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8 Effects of Gestational Weight Gain on Outcome in Singleton Pregnancies The subcommittee reviewed the evidence concerning the effects of gestational weight gain on short-term fetal, infant, and maternal health outcomes, as well as maternal factors that could modify those effects. The following outcomes were considered: fetal and neonatal mortality, fetal growth, gestational duration, spontaneous abortion (miscarriage), congen- ital anomalies, maternal mortality, complications of pregnancy, lactation performance, and postpartum obesity. The concepts and terms illustrated in Figure 2-1 were used to analyze and review published studies of human populations bearing on these potential consequences of maternal weight gain. Particular attention was given to controlling for other maternal factors that could confound the relationship between weight gain and preg- nancy outcome. Animal studies were considered only when the clinical and epidemiologic literature was too sparse or contradictory to permit rea- sonable inferences (e.g., for lactation performance). The discussion here is restricted to singleton pregnancies; twin pregnancies are considered in Chapter 9. The subcommittee focused on the links between gestational weight gain and short-term pregnancy outcomes because data relating weight gain to long-term outcomes are relatively scanty, and there is no strong evidence indicating that weight gain affects long-term outcomes directly, i.e., without first affecting shorter-term outcomes. For example, several reports (Naeye and Chez, 1981; Singer et al., 1968; Tavris and Read, 1982) have linked maternal weight gain to subsequent cognitive development in the offspring, but none has shown that such effects occur independently of the effects on 176

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GESTATIONAL WEIGHT GAIN IN SINGLETON PREGNANCIES 25 20 CO a) a: .^ 15 o 10 a) CL 5 o - \ \ >135% (Overweight) _ _ _ _ ~ 90-13 Curves Are % of Mean Prepregnancy Weight-for-Height Values (Metropolitan) . - < 90% (Underweight) 10 177 15 Pregnancy Weight Gain, kg FIGURE ~1 Pennatal mortality as a function of maternal weight gain. From Naeye (1979) with permission. fetal (including brain) growth. The long-term child health consequences of preterm birth and intrauterine growth retardation (IUGR) are reviewed briefly later in this chapter. Links between other short-term and longer- term outcomes for both mothers and children (see Figure 2-3) are discussed in Chapter 10, along with other general issues regarding the entire causal pathway. FETAL AND INFANT OUTCOMES Mortality Fetal and infant mortality rates have been used extensively to track progress in improving infant health and, indeed, to reflect the overall health status of the nation. Because these rates are quite low (approximately 1%), however, very large numbers of births are required to study the relationship between weight gain and fetal and infant deaths. Thus, few such studies have been conducted. No exceptions are the Collaborative Perinatal Project (Naeye, 1979) and a National Center for Health Statistics (NCHS) study linking data from the 1980 National Fetal Mortality Survey and the 1980 National Natality SuIvey (duffel, 1986). Data from the Collaborative Perinatal Project (Figure 8-1) indicate that the relationship between gestational weight gain and perinatal mortality is strongly influenced by maternal prepregnancy nutritional status; i.e., there is evidence for important effect modification (see Chapter 2). For women

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178 NUTRITIONAL STATUS AND WEIGHT GAIN who were underweight prior to pregnancy, the greater the gestational weight gain, the lower the perinatal mortality. However, for women with desirable prepregnancy weight for height (based on the 1959 Metropolitan Life Insurance Company's tables), perinatal mortality began to rise with gestational weight gains in excess of 11.4 kg (25 lb), which might be partially explained by a rise in the rate of high birth weight and a corresponding increased risk for shoulder dystocia and other complications of labor and delivery (see below). For weight gains above 6.8 to 7.3 kg, (15 to 16 lb) the highest perinatal mortality rates occurred among overweight women (i.e., those with prepregnancy weights greater than 135% of standard weight for height). Data shown in Figure 8-1 may be biased (because women who deliver preterm infants will have had less time to gain weight, and preterm infants are at increased risk for perinatal death). Nevertheless, other data in the same report indicate similar trends even when gestational weight gain was considered as a percentage of a gestational age-adjusted "optimum" gain. According to Naeye, the effects shown were not confounded by maternal age, parity, race, family income, number of prenatal care visits, cigarette smoking, or prior pregnancy history. The NCHS study (duffel, 1986) focused on late fetal deaths (>28 weeks of gestational age). The results, stratified by gestational age (Figure 8-2), are consistent with those from the Collaborative Perinatal Project. The trend toward higher fetal deaths per 1,000 live births for women with lower weight gains (below 11.8 kg, or 26 lb) was most marked among women with low prepregnancy weights and persisted after stratification (one variable at a time) for maternal age, education, and cigarette smoking. Beyond this direct evidence, there is a fairly strong link between fetal growth and mortality (see discussion below). Because of this strong rela- tionship, it is also reasonable to assume, even in the absence of abundant direct evidence, that any effects of gestational weight gain on intrauter- ine growth will be reflected by corresponding, albeit smaller, effects on mortality. Fetal Growth Importance of Birth Weight as a Pregnancy Outcome Infant size at birth is a key determinant of child health, especially in early infancy, but even beyond (see the review by McCormick, 1985~. As shown in Figure 8-3A, for example, neonatal mortality decreases sharply with increasing birth weight up to 2,700 or 2,800 g, declines more slowly up to 3,500 g, is relatively flat from 3,500 to 4,250 g, and then begins to rise slightly (Hogue et al., 1987~. A similar but less pronounced trend is seen for postneonatal mortality (Figure 8-3B).

