Effect of bariatric surgery on pregnancy outcome☆

1. Introduction 

The prevalence of people who are overweight or obese has increased dramatically in high-income countries over the past 20 years [1], [2], [3]. Figures for 1999–2002 showed that in the United States approximately two-thirds (65.1%) of Americans aged 20 years or older had a body mass index (BMI, calculated as weight in kilograms divided by height in meters squared) greater than 25 and were considered overweight, one-third (30.4%) were considered obese (BMI greater than 30), and 4.9% were morbidly obese (BMI greater than 40) [1]. Between 1999 and 2002, close to one-third of women of childbearing age (20–39 years) were classified as obese in the United States, and an additional 25% of women in this age cohort were overweight [1]. In Sweden, the increase in numbers of overweight women has been less prominent, but is indisputable nonetheless [4]. In the United Kingdom up to 40% of women in one study had a maternal BMI classified as either moderately or very obese [5]. In Israel, obesity rates are high and similar to those reported in the United States [6].

In addition to the escalating prevalence of overweight and obese women of reproductive age, the rates of adverse perinatal outcomes and comorbidities are also rising. Pregravid obesity is a significant risk factor for both adverse maternal and perinatal outcomes [7], [8], [9], [10], [11], with an increased risk for spontaneous abortions and congenital anomalies encountered in early pregnancy [10], [12], [13], [14]. Gestational hypertensive disorders and diabetes, the maternal manifestations of the metabolic syndrome, become clinically recognized in the later stages of pregnancy [7], [8], [9], [12]. The combination of pregestational metabolic syndrome and the physiological changes of pregnancy cause an increased risk for problems such as chronic cardiac dysfunction, proteinuria, sleep apnea, and nonalcoholic fatty liver disease [12]. During labor, obesity increases the risk for cesarean delivery and the associated complications of anesthesia, infection, wound disruption, and deep venous thromboembolism [7], [12]. Obesity is also associated with short-term perinatal risks of macrosomia, birth trauma, and shoulder dystocia, and long-term risks of adolescent and adult metabolic syndrome [7], [8], [9], [12], [13], [14], [15].

Weight loss before conception is the optimum way to decrease the risk for medical and obstetric complications in obese women of reproductive age. Because medical therapy and lifestyle changes have had limited success in maintaining long-term weight loss, bariatric surgery has become a popular alternative for obese women planning pregnancy [12]. Recent evidence reported that pregnancies after bariatric surgery were uncomplicated and well tolerated by the mothers, even in the presence of gestational diabetes mellitus [16], [17], [18]. The purpose of the present study was to examine the perinatal outcomes of women who delivered before bariatric surgery with women who delivered after bariatric surgery. We hypothesized that the perinatal outcomes of pregnancies following bariatric surgery would be improved compared with the perinatal outcomes of deliveries before the surgery.

3. Results 

Between 1988 and 2006, over 180000 singleton deliveries occurred in the Soroka University Medical Center. Of these, 176 women had 301 (0.17%) deliveries that occurred before bariatric surgery and 354 women had 507 (0.28%) deliveries that occurred after bariatric surgery. Pregnancies following bariatric surgery were characterized by advanced maternal age and greater parity and gravidity (Table 1). Significantly higher rates of previous cesarean delivery were reported for women who delivered after bariatric surgery compared with deliveries that occurred before surgery. Rates of obesity (defined as a maternal prepregnancy BMI of 30 or greater) and pregestational diabetes mellitus were significantly reduced after bariatric surgery. The population was almost exclusively comprised of Jewish parturients.

Table 1. Clinical characteristics of women who delivered before and women who delivered after bariatric surgery a

	Characteristics	Deliveries before bariatric surgery	Deliveries after bariatric surgery	P value
		(n=301)	(n=507)
	Maternal age, y	26.5±4.3	31.3±5.1	<0.001
	Gestational age, wk	38.9±2.5	38.7±2.4	0.14
	Ethnicity			0.28
	Jewish	98.3	97.4
	Bedouin	1.7	2.6
	Gravidity			<0.001
	1	43.2	26.2
	2–4	51.8	65.5
	≥5	5.0	8.3
	Parity			<0.001
	1	35.9	18.5
	2–4	51.8	60.0
	≥5	12.3	21.5
	Previous cesarean delivery	7.6	20.1	<0.001
	Obesity b	19.6	9.5	<0.001
	Pregestational diabetes	5.6	2.4	0.014

a Values are given as mean±SD, or percentage. b Maternal prepregnancy body mass index of 30 or greater (calculated as weight in kilograms divided by height in meters squared).

