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Impact of bariatric surgery on fetal growth restriction: experience of a perinatal and bariatric surgery center

Published:November 25, 2015DOI:https://doi.org/10.1016/j.ajog.2015.11.017

      Background

      Bariatric surgery is known to improve some pregnancy outcomes, but there is concern that it may increase the risk of small for gestational age.

      Objective

      To assess the impact of bariatric surgery on pregnancy outcomes and specifically of the type of bariatric surgery on the risk of fetal growth restriction.

      Study Design

      A single-center retrospective case-control study. The study group comprised all deliveries in women who had undergone bariatric surgery. To investigate the effects of weight loss on pregnancy outcomes, we compared the study group with a control group matched for presurgery body mass index. Secondly, to assess the specific impact of the type of surgery on the incidence of fetal growth restriction in utero, we distinguished subgroups with restrictive and malabsorptive bariatric surgery, and compared outcomes for each of these subgroups with a second control group, matched for prepregnancy body mass index.

      Results

      Among 139 patients operated, 58 had a malabsorptive procedure (gastric bypass) and 81 a purely restrictive procedure (72 a gastric banding and 9 a sleeve gastrectomy). Compared with controls matched for presurgery body mass index, the study group had a decreased rate of gestational diabetes (12% vs 23%, P = .02) and large for gestational age >90th percentile (11% vs 22%, P = .01) but an increased rate of small for gestational age <10th percentile. The incidence of small for gestational age was higher after gastric bypass (29%) than it was after restrictive surgery (9%) or in controls matched for prepregnancy body mass index (6%) (P < .01 between bypass and controls). In multivariable analysis, after adjustment for other risk factors, gastric bypass remained strongly associated with small for gestational age (adjusted odds ratio, 7.16; 95% confidence interval, 2.74–18.72).

      Conclusion

      Malabsorptive bariatric surgery was associated with an increased risk of fetal growth restriction.

      Key words

      Obesity is a major healthcare problem, and its prevalence is increasing worldwide. In France, according to the 2012 ObEpi survey,

      ObÉpi, Enquête épidémiologique nationale sur le surpoids et l’obésité. Enquête INSERM/TNS HEALTHCARE/ROCHE 2012. Available at: http://www.roche.fr/content/dam/corporate/roche_fr/doc/obepi_2012.pdf. Accessed Aug. 15, 2015.