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GESTATIONAL WEIGHT GAIN IN SINGLETON PREGNANCIES 60 50 40 30 a) CO o 20 In ._ m a) ._ J lo lo lo - a) Q In - Ct a) CO a) a) - _ 10 9 8 7 6 4 3 2 1 . ., i, Under 32 weeks 32-35 weeks 36 weeks AJI gestational periods 37-39 weeks 40 weeks and over . 1 1 1 1 413 ~9.3 1 ~9A' ss6 Maternal Weight Gain, kg `~5 sib\ ~67 7 179 FIGURE S-2 Fetal death ratios by maternal weight gain and period of gestation in the United States, based on data from the 1980 National Natality and National Fetal Mortality Surveys. From duffel (1986~. In an attempt to identify those infants at highest risk, many researchers and policymakers have compared infants with low birth weights (LBWs), i.e., <2,500 g, with infants who weigh more. This dichotomy is crude but provides striking contrasts in outcomes: compared with infants who weigh >2,500 g, LBW babies are nearly 40 times as likely to die during the neonatal period, and those that survive are five times as likely to die during the postneonatal period. Of those who survive infancy, LBW babies are

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18() NUTRITIONAL STATUS AND WEIGHT GAIN 1 ,000 cn ._ m ~ 100 to to to a) Q 10 in - ct o In 1,000 o 2 in ~ 100 o it g ~10 a, Q in Cat ~O -a A _ \` I'm V-N All Races Blacks Whites V'N N.x -;~ 500 1,500 ~ B 1 1 500 1,500 2,500 3,500 4,500 Birth Weight, 9 HI Races - Blacks VVhites 2,500 3,500 4,500 Birth Weight, 9 FIGURE 8-3 (A) Neonatal mortality risks By race and birth weight, United States, 1980 live birth cohort. (B) Postneonatal mortality risks by race and birth weight, United States, neonatal survivors of 1980 live-birth cohorts. From Hogue et al. (1987). about 50% more likely to have serious developmental problems or other illnesses (Shapiro et al., 1980). Further subdivisions based on birth weight have been used to refine risk categories. For example, the LBW group is often subdivided into very low birth weight (VLBW), i.e., <1,500 g, and moderately LBW, i.e., 1,500 to 2,499 g. The VLBW infants are at much greater risk of death and

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GESTATIONAL WEIGH GAIN IN SINGLETON PREGNANCIES 181 disability than are infants in the moderately LBW group (Kleinman and Kessel, 1987~. At the other end of the scale, high-birth-weight (>4,000 g) infants, especially those weighing >4,500 g, are also at higher risk than normal-weight infants (2,500 to 4,000 g) for adverse outcomes, including mortality (but less so than for the moderately LBW group; see Figure 8-3A), meconium aspiration, clavicular fracture, brachial plexus injury, and birth asphyxia (Boyd et al., 1983; Koff and Potter, 1939; Modanlou et al., 1980~. Birth weight is a composite of two outcomes: the rate of fetal growth and gestational duration. Thus, the use of birth weight often hides more than it reveals. For example, survival among VLBW infants with the same birth weights is considerably higher among those who are small for gestational age (SGA) than it is among those who have a lower gestational age but are larger for their age (Arnold et al., 1988~. A combined classification based on both birth weight and gestational age provides a more discriminating basis for etiologic and prognostic distinc- tions. It is possible to distinguish those LBW infants who are small because they are born preterm (gestational age <37 weeks) from those with IUGR (also referred to as SGA), which is usually defined as a birth weight below the 10th percentile for gestational age. This definition obviously depends on the choice of reference population. Birth weight and gestational age have independent effects on fetal and neonatal mortality (Erhardt et al., 1964; Hoffman et al., 1977; Koops et al., 1982; Lubchenco et al., 1972; Yerushalmy et al., 1965~. Both IUGR and, to a greater extent, preterm infants have an increased risk of developing cerebral palsy (Ellenberg and Nelson, 1979~. Preterm infants (especially those born extremely early) have a far greater risk of developing respira- tory distress syndrome, apnea, ~ntracranial hemorrhage, seps~s, retrolental fibroplasia, and other conditions related to physiologic immaturity. IUGR infants appear to have increased risks of hypoglycemia, hypocal- cemia, polycythemia, and birth asphyxia (Arora et al., 1987; Kramer et al., 1989; Ounsted et al., 1988; Usher, 1970~. The extent to which these neonatal complications are responsible for the increased risk of mortality or later neurocognitive deficits (see below) is not clear. Some degree of deficit in both stature and head circumference may persist (Babson, 1970; Babson and Phillips, 1973; Fancourt et al., 1976; Fitzhardinge and Inwood, 1989; Fitzhardinge and Steven, 1972; Hill et al., 1984; Low et al., 1982; Neligan et al., 1976; Ounsted and lkylor, 1971; Villa r et al., 1984; Walther, 1988; Walther and Ramaekers, 1982; Westwood et al., 1983~. Long-term deficits in neurocognitive performance have been observed in IUGR infants (Fitzhardinge and Steven, 1972; Neligan et al., 1976; Ounsted et al., 1984; Rubin et al., 1973; Westwood et al., 1983; Ylitalo et al., 1988~. However, since asphyxia is a frequent concomitant of growth retardation and studies

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182 NUTRITIONAL STATUS AND WEIGHT GAIN have not been limited to nonasphyxiated infants (Westwood et al., 1983), the magnitude of neurocognitive deficits due to growth retardation may be somewhat less than is generally reported. Heterogeneity of IUGR Several methodologic issues should be kept in mind before considering the relationship between gestational weight gain and fetal growth. Problems include measurement of gestational age, as discussed in Chapter 4, and the definition of retarded fetal growth (IUGR). Growth-retarded infants represent a highly heterogeneous group in terms of etiology, severity, and body proportionality. A number of chromosomal and other congenital anomalies associated with growth retardation may lead to prognoses much worse than those for infants without those anomalies. Major congenital anomalies affect only a small percentage of IUGR infants but account for a disproportionate number of deaths. For example, Ounsted et al. (1981) reported that 6.9% of the IUGR infants in their study had such anomalies but represented 62% of the total deaths. It would be quite surprising if two full-term infants, one weighing 2,000 g and the other weighing 2,800 g, had the same prognosis for subsequent morbidity and mortality. Yet, follow-up studies have not subdivided their IUGR cohorts by severity of growth retardation. Thus, little is known about the magnitude of such prognostic distinctions. In recent studies, IUGR infants have been subdivided according to their body proportions, especially as defined by Rohrer's ponderal index (birth weight divided by the length cubed). Those with low ponderal indices are said to be d~sproporaonal (also referred to as asymmetric or wasted). Several investigators have reported higher neonatal mortality rates among disproportional IUGR infants (Guaschino et al., 1986; Haas et al., 1987; Hoffman and Bakketeig, 1984), but better early catch-up growth and better prognoses for long-term growth and development than for those among proportional IUGR infants (Fancourt et al., 1976; Harvey et al., 1982; Hill et al., 1984; Villar et al., 1984~. Unfortunately, most studies in this area have not controlled for the severity of IUGR, with which disproportionality appears to be associated (Kramer et al., 1989), nor have they ensured accurate measurements of gestational age or controlled for confounding by short maternal stature or the postnatal nutritional and other environmental influences listed in Figure 2-2. Other Methodologic Caveats Interpretation of the literature relating gestational weight gain to fetal growth requires adequate consideration of several other factors: problems in measurement of length of gestation and gestational weight gain (Chapter

