According to the World Health Organization (WHO), global obesity has more than doubled between 1980 and 2014.1 In 2014 more than 1.9 billion adults, 18 years and over, were overweight with over 600 million of these being classified as obese.1 With this continuing trend it is anticipated that more than 50% of adults worldwide will be obese by 2030.2 A basic population measurement tool for obesity is body mass index (BMI) which is the weight of an individual divided by the square of their height.1 However, BMI only provides an indication of healthy body weight as it does not take into account levels of fat distribution between individuals.3 According to WHO guidelines, the recommended BMI is 18.5–24.9 kg/m2, overweight is classified as 25–29.9 kg/m2 and obese is ≥30 kg/m2.1 Obesity is further classified by BMI into Class I (30–34.9 kg/m2), Class II (35–39.9 kg/m2) and Class III or morbidly obese (BMI>40 kg/m2)1; with a final subset of the population referred to as “super-obese”,3 defined as having a BMI >50 kg/m2. Obesity may significantly reduce life expectancy due to extensive morbidities including cardiovascular disease, diabetes mellitus and hypertension; if an obese woman becomes pregnant, these co-morbidities constitute considerable complications for both patients and healthcare providers.4 In high income nations, in excess of 50% of women enter pregnancy with a BMI greater than 25 kg/m2;5-7 this statistic is alarming as obesity is considered the commonest risk factor in obstetric practice, complicating one per five pregnancies, and Class III obesity complicating up to 10% of pregnancies.8
Obesity affects pregnancy in both the prenatal and perinatal setting. Obese gravida have an increased risk of miscarriage, stillbirth, pre-eclampsia, gestational diabetes and thromboembolic disorders,9-18 as well as a higher incidence of cesarean section, anesthetic problems and wound infections.19 Infants of obese mothers are at risk of birth difficulties, macrosomia and perinatal death.9,10 Maternal obesity affects prenatal diagnosis and management of pregnancy in a significant manner. Literature16-18 has demonstrated that maternal obesity is associated with an increased risk of neural tube defect (NTD),20 with one study reporting a 1.7-fold increase with maternal obesity and a threefold increased risk of NTD with morbid obesity;21 other known fetal anomalies include: orofacial clefts, i.e. cleft lip or palate, anorectal atresia, omphalocele, diaphragmatic hernia and congenital heart defects.10,11,15-17,22 Fetal management and interventions may be required and sonography plays an essential role in prenatal diagnosis.12-14
Routine mid second trimester fetal screening ultrasound examinations, often referred to as “fetal morphology” or “fetal anomaly” scans are offered to pregnant women as part of their antenatal care and are generally performed between 18–22 weeks.8,9,11,12 Ultrasound is used to assess fetal anatomy, screening for fetal anomalies, including aneuploidy assessment to aid in the management of pregnancies.3,5,13 Detection of fetal anomalies and estimation of fetal weight in the obese gravida is a challenge for clinicians.5 Various studies have shown suboptimal visualization rates of cardiac18,23,24 and craniospinal structures ranging from 20% to 50% in obese women during the second trimester fetal anomaly scan9; in the obese pregnant woman this is a challenging examination in a number of ways. During an ultrasound examination the abdominal panniculus in the obese gravida limits visualization12 both by the actual depth of ultrasound insonation required and the increased absorption of ultrasound energy by the adipose layer, resulting in degraded image quality.3,5,8,12,25,26 The relationship between ultrasound visualization and specific BMI groups is difficult to quantify due to physical manifestations of maternal obesity.12 Women classified with Class I obesity may have no abdominal folds but have a tense hard abdomen which is difficult for ultrasound penetration.27 Conversely women with Class III obesity always have abdominal folds and it may be possible to scan through a small abdominal “window”.27 However, in a recent study, 44.1% of ultrasound scans in pregnant women with Class III obesity were deemed incomplete, compared to 10.2% in the normal BMI category.28 Ultrasound examinations of obese gravida may result in the inability to view or measure structures accurately or see some structures at all, necessitating a repeat visit. Literature9 suggests that 26% of obese gravida are recalled for a repeat scan due to suboptimal visualization or an incomplete anatomic survey with 64% of this patient subset continuing to have an incomplete or unsatisfactory repeat ultrasound examination.9 A 2009 study23 projected that for 100 obese women, an extra 33 anatomic ultrasounds were required for completion, thereby further increasing demands on healthcare systems. Due to the technical complexities associated with scanning obese gravida, additional physical and emotional demands are placed on sonographers during examinations.
