Pregnancy After Laparoscopic Sleeve Gastrectomy (LSG): The Effect of Gestational Weight Gain (GWG) On Pregnancy and Perinatal Outcomes

Introduction: We aimed to evaluate the effect of gestational weight gain (GWG) according to Institute of Medicine (IOM) recommendation after laparoscopic sleeve gastrectomy (LSG) on maternal and fetal outcomes. Materials and methods: A retrospective, observational study on the medical charts of pregnant women who had previously undergone LSG between 2012 and 2020. According to IOM, GWG was grouped as insucient, appropriate, and excessive. Results: 82 pregnancies were included in this study. GWG was appropriate in 19 of the pregnancies (23%) and was insucient in 18 (22%) and excessive in 45 (55%) of the cases. The time from operation till conception of excessive group is signicantly longer than insucient and appropriate group (p 1 :0.000; p 2 :0.029; p<0.05). There was no statistically signicant difference between the groups regarding birthweight, gestational age, cesarean deliveries (CD), preterm birth, whether their child was small or large for their gestational age. There was no difference between mean hemoglobin, anemia, low ferritin level and ferritin level at early pregnancy and predelivery between groups (p<0.05). There was no signicant correlation between the time from operation till conception, birthweight and gestational age. There was no signicant correlation between body mass index (BMI) at conception, birthweight and gestational age. There was no signicant correlation between early and predelivery ferritin and hemoglobin and birthweight and gestational age. There was no correlation between mean GWG and mean BMI at conception between birthweight in either study group. Conclusion: The gestational weight gain (GWG) did not impact maternal and neonatal outcomes.


Introduction
Obesity during pregnancy increases the frequency of obstetrical complications, including preeclampsia, gestational diabetes mellitus (GDM), miscarriage, macrosomia, cesarean delivery (CD), labor induction, and anesthetic complications. Weight loss prior to pregnancy is critical for improving maternal and fetal health outcomes [1]. When other weight-loss measures have proven unsuccessful, bariatric surgery (BS) is a treatment option for morbidly obese patients and has gained wide acceptance as a safe and effective treatment for obesity [2]. The number of bariatric procedures performed annually is rapidly increasing worldwide and laparoscopic sleeve gastrectomy (LSG) has recently emerged as the preferred surgical option [3].
Increasing studies have focused on improving maternal and fetal health outcomes after BS [4,5], but there are reports of increased risk of being small for their gestational age (SGA) [5,6] and preterm birth [4][5][6], the cause of which is not yet clear.
Thus, maternal obesity, gestational weight gain (GWG) or gestational weight loss are all affect fetal growth [7]. Weight gain during pregnancy is an important and could affect fetal growth and correlates to low birthweight [7]. Insu cient GWG has been shown to be associated with lower fetal growth and birthweight and increase in SGA infants risk and in preterm birth, whereas excessive GWG was associated with higher risks of Large-for-gestational-age (LGA) and macrosomia [7]. Therefore, the Institute of Medicine (IOM) [8] standarts for adequate weight gain according to the preconception BMI to reduce the risk of growth abnormalities.
With these recommendations, it is aimed to improve maternal and child health and reduce obstetric complications. GWG has been studies in obese patients and in the general population [9,10]. But there is no evidence regarding weight gain recommendations in bariatric pregnancies exits [11][12][13]. Some relatively small studies have examined the subject of the GWG in pregnant patients after BS on maternal and neonatal outcomes; most of them included different time intervals between pregnancy and BS or a mixture of different BS techniques [14][15][16]. Hence the purpose of this research was to examine the effect of GWG on maternal and neonatal outcomes with a history of LSG.