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GESTATIONAL WEIGHT GAIN IN SINGLETON PREGNANCIES 183 4), differences in components of the gain (Chapter 6), and maternal factors that might either confound or modify the relationship (Chapter 5~. The subcommittee emphasizes that use of total weight gain leads to overstatements of the association between gestational weight gain and fetal growth. That is, if the baby's weight is not subtracted from the mother's weight gain, the association is biased by a part-whole correlation problem (i.e., y is being correlated with x + y). Net gain avoids this problem by subtracting the baby's weight. Overstatements of the association of gestational weight gain and fetal growth are also expected unless birth weight is adjusted for gestational age, either by dividing net weight gain by the number of weeks of gestation or by using analytic methods to adjust for the expected gain at each week of gestation. The most appropriate measure of weight gain would be based on serial measurements of weight gain (i.e., the pattern of weight gain) during the course of normal pregnancies. Effects on Birth Weight (for Gestational Age) Despite the methodologic caveats discussed in the preceding section, the published data concerning the effect of gestational weight gain on fetal growth are quite convincing. Methodologically acceptable studies have been virtually unanimous in reporting a positive relationship of gestational weight gain with gestational age-adjusted birth weight and with the risk for IUGR. Based on a meta-analysis (Kramer, 1987) of 61 English- and French-language studies published between 1970 and 1984, the average magnitude of the effect on mean birth weight in women with adequate prepregnancy weight for height is approximately 20 g/kg of total weight gain. The relative risk for IUGR in women with low (<7 kg, or 15 lb) total gestational weight gain is approximately 2.0. Given the prevalence of low weight gain, the etiologic fraction (population attributable risk) in women with average prepregnancy weight for height in developed countries is approximately 14%. In other words, low weight gain can account for about one in seven cases of IUGR. All these quantitative estimates are likely to be inflated, because they are based on total weight gain and thus reflect some degree of part-whole correlation. The effect on mean birth weight, for example, appears to be reduced by about one-third (from 20 to 13 g/kg) when based on net gain rather than total gain (Kramer et al., 1989~. Investigators who have examined the effect of a given gestational weight gain in women with different prepregnancy weight-for-height status have been virtually unanimous in concluding that the two factors strongly interact (i.e., that prepregnancy weight for height is an effect modipery (see Chapter 2~. Miller and Merritt (1979), for example, showed a clear trend for increasing rates of IUGR with decreasing prepregnant weight

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184 NUTRITIONAL STATUS AND WEIGHT GAIN 3,600 3,500 , 3 400 ~, ._ a) s m a) ._ an 3,300 3,200 3,100 3,000 2,900 Very Overweight - Moderately Overweight ~~ Ideal weight/' ~ Underweight I 1 1 1 1 1 1 1 1 0 2 4 6 8 10 12 14 16 18 20 Maternal Weight Gain, kg FIGURE 8-4 Birth weight as a [unction of maternal weight and prepregnangy weight for height. Adapted from Abrams and Laros (1986) with permission. for height among women with low gestational weight gain. Similar results were reported in several studies investigating mean birth weight (Abrams and Laros, 1986; Frentzen et al., 1988; Mitchell and Lerner, 1989; Naeye, 1981b,d; Seidman et al., 1989; Winikoff and Debrovner, 1981~. Illustrative data from Abrams and Laros (1986), as adapted by B. Abrams (University of California at Berkeley, personal communication, 1989), are shown in Figure 8-4. Thus, underweight women appear to derive a greater benefit from a given gestational weight gain than do those with adequate or excessive weights. Nonetheless, prepregnancy weight for height is itself a determinant of fetal growth above and beyond the effect of gestational weight gain (Kramer, 1987~. Women who are thinner before pregnancy tend to have smaller babies than do heavier women with the same weight gain. Thus, desirable weight gains in thin women are higher than those in normal- weight women, despite the effect modification, and desirable weight gains for overweight and obese women are lower. The effect of gestational weight gain on fetal growth is weak, or perhaps

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GESTATIONAL WEIGHT GAIN IN SINGLETON PREGNANCIES 185 even absent, in obese women (~35% of standard prepregnancy weight for height) (Abrams and Laros, 1986; Brown et al., 1986; Frentzen et al., 1988; Harrison et al., 1980; Luke et al., 1981; Mitchell and Lerner, 1987; Naeye, 1981b; Rosso, 1985; Winikoff and Debrovner, 1981~. Nonetheless, obese women clearly have infants that are larger than those of nonobese women for the same weight gain (Kramer, 1987~. It seems prudent to recommend that obese women gain a minimum equivalent to the weight of the products of conception (6.8 kg, or 15 lb), although lower weight gains in such women are often compatible with optimal birth weights. The subcommittee has not identified an upper limit for this group. The evidence for other effect modifiers is not nearly as strong as that for prepregnancy weight for height. Recent data indicate that the relationship of gestational weight gain to fetal growth is similar in adolescents and older women after controlling for prepregnancy weight for height and other potentially confounding differences (Scholl et al., 1988), although one recent Israeli study reported a substantially (but nonsignificantly) reduced relationship in women under age 20 (Seidman et al., 1989~. These data are concordant with the results of several earlier studies indicating no significant differences in fetal growth in adolescents (even those within 1 or 2 years of menarche), once differences in gestational weight gain, prepregnancy weight, and other confounders have been controlled (Duenhoelter et al., 1975; Horon et al., 1983; Scholl et al., 1984), thus undermining the notion of a competition between the adolescent's own requirements for growth and those of the fetus. Research findings have not been unanimous on this point, however, especially for younger adolescents (<16 years). In an analysis of young, black adolescent mothers in the Collaborative Perinatal Project, Naeye (1981d) found significantly lower mean birth weights among infants born at 38 to 44 weeks of gestation to nonsmokers who were not obese prior to pregnancy. This was particularly true in those aged 10 to 14, in whom deficits averaged approximately 150 to 200 g. However, potential differences in alcohol or drug use were not controlled. In a study of poor, young, urban Peruvian mothers, Frisancho et al. (1985) reported a birth weight deficit of approximately 200 g in young adolescents (<15 years) compared with that in older women (17 to 25 years), even after controlling for gestational weight gain. But these results were not controlled for potentially confounding differences in parity or socioeconomic status. A recent study from New York City (Haiek and Lederman, 1989) showed large (200 to 400 g) deficits in birth weight among full-term infants born to young adolescents (<15 years) compared with those born to 19- to 30-year-old women, even after stratification by weight for height at full-term, unless the adolescents had achieved 140~o of their standard (nonpregnant) weight for height.

