IJG-08245; No of Pages 4 International Journal of Gynecology and Obstetrics xxx (2015) xxx–xxx
Contents lists available at ScienceDirect
International Journal of Gynecology and Obstetrics journal homepage: www.elsevier.com/locate/ijgo
CLINICAL ARTICLE
Pregnancy outcome according to pre-pregnancy body mass index and gestational weight gain Joanna Gesche ⁎, Lisbeth Nilas Department of Obstetrics and Gynecology, Hvidovre Hospital, University of Copenhagen, Hvidovre, Denmark
a r t i c l e
i n f o
Article history: Received 17 November 2014 Accepted 2 March 2015 Keywords: Body mass index Fetal weight Gestational weight gain Obesity Pregnancy
a b s t r a c t Objective: To assess birth weight in relation to gestational weight gain (GWG) among women who were and were not obese before pregnancy. Methods: For a retrospective cohort study, data were obtained for women with a prepregnancy body mass index (BMI, calculated as weight in kilograms divided by the square of height in meters) of at least 30 who had a singleton delivery at a center in Denmark in 2010–2011. Data were also obtained for 455 non-obese women (BMI 20.0–24.9). GWG was expressed in absolute terms and relative to published recommendations (11–16 kg in non-obese women; 5–9 kg in obese women). Results: A total of 231 obese women were included in analyses. In non-obese and obese women, fetal weight was highest when GWG was above the recommended amount. Among women who had a GWG in line with the recommendations, mean birth weight was higher among those with a pre-pregnancy BMI of 35.0–39.9 (3758 ± 410 g) or at least 40 (3671 ± 374 g) than among non-obese women (3394 ± 453 g; P = 0.0058). Conclusion: Birth weight is related to both maternal BMI and GWG. In obese women, adherence to GWG recommendations does not seem to prevent increased birth weights. © 2015 International Federation of Gynecology and Obstetrics. Published by Elsevier Ireland Ltd. All rights reserved.
1. Introduction Overweight and obesity are related to many health problems that challenge healthcare systems worldwide. The prevalence of obesity has been steadily increasing worldwide [1], including among pregnant women. The proportion of pregnant women who are obese is now 12.2% in Denmark [2], and is even higher in other countries [3]. Obesity is associated with an increased risk of metabolic pregnancy complications, hypertensive disorders [4], gestational diabetes [5], delivery problems [6,7], and adverse pregnancy outcomes (e.g. macrosomia [8]). The risk of pregnancy complications and adverse fetal outcome in obese pregnant women can be modified by limiting gestational weight gain (GWG) [9–12]. Indeed, women who were not obese before pregnancy but gain excessive weight during pregnancy and are obese at term have an increased risk of pregnancy complications and adverse pregnancy outcome compared with women with a lower weight gain [13]. The US Institute of Medicine (IOM) recommendations on GWG differentiate according to pre-pregnancy body mass index (BMI; calculated as weight in kilograms divided by the square of height in meters) and advise limiting GWG to 11–16 kg for women with a pre-pregnancy BMI of 18.5–24.9 and 5–9 kg for women with a BMI of at least 30 [14,15]. It has
⁎ Corresponding author at: Department of Obstetrics and Gynecology, Hvidovre Hospital, Kettegårds Allé 30, 2650 Hvidovre, Denmark. Tel.: +45 41 14 59 62; fax: +45 38 62 27 04. E-mail address: [email protected] (J. Gesche).
been suggested that a GWG of less than the IOM recommendations in obese and morbidly obese women can improve pregnancy outcomes further, but the results are inconsistent, and possible risks associated with lower GWG or even weight loss have not been identified [16,17]. The aim of the present study was to assess birth weight in relation to compliance with the IOM GWG recommendations in nonobese and obese pregnant women. Additionally, the occurrence of macrosomia, pregnancy complications, and adverse pregnancy outcomes was compared. 2. Materials and methods For a retrospective study, all women with a pre-pregnancy BMI of at least 30 who had a singleton delivery at the Department of Obstetrics, Hvidovre Hospital, Hvidovre, Denmark, between January 1, 2010, and December 31, 2011, were considered for inclusion. Additionally, women with a pre-pregnancy BMI of 20.0–24.9 who had a singleton delivery at the study center were selected for inclusion in a control group. On the basis of power calculations, it was determined that 455 women would need to be included in the control group. All births on the 15th and 30th of each month in the study period were identified and included in this group. The study was approved by the Danish Data Protection Agency (Jr.nr. 2012-41-0400). Informed consent from all study participants had been obtained. Self-reported pre-pregnancy weight registered in the obstetric database was used to calculate pre-pregnancy BMI. Women with a pre-pregnancy BMI of at least 30 were stratified into obesity class I
http://dx.doi.org/10.1016/j.ijgo.2014.12.013 0020-7292/© 2015 International Federation of Gynecology and Obstetrics. Published by Elsevier Ireland Ltd. All rights reserved.
