Pregnancy after bariatric surgery: Consensus recommendations for periconception, antenatal and postnatal care

Summary The objective of the study is to provide evidence‐based guidance on nutritional management and optimal care for pregnancy after bariatric surgery. A consensus meeting of international and multidisciplinary experts was held to identify relevant research questions in relation to pregnancy after bariatric surgery. A systematic search of available literature was performed, and the ADAPTE protocol for guideline development followed. All available evidence was graded and further discussed during group meetings to formulate recommendations. Where evidence of sufficient quality was lacking, the group made consensus recommendations based on expert clinical experience. The main outcome measures are timing of pregnancy, contraceptive choice, nutritional advice and supplementation, clinical follow‐up of pregnancy, and breastfeeding. We provide recommendations for periconception, antenatal, and postnatal care for women following surgery. These recommendations are summarized in a table and print‐friendly format. Women of reproductive age with a history of bariatric surgery should receive specialized care regarding their reproductive health. Many recommendations are not supported by high‐quality evidence and warrant further research. These areas are highlighted in the paper.


| INTRODUCTION
The prevalence of obesity worldwide has nearly tripled between 1975 and 2016. In 2016, 1.9 billion adults aged 18 years or older (40% of women and 39% of men) were affected by overweight (BMI [25][26][27][28][29] kg/m 2 ) with 650 million (11% men and 15% women) having obesity (BMI ≥ 30 kg/m 2 ). 1 Obesity increases complications for both mother and offspring during pregnancy and childbirth. 2 Furthermore, there is growing evidence that parental nutrition and lifestyle affect embryonic development with potential long-term health implications for the infant through on the process of developmental programming. 3,4 As such, it is generally recommended that both women and men with obesity lose weight before conception. 5,6 Based on international guidelines, 7 patients with class III obesity (BMI ≥ 40 kg/m 2 ) or class II obesity (BMI 35-39 kg/m 2 ) with associated comorbidities may be eligible for bariatric surgery (BS). Poor success with weight loss by diet alone has led to BS becoming increasingly popular. 8 Common procedures include (1) sleeve gastrectomy (SG), the most frequently performed operation, 9 in which the greater curvature of the stomach is resected, reducing stomach volume by 75%, thus limiting food intake. This procedure also removes ghrelin-producing secreting endocrine cells present in the greater curvature of the stomach, which aid in appetite reduction.
Weight loss as well as alterations in other metabolic hormones results in the improvement of glucose homeostasis and results in positive effects on comorbidities therefore reducing appetite and aiding in subsequent diabetes remission. 10 (2) Roux-en-Y gastric bypass (RYGB), a mixed procedure in which the volume of the stomach is reduced to approximately 15 to 30 mL and the absorption of nutrients, is impaired by bypassing part of the small intestine and diverting the food flow to the distant small intestine. This approach not only results in a limited oral intake but also induces malabsorption, although this is reduced over time because of intestinal hypertrophy. Furthermore, an increase in gut hormone secretion (including GLP-1 and PYY) hormones associated with RYGB may diminish appetite and result in better glucose homeostasis. 11 (3) Adjustable gastric band (AGB) procedures where an inflatable restrictive band is placed around the upper portion of the stomach creating a small pouch with a narrow opening to the lower stomach, adjusted by adding or removing fluid to the band via a subdermal port. This reduces stomach capacity and appetite. 12 Other types of surgery include biliopancreatic diversion with duodenal switch, intragastric balloon, and vertical banded gastroplasty, but these are outdated or rarely performed.
As a result of weight loss and enteroendocrine alteration, BS has also been shown to reduce the incidence of obesity-related comorbidities and complications. 13 BS is however associated with a potential increase in adverse events due to surgical complications and micronutrient deficiencies and derangements in (neuro)endocrine and metabolic homeostasis. [14][15][16][17] Approximately 80% of BS is in women, many of whom are of reproductive age. [18][19][20] BS may improve fertility through restoration of ovulation, and pregnancies after BS are becoming increasingly common. 21 It has been recognized that changes in gut anatomy and physiology with potential for malnutrition incur increased potential for adverse perinatal outcomes such as small for gestational age (SGA), preterm birth, congenital abnormalities, and perinatal mortality. Pregnancy soon after surgery may increase risk of maternal morbidity and/or mortality. 22 A need for more specific guidance and nutritional management was recognized, and an international group of experts was assembled to review the available evidence and provide recommendations on the periconception, antenatal, and postnatal care of pregnancies after BS.