The gestational risk factors and perinatal complications of the patients who delivered before and after bariatric surgery are presented in Table 2. There were significantly lower rates of hypertensive disorders in general and severe pre-eclampsia in particular, as well as lower rates of diabetes mellitus and anemia (defined as maternal hemoglobin less than 10 g/dL) following bariatric surgery. There was a trend toward higher rates of malpresentations in deliveries after bariatric surgery compared with deliveries that occurred before the surgery. No statistically significant differences were noted between the groups regarding fertility treatment, recurrent abortion, gestational diabetes mellitus, placental abruption, premature rupture of membranes, or intrauterine growth restriction.

Table 2. Gestational risk factors and perinatal complications in women who delivered before and women who delivered after bariatric surgery a

	Characteristics	Deliveries before bariatric surgery	Deliveries after bariatric surgery	OR	95% CI	P value
		(n=301)	(n=507)
	Fertility treatment	6.6	7.5	1.1	0.6–1.9	0.38
	Recurrent abortion	4.3	5.5	1.3	0.7–2.5	0.28
	Hypertensive disorders (total)	23.6	11.2	0.4	0.3–0.6	<0.001
	Severe pre-eclampsia	4.0	1.0	0.2	0.1–0.7	0.005
	Diabetes mellitus (total)	17.3	11.0	0.6	0.4–0.9	0.009
	Gestational diabetes mellitus	11.6	8.7	0.7	0.5–1.2	0.11
	Placental abruption	0.3	0.8	2.4	0.3–21.4	0.39
	PROM	7.6	10.5	1.4	0.8–2.4	0.11
	Malpresentation	5.3	8.7	1.7	0.9–3.1	0.056
	IUGR	2.3	3.9	1.7	0.7–4.1	0.15
	Anemia (Hb<10 g/dL)	70.9	61.8	0.7	0.5–0.9	0.014

Abbreviations: PROM, premature rupture of membranes; IUGR, intrauterine growth restriction; Hb, hemoglobin; OR, odds ratio; CI, confidence interval.

a Values are given as percentages unless otherwise indicated.

The pregnancy and delivery outcomes of patients who delivered before and after bariatric surgery are described in Table 3. Significantly lower mean neonatal birth weight and lower rates of large for gestational age neonates (birth weight of 4000 g and greater) were noted in deliveries that occurred following bariatric surgery. On the other hand, rates of cesarean delivery and fetal malformations were significantly higher after bariatric surgery. When controlling for previous cesarean delivery applying the Mantel-Haenszel test, rates of cesarean delivery no longer remained significant (OR 2.34, 95% CI 0.9–6.1; P=0.075). There were no significant differences between the groups in the rates of low birth weight, low Apgar scores at 1 and 5 minutes, or in rates of perinatal mortality.

Table 3. Pregnancy and delivery outcomes of women who delivered before and women who delivered after bariatric surgery a

	Characteristics	Deliveries before bariatric surgery	Deliveries after bariatric surgery	OR	95% CI	P value
		(n=301)	(n=507)
	Birth weight, g	3264±599	3079±567	-	-	<0.001
	Cesarean delivery	17.9	30.0	1.9	1.4–2.8	<0.001
	Fetal malformations	3.3	7.9	2.5	1.2–5.1	0.006
	Macrosomia (≥4000 g)	7.6	3.2	0.4	0.2–0.8	0.004
	Low birth weight	9.0	11.8	1.4	0.8–2.2	0.12
	Apgar <7 at 1 min	4.1	5.4	1.3	0.7–2.7	0.25
	Apgar <7 at 5 min	0.7	1.2	1.8	0.4–8.9	0.38
	Perinatal mortality	2.3	1.0	0.4	0.1–1.3	0.11

a Values are given as mean±SD, or percentage unless otherwise indicated.

The cesarean delivery rate was significantly higher in deliveries following bariatric surgery. The indications for cesarean delivery in both groups are presented in Table 4. A significant reduction in fetal macrosomia as an indication for cesarean delivery was noted following bariatric surgery, and no cases of second stage dystocia were noted. Repeat cesarean delivery was the major indication in patients following bariatric surgery. No cases of placenta previa were noted. Other indications for cesarean delivery were not significantly different between the groups.

Table 4. Indications for cesarean delivery before and after bariatric surgery a

	Indications for cesarean delivery b	Cesarean deliveries before bariatric surgery	Cesarean deliveries after bariatric surgery	OR	95% CI	P value
		(n=54)	(n=152)
	Fetal macrosomia	14.8	3.9	0.24	0.08–0.72	0.011
	Previous cesarean	24.1	50.7	3.24	1.6–6.5	0.001
	Hypertension disorders	25.9	17.1	0.6	0.3–1.2	0.11
	Placental abruption	1.9	2.0	1.0	0.1–10.5	0.72
	Suspected fetal distress	9.3	6.6	0.7	0.2–2.1	0.35
	First stage labor dystocia	18.5	10.5	0.5	0.2–1.2	0.10
	Malpresentation	29.6	25.0	0.8	0.4–1.6	0.31

a Values are given as percentage unless otherwise indicated. b No cases of second stage dystocia or placenta previa were noted.