Please cite this article as: Gesche J, Nilas L, Pregnancy outcome according to pre-pregnancy body mass index and gestational weight gain, Int J Gynecol Obstet (2015), http://dx.doi.org/10.1016/j.ijgo.2014.12.013
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J. Gesche, L. Nilas / International Journal of Gynecology and Obstetrics xxx (2015) xxx–xxx
(pre-pregnancy BMI 30.0–34.9), obesity class II (35.0–39.9), and obesity class III (≥40.0). Participant characteristics, pregnancy and delivery data, and neonatal outcome were obtained from a local obstetric database. Characteristics assessed were age, parity, place of birth (Denmark vs elsewhere), and smoking status at first hospital visit (yes vs no). Pregnancy induced hypertension (PIH) was defined as a diastolic blood pressure over 90 mm Hg or a systolic blood pressure over 140 mm Hg after 20 weeks of pregnancy in women who had had a normal blood pressure at the onset of pregnancy. PIH and proteinuria (measured by positive dip-stick; at least two positive results needed) was defined as pre-eclampsia. Severe pre-eclampsia included general symptoms of PE and/or a diastolic blood pressure over 110 mm Hg or a systolic blood pressure over 160 mm Hg. Delivery complications assessed were shoulder dystocia, instrumental vaginal delivery, induction of labor, and the occurrence of cesarean. Outcome data analyzed were the newborn’s length and weight, gestational age (determined at a nuchal scan at 11–14 weeks of pregnancy), umbilical artery pH, placental weight, and admission to the neonatal intensive care unit within 24 hours of delivery. Fetal weight was also expressed as Z-scores, which are defined as percentage of expected birth weight adjusted for sex and gestational age on standardized growth charts expressed as standard deviations of the mean [18]. A small-for-gestational-age newborn had a Z-score of less than –2, or below –22% of the mean; a large-for-gestational-age newborn had a Z-score greater than + 2, or over 22% of the expected mean [18]. Low birth weight was defined as a birth weight under 2500 g and macrosomia as a birth weight over 4000 g. Uncomplicated vaginal delivery was defined as vaginal delivery without labor induction or instrumentation during delivery. The mother’s weight at term (at 35 full weeks or later) was recorded. GWG was defined as weight at term minus self-reported weight at the beginning of pregnancy. GWG was used as a continuous variable and stratified according to the current recommendations by the IOM: less than 5 kg, 5–9 kg, and more than 9 kg for obese women; and less than 11 kg, 11–16 kg, and more than 16 kg for normal weight women [14]. The groups were compared using Wilcoxon rank-sum and KruskalWallis tests for continuous variables, and χ2 and Fisher exact tests for categorical variables. A 0.05 significance level and 80% power were used. Analyses were performed using R version 2.15.0 (http://www.rproject.org/).
Table 2 Pregnancy complications and outcomes.a Complication/outcome
Non-obese women (n = 455)b
Obese women (n = 231)c
P value
Pregnancy-induced hypertension Pre-eclampsia Urinary infection Birth weight, g Macrosomia Small-for-gestational-age neonate Large-for-gestational-age neonate Admission to neonatal intensive care unit Gestational age, d Placental weight, g Instrumental delivery Induced delivery Labor augmentation Epidural Uncomplicated vaginal delivery Cesarean delivery Emergency Elective Perineal tear Episiotomy
7 (1.5) 21 (4.6) 75 (16.5) 3482 ± 509 62 (13.6) 16 (3.5) 8 (1.8) 9 (2.0)
11 (4.4) 31 (13.4) ¨50 (21.6) 3518 ± 578 41 (17.7) 6 (2.6) 15 (6.5) 19 (8.2)
0.031 b0.001 NS b0.001 NS NS 0.039 b0.001
279.9 ± 10.8 652.8 ± 144.9 55 (12.1) 110 (24.2) 195 (42.9) 102 (22.4) 236 (52.5) 89 (19.6) 53 36 260 (57.1) 17 (3.7)
276.3 ± 14.6 678.5 ± 154.7 20 (8.7) 79 (34.2) 107 (46.3) 77 (33.3) 82 (35.5) 75 (32.5) 34 41 115 (49.8) 2 (0.8)
0.0016 0.038 NS 0.007 NS 0.0028 b0.001 b0.001
b0.001 0.026
Abbreviations: NS, nonsignificant; BMI, body mass index (calculated as the weight in kilograms divided by the square of height in meters). a Values are given as number (percentage) or mean ± SD, unless indicated otherwise. b BMI 20.0–24.9. c BMI ≥30.0.
Mean birth weight and the frequencies of admission to the neonatal intensive care unit, large-for-gestational-age neonates, PIH, and preeclampsia were all significantly higher among obese women than among non-obese women (Table 2). The frequency of uncomplicated vaginal delivery was lower among obese women than among nonobese women (P b 0.001), and the frequencies of induced delivery (P = 0.007), epidural (P = 0.0028), and cesarean (P b 0.001) were higher in the obese women. The frequencies of perineal tears and episiotomy were significantly lower in the obese women (Table 2). In the total population, there was a decreasing trend in vaginal delivery with increasing BMI (P = 0.0012).
3. Results Of 750 women with a pre-pregnancy BMI of at least 30, 485 had been approached for a randomized controlled trial of a dietary intervention, and 43 had missing data. Therefore, 231 obese women and 455 non-obese women with a pre-pregnancy BMI of 20–24.9 were included in analyses. Data on GWG were available for 174 obese women and 236 non-obese women. The obese women were significantly younger than were the non-obese women, fewer were nulliparous, and more were smokers (Table 1).
Table 1 Participant characteristics.a Characteristics
Non-obese women (n = 455)b
Obese women (n = 231)c
P value
Age, y Nulliparous Smoker
31.28 ± 4.55 233 (51.2) 26 (5.7)
30.07 ± 4.93 97 (42.0) 45 (19.5)
0.0018 0.027 b0.001
Abbreviation: BMI, body mass index (calculated as weight in kilograms divided by the square of height in meters). a Values are given as mean ± SD or number (percentage), unless indicated otherwise. b BMI 20.0–24.9. c BMI ≥30.0.