| METHODS
An expert meeting focused on pregnancy after BS was organized at the University of Surrey, UK in April 2017 with a follow-up meeting at University Hospital Leuven, Belgium, in November 2017. These meetings brought together national and international expertise from a multidisciplinary group of researchers and clinicians including specialists in obstetrics and gynaecology, bariatric surgery, endocrinology, dietetics, nutrition, nursing and midwifery, health psychology, epidemiology, and public health. Additional international colleagues were able to join both meetings through teleconferencing.
The objectives of the meetings were to discuss the key questions, to advance scientific knowledge and practice in the area of pregnancy after BS, and to identify key areas of focus for collaborative work to produce consensus clinical guidelines on best practice for facilitating healthy pregnancies after BS.
The clinical guideline was developed using the structure from ADAPTE. 23 The group formulated specific clinical questions in relation to pregnancy after BS (Table 1). For each question, a systematic search of the available literature was performed, identifying articles published from inception to July 2018. Search terms related to pregnancy ("pregnancy," "prepregnancy," "mother," "maternal," "conception," "preconception," "gravid," "pregravid") were combined with terms related to BS ("bariatric surgery," "weight loss surgery," "gastric bypass," "Rouxen-Y," "RYGB," "sleeve gastrectomy," "gastric sleeve," "gastroplasty," "gastric band," "LAGB," "biliopancreatic diversion," "BPD," "duodenal switch") and terms specific for each clinical question. Articles resulting from these searches and relevant references cited in those articles were reviewed. All evidence was graded ( Table 2) 24 and discussed during group meetings. When evidence of sufficient quality was lacking, the group made consensus recommendations based on expert clinical experience. Consensus on the guidelines was declared when 100% of the group agreed with the recommendations. The final document was reviewed by all authors. The recommendations made by this group are summarized in Table 3.

| Bariatric surgery to conception interval
The period after BS is characterized by weight loss which may be rapid after SG and RYGB procedures and slower after AGB, once optimal adjustment has been achieved. During this period postsurgery, 25,26 women are recommended to postpone pregnancy in order to ensure maximal weight loss, weight stabilization, and to reduce the risk of macronutrient and micronutrient deficiencies and electrolyte imbalances. 5 Evidence in regard to this recommendation is however scarce.
We identified 14 studies reporting on the surgery-to-conception interval and pregnancy outcomes, but many studies have limitations in methodology thus preventing comparison.
Parent et al 22 found that a shorter surgery-to-birth interval (less than 2 years) was associated with a higher risk for prematurity, SGA, and neonatal intensive care unit (NICU) admission (level 2++), but data on long-term outcomes were missing. In contrast, Stentebjerg et al 27 and Nomura et al 28 found an increased risk for certain pregnancy complications (iron deficiency, excessive gestational weight gain (GWG), and delivery by caesarean section) if the pregnancy was postponed according to this recommendation (level 2+). Norgaard et al 29 found no difference in the prevalence of SGA prior to, or after, 18 months (level 2++). Other studies also did not find a difference in gestational outcomes according to surgery to conception interval. 27,[30][31][32][33][34][35][36][37] Based on level 2++ evidence, the members of this group recommend postponing pregnancy until a stable weight is achieved. This is typically achieved 1 year after SG or RYGB procedures and 2 years after AGB.

| Contraception
Women recommended to postpone pregnancy during the period of rapid weight loss (1-2 years) require adequate counselling regarding safe and effective contraception. 38 As obesity is associated with impaired fertility due to metabolic syndrome and PCOS, patients

Clinical Questions to be Answered in This Guideline
What is the recommended time interval between bariatric surgery and conception?
What types of contraception should be advised to women after bariatric surgery?
Are there special recommendations regarding dietary behaviour?
Which micronutrients should be monitored? Which types of supplements should be prescribed?
Should patients be screened for gestational diabetes and how should they be screened?
Which medical and surgical complications should be monitored, and can they be prevented?
Is breastmilk composition affected by bariatric surgery and can it safely be recommended to patients?    may not be using contraception presurgery. They should be made aware that fertility increases postoperatively, and contraception usage should be discussed (level 2+). 39 There is sufficient evidence to show that perioperative contraceptive counselling increases the postoperative use of contraception (level 2+). 40,41 Contraceptive counselling and contraceptive knowledge by health care providers could however be improved (level 2−), 42,43 as contraceptive use after BS is often suboptimal, with many women using least reliable methods (level 2+). 39,40,[44][45][46][47][48] This is even more important in patients with a history of infertility, as they have been found to be at increased risk for unprotected intercourse without intent to conceive and have higher early postoperative conception rates. 39 Both RYGB and, to a lesser extent, SG significantly alter the anatom-

| Nutritional supplementation and monitoring
Men and women after BS have an increased risk to develop micronutrient deficiencies. 73 In the formulation of this guidance, it is recognized that there is a lack of evidence on the optimal nutritional monitoring and supplementation strategies in pregnancy after BS.
We have therefore used data and guidelines for the nonpregnant postoperative population and supplemented this with pregnancy-spe-

| Breastfeeding
Limited data are available on breastfeeding after BS. In longitudinal studies, the composition of breastmilk from women after BS was found to be largely comparable with women without prior BS (level 2++). 89 we advise supporting women wishing to breastfeed after BS (level 2+) and suggest that their nutritional status is closely monitored during lactation with additional supplements to those routinely advised after BS prescribed when necessary (level 3).

