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Department of International Health, The Rollins School of Public Health of Emory University, Atlanta, GA 30322 and a Instituto de Nutrición de Centro América y Panamá, Carretera Roosevelt, Zona 11, Guatemala City, Guatemala
| ABSTRACT |
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KEY WORDS: birth weight birth length intergenerational effects Guatemala
| INTRODUCTION |
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Linear growth is the phenotypic expression of the interaction of both
genetic and environmental factors. For example, during pregnancy,
characteristics of the maternal environment such as smoking and
adequacy of dietary intakes are well-known determinants of birth size
(Gulmezoglu et al. 1997
, Ramakrishnan et al. 1998
). Maternal height and
prepregnancy weight, which are the result of genetic and environmental
influences before pregnancy, are also important determinants of birth
size, particularly in developing countries (Kramer 1987
). Recent
evidence from Guatemala has also shown that intrauterine growth
retardation (IUGR)4 and growth during early childhood are
important determinants of height and body composition later in life,
and that girls who were stunted during early childhood grow to be
shorter adults and in turn give birth to smaller babies (Martorell et al. 1996 and 1998
). Emanuel (1993)
proposed that IUGR deficits are
associated with reduced organ weights primarily as a result of a
reduced amount of cytoplasm per cell rather than a reduced number of
cells, and this may be responsible for the nongenetic transmission of
intergenerational effects on birth weight. In contrast, research from
developed countries linking fetal undernutrition to chronic disease
outcomes in later life suggests that the maternal environment during
the prenatal period may modify the genetic predisposition of the unborn
fetus for later outcomes and that the timing of the insult during the
prenatal period may be critical (Barker 1996
, Lumey et al. 1995
). This
interaction between genetics and maternal environment, especially
during the intrauterine period, may hold important clues to the
underlying mechanisms that might explain intergenerational effects on
linear growth.
The main objective of this paper is to examine the evidence of intergenerational effects on linear growth and will include an examination of the following relationships:
Birth size of parents and their children
Adult height of parents and their children
Patterns of linear growth across two generations
The results presented in the following sections are based on a review of the literature, and recent work from an intergenerational study in Guatemala.
| LITERATURE REVIEW |
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Intergenerational relationships in birth weight.
A brief description of the study design and key findings for each
of the studies that examined intergenerational relationships in birth
weight are presented in Table 1
.The studies have been organized according to the type of analysis used.
Two studies reported simple and/or adjusted correlation coefficients
(Carr-Hill et al. 1987
, Hackman et al. 1983
); four provided slope
estimates, both unadjusted and adjusted for various factors such as
socioeconomic status of parents, grandparents and/or adult height
(Coutinho et al. 1997
, Emanuel et al. 1992
, Langhoff-Roos et al. 1987
,
Little 1987
); five studies included relative risk estimates of low
birth weight and/or preterm births as a function of mother's birth
outcome (Coutinho et al. 1997
, Klebanoff et al. 1984
, 1987
and 1989
,
Sanderson et al. 1995
); and two used ANOVA to compare different groups
according to the extent or nature of growth retardation of the mother
(Lumey 1992
, Ounsted 1969
, Ounsted and Ounsted 1973
). One of the
studies used more than one approach (Coutinho et al. 1997
). All of
these studies were conducted in developed countries, namely, the United
Kingdom (U.K.), United States (U.S.), Sweden and the Netherlands. The
study samples were primarily from middle-class populations of Caucasian
origin. A few studies in the U.S. also included African Americans who
are known to be at greater risk of adverse pregnancy outcomes (Coutinho et al. 1997
, Klebanoff et al. 1987
, Sanderson et al. 1985
). In general,
the births of the mothers occurred during the 1950s to 1960s, and the
children were born during the 1970s and 1980s. The mean adult height
and prepregnant weight of the women ranged between 162 and 168 cm and
55 and 62 kg, respectively. The prevalence of low birth weight was
<10% and mean birth weight for both mothers and their children was
>3.0 kg.
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The adjusted regression coefficients for intergenerational
relationships between maternal birth weight and her child's birth
weight ranged between 0.10 and 0.20, i.e., for every 100 g
increase in maternal birth weight, her child's birth weight increased
by 1020 g. Among the studies that included birth weight of both
parents, both paternal and maternal birth weight were found to have
significant independent effects, although the magnitude of the
relationship was greater for maternal birth weight. In the multivariate
models, the effect of maternal stature on her infant's birth weight
was no longer significant when her birth weight was included in the
final model in three studies (Emanuel et al. 1992
, Hackman et al. 1983
,
Langhoff-Roos et al. 1987
), suggesting that the relationship between
maternal height and birth weight is explained by intergenerational
effects. Emanuel et al. (1992)
, who had data on three generations and
social class, found that only the maternal grandmother's height was
predictive of her grandchild's birth weight, suggesting the
significance of the maternal lineage. The social class of the mother,
but not the father, was a significant predictor of the child's birth
weight.
