Rode, Line MD*; Nilas, Lisbeth MD, Dr Sci*; Wøjdemann, Karen MD, PhD*; Tabor, Ann Dr Sci*†
Adults who are overweight are an increasing problem in modern society. As many as 30–40% of Danish adults are overweight, and 10–13% are obese.1 In addition, the risk of obesity has doubled within a 10-year period.2 A large body mass index (BMI) in women before pregnancy increases their risk of maternal disease, for example, gestational diabetes, hypertension, and preeclampsia, during pregnancy.2,3 Overweight and obese women have an increased risk of delivery complications, such as induction of labor, vacuum extraction, cesarean delivery, and infectious complications.4–6 Several studies also have described an association between maternal weight and neonatal morbidity, such as a higher rate of stillbirth, birth defects, and fetal macrosomia.7–9
Most studies addressing the relationship between maternal BMI and pregnancy outcome are from American researchers, whereas little is known about the importance of the changing weight distribution in the general population on pregnancy outcome in Scandinavia.2,7,10,11 Large differences exist in the ethnic composition of different populations, and cultural and social differences may have an impact on pregnancy outcome. The cesarean delivery rate varies from country to country (15.2% in Denmark in 200112 compared with 26.1% in the United States in 200213), which implies that pregnancies and deliveries are handled differently in different countries.
The objective of this study was to analyze the relationship between the prepregnancy BMI and maternal complications, complications during delivery, and fetal/neonatal complications in a large, unselected Danish cohort of pregnant women. We specifically wanted to estimate the risk of being overweight on adverse pregnancy outcome in a population of women with singleton cephalic term delivery and compare these outcomes in nulliparous and multiparous women.
MATERIALS AND METHODS
In the present study, we included women participating in the Copenhagen First Trimester Study.14 At inclusion into the Copenhagen First Trimester Study, women underwent an ultrasound examination to assess whether the gestational age before 15 weeks of gestation. Women presenting at a gestational age later than this were not included. Between 1998 and 2001, 10,045 women were enrolled at 3 hospitals in Copenhagen, and among these, 9,122 had a self-reported prepregnancy BMI registered at the time of inclusion. A total of 9,017 women delivered, whereas 105 women had a miscarriage. The Copenhagen First Trimester Study was approved by the Scientific Ethics Committee of the cities of Copenhagen and Frederiksberg (No. [KF] 01–288/97). Informed consent was obtained from all participants.
The cohort of the 9,017 pregnancies was divided into 8 subgroups according to parity, gestational age, number of fetuses, and their presentation using Robson's 10 groups15 as a guideline. We defined our study population as the 8,092 pregnancies with single cephalic delivery at 37 weeks or greater of gestation. The following complications were registered: different maternal complications throughout pregnancy (diabetes, hypertension, preeclampsia), complications during delivery (premature rupture of the membranes, placental abruption, cesarean delivery, vacuum extraction, shoulder dystocia, and perineal rupture), as well as fetal or neonatal complications: preterm or post-term delivery (< 37 weeks of gestation or > 42 weeks of gestation), low arterial umbilical cord pH (< 7.0), low Apgar score (< 7 at 5 minutes), and birth weight less than 2,500 g or greater than 3,999 g. The population was unselected, and women with known pregestational diabetes and hypertension were therefore included in the population. The rate of shoulder dystocia and perineal rupture (third and fourth degree) was determined in a selected subpopulation of 3,635 women (2,237 of whom were nulliparous), ie, those women who delivered at 1 of the 3 university hospitals participating in the study.
The BMI was defined as the weight in kilograms divided by the square of the height in meters. We stratified the women according to BMI into 3 groups: BMI less than 25 kg/m2 (normal weight), BMI 25–29.9 kg/m2 (overweight), and BMI 30 kg/m2 or greater (obese). Hypertension was defined as a systolic blood pressure of greater than 140 mm Hg and a diastolic blood pressure of greater than 90 mm Hg or an increase of 20 mm Hg or greater in the diastolic blood pressure during pregnancy. Preeclampsia was defined as hypertension (as mentioned previously) and significant proteinuria (protein > 0.5 g/d). Diabetes included both pregestational and gestational diabetes.
