. An individual's height is the
result of a lifetime of growth, including the prenatal
phase (23). The importance of maternal prenatal
growth was recognized by studies assessing the link
between mother's birth weight and infant prenatal
growth, first documented almost 30 years ago by a
study conducted in Oxford, England (24). This study
compared birth weight distributions of mothers for
three categories of infants: small for gestational age
(SGA), appropriate for gestational age (AGA), and
large for gestational age (LGA). In comparison with
AGA mothers, the birth weight distribution among the
SGA mothers was shifted downward, and that of the
LGA mothers was shifted upward.
Subsequent research in various countries has shown
an inverse association between mother's birth weight
and numerous infant outcomes, including low birth
weight, very low birth weight (< 1,500 g), moderately
low birth weight (1,500-2,499 g), preterm delivery
Am J Epidemiol
Vol. 146, No. 10, 1997
821
(<37 completed weeks of gestation), relative intrauterine growth (SGA, AGA, LGA), respiratory distress syndrome, infant mortality, and perinatal mortality (4, 5, 25-31). Maternal intrauterine growth
retardation (SGA) is a risk factor for infant SGA (14,
32), but the importance of maternal preterm birth in
subsequent reproduction is not as clear at this time (6,
9, 14, 29, 32). A number of studies using linear regression have found direct associations between mother's birth weight and infant birth weight, with or
without adjustment for other factors (4, 6, 9, 33, 34).
Some of these studies did not include preterm or low
birth weight infants or those who died, thus decreasing
the strength of any associations by excluding some of
the smallest and most preterm infants (29, 34). Two
studies have found a direct association between mother's birth weight and maternal weight gain during
pregnancy, indicating that mother's birth weight also
has long-term physiologic consequences (4, 25). It
seems clear that by the time a first pregnancy occurs,
significant maternal risk factors have already been
established (35-37). In summary, relative risks associated with low maternal birth weight for various
suboptimal infant outcomes are approximately 2 (1,
14, 25-29)—of the same order of magnitude as maternal smoking during pregnancy (38, 39).
EXPLANATIONS FOR INTERGENERATIONAL
FACTORS
Prenatal and postnatal growth are genetically influenced, but socioeconomic factors play a very important role in the expression of genetic potential (9, 23,
40-42). For example, both prenatal and postnatal
growth have undergone rapid positive secular increases, even in affluent countries. Conversely, economically deteriorating populations have shown negative secular trends in growth (42-45). Finally, the
intergenerational increase in stature from parents to
offspring was directly related to the relative intrauterine growth of the offspring, and it occurred in all
social classes (44). Such associations between maternal growth, socioeconomic factors, and birth outcome
have been found for decades (46-49) and are a key to
understanding the intergenerational phenomenon.
It has been proposed that the pathway for the intergenerational phenomenon on a population basis is the
secular change in prenatal and postnatal growth. On an
individual basis, it may not be maternal size per se that
is important but the degree to which a mother has
achieved her genetic potential for growth (42). Results
from two studies support this possibility. Peruvian
teenage mothers who exceeded their mothers' statures
had bigger babies than those who did not (50). British
mothers whose stature equaled or exceeded that pre-
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Emanuel
dieted from midparental height had bigger babies than
mothers whose stature did not (unpublished data from
the 1958 British birth cohort).
A biologically plausible, nongenetic mechanism
which could account for the intergenerational phenomenon is suggested by both human and animal data,
described more fully elsewhere (42). Briefly, poorly
grown human infants have small organs, primarily
because of a reduced cytoplasmic: nuclear ratio but
also because of reduced cell number. Reduced cell size
and/or cell number are both consistent with a nongenetic mechanism resulting in long-term physiologic
consequences. It is difficult to determine which organs
may be responsible, since most of the organs of the
body, not just the ovary and uterus, are involved in
sustaining a pregnancy. Long-term, continuous prenatal and postnatal malnutrition in rats over many generations produced decreased birth size and adult size,
increased mortality, persistent decreases in the size of
most organs, and behavioral deficits (51). Depending
on when it was initiated, nutritional rehabilitation took
more than one generation to normalize growth (52).
FUTURE DIRECTIONS FOR
INTERGENERATIONAL RESEARCH
The two articles published in this issue of the Journal offer further support for the importance of maternal prenatal growth and birth weight for the health of
infants, and add to a substantial body of literature on
this topic. Findings from these two studies and thenpredecessors are remarkably consistent. The results
from the Dutch Famine Birth Cohort Study (2) at first
seem contradictory to those of the Norwegian study,
which found no difference in perinatal mortality
among infants born to 5-year cohorts of mothers born
during and after World War II (53). This apparent
contradiction may be related either to the use of 5-year
birth cohorts or to the fact that Norway did not experience extreme wartime malnutrition, or both. In any
event, the more recent Norwegian study which found
an association between mother's birth weight and perinatal mortality provided direct evidence of the importance of maternal prenatal growth in infant outcome
(31).
