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ORIGINAL RESEARCH |
From the 1Department of Obstetrics, Gynecology, and Reproductive Sciences, University of California, San Francisco, California; 2Division of Biostatistics, School of Public Health, University of California, Berkeley, California; 3Division of Epidemiology, School of Public Health, University of California, Berkeley, California.
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ABSTRACT |
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 ABSTRACT PARTICIPANTS AND METHODSRESULTSDISCUSSIONREFERENCES |
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METHODS: This was a retrospective cohort study of singleton births to women of normal or low prepregnancy body mass index. Gestational weight gain was measured as total weight gain divided by weeks of gestation at delivery, and weight gain was categorized as low (less than 0.27 kg/wk,), normal (0.27–0.52 kg/wk), or high (more than 0.52 kg/wk). Univariable and multivariable analyses were performed on the relationship between weight gain categories and spontaneous preterm birth, stratified by maternal race or ethnicity and history of previous preterm birth.
RESULTS: Overall, low weight gain was associated with spontaneous preterm birth (adjusted odds ratio [AOR] 2.5, 95% confidence interval [CI] 2.0–3.1). Although low gain was consistently associated with increased spontaneous preterm birth, some differences were found in subgroup analysis. Among African Americans with a previous preterm birth, both low and high weight gain were associated with increased odds of spontaneous preterm birth (AOR for low weight gain 4.3, 95% CI 1.2–15.5; AOR for high weight gain 6.1, 95% CI 1.8–20.2). For all other groups, high weight gain was not associated with spontaneous preterm birth. Among Asians with a previous preterm birth, low weight gain was not statistically significantly associated with spontaneous preterm birth (AOR 1.9, 95% CI 0.5–7.7). Among Asians there was also a non–statistically significant inverse relationship between high weight gain and spontaneous preterm birth (AOR 0.5, 95% CI 0.3–1.1).
CONCLUSION: These results confirm an association between low maternal weight gain and spontaneous preterm birth. The effect modification of maternal race or ethnicity and history of previous preterm birth on this association deserves further study.
LEVEL OF EVIDENCE: II-2
Although African-American women are more likely to be obese and tend to gain about the same amount of weight (on average) as white women, they paradoxically have higher rates of low birth weight and preterm birth compared with white women.6 Hickey et al7 studied the relationship between gestational weight gain and spontaneous preterm birth among nonobese, low-income, multiparous African-American and white women. They found that third-trimester rates of gain below the Institute of Medicine (IOM) guidelines were associated with increased preterm delivery among both groups. The adjusted odds ratio for white women was 4.05 (95% confidence interval [CI] 1.41–11.66), and for African-American women it was 1.88 (95% CI 1.16–3.41). It is unclear whether or not the relationship between weight gain and spontaneous preterm birth is the same between women of different racial or ethnic groups, but this evidence suggested that adequate weight gain may be less protective against preterm birth for African-American women than it is for white women. Similarly, among term deliveries, Schieve et al8 found that gaining in the upper end of the IOM guidelines was protective against low birth weight for all women but not for the subgroup of African-American women. Finally, very little is known about weight gain and spontaneous preterm birth among Asian-American women, a group that made up over 11% of births in California in 2004.9
Along with maternal race or ethnicity, previous preterm birth is consistently found to be a strong predictor of spontaneous preterm birth.10,11 Some investigators have found that African-American women have higher rates of recurrent preterm birth than white women.12 Women with a previous history of preterm birth are an obvious group to target for interventions to prevent preterm birth, such as improvement of gestational weight gain. Therefore, we sought to study the role of race or ethnicity and previous preterm birth on the relationship between gestational weight gain and spontaneous preterm birth.