Fig. 1. GWG, by pre-pregnancy BMI. Abbreviations: GWG, gestational weight gain; BMI, body mass index (calculated as weight in kilograms divided by the square of height in meters). Boxes show medians and interquartile ranges. Error bars show ranges. Circles show outliers.
Please cite this article as: Gesche J, Nilas L, Pregnancy outcome according to pre-pregnancy body mass index and gestational weight gain, Int J Gynecol Obstet (2015), http://dx.doi.org/10.1016/j.ijgo.2014.12.013
J. Gesche, L. Nilas / International Journal of Gynecology and Obstetrics xxx (2015) xxx–xxx
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There were no differences in characteristics, pregnancy and delivery complications, and pregnancy outcome between the different obesity classes (data not shown). Obese women had a significantly lower mean GWG than did the non-obese women (10.5 kg vs 15.0 kg; P b 0.001). GWG decreased with increasing BMI (P = 0.030) (Fig. 1). The risk of macrosomia increased significantly (P = 0.002) with increasing GWG in the total population. The proportion of macrosomic newborns was highest among women whose GWG was above the recommended value in most groups (Table 3). Overall, 49 (28.2%) obese women and 106 (44.9%) non-obese women fulfilled the IOM GWG recommendations (P = 0.013). GWG was in line with the recommendations for 33 (28.4%) of 116 women in obesity class I, 9 (24.3%) of 37 women in obesity class II, and 7 (33.3%) of 21 women in obesity class III. Birth weight did not differ between non-obese women and women in obesity class I who had met the GWG recommendations, but it was significantly higher among women in obesity classes II and III (P = 0.0058) (Table 3, Fig. 2). Stratifying the women according to GWG in relation to the IOM recommendations showed that birth weight was related to both maternal BMI and GWG in non-obese and obese women (Table 3). 4. Discussion In the present study, the relationship between pre-pregnancy BMI, GWG, and the occurrence of adverse pregnancy outcomes has been examined. Both birth weight and likelihood of macrosomia were related to increasing maternal GWG. Although mean GWG was lower among obese women than among non-obese women, it was still higher than the IOM recommendation of 5–9 kg. Even when women in obesity classes II and III did adhere to GWG recommendations, the birth weight was significantly higher than among non-obese women and those in obesity class I who also had a GWG in line with advised values. Several intervention trials have been performed to minimize GWG in obese women, because obesity and excessive GWG have been associated with negative pregnancy outcomes [19,20]. Currently, there is only one GWG recommendation for obese women; little is known about the appropriate GWG for women in obesity classes II and III and the consequences of inadequate GWG [21]. In the present study, women in obesity classes II and III gave birth to heavier neonates than did non-obese women, even when following the IOM GWG recommendations. Therefore, separate GWG recommendations according to obesity class are needed. The present results indicate that women in obesity classes II and III should probably gain less than is currently recommended by the IOM. Even though obese women have a significantly lower GWG than do non-obese women, only approximately one-third of obese women in the present study met the GWG recommendations, compared with
Fig. 2. Birth weight among women whose GWG was in line with recommendations (11–16 kg for non-obese women; 5–9 kg for obese women), by pre-pregnancy BMI. Abbreviations: GWG, gestational weight gain; BMI, body mass index (calculated as the weight in kilograms divided by the square of height in meters). Boxes show medians and interquartile ranges. Error bars show ranges. Circles show outliers. Birth weight was significantly higher among women in obesity classes II and III than among non-obese women (P = 0.0058).
44.9% of non-obese women. It has previously been shown that excessive GWG could be associated with childhood obesity [12], and GWG might have long-term effects on the offspring. Healthcare professionals have the opportunity to help pregnant women to adopt a healthier lifestyle, and behavioral intervention has proven effective in lowering GWG [19], which could modify some of the negative effects of pre-pregnancy obesity. The present study also showed an increasing prevalence of macrosomia with increasing GWG, independent of pre-pregnancy BMI. It has previously been shown that the body fat of the neonate increases for each additional kilogram of GWG [22]. Delivering a macrosomic fetus entails complications [23], and lowering GWG could minimize the risk of macrosomia, both for obese and non-obese women. However, reducing the GWG recommendations for obese women, especially those in obesity classes II and III, could increase the risk that a newborn is small for its gestational age. Nevertheless, little is known about the implications of too low a weight gain during pregnancy or even weight loss [21]. One limitation of the present study was that the GWG entries in the database relied on self-reported data from the patients’ files. It has
Table 3 Fetal weight and occurrence of macrosomia, by GWG.a Non-obese women (n = 236)b
Fetal weight when GWG less than recommended, g Macrosomic newborns Fetal weight when GWG as recommended, g Macrosomic newborns Fetal weight when GWG above recommended, g Macrosomic newborns
3292 ± 630 4/45 (8.9) 3394 ± 453 9/106 (8.5) 3708 ± 517g 23/85 (27.1)
Obese women (n = 174) Class Ic (n = 116)
Class IId(n = 37)
Class IIIe(n = 21)
3209 ± 877 0/14 3539 ± 499 6/33 (18.2) 3548 ± 530 12/69 (17.4)
3342 ± 488 1/10 (10.0) 3758 ± 410f 2/9 (22.2) 3685 ± 297 5/18 (27.8)
3646 ± 351 1/8 (12.5) 3671 ± 374f 2/7 (28.6) 3861 ± 333 2/6 (33.3)
Abbreviations: GWG, gestational weight gain; BMI, body mass index (calculated as weight in kilograms divided by the square of height in meters). a Values are given as mean ± SD or number/total number (percentage). b BMI 20.0–24.9. c BMI 30.0–34.9. d BMI 35.0–39.9. e BMI ≥40. f P = 0.0058. g P b 0.001.