Obese gravida present a myriad of issues for an ultrasound department with regards to scheduling of patients,9 allocating extra time for completion and rebooking patients for repeat examinations.29 Ergonomic issues occur with sonographers presenting with musculoskeletal workplace injuries due to scanning heavy abdominal panniculus.30-32 There are also the associated stresses with dealing with obese gravida who exhibit maternal anxiety because of equivocal ultrasound findings and the need for repeat examinations,33 especially if there is an increased maternal background risk for aneuploidy.13
The sonographic inability to exclude “soft” markers for aneuploidy in obese gravida results in management and counseling issues for obese patients regarding their likelihood ratios for major fetal abnormalities.13 The FaSTER trial15 found that maternal obesity decreased the sensitivity of particular aneuploidy soft markers11 (short femur, short humerus and pyelectasis) while others (nuchal fold, echogenic bowel and echogenic intracardiac focus) were not altered.11 Also, the missed diagnosis rates were higher in obese women, for example, with the “nuchal fold” marker the missed diagnosis rate for obese women was 51% compared with 39% in normal-weight women.11
It is well documented that maternal obesity has a detrimental effect on ultrasound image quality, thereby decreasing adequate visualisation of fetal structures.3,8,9,12 This continues to be problematic as prenatal counseling and/or early intervention is hampered by lack of detection of fetal anomalies.34 The aim of this review is to examine the impact of obesity in regards to second trimester sonography during pregnancy. This is to enable evidence to be synthesized to inform practice guidelines for sonographic scanning of obese gravida with regard to visualization and timing of examinations. The review will also provide important information for both healthcare providers and patients to consider with regard to counseling obese pregnant patients about the realistic expectations of ultrasound examinations, fetal management and interventions, including possible pregnancy termination, which is subjected to rigorous government regulation. Whilst systematic reviews exist regarding first trimester ultrasound accuracy of fetal anomalies,35-37 a search in the Cochrane Database of Systematic Reviews and the JBI Database of Systematic Reviews and Implementation Reports did not reveal any previous systematic reviews specific to this topic.
This review will consider studies that include pregnant women, including obese gravida (BMI of at least 30 kg/m2), with a confirmed singleton pregnancy (regardless of age), both primiparas and multiparas, regardless of education, pregnancy status (natural or assisted reproduction), race, culture and ethnicity, who have undergone a mid-second trimester ultrasound examination (including 3D/4D if appropriate) generally between 18–22 weeks of gestation. Studies will not be considered if they refer to multiple pregnancies, known fetal chromosomal or teratogenic anomalies, or do not include the use of ultrasound as an imaging modality.
This review will consider studies that include the use of ultrasound as a diagnostic imaging tool for mid-second trimester obstetric screening examinations in women who are obese (BMI of at least 30 kg/m2).
The WHO uses BMI as an index of weight for height.1 Body mass index is commonly used to classify levels of obesity and is categorized under the following range:
- Normal weight: less than 25 kg/m2
- Overweight: 25–29.9 kg/m2
- Obese: 30–39.9 kg/m2
- Morbidly obese: at least 40 kg/m2
The review will categorize obesity as a BMI of at least 30 kg/m2
This review will include studies that compare obese women (and the varying classes of obesity) to normal weight women (BMI 18.5–24.9 kg/m2). The presence of comparative data (i.e. obese versus normal weight) is not a requirement for inclusion.
This review will consider studies that address outcomes related to the completion of a mid-second trimester fetal morphology scan which adheres to recognized practice parameters or guidelines including, but not limited to: American Institute of Ultrasound in Medicine (AIUM),38 International Society of Ultrasound in Obstetrics and Gynecology (ISUOG),39 Australasian Society for Ultrasound in Medicine (ASUM),40 National Institute for Health and Care Excellence, Antenatal Care Guidelines,41 British Medical Ultrasound Society,42 Royal Australian and New Zealand College of Obstetricians and Gynaecologists (RANZCOG),43 and Royal College of Obstetricians and Gynaecologists (RCOG) incorporating specialist society: British Maternal and Fetal Medicine Society (BMFMS) and the Society and College of Radiographers, and Public Health England.44
Adherence to guidelines will be measured using the following outcomes and related measurements:
- Number and type of anatomical structures not adequately visualized – detection rates (using terms such as visualized, suboptimal visualization, not visualized, abnormal) will be reported by percentage, gestational age at time of scan, and grouped into body regions, for example, head, face, cardiac, chest, abdomen, genitourinary, spine and extremities; data will also be grouped into obesity levels as per WHO definitions where appropriate.