Materials And Methods
A retrospective, observational study was conducted to evaluate the maternal and fetal health outcomes of 142 pregnancies in 113 women who had previously undergone LSG between 2012 and 2020 at the University of Health Sciences, Fatih Sultan Mehmet Training and Research Hospital. We analyzed the charts of women (Fig. 1). If a patient had more than one pregnancy after BS, only the rst delivery was included in this study.
GWG was de ned as the difference between the nal weight and the weight at the conception (kg) and was recorded for each patient as underweight, overweight, or normal, according to the recommended weight gain for their body mass index (BMI) at conception [8]. If pregnant women gained less weight than recommended, they were grouped as insu cient weight gain. If pregnant women gained more weight than recommended, they were grouped as excessive weight gain. And if the pregnant women gained appropriate weight as recommended, they were grouped as appropriate weight gain.
Prematurity was de ned as a gestational age of less than 37 weeks at birth. Low birthweight was de ned as a newborn weight of less than 2500 g. Macrosomia was de ned as a newborn weight of greater than 4000 g. LGA infants were de ned as those with a birthweight above the 90th percentile, and SGA as those with a birthweight below the 10th percentile. Percent excess weight loss (%EWL) was calculated by [(presurgery weight − weight at last follow-up (kg) / (presurgery weight -ideal weight)] × 100 with ideal weight based on body mass index (BMI) of 25 kg/m 2 . Percent total weight loss (%TWL) was calculated by (presurgery weight-weight at last follow-up (kg) / presurgery weight) x 100.
Anemia was de ned using the age-and gender-speci c World Health Organization criteria (hemoglobin (Hgb) < 11 g/dl during pregnancy) [17] and low ferritin was evaluated according to cutoff values < 30 ng/mL [18]. In addition, hemoglobin, ferritin levels at early pregnancy and at the predelivery and the administration of intravenous (iv)/oral iron supplementation were recorded. Patients had been advised to take multivitamins for the rst postoperative year. At each follow up visit we prescribed spesi c supplements if a de ciency was detected on laboratory outcomes. We treated iron de ciencies orally or if necessary intravenously. Statistical analysis IBM Statistics 22 program (IBM, SPSS, Turkey) was used for statistical analysis. The compliance of the parameters to normal distribution was evaluated by Kolmogorov-Smirnov and Shapiro Wilks tests. In the evaluation ot the study data, descriptive statistical methods (mean, standart deviation) as well as the Oneway Anova test for the comparison of the parameters showing normal distribution between the groups in the comparison of the quantitative data, and the Tukey HDS test was used to determine the group that caused the difference. Kruskal Wallis test was used for intergroup comparisons of parameters that did not show normal distribution, and Dunn's test was used to determine the group that caused the difference. Student t test was used for the comparison of parameters showing normal distribution between two groups, and Mann Whitney U test was used for the comparison of parameters that did not show normal distribution between two groups. In comparison of qualitative data, Chi-Square test, Fisher's Exact Chi-Square test, Fisher Freeman Halton Test and Continuity (Yates) Correction were used. Pearson's correlation analysis was used to examine the relationships between parameters suitable for normal distribution, and Spearman'srho correlation analysis was used to examine the relationships between parameters not compatible with normal distribution. All p values < 0.05 were considered as statistically signi cant.

Results
GWG was appropriate according to the recommendations in only 23% of the pregnancies (n = 19) and was insu cient in 22% (n = 18) and excessive in 55% (n = 45) of the cases. We compared maternal characteristics, pregnancy, and neonatal outcomes in the three groups.

Demographic characteristics
Demographic characteristics are reported in Table 1. There is a statistically signi cant difference between the groups in mean of time from operation till conception (p < 0.05). The time from operation till conception of excessive group is signi cantly longer than insu cient and appropriate group (p 1 :0.000; p 2 :0.029; p < 0.05). There is no statistically signi cant difference between the insu cient and appropriate groups in mean of the time from operation till conception (p > 0.05). Table 2 shows pregnancy and perinatal outcomes in the groups. There is no statistically signi cant difference in mean BMI and weight at conception between the groups (p > 0.05). There was a signi cant difference in mean GWG between the groups (p < 0.05). The mean of GWG in excessive group was signi cantly higher than appropriate and insu cient group (p 1 :0.000; p 2 :0.000; p < 0.05), whereas there was no signi cant difference in mean GWG between insu cient and appropriate groups (p < 0.05). In the insu cient group, 3 patients lost weight during pregnancy (-10,-14,-30 kg respectively).

Pregnancy course and outcomes
There was no difference between mean hemoglobin, anemia, low ferritin level and ferritin level at early pregnancy and predelivery between groups (p < 0.05). There was no signi cant difference between the groups in terms of receiving iron supplement.
There was a signi cant difference in mode of delivery or type of labor between the groups (p < 0.05). Vaginal delivery in su cient group (50%) is signi cantly higher than appropriate (15.8%) and excessive group (24.4%) (p 1 :0.026; p 2 :0.049; p < 0.05). There is no statistically signi cant difference in mean mode of delivery between appropriate and excessive group (p > 0.05). The groups were similar in terms of indications for CD (p > 0.05).
In our study, GDM, hypertension, preeclampsia and postpartum hemorrhage were not recorded.

Neonatal characteristics and outcomes
Neonatal characteristics and outcomes were reported in Table 3. There was no signi cant difference in the mean gestational age at delivery, birthweight, LGA and SGA births, low birthweight, and preterm delivery between the groups (Table 3).
There was no signi cant correlation between GWG, baby birth weight and gestational age. There was no signi cant correlation between the time from operation till conception, birthweight and gestational age.
There was no signi cant correlation between BMI at conception, birthweight and gestational age. There was no signi cant correlation between early and predelivery ferritin and Hbg and birthweight and gestational age.

