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Guidelines for the management of pregnant women with obesity: A systematic review

Summary Multiple clinical practice guidelines (CPGs) have been established for pregnant women with obesity. The quality and consistency of recommendations remain unknown. The objective of this study is to conduct a systematic review to synthesize and appraise evidence from CPGs, available worldwide, for pregnant women affected by obesity. An experienced information specialist performed a rigorous search of the literature, searching MEDLINE, Embase, grey literature, and guideline registries to locate CPGs that reported on pregnancy care relating to obesity. CPGs related to antenatal care of pregnant women with obesity (pre‐pregnancy body mass index [BMI] ≥ 30 kg/m2) in low‐risk (eg, care provider = family physician or midwife) or high‐risk settings (eg, obstetrician or maternal fetal medicine) were included. CPGs were appraised for quality with independent data collection by two raters. Information was categorized into five domains: preconception care. care during pregnancy, diet and exercise during pregnancy, care immediately before, during, and after delivery, and postpartum care. The literature search yielded 2614 unique citations. Following screening of abstracts and full texts, 32 CPGs were included, with quality ranging between 0 and 100 on the AGREE II tool. The strongest evidence related to nutritional advice, exercise, and pregnancy risk counselling. Guidance was limited for timing of screening tests, antenatal visits and delivery, ideal postpartum care, and management of adverse pregnancy outcomes. Most guidelines in this population are not evidence based. Research is needed to bridge knowledge gaps pertaining to fetal antenatal surveillance, management of adverse outcomes and postpartum care, and enhance consistency across CPGs.


| INTRODUCTION
Obesity is a major public health concern around the world. Approximately 13% of the world's adult population were affected by obesity in 2016, with similar rates in pregnancy. 1 Over the past few decades, the worldwide rise in excessive weight gain during pregnancy has accompanied concurrent increases in rates of pregnancy complications.
Between 1996 and 2010, there was a doubling in the rate of both gestational diabetes (from 2.7% to 5.6%) and pregestational diabetes (from 0.7% to 1.5%). 2 Rates of preeclampsia and gestational hypertension increased 25% and 184%, respectively, in the United States between 1987 and 2004. 3 The fetuses of mothers affected by obesity are at risk of both overgrowth and growth restriction, stillbirth and birth injury. 4 Furthermore, obesity in pregnancy can pose risks for long-term adverse health outcomes for not only the mother, but also their offspring. 4 These risks include cardiovascular disease, diabetes, hypertension, future obesity among the offspring, and premature death.
Given the well-documented association between pregnant women with obesity and adverse outcomes both during pregnancy and longer term, [5][6][7][8] there is a need for consistent clinical care that follows best evidence-based practice. A number of studies have shown that guidelines can improve health care processes and patient outcomes, but are often of low quality because they contain conflicting recommendations, insufficient consideration of relevant patient characteristics, low quality evidence underlying the recommendations, lack of transparency, and inadequate management of potential conflicts of interest. 9 Access to high quality clinical practice guidelines (CPGs) facilitates informed discussions with patient and decision making that follows best evidence-based practice.
Production of CPGs occurs at national and international levels by medical associations or government bodies. Databases of evidencebased CPGs are developed and maintained by many countries including the United States (National Guideline Clearinghouse). In 2002, the Guidelines International Network (G-I-N) was established to facilitate the international collaboration in guideline development, adaption, and implementation. 10 Currently, G-I-N includes representation from approximately 46 countries around the world. 10 Although national and international guidelines for the management of obesity during pregnancy have already been established, the quality and consistency of these CPGs is currently unknown.
The objective of this review was to identify and synthesize currently available CPGs for pregnant women with obesity. Findings from this review will serve to evaluate the quality of existing CPGs and determine the need for rigorous updating.

| METHODS
A systematic review protocol was prepared following the PRISMA-P checklist 11 and then posted to the University of Ottawa Health Sciences Library's online repository (https://ruor.uottawa.ca/handle/ 10393/35998). The review was registered in the PROSPERO database (CRD42017060503).