We used the SPSS 12.0 software (SPSS Inc., Chicago, IL) for all statistical analyses, which were performed as multivariate regression analyses of the associations between BMI and parity and complications. We included the categorical variables: maternal age (< 25, 25–29, 30–34, or > 34 years), smoking (none, 1–5, 6–10, 11–20, or > 20 cigarettes per day), ethnic background (Caucasian, Asian, black, or other), and type of conception (assisted or spontaneous). Variables were excluded from the multivariate logistic regression analyses using backward stepwise removal (using P < .05 as exclusion criterion). Results were expressed as odds ratios (ORs) including the corresponding 95% confidence interval (CI).
Among the 9,122 women, the mean BMI was 22.9 kg/m2, and it was similar in nulliparous (22.7 kg/m2) and multiparous women (23.2 kg/m2). We found a BMI ≥ 25 kg/m2 in 21.8% of all the women, with 16.3% being overweight and 5.5% obese. A total of 24.2% multiparous women had a BMI ≥ 25 kg/m2 compared with 19.9% of nulliparous women (P < .001).
Among the 9,017 women who delivered, 371 women gave birth to a live child before 37 weeks of gestation, 331 had a breech presentation or abnormal lie, and 199 carried multiple pregnancies. Information on parity was not available for 24 women. The OR for multiple pregnancies was 1.49 (95% CI 1.09–2.02) in women with a BMI of 25 kg/m2 or greater. No significant difference was found in the rate of breech presentation or abnormal lie between normal-weight and overweight or obese women.
For the group of women with single cephalic pregnancies (n = 8,463) we found an OR of 1.4 (95% CIs 1.2–1.7 and 0.9–1.91.9) for preterm pregnancies (< 37 weeks of gestation) in both overweight and obese women, respectively. The OR for nulliparous women was 1.4 (95% CI 1.1–1.7) compared with multiparous women (maternal age included in the analysis). Of the preterm deliveries, 37.6% had induced labor compared with 18.5% of the term deliveries (P < .001). Induced labor was mainly performed because of premature rupture of membranes, preeclampsia, intrauterine growth restriction, and placental abruption. We also found an OR of 1.4 (95% CIs 1.2–1.7 and 1.1–1.9) for postterm pregnancies (> 42 weeks of gestation) and, again, nulliparous women had an OR of 1.8 (95% CI 1.5–2.1) compared with multiparous women. A term pregnancy was therefore achieved by 87.2% of normal weight women and 83.1% in women with a BMI of 25 kg/m2 or greater (P < .001), and 89.3% multiparous women carried term pregnancies compared with 84.6% of nulliparous women (P < .001).
The remaining 8,092 single cephalic pregnancies with an outcome at 37 weeks or greater of gestation consisted of 5,044 nulliparous and 3,048 multiparous women. In this population, overweight and obese women were more frequent in the multiparous group (15.2% versus 17.4% and 4.7% versus 6.7%, P values .01).
The frequency of maternal diabetes, hypertension, and preeclampsia increased with an increasing BMI (Table 1). Nulliparous women had an increased risk of developing preeclampsia (OR 2.8, 95% CI 2.0–4.1) and hypertension (OR 1.9, 95% CI 1.01–3.4) compared with multiparous women but no significant difference in the risk of diabetes.
We did not find any significant difference in the frequency of premature rupture of membranes, placental abruption, vacuum extraction, shoulder dystocia, or perineal rupture between the 3 BMI groups. However, nulliparous women had an increased risk (OR 5.6, 95% CI 4.5–6.8) of having vacuum extraction compared with multiparous women, as well as an increased risk (OR 2.2, 95% CI 1.4–3.5) of perineal rupture (OR 1.7, 95% CI 1.1–2.8) when including vacuum extraction in the multivariate logistic regression analysis).