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186 NUTRITIONAL STATUS AND WEIGHT GAIN Potentially confounding differences in cigarette, alcohol, and drug use were not controlled. Even those studies showing reduced fetal growth in young adolescents do not necessarily demonstrate a true effect modification of weight gain by age. Even if the infants of young teenage mothers have lower birth weights for gestational age after controlling for gestational weight gain (and a variety of potential confounders), this may not indicate a smaller effect of a given weight gain on fetal growth. The lower birth weights might reflect true biologic differences in potential for fetal growth (perhaps related to the young adolescents' own nutritional requirements for growth (Scholl et al., 1989) or to other, unknown mechanisms) in fetal growth or unmeasured or inadequately controlled confounding factors. Of the three studies cited above (Frisancho et al., 1985; Haiek and Lederman, 1989; Naeye, 1981d), only Frisancho et al. present data that directly bear on effect modification. Although the regression coefficients (adjusted slopes) for gestational weight gain in that study decrease with lower maternal age (13 to 15 years), the absolute magnitude of the slopes for 16 year aids (44.4-g birth weight per kilogram of total gestational weight gain) and 17 to 25 year olds (52.2 g/kg) is far higher than the usual effect size of approximately 20 g/kg cited above and, therefore, is difficult to accept at face value, even considering the poor, potentially undernourished population under study. These extremely large effect sizes strongly suggest the existence of residual confounding by socioeconomic or other differences. But lower birth weights seen in infants of young adolescents compared with those seen in infants of older women with the same weight gain, even in the absence of effect modification, argue for promotion of weight gains toward the upper end of the range recommended for older women with a similar weight for height. The subcommittee was able to locate only a single study (Seidman et al., 1989) bearing on possible effect modification by older age (i.e., >35 years). That study reported a slightly but significantly increased effect of gestational weight gain in Israeli women over age 30 as compared with those between the ages of 20 and 30, after controlling for prepregnancy weight for height and other potential confounding variables. (The reported effect was 16.6- compared with 14.0-g birth weight per kilogram of gestational weight gain, respectively.) In addition, since weight does increase with age, older women might be protected to some degree against the adverse effects of low weight gains. Few data are available concerning differences in the effect of weight gain on fetal growth among women of different racial or ethnic back- grounds. Analysis of the 1980 National Natality Survey Duffel, 1986), however, indicates similar effects of gestational weight gain on mean birth weight among white as well as black women. But as with the case of young

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GESTATIONAL WEIGHT GAIN IN SINGLETON PREGNANCIES 201 of subsequent gestational hypertensive disorders, but firmer inferences must await the results of future research. As previously discussed, large gestational weight gains are associated with an increased risk of high birth weight and a corresponding increase in risk for dysfunctional labor, midforceps delivery, and cesarean delivery (Boyd et al., 1983; Koff and Potter, 1939; Modanlou et al., 1980~. Moreover, there is some evidence that these consequences of fetopelvic disproportion are exacerbated in women with short stature or small pelvic size (Frame et al., 1985; Hughes et al., 1987~. Cesarean delivery rates have skyrocketed over the last 15 to 20 years (Placek and Taffel, 1980; Placek et al., 1983), but the remarkable increase has been accompanied by rather modest increases in the rates of high birth weight (see Chapter 3~. Thus, even if larger gestational weight gains are partly responsible for the trend toward slightly larger infants, their contribution to complications of labor and delivery must be quite small. Varma (1984) examined the direct relationship between gestational weight gain and pregnancy complications. Although he reports a signifi- cantly higher rate of forceps and cesarean deliveries among women with fetal weight gains >16 kg (35.2 lb), and especially >21 kg (46.2 lb), these re- sults are unadjusted for potentially confounding differences among women with different weight gains. Using a more sophisticated multivariate ap- proach, however, Shepard et al. (1986) confirmed that women with large weight gains (~35% of their prepregnancy weight) had higher rates of cesarean deliveries and other operative deliveries (forceps and vacuum extraction), as well as a prolonged second stage of labor. Lactation Performance There is a general perception that fat deposition during pregnancy is required for optimal lactation performance. Although several studies have examined the relationship between milk production and maternal nutrition during lactation, few have related lactation performance to gestational weight gain. In one longitudinal study of well-nourished women in the United States, gestational weight gain was not related to milk quantity or quality (Butte et al., 1984~. Fat mobilization was not a prerequisite to adequate milk production, as indicated by the inverse relationship between the amount of energy mobilized from maternal stores and dietary energy intake. Other studies on humans do not support the hypothesis that fat de- posited during pregnancy is necessarily mobilized later during lactation. In one study of Swedish women, the mean gestational weight gain (13.8 kg, or ~30 lb) included substantial quantities of fat (5.8 kg, or ~13 lb) (Sadurskis et al., 1988~. During the first 2 months of lactation, total body fat did not