Please cite this article as: Gesche J, Nilas L, Pregnancy outcome according to pre-pregnancy body mass index and gestational weight gain, Int J Gynecol Obstet (2015), http://dx.doi.org/10.1016/j.ijgo.2014.12.013
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previously been shown that self-reported pre-pregnancy weight can be underestimated, which leads to an overestimation of GWG [24]. GWG was calculated the same way in all groups in the present study, but no data are available showing whether obese women preferentially overestimated or underestimated their pre-pregnancy weight. Another limitation was that weight at the end of pregnancy was the last entry, but it could have been measured at any point between 35 weeks to delivery. Weekly weight measurements are officially recommended from 38 weeks of pregnancy on, but both healthcare professionals and patients are reluctant to practice this, probably to avoid embarrassment. A strength of the present study is that it included an unselected cohort of a group of women from all obesity classes who received no dietary counseling or intervention, as well as a large group of randomly chosen non-obese women, thereby minimizing the risk of selection bias. Previous findings of an association between obesity and an elevated risk of large-for-gestational-age newborns, PIH, pre-eclampsia, and cesarean delivery [5,25–27], indicating that the population assessed resembles others. In summary, our study shows that obese women, although gaining significantly less weight than non-obese women, have a GWG above the value recommended by the IOM and that such excessive GWG increases the risk of macrosomia. Women in obesity class II and III with a GWG in line with the recommendations gave birth to heavier children than did non-obese weight women, indicating that GWG recommendations should be stratified according to obesity class. Further studies are needed to evaluate the IOM GWG recommendations and their implications for obesity classes II and III. Conflict of interest The authors have no conflicts of interest. References [1] Heitmann BL. Ten-year trends in overweight and obesity among Danish men and women aged 30–60 years. Int J Obes Relat Metab Disord 2000;24(10):1347–52. [2] Danish Health and Medicines Authority. Births, pregnancy and BMI 2004–1st half of 2008. Copenhagen: Danish Health and Medicines Authority; 2008. [3] Reynolds RM, Allan KM, Raja EA, Bhattacharya S, McNeill G, Hannaford PC, et al. Maternal obesity during pregancy and premature mortality from cardiovascular event in adult offsprint: follow-up of 1 323 275 years. BMJ 2013;347:f4539. [4] Schneider S, Freerksen N, Maul H, Roehrig S, Fischer B, Hoeft B. Risk groups and maternal-neonatal complications of preeclampsia—current results from the national German Perinatal Quality Registry. J Perinat Med 2011;39(3):257–65. [5] 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(8):1175–82.
[6] Wolfe KB, Rossi RA, Warshak CR. The effect of maternal obesity on the rate of failed induction of labor. Am J Obstet Gynecol 2011;205(2):128.e1–7. [7] Bhattacharya S, Campbell DM, Liston WA, Bhattacharya S. Effect of body mass index on pregnancy outcomes in nulliparous women delivering singleton babies. BMC Public Health 2007;7:168. [8] Catalano PM, McIntyre HD, Cruickshank JK, McCance DR, Dyer AR, Metzger BE, et al. The hyperglycemia and adverse pregnancy outcome study: associations of GDM and obesity with pregnancy outcomes. Diabetes Care 2012;35(4):780–6. [9] Jensen DM, Ovesen P, Beck-Nielsen H, Mølsted-Pedersen L, Sørensen B, Vinter C, et al. Gestational weight gain and pregnancy outcomes in 481 obese glucosetolerant women. Diabetes Care 2005;28(9):2118–22. [10] Nohr EA, Vaeth M, Baker JL, Sørensen TIA, Olsen J, Rasmussen KM. Combined associations of prepregnancy body mass index and gestational weight gain with the outcome of pregnancy. Am J Clin Nutr 2008;87(6):1750–9. [11] Kaar JL, Crume T, Brinton JT, Bischoff KJ, McDuffie R, Dabelea D. Maternal obesity, gestational weight gain, and offspring adiposity: the Exploring Perinatal Outcomes among Children Study. J Pediatr 2014;165(3):509–15. [12] Sridhar SB, Darbinian J, Ehrlich SF, Markman MA, Gunderson EP, Ferrara A, et al. Maternal gestational weight gain and offspring risk for childhood overweight or obesity. Am J Obstet Gynecol 2014;211(3):259.e1–8. [13] Mamula O, Severinski NS, Mamula M, Severinski S. Complications during pregnancy, labor and puerperium in women with increased BMI at pregnancy term. Cent Eur J Med 2009;4(1):71–5. [14] Rasmussen KM, Yaktine AL. Weight Gain During Pregnancy: Reexamining the Guidelines. Washington, DC: National Academies Press (US); 2009. [15] Rasmussen KM, Abrams B, Bodnar LM, Butte NF, Catalano PM, Maria Siega-Riz A. Recommendations for weight gain during pregnancy in the context of the obesity epidemic. Obstet Gynecol 2010;116(5):1191–5. [16] Hinkle SN, Sharma AJ, Dietz PM. Gestational weight gain in obese mothers and associations with fetal growth. Am J Clin Nutr 2010;92(3):644–51. [17] Blomberg M. Maternal and neonatal outcomes among obese women with weight gain below the new Institute of Medicine recommendations. Obstet Gynecol 2011; 117(5):1065–70. [18] Marsál K, Persson P, Larsen