Intergenerational relationships in adult height.
Few studies have examined the association between the adult height of
parents and that of their offspring, and most of them are from
developed countries (Alberman et al. 1991
, Kuh and Wadsworth 1989
). The
associations were greater for adult height compared with that found for
birth size. Correlation coefficients of 0.420.50 were reported. An
earlier study using cross-sectional data from Guatemala reported
similar coefficients between childrens' height and parents' height
(Martorell et al. 1977
). After adjusting for indicators of
socioeconomic status, the slope estimates were still significant and
ranged from 0.29 to 0.54.
| INTERGENERATIONAL STUDY IN GUATEMALA |
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Hypotheses.
The following hypotheses were tested: 1) After adjusting for the effects of maternal age, sex and gestational age of the infants, maternal birth weight is a significant predictor of her child's birth weight and length, and maternal birth length is a significant predictor of her child's birth weight and length. 2) The magnitude and significance of the above-mentioned intergenerational relationships will be altered after adjusting for current socioeconomic status. 3) The magnitude and significance of the above-mentioned intergenerational relationships will be reduced after adjusting for maternal adult height and prepregnancy weight.
Analytical sample.
The sample was restricted to singleton, term (>37 wk of
gestation) births that occurred in the four study villages between 1991
and 1996, to women who were born during the original longitudinal study
(19691977). The inclusion criteria were as follows: 1)
birth weight and length for both generations, 2) gestational
age and sex of the infants and 3) age, adult height,
prepregnant weight and current socioeconomic status for the mothers.
All anthropometric data were collected according to similar
standardized techniques for newborns and adults in both studies (Lohman et al. 1988
). Birth weight was measured within the first 48 h to
the nearest centigram for both generations. Newborn length was assessed
at 15 d to the nearest millimeter in the case of the mothers, and
was measured at the same time as birth weight for their infants.
Gestational age (expressed in weeks) of the mothers was estimated from
the recall of the date of the last menstrual period. In the case of the
children, a physical exam was carried out by a trained physician within
48 h of birth and gestational age was estimated using a modified
version of a scale created by Capurro et al. (1978)
. Socioeconomic
status (SES) was based on a factor score derived from a principal
components analysis of household characteristics and possessions that
was assessed during a follow-up study in 19881990 (Rivera et al. 1995
). Complete data were available for 215 mother-child pairs, and
~60% of the mothers (n = 140) contributed data for
>1 child. This sample represents ~30% of all female subjects who
were born during the original longitudinal study, and had birth weight
data (n = 453).
Analysis.
All statistical analysis was done using SAS for Windows, version
6.12 (SAS Institute 1996
). Because some mothers contributed >1 child,
the SAS Proc Mixed procedure was used so that the maximum number of
mother-child pairs could be included in the analysis. Most of the
variables used were continuous in nature and normally distributed
except for the sex of the child, which was expressed as a dummy
variable (0 = male, 1 = female). P-values of 0.05
were considered to be significant. Because of the high correlation
between maternal birth weight and length, separate models were
developed for these independent variables. Current SES was used as a
covariate along with the age of the mother. The main analytical
approach that was followed was to derive adjusted slope estimates of
the effect of maternal birth size on her child's birth size after
adjusting for the following: 1) known confounders, namely,
maternal age, gestational age and sex of the infant; 2)
known confounders (see 1) and current socioeconomic status
(SES); and 3) known confounders (see 1), current
SES, maternal prepregnant height and weight.
Results of analysis.
The descriptive statistics for birth outcomes in both generations are
presented in Table 2
.Mean birth weight and gestational age were similar for both mothers and
their children and were ~3.0 kg and 39.3 wk, respectively. The
prevalence of low birth weight was 5.1 and 13.5% among mothers and
their children, respectively. Nearly 50% of both the mothers and their
children were below -1 Z-score of length/age at birth based on the
WHO/NCHS median values (WHO 1986
), indicating that linear growth
retardation in utero was common in this population.
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| DISCUSSION |
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The results also suggest that the known effects of maternal height and
prepregnant weight on her child's birth size (Kramer, 1987
) are due to
a large extent to intergenerational effects of maternal birth size. For
example, the magnitude of the relationship between maternal birth
length and her child's birth weight was reduced by nearly half, i.e.,
to 38 g/cm, when maternal height and prepregnant weight were included
in the model. Similarly, the relationship between maternal birth length
and her child's birth length was not significant when maternal adult
size was included in the final model.