      10% of reproductive-age women are obese. During pregnancy, obesity is a cause of maternal, obstetric, and neonatal complications and has long-term consequences on the child. The incidences of gestational diabetes and hypertension/preeclampsia increase, especially for high body mass index (BMI).
      • Ovesen P.G.
      • Jensen D.M.
      • Damm P.
      • Rasmussen S.
      • Kesmodel U.S.
      Maternal and neonatal outcomes in pregnancies complicated by gestational diabetes. A nation-wide study.
      The risks of cesarean section, postpartum hemorrhage, fetal macrosomia, and shoulder dystocia are increased.
      • Weiss J.L.
      • Malone F.D.
      • Emig D.
      • et al.
      Obesity, obstetric complications and cesarean delivery rate–a population-based screening study.
      The rate of fetal malformations, primarily spina bifida, increases, as well as neonatal morbidity and mortality.
      • Blomberg M.I.
      • Källén B.
      Maternal obesity and morbid obesity: the risk for birth defects in the offspring.
      In the longer term, the rates of childhood obesity and metabolic syndrome are higher among children born to obese mothers.
      • Boney C.M.
      • Verma A.
      • Tucker R.
      • Vohr B.R.
      Metabolic syndrome in childhood: association with birth weight, maternal obesity, and gestational diabetes mellitus.
      Bariatric surgery is currently the reference treatment for severe obesity, allowing for major weight loss and improvements in a number of health outcomes.
      • Sjöström L.
      • Peltonen M.
      • Jacobson P.
      • et al.
      Bariatric surgery and long-term cardiovascular events.
      • Maggard M.A.
      • Shugarman L.R.
      • Suttorp M.
      • et al.
      Meta-analysis: surgical treatment of obesity.
      A number of observational studies have reported reductions in the incidence of gestational diabetes and macrosomia in pregnancies after bariatric surgery.
      • Galazis N.
      • Docheva N.
      • Simillis C.
      • Nicolaides K.H.
      Maternal and neonatal outcomes in women undergoing bariatric surgery: a systematic review and meta-analysis.
      • Johansson K.
      • Stephansson O.
      • Neovius M.
      Outcomes of pregnancy after bariatric surgery.
      • Lesko J.
      • Peaceman A.
      Pregnancy outcomes in women after bariatric surgery compared with obese and morbidly obese controls.
      • Yi X.Y.
      • Li Q.F.
      • Zhang J.
      • Wang Z.H.
      A meta-analysis of maternal and fetal outcomes of pregnancy after bariatric surgery.
      However, bariatric surgery can lead to complications, in particular intestinal occlusions through various mechanisms, which can have severe consequences during pregnancy.
      • Chevrot A.
      • Lesage N.
      • Msika S.
      • Mandelbrot L.
      Digestive surgical complications during pregnancy following bariatric surgery: experience of a center for perinatology and obesity [in French].
      • Wax J.R.
      • Pinette M.G.
      • Cartin A.
      Roux-en-Y gastric bypass-associated bowel obstruction complicating pregnancy-an obstetrician's map to the clinical minefield.
      Moreover, the fact that bariatric surgery could favor fetal growth restriction is a major concern. A small increase in the rate of small for gestational age (SGA) was found in several studies,
      • Johansson K.
      • Stephansson O.
      • Neovius M.
      Outcomes of pregnancy after bariatric surgery.
      • Lesko J.
      • Peaceman A.
      Pregnancy outcomes in women after bariatric surgery compared with obese and morbidly obese controls.
      • Kjær M.M.
      • Lauenborg J.
      • Breum B.M.
      • Nilas L.
      The risk of adverse pregnancy outcome after bariatric surgery: a nationwide register-based matched cohort study.
      • Roos N.
      • Neovius M.
      • Cnattingius S.
      • Trolle Lagerros Y.
      • Sääf M.
      • Granath F.
      • Stephansson O.
      Perinatal outcomes after bariatric surgery: nationwide population based matched cohort study.
      although there are conflicting data.
      • Fumery L.
      • Pigeyre M.
      • Fournier C.
      • et al.
      Impact of bariatric surgery on obstetric prognosis.
      In a preliminary study of 24 pregnancies,
      • Santulli P.
      • Mandelbrot L.
      • Facchiano E.
      • et al.
      Obstetrical and neonatal outcomes of pregnancies following gastric bypass surgery: a retrospective cohort study in a French referral centre.
      we found a nonsignificant increased risk of SGA in case of gastric bypass compared to a nonoperated control population and a significant decrease in birthweight after gastric bypass, compared to obese women matched for prepregnancy BMI and normal-weight women. Recently, a large population-based Swedish study
      • Johansson K.
      • Stephansson O.
      • Neovius M.
      Outcomes of pregnancy after bariatric surgery.
      confirmed a very significant increase in the incidence of SGA after bariatric surgery compared with matched controls on presurgical BMI. However, neonatal outcomes were not analyzed according to the type of weight loss surgery that was performed.
      Indeed, there are 2 main types of bariatric surgery, purely restrictive procedures (gastric banding, sleeve gastrectomy) and malabsorptive or mixed procedures (gastric bypass, biliopancreatic diversion). The choice of type of procedure depends on several factors, particularly the patient’s BMI and comorbidities. Mixed techniques have been preferred for many years because of their greater effectiveness on weight loss compared to gastric banding, but they have the disadvantage that they lead to nutritional deficiencies, which could have an impact on fetal development. Thus, one can hypothesize that the increased risk of SGA is specifically related to malabsorption. In a previous study comparing pregnancies after gastric bypass and banding,
      • Facchiano E.
      • Iannelli A.
      • Santulli P.
      • Mandelbrot L.
      • Msika S.
      Pregnancy after laparoscopic bariatric surgery: comparative study of adjustable gastric banding and Roux-en-Y gastric bypass.
      we did not observe any difference in birthweight. Other studies comparing outcomes following gastric banding and gastric bypass also failed to reveal any difference in the incidence of SGA,
      • Kjær M.M.
      • Lauenborg J.
      • Breum B.M.
      • Nilas L.
      The risk of adverse pregnancy outcome after bariatric surgery: a nationwide register-based matched cohort study.
      • Fumery L.
      • Pigeyre M.
      • Fournier C.
      • et al.
      Impact of bariatric surgery on obstetric prognosis.
      • Facchiano E.
      • Iannelli A.
      • Santulli P.
      • Mandelbrot L.
      • Msika S.
      Pregnancy after laparoscopic bariatric surgery: comparative study of adjustable gastric banding and Roux-en-Y gastric bypass.
      • Ducarme G.
      • Parisio L.
      • Santulli P.
      • Carbillon L.
      • Mandelbrot L.
      • Luton D.
      Neonatal outcomes in pregnancies after bariatric surgery: a retrospective multi-centric cohort study in three French referral centers.
      including a large population-based study.
      • Roos N.
      • Neovius M.
      • Cnattingius S.
      • Trolle Lagerros Y.
      • Sääf M.
      • Granath F.
      • Stephansson O.
      Perinatal outcomes after bariatric surgery: nationwide population based matched cohort study.
      There is as yet no consensus on the type of intervention to favor in a woman with a perspective of pregnancy.
      The objectives of our study were to assess the impact of bariatric surgery on pregnancy outcomes and, specifically, to assess the impact of the type of bariatric surgery on the risk of fetal growth restriction.

