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Articles

Low Maternal Weight Gain in the Second or Third Trimester Increases the Risk for Intrauterine Growth Retardation¹

Division of Pediatric Gastroenterology and Nutrition, UMDNJ-Robert Wood Johnson School of Medicine, New Brunswick, NJ and ^* Division of Pediatric Gastroenterology and Nutrition, The Floating Hospital for Children at New England Medical Center and Tufts University School of Medicine, Boston, MA

²To whom correspondence should be addressed.

	ABSTRACT

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Low maternal weight gain during pregnancy has been suggested as a cause of intrauterine growth retardation (IUGR). However, pregnancy weight gain and fetal growth vary greatly throughout pregnancy. We examined the relationship between maternal weight gain in individual trimesters to the risk of IUGR in 10,696 women enrolled in the National Collaborative Perinatal Project (NCPP) and the Child Health and Development Study (CHDS). Low weight gain was defined as <–0.1 kg/wk for the first trimester and <0.3 kg/wk for the second and third trimester. IUGR was defined as a birth weight <2500 g in full-term infants. Low weight gain in the first trimester was not associated with an increased risk of IUGR. After controlling for confounding factors (maternal height, body mass index, parity, race, toxemia, diabetes), low weight gain in the second trimester was associated with a relative risk of IUGR of 1.8 (1.3–2.6) in the NCPP cohort and 2.6 (1.6–4.1) in the CHDS cohort. Similarly, low weight gain in the third trimester was associated with a relative risk of IUGR of 1.7 (1.3–2.3) in the NCPP cohort and 2.5 (1.7–3.8) in the CHDS cohort. After correcting for weight gain in other trimesters, this increased risk remained. Increased risk of IUGR was observed with low second and third trimester weight gain across the spectrum of maternal body mass index. The risk of low weight gain in the second or third trimester was significantly lower in teenagers and significantly greater in overweight women and women aged 35 y or older. Low weight gain in either the second or third trimester was associated with a significantly greater risk of intrauterine growth retardation in two distinct cohorts. We conclude that increased awareness of maternal weight gain in mid and late pregnancy is critical to identifying infants at risk for IUGR.

KEY WORDS: • intrauterine growth retardation • pregnancy • weight gain • trimester • humans

	INTRODUCTION

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Children born with intrauterine growth retardation (IUGR)³ have an increased risk of birth asphyxia (Koops et al. 1982 , Kramer et al. 1990 ) and hypoglycemia (Koops et al. 1982 , Kramer et al. 1990 ) and may retain substantial weight and height deficits (Babson et al. 1973 , Henrichson et al. 1986 , Koops et al. 1982 , Kramer et al. 1990 , Low et al. 1982 , Paz et al. 1993 , Strauss and Dietz 1998 , Westwood et al. 1983 ). The causes of intrauterine growth retardation are multifactorial. Previous studies demonstrate an increased risk of intrauterine growth retardation in women who smoke during pregnancy (Kramer 1987 ) as well as in women with short stature (Frederick and Adelstein 1978 , Kramer 1987 ) or low prepregnancy weight (Edwards et al. 1979 , Kramer 1987 ).

Studies of maternal weight gain during pregnancy also reveal an increased risk of IUGR in mothers with low pregnancy weight gain (Edwards et al. 1979 ,Kramer 1987 , Naeye 1981 , Smith 1947 , Stein et al. 1995 ). However, maternal weight gain and fetal growth vary greatly throughout pregnancy. Low weight gain in early, middle and late pregnancy are likely to affect the fetus differently. Siega-Riz et al. (1996 ) reported a twofold increase in the risk of prematurity with low maternal weight gain in the third trimester. Lantz et al. (1996 ) demonstrated increased weight in twins when higher maternal weight gain occurred both before and after 20 wk gestation. In adolescents, low weight gain by 12 wk gestation was not associated with a significantly increased risk of delivering a low-birth-weight infant, but low weight gain by 20 wk gestation was associated with a twofold increased risk (Scholl et al. 1990 ).