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202 NUTRITIONAL STATUS AND WEIGHT GAIN change; milk production and composition were normal. Energy costs of lactation were met by increased energy intake, not by body fat mobilization. By contrast, investigators from The Gambia have inferred that fat deposition during pregnancy is of crucial importance for lactation perfor- mance. In one Gambian study, milk output at 3 months post partum was negatively correlated with the change in skinfold thicknesses from 6 to 12 weeks post partum (Paul et al., 1979~. In women who were replenish- ing their fat stores during the dry (harvest) season, milk output was low. Although the investigators interpreted this observation to indicate compe- tition between replenishment of maternal body fat and milk production, the data are also consistent with mobilization of maternal fat for milk pro- duction. Subsequent, conflicting results indicated higher milk production rates during the dry season compared with those during the wet (farming) season (Prentice and Whitehead, 1987~. One study conducted in East Java, Indonesia, demonstrated that energy supplementation in the last trimester of pregnancy did not increase milk output among women with habitually low energy intakes (van Steenbergen et al., 1989~. The limited evidence from studies on the relationship between ges- tational weight gain and lactation performance in humans can be supple- mented with findings from animal studies. Extrapolation of data on re- production from nonprimate animal models to humans can be hazardous, since marked differences in the energy costs of gestation and lactation exist between primates and other mammals. Nonetheless, the evidence from animal studies indicates that gestaizonal nutrition is less important than postpartum nutrition for lactation (Jenness, 1986; Kliewer and Rasmussen, 1987; Lodge, 1969; O'Grady et al., 1973; Sadurskis, 1988~. This evidence thus supports the notion that gestational weight gain in humans has little impact on subsequent milk quantity or quality. Postpartum Obesity It is often alleged that women in developing countries become pro- gressively malnourished (experience maternal depleiion) and have corre- spondingly worse outcomes with successive pregnancies (Jelliffe, 1966~. In contrast, many investigators report a net increase in body weight among women in industrialized countries during the interconceptional period that may persist and even increase with successive pregnancies. Studies by Stander and Pastore (1940), Beazley and Swinhoe (1979), and Samra et al. (1988) did not control for the expected weight increase that normally occurs with age. In several population-based cross-sectional studies (Forster et al., 1986; Heliovaara and Aromaa, 1981; McKeown and Record, 1957; Newcombe, 1982; Noppa and Bengtsson, 1980), stratification or multivariate statistical approaches have been used to adjust for the

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GESTATIONAL WEIGHT GAIN IN SINGLETON PREGNANCIES 203 confounding effect of age and, in some cases, for interpregnancy interval, socioeconomic status, and other potential confounders. But cross-sectional studies are prone to cohort effects; i.e., there has been a trend over time toward higher total body weights at any given age and parity. A recent longitudinal study in The Netherlands (Rookus et al., 1987) reported a slightly (but nonsignificantly) higher increase in BMI at 9 months post partum in 49 pregnant women compared with that in 400 nonpregnant controls followed for the same period. Similarly, in a cross-sectional study (Cederlof and Kaij, 1970) comparing parous monoygotic twins with their childless co-twins, and in longitudinal studies of repeated pregnancies in Scotland (Billewicz and Thomson, 1970) and the United States (Greene et al., 1988), an independent effect of parity on body weight was confirmed. Overall, the evidence suggests an average weight retention of approximately 1 kg (2.2 lb) per birth. The studies in Scotland and the United States are the only ones found by the subcommittee that attempt to relate the magnitude of the parity effect to the amount of weight gained in the preceding pregnancies. Billewicz and Thomson (1970) reported that weight increases (adjusted for age and cohort effects) above 2.5 kg (5.5 lb) between the first and second pregnancies were associated with high weight gains (average 10 to 12 kg, or 22 to 26 lb) after 20 weeks of gestation during the first pregnancy. Greene et al. (1988) reported an analysis of 7,116 women who had at least two singleton births in the 1959-1965 Collaborative Perinatal Project. There was a monotonic trend toward increasing (adjusted) interpregnancy retention of weight with increasing gestational weight gains in the earlier pregnancy. For the minority of women who had very high gestational weight gains, the increases were substantial: 5 kg (10.9 lb) for women gaining 16.4 to 18.2 kg (36 to 40 lb) and 8.0 kg (17.7 lb) for those gaining more than 18.2 kg. (The mean weight gain among the study women was 9.5 kg, or 20.8 lb.) These data should be interpreted with caution, however, since the pregnancies studied occurred nearly four decades ago, when gestational weight gains were considerably lower than those observed more recently (see Chapter 3~. Women gaining >16.4 kg (36 lb) represented only 8% of those studied; that percentage would be far higher today. The fact that the study population was skewed toward black, urban, and poor women and was restricted to the 7,116 women with at least two singleton births during the study period (out of the 58,760 total study population) also limits the generalizabili~ of the findings. In summary, the evidence suggests that women with average gestational weight gains retain about 1 kg (2.2 lb) above and beyond their expected weight increase with age. The 1-kg figure is based largely on data from older studies, however, and may underestimate weight retention associated with the higher gestational weight gains seen in recent years. Women

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204 NUTRITIONAL STATUS AND WEIGHT GAIN with very large weight gains appear to be at risk for considerably larger postpartum weight increases. For women who are well- or over-nourished prior to pregnancy, these large increases may contribute to the development of obesity and its adverse health sequelae. Since a given weight increase will have a greater impact on relative weight and, hence, obesity in short women, large weight gains may be particularly undesirable in such women. Further studies are required to document the effects of high gestational weight gain on subsequent maternal obesity. SUMMARY A large body of evidence indicates that gestational weight gain is a determinant of fetal growth, although the magnitude of the causal impact is somewhat less than that usually reported because of the failure of previous studies to adjust total weight gain for fetal weight. Even after such adjustment, however, lower net weight gains are associated with an increased risk of IUGR and increased perinatal mortality (probably mediated by effects on IUGR), whereas higher weight gains are associated with high birth weight and, secondarily, prolonged labor, shoulder dystocia, cesarean delivery, and birth trauma and asphyxia. There is convincing evidence that the effect of maternal weight gain on fetal growth is modified by pregnancy weight for height. Published data do not suggest an effect modification by age or ethnic background. Data concerning the effects of maternal weight gain on gestational duration are suggestive but less conclusive, particularly in light of the difficulties in determining gestational age with accuracy. Further research is clearly indicated in this area, because even small reductions in risk for preterm deliveries, especially those that occur very early in gestation, would have a favorable impact on perinatal and later mortality and on infant and child morbidity and performance. There is little evidence to suggest an important association between gestational weight gain and spontaneous abortion (miscarriage), congeni- tal anomalies, maternal mortality, or lactation performance. There does appear to be a statistical association with PIH and preeclampsia, but it is difficult to interpret this association because of directionality (increased body water leads to increased weight gain) and the absence of data relating PIH to early gestational changes in maternal fat or lean body mass. Pregnancy, in general, and gestational weight gain, in particular, are associated with retained maternal weight post partum. Women with ex- tremely high weight gains during pregnancy may be at increased risk of subsequent obesity.