      Materials and Methods

      This is a single-center retrospective case-control study. It was performed at Louis Mourier Hospital, in Colombes, France, a university center that includes both a level 3 maternity and a reference center for the treatment of obesity. We included all deliveries in women who had a history of bariatric surgery, whether they had been operated in the same center or elsewhere, between Jan 1, 2004 and Dec 31, 2013. Thirty-six patients were included in previous publications.
      • Santulli P.
      • Mandelbrot L.
      • Facchiano E.
      • et al.
      Obstetrical and neonatal outcomes of pregnancies following gastric bypass surgery: a retrospective cohort study in a French referral centre.
      • Facchiano E.
      • Iannelli A.
      • Santulli P.
      • Mandelbrot L.
      • Msika S.
      Pregnancy after laparoscopic bariatric surgery: comparative study of adjustable gastric banding and Roux-en-Y gastric bypass.
      • Ducarme G.
      • Parisio L.
      • Santulli P.
      • Carbillon L.
      • Mandelbrot L.
      • Luton D.
      Neonatal outcomes in pregnancies after bariatric surgery: a retrospective multi-centric cohort study in three French referral centers.
      In order to avoid recruitment bias, we excluded multiple pregnancies, in utero fetal demises, and miscarriages. This treatment group was called group A.
      To investigate the effects of weight loss on pregnancy outcomes, we compared patients in group A with control patients (group B), obese patients who never underwent bariatric surgery matched for BMI (weight [kg]/height [m]2) before bariatric surgery and who delivered in the institution over the same period.
      Secondly, to assess the specific impact of the type of surgery on the incidence of fetal growth restriction, we distinguished restrictive and malabsorptive bariatric surgery, and compared the characteristics and outcomes for each of these subgroups with a control group (group C) matched for prepregnancy BMI who gave birth in the institution over the same period. Prepregnancy BMI was calculated using weight measured at the first prenatal visit before 12 weeks. Matching on prepregnancy BMI was performed in order to test the hypothesis that bariatric surgery could have an impact on fetal growth independently of the actual weight loss obtained following the procedure.
      Controls were chosen randomly on the same period of birth (by year) and matched individually on BMI (<25, 25–30, 30–35, 35–40, 41–45, and >45). The other matching factors were, when possible, maternal age (<20, 20–35, and >35), ethnic origin, and parity (nulliparous or parous).
      SGA was defined as below the 10th percentile and large for gestational age (LGA) as >90th percentile, using birthweight z-scores calculated with the formulas published by Capmas et al
      • Capmas P.
      • Salomon L.J.
      • Picone O.
      • Fuchs F.
      • Frydman R.
      • Senat M.V.
      Using Z-scores to compare biometry data obtained during prenatal ultrasound screening by midwives and physicians.
      on a similar population in France, adjusting for gestational age and the infant’s sex.
      The study was approved by the Ethics Committee for Biomedical Research Paris-Nord (Institutional Review Board - IRB 00,006,477) (Study No. 13-044, No. 09-050, November 9, 2009).
      The data were collected prospectively in the department’s computerized database (DiammG; Micro6, Vandoeuvre-les-Nancy, France), which is approved by the French Computer Watchdog Commission (CNIL). The database is constituted by patient records, which are used for routine patient follow-up, and all of the variables required for the study were recorded prospectively at prenatal visits as part of routine care for all cases and controls. Continuous variables were analyzed by analysis of variance, and categorical variables were compared with chi-square or Fisher exact test. The independent effect of bariatric surgery on SGA or LGA was tested and quantified with a multivariable logistic regression. We adjusted for covariables previously described as risk factors of LGA and SGA and for variables found to be potential confounders in bivariate analyses. Stata 13.0 software (StataCorp, College Station, TX) was used for the statistical analysis.

      Results

      Between January 2004 and December 2013, 139 patients who underwent bariatric surgery were included in the study. Among them, 58 had a malabsorptive surgery (gastric bypass) and 81 a restrictive one (72 a gastric banding and 9 a sleeve gastrectomy). The mean interval between surgery and delivery was 38 months.

