Background Obesity before pregnancy is associated with an increasedrisk of several adverse outcomes of pregnancy. The risk profilesamong lean, normal, or mildly overweight women are not, however,well established.
Methods We studied the associations between prepregnancy body-massindex (defined as the weight in kilograms divided by the squareof the height in meters) and the frequency of late fetal death,early neonatal death, preterm delivery, and delivery of a small-for-gestational-ageinfant in a population-based cohort of 167,750 women in Swedenin 1992 and 1993. The women were categorized as follows, accordingto body-mass index: lean, less than 20.0; normal, 20.0 through24.9; overweight, 25.0 through 29.9; and obese, 30.0 or more.The estimates were adjusted for maternal age, parity, smoking,education, whether the mother was living with the father, andmaternal height.
Results Among nulliparous women, the odds ratios for late fetaldeath were increased among women with higher body-mass indexesas compared with lean women, as follows: normal women, 2.2 (95percent confidence interval, 1.2 to 4.1); overweight women,3.2 (95 percent confidence interval, 1.6 to 6.2); and obesewomen, 4.3 (95 percent confidence interval, 2.0 to 9.3). Amongparous women, only obese women had a significant increase inthe risk of late fetal death (odds ratio, 2.0; 95 percent confidenceinterval, 1.2 to 3.3). Among nulliparous women, the risk ofvery preterm delivery (at <32 weeks' gestation) was significantlyincreased among obese as compared with lean women (odds ratio,1.6; 95 percent confidence interval, 1.1 to 2.3), whereas amongparous women, the risk was highest among those who were lean.The risk of delivering a small-for-gestational-age infant decreasedmore with increasing body-mass index among parous than amongnulliparous women.
Conclusions Higher maternal weight before pregnancy increasesthe risk of late fetal death, although it protects against thedelivery of a small-for-gestational-age infant.
Obesity before pregnancy is associated with an increased riskof fetal macrosomia and perinatal mortality.1,2,3 The mother'sbeing leaner than average (underweight), on the other hand,is associated with an increased risk of delivering an infantwho is small for gestational age and perhaps also the risk ofpreterm delivery.3,4,5,6 Pregnancies among underweight or overweightwomen are therefore often regarded as high-risk pregnancies,and thin women are frequently advised to gain weight beforebecoming pregnant.7,8 Nonetheless, the optimal weight or body-massindex for women who wish to become pregnant is not known.7,8,9
The Swedish Medical Birth Register covers virtually all birthsin Sweden and includes prospectively collected data on maternalcharacteristics and complications during pregnancy, delivery,and the neonatal period. Using this data set, and adjustingfor potentially confounding factors, we studied the effect ofthe prepregnancy body-mass index (defined as the weight in kilogramsdivided by the square of the height in meters) on the risk oflate fetal death, early neonatal death, preterm delivery, anddelivery of an infant who was small for gestational age.
Methods
For the years 1992 and 1993, the birth register recorded thebirths of 204,555 singleton infants to women who were themselvesborn in Sweden, Denmark, Norway, Finland, or Iceland. The finalstudy population included 167,750 women for whom informationon prepregnancy body-mass index was available.
In Sweden, maternal characteristics are recorded in a standardizedmanner at the first visit for antenatal care, which occurs beforethe 15th week of gestation in more than 95 percent of the pregnancies.Maternal height and prepregnancy weight are recorded by recallin centimeters and kilograms, respectively, and used to calculatethe prepregnancy body-mass index. We used the body-mass indexto characterize women as lean (body-mass index, less than 20.0),normal (20.0 through 24.9), overweight (25.0 through 29.9),or obese (30.0 or more). Maternal smoking was categorized asno daily smoking, 1 to 9 cigarettes per day, or 10 or more cigarettesper day. Also recorded was whether the woman was living withthe father. Information on the mother's years of formal educationwas obtained through linkage to another population-based register.Total maternal weight gain during pregnancy was recorded onadmission to the delivery ward. Weight gain per completed weekof gestation was calculated and used in this analysis.