- Delayed or missed diagnosis of fetal abnormalities such as brain, face, spine and cardiac anomalies – rates will be reported by percentage, gestational age and body region, and grouped into obesity levels where appropriate.
- Limitation of ultrasound in the evaluation of “soft markers” for aneuploidy – detection rates (using terms such as visualized, suboptimal visualization, not visualized, abnormal) will be reported by percentage, gestational age and categorized as: shortened femur, shortened humerus, pyelectasis, nuchal fold, echogenic bowel, choroid plexus cysts, 3 vessel cord, and echogenic intracardiac focus.
- Repeat examinations – measured by number of repeat visits to complete examination.
- Length of examination – rates will be reported by number of minutes.
Types of studies
This review will primarily consider experimental study designs including randomized and pseudo-randomized controlled trials. This review will also consider other study designs including non-randomized controlled trials, quasi-experimental, before and after studies, prospective and retrospective cohort studies, case-control studies, and analytical cross-sectional studies for inclusion.
The search strategy aims to find both published and unpublished studies. A three-step search strategy will be utilized in this review. An initial limited search of PubMed and CINAHL will be undertaken followed by an analysis of the text words contained in the title and abstract, and of the index terms used to describe the article. Initial keywords to be used will be: maternal obesity, congenital abnormalities, obstetric ultrasound, second trimester, anomaly scan, fetal ultrasound, prenatal sonography, fetal anomaly, fetal malformation, aneuploidy.
A second search using all identified keywords and index terms will then be undertaken across all included databases. Thirdly, the reference list of all identified reports and articles will be searched for additional studies.45 Due to time limits all studies identified and published in English will be considered for inclusion in this review. Studies published after 1995 (due to technological ultrasound advances including tissue harmonic imaging) will be considered for inclusion in this review.
The databases to be searched include: PubMed, CINAHL, EMBASE, Web of Science and Scopus.
The search for unpublished studies will include: MedNar, OpenGrey, ProQuest Theses and Dissertations, and Libraries Australia.
The full database search planned for PubMed is detailed in Appendix I.
Following the search, all identified citations will be collated and uploaded into Endnote (Clarivate Analytics, PA, USA) and duplicates removed. Titles and abstracts will then be screened for assessment against the inclusion and exclusion criteria for the review by two reviewers to ensure transparency and reduce the possibility of rejecting relevant papers. In addition, an initial pilot phase, using screening forms based on the eligibility criteria, will be used to screen a small number of studies to ensure consistency of interpretation of inclusion criteria.46 Studies that meet the inclusion criteria will be retrieved in full and their details imported into Joanna Briggs Institute System for the Unified Management, Assessment and Review of Information (JBI SUMARI). The full text of selected studies will be retrieved and assessed in detail against the inclusion criteria; these will be reviewed independently by two authors. Full text studies that do not meet the inclusion criteria will be excluded and reasons for exclusion will be provided in an appendix in the final systematic review report. Included studies will undergo a process of critical appraisal. The results of the search will be reported in full in the final report and presented in a PRISMA flow diagram.47
Assessment of methodological quality
Studies selected for retrieval will be assessed by two independent reviewers for methodological validity prior to inclusion in the review using the predefined standardized critical appraisal instruments from JBI.48-53 An appropriate critical appraisal tool will be selected based on the type of study being analysed such as: randomized controlled trials, case-control studies, cohort studies, quasi-experimental studies, and analytical cross-sectional studies.48-53 An initial “pilot” test of a small number of studies will be performed to ensure appraisal criteria congruence between reviewers. Any disagreements that arise will be resolved through discussion, or with a third reviewer.46 All studies, regardless of the results of the methodological quality assessment, will be included in this review.
Data will be extracted from papers included in the review, by two reviewers, using the standardized data extraction tools in JBI SUMARI and an excel spreadsheet.54 The data extracted will include study characteristics (author, country, study type), aim/objective of study, setting (e.g. hospital or specialist practice), healthcare providers involved (profession e.g. sonographer and/or obstetrician), equipment type (e.g. high end or low end), stated BMI and whether this is self-reported or clinically measured, actual week of scan (e.g. 18 weeks, 20 weeks, 22 weeks) and author's conclusion. Additional details to be extracted regarding the exposure of interest will include: gestational age, sonographic levels of visualization of anatomical components stratified into BMI categories (e.g. head, face, cardiac, chest, abdomen, genitourinary, spine, and extremities categorized into normal BMI 18.5–24.9 kg/m2, overweight 25–29.9 kg/m2 obese ≥30 kg/m2. Obesity will further classified by BMI into Class I (30–34.9 kg/m2), Class II (35–39.9 kg/m2) and Class III or morbidly obese (BMI>40 kg/m2), delayed or missed diagnosis of any fetal anomalies described via the BMI categories as above, type of sonographic examination performed (e.g. standard versus detailed), and examination details (length of examination and repeat examinations). Any disagreements that arise between the reviewers will be resolved through discussion, or with a third reviewer. Authors of papers will be contacted to request missing or additional data where required. If authors do not provide information and data cannot be clearly separated into overweight and obese groups, we will include data where it is clear that 70% of the group were in fact obese (BMI over 30).