      Pregnancy outcomes after bariatric surgery

      We compared patients who underwent bariatric surgery (study group A) with the nonoperated obese patients matched for presurgical BMI (control group B). In the study group, the mean BMI before surgery was 45 (kg/m2), compared with the prepregnancy BMI of 34.1, which was a mean decrease of 11 ± 6.8 and a relative decrease of 24.4%. The absolute mean decrease in weight was 31 kg.
      The study group had a greater gestational weight gain, but a lower rate of gestational diabetes, than the nonoperated controls (Table 1).
      Table 1Maternal characteristics and obstetric and neonatal outcomes, comparing the study group who had bariatric surgery (group A) and obese controls (group B) matched for presurgery BMI, age, ethnic origin, and parity
      Bariatric surgery group A

      n = 139 (%)
      Obese controls group B

      n = 139 (%)
      P
      Maternal age (years), mean ± SD31.7 ± 4.932.4 ± 5.0.87
      Smoking19 (14)23 (17).52
      Nulliparous39 (28)44 (32).51
      Geographic origin:
       Europe59 (42)53 (38).81
       North Africa49 (35)50 (36)
       Sub-Saharan Africa18 (13)23 (17)
       Other12 (10)13 (9)
      Gestational hypertension/preeclampsia11 (7.9)16 (12).31
      Gestational diabetes mellitus17 (12)32 (23).02
      Prepregnancy BMI, mean ± SD (kg/m2)34.1 ± 6.041.5 ± 1.7<.001
      Weight gain during pregnancy (kg), mean ± SD8.0 ± 8.55.8 ± 8.4.05
      Type of labor:.42
       Spontaneous71 (65)64 (60)
       Induced38 (35)43 (40)
      Mode of delivery:.59
       Vaginal92 (66)87 (63)
       Cesarean section during labor17 (12)23 (17)
       Cesarean section before labor30 (22)29 (21)
      Postpartum hemorrhage10 (7.2)11 (7.9).82
      Preterm delivery <37 weeks GA12 (8.6)10 (7.2).66
      Birthweight, g (mean ± SD)3317 ± 5203528 ± 514.001
      Small for gestational age (<10th percentile)24 (17)12 (9).03
      Large for gestational age (>90th percentile)15 (11)30 (22).01
      Apgar at 5 minutes <703 (2.2).08
      Transfer to neonatal intensive care12 (8.6)6 (4.3).14
      Results presented as n (%) unless indicated otherwise. Totals do not always equal the total N for the group in case of missing data.
      BMI, body mass index; GA, gestational age.
      Chevrot et al. Impact of bariatric surgery on fetal growth restriction. Am J Obstet Gynecol 2016.
      There was no significant difference between the 2 groups for any of the obstetric and neonatal characteristics studied (Table 1) except for birthweight, which was significantly lower in the study group than in controls (3317 ± 520 g vs 3528 ± 514 g; P = .001), with both a lower proportion of LGA and a higher proportion of SGA.

      Analysis of pregnancy outcomes according to type of bariatric surgery

      We compared the women in group C (matched on prepregnancy BMI) with women in group A, divided into 2 subgroups depending on the type of surgery (restrictive or malabsorptive).
      • Weiss J.L.
      • Malone F.D.
      • Emig D.
      • et al.
      Obesity, obstetric complications and cesarean delivery rate–a population-based screening study.
      Maternal characteristics did not differ significantly between the 3 groups, indicating that the controls were correctly matched with the cases. However, women who had a malabsorptive procedure had a higher BMI before surgery than women who had a purely restrictive procedure (47.9 ± 5.6 kg/m2 vs 43.4 ± 4.3 kg/m2, respectively; P < .001).
      Pregnancy outcomes did not differ significantly between the 3 groups regarding maternal weight gain during pregnancy, complications of pregnancy including gestational diabetes and pregnancy-induced hypertension, cesarean rate, and preterm delivery (Table 2). In contrast, the mean term birthweight was lower in the group that had a gastric bypass compared to the group who had a purely restrictive surgery and nonoperated controls matched for prepregnancy BMI (3093 g vs 3473 g and 3493 g, respectively, P < .01). This difference was accounted for by a decreased incidence of LGA and an incidence of SGA 3 times higher in the bypass group than in the restrictive group and controls (Table 2).
      Table 2Maternal characteristics according to the type of bariatric surgery, compared to unexposed controls matched for prepregnancy BMI, age, ethnic origin, and parity (group C)
      Malabsorptive