Information about maternal age, parity, and complications duringpregnancy or delivery was obtained from records routinely filledout when the woman was discharged from the hospital. Maternalage was defined as age in completed years at the time of delivery,and parity as the number of previous births, including stillbirthsat 28 weeks of gestation or later. Complications during pregnancyand delivery were classified by a physician at the time of hospitaldischarge, according to the Swedish version of the InternationalClassification of Diseases,Ninth Revision (ICD-9).10 For thisanalysis, we used two groups of diagnoses associated with prepregnancybody-mass index and the risk of adverse pregnancy outcomes2,3:hypertensive diseases, defined as essential hypertension, preeclampsia,and eclampsia (ICD-9 codes 642A, 642E, 642F, and 642G), anddiabetes mellitus, defined as insulin-dependent or non-insulin-dependentdiabetes mellitus present before pregnancy or gestational diabetes(ICD-9 codes 250, 648A, and 648W).
Information about late fetal death, the duration of gestation,birth weight, and the infant's sex was obtained from the standardizedpediatric record, routinely filled out immediately after delivery.Information about early neonatal deaths was obtained throughlinkage of individual records to the population-based Causeof Death Register. Late fetal death was defined as stillbirthoccurring at 28 or more completed weeks of gestation, and earlyneonatal death as death occurring during the first week afterbirth. Preterm delivery (i.e., delivery at less than 37 completedweeks of gestation) was classified as very preterm (<32 weeks)or moderately preterm (33 to 36 weeks). Small-for-gestational-ageinfants were defined as those with birth weights more than 2SD below the mean birth weight for gestational age, accordingto a Swedish reference curve.11 Estimated gestational age wasbased on ultrasound examinations performed routinely at no laterthan 18 completed weeks of gestation.
Statistical Analysis
We used multiple logistic-regression analysis to evaluate theassociation between prepregnancy body-mass index and late fetaldeath, early neonatal death, preterm delivery, and deliveryof a small-for-gestational-age infant. The estimates were adjustedfor maternal age, parity, education, smoking, height, whetherthe mother was living with the father, and weight gain duringpregnancy. We excluded from our analyses women who had missinginformation on covariates.
Because information on weight gain during pregnancy was missingfor 45 percent of the women, we performed a detailed analysisof the effects of adjustment for this variable. Three differentmodels were estimated for each dependent variable. The firstwas based on the complete data set, without adjustment for weightgain; the second, on the women for whom data on weight gainwere available, but without adjustment for weight gain; andthe third, on the women with data on weight gain and with adjustmentfor weight gain. Thus, it was possible to determine whetherthe inclusion of weight gain in the model altered the effectof body-mass index and whether this alteration was due to changesin the subgroup analyzed or to genuine confounding.
Interactions between body-mass index and parity were assessedby means of a likelihood-ratio test comparing a base-line multivariatemodel without interaction terms to a model that included termsfor the interaction between parity and body-mass index. To facilitatethe interpretations of the effects of body-mass index, estimatesare presented separately for parous and nulliparous women. Oddsratios were calculated to approximate relative risk and arepresented with 95 percent confidence intervals.
Results
The risk of late fetal death increased consistently with increasingprepregnancy body-mass index in the univariate analyses (Table 1).As compared with lean women, overweight and obese womenhad significantly increased odds ratios for late fetal death.The rates of late fetal death were 1.7 per 1000 among womenfor whom information about weight gain during pregnancy wasavailable and 4.1 per 1000 among those for whom it was missing(P<0.001); the corresponding rates of early neonatal deathwere 1.1 and 2.7 per 1000, respectively (P<0.001). When dataon weight gain during pregnancy were available, this factordid not influence the risk of late fetal death. Low weight gain(<0.25 kg per week of gestation) was associated with a marginallysignificant increase in the risk of early neonatal death (Table 1).
Table 1. Characteristics of Women Delivering Singleton Infants in 1992 and 1993 in Sweden and Univariate Associations with the Risk of Late Fetal Death and Early Neonatal Death.
In preliminary multivariate analyses, we found no evidence ofconfounding of the effect of body-mass index by weight gainduring pregnancy. This was true with respect to the adverseoutcomes of late fetal death, early neonatal death, and pretermdelivery, for which weight gain had little explanatory power,but also with respect to the delivery of a small-for-gestational-ageinfant, for which weight gain was an important explanatory variable.Detailed results for the delivery of a small-for-gestational-ageinfant are shown in Table 2. After adjustment for weight gainduring pregnancy, the effects of body-mass index before pregnancywere unaltered despite the strong association between weightgain and the risk of delivering a small-for-gestational-ageinfant. This finding may be explained by the lack of correlationbetween prepregnancy body-mass index and weight gain duringpregnancy. On the basis of these results, and in order to increasethe precision of our analyses, we excluded weight gain duringpregnancy from subsequent models.