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PARTICIPANTS AND METHODS |
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ABSTRACTPARTICIPANTS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Because women delivering at later gestations have more time to gain weight, we used an estimated rate of gain instead of total weight gain. Rate of gain was estimated by dividing the total weight gain by the weeks of gestation at delivery, minus 2 weeks that were subtracted from the denominator because calculation of gestational age was based on the last menstrual period. Estimated rate of gain was then examined in the following ways: as a continuous variable, as a three-way categorical variable according to gain below, within, or above the IOM guidelines, and as a three-way categorical variable, low (less than 0.27 kg/wk), normal (between 0.27 and 0.52 kg/wk), and high (greater than 0.52 kg/wk). The 0.27 kg/wk cutoff represents a total weight gain at 38 weeks of gestation of approximately 10 kg (22 lb) and has been associated with spontaneous preterm birth risk in a previous cohort.16 The high cutoff of 0.52 kg/wk represents a total weight gain at 38 weeks of gestation of about 20 kg (44 lb).
Spontaneous preterm birth was defined as birth at less than 37 weeks of gestation without a medical indication, with or without preterm premature rupture of membranes. Gestational age at delivery was determined by the delivering physician using a combination of last menstrual period, ultrasound examinations when available, and Dubowitz score.
Results were analyzed with Stata 8 (Stata Corporation, College Station, TX). Statistical methods included the 
2 test to compare proportions and multivariable logistic regression to control for potential confounding. We stratified the cohort based on race or ethnicity, parity, and prior preterm birth status (multiparous with prior preterm birth, multiparous with no prior preterm birth, and nulliparous). Previous preterm birth history (as opposed to spontaneous preterm birth in the index pregnancy) was based on patient report as noted in the prenatal chart and did not distinguish between prior spontaneous preterm birth and prior medically indicated preterm birth. Initial covariates were chosen based on prior studies of preterm birth in the literature. Variables were included in the regression models if they were significantly associated with spontaneous preterm birth in 2 analysis. A backward variable selection technique was used to eliminate nonsignificant variables, which included substance abuse, year of delivery, and insurance status. In the final logistic regression models, we controlled for the following variables: parity, history of previous preterm birth (only in models that did not stratify by these variables), maternal race or ethnicity, prepregnancy body mass index, year of delivery, maternal age, and smoking. We also included a term that represented the number of days between last weighing and the date of birth, because preterm patients have less frequent prenatal visits than patients at term. For the logistic regression, we ran separate models stratifying by maternal race or ethnicity, parity, and previous preterm birth status. The standard errors were adjusted to account for the lack of independence between births to the same mother within the study cohort. In addition, we applied these methods to examine the relationship between weight gain and spontaneous preterm birth at less than 34 weeks of gestation. We performed tests of interaction between race or ethnicity and weight gain (stratified by parity and previous preterm birth history) using weight gain as a continuous as well as a categorical variable. For all analyses, P<.05 was considered statistically significant, except for tests of interaction, which were considered statistically significant at P<.2.
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RESULTS |
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ABSTRACTPARTICIPANTS AND METHODSRESULTSDISCUSSIONREFERENCES |
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The percentage of spontaneous preterm birth in the cohort was 4.0%, and African-American women had the highest percentage of spontaneous preterm birth at 6.4% (Table 1). Women gaining less than 0.27 kg/wk made up 10.7% of the total, and African-Americans were the most likely to gain below this threshold; 16.9% of them gained below 0.27 kg/wk compared with only 7.4% of white women. African-American women were also the most likely to report a history of a previous preterm birth (8.3% versus 4.1% in white women). The percentage of women gaining above 0.52 kg/wk varied widely by race or ethnicity, with only 13.8% of Asians compared with 24.6% of white women and 23.0% of African Americans gaining this amount.