T, Lilja H, Selbing A, Sultan B. Intrauterine growth curves based on ultrasonically estimated foetal weights. Acta Paediatr 1996;85(7):843–8. [19] Agha M, Agha RA, Sandell J. Interventions to reduce and prevent obesity in preconceptual and pregnant women: a systematic review and meta-analysis. PLoS One 2014;9(5):e95132. [20] Walsh JM, McGowan CA, Mahony RM, Foley ME, McAuliffe FM. Obstetric and metabolic implications of excessive gestational weight gain in pregnancy. Obesity (Silver Spring) 2014;22(7):1594–600. [21] Oza-Frank R, Keim SA. Should obese women gain less weight in pregnancy than recommended? Birth 2013;40(2):107–14. [22] Carlsen EM, Renault KM, Nørgaard K, Nilas L, Jensen JE, Hyldstrup L, et al. Newborn regional body composition is influenced by maternal obesity, gestational weight gain and the birthweight standard score. Acta Paediatr 2014;103(9):939–45. [23] Stotland NE, Caughey AB, Breed EM, Escobar GJ. Risk factors and obstetric complications associated with macrosomia. Int J Gynecol Obstet 2004;87(3):220–6. [24] Mandujano A, Huston-Presley L, Waters TP, Catalano PM. Women’s reported weight: is there a discrepancy? J Matern Fetal Neonatal Med 2012;25(8):1395–8. [25] Ovesen P, Rasmussen S, Kesmodel U. Effect of prepregnancy maternal overweight and obesity on pregnancy outcome. Obstet Gynecol 2011;118(2 Pt 1):305–12. [26] Rode L, Hegaard HK, Kjaergaard H, Møller LF, Tabor A, Ottesen B. Association Between maternal weight gain and birth weight. Obstet Gynecol 2007;109(6): 1309–15. [27] Cedergren M. Effects of gestational weight gain and body mass index on obstetric outcome in Sweden. Int J Gynecol Obstet 2006;93(3):269–74.
Please cite this article as: Gesche J, Nilas L, Pregnancy outcome according to pre-pregnancy body mass index and gestational weight gain, Int J Gynecol Obstet (2015), http://dx.doi.org/10.1016/j.ijgo.2014.12.013
Contents lists available at ScienceDirect
International Journal of Gynecology and Obstetrics journal homepage: www.elsevier.com/locate/ijgo
CLINICAL ARTICLE
Pregnancy outcome according to pre-pregnancy body mass index and gestational weight gain Joanna Gesche ⁎, Lisbeth Nilas Department of Obstetrics and Gynecology, Hvidovre Hospital, University of Copenhagen, Hvidovre, Denmark
a r t i c l e
i n f o
Article history: Received 17 November 2014 Accepted 2 March 2015 Keywords: Body mass index Fetal weight Gestational weight gain Obesity Pregnancy
a b s t r a c t Objective: To assess birth weight in relation to gestational weight gain (GWG) among women who were and were not obese before pregnancy. Methods: For a retrospective cohort study, data were obtained for women with a prepregnancy body mass index (BMI, calculated as weight in kilograms divided by the square of height in meters) of at least 30 who had a singleton delivery at a center in Denmark in 2010–2011. Data were also obtained for 455 non-obese women (BMI 20.0–24.9). GWG was expressed in absolute terms and relative to published recommendations (11–16 kg in non-obese women; 5–9 kg in obese women). Results: A total of 231 obese women were included in analyses. In non-obese and obese women, fetal weight was highest when GWG was above the recommended amount. Among women who had a GWG in line with the recommendations, mean birth weight was higher among those with a pre-pregnancy BMI of 35.0–39.9 (3758 ± 410 g) or at least 40 (3671 ± 374 g) than among non-obese women (3394 ± 453 g; P = 0.0058). Conclusion: Birth weight is related to both maternal BMI and GWG. In obese women, adherence to GWG recommendations does not seem to prevent increased birth weights. © 2015 International Federation of Gynecology and Obstetrics. Published by Elsevier Ireland Ltd. All rights reserved.
1. Introduction Overweight and obesity are related to many health problems that challenge healthcare systems worldwide. The prevalence of obesity has been steadily increasing worldwide [1], including among pregnant women. The proportion of pregnant women who are obese is now 12.2% in Denmark [2], and is even higher in other countries [3]. Obesity is associated with an increased risk of metabolic pregnancy complications, hypertensive disorders [4], gestational diabetes [5], delivery problems [6,7], and adverse pregnancy outcomes (e.g. macrosomia [8]). The risk of pregnancy complications and adverse fetal outcome in obese pregnant women can be modified by limiting gestational weight gain (GWG) [9–12]. Indeed, women who were not obese before pregnancy but gain excessive weight during pregnancy and are obese at term have an increased risk of pregnancy complications and adverse pregnancy outcome compared with women with a lower weight gain [13]. The US Institute of Medicine (IOM) recommendations on GWG differentiate according to pre-pregnancy body mass index (BMI; calculated as weight in kilograms divided by the square of height in meters) and advise limiting GWG to 11–16 kg for women with a pre-pregnancy BMI of 18.5–24.9 and 5–9 kg for women with a BMI of at least 30 [14,15]. It has
⁎ Corresponding author at: Department of Obstetrics and Gynecology, Hvidovre Hospital, Kettegårds Allé 30, 2650 Hvidovre, Denmark. Tel.: +45 41 14 59 62; fax: +45 38 62 27 04. E-mail address: [email protected] (J. Gesche).