Table 2. Adjusted Odds Ratios for the Delivery of a Small-for-Gestational-Age Infant Associated with Prepregnancy Body-Mass Index and Weight Gain during Pregnancy among Women Delivering Live Singleton Infants in Sweden in 1992 and 1993.
The risk of late fetal death consistently increased with greaterprepregnancy body-mass index (Table 3). As compared with leanwomen, women with a normal body-mass index and overweight womenwere at decreased risk of preterm delivery.
Table 3. Adjusted Odds Ratios for Adverse Outcomes Associated with Prepregnancy Body-Mass Index among Women Delivering Singleton Infants in Sweden in 1992 and 1993.
Obese women were more likely than lean women to have 11 yearsof formal education or less (75 percent vs. 56 percent), tobe daily smokers (28 percent vs. 24 percent), and to have diabetesmellitus present before pregnancy or gestational diabetes mellitus(1.1 percent vs. 0.3 percent). The rate of preeclampsia increasedwith increasing body-mass index, as follows: lean women, 1.8percent; normal women, 2.5 percent; overweight women, 4.2 percent;and obese women, 7.0 percent. Hypertensive disease was morecommon among nulliparous women (4.6 percent) than among parouswomen (1.9 percent) and was a major risk factor for adversepregnancy outcomes (data not shown). On the basis of these patterns,we explored possible interactions between body-mass index andparity with respect to adverse pregnancy outcome.
Among nulliparous women, the risk of late fetal death was roughlydoubled among women with a normal body-mass index, as comparedwith lean women, tripled among those who were overweight, andquadrupled among those who were obese (Table 4). Among the parouswomen, the risk of late fetal death was significantly increasedonly among the obese women. For early neonatal death, the riskamong the nulliparous women was lowest among lean women andwas approximately twice as high among women with higher body-massindexes. Among the parous women, body-mass index did not influencethe risk of early neonatal death.
Table 4. Adjusted Odds Ratios for Late Fetal Death and Early Neonatal Death Associated with Prepregnancy Body-Mass Index among Nulliparous and Parous Women Delivering Singleton Infants in Sweden in 1992 and 1993.
Among nulliparous women, the risk of very preterm delivery (at<32 weeks of gestation) was significantly increased for obesewomen, whereas body-mass index did not significantly influencethe risk of moderately preterm delivery (at 33 to 36 weeks)(Table 5). In contrast, among parous women, the risks of verypreterm and moderately preterm delivery were lower among normaland overweight women than among lean women. The risk of deliveringan infant who was small for gestational age was highest amongboth the lean nulliparous women and the lean parous women (Table 5),although the decrease in the risk of delivering a small-for-gestational-ageinfant with increasing body-mass index was greater among theparous women.
Table 5. Adjusted Odds Ratios for Preterm Delivery and Delivery of a Small-for-Gestational-Age Infant Associated with Prepregnancy Body-Mass Index among Nulliparous and Parous Women Delivering Live Singleton Infants in Sweden in 1992 and 1993.
The rate of hypertensive disease among nulliparous women consistentlyincreased with body-mass index, from 2.8 percent among the leanwomen to 10.2 percent among the obese women. Excluding womenwith hypertensive diseases did not lower the risk of late fetaldeath associated with increasing body-mass index, whereas therisk of very preterm delivery (at <32 weeks) associated withobesity decreased and was no longer significant after this exclusion(data not shown). Excluding women with diabetes did not changethese estimates (data not shown).
Discussion
The results of this large, population-based cohort study suggestthat the risk of late fetal death consistently increases withprepregnancy body-mass index among nulliparous women, whereasthe risk of early neonatal death is almost doubled among nulliparouswomen with higher body-mass indexes. The pattern of risk amongparous women was different; obesity was associated with latefetal death but not with early neonatal death.
Chance is an unlikely explanation for our findings, becauseof the large sample and the consistency of our results. Besidesthe adjustment for possible confounding variables, the relativelyhomogeneous population of women born in Sweden, Denmark, Norway,Finland, or Iceland and the use of standardized records shouldfurther minimize the potential for confounding by unmeasuredsociodemographic factors or differences in management. Inadequateweight gain has been linked to an increased risk of the deliveryof a small-for-gestational-age infant,6 but its associationwith other adverse pregnancy outcomes is less certain.12,13,14,15,16Weight gain during pregnancy is poorly correlated with prepregnancybody-mass index.17 In the present study, low weight gain wasabove all positively associated with the delivery of a small-for-gestational-ageinfant. Caution is advised in interpreting these results, however,because of the large proportion of women with missing informationon weight gain during pregnancy.