To explore the risk of IUGR in infants by weight gain in each trimester, we analyzed data from the National Collaborative Perinatal Project (NCPP) as well as the Child Health and Development Study (CHDS). Both studies were large, prospective studies designed to investigate the relationship between pregnancy and environmental-related variables in childhood growth and development. Because of the large number of patients enrolled and comprehensive prenatal and postnatal follow-up, these cohorts are ideal for calculating the effect of maternal weight gain in each trimester to subsequent fetal outcome.

	METHODS

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Sample: Two cohorts of patients were analyzed.

The NCPP cohort consisted of all mothers and full-term infants enrolled in the NCPP, an eight-center multicenter prospective study conducted from 1959 to 1976 that followed women enrolled during pregnancy and their infants. Women were predominantly enrolled from a mixed racial, urban population. The Child Health and Development Study, conducted from 1959 to 1973, followed women and their infants in the San Francisco Bay are in the Kaiser Health system, predominantly a white suburban population. To more accurately capture gestational age, prepregnancy weight and first trimester weight gain, we only included patients enrolled within 14 wk of their last menstrual period (LMP). Pregnancy complications were elicited at the time of registration and throughout pregnancy. Gestational age was measured by dating the last menstrual period at the time of registration. Prepregnancy weight was determined by maternal recall at the time of registration.

Measures.

First trimester weight gain was calculated as the average weekly weight gain between the prepregnancy weight and the end of the first trimester (13–16 wk from LMP). Second trimester weight gain was calculated as the average weekly weight gain between the end of the first trimester and the end of the second trimester (26–29 wk from LMP). Third trimester weight gain was calculated as the average weekly weight gain between the end of the second trimester and delivery. Total pregnancy weight gain was calculated as the difference between the prepregnancy weight and maternal weight at delivery.

We defined low weight gain in the second and third trimester as <0.3 kg/wk, in accordance with the suggestions of The Institute of Medicine (1990a) . No guidelines for first trimester weight gain were given by the Institute of Medicine; therefore, we defined low first trimester weight gain as < -0.1 kg/wk, which corresponds to ~1 SD below the mean weight of healthy, normal women (Abrams and Selvin 1995 ). Low pregnancy weight gain was defined as <6.8 kg (fifteenth percentile of NCPP and CHDS cohorts), which also corresponds to the recommendations of the Institute of Medicine (1990a) .

All infants were initially measured by trained study staff at the time of admission to the nursery. Birth weight was measured on calibrated scales, and birth length was measured with standard measuring tapes. Patients were classified as having IUGR if their birth weight at term was <2500 g. Infants were excluded in they had a gestational age <37 wk, multiple gestation, neural tube defect, chromosomal anomaly, or other severe congenital disease. Maternal body mass index (BMI) was calculated using prepregnancy weight and height (kg/m²). Maternal BMI was categorized as low (BMI <20.0 kg/m²), normal (20.0 kg/m² BMI < 25 kg/m²), or high (25.0 kg/m² BMI) according to the World Health Organization guidelines (1988) . Too few women with very high BMI (BMI > 30 kg/m²) were included in the study to calculate separate relative risks. In the NCPP study 10,696 women met the entry criteria, and data to calculate weight gain in every trimester were available in 5,403 (51%). In the CHDS study 9,229 women met the entry criteria; adequate data were available in 5,353 (58%). The remainder of patients in both the NCPP and CHDS studies were excluded because they enrolled after 14 wk gestation or delivered preterm infants.

Statistics.

Data were analyzed using the SPSS-X program (SPSS, Chicago, IL.). Differences in proportions were compared with ². Differences in continuous variables were determined by independent t-test. Relative risk was assessed using multivariate logistic regression, and 95% confidence intervals were calculated from these regressions. Combined data from both cohorts were used to calculate the relative risk of IUGR in women with differing BMI. Multivariate logistic regression was utilized to assess the effects of demographic variables on the risk of low weight gain in the second or third trimester.