Discussion
The aim of our study was to evaluate the GWG and compare it according to the IOM recommendation [8].
In addition, the results on maternal and neonatal outcomes were evaluated by classifying GWG as insu cient, appropriate and excess according to IOM.
GWG after BS can vary widely in studies [16,19,20]. The average GWG was 12.59 kg in our study, with 3 patients losing weight during pregnancy.
Our ndings are line with those of Hammeken et al. [19] showed that GWG in the RYGB group was 11.5 ± 9.9 kg and Ceulemans et al. [16] showed that the average GWG in the malabsorptive and restrictive group was 12.5 kg. Whereas Chagas et al. [20] found a mean GWG of 7.68 kg in pregnant patients who had undergone gastric bypass.
In our study GWG was insu cient for 22%, appropriate for 23% and excessive for 55% of the pregnancies.
Our insu cient GWG rate was similar the general population's. The IOM [8] described a 25.5% rate of insu cient GWG in obese and normal BMI populations and 14% rate of insu cient GWG in overweight patients. Lindberg et al. [21] showed that insu cient GWG was between 12.2%-25.5% in overweight and grade II obesity.
Obese patients tend to gain excessive weight gain during pregnancy. However, a higher percentage of patients in the studies presented with obesity, the pregnant women lost weight during gestation despite being overweight and obese. This can be explained by the fact that a relatively larger proportion of the pregnant women having a surgery-to-conception interval of less than 18 months and there are in the catabolic phase and therefore cannot gain su cient weight. As the greatest weight loss occurs during the rst 6-18 months postsurgery, this period may be physiologically catabolic because of lower food intake or less absorption of nutrients. During the second year after surgery, the rate of weight loss decreases and weight stabilizes [22].
In our study, average prepregnancy BMI was 30.91 ± 6.18 kg/m2 and there is no statistically signi cant difference in mean BMI at conception between the groups. 26.9% of the patients were overweight and 53.6% were obese. The mean time from operation till conception was 27.74 months. The time from operation till conception of excessive group is signi cantly longer than insu cient and appropriate group. These ndings are in line with those of Stentebjerg et al. [15] after RYGB. They found that 62% of the women with BS who became pregnant were still obese at conception and there was no statistically signi cant difference in mean BMI at conception between the groups. But 43% of their patients had insu cient GWG, which was 22% in our study. Despite being a higher percentage of patients presented with obesity in the study of Stentebjerg et al. [15] the time from operation till conception was shorter than our study. The median time from operation till conception was 14 months which was 27.74 months in our study.
Grand ls et al. [14] found that the women with BS who became pregnant were still obese at conception and women with insu cient GWG had higher pre-pregnancy BMIs when compared to women with normal or excessive GWG. There was no statistically signi cant difference in mean the median time from operation till conception between the groups. Grand ls et al. [14] showed that GWG was insu cient for 35%, was appropriate 27% and was excessive for 38% of the pregnancies and the mean time from operation till conception of insu cient group was shorter than adapted and excessive groups.
Chagas et al. [20] showed that average prepregnancy BMI was 27.36 ± 3.26 kg/m2. 53.3% of the patients were overweight and 23.3% were class I obese. Additionally, they showed that 51.7% of the women presenting insu cient, 34.5% of appropriate, 13.8% of excessive weight gain [20]. The mean time from operation till conception was 17.70 months. This situation can be explained by the lower BMI at conception and the shorter time from operation till conception than our results due to the fact that they gained insu cient weight.
Finally, in a retrospective analysis of 127 pregnancies after malabsorptive and restrictive surgery, Ceulemans et al. [16] reported that 24% of patients gained insu cient, 20% patients gained appropriate and 56% of patients gained excessive weight. These results are in line with our ndings: In our study GWG was insu cient for 22%, appropriate for 23% and excessive for 55% of the pregnancies. Ceulemans et al. [16] found that the women with BS who became pregnant were still obese at conception (37% overweight, 32% obese). Although there was no difference between the groups in terms of BMI and the time from operation till conception, 56% of patients gained excessive weight (80% of these pregnancies occured 18 months after surgery). And the LRYGB patients with BMI above 32.5 kg m2 gained the largest amount of weight during pregnancy [23].
In our study, there was no signi cant difference in the mean birthweight, LGA and SGA births, low birthweight between the groups. Considering the literature studies according to IOM, there are different results in terms of SGA risk. When et al. [24] found that SGA rate was higher in normal weight women who gained insu cient weight during pregnancy.
Catalano et al. [25] showed that an increase in the incidence of SGA was found in the obese or overweight patient group with a weight gain of less than 5 kg during pregnancy.