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In the entire cohort, as well as in every racial or ethnic subgroup, low weight gain was associated with an increased risk of spontaneous preterm birth. Table 2 shows the percentage in each subgroup with a spontaneous preterm birth by gestational weight gain category. Among multiparous women with a previous preterm birth, 38.1% of white women with low gain had recurrent spontaneous preterm birth compared with 15.0% of those with normal gain and 12.5% of those with high gain (P=.03). Among African Americans with a previous preterm birth, spontaneous preterm birth rates were elevated in both low and high gainers compared with normal gainers: 33.3% of those with low gain had recurrent spontaneous preterm birth compared with 11.8% of those with normal gain and 38.5% of those with high gain (P=.006). Among multiparous women without a previous preterm birth as well as nulliparous women, the white subgroup had the weakest association between low gain and spontaneous preterm birth, and high gain was not associated with spontaneous preterm birth.
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When we controlled for potential confounding bias using multivariable logistic regression analysis, the findings from the unadjusted analyses persisted (Table 3). Weight gain of less than 0.27 kg/wk was associated with increased odds of spontaneous preterm birth in all racial or ethnic subgroups. Among African Americans, both low and high gain were associated with spontaneous preterm birth, although for high gain the statistical significance was borderline (adjusted odds ratio [AOR] 1.7, 95% CI 1.0–2.9). Among Asians, there was a non–statistically significant inverse association between high gain and spontaneous preterm birth (AOR 0.5, 95% CI 0.3–1.1). Among multiparous women with a previous preterm birth, low weight gain was associated with spontaneous preterm birth (AOR 2.2, 95% CI 1.2–3.9). Among racial or ethnic subgroups with a previous preterm birth, African-American women were the only subgroup with elevated spontaneous preterm birth associated with both low gain (AOR 4.3, 95% CI 1.2–15.5) and high gain (AOR 6.1, 95% CI 1.8–20.2). For Asian women with a previous preterm birth, low gain showed a trend toward increased risk of spontaneous preterm birth but did not reach statistical significance (AOR 1.9, 95% CI 0.5–7.7). There were no Latina women in the cohort with all three of the following: prior preterm birth, low weight gain, and recurrent spontaneous preterm birth, so we could not estimate odds ratios for this subgroup. Among multiparous women with no history of previous preterm birth, weight gain of less than 0.27 kg/wk was associated with increased odds of spontaneous preterm birth (AOR 2.8, 95% CI 2.0–4.0), and this association was seen for all racial or ethnic subgroups. Among nulliparous women, weight gain of less than 0.27 kg/wk was associated with spontaneous preterm birth (AOR 2.5, 95% CI 1.8–3.3), and among racial or ethnic subgroups, white women had the lowest AOR associated with low gain, but odds ratios were similar across groups.
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We ran the same models looking at the association between weight gain of less than 0.27 kg/wk and spontaneous preterm birth under 34 weeks (instead of under 37 weeks). The cell sizes were too small (less than 10) to stratify by prior preterm birth as well as race or ethnicity, but we had the following findings when stratified by race or ethnicity alone: weight gain of less than 0.27 kg/wk was associated with spontaneous preterm birth at less than 34 weeks for all racial or ethnic categories (AOR 3.0, 95% CI 2.0–4.8), for white women (AOR 3.3, 95 % CI 1.5–7.4), for African-American women (AOR 3.9, 95% CI 1.6–9.2), for Latina women (AOR 4.0, 95% CI 1.1–15.9), and for Asian women, although the result lacked statistical significance (AOR 2.5, 95% CI 0.9–7.0). When we examined weight gain in kilograms per week as a continuous variable or as a three-way categorical variable according to gain below, within, or above IOM guidelines, we saw relationships similar to those reported above for the low, normal, and high gain cutoffs (data not shown).
When the three-way categorical variable was used for weight gain in kilograms per week, interactions were not statistically significant between weight gain of less than 0.27 kg/wk and maternal race or ethnicity for the outcome of spontaneous preterm birth at less than 37 weeks. There was an interaction between weight gain of more than 0.52 kg/wk and race ethnicity among women with a previous preterm birth (P=.03). When weight gain in kilograms per week was examined as a continuous variable, there was a statistically significant interaction between gestational weight gain and maternal race or ethnicity among women with a previous preterm birth (P=.04) and multiparous women with no prior preterm birth (P=.12). For nulliparous women there was no statistically significant interaction between weight gain and race or ethnicity (P=.37). As noted in PARTICIPANTS AND METHODS, interactions were considered statistically significant at P<.2.