	RESULTS

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Demographic variables.

Both the NCPP and CHDS cohorts differed significantly in their racial and socioeconomic backgrounds (Table 1 ). A significantly higher proportion of African-Americans (P < 0.001), single mothers (P < 0.001), teenage mothers (P < 0.001), and smokers (P < 0.001) were enrolled in the NCPP study, reflecting the urban environment from which these women were predominantly recruited. In contrast, women enrolled in the CHDS study were more likely to have graduated from high school (P < 0.001) and were older (P < 0.001). Infant length (P < 0.001) and weight (P < 0.001) were also significantly lower in the NCPP cohort.

Risk for IUGR.

Low maternal weight gain during the first trimester had no significant effect on the prevalence of IUGR in either cohort (Table 2 ). However, in both the NCPP and the CHDS studies low weight gain in the second trimester increased the risk of intrauterine growth retardation significantly [NCPP: 1.52 (1.03–1.97); CHDS: 1.87 (1.24–2.82)]. Low weight gain in the third trimester also significantly increased the risk of intrauterine growth retardation in both cohorts [NCPP: 1.52 (1.04–1.91); CHDS: 1.82 (1.24–2.65)]. The risk of intrauterine growth retardation was even higher after controlling for other factors known to affect fetal weight, such as maternal height, BMI, parity, smoking, toxemia and diabetes (Table 2) . The increased risk of intrauterine growth retardation with low weight gain in the second or third trimester remained significantly elevated, even after controlling for the rate of weight gain in the other two trimesters (Table 2) .

Because of limited numbers of patients with IUGR in the low and high BMI categories, relative risks were calculated using data from the combined cohorts. Low first trimester weight gain did not significantly increase the risk of intrauterine growth retardation in women with either low or elevated prepregnancy BMI (Table 3 ). Women with normal prepregnancy BMI demonstrated a mildly increased risk of IUGR with low first trimester weight gain, although this risk was no longer significant after controlling for confounding factors (Table 3) . In contrast, women with low weight gain in the second trimester demonstrated an approximately twofold increase in the rate of intrauterine growth retardation across the maternal weight spectrum (Table 3) . A similar trend was observed with low maternal third trimester weight gain, although this relationship was not statistically significant in overweight women after controlling for confounding factors (Table 3) .

Approximately three-quarters (73–82%) of patients with low weight gain in the second or third trimester had normal weight gain over the entire pregnancy (Table 4 ). Maternal marital status, race, and educational status were not consistently related to low weight gain in either the second or third trimester in both the NCPP and CHDS study (Table 5 ). Maternal age and body mass index in both cohorts significantly affected the risk of low weight gain. In particular, teenage mothers were approximately one half as likely to have low weight gain in either the second or third trimester as nonteenage mothers. In contrast, women aged 35 y or older were approximately twice as likely to have low weight gain in the second or third trimester.

In both cohorts, the risk of obtaining erroneous gestational ages (i.e., gestational age >43 wk) was two-to-three times more likely in women enrolled during the second or third trimester compared to women enrolled during the first trimester. Therefore, to obtain the most accurate assessment of gestational age, women were only included who enrolled in the first trimester of pregnancy. Women with complete and incomplete first trimester data demonstrated only minor differences in demographic characteristics and pregnancy weight gain (Table 6 ). In contrast, women enrolled in the second or third trimester were less educated, younger, and more likely to be African-American compared to women enrolled in the first trimester. Because accurate assessment of third trimester weight gain was also possible in women enrolled in the second trimester of pregnancy, risk of IUGR was calculated in these women (Table 7 ). Similarly, increased risks of intrauterine growth retardation with low third trimester weight gain were observed in both cohorts independent of when the women enrolled in the study. This suggests that enrollment bias had little effect on the studies main outcomes.