The women had an increased risk of cesarean delivery with an increasing BMI, and there was an association with parity (Table 2). Both overweight and obese women had an increased risk of an emergency cesarean delivery (all nonplanned cesarean deliveries), whereas the risk of an elective cesarean delivery only was increased in obese women. Nulliparous women had a greater risk of having an emergency cesarean delivery than multiparous women (OR 3.4, 95% CI 2.8–4.2), and multiparous women had an elective cesarean delivery more frequently than nulliparous women (OR 4.0, 95% CI 3.0–5.3). Whereas as emergency cesarean delivery was performed mainly because of fetal distress (36.6%), cephalopelvic disproportion (33.0%), and lack of progression of labor (10.1%), 48.9% of elective cesarean deliveries were performed because of previous delivery complications or previous cesarean delivery. When excluding women with an elective cesarean delivery based on the indication of a previous cesarean delivery, the frequency of elective cesarean deliveries declined from 6.5% to 3.6% (P < .001), and the frequency of emergency cesarean deliveries remained unchanged (4.8% compared with 4.7%). This resulted in a total of 8.3% of cesarean deliveries among multiparous compared with the 13.2% among nulliparous (P < .001).
We found no association between intrauterine growth restriction and BMI or parity. However, obese women had an OR of 2.8 (95% CI 1.4–5.6) of having a low birth weight child (< 2,500 g at term) whereas overweight women had an unchanged risk compared with normal-weight women (Table 3). An increasing BMI resulted in an increasing risk of having a macrosomic child (> 3,999 g) for overweight OR 1.3 (95% CI 1.1–1.5) and obese 1.8 (95% CI 1.4–2.2) women. Nulliparous women had an OR of 1.8 (95% CI 1.1–3.1) of having a low birth weight child compared with multiparous women, whereas multiparous women had an OR of 1.5 (9% CI 1.3–1.7) of having a macrosomic child compared with nulliparous women.
No difference was found in the frequency of Apgar score less than 7 at 5 minutes (0.5–0.8%), the frequency of umbilical cord pH less than 7.0, or the need for admission to the neonatal intensive care unit (NICU) between the 3 BMI groups. Infants who were delivered via vacuum extraction or emergency cesarean delivery had an increased risk of a low Apgar score (OR 2.5, 85% CI 1.3–4.9 and OR 5.0, 95% CI 2.7–9.2, respectively). When these variables were included in the multivariate logistic regression analysis, no difference was found between nulliparous and multiparous women.
In this study, we have shown that Danish women, especially nulliparous women, with a high prepregnancy BMI are at increased risk of having complications during pregnancy (diabetes, hypertension, and preeclampsia) and delivery (vacuum extraction, cesarean delivery). This conclusion is in accordance with previous studies from other populations. However, there are only few Scandinavian studies based on prospectively collected data reporting the relationship between prepregnancy BMI and both maternal complications, delivery complications, and complications to the unborn/newborn child2,7 and only one that includes the significance of parity.7 From an unselected sample of the population, we selected single cephalic pregnancies with an outcome after 37 gestational weeks and then compared nulliparous and multiparous women. By excluding women with multiple pregnancies and/or preterm pregnancies and breech presentation, who are at higher risk of complications, we created a more homogenous group with a similar basic risk profile.
All women in this study were included during the first trimester of their pregnancy. Although the prepregnancy weight was self-reported, this early time of registration may decrease the underestimation of BMI compared with studies that include women presenting during the second trimester of the pregnancy. However, underreporting is likely to occur in any study based on self-reported weight.