It is important to recognize some limitations of the analytical
strategies that have been used to date in defining these relationships.
Specifically, we are faced with the problem of "endogeneity" in
that variables such as maternal adult height are in the causal pathway
linking birth weight of one generation with the next. Although this
problem could be addressed in part by including "exogenous" or
more distal determinants that would serve as a proxy, e.g., for
grandmother's height, this is often difficult due to problems of
collinearity. The use of techniques that have been commonly used in the
social sciences such as structural equation modeling (Biddle and Marlin 1987
, Farrell 1994
) may be useful for future analyses because this
would allow us to examine the significance of the various pathways in
the causal web linking outcomes across generations. In summary, some
areas of interest for future research are as follows:
explore the role of paternal birth size
compare the nature of the relationship between different groups, namely, those that have not experienced any changes in environment across two generations with those that have experienced significant improvements
examine the intergenerational effects of specific interventions (e.g., supplementary feeding)
compare linear growth patterns across generations
As more data on the significance of intergenerational effects on linear growth become available for developing countries, we will be able to assign priorities to appropriate interventions that can effectively break the vicious cycle of malnutrition and help reduce the high rates of stunting that exist in many developing countries.
| FOOTNOTES |
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1 Presented at the symposium "Causes and
Etiology of Stunting" as part of Experimental Biology 98, April
1822, 1998, San Francisco, CA. The symposium was sponsored by the
American Society for Nutritional Sciences and the Society for
International Nutrition Research. Published as a supplement to
The Journal of Nutrition. Guest editor for the symposium
publication was Edward A. Frongillo, Jr., Cornell University, Ithaca,
NY. ![]()
2 Supported in part by awards from the Thrasher
Research Fund and the National Institutes of Health (HD 29927). ![]()
3 Abbreviations used: IUGR, Intrauterine growth
retardation; CBW, child's birth weight; INCAP, Institute of Nutrition
of Central America and Panama; MBW, maternal birth weight; NCHS,
National Center for Health Statistics; SES, socioeconomic status. ![]()
| REFERENCES |
|---|
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1. Alberman E., Filakti H., Williams S., Evans S.J.W.. Early influences on the secular change in adult height between the parents and children of the 1958 birth cohort. Ann. Hum. Biol. 1991;18:127-136.[Medline]
2. Barker D.J.P.. Fetal growth and lung development and long-term consequences. Boulton J. Laron Z. Rey J. eds. Long-Term Consequences of Early Feeding 1996;vol. 36. Nestle Nutrition Workshop Series Nestec Ltd./Lippincott-Raven Publishers Philadelphia, PA.. .
3. Biddle B. J., Marlin M. M.. Casualty, confirmation, credulity and structural equation modeling. Child Dev 1987;58:4-17.
4. Capurro H., Konichezky S., Fonseca D., Caldeyro-Barcia R.. A simplified method for diagnosis of gestational age in the newborn infant. J. Pediatr. 1978;93:120-122.[Medline]
5. Carr-Hill R., Campbell D. M., Hall M., Meredith A.. Is birth weight determined genetically?. Br. Med. J. 1987;295:687-689.
6.
Coutinho R., David R. J., Collins J. W.. Relation of parental birth weights to infant birth weight among African Americans and Whites in Illinois. Am. J. Epidemiol. 1997;146:804-809.
7. Emanuel I.. Intergenerational factors in pregnancy outcomesImplications for teratology?. Issues Rev. Teratol. 1993;6:47-83.
8. Emanuel I., Filakti H., Alberman E., Evans S.J.W.. Intergenerational studies of human birth weight from the 1958 birth cohort. IEvidence for a multigenerational effect. Br. J. Obstet. Gynaecol. 1992;99:67-74.[Medline]
9. Farrell A. D.. Structural equation modeling with longitudinal datastrategies for examining group differences and reciprocal relationships. J. Consult. Clin. Psychol. 1994;62:477-487.[Medline]
10. Gulmezoglu M., de Onis M., Villar J.. Effectiveness of interventions to prevent or treat impaired fetal growth. Obstet. Gynecol. Surv. 1997;52:139-149.[Medline]
11.
Hackman E., Emanuel I., Van Belle G., Daling J.. Maternal birth weight and subsequent pregnancy outcome. J. Am. Med. Assoc. 1983;250:2016-2019.