      Surgery (MS)

      n = 58
      Restrictive

      Surgery (RS)

      n = 81
      Controls (group C)

      n = 139
      P

      MS vs C
      P

      RS vs C
      Age (years)32.0 ± 4.931.5 ± 4.831.9 ± 4.7.91.53
      BMI prepregnancy (kg/m2), mean ± SD33.1 ± 6.234.9 ± 5.833.8 ± 5.9.46.20
      Geographic origin, n (%).26.83
       Europe26 (45)33 (41)54 (39)
       North Africa21 (36)28 (35)52 (37)
       Sub-Saharan Africa5 (9)13 (16)25 (18)
       Other6 (10)7 (9)8 (6)
      Nulliparous18 (31)21 (26)34 (24).34.81
      Smoking4 (7)15 (19)17 (12).28.20
      Gestational hypertension/preeclampsia8 (5.8)6 (7.4)5 (8.6).46.63
      Weight gain during pregnancy (kg), mean ± SD6.8 ± 6.78.0 ± 9.58.4 ± 6.8.14.72
      Gestational diabetes mellitus4 (7)13 (16)15 (10).40.26
      Mode of delivery.22.86
       Vaginal37 (64)55 (68)96 (69)
       Cesarean before labor6 (10)11 (14)21 (15)
       Cesarean in labor15 (26)15 (19)22 (16)
      Preterm delivery <37 weeks GA6 (10)6 (7)13 (9).83.62
      Birthweight, g
      For deliveries >37 weeks GA (n = 253).
      mean ± SD
      3093 ± 4523473 ± 5093493 ± 479<.001.79
      SGA (<10th percentile)17 (29)7 (9)8 (6)<.001.41
      LGA (>90th percentile)3 (5)12 (15)24 (17).02.63
      Transfer to neonatal intensive care6 (10)6 (7)9 (6).35.79
      All results presented as n (%) unless indicated otherwise.
      BMI, body mass index; GA, gestational age; LGA, large for gestational age; SGA, small for gestational age.
      Chevrot et al. Impact of bariatric surgery on fetal growth restriction. Am J Obstet Gynecol 2016.
      a For deliveries >37 weeks GA (n = 253).
      In the multivariable analysis (Table 3), after adjustment for risk factors potentially related to SGA, gastric bypass remained strongly associated with SGA (odds ratio, 7.16; 95% confidence interval, 2.74–18.72). This difference was not changed when adding to this model prepregnancy BMI or weight gain during pregnancy.
      Table 3Multivariable analysis of risk factors for SGA (birthweight <10th percentile)
      No SGA

      n = 246 (%)
      SGA

      n = 32 (%)
      OR (95% CI)aOR (95% CI)
      All of the variables in the table were included in the logistic regression model
      Maternal age (years), mean ± SD
      Continuous variable, OR per year of age or 1 point of BMI, respectively.
      31.8 ± 4.732.2 ± 5.71.02 (0.94–1.10)1.6 (0.97–1.16)
      Geographic origin
       Europe100 (41)13 (41)11
       North Africa90 (36)11 (34)0.94 (0.40–2.20)1.01 (0.40–2.58)
       Sub-Saharan Africa38 (15)5 (16)1.01 (0.34–3.03)1.53 (0.46–5.03)
       Other18 (7)3 (9)1.28 (0.33–4.95)0.94 (0.21–4.21)
      Nulliparous59 (24)14 (44)2.46 (1.15–5.26)2.90 (1.16–7.30)
      Smoking during pregnancy33 (13)3 (8)0.92 (0.41–2.06)0.99 (0.25–3.90)
      BMI prepregnancy, mean ± SD
      Continuous variable, OR per year of age or 1 point of BMI, respectively.
      34.0 ± 5.833.6 ± 7.00.99 (0.93–1.05)0.99 (0.93–1.06)
      Gestational diabetes mellitus30 (12)2 (6)0.48 (0.11–2.11)0.66 (0.14–3.51)
      Gestational hypertension/preeclampsia14 (6)5 (16)3.07 (1.03–9.18)2.65 (0.76–9.17)
      Bariatric surgery
       None (nonobese controls)131 (53)8 (25)11
       Restrictive procedure74 (30)7 (22)1.55 (0.54–4.44)1.66 (0.56–4.88)
       Malabsorptive procedure41 (17)17 (53)6.79 (2.73–16.9)7.16 (2.74–18.72)
      Totals do not always equal the total N for the group in case of missing data.
      aOR, adjusted odds ratio; BMI, body mass index; CI, confidence interval; OR, odds ratio; SGA, small for gestational age.
      Chevrot et al. Impact of bariatric surgery on fetal growth restriction. Am J Obstet Gynecol 2016.
      a All of the variables in the table were included in the logistic regression model
      b Continuous variable, OR per year of age or 1 point of BMI, respectively.