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DISCUSSION |
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ABSTRACTPARTICIPANTS AND METHODSRESULTSDISCUSSIONREFERENCES |
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High weight gain was significantly associated with spontaneous preterm birth in one subgroup: African-American women with a previous preterm birth. This association was seen in both the unadjusted and the adjusted analyses. In this relatively high-risk population, both low and high gains independently predict spontaneous preterm birth risk. Recently, an association was reported between very high gain (more than 0.79 kg/wk) and increased risk of spontaneous preterm birth in a multiethnic population, but results were not stratified by prior preterm birth status and race or ethnicity.5 We did not have adequate power to look at the relatively small percentage of women who gain more than 0.79 kg/wk, but further research should explore the relationship between excessive weight gain and spontaneous preterm birth among subgroups of women.
We also found the suggestion of an inverse relationship between high gain and spontaneous preterm birth among Asian women, although we lacked power in this subgroup and the association did not reach statistical significance. Asian women have lower prepregnancy BMI on average compared with other groups, and low BMI has been associated with increased risk of spontaneous preterm birth in some cohorts.15,17 However, we saw the same inverse association with or without controlling for BMI in the multivariable analyses. Little is known about weight gain and perinatal outcomes among Asian-American women, and this group is very diverse within our cohort, consisting of ethnic Chinese, Japanese, Filipina, and other groups combined for statistical power. Future research should explore the role of weight gain and BMI in spontaneous preterm birth among Asian Americans and whether the current weight gain recommendations are appropriate for this population.
We found that the relationship between gestational weight gain and spontaneous preterm birth differed for recurrent versus primary spontaneous preterm birth and was further modified by maternal race or ethnicity. Mercer et al18 found that prior preterm births between 23 and 27 weeks of gestation were more strongly associated with subsequent preterm birth than were prior preterm births at later gestations. African-American women in our cohort who delivered preterm did so, on average, one week earlier than white women who delivered preterm. Because early (less than 28 weeks) preterm births have been associated more strongly with some etiologic mechanisms, such as infection, it is possible that gestational weight gain may play more of a role in later preterm births than in earlier preterm births.19 Future research may help explore the relationships between maternal race or ethnicity, gestational weight gain, and possible etiologic mechanisms for preterm birth such as infectious, inflammatory, and cervical factors.
Our study serves to further support the previously identified association between gestational weight gain and risk of spontaneous preterm birth. There is some biological plausibility for the observed relationship between low weight gain and preterm birth because multiple studies have found an association between low prepregnancy BMI and risk of spontaneous preterm birth.15,17,20,21 One recent study found an increased rate of postterm or prolonged pregnancy among women with high prepregnancy BMIs.22 The possible mechanisms for this relationship include hormonal effects of increased body fat or deficiencies of macro- or micro-nutrients, but these hypotheses require further investigation.
Although there may be biological plausibility for a causal relationship between gestational weight gain and spontaneous preterm birth, poor weight gain may simply be a marker or sign of abnormal pregnancy physiology. Preterm birth has been associated with both uteroplacental insufficiency and poor increase in plasma volume (one component of gestational weight gain).23,24 Poor gestational weight gain could also be a marker for maternal stress, depression, or other unmeasured factors that may be involved in a causal link to preterm delivery.