| Electronic literature search and process of study selection
The search strategies were developed and tested through an iterative process by an experienced medical information specialist (BS) in consultation with the review team. The strategies were peer reviewed by another senior information specialist prior to execution using the PRESS Checklist. 12  Strategies utilized a combination of controlled vocabulary (eg, "Pregnancy," "Prenatal Care," and "Obesity") and keywords (eg, "pregnant," "antenatal," and "obese").
Search filters for the retrieval of CPGs, outlined by the Canadian Agency for Drugs and Technologies in Health (CADTH), were applied.
These filters are extensively tested and routinely used by CADTH.
We applied CADTH's guideline/care pathway filter, which helped to retrieve relevant CPGs within our selected databases. The CADTHderived filters were adjusted to include the vocabulary and syntax appropriate to each database. In addition, the CADTH filters were slightly amended to include additional terms (eg, "continuity of care" and "patient care") deemed relevant to our project. We excluded documents that were animal-only, as well as opinion pieces from our results. Our database search strategy, which omitted restrictions based on geographic location, combined with the grey literature search of guideline registries both nationally (eg, SOGC) and internationally (eg, National Guideline Clearinghouse), allowed coverage of CPGs available globally. Specific details regarding the strategies appear in Appendix S1.
Duplicates from bibliographic and grey literature searches for the review were identified and removed. Remaining articles were uploaded into an online systematic review software package, Distiller SR (Evidence Partners, Inc, Ottawa, Canada) for level 1 (titles and abstracts) and level 2 (full-text) screening. Before initiating each level, a pilot screening test was completed by each reviewer to confirm understanding. Two reviewers (M.P. and A.S.) then systematically and independently screened the titles and abstracts of the references at level 1, using the "liberal accelerated" method established by Khangura et al. 13 Within this method, only one reviewer is required to retain the abstract for full text screening; however, exclusion from full text screening requires two reviewers to assign the abstract as irrelevant. The same reviewers screened all full-text articles at level 2, and discrepancies were settled by discussion or involvement of a third party (L.G.) if necessary. The process of study selection was summarized using a PRISMA flow diagram ( Figure 1). 14

| Study selection criteria
We sought CPGs that addressed the population of pregnant women meeting criteria for obesity (pre-pregnancy body mass index [BMI] ≥ 30 kg/m 2 ), receiving antenatal care in either low-risk (eg, care provider = family physician or midwife) or high-risk settings (eg, obstetrician or maternal fetal medicine). Guidelines referring to pregnant women with obesity but not clearly defining obesity as a BMI of ≥30 kg/m 2 were also included. Guidelines that included pregnant women affected by obesity with medical complications (such as pre-existing diabetes or hypertension) were not excluded. No selection criteria related to interventions or outcomes were used. There were no date restrictions on the searches, but reports with full texts published in languages other than English or French were excluded. If two guidelines were identified from one source, the most recently updated guideline was selected. Studies not reporting CPGs were excluded.

| Data extraction and quality assessment
Two reviewers (A.S. and M.P.) performed single extraction, with verification of 50% of data extractions (extracted by both A.S. and M.P. and cross-checked to ensure data quality). The following data were collected from the included studies: authorship list, date of publication, journal of publication, country/language of publication, guideline objective, methodology used, type of care (family physician, midwife, obstetrician, or maternal fetal medicine), setting of care (high-or low-risk), general recommendations, and grading of the evidence.
The Appraisal of Guidelines for Research & Evaluation II tool (AGREE II) was used to assess the methodological quality of each CPG. The AGREE II scale is composed of 23 items in six domains: scope and purpose, stakeholder involvement, rigor of development, clarity of presentation, applicability, and editorial independence. Each item was scored from 1 (strongly disagree) to 7 (strongly agree). 15 Domain scores were calculated by summing up all the scores of the individual items in a domain and by scaling the total as a percentage of the maximum possible score for that domain. A detailed summary F I G U R E 1 Systematic review flow chart of these assessments was compiled and included in the summary of findings. While no firm criteria currently are in place, we considered scores of 1, 2, or 3 to correspond to a score of "not recommended," scores of 4 and 5 were considered to represent "recommended with modifications," and scores of 6 and 7 were considered to correspond to "recommended." As the AGREE-II Consortium has not set minimum domain scores or patterns of scores across domains to differentiate between high-quality or poor-quality guidelines, 15 an overall quality score of 1 to 3 was considered low quality, and therefore, the CPG was not recommended. An overall quality score of 4 or 5 was considered good quality, and the CPG was recommended with modifications. Lastly, a score of 6 or 7 was considered high quality, and the CPG was recommended.
Two raters independently completed the AGREE II appraisals.
Disagreements were identified in cases where a difference of more than 2 points within an item occurred. Consensus was reached through general discussion within the pair and involvement of a third party when necessary.

| RESULTS
A flow diagram capturing the process of study selection is presented in Figure 1. Ultimately, 252 articles underwent full text review, and 33 publications related to 32 CPGs were selected for inclusion.
Most CPGs considered obesity to be a BMI of >30 kg/m 2 or ≥30 kg/m 2 . Two guidelines did not define obesity 16,17 ; four others did not define obesity, but referred to populations with BMIs over 25 kg/m 2,18 over 30 kg/m 2,19 or ≥35 kg/m 2.20,21 Table 1  The included CPGs applied formal grading systems to assign strength of their recommendations in 12 of the 32 available CPGs (38%).There were a variety of grading systems identified in the included CPGs, including the GRADE system (three CPGs [9%]), [25][26][27] the Canadian Task Force on Preventive Health Care grading system (one CPG [3%]), 25 the US Preventative Services Task Force grading system (two CPGs [8%]), 28,29 and the Royal College of Obstetricians and Gynecologists grading system (one CPG [3%]). 30 One CPG (3%) 23 stated that a grading system was used but did not provide details.