In the study that 74% of their patients had RYGB, Ceulemans et al. [16] found that a signi cant difference in the prevalence of SGA infants with 47% in patients with insu cient group versus 15% and 13% in those with appropriate and excessive group, respectively. Similar to ndings, Grand ls et al. [14] suggest that the large proportion of women with insu cient GWG may account for increased rates of SGA after restrictive and malabsorptive surgery (34% in the insu cient group versus 27% in the appropriate and 19% in the excessive group). Stentebjerg et al. [15] showed reductions in birth weight when GWG was insu cient, but no statistical signi cance was found after RYGB. Berglind et al. [26] showed that birthweight increased with GWG. Ducarme et al. [27] showed a signi cant reduction in low birthweight and macrosomia after BS despite lower mean GWG compared with controls with obesity.
Because one of the reasons for SGA with BS is insu cient GWG, especially among women with short interval to pregnancy after BS. The pregnant women lost weight during gestation.
In our study, there was no signi cant difference in the mean gestational age at delivery between the groups. These results are in line with Stentebjerg et al. [15]. Ceulemans et al. [16] showed that the gestational age at delivery was comparable between the 3 GWG groups but more patients with insu cient GWG delivered before 37 weeks. In contrast, Grand ls et al. [14] showed that gestational age was signi cantly different between groups and it occurred when the GWG was insu cient.
In the general population, preterm delivery has been associated with insu cient GWG, regardless of BMI at conception [9]. In our study, there was no signi cant difference in the mean preterm delivery between the groups. Stentebjerg et al. [15] found no difference in the prevalence of preterm deliveries between groups. Grand ls et al. [14] found patients with insu cient GWG to be at an increased risk for preterm labor, especially compared with those patients with excessive GWG. These results are in line with Ceulemans et al. [16].
Anemia is frequent in fertile women; and during pregnancy, Hbg and hematocrit (Hct) levels decrease physiologically due to hemodilution caused by physiological plasma volume expansion [28]. Patients who undergo both malabsorptive and restrictive procedures are at risk for iron de ciency [29].
Several studies have established a relationship between anemia and SGA and birth low birth weight [30,31]. There was no difference between mean hemoglobin, anemia, low ferritin level and ferritin level at early pregnancy and predelivery between groups (p < 0.05). There was no signi cant difference between the groups in terms of receiving iron supplement. These results are consisting with Stentebjerg et al. [16].
There was a signi cant difference in mode of delivery or type of labor between the groups (p < 0.05). Vaginal delivery in su cient group (50%) is signi cantly higher than appropriate (15.8%) and excessive group (24.4%) whereas CD rate was found to be signi cantly lower in the groups with insu cient weight gain than the other groups, while the groups were similar in terms of indications for CD. The CD rate in all deliveries in Turkey is high, around 53% [32]. The frequency of cesarean section in pregnant women after BS ranges from 15.4%-61.5% [33]. In our study, the rate of CD was 72% and 44% of it was former CD. Grand ls et al. [15] found that, no signi cant difference was found between the cesarean rates between the groups that were insu cient, appropriate and excessive weight gain. Stentebjerg et al. [16] showed that, CD with excess weight gain was found to be higher than in other groups, and its detection in the excessive group was explained by the maternal age. And the lowest rate was in the group with appropriate weight gain.

Conclusion
There is no statistically signi cant relationship between birthweight and early pregnancy and predelivery ferritin and Hb level, interval from surgery to conception, CD and GWG. But GWG is probably affected by the time period between surgery and conception.
Even so, due to the lack of robust evidence, especially in long-term outcomes, practitioners should continue to recommend to delay pregnancy for 12-18 months after surgery, because of a rapid weight loss and lower food intake or less absorption of nutrients and the catabolic phase after their LSG and its speci c stressful in uence on the organs.
This study had some limitations, due to its retrospective nature-namely the impossibility of evaluating certain nutritional de cits, such as folic acid, magnesium and others and the fact that is it was not possible to obtain all the parameters of all the pregnant women and their newborns.

Declarations
Funding: This research did not receive any speci c grant from funding agencies in the public, commercial or not-for-pro t sectors.
Con ict of interest The authors declare that they have no con icts of interest Data Availability: The data that support this study are available upon request from the 12 corresponding author. The data are not publicly available due to privacy and ethical concerns.
Ethics approval The retrospective, observational study approved by local institutional review board and ethics committee and informed consent for this study was obtained and all the procedures being performed were part of the routine care.  Flowchart of the Study