Preeclampsia is more common among nulliparous than parous women,18and the rates of preeclampsia increase with increasing maternalweight.19,20 Because preeclampsia may lie on the causal pathwaybetween excessive weight and adverse pregnancy outcomes,18,21we did not control for hypertensive diseases in the primarymultivariate models. When we excluded nulliparous women withhypertensive diseases, however, the risk of very preterm deliverythat was associated with higher body-mass index decreased, whereasthe corresponding risk of late fetal death did not change.
The biologic mechanisms underlying the association between increasingprepregnancy body-mass index and a greater risk of late fetaldeath among nulliparous women remain speculative. Thinner womenmay have healthier habits or may be more able to perceive adecrease in fetal movements. Maternal overweight and obesityare associated with hyperlipidemia, which reduces prostacyclinsecretion and enhances peroxidase production, resulting in vasoconstrictionand platelet aggregation.20 These changes may increase the riskof preeclampsia, but they probably occur even in the absenceof preeclampsia.
Lean mothers, who are often considered to be underweight, havean elevated risk of delivering small-for-gestational-age infants.3,8,22The association between low maternal body-mass index and pretermdelivery is less consistent.12,22,23 In studies in three developedcountries, the risks of stillbirth and perinatal or infant deathwere lowest among infants born to the leanest women,2,13,24and the rates of preeclampsia are lowest among lean women.19The collective evidence, although limited, is thus compatiblewith our findings and suggests that pregnancies among lean womenshould be regarded as characterized by a low rather than a highrisk of adverse outcome and that advising lean women to gainweight before becoming pregnant may not be justified.
From the standpoint of primary prevention, adverse pregnancyoutcomes related to overweight may, at least theoretically,be preventable. If women with a body-mass index of 25.0 or morereduced it to 20.0 to 24.9, and thereby reduced their risk ofadverse outcomes accordingly, we estimate that the rate of latefetal death would be reduced by 11 percent. If all women witha body-mass index of 20.0 or more reduced it to less than 20.0,the rate of late fetal death would be reduced by 27 percent.
It is important that our results were obtained in a developedcountry where even lean women are likely to have adequate nutritionalstores to meet the basic requirements of pregnancy. These resultsmust not be generalized to developing countries, particularlythose in which maternal undernutrition is highly prevalent,nor should they be used to undermine public health efforts toimprove prepregnancy and gestational energy intake in areaswhere the quantity or quality of food is insufficient.
The prevalence of overweight has increased among women in manycountries in recent decades.25,26,27,28 In the United States,for example, the prevalence of overweight (body-mass index,>27.8) among women 20 to 29 years of age increased from 12.6percent in 1971 through 1974 to 20.2 percent in 1988 through1991.26 In Sweden, the increase of overweight among women hasbeen less prominent, but it is nevertheless indisputable.27Although these trends are evident in all demographic subgroups,overweight is more common among less well educated women and,in the United States, among black women.25,26,27 Furthermore,the upward trend in the prevalence of overweight is continuingdespite its well-publicized adverse effects on health.29,30Maternal overweight may be one of the most important preventablerisk factors for perinatal mortality and could partly explainthe socioeconomic differences in the rates of perinatal mortalityin developed countries, especially among nulliparous women.Our findings thus provide further justification for the developmentof effective strategies to reverse the trends toward increasingbody weight and a higher prevalence of overweight.
Dr. Kramer is a Distinguished Scientist of the Medical ResearchCouncil of Canada.
Source Information
From the Department of Medical Epidemiology, Karolinska Institute, Stockholm, Sweden (S.C., R.B., L.L.); the Department of Statistics, Uppsala University, Uppsala, Sweden (R.B.); the Department of Community Medicine, Mount Sinai School of Medicine, New York (L.L.); and the Departments of Pediatrics and of Epidemiology and Biostatistics, McGill University Faculty of Medicine, Montreal (M.S.K.).
Address reprint requests to Dr. Cnattingius at the Department of Medical Epidemiology, P.O. Box 281, Karolinska Institute, S-171 77 Stockholm, Sweden.
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