In accordance with other studies, we found that being overweight prior to is associated with fetal macrosomia.16 The increased risk of macrosomia has been explained by an increased incidence of diabetes mellitus (maternal hyperglycemia) in obese women. However, Jensen et al2 also found an association between macrosomia and being overweight in a population of 2,459 glucose-tolerant Danish women, which indicates that being overweight or obese may influence the nutrition and growth of the fetus in ways not yet explained. We found no association between intrauterine growth restriction and obesity, but our data indicate that there may be a small group of obese nulliparous women with an increased risk of having a low birth weight child, an observation that, to our knowledge, is new. This could indicate that this group of women is a subgroup with a different pathophysiology than other obese women. However, our results are based on a small number of observations.
The rate of cesarean delivery increased with an increasing BMI, with emergency cesarean deliveries being more frequent in nulliparous women and elective cesarean deliveries more frequent in multiparous women. The increased cesarean delivery rate in overweight and obese women may explain the fact that we did not find an association between shoulder dystocia and obesity. There was no relationship between the prepregnancy BMI and the rate of vacuum extraction, which may explain why we did not find an increased risk of severe complications during vaginal delivery (perineal rupture) in overweight and obese women.
Our results on the association between obesity and emergency cesarean delivery are in accordance with other studies.4,7,10,11 The main indications for cesarean delivery are cephalopelvic disproportion, fetal distress, and lack of progression of labor,17 which are responsible for nearly 80% of the emergency cesarean deliveries in our study. Some studies find that the increased risk of surgical delivery is directly related to the higher risk of induction of labor,18 and Galtier-Dereure19 explains the increased frequency of cesarean delivery by pregnancy-related complications as diabetes and hypertension. A Swedish study18 similarly found that the increased rate of cesarean delivery was only observed in cases of women with obesity-related complications and not in obese women without complications. It is therefore possible that the increased rate of cesarean delivery is limited to certain subgroups of overweight women. An increased rate of cesarean delivery has, however, also been reported in overweight women with a normal oral glucose tolerance test.2
We found a higher risk of preterm delivery in overweight and obese women, with nulliparous women being at increased risk. This is in accordance with the findings of Cnattingius,7 who found that the risk of preterm delivery was increased in obese nulliparous women. Induced labor was more common in preterm deliveries because of pregnancy complications such as premature rupture of the membranes, preeclampsia, and intrauterine growth restriction.
In our single cephalic term population, we did not find a relationship between the prepregnancy BMI and either the Apgar score at 5 minutes or an umbilical cord pH of less than 7.0. As expected, both vacuum extraction and emergency cesarean delivery were associated with an increased frequency of a low Apgar score at 5 minutes. However, the data showed a similar rate of postnatal admittance to a NICU, which may indicate that there are no adverse short-term effects on neonatal morbidity. However, in a study of 188 morbidly obese women (BMI > 40 kg/m2), Kumari16 reported an increased rate of admittance to the NICU (16%) as compared with nonobese women (4%). There was no difference in the Apgar score (< 7 at 1 minute), and macrosomia was the main reason for referral. In our population, only 37 women (0.5%) had a prepregnancy BMI of 40 kg/m2 or greater.
Our results on single cephalic term pregnancies stress the importance of concentrating on trying to reduce the increasing incidence of overweight and obesity in fertile women, especially in nulliparous women. The best time of intervention may be before a woman even considers a pregnancy, because it is not recommended that obese women lose weight during pregnancy as a result of the increased risk of ketosis.20 Although there may be some obstacles (eg, a minimum weight gain, importance of a sufficient dietary intake, and precautions concerning excessive exercise), early pregnancy may, however, be a good time to instruct overweight and obese women to reduce their weight gain and thereby the many complications that occur during pregnancy and delivery. Motivating people to weight loss has turned out to be a very difficult task, and reduced weight gain among pregnant women may therefore require a rather large effort and a significant interdepartmental co-operation in health services. However, results from smoking campaigns suggest that women may be more motivated at this point in life.21 It still remains to be seen whether a reduced weight gain during pregnancy can assist in reducing the number of complications during pregnancy and delivery in overweight and obese women. Meanwhile, in addition to an effort in reducing the average BMI in the population, it may be beneficial to monitor overweight and obese women more carefully, with the main focus on nulliparous women to be able to intervene earlier if complications arise.