been suggested that a GWG of less than the IOM recommendations in obese and morbidly obese women can improve pregnancy outcomes further, but the results are inconsistent, and possible risks associated with lower GWG or even weight loss have not been identified [16,17]. The aim of the present study was to assess birth weight in relation to compliance with the IOM GWG recommendations in nonobese and obese pregnant women. Additionally, the occurrence of macrosomia, pregnancy complications, and adverse pregnancy outcomes was compared. 2. Materials and methods For a retrospective study, all women with a pre-pregnancy BMI of at least 30 who had a singleton delivery at the Department of Obstetrics, Hvidovre Hospital, Hvidovre, Denmark, between January 1, 2010, and December 31, 2011, were considered for inclusion. Additionally, women with a pre-pregnancy BMI of 20.0–24.9 who had a singleton delivery at the study center were selected for inclusion in a control group. On the basis of power calculations, it was determined that 455 women would need to be included in the control group. All births on the 15th and 30th of each month in the study period were identified and included in this group. The study was approved by the Danish Data Protection Agency (Jr.nr. 2012-41-0400). Informed consent from all study participants had been obtained. Self-reported pre-pregnancy weight registered in the obstetric database was used to calculate pre-pregnancy BMI. Women with a pre-pregnancy BMI of at least 30 were stratified into obesity class I
http://dx.doi.org/10.1016/j.ijgo.2014.12.013 0020-7292/© 2015 International Federation of Gynecology and Obstetrics. Published by Elsevier Ireland Ltd. All rights reserved.
Please cite this article as: Gesche J, Nilas L, Pregnancy outcome according to pre-pregnancy body mass index and gestational weight gain, Int J Gynecol Obstet (2015), http://dx.doi.org/10.1016/j.ijgo.2014.12.013
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(pre-pregnancy BMI 30.0–34.9), obesity class II (35.0–39.9), and obesity class III (≥40.0). Participant characteristics, pregnancy and delivery data, and neonatal outcome were obtained from a local obstetric database. Characteristics assessed were age, parity, place of birth (Denmark vs elsewhere), and smoking status at first hospital visit (yes vs no). Pregnancy induced hypertension (PIH) was defined as a diastolic blood pressure over 90 mm Hg or a systolic blood pressure over 140 mm Hg after 20 weeks of pregnancy in women who had had a normal blood pressure at the onset of pregnancy. PIH and proteinuria (measured by positive dip-stick; at least two positive results needed) was defined as pre-eclampsia. Severe pre-eclampsia included general symptoms of PE and/or a diastolic blood pressure over 110 mm Hg or a systolic blood pressure over 160 mm Hg. Delivery complications assessed were shoulder dystocia, instrumental vaginal delivery, induction of labor, and the occurrence of cesarean. Outcome data analyzed were the newborn’s length and weight, gestational age (determined at a nuchal scan at 11–14 weeks of pregnancy), umbilical artery pH, placental weight, and admission to the neonatal intensive care unit within 24 hours of delivery. Fetal weight was also expressed as Z-scores, which are defined as percentage of expected birth weight adjusted for sex and gestational age on standardized growth charts expressed as standard deviations of the mean [18]. A small-for-gestational-age newborn had a Z-score of less than –2, or below –22% of the mean; a large-for-gestational-age newborn had a Z-score greater than + 2, or over 22% of the expected mean [18]. Low birth weight was defined as a birth weight under 2500 g and macrosomia as a birth weight over 4000 g. Uncomplicated vaginal delivery was defined as vaginal delivery without labor induction or instrumentation during delivery. The mother’s weight at term (at 35 full weeks or later) was recorded. GWG was defined as weight at term minus self-reported weight at the beginning of pregnancy. GWG was used as a continuous variable and stratified according to the current recommendations by the IOM: less than 5 kg, 5–9 kg, and more than 9 kg for obese women; and less than 11 kg, 11–16 kg, and more than 16 kg for normal weight women [14]. The groups were compared using Wilcoxon rank-sum and KruskalWallis tests for continuous variables, and χ2 and Fisher exact tests for categorical variables. A 0.05 significance level and 80% power were used. Analyses were performed using R version 2.15.0 (http://www.rproject.org/).
Table 2 Pregnancy complications and outcomes.a Complication/outcome
Non-obese women (n = 455)b
Obese women (n = 231)c
P value
Pregnancy-induced hypertension Pre-eclampsia Urinary infection Birth weight, g Macrosomia Small-for-gestational-age neonate Large-for-gestational-age neonate Admission to neonatal intensive care unit Gestational age, d Placental weight, g Instrumental delivery Induced delivery Labor augmentation Epidural Uncomplicated vaginal delivery Cesarean delivery Emergency Elective Perineal tear Episiotomy
7 (1.5) 21 (4.6) 75 (16.5) 3482 ± 509 62 (13.6) 16 (3.5) 8 (1.8) 9 (2.0)
11 (4.4) 31 (13.4) ¨50 (21.6) 3518 ± 578 41 (17.7) 6 (2.6) 15 (6.5) 19 (8.2)
0.031 b0.001 NS b0.001 NS NS 0.039 b0.001
279.9 ± 10.8 652.8 ± 144.9 55 (12.1) 110 (24.2) 195 (42.9) 102 (22.4) 236 (52.5) 89 (19.6) 53 36 260 (57.1) 17 (3.7)
276.3 ± 14.6 678.5 ± 154.7 20 (8.7) 79 (34.2) 107 (46.3) 77 (33.3) 82 (35.5) 75 (32.5) 34 41 115 (49.8) 2 (0.8)
0.0016 0.038 NS 0.007 NS 0.0028 b0.001 b0.001
b0.001 0.026
Abbreviations: NS, nonsignificant; BMI, body mass index (calculated as the weight in kilograms divided by the square of height in meters). a Values are given as number (percentage) or mean ± SD, unless indicated otherwise. b BMI 20.0–24.9. c BMI ≥30.0.