	DISCUSSION

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Other studies also indicated that low trimester weight gain, particularly in the second trimester, is important for fetal growth. Abrams and Selvin (1995) demonstrated that low maternal weight gain in the second trimester (<5.7 kg) was associated with decreased birth weights ranging from 48 to 248 g, depending on the pattern of weight gain in the other trimesters. In contrast, isolated low first and third trimester weight gain was not associated with significantly decreased birth weight in that study by Abrams and Selvin (1995) . Similarly, Hickey et al. (1996) also demonstrated that low prenatal weight gain, particularly involving the second trimester, significantly decreased birth weight. Finally, Lawton et al. (1988) showed significantly lower maternal weight gain between 28 and 32 wk gestation resulted in infants born small for gestation compared to normal weight infants.

These results are particularly important because the majority of patients with low weight gain in an individual trimester have normal total pregnancy weight gain. In addition, the increased risk of IUGR remained even after controlling for the amount of weight gain in the other trimesters. Our results support the work by Scholl et al. (1990) who also demonstrated a twofold increase in low birth weight infants associated with low maternal weight gain in mid or late pregnancy. Hediger et al. (1989) also demonstrated that low weight gain by 24 wk gestation increased the risk of low birth weight infants, even if total weight gain was normal. . However, both previous studies were limited to adolescent mothers, whereas our study demonstrates similar results in a more comprehensive cohort.

Our data supports the Institute of Medicine (1990a) recommendation that overweight women should gain at least 0.3 kg/wk over both the second and third trimesters. We demonstrated that the elevated risk of intrauterine growth retardation remained in overweight women with low second trimester weight gain and low third trimester weight gain, even after controlling for confounding variables. In addition, particular attention must be given to women aged 35 y or older because these women are almost twice as likely to have low weight gain in either the second or third trimester. Similarly, overweight women and women who smoke also demonstrated lower rates of second and third trimester weight gain. Our results confirm data of Abrams et al. (1995) who also demonstrated decreased rates of second and third trimester weight gain associated with smoking, older maternal age, as well as increased body mass index. Similarly, other investigators (Ancri et al. 1997 , Muscati et al. 1988 ) also demonstrated lower total pregnancy weight gain in older women compared to younger women.

Our findings also support the hypothesis that the timing of pregnancy-related variables greatly influences fetal growth. Maternal weight gain and fetal growth vary greatly throughout pregnancy (Bernstein et al. 1997 , Hytten and Leitch 1971 , Widdowson 1994 ). During the first trimester, the fetus mainly undergoes organogenesis, while growth is minimal. First trimester insults are therefore likely to be teratogenic, with little effect on neonatal growth. We found no consistently increased risk of intrauterine growth retardation even with mild maternal weight loss in the first trimester, consistent with these assumptions. In contrast, a study by Smith et al. (1998) demonstrates a twofold increased risk of full-term IUGR with poor first trimester fetal growth. However, the study by Smith et al. may be limited by sample bias. Only 3,397 of 31,269 infants with fetal ultrasounds met the strict entry criteria. In addition, only 3% of full-term infants who had poor first trimester growth were born with a birth weight <2500 g. Finally, because fetal size, and hence energy demands, are relatively small in the first trimester, first trimester fetal growth is unlikely to be dependent on adequate maternal weight gain.

In the second trimester, fetal growth is the most rapid, and therefore, most likely to be influenced by maternal nutrition. Fetal weight increases by ~12-fold between 14 and 28 wk (Moore 1982 ). Low maternal weight gain during the second trimester doubled the risk of intrauterine growth retardation even though the contribution of fetal weight to maternal weight gain during this trimester is minimal. In the third trimester, the fetus quadruples its fat mass (Moore 1982 ). Adequate fetal nutrition during this period also remains critical. However, fetal and placental weight gain in the third trimester may account for up to one half of maternal weight gain. Therefore, low maternal weight gain in the third trimester may be an effect of intrauterine growth retardation and not a cause.