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GESTATIONAL WEIGHT GAIN IN SINGLETON PREGNANCIES CLINICAL IMPLICATIONS 205 Recommendations for gestational weight gain must be based on an adequate appreciation of potential benefits and risks for fetal growth, perinatal mortality, complications of labor and delivery, and birth trauma and asphyxia. Desirable weight gains are highest in thin women and lowest In obese, overweight, and short women (see Bible 1-1 in Chapter 1~. Young adolescent and black mothers should be encouraged to strive for weight gains toward the upper range desirable for adult white mothers with similar prepregnancy weights for height and heights. REFERENCES Abrams, B.F., and R.K Laros, Jr. 1986. Prepregnancy weight, weight gain, and birth weight. Am. J. Obstet. Gynecol. 154:503-509. Abrams, B., V. Newman, T. Key, and J. Parker. 1989. Maternal weight gain and preterm delivery. Obstet. Gynecol. 74:577-583. Acker, D.B., B.P. Sachs, and E.^ Friedman. 1985. Risk factors for shoulder dystocia. Obstet. Gynecol. 66:762-768. Anonymous. 1917. Eclampsia rare on war diet in Germany. J. Am. Med. Assoc. 68:732. Arnold, C.C., C.A. Hobbs, R.H. Usher, and M.S. Kramer. 1988. What's wrong with the concept of 'fiery low birth weight" (VLBW)? Pediatr. Res. 23:288A. Arora, N.K., V.K. Paul, and M. Singh. 1987. Morbidity and mortality in term infants with intrauterine growth retardation. J. Stop. Pediatr. 33:186-189. Babson, S.G. 1970. Growth of low-birth-weight infants. J. Pediatr. 77:11-18. Babson, S.G., and D.S. Phillips. 1973. Growth and development of twins dissimilar in size at birth. N. Engl. J. Med. 289:937-940. Beazley, J.M., and R.J. Swinhoe. 1979. Body weight in parous women: is there any alteration between successive pregnancies? Acta Obstet. Gynecol. Scand. 58:45-47. Berkowitz, G.S. 1981. An epidemiologic study of pretend delivery. Am. J. Epidemiol. 113:81-92. Billewicz, W.Z., and A M. Thomson. 1970. Body weight in parous women. Br. J. Prev. Soc. Med. 24:97-104. Boyd, M.E., R.H. Usher, and F.H. McLean. 1983. Fetal macrosomia: prediction, risks, proposed management. Obstet. Gynecol. 61:715-722. Bnend, A. 1985. Do maternal energy reserves limit fetal growth? Lancet 1:38-40. Brown, J.E., K.W. Berdan, P. Splett, M. Robinson, and L^J. Harris. 1986. Prenatal weight gains related to the birth of healthy-sized infants to low-income women. J. Am. Diet. Assoc. 86:1679-1683. Buehler, J.W., AM. Kaunitz, CJ.R. Hogue, J.M. Hughes, J.C. Smith, and R.W. Rochat. 1986. Maternal mortality in women aged 35 years or older United States. J. Am. Med. Assoc. 255:53-57. Butte, N.F., C. Garza, J.E. Stuff, E.O. Smith, and B.L. Nichols. 1984. Effect of maternal diet and body composition on lactational performance. Am. J. Clin. Nutr. 39:296-306. Campbell, D.M., and I. MacGillivray. 1975. The effect of a low calorie diet or a thiazide diuretic on the incidence of pre-eclampsia and on birth-weight. Br. J. Obstet. Gynaecol. 82:572-577. Campbell-Brown, M., and I.R. McFadyen. 1985. Maternal energy reserves and birthweight. Lancet 1:574-575. Cederlof, R., and L. Kaij. 1970. The effect of childbearing on body-weight. Acta Psychiatr. Scand., Suppl. 219:47-49.