Since fetal malformations were significantly higher in deliveries after bariatric surgery than in those that occurred before surgery (7.9% vs 3.3%; P=0.006), another multivariate analysis was constructed, with fetal malformations as the outcome variable. The model controlled for possible confounders, such as maternal age, diabetes mellitus, and birth weight. There was a nonsignificant trend toward higher rates of fetal malformations in deliveries following bariatric surgery compared with deliveries that occurred before the surgery. Nevertheless, bariatric surgery was not found to be an independent risk factor for fetal malformations (OR 1.9, 95% CI 0.88–4.1; P=0.089; Table 5).

Table 5. Independent risk factors for fetal malformations a

	Characteristics	OR	95% CI	P value
	Maternal age	1.07	1.00–1.13	0.037
	Bariatric surgery	1.9	0.88–4.12	0.089
	Preterm delivery	5.9	2.75–12.7	<0.001

a Results from a multivariate analysis with fetal malformations as the outcome variable. The initial model also included diabetes mellitus and birth weight.

Using a multivariate analysis, with backward elimination (Table 6), the following conditions were found to be significantly lower after bariatric surgery: diabetes mellitus (OR 0.42, 95% CI 0.26–0.67; P<0.001), hypertensive disorders (OR 0.38, 95% CI 0.25–0.59; P<0.001), and fetal macrosomia (OR 0.45, 95% CI 0.21–0.94; P=0.033).

Table 6. Reduction in perinatal complications independently associated with bariatric surgery status a

	Characteristics	OR	95% CI	P value
	Diabetes mellitus	0.42	0.26–0.67	<0.001
	Hypertensive disorders	0.38	0.25–0.59	<0.001
	Fetal macrosomia	0.45	0.21–0.94	0.033

a Results from a multiple logistic regression model with backward elimination. The initial model included, in addition, maternal age.

4. Discussion 

The present study addressed the importance of weight reduction to decrease the risk of medical and obstetric complications in obese women. The study examined a relatively large cohort from southern Israel, and addressed some of the gestational complications and adverse outcomes known to be associated with maternal obesity. The present study showed a significant reduction in the rates of hypertensive disorders, diabetes mellitus, and fetal macrosomia in pregnancies following bariatric surgery compared with pregnancies that preceded surgery.

The surgical treatment of obesity is a rapidly growing area of surgical practice today. This rapid growth reflects the ability of bariatric surgery to achieve major and durable weight loss, as well as the evolution of safer, less invasive procedures. The aim of bariatric surgery is to reduce caloric intake by using either restrictive procedures or malabsorptive procedures. Roux-en-Y gastric bypass (restrictive and some malabsorptive), laparoscopic adjustable gastric banding (restrictive only), and the biliopancreatic diversion with duodenal switch (malabsorptive and some restrictive) are the most commonly used techniques [4], [11], [21], [22], [23]. Information regarding pregnancy outcomes following bariatric surgery according to the different types of surgery is scarce [11], [24].

After major weight loss, many health benefits are noted. Changes in obesity-related illness, quality of life (QOL), and psychological well-being are probably the most significant outcomes of bariatric surgery [15]. Major weight loss in the severely obese leads to complete or partial control of common serious diseases, such as diabetes, heart disease, and hypertension [3]. Dramatic improvement or resolution of serious medical comorbidities accompanying weight loss following bariatric surgery have been reported [15], [16], [17], [21], [22], [23], [24]. It is possible that the decrease in gestational hypertensive disorders following bariatric surgery could reflect the decrease in primigravidas (43.2% vs 26.2%), a status known to be a risk factor for gestational hypertensive morbidity. However, pregnancies following bariatric surgery were characterized by advanced maternal age, another known risk factor for gestational hypertensive morbidity. However, using a multivariate analysis controlling for possible confounders, the rate of hypertensive disorders was significantly lower following bariatric surgery. Our results are in accordance with other studies conducted in pregnant and nonpregnant patients [15], [25]. In addition, rates of obesity were significantly reduced following bariatric surgery (19.6 vs 9.5, OR 0.43, 95%CI 0.28–0.65; P<0.001), indicating the relative success of the surgical intervention. Unfortunately, our database does not include data regarding weight gain.