| Overview of recommendations made by included guidelines
The following sections summarize recommendations from the included set of 32 CPGs. Table 3 presents a comprehensive visual representation of the recommendations available for the care of pregnant women with obesity.

| Recommendations for preconception care of pregnant women with obesity
It was generally suggested that women of childbearing age with obesity should receive information from health care providers about both the risks of being affected by obesity and the benefits of weight loss before pregnancy, specifically improving pregnancy outcomes for both mother and baby by reducing the risks of miscarriage, preeclampsia, and gestational diabetes mellitus (GDM). Women should be reminded that weight loss also reduces long-term health risks, including hypertension, sleep apnoea, pulmonary disease, and cardiac disease, 23,25,29,32,38,39,45 especially in women with diabetes. 41 Four CPGs also noted that women with a BMI ≥30 wishing to become pregnant should be advised to take 5 mg of folic acid supplementation daily, starting at least 1 month before conception and continuing during the first trimester of pregnancy. 30

Recommended with modifications
Note. This table presents results from the AGREE II quality assessment, comprising 23 items in six domains (scope and purpose, stakeholder involvement, rigor and development, clarity of presentation, applicability, and editorial independence). Each item was scored from 1 (strongly disagree) to 7 (strongly agree). Domain scores were calculated by summing up all the scores of the individual items in a domain and by scaling the total as a percentage of the maximum possible score for that domain.   Note. This table presents a comprehensive summary of all the recommendations available for the care of pregnant women with obesity. The numbers above each line represents the total number of clinical practice guidelines (CPGs) that included information regarding each recommendation, by the stage of pregnancy in which it was recommended. A total of 32 CPGs were included. Abbreviations: BMI, body mass index; CPGs, clinical practice guidelines; GDM, gestational diabetes mellitus; PCOS, polycystic ovary syndrome. that prior to attempting to conceive, women of childbearing age should stop taking medication for weight loss. 23 One CPG recommended that bariatric surgery could be considered to improve fertility outcomes in women with PCOS who are anovulatory, have a BMI ≥ 35 kg/m 2 , and who remain infertile despite undertaking an intensive structured lifestyle management programme involving reducing dietary energy intake, exercise, and behavioural interventions preferably for a minimum of 6 months. 22 This recommendation contradicted that of another CPG that suggested bariatric surgery should not be considered as a treatment for infertility. 28 One CPG recommended that if a woman has had bariatric surgery prepregnancy, ongoing follow-up by a dietician should be ensured. 45

| Diet and exercise during pregnancy
Thirteen of the included guidelines recommended that pregnant women with obesity be informed of the importance of controlling their weight during pregnancy. 16,18,22,23,25,30,31,[38][39][40][41]45,46 One CPG suggested the use of newer techniques (eg, text messages, reminder letters, personal, or group coaching) to reinforce dietary measures to control weight gain during pregnancy. 18 Use of the patient's BMI at first prenatal visit to provide diet and exercise counselling guided by IOM recommendations was supported. 23,25,29,30,45,46 Beginning with low-intensity exercise 29 and working towards 150 minutes per week 23 or 30 minutes per day of moderate intensity exercise 30,31 were mentioned in some CPGs, while others did not make specific recommendations for the amount of exercise, but outlined the need for it to be "regular exercise" 40 or to align with national guidelines. 45 One CPG recommended that weight loss during pregnancy should be based on medical considerations (such as co-existing diabetes or hypertension), 47  It was generally recommended that a daily dose of 5 mg of folic acid be continued until the end of the first trimester of pregnancy. Vitamin D supplementation during pregnancy was recommended by some CPGs for women who are confirmed to be vitamin D deficient. 30,38,45 One also noted that women with a BMI ≥ 35.0 kg/m 2 may be advised to take at least 75 mg of aspirin (but not more than 180 mg) daily from 12 weeks until the birth of the baby to reduce the risk of preeclampsia, provided their risk of gastrointestinal haemorrhage was considered to be low. 21 Recommendations for ultrasound assessment in the CPGs included nuchal scan between 11 weeks, 4 days, and 13 weeks, 6 days gestation for women with BMI greater than 40 kg/m 2 , assessment of early anatomy between 14 and 16 weeks gestation (to reduce the problem of impaired acoustic windows), routine morphology scan at 20 to 22 weeks gestation, and where clinical assessment is limited by obesity, growth scan at 28 to 32 weeks gestation to aid in the detection of late-onset fetal growth restriction. 38 Another CPG recommended fetal growth scans at 26 and 32 weeks for women affected by obesity with BMI greater than 40 kg/m 2.40 One CPG 29  Options/approaches for antenatal thromboprophylaxis 23,25,30 conflicted, with two CPGs 23,30 not providing any details. One CPG recommended thromboprophylaxis before Caesarean section (C-section), another suggested considering thromboprophylaxis in women with "extreme obesity" who are hospitalized prior to delivery, and another recommended consideration of thromboprophylaxis for patients with obesity, on bed rest or having surgery during the antenatal period.
Antenatal patient referral to an anaesthesiologist was recommended by four guidelines, 23,25,29,45 one of which specifically made mention of this for women with BMI greater than 40 kg/m 2.38 During that consultation, it was advised that the limitations and risks of anaesthesia during delivery be discussed.
In women with a history of bariatric surgery, the importance of good communication between the obstetrician and the bariatric surgery team was noted, as was the need for referral to a dietician and nutritional supplements over and above the usual requirements in a normal pregnancy. 23,28,38,45 One CPG noted that alternative testing for gestational diabetes be considered for those patients with a history of malabsorptive surgery, consisting of 1 week of home glucose monitoring of fasting and 2-hour postprandial blood sugars, completed between 24 and 28 weeks of gestation 28 . This CPG also noted that bariatric surgery should not be considered an indication for Caesarean delivery. 28 The importance of fetal growth monitoring during pregnancy was noted, 22,38 as was the value of maintaining a high index of suspicion for complications of bariatric surgery, which may present as common pregnancy complaints. 38