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206 NUTRITIONAL STAINS AND WEIGHT GAIN Chesley, L C. 1976. Blood pressure, edema and proteinuria in pregnancy. 1. Historical developments. Prog. Clin. Biol. Res. 7:19 66. Duenhoelter, J.H., J.M. Jimenez, and G. Baumann. 1975. Pregnancy performance of patients under fifteen years of age. Obstet. Gynecol. 46:49-52. Duffus, G.M., I. MacGillivray, and KJ. Dennis. 1971. Ibe relationship between baby weight and changes in maternal weight, total body water, plasma volume, electrolytes and proteins, and urinary oestriol excretion. J. Obstet. Gynaecol. Br. Commonw. 78:97-104. Ellenberg, J.H., and KB. Nelson. 1979. Birth weight and gestational age in children with cerebral palsy or seizure disorders. Am. J. Dis. Child. 133:1044-1048. Erhardt, C.L., G.B. Joshi, F.G. Nelson, B.FI. Kroll, and L. Weiner. 1964. Influence of weight and gestation on perinatal and neonatal mortality by ethnic group. Am. J. Public Health 54:1841-1855. Fancourt, R., S. Campbell, D. Harvey, and ~P. Norman. 1976. Follow-up study of small-for-date babies. Br. Med. J. 1:1435-1437. Fitzhardinge, P.M., and S. Inwood. 1989. Long-term growth in small-for-date children. Acta Paediatr. Scand., Suppl. 349:27-33. Fitzhardinge, P.M., and E.M. Steven. 1972. Il~e small-for-date infant. I. Later growth patterns. Pediatrics 49:671-681. Forster, J.L, E. Bloom, G. Sorensen, R.W. Jeffe~y, and RJ. Prineas. 1986. Reproductive history and body mass index in black and white women. Prev. Med. 15:685-691. Frame, S., J. Moore, A. Peters, and D. Hall. 1985. Maternal height and shoe size as predictors of pelvic disproportion: an assessment. Br. J. Obstet. Gynaecol. 92:1239- 1245. Frentzen, B.H., D.L Dimperio, and AC. Cruz. 1988. Maternal weight gain: effect on infant birth weight among overweight and average-weight low-income women. Am. J. Obstet. Gynecol. 159:1114-1117. Frisancho, AR., J.E. Klayman, and J. Matos. 1977. Influence of maternal nutritional status on prenatal growth in a Peruvian urban population. Am. J. Phys. Anthropol. 46:265-274. Frisancho, A.R., J. Matos, W.R. Leonard, and L.A. Yaroch. 1985. Developmental and nutritional determinants of pregnancy outcome among teenagers. Am. J. Phys. Anthropol. 66:247-261. Greene, G.W., H. Smiciklas-Wright, T.O. Scholl, and RJ. Karp. 1988. Postpartum weight change: how much of the weight gained in pregnancy will be lost after delive~y? Obstet. Gynecol. 71:701-707. Gross, S., C. Librach, and A. Cecutti. 1989. Maternal weight loss associated with hyperemesis gravidarum: a predictor of fetal outcome. Am. J. Obstet. Gynecol. 160:906-909. Guaschino, S., A. Spinillo, E. Stola, P.C Pesando, G.P. Gancia, and G. Rondini. 1986. The significance of ponderal index as a prognostic factor in a low-birth-weight population. Biol. Res. Preg. Perinatol. 7:121-127. Haas, J.D., H. Balcazar, and L. Caulfield. 1987. Variation in early neonatal mortality for different types of fetal growth retardation. Am. J. Phys. Anthropol. 73:467-473. Haiek, L., and S.A. Lederman. 1989. The relationship between maternal weight for height and term birth weight in teens and adult women. J. Adol. Health Care 10:16-22. Harrison, G.G., J.N. Udall, and G. Morrow III. 1980. Maternal obesity, weight gain in pregnancy, and infant birth weight. Am. J. Obstet. Gynecol. 136:411-412. Harvey, D., J. Prince, J. Bunton, C Parkinson, and S. Campbell. 1982. Abilities of children who were small-for-gestational-age babies. Pediatrics 69:296-300. Hediger, M.L., T.O. Scholl, D.H. Belsky, I.G. Ances, and R.W. Salmon. 1989. Patterns of weight gain in adolescent pregnancy: effects on birth weight and preterm delive~y. Obstet. Gynecol. 74:6-12. Heliovaara, M., and A. Aromaa. 1981. Parity and obesiW. J. Epidemiol. Community Health 35:197-199.

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GESTATIONAL WEIGHT GAIN IN SINGLETON PREGNANCIES 207 Herrera, M.G., J.O. Mora, B. de Paredes, and M. Wagner. 1980. Maternal weight/height and the effect of food supplementation during pregnancy and lactation. Pp. 252-263 in H. Aebi and R. Whitehead, eds. Maternal Nutrition during Pregnancy and Lactation. Hans Huber, Bern. Hill, R.M., SUM. Ve~niaud, R.L. Deter, L M. Tennyson, G.M. Rettig, T.E. Zion, A.L. Vorderman, P.G. Helms, L^B. McCulley, and L L. Hill. 1984. The effect of intrauterine malnutrition on the term infant: a 14-year progressive study. Acta Paediatr. Scand. 73:482-487. Hingson, R., JJ. Alpert, N. Day, E. Dooling, H. Kayne, S. Morelock, E. Oppenheimer, and B. Zuckerman. 1982. Effects of maternal drinking and marijuana use on fetal growth and development. Pediatrics 70:539-546. Hoffman, HJ., and L S. Bakketeig. 1984. Heterogeneity of intrauterine growth retardation and recurrence risks. Semin. Perinatol. 8:15-24. Hoffman, H.J., F.E. Lundin, Jr., US. Bakketeig, and E.E. Harley. 1977. Classification of births by weight and gestational age for future studies of prematurity. Pp. 297-333 in D.M. Reed and F.J. Stanley, eds. The Epidemiology of Prematurity. Urban & Schwa~zenberg, Baltimore. Hague, CJ.R., J.W. Buehler, L.T. Strauss, and J.C Smith. 1987. Overview of the National Infant Mortality Surveillance (NIMS) Project-design, methods, results. Public Health Rep. 102:126-138. Horon, I.L., D.M. Strobino, and H.M. MacDonald. 1983. Birth weights among infants born to adolescent and young adult women. Am. J. Obstet. Gynecol. 146:444449. Hughes, A.B., D.A. Jenkins, R.G. Newcombe, and J.F. Pearson. 1987. Symphysis-fundus height, maternal height, labor pattern, and mode of delivery. Am. J. Obstet. Gynecol. 156:644-648. Hytten, F.E., and A.M. Thomson. 1976. Weight gain in pregnancy. Pp. 179-187 in M.D. Lindheimer, HI. Katz, and F.P. Zuspan, eds. Hypertension in Pregnancy. John Wiley & Sons, New York. Jelliffe, D.B. 1966. The Assessment of the Nutritional Status of the Community. WHO Monograph Series No. 53. World Health Organization, Geneva. 271 pp. Jenness, R. 1986. Lactational performance of various mammalian species. J. Dairy Sci. 69:869-885. Kaminski, M., and E. Papiernik. 1974. Multifactorial study of the risk of prematurity at 32 weeks of gestation. II. A comparison between an empirical prediction and a discriminant analysis. J. Perinat. Med. 2 37-44. Kleinman, J.C. 1990. Maternal Weight Gain During Pregnancy Determinants and Conse- quences. NCHS Working Paper Series No. 33. National Center for Health Statistics, Public Health Service, U.S. Department of Health and Human Services, Hyattsville, Md. 24 pp. Kleinman, J.C., and S.S. Kessel. 1987. Racial differences in low birth weight: trends and risk factors. N. Engl. J. Med. 317:749-753. Kliewer, R.L., and K.M. Rasmussen. 1987. Malnutrition during the reproductive cycle: effects on galactopoietic hormones and lactational performance in the rat. Am. J. Clin. Nutr. 46:926-935. Koff, ~K, and E.L Potter. 1939. The complications associated with excessive development of the human fetus. Am. J. Obstet. Gynecol. 38:412423. Koops, B.L~, LO. Morgan, and F.C. Battaglia. 1982. Neonatal mortality risk in relation to birth weight and gestational age: update. J. Pediatr. 101:969-977. Kramer, M.S. 1987. Determinants of low birth weight: methodological assessment and meta-analysis. Bull. W.H.O. 65:663-737. Kramer, M.S., F.H. McLean, M. Olivier, D.M. Willis, and R.H. Usher. 1989. Body proportionality and head and length 'sparing' in growth-retarded neonates: a critical reappraisal. Pediatrics 84:717-723. Langhoff-Roos, J., G. Lindmark, and M. Gebre-Medhin. 1987. Maternal fat stores and fat accretion during pregnancy in relation to infant birthweight. Br. J. Obstet. Gynaecol. 94:1170-1177.