Unfortunately, efforts to manipulate fetal nutrition through maternal dietary changes have been contradictory. Data from developing countries suggest that nutritional supplementation in pregnancy leads to significantly increased total pregnancy weight gain (Mardones-Santander et al. 1981 , Tontisirin et al. 1986 ) and modest increases in birth weight (30–250 g) in women at nutritional risk (Lechtig et al. 1975 , Mardones-Santander et al. 1981 ,Tontisirin et al. 1986 ). However, little equivalent data exists to support the use of routine nutritional supplementation in the USA or Europe. Rush et al. (1980) performed a double blinded study of nutritional supplementation during pregnancy in poor, black, urban women who were at high risk for delivering infants with intrauterine growth retardation. Women who received a high protein supplement had increased number of preterm deliveries, neonatal death and growth retardation up to 37 wk gestation, despite increased maternal weight gain. However, in women receiving supplemental food aid through the WIC program, there was a significant increase in head circumference at birth, although there was no noticeable effect on birth weight or intrauterine growth retardation (Rush et al. 1988 ). Unfortunately, maternal weight gain was not evaluated. Studies of nutritional supplementation in Canada also revealed small, but significant influences on average birth weight, but no significant differences in the incidence of low birth weight infants or the amount of maternal weight gain during pregnancy (Rush 1981 ).

We chose to define intrauterine growth retardation as a term birth weight below 2500 g. Our definition is consistent with previous studies (reviewed by Kramer 1987 ), and is largely based on the increased morbidity and mortality in infants born below this birth weight (McCormick 1985 ). Long-term health consequences were also described in full term-infants born below 2500 g (Barker 1997 ,Curhan et al. 1996 ). Other authors have variably defined IUGR as a birth weight less than the tenth percentile for gestational age, less than the fifth percentile for gestational age, or <2 SD (third percentile) for gestational age. However, gestational age based criteria are limited by the reference standard utilized (Miller 1981 ). Finally, we have limited the accidental misclassification of preterm infants by only including patients enrolled within the first trimester. In women enrolled in prenatal care before 16–18 wk gestation, Kramer et al. (1988) have demonstrated gestational dating by LMP is extremely accurate in term infants.

Unfortunately, this study utilizes relatively old data. During the 1960s to 1970s recommendations for the amount of weight a pregnant women should gain were substantially lower than current recommendations (Institute of Medicine 1990b ). In fact, the 12^th edition of Williams Obstetrics (1961) recommended limiting pregnancy weight gain to 11.4 kg (Eastman and Hellman 1961 ). As a result, mean weight gain in the two cohorts averaged 2–4 kg lower than currently observed averages. Nevertheless, in the 1990s, ~40% of black women and 25% of white women continue to gain <9 kg throughout their pregnancy (Caulfield et al. 1996 ), which is less than the average weight gain in both cohorts in the current study. In addition, the definition of low trimester gain utilized in this study (0.3 kg/wk for second and third trimester) is consistent with rates of weight gain occurring in ~15–25% of contemporary pregnancies (Abrams and Selvin 1995 , Carmichael et al. 1997 ).

In conclusion, increased awareness of maternal weight gain in mid and late pregnancy is critical to identifying infants at risk for IUGR. Fetal growth may be impaired by relatively short periods of poor maternal weight gain, even if subsequent weight gain is adequate. However, nutritional supplementation of all mothers with poor gestational weight gain is not currently indicated because previous experience has been contradictory. According to The Institute of Medicine (1990a) : "When abnormal weight gain appears to be real, rather than a result of an error in measurement or recording, try to determine the cause and then develop and implement corrective actions jointly with the women If it appears that a lower than recommended weight gain is the result of an inadequate food supply or inappropriate self-restriction, corrective measures should be taken promptly."

	FOOTNOTES

 
¹ This study was supported by grants P30 DK 46200 from the National Institutes of Health and the Massachusetts Department of Public Health.

³ Abbreviations used: BMI, body mass index; CHDS, Child Health and Development Study; IUGR, Intrauterine growth retardation; LMP, last menstrual period; NCPP, National Collaborative Perinatal Project.

Manuscript received September 30, 1998. Initial review completed December 30, 1998. Revision accepted January 29, 1999.

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