We also found evidence of a weight gain threshold for spontaneous preterm birth risk at 0.27 kg/wk (about 10.3 kg over 38 weeks of gestation). This cutoff was used in a prior study in a different but comparable cohort of women in California.16 For most subgroups, once weight gain reached a threshold of 0.27 kg/wk, additional gain was not associated with decreasing risk of spontaneous preterm birth. Indeed, among the most high-risk subgroup, African-American women with a previous preterm birth, gain of more than 0.52 kg/wk was associated with increased odds of spontaneous preterm birth. Although our findings support efforts to prevent inadequate gestational weight gain, there does not appear to be any benefit among most subgroups, and there may be harm from excessive gain with regard to the outcome of spontaneous preterm birth. The possible exception may be Asian-American women, among whom, as noted above, there was a trend toward lower risk of spontaneous preterm birth with gain of more than 0.52 kg/wk.
Despite our efforts to examine the relationship between gestational weight gain and spontaneous preterm birth, the study was not without limitations. We did not have adequate power to stratify by BMI after also stratifying by race or ethnicity, parity, and previous preterm birth status. We excluded overweight and obese women from this analysis because this group has a lower rate of spontaneous preterm birth, and studies have suggested there may be a weaker relationship between gestational gain and spontaneous preterm birth among obese women. It remains unclear to what degree low weight gain puts overweight and obese women at risk for adverse perinatal outcomes.
To have adequate statistical power to doubly stratify by race or ethnicity and previous preterm birth history, we used our entire birth cohort beginning in 1976 when many aspects of obstetric care differed from today’s standard. To address this issue we controlled for year of birth in the multivariable analyses, and we also ran analyses using only births since 1990 and saw similar results to those from the longer time period.
Another limitation of our study is that we used total gestational weight gain because we did not have serial weight gain measurements in our database. Because women who deliver preterm have less time to gain weight, length of gestation is an obvious source of bias. To control for this we used an estimated rate of gain as our primary predictor variable; that is, we divided total weight gain by length of gestation, thereby estimating a weekly "rate" of gain. The rate of gain varies throughout pregnancy, with slowest gains in the first trimester (0.17 kg/wk), fastest gains in the second trimester (0.56 kg/wk), and then slightly slower rates of gain in the third trimester (0.52 kg/wk).28 Although most studies have controlled for or accounted for the confounding role of gestational age when studying the association between weight gain and spontaneous preterm birth, there remains the bias related to the fact that rate of gain is lower in the first trimester, and women delivering preterm have a total weight gain that is more influenced by the first trimester than women delivering at term. However, there is recent evidence from a large population-based study that weight gain in the second and third trimesters alone was predictive of spontaneous preterm birth.5 Also, a previous study in a smaller cohort of births at the University of California, San Francisco Medical Center examined the relationship between pattern of gain and spontaneous preterm birth, and found that weight gain that either slowed or speeded up greatly toward the end of pregnancy was associated with an increased risk of spontaneous preterm birth.29 It is, therefore, unlikely that the observed relationship between rate of gain and spontaneous preterm birth is merely an artifact of the slower gain in the first trimester.
Low gestational weight gain was relatively uncommon in this cohort, and excessive gain is becoming increasingly common in the United States.6 The robust association between low gain and spontaneous preterm birth suggests that, in this era of appropriate concern over an obesity epidemic, we must strike a careful balance between excessive and inadequate gestational weight gain. Among African-American women with a previous preterm birth, both extremes of weight gain were associated with increased risk, so increased vigilance about appropriate weight gain in this subgroup may be warranted. Our findings suggest that future research exploring risk factors or mechanisms for spontaneous preterm birth should consider both maternal race or ethnicity and previous preterm birth status, because these variables modify the relationship between gestational weight gain and spontaneous preterm birth.
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Footnotes |
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Corresponding author: Naomi E. Stotland, MD, Assistant Adjunct Professor, University of California, San Francisco, Department of Obstetrics, Gynecology, and Reproductive Sciences, San Francisco General Hospital, Ward 6D-1, 1001 Potrero Avenue, San Francisco, CA 94110; e-mail: stotlandn{at}obgyn.ucsf.edu.
doi:10.1097/01.AOG.0000247175.63481.5f
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