12. Klebanoff M. A., Graubard B. I., Kessel S. S., Berendes H. W.. Low birth weight across generations. J. Am. Med. Assoc. 1984;25:2423-2427.
13.
Klebanoff M. A., Meirik O., Berendes H. W.. Second generation consequences of small-for-dates birth. Pediatrics 1989;84:343-347.
14. Klebanoff M. A., Yip R.. Influence of maternal birth weight on rate of fetal growth and duration of gestation. J. Pediatr. 1987;111:2287-2292.
15. Kramer M. S.. Determinants of low birth weightmethodological assessment and meta-analysis. Bull. WHO 1987;65:633-737.
16.
Kuh D., Wadsworth M... Parental heightchildhood environmental and subsequent adult height in a national birth cohort. Int. J. Epidemiol. 1989;18:663-668.
17. Langhoff-Roos J., Lindmark G., Gutstavson K. H., Gebre-Medhin M., Meirik O.. Relative effect of parental birth weight on infant birth weight at term. Clin. Genet. 1987;32:240-248.[Medline]
18. Little R. E.. Mother's and father's birth weight as predictors of infant birth weight. Pediatr. Perinat. Epidemiol. 1987;1:19-31.[Medline]
19. Lohman T. G., Roche A. F., Martorell R.. Anthropometric Standardization Reference Manual 1988:3-9 Human Kinetics Books Champaign, IL.. .
20. Lumey L. H.. Decreased birthweights in infants after maternal in utero exposure to the Dutch famine of 19441945. Pediatr. Perinat. Epidemiol. 1992;6:240-253.[Medline]
21. Lumey L. H., Stein A. D., Ravelli A. C.. Timing of prenatal starvation in women and birthweight in their first and second born offspringThe Dutch Famine Birth Cohort Study. Eur. J. Obstet. Gynecol. Rep. Biol. 1995;61:23-30.[Medline]
22. Martorell R., Habicht J.-P., Rivera J. A.. History and design of the INCAP longitudinal study (196977) and its follow up (198889). J. Nutr. 1995;125 (suppl.):1027S-1041S.
23. Martorell R., Ramakrishnan U., Schroeder D. G., Melgar P., Neufeld L.. Intrauterine growth retardation, body size, body composition and physical performance in adolescence. Eur. J. Clin. Nutr. 1998;52 (suppl. 1):S43-S53.
24. Martorell R., Ramakrishnan U., Schroeder D. G., Ruel M.. Reproductive performance and nutrition during childhood. Nutr. Rev. 1996;54:S15-S21.[Medline]
25. Martorell R., Yarbrough C., Lechtig A., Delgado H., Klein R. E.. Genetic-environmental interactions in physical growth. Acta Paediatr. Scand. 1977;66:579-584.[Medline]
26. Ounsted C.. Rate of intrauterine growth. Nature (Lond.) 1969;220:599-600.
27. Ounsted M., Ounsted C.. On Fetal Growth Rateits Variations and Consequences 1973 J. B. Lippincott Co Philadelphia, PA.. .
28. Pelletier D. L., Frongillo E. A., Schroeder D. G., Habicht J.-P.. The effects of malnutrition on child mortality in developing countries. Bull. WHO 1995;73:443-448.[Medline]
29. Ramakrishnan U., Manjrekar R., Rivera J., Gonzáles-Cossío T., Martorell R.. Micronutrients and pregnancy outcomea review of the literature. Nutr. Res. 1998;19:103-159.
30. Rivera J., Martorell R., Ruel M., Habicht J.-P., Haas J.. Nutritional supplementation during the preschool years and body size and composition at adolescence. J. Nutr. 1995;125 (suppl.):1068S-1077S.
31. SAS Institute Inc. (1996) SAS-PC, Version 6.12. SAS Institiute, Cary, NC. .
32. Sanderson M., Emanuel I., Holt V. L.. The intergenerational relationship between mother's birth weight, infant birth weight and infant mortality in black and white mothers. Pediatr. Perinat. Epidemiol. 1995;9:391-405.[Medline]
33. Schroeder, D. G., Ramakrishnan, U. & Martorell, R. Nutritional determinants of growth and development. In: Child Nutrition: An International Perspective (Solomons, N. W., Brown, K. H. & Caballero, B., eds.) (in press). .
34. Stephensen C. B.. Burden of infection on growth failure. J. Nutr. 1999;129:xxxS-xxxS.
35. . UNICEF. State of the World Children Report 1998 Oxford University Press New York, NY.. .
36. . World Health Organization Working Group. Use and interpretation of anthropometric indicators of nutritional status. Bull. WHO 1986;64:929-941.[Medline]
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