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208 NUTRITIONAL STATUS AND WEIGHT GAIN Lawton, F.G., G.C. Mason, Key Kelly, I.N. Ramsay, and G.A. Morewood. 1988. Poor maternal weight gain between 28 and 32 weeks gestation may predict small-for- gestational-age infants. Br. J. Obstet. Gynaecol. 95:884887. Lazar, R. 1981. General commentary. Pp. 181-186 in J. Dabbing, ed. Maternal Nutrition in Pregnancy: Eating for Two? Academic Press, London. Lechtig, A, J.P. Habicht, H. Delgado, R.E. Klein, C. Yarbrough, and R. Martorell. 1975. Effect of food supplementation during pregnancy on birthweight. Pediatrics 56:508-520. Lodge, G.A. 1969. The effects of pattern of feed distribution during the reproductive cycle on the performance of sows. Anim. Prod. 11:133-143. Low, J.A., R.S. Galbraith, D. Muir, H. Killen, B. Pater, and J. Karchmar. 1982. Intrauterine growth retardation: a study of long-term morbidity. Am. J. Obstet. Gynecol. 142:670- 677. Lubchenco, LO., D.T. Searls, and J.V. Brazie. 1972. Neonatal mortality rate: relationship to birth weight and gestational age. J. Pediatr. 81:814-822. Luke, B., C. Dickinson, and R.H. Petrie. 1981. Intrauterine growth: correlations of maternal nutritional status and rate of gestational weight gain. Eur. J. Obstet., Gynecol. Reprod. Biol. 12:113-121. Maso, M.J., EJ. Gong, M.S. Jacobson, D.S. Bross, and F.P. Heald. 1988. Anthropometric predictors of low birth weight outcome in teenage pregnancy. J. Adol. Health Care 9:188-193. McCormick, M.C. 1985. The contribution of low birth weight to infant mortality and childhood morbidity. N. Engl. J. Med. 31282-90. McKeown, T., and R.G. Record. 1957. The influence of reproduction on body weight in women. J. Endocrinol. 15:393-409. Metropolitan Life Insurance Company. 1959. New weight standards for men and women. Stat. Bull. Metrop. Life Insur. Co. 40:1-4. Miller, H.C., and T.^ Merritt. 1979. Fetal Growth in Humans. Year Book Medical Publishers, Chicago. 180 pp. Mitchell, M.C., and E. Lerner. 1987. Factors that influence the outcome of pregnancy in middle-class women. J. Am. Diet. Assoc. 87:731-735. Mitchell, M.C., and E. Lerner. 1989. Weight gain and pregnancy outcome in underweight and normal weight women. J. Am. Diet. Assoc. 89:634-638. Modanlou, H.D., W.L Dorchester, A. Thorosian, and R.K Freeman. 1980. Macrosomia maternal, fetal, and neonatal implications. Obstet. Gynecol. 55:420-424. Mora, J.O., B. de Paredes, M. Wagner, L~ de Navarro, J. Suescum, N. Christiansen, and M.G. Herrera. 1979. Nutritional supplementation and the outcome of pregnancy. I. Birth weight. Am. J. Clin. Nutr. 32:455-462. Naeye, R.L 1979. Weight gain and the outcome of pregnancy. Am. J. Obstet. Gynecol. 135:3-9. Naeye, R.L~ 1981a. Maternal blood pressure and fetal growth. Am. J. Obstet. Gynecol. 141:780-787. Naeye, R.L~ 1981b. Maternal nutrition and pregnancy outcome. Pp. 89-111 in J. Dobbing, ed. Maternal Nutrition in Pregnancy: Eating for Two? Academic Press, London. Naeye, R.L" 1981c. Nutritional/nonnutritional interactions that affect the outcome of pregnancy. Am. J. Clin. Nutr. 34:727-731. Naeye, R.L~ 1981d. Teenaged and pre-teenaged pregnancies: consequences of the fetal- maternal competition for nutrients. Pediatrics 67:146-150. Naeye, R.L~, and R.A. Chez. 1981. Effects of maternal acetonuria and low pregnan~y weight gain on children's psychomotor development. Am. J. Obstet. Gynecol. 139:189-193. NCHS (National Center for Health Statistics). 1987. Vital Statistics of the United States, 1983. Vol. ~Mortality, Part A. DHHS Publ. No. (PHS) 87-1102. National Center for Health Statistics, Public Health Service, U.S. Department of Health and Human Services, Hyattsville, Md. 713 pp. Neligan, G.A., I. Kolvin, D.McI. Scott, and R.F. Garside. 1976. Born Too Soon or Born Too Small: A Follow-up Study to Seven Years of Age. Clinics in Developmental Medicine, No. 61. Heineman, London. 101 pp.

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