2. Jensen DM, Damm P, Sorensen B, Molsted-Pedersen L, Westergaard JG, Ovesen P, et al. Pregnancy outcome and prepregnancy body mass index in 2459 glucose-tolerant Danish women. Am J Obstet Gynecol 2003;189(1):239–44.
3. Baeten JM, Bukusi EA, Lambe M. Pregnancy complications and outcomes among overweight and obese nulliparous women. Am J Public Health 2001;91:436–40.
4. Crane SS, Wojtowycz MA, Dye TD, Aubry RH, Artal R. Association between pre-pregnancy obesity and the risk of cesarean delivery. Obstet Gynecol 1997;89:213–6.
5. Cedergren MI. Maternal morbid obesity and the risk of adverse pregnancy outcome. Obstet Gynecol Surv 2004;103:219–24.
6. Sebire NJ, Jolly M, Harris JP, Wadsworth J, Joffe M, Beard RW, et al. Maternal obesity and pregnancy outcome: a study of 287,213 pregnancies in London. Int J Obes Relat Metab Disord 2001;25:1175–82.
7. Cnattingius S, Bergstrom R, Lipworth L, Kramer MS. Prepregnancy weight and the risk of adverse pregnancy outcomes. N Engl J Med 1998;338:147–52.
8. Stephansson O, Dickman PW, Johansson A, Cnattingius S. Maternal weight, pregnancy weight gain, and the risk of antepartum stillbirth. Am J Obstet Gynecol 2001;184:463–9.
9. Watkins ML, Rasmussen SA, Honein MA, Botto LD, Moore CA. Maternal obesity and risk for birth defects. Pediatrics 2003;111:1152–8.
10. Jensen H, Agger AO, Rasmussen KL. The influence of prepregnancy body mass index on labor complications. Acta Obstet Gynecol Scand 1999;78:799–802.
11. Valentin TD, Sorensen JA, Andreasen EE. [Obese pregnant women have complicated deliveries]. Ugeskr Laeger 2003;165:1027–30.
13. Martin JA, Hamilton BE, Sutton PD, Ventura SJ, Menacker F, Munson ML. Births: final data for 2002. Natl Vital Stat Rep 2003;52:1–113.
14. Wojdemann KR, Larsen SO, Shalmi A, Sundberg K, Christiansen M, Tabor A. First trimester screening for Down syndrome and assisted reproduction: no basis for concern. Prenat Diagn 2001;21:563–5.
15. Robson MS. Can we reduce the caesarean section rate? Best Pract Res Clin Obstet Gynaecol 2001;15:179–94.
16. Kumari AS. Pregnancy outcome in women with morbid obesity. Int J Gynaecol Obstet 2001;73:101–7.
17. Brost BC, Goldenberg RL, Mercer BM, Iams JD, Meis PJ, Moawad AH, et al. The Preterm Prediction Study: association of cesarean delivery with increases in maternal weight and body mass index. Am J Obstet Gynecol 1997;177:333–337; discussion 337-41.
18. Ekblad U, Grenman S. Maternal weight, weight gain during pregnancy and pregnancy outcome. Int J Gynaecol Obstet 1992;39:277–83.
19. Galtier-Dereure F, Boegner C, Bringer J. Obesity and pregnancy: complications and cost. Am J Clin Nutr 2000;71(Suppl 5):1242S–8S.
20. Dewey KG, McCrory MA. Effects of dieting and physical activity on pregnancy and lactation [review]. Am J Clin Nutr 1994;59(suppl 2):446S–52S; discussion 452S-3S.
21. Hegaard HK, Kjaergaard H, Moller LF, Wachmann H, Ottesen B. Multimodal intervention raises smoking cessation rate during pregnancy. Acta Obstet Gynecol Scand 2003;82:813–9.