      Discussion

      Principal findings

      The most important finding in our study was a 2-fold increase in SGA associated with bariatric surgery, with a clear association between the type of procedure and SGA. Gastric bypass was an independent risk factor for fetal growth restriction, which persisted when adjusting for other risk factors in a multivariable analysis.
      Bariatric surgery was also associated with a reduction in gestational diabetes and LGA, as reported in previous studies.
      • Johansson K.
      • Stephansson O.
      • Neovius M.
      Outcomes of pregnancy after bariatric surgery.
      • Lesko J.
      • Peaceman A.
      Pregnancy outcomes in women after bariatric surgery compared with obese and morbidly obese controls.
      • Kjær M.M.
      • Lauenborg J.
      • Breum B.M.
      • Nilas L.
      The risk of adverse pregnancy outcome after bariatric surgery: a nationwide register-based matched cohort study.
      • Roos N.
      • Neovius M.
      • Cnattingius S.
      • Trolle Lagerros Y.
      • Sääf M.
      • Granath F.
      • Stephansson O.
      Perinatal outcomes after bariatric surgery: nationwide population based matched cohort study.
      • Fumery L.
      • Pigeyre M.
      • Fournier C.
      • et al.
      Impact of bariatric surgery on obstetric prognosis.
      • Sheiner E.
      • Balaban E.
      • Dreiher J.
      • Levi I.
      • Levy A.
      Pregnancy outcome in patients following different types of bariatric surgeries.
      The rate of cesarean section did not differ from controls, but remained high in women who had bariatric surgery in comparison with the current cesarean rate of 21% in our institution (unpublished). The literature is discordant regarding the impact of bariatric surgery on reducing cesarean section rates.
      • Galazis N.
      • Docheva N.
      • Simillis C.
      • Nicolaides K.H.
      Maternal and neonatal outcomes in women undergoing bariatric surgery: a systematic review and meta-analysis.
      • Yi X.Y.
      • Li Q.F.
      • Zhang J.
      • Wang Z.H.
      A meta-analysis of maternal and fetal outcomes of pregnancy after bariatric surgery.
      • Maggard M.A.
      • Yermilov I.
      • Li Z.
      • et al.
      Pregnancy and fertility following bariatric surgery: a systematic review.
      We did not observe an increase in preterm delivery, contrary to Roos et al,
      • Roos N.
      • Neovius M.
      • Cnattingius S.
      • Trolle Lagerros Y.
      • Sääf M.
      • Granath F.
      • Stephansson O.
      Perinatal outcomes after bariatric surgery: nationwide population based matched cohort study.
      but similarly to 2 large studies comparing women who had bariatric surgery with obese controls.
      • Johansson K.
      • Stephansson O.
      • Neovius M.
      Outcomes of pregnancy after bariatric surgery.
      • Lesko J.
      • Peaceman A.
      Pregnancy outcomes in women after bariatric surgery compared with obese and morbidly obese controls.

      Meaning

      Our main hypothesis was that the risk of SGA is related to malabsorptive procedures. A French multicenter study found an increased risk of low birthweight after bypass vs banding.
      • Ducarme G.
      • Parisio L.
      • Santulli P.
      • Carbillon L.
      • Mandelbrot L.
      • Luton D.
      Neonatal outcomes in pregnancies after bariatric surgery: a retrospective multi-centric cohort study in three French referral centers.
      In the Swedish study by Johansson et al,
      • Johansson K.
      • Stephansson O.
      • Neovius M.
      Outcomes of pregnancy after bariatric surgery.
      the risk of SGA increased after bariatric surgery (gastric bypass in 98% of cases) compared with obese women matched on presurgical BMI, while Roos et al
      • Roos N.
      • Neovius M.
      • Cnattingius S.
      • Trolle Lagerros Y.
      • Sääf M.
      • Granath F.
      • Stephansson O.
      Perinatal outcomes after bariatric surgery: nationwide population based matched cohort study.
      found that the risk of SGA was highest in the subgroup with gastric bypass. The use of very obese controls could bias the results because growth restriction in this population could be masked owing to the metabolic impact of obesity itself and frequently associated diabetes. Only 1 study, from Lille, France,
      • Fumery L.
      • Pigeyre M.
      • Fournier C.
      • et al.
      Impact of bariatric surgery on obstetric prognosis.
      reported a decreased risk of SGA after bariatric surgery compared to obese controls, with no difference according to the type of surgery; however, gastric banding predominated. To better explore the risk of SGA associated with the surgery itself, we used an original approach comparing the group with gastric bypass surgery with a group with restrictive surgery and a control group matched for preconceptional BMI. The increase in SGA was highly significant in the group with bypass, even after adjustment for other risk factors. On the contrary, there was no increase in SGA in the group with purely restrictive surgery, consisting mainly of gastric banding.