| Ultrasound monitoring of fetal growth and anomalies
Most types of BS have been found to double the risk of fetal growth restriction (FGR) and SGA infants in comparison with BMI-matched women 96 and women with obesity. 97 This risk is higher with procedures that potentially further induce malabsorption (such as RYGB), when compared with procedures such as AGB or SG (level 2+). 96,98 Studies suggest that it would seem preferable for women of reproductive age to consider more restrictive procedures to limit this risk. AGB is however also associated with lower birth weight when the band remains inflated during pregnancy (level 2++). 99 Ultrasound monitoring of fetal growth should be offered to all women with a history of BS (level 2++). We recommend monthly screening from viability, especially in the presence of additional risk factors (eg, smokers, low GWG, teenagers) (level 4).
It is still unclear whether BS increases the risk for congenital malformations in the offspring as strong epidemiological data are lacking. 33 Several case reports and case studies have reported on the association between nutritional deficiencies in the mother and congenital anomalies in the offspring (level 3). 83,100-104 We therefore suggest an additional detailed anomaly scan during the late first or second trimester, especially in women with nutritional deficiencies (level 3), and sonographic follow-up of fetal growth during the third trimester (level 2++).

| Weight management in pregnancy
Weight regain following BS is a known problem in a substantial number of patients. [105][106][107] It is therefore important to avoid excessive GWG and postpartum weight retention in women after BS. On the other hand, insufficient GWG increases the risk for FGR and low birth weight. 108 So far, no specific guidelines for GWG during pregnancy in postbariatric women are available and few studies have focussed on the subject.
Overall, women with a history of BS gain less weight during pregnancy compared with women without prior BS, especially during the third trimester (level 2++). 27,[109][110][111][112][113] Women who conceive within 18 months after surgery also appear to have less GWG in comparison with those who conceive after this period (level 2+). 27  In women with AGB, evidence regarding band management and weight gain during pregnancy is also limited. Active band management appears to facilitate adherence to the IOM guidelines and was not associated with low birth weight (level 2++). 26,99,109,117 In contrast, band deflation was associated with macrosomia (level 3). 117 We recommend health professionals caring for women after BS to measure BMI and monitor GWG in order to advise regarding adequate GWG relating to their prepregnancy BMI in accordance to the IOM guidelines (level 2+). If GWG is excessive, women should be assessed for complications (level 2+). In the case of insufficient GWG, diet should be revised and fetal growth carefully monitored (level 4).

| Diabetes screening
Currently, there are no specific guidelines on screening and treatment for diabetes during pregnancy in women after BS.

| Assessment and prevention of surgical complications
Evidence for two common surgical complications during pregnancy was found: internal herniation following RYGB and gastric band slippage following AGB. With regards to internal herniation, an incidence of 8% has been reported during pregnancies after RYGB. 132 135 We recommend that all women with RYGB should be advised about the risks and symptoms of internal herniation and should seek appropriate medical assistance without delay. Care providers should be advised that any pregnant women with a history of RYGB that presents with abdominal pain should be assumed to have a small bowel obstruction due to internal herniation until proven otherwise (level 4) 136 and that imaging techniques and operative intervention, often performed with reluctance in pregnant women, should not be delayed (level 2++).
Gastric band slippage may be increased during pregnancy due to vomiting and increased intraabdominal pressure. One study reported an incidence of 12% during pregnancy compared with 3% to 5% in the general AGB population (level 3). 137 A shorter time interval between AGB and pregnancy was associated with a higher rate of primary band revisions after pregnancy (level 2+). 138 Patients should be

| Research gaps
The recommendations issued in this review are based on a systematic research of the literature by a multidisciplinary group of international experts. The group has identified areas for which the level of evidence and therefore the quality of the recommendations is largely based on expert opinion. It is felt by the group that following areas need further robust investigation with regard to women and children's health in pregnancy following BS: • Contraceptive counselling, safety, efficacy, and use  Table 3 and presented in a print-friendly format for practical use in the clinical setting ( Figure 1). Our work highlights the paucity of studies on the optimal care for this growing group of women and identifies research gaps in this field. The publication of these guidelines will be the first step in a research collaboration which will address these unanswered questions.