Mean birth weight and the frequencies of admission to the neonatal intensive care unit, large-for-gestational-age neonates, PIH, and preeclampsia were all significantly higher among obese women than among non-obese women (Table 2). The frequency of uncomplicated vaginal delivery was lower among obese women than among nonobese women (P b 0.001), and the frequencies of induced delivery (P = 0.007), epidural (P = 0.0028), and cesarean (P b 0.001) were higher in the obese women. The frequencies of perineal tears and episiotomy were significantly lower in the obese women (Table 2). In the total population, there was a decreasing trend in vaginal delivery with increasing BMI (P = 0.0012).
3. Results Of 750 women with a pre-pregnancy BMI of at least 30, 485 had been approached for a randomized controlled trial of a dietary intervention, and 43 had missing data. Therefore, 231 obese women and 455 non-obese women with a pre-pregnancy BMI of 20–24.9 were included in analyses. Data on GWG were available for 174 obese women and 236 non-obese women. The obese women were significantly younger than were the non-obese women, fewer were nulliparous, and more were smokers (Table 1).
Table 1 Participant characteristics.a Characteristics
Non-obese women (n = 455)b
Obese women (n = 231)c
P value
Age, y Nulliparous Smoker
31.28 ± 4.55 233 (51.2) 26 (5.7)
30.07 ± 4.93 97 (42.0) 45 (19.5)
0.0018 0.027 b0.001
Abbreviation: BMI, body mass index (calculated as weight in kilograms divided by the square of height in meters). a Values are given as mean ± SD or number (percentage), unless indicated otherwise. b BMI 20.0–24.9. c BMI ≥30.0.
Fig. 1. GWG, by pre-pregnancy BMI. Abbreviations: GWG, gestational weight gain; BMI, body mass index (calculated as weight in kilograms divided by the square of height in meters). Boxes show medians and interquartile ranges. Error bars show ranges. Circles show outliers.
Please cite this article as: Gesche J, Nilas L, Pregnancy outcome according to pre-pregnancy body mass index and gestational weight gain, Int J Gynecol Obstet (2015), http://dx.doi.org/10.1016/j.ijgo.2014.12.013
J. Gesche, L. Nilas / International Journal of Gynecology and Obstetrics xxx (2015) xxx–xxx
3
There were no differences in characteristics, pregnancy and delivery complications, and pregnancy outcome between the different obesity classes (data not shown). Obese women had a significantly lower mean GWG than did the non-obese women (10.5 kg vs 15.0 kg; P b 0.001). GWG decreased with increasing BMI (P = 0.030) (Fig. 1). The risk of macrosomia increased significantly (P = 0.002) with increasing GWG in the total population. The proportion of macrosomic newborns was highest among women whose GWG was above the recommended value in most groups (Table 3). Overall, 49 (28.2%) obese women and 106 (44.9%) non-obese women fulfilled the IOM GWG recommendations (P = 0.013). GWG was in line with the recommendations for 33 (28.4%) of 116 women in obesity class I, 9 (24.3%) of 37 women in obesity class II, and 7 (33.3%) of 21 women in obesity class III. Birth weight did not differ between non-obese women and women in obesity class I who had met the GWG recommendations, but it was significantly higher among women in obesity classes II and III (P = 0.0058) (Table 3, Fig. 2). Stratifying the women according to GWG in relation to the IOM recommendations showed that birth weight was related to both maternal BMI and GWG in non-obese and obese women (Table 3). 4. Discussion In the present study, the relationship between pre-pregnancy BMI, GWG, and the occurrence of adverse pregnancy outcomes has been examined. Both birth weight and likelihood of macrosomia were related to increasing maternal GWG. Although mean GWG was lower among obese women than among non-obese women, it was still higher than the IOM recommendation of 5–9 kg. Even when women in obesity classes II and III did adhere to GWG recommendations, the birth weight was significantly higher than among non-obese women and those in obesity class I who also had a GWG in line with advised values. Several intervention trials have been performed to minimize GWG in obese women, because obesity and excessive GWG have been associated with negative pregnancy outcomes [19,20]. Currently, there is only one GWG recommendation for obese women; little is known about the appropriate GWG for women in obesity classes II and III and the consequences of inadequate GWG [21]. In the present study, women in obesity classes II and III gave birth to heavier neonates than did non-obese women, even when following the IOM GWG recommendations. Therefore, separate GWG recommendations according to obesity class are needed. The present results indicate that women in obesity classes II and III should probably gain less than is currently recommended by the IOM. Even though obese women have a significantly lower GWG than do non-obese women, only approximately one-third of obese women in the present study met the GWG recommendations, compared with
Fig. 2. Birth weight among women whose GWG was in line with recommendations (11–16 kg for non-obese women; 5–9 kg for obese women), by pre-pregnancy BMI. Abbreviations: GWG, gestational weight gain; BMI, body mass index (calculated as the weight in kilograms divided by the square of height in meters). Boxes show medians and interquartile ranges. Error bars show ranges. Circles show outliers. Birth weight was significantly higher among women in obesity classes II and III than among non-obese women (P = 0.0058).