      Clinical implications

      Our findings suggest that the increased incidence of SGA after bypass is due to fetal growth restriction (FGR). Since this FGR appears to be related to malabsorptive procedures, it would seem preferable for reproductive-age women to have purely restrictive procedures. Sleeve gastrectomy is increasingly popular for this indication, but there are as yet few reports on subsequent pregnancies; it is thus of importance to study pregnancy outcomes following this procedure. Because pregnancies after bariatric surgery are at risk of both surgical and nutritional complications, there is a need for multidisciplinary preconception and pregnancy care.

      Research implications

      Fetal growth restriction may be the result of metabolic disorders. An important issue is whether FGR can be prevented by supplementing the mother. The most common nutritional deficiencies after gastric bypass are for calcium, iron, vitamin B12, vitamin D, and, more rarely, proteins.
      • Coupaye M.
      • Rivière P.
      • Breuil M.C.
      • et al.
      Comparison of nutritional status during the first year after sleeve gastrectomy and Roux-en-Y gastric bypass.
      • Ledoux S.
      • Calabrese D.
      • Bogard C.
      • et al.
      Long-term evolution of nutritional deficiencies after gastric bypass: an assessment according to compliance to medical care.
      These deficiencies can have a significant impact on pregnancy and neonatal outcomes. Few studies have focused on the nutritional status of pregnant women after bariatric surgery, and only 2 have compared nutritional status according to the type of procedure performed.
      • Devlieger R.
      • Guelinckx I.
      • Jans G.
      • Voets W.
      • Vanholsbeke C.
      • Vansant G.
      Micronutrient levels and supplement intake in pregnancy after bariatric surgery: a prospective cohort study.
      • Mead N.C.
      • Sakkatos P.
      • Sakellaropoulos G.C.
      • Adonakis G.L.
      • Alexandrides T.K.
      • Kalfarentzos F.
      Pregnancy outcomes and nutritional indices after 3 types of bariatric surgery performed at a single institution.
      Surprisingly, Devlieger et al
      • Devlieger R.
      • Guelinckx I.
      • Jans G.
      • Voets W.
      • Vanholsbeke C.
      • Vansant G.
      Micronutrient levels and supplement intake in pregnancy after bariatric surgery: a prospective cohort study.
      did not find a difference in the nutritional status of women between gastric bypass and banding and only partial normalization of low levels of micronutrients with supplementation. Mead et al
      • Mead N.C.
      • Sakkatos P.
      • Sakellaropoulos G.C.
      • Adonakis G.L.
      • Alexandrides T.K.
      • Kalfarentzos F.
      Pregnancy outcomes and nutritional indices after 3 types of bariatric surgery performed at a single institution.
      found no significant difference concerning iron, B12 vitamin, or calcium deficiencies between biliopancreatic diversion (BPD), gastric bypass, and sleeve gastrectomy in women following nutritional supplement guidelines before and during pregnancy, but they found more protein deficiencies after BPD than after gastric bypass or sleeve gastrectomy. Interestingly, neonates had significantly lower average birthweights after BPD, compared to gastric bypass or sleeve gastrectomy, but no significant increase in low birthweight, defined as <2500 g. Some of our patients had regular follow-up with vitamin blood tests and nutritional supplements before and during pregnancy. It would be interesting to see if the newborns of the women who benefited from this multidisciplinary care have a lower incidence of SGA than those whose mothers did not have nutritional follow-up.