| Delivery and postpartum care
In the included CPGs, there was little guidance provided for care around timing of delivery. Only one CPG provided specific recommendations, 30 stating that in the absence of other obstetric or medical indications, obesity alone is not an indication for induction of labour and a normal birth should be encouraged.
Early establishment of venous access during labour was recommended in women with a BMI above 40. 30,45 The allowance of a longer first stage of labour prior to performing a C-section for labour arrest should be considered. 29 All women with a BMI ≥30 should have active management of the third stage of labour due to an increased risk of postpartum haemorrhage.
The majority of recommendations for delivery care related to Csection procedures. It was noted that obesity alone is not an indication for elective C-section 30,38 ; however, based upon the fact that the operative and anaesthetic risks of emergency C-section are higher for women with obesity, one CPG noted that informed discussion should be held with women regarding the mode of delivery. 45 This CPG noted that as a C-section delivery approaches, operating room staff should be alerted regarding any woman whose weight exceeds 120 kg in order to ensure that adequate staffing and equipment are available. 45 Suturing of the subcutaneous tissue space to reduce the risk of wound infection and wound separation in women with more than 2 cm of subcutaneous fat was recommended. 30 It was recommended that mechanical thromboprophylaxis using pneumatic compression devices be applied before C-section, if possible, as well as after C-section delivery and that weight-based dosing of pharmacologic options for thromboprophylaxis be considered, as such a strategy may be more effective than BMI-stratified dosage strategies in class III women with obesity after C-section. 29 One CPG recommended that behavioural interventions including diet and exercise be recommended, geared towards reduction of weight postpartum. 29,39 One guideline recommended the offering of additional support for breastfeeding, 30 while another reinforced involvement of a lactation consultant to increase supervision during breastfeeding and to provide early postpartum support. 23 Another CPG also suggested providing advice that weight loss incurred during breastfeeding through eating a healthy diet and performing regular exercise does not impact the quantity or quality of milk production. 31 4 | DISCUSSION As other studies 36

| Strengths and limitations
To our knowledge, this is the first review to identify, synthesize, and assess the CPGs available on the care of pregnant woman with obesity. Other strengths include the systematic and comprehensive literature search of guidelines by an experienced medical information specialist and the review of eligible studies by a team of reviewers.
Original study sources were neither retrieved nor evaluated in this study. It was beyond the scope of the current project to interrogate individual care elements within the CPGs, but the limited utility of vague recommendations within CPGs is highlighted. An additional drawback was the language limitation, as only English and French materials were included. As such, we may have missed beneficial information present in guidelines of other languages.
Finally, we were limited to the information present in the CPGs, which often omitted details such as optimal method and timing of antenatal surveillance.

| CONCLUSION
This study presents a systematic review of CPGs for pregnant women with obesity. The ideal management of this population remains a priority to improve both their own health and that of their future generations. Over the past decade, a number of CPGs have been developed with variation in methodologic rigor, specific objectives, and target populations. This study highlights some strong and consistent recommendations on healthy diet, exercise, and dietician referral and revealed some weaknesses regarding important aspects of care. More effort and research are needed to bridge knowledge gaps and enhance consistency in development and reporting of CPGs. The importance of CPGs targeting obesity and weight management during pregnancy is internationally apparent; however, ongoing investigations are required to ensure information detailed in these guidelines are sufficient and consistent.