There are four promising directions for future intergenerational research. First, efforts should be directed
toward further elucidation of the relative contributions
of the various measures of parental prenatal and postnatal growth to later birth outcomes. A second goal
would be to clarify the role of intergenerational factors
in cyclic poor pregnancy outcomes, such as those
experienced by African-American women relative to
whites (1,3, 25, 26, 30, 42, 54). Maternal birth weight
distributions of African-American mothers are skewed
downward in comparison with those of white mothers
(25, 26). For some suboptimal birth outcomes, AfricanAmerican mothers appear to be at higher risk at all levels
of maternal birth weight (1, 25, 26). Disparities in birth
outcomes occur even between highly educated African
Americans and whites (55, 56). One explanation may be
that during the periods of these studies, most African
Americans with high educational or occupational status
were probably the first in their families to reach those
levels and thus, like the upwardly mobile women in the
British studies (21, 22), still experienced some reproductive disadvantage.
A third direction for research would be to use the
methodology of intergenerational research to elucidate
links between poor pregnancy outcome and later socioeconomic disadvantage. For instance, the 23-year
follow-up of the 1958 British National Birth Cohort
found that a birth weight of <3,000 g was associated
with long-term residence in substandard housing and
with financial difficulties (57). In the United States, an
analysis of the 1988 National Maternal and Infant
Survey found that mother's birth weight was directly
related to later educational attainment and was inversely related to the risk of being unmarried (25).
Similarly, US infants with low birth weights were at
increased risk for disadvantaged living conditions between the ages of 2 and 11 years. These conditions
included living in a low-income family in crowded
housing and having mothers who were more apt to be
single, in poor health, and of low educational attainment (58). Thus, it seems that low birth weight infants
tend to be born into and to grow up in poor, high-risk
families, are subjected to continued deprivation during
childhood, and at the time of pregnancy tend to be
mothers at high risk for suboptimal pregnancy outcome. Escape from this cycle seems to relate to a
family's efforts to foster child health and development
(21, 22), which may be more apt to occur in a receptive social environment.
The fourth promising direction for intergenerational
research is related to recent work documenting an
inverse relation of birth weight and early growth to
several nonreproductive adult diseases, including noninsulin-dependent diabetes mellitus, hypertension, and
coronary disease (59). The research related to this
so-called "fetal/infant origins hypothesis" has recently
been reviewed (60); criticisms include a failure to
control for social class, substantial loss to follow-up
because of elapsed time between birth and the time of
study, conflicting evidence, and the potential importance of factors intervening between birth and adulthood.
Notwithstanding these criticisms, it is likely that
prenatal and postnatal growth are factors in several
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Vol. 146, No. 10, 1997
Intergenerational Factors in Pregnancy Outcome
adult nonreproductive diseases. Stature has been
shown to be inversely related to risk of coronary
disease (61, 62) and glucose intolerance (63). Since
stature itself is related to birth weight (23), it appears
possible that coronary disease and adult-onset diabetes
mellitus will prove to be related to birth weight. The
importance of growth is further supported by the finding that adult mortality is inversely related to stature,
independently of weight (64). Reports from the Dutch
Famine Birth Cohort Study, including the Lumey and
Stein report in this issue of the Journal (2), and studies
of mothers who were twins (15, 16) indicate that an
important time for optimal growth is the mother's own
early intrauterine life. In one study, twins were also
shown to be at slightly lower risk for coronary disease
mortality (65). Thus, intrauterine processes which relate to long-term effects on both female reproduction
and coronary disease seem to pertain to early gestational growth and development (66).
Childhood growth, particularly stature at age 6
years, has been proposed as the best predictor of
mortality among populations (67). Economists have
suggested that stature is an excellent indicator of the
standard of living of populations, and that child
growth is a good indicator of economic development
(45). The importance of the long-term secular increases in stature to the secular decreases in both
mortality and chronic disease prevalence was proposed by Fogel (68). It seems that good growth means
good health and good health means good growth, and
it appears that the quality of growth is both a cause
and a consequence of the health status of individuals
and populations.
The link between maternal prenatal growth and
pregnancy outcome shown in the two papers appearing
in this issue of the Journal (1,2) illustrates one possible pathway whereby maternal socioeconomic factors impact the health of infants. Clearly there are
many determinants of pregnancy success or failure,
but the significance of preconceptional and intergenerational factors persists after adjustment for important
risk factors pertaining to the pregnancy itself. On the
basis of existing evidence, there is no reason to expect
that any one factor will have a very dramatic effect
relative to pregnancy outcome; and unfortunately,
there is evidence that advantaged living conditions
may not quickly override intergenerational effects.
SUMMARY
The increasing evidence that both prenatal and postnatal growth are important in the development of
reproductive and other adult health problems would
seem to warrant an expanded view of maternal and
child health. We need to recognize that each one of us
Am J Epidemiol
VoL 146r No. 10,1997
823
is a pregnancy outcome. The associations between
suboptimal growth and various health problems are
probably similar manifestations of the same underlying processes. There is substantial evidence of the
importance of growth to health from both human and
animal studies, and the concept is biologically plausible. Further investigations—clinical, epidemiologic,
and experimental—will be necessary to better determine this concept's validity and relative importance.
ACKNOWLEDGMENTS
This commentary was supported in part by training grant
MCJ 9043 and research grant MCJ 530807 from the Maternal and Child Health Bureau, Health Resources and Services Administration, US Public Health Service.
Appreciation is expressed to Drs. Christiane Hale and
Michelle Williams for their critical review of the manuscript.
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