      Strengths and weaknesses

      We analyzed the birthweight from z-scores, taking into account sex and gestational age, on a reference curve after a similar population in Ile de France.
      • Capmas P.
      • Salomon L.J.
      • Picone O.
      • Fuchs F.
      • Frydman R.
      • Senat M.V.
      Using Z-scores to compare biometry data obtained during prenatal ultrasound screening by midwives and physicians.
      A strength of our study is to have compared the study group with a control group of women matched for preconceptional BMI. Then, a multivariable analysis was performed adjusting for factors that influence the growth potential, age, ethnicity, smoking, and diabetes. When preconceptional BMI and weight gain during pregnancy were introduced into the multivariable model, the influence of bypass surgery was not changed. This shows that our results are robust, although our bypass patients often remained obese, with a mean BMI of 33.1 kg/m2. Thus, we can interpret the increase in SGA as a phenomenon of growth restriction.
      The main limitation of this study is the small study size, compared to the Swedish
      • Johansson K.
      • Stephansson O.
      • Neovius M.
      Outcomes of pregnancy after bariatric surgery.
      • Roos N.
      • Neovius M.
      • Cnattingius S.
      • Trolle Lagerros Y.
      • Sääf M.
      • Granath F.
      • Stephansson O.
      Perinatal outcomes after bariatric surgery: nationwide population based matched cohort study.
      and Danish studies.
      • Kjær M.M.
      • Lauenborg J.
      • Breum B.M.
      • Nilas L.
      The risk of adverse pregnancy outcome after bariatric surgery: a nationwide register-based matched cohort study.
      There are advantages, however, to a hospital-based study with access to complete obstetric and perinatal data, as compared to the large population-based studies, which rely on national health care databases. Furthermore, our study included women who had gastric banding and gastric bypass, as well as some sleeve gastrectomies. The latter 2 types of bariatric surgery reflect current practices in France, which is not the case of the reports from Sweden. In the study by Roos et al,
      • Roos N.
      • Neovius M.
      • Cnattingius S.
      • Trolle Lagerros Y.
      • Sääf M.
      • Granath F.
      • Stephansson O.
      Perinatal outcomes after bariatric surgery: nationwide population based matched cohort study.
      the majority of women had vertical banded gastroplasty, a procedure that is no longer recommended in France since the year 2000, whereas in the study by Johansson et al,
      • Johansson K.
      • Stephansson O.
      • Neovius M.
      Outcomes of pregnancy after bariatric surgery.
      98% had a gastric bypass procedure, which did not allow for comparison with other procedures regarding the risk of fetal growth restriction.

      Next step in research

      Among the most interesting outcomes are the long-term benefits for the child. In utero starvation has been known since Barker’s hypothesis
      • Wadhwa P.D.
      • Buss C.
      • Entringer S.
      • Swanson J.M.
      Developmental origins of health and disease: brief history of the approach and current focus on epigenetic mechanisms.
      to increase the risk of metabolic syndrome in the offspring. However, the risk of childhood obesity has been reported to decrease following maternal malabsorptive bariatric surgery.
      • Kral J.G.
      • Biron S.
      • Simard S.
      • et al.
      Large maternal weight loss from obesity surgery prevents transmission of obesity to children who were followed for 2 to 18 years.
      Researchers in Quebec have found a decrease in metabolic syndrome
      • Marceau P.
      • Kaufman D.
      • Biron S.
      • et al.
      Outcome of pregnancies after biliopancreatic diversion.
      and reported convincing evidence suggesting an epigenetic effect through modifications in the intrauterine environment.
      • Guénard F.
      • Tchernof A.
      • Deshaies Y.
      • et al.
      Methylation and expression of immune and inflammatory genes in the offspring of bariatric bypass surgery patients.
      Further studies with long-term follow-up will be required to investigate whether the reduced birthweights associated with malabsorptive bariatric surgery are detrimental or possibly beneficial for the child’s health and future.

      Acknowledgments

      We thank Chloé Dussaux and Pietro Santulli for their participation in the conception of the study and data collection and thank the women who accepted that their data be used for the study.

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      Linked Article

      • Restrictive bariatric procedures improve pregnancy outcomes compared with malabsorptive procedures
        American Journal of Obstetrics & GynecologyVol. 214Issue 6
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          We have read with great interest the study by Chevrot et al,1 which assesses pregnancy outcomes after bariatric surgery (BS), with emphasis on birthweight and the different BS techniques (malabsorptive and restrictive procedures). The authors report a significant reduction in gestational diabetes (GDM) and large-for-gestational-age neonates (LGA) and an overall increase in small-for-gestational-age neonates (SGA).1
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        American Journal of Obstetrics & GynecologyVol. 214Issue 6
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          We thank Drs Galazis and Sein1 for their kind comments on our study.2 As they mention, our findings are consistent with the meta-analysis by Galazis et al3 showing that the incidence of small-for-gestational age (SGA) was increased in women who underwent bariatric surgery but not when adjustable gastric banding (a restrictive procedure) was performed. We do suggest that restrictive, rather than malabsorptive, procedures should be preferred in young women planning to have children. Gastric banding, however, is less effective than gastric bypass for weight loss and thus less popular, and it carries an increased risk of surgical complications during pregnancy.
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