44.9% of non-obese women. It has previously been shown that excessive GWG could be associated with childhood obesity [12], and GWG might have long-term effects on the offspring. Healthcare professionals have the opportunity to help pregnant women to adopt a healthier lifestyle, and behavioral intervention has proven effective in lowering GWG [19], which could modify some of the negative effects of pre-pregnancy obesity. The present study also showed an increasing prevalence of macrosomia with increasing GWG, independent of pre-pregnancy BMI. It has previously been shown that the body fat of the neonate increases for each additional kilogram of GWG [22]. Delivering a macrosomic fetus entails complications [23], and lowering GWG could minimize the risk of macrosomia, both for obese and non-obese women. However, reducing the GWG recommendations for obese women, especially those in obesity classes II and III, could increase the risk that a newborn is small for its gestational age. Nevertheless, little is known about the implications of too low a weight gain during pregnancy or even weight loss [21]. One limitation of the present study was that the GWG entries in the database relied on self-reported data from the patients’ files. It has
Table 3 Fetal weight and occurrence of macrosomia, by GWG.a Non-obese women (n = 236)b
Fetal weight when GWG less than recommended, g Macrosomic newborns Fetal weight when GWG as recommended, g Macrosomic newborns Fetal weight when GWG above recommended, g Macrosomic newborns
3292 ± 630 4/45 (8.9) 3394 ± 453 9/106 (8.5) 3708 ± 517g 23/85 (27.1)
Obese women (n = 174) Class Ic (n = 116)
Class IId(n = 37)
Class IIIe(n = 21)
3209 ± 877 0/14 3539 ± 499 6/33 (18.2) 3548 ± 530 12/69 (17.4)
3342 ± 488 1/10 (10.0) 3758 ± 410f 2/9 (22.2) 3685 ± 297 5/18 (27.8)
3646 ± 351 1/8 (12.5) 3671 ± 374f 2/7 (28.6) 3861 ± 333 2/6 (33.3)
Abbreviations: GWG, gestational weight gain; BMI, body mass index (calculated as weight in kilograms divided by the square of height in meters). a Values are given as mean ± SD or number/total number (percentage). b BMI 20.0–24.9. c BMI 30.0–34.9. d BMI 35.0–39.9. e BMI ≥40. f P = 0.0058. g P b 0.001.
Please cite this article as: Gesche J, Nilas L, Pregnancy outcome according to pre-pregnancy body mass index and gestational weight gain, Int J Gynecol Obstet (2015), http://dx.doi.org/10.1016/j.ijgo.2014.12.013
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J. Gesche, L. Nilas / International Journal of Gynecology and Obstetrics xxx (2015) xxx–xxx
previously been shown that self-reported pre-pregnancy weight can be underestimated, which leads to an overestimation of GWG [24]. GWG was calculated the same way in all groups in the present study, but no data are available showing whether obese women preferentially overestimated or underestimated their pre-pregnancy weight. Another limitation was that weight at the end of pregnancy was the last entry, but it could have been measured at any point between 35 weeks to delivery. Weekly weight measurements are officially recommended from 38 weeks of pregnancy on, but both healthcare professionals and patients are reluctant to practice this, probably to avoid embarrassment. A strength of the present study is that it included an unselected cohort of a group of women from all obesity classes who received no dietary counseling or intervention, as well as a large group of randomly chosen non-obese women, thereby minimizing the risk of selection bias. Previous findings of an association between obesity and an elevated risk of large-for-gestational-age newborns, PIH, pre-eclampsia, and cesarean delivery [5,25–27], indicating that the population assessed resembles others. In summary, our study shows that obese women, although gaining significantly less weight than non-obese women, have a GWG above the value recommended by the IOM and that such excessive GWG increases the risk of macrosomia. Women in obesity class II and III with a GWG in line with the recommendations gave birth to heavier children than did non-obese weight women, indicating that GWG recommendations should be stratified according to obesity class. Further studies are needed to evaluate the IOM GWG recommendations and their implications for obesity classes II and III. Conflict of interest The authors have no conflicts of interest. References [1] Heitmann BL. Ten-year trends in overweight and obesity among Danish men and women aged 30–60 years. Int J Obes Relat Metab Disord 2000;24(10):1347–52. [2] Danish Health and Medicines Authority. Births, pregnancy and BMI 2004–1st half of 2008. Copenhagen: Danish Health and Medicines Authority; 2008. [3] Reynolds RM, Allan KM, Raja EA, Bhattacharya S, McNeill G, Hannaford PC, et al. Maternal obesity during pregancy and premature mortality from cardiovascular event in adult offsprint: follow-up of 1 323 275 years. BMJ 2013;347:f4539. [4] Schneider S, Freerksen N, Maul H, Roehrig S, Fischer B, Hoeft B. Risk groups and maternal-neonatal complications of preeclampsia—current results from the national German Perinatal Quality Registry. J Perinat Med 2011;39(3):257–65. [5] 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(8):1175–82.
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Please cite this article as: Gesche J, Nilas L, Pregnancy outcome according to pre-pregnancy body mass index and gestational weight gain, Int J Gynecol Obstet (2015), http://dx.doi.org/10.1016/j.ijgo.2014.12.013