Papers will, where possible, be pooled in statistical meta-analysis using JBI SUMARI or OpenMeta-Analyst55 for head-to-head comparative data. Effect sizes will be expressed as either odds ratios for dichotomous data and weighted (or standardized) mean differences for continuous data and their 95% confidence intervals will be calculated for analysis. The model for meta-analysis will depend on the amount of studies contributing data to the analysis.56 Heterogeneity will be assessed statistically using the standard chi-squared and I squared tests and also explored using subgroup analysis based on the different study designs included in this review.56 For single group data, proportional meta-analysis will be conducted where results have been presented as proportions (outcome/sample) and weighted means for continuous data. Subgroups will be implemented to ensure judicious data synthesis and knowledge translation from this review. Examples of likely subgroups may be fetal body regions not visualized (such as head, face, cardiac, chest, abdomen, genitourinary, spine and extremities), fetal body region abnormalities (such as head, face, cardiac, chest, abdomen, genitourinary, spine and extremities) and BMI categories (normal BMI 18.5–24.9 kg/m2, overweight 25–29.9 kg/m2 obese ≥30 kg/m2. Obesity will further classified by BMI into Class I (30–34.9 kg/m2), Class II (35–39.9 kg/m2) and Class III or morbidly obese (BMI>40 kg/m2). Further subgroups may include equipment type (e.g. high end or low end), stated BMI and whether this is self-reported or clinically measured, and actual week of scan (e.g. 18 weeks, 20 weeks, 22 weeks) Where statistical pooling is not possible, the findings will be presented in narrative form including tables and figures to aid in data presentation where appropriate.
A funnel plot will be generated to assess publication bias if there are 10 or more studies included in a meta-analysis. Statistical tests for funnel plot asymmetry (Egger test, Begg test, Harbord test) will be performed where appropriate.57
Assessing certainty in the findings
A Summary of Findings table will be created using GRADEPro GDT software. The Grading of Recommendations Assessment, Development and Evaluation (GRADE) approach, via The GRADE Handbook,58 for grading the quality of evidence will be followed. The Summary of Findings table will present the following information where appropriate: absolute risks for obesity and normal (if possible), estimates of relative risk, and a ranking of the quality of the evidence based on study limitations (risk of bias), indirectness, inconsistency, imprecision and publication bias.
The following patient important outcomes will be included in the Summary of Findings table:
- Fetal anatomy not adequately seen at second trimester morphology scan.
- Delayed or missed diagnosis of fetal abnormalities at second trimester morphology scan.
- Limitations of second trimester morphology scanning for ‘soft markers’ for aneuploidy in obese pregnant women.
- Repeat examinations.
- Length of scans.
The authors would like to acknowledge Maureen Bell, Research Librarian, The University of Adelaide, for her invaluable contribution in assisting with refining the database searches.
This systematic review contributes towards the degree award of Master of Clinical Science for CP.
Appendix I: Search strategy for PubMed
(obesity[mh] OR obese[tiab] OR obesity[tiab]) OR body mass index[mh] OR body mass index[tiab] OR “maternal obesity” [tiab] OR “obese gravida”[tiab])
(Ultrasonography, Prenatal[mh] OR Diagnostic imaging[mh] OR fetus/diagnostic imaging OR ultrasound[tiab] OR ultrasonog*[tiab] OR scan*[tiab] OR screen*[tiab]) AND (fetal[tiab] OR foetal[tiab] OR prenatal[tiab] OR Congenital abnormalities [mh] OR congenital defects[tiab] OR fetal abnormalities[tiab] OR foetal abnormalities[tiab] OR fetal anatomy[tiab] or foetal anatomy[tiab] OR fetal anomaly[tiab] OR foetal anomaly[tiab] OR aneuploidy[tiab] OR fetal malformation[tiab] OR foetal malformation[tiab])
(pregnancy[mh:noexp] OR (pregnancy, second trimester[mh] OR second trimester*[tiab] OR morphology[tiab])
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