In nonpregnant patients there are major improvements in the conditions of the metabolic syndrome, characterized by impaired glucose tolerance, dyslipidemia, and hypertension. Dixon and O'Brien [15] reported that improvements in insulin sensitivity and pancreatic beta-cell function associated with weight loss induce a remission in the majority of type 2 diabetics and reduce the risk of others developing type 2 diabetes [15]. Raised levels of high-density lipoprotein cholesterol and lower triglyceride concentrations characterize improvement in dyslipidemia. In addition to lower blood pressure, these changes provide a sizeable reduction in cardiovascular risk. Improvement in other medical conditions caused or aggravated by obesity, such as sleep apnea, daytime sleepiness, asthma, and gastroesophageal reflux are also significant [15].

Indeed, many health benefits are noted in pregnancies following bariatric surgery. Bar-Zohar et al. [26] evaluated the pregnancy and perinatal outcomes of women who underwent laparoscopic adjustable gastric banding (LAGB) for treatment of morbid obesity. They found that LAGB is safe for both mother and newborn during gestation and delivery. Our group [17] conducted a population-based study that compared all pregnancies of patients with and without previous obesity operations. No significant differences were noted between the groups regarding perinatal complications such as placental abruption, placenta previa, labor dystocia, or perinatal complications (such as meconium-stained amniotic fluid, perinatal mortality, congenital malformations and low Apgar scores at 1 and 5 minutes). Nevertheless, bariatric surgery was found to be an independent risk factor for cesarean delivery [26]. Moreover, even in patients with gestational diabetes mellitus, previous bariatric surgery was not associated with adverse perinatal outcome [25].

Previous studies conducted in our center [17], [18], and others [26], have compared pregnancies in women who had had bariatric surgery with pregnancies in women who had not had previous obesity operations. Few studies have examined the perinatal outcomes of women who delivered before and after bariatric surgery [25], [27]. Even while controlling for confounders using a multivariate analysis, the rates of diabetes mellitus, hypertensive disorders, and fetal macrosomia were significantly lower following bariatric surgery. No significant differences between groups were noted regarding low Apgar scores at 1 and 5 minutes or in rates of perinatal mortality.

Obesity was found to be an independent risk factor for cesarean delivery in a previous study (OR 3.2, 95% CI 2.9–3.5; P<0.001) [9]. It could be expected that the reduction in weight following bariatric surgery would lead to a decrease in the rates of cesarean delivery. However, in a previous study from our center, previous bariatric surgery was found to be an independent risk factor for cesarean delivery [17]. In the present study, rates of cesarean delivery were significantly higher after bariatric surgery. This was attributed to the previous status of the patients, namely higher rates of previous cesarean delivery, because while controlling for previous cesarean (using the Mantel-Haenszel test), rates of cesarean delivery were no longer significantly different between groups. A significant reduction in fetal macrosomia as an indication for cesarean delivery was noted following bariatric surgery.

Controversy exists regarding the association between obesity and congenital malformations. Watkins et al. [14] explored the relation between several birth defects and obesity in a population-based case-control study. The risks for obese women (BMI≥30) and overweight women (BMI 25.0–29.9) were compared with those for average-weight women (BMI 18.5–24.9). The authors concluded that obesity is significantly associated with fetal malformations. Recent studies evaluating perinatal outcomes following bariatric surgery did not find a significant difference between the groups regarding congenital malformations, even in the presence of gestational diabetes [25], [26], [27]. However, abnormal vitamin and trace mineral values are common postoperatively in bariatric surgery patients; this effect is more profound following malabsorptive procedures. This could predispose the development of fatal congenital malformations. In the present study fetal malformations were significantly higher in deliveries following bariatric surgery than in those that occurred before the surgery. Nevertheless, postbariatric surgery patients were significantly older, and when controlling for this important factor using a multivariate analysis with fetal malformations as the outcome variable, the association was no longer significant (OR 1.9, 95% CI 0.88–4.1; P=0.089).

Studies of such large databases are limited because of different forms of bias, especially reporting bias. Accordingly, there are inherent limitations to our study. All forms of bariatric surgery were included and grouped together, including restrictive and malabsorptive procedures that were performed using both open and laparoscopic techniques. The indication for a particular type and technique was broadly similar—morbid obesity—and management did not differ according to the procedures. Another limitation of our study is lack of information regarding BMI or weight gain during pregnancy. However, we added data regarding obesity, showing that the rates of obesity (defined as maternal prepregnancy BMI of 30 or greater) were significantly reduced following bariatric surgery. This could be an indication of the relative success of the surgical intervention. The major strength of our study is that we examined a relatively large cohort of deliveries that occurred in one center, the sole hospital in the Negev, Israel, serving the entire obstetric population in the area. Thus, the study represents nonselective data.

In conclusion, a decrease in maternal complications, such as diabetes mellitus and hypertensive disorders, as well as a decrease in fetal macrosomia can be achieved following bariatric surgery. In addition, bariatric surgery is not an independent risk factor for adverse perinatal outcomes.