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Please cite this paper as: Best K, Tennant P, Bell R, Rankin J. Impact of maternal body mass index on the antenatal detection of congenital anomalies. BJOG 2012;119:1503–1511.
Objective To investigate the association between maternal body mass index (BMI) and antenatal ultrasound detection of congenital anomalies.
Design Population-based register study.
Setting North of England (UK).
Population All pregnancies (n = 3096) associated with a congenital anomaly notified to the Northern Congenital Abnormality Survey (NorCAS) during 2006–2009. Cases with chromosomal and teratogenic anomalies (n = 611) or without information on antenatal scanning (n = 4) were excluded.
Methods Adjusted odds ratios (aORs) and 95% confidence intervals (CIs) for antenatal detection according to maternal BMI categories were estimated using logistic regression.
Main outcome measures For all anomalies combined, cases were defined as ‘detected’ if any congenital anomaly was suspected antenatally. Organ system-specific anomalies were defined as detected if an anomaly of the correct system was suspected.
Results Antenatal detection of any anomaly occurred in 1146 of 2483 (46.2%) cases with normal karyotype. The odds of detection were significantly decreased in obese (BMI ≥ 30 kg/m2) women compared with women of recommended BMI (18.5–24.9 kg/m2; aOR, 0.77; 95% CI, 0.60–0.99; P = 0.046). Cardiovascular system anomalies were suspected antenatally in 109 of 945 (11.5%) cases. The odds of detecting a cardiovascular anomaly were significantly greater in underweight women (BMI < 18.5 kg/m2) than in women of recommended BMI (aOR, 2.95; 95% CI, 1.13–7.70; P = 0.027). There was no association between BMI and detection in any other organ system or between BMI and termination of pregnancy for fetal anomaly.
Conclusions Antenatal ultrasound detection of a congenital anomaly is decreased in obese pregnant women. This has implications for the scanning and counselling of obese women.
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The proportion of overweight and obese women of childbearing age is increasing, with first-trimester obesity [body mass index (BMI) ≥ 30 kg/m2] more than doubling from 7.6% in 1989 to 15.6% in 2007 in England.1 This has implications for the prevalence of congenital anomalies, some of which occur more frequently in overweight (BMI = 25–29.9 kg/m2) and obese pregnant women.2,3
Antenatal detection of congenital anomalies gives the opportunity to prepare parents for the birth of a child with a congenital anomaly, to plan postnatal management or to consider termination of pregnancy. However, between 2005 and 2009, antenatal diagnosis occurred in only 47% of nonchromosomal cases notified to UK congenital anomaly registers.4
Evidence suggests that the sensitivity of antenatal ultrasound detection of congenital anomalies is further reduced with increasing BMI.5,6 Dashe et al.6 found a decreasing trend in ultrasound detection rates for congenital anomaly as BMI at the first antenatal visit increased. Similarly, Tabor et al.5 found that women with a BMI > 25 kg/m2 had a significantly lower detection rate than women with a BMI ≤ 25 kg/m2. Although both were large cohort studies, they only included 181 and 100 cases of congenital anomaly respectively, and neither investigated trends in specific anomaly groups.
Several studies have found associations between increased maternal BMI and suboptimal visualisation of the fetus.7–12 Visualisation of cardiac structures12,13 and soft tissues12 has been shown to be particularly impaired with increasing BMI. This association may partly explain the increased prevalence of congenital anomalies at birth in overweight and obese women,2 if a lower proportion are detected antenatally and, subsequently, fewer cases result in the termination of pregnancy, but this hypothesis has not been investigated.
This study investigated the association between maternal BMI and the antenatal ultrasound detection of congenital anomalies and between maternal BMI and pregnancy outcome in a population-based case series from the north of England.
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There were 3096 cases of congenital anomaly confirmed postnatally among 132 885 pregnancies during the four-year study period, giving a total prevalence of 23.3 (95% CI: 22.5–24.1) per 1000 live and stillbirths. There were 597 (19.3%) cases associated with chromosomal anomalies and 14 (0.5%) associated with a teratogenic syndrome excluded from further analysis. Two cases that were not antenatally scanned and two with missing information on whether or not they were antenatally scanned were also excluded.
Of the remaining 2483 cases, 40 (1.6%) occurred in women with pre-gestational diabetes, 128 (5.2%) in twin pregnancies and three in separate triplet pregnancies. Other summary statistics are shown in Table 1.
Table 1. Demographic statistics by antenatally suspected and unsuspected congenital anomalies*
|Variable||All cases, n (%)||Undetected cases, n (%)||Detected cases, n (%)|| P |
| BMI (kg/m2) |
|Underweight (<18.5)||67 (2.7)||27 (40.3)||40 (59.7)||0.007μ****|
|Recommended weight (18.5–24.9)||793 (31.9)||376 (47.4)||417 (52.6)|
|Overweight (25–29.9)||468 (18.9)||243 (51.9)||225 (48.1)|
|Obese (≥30)||358 (14.4)||194 (54.2)||164 (45.8)|
|Missing||797 (32.1)||497 (61.4)||300 (37.6)|
| Maternal age at delivery (years)|
|<20||267 (10.8)||125 (46.8)||142 (53.2)||<0.001****|
|20–34||1820 (73.3)||956 (52.5)||864 (47.5)|
|≥35||383 (15.4)||244 (63.7)||139 (36.3)|
|Missing||13 (0.5)||12 (92.3)||1 (7.69)|
| Index of Multiple Deprivation |
|Least deprived||773 (31.1)||435 (56.3)||338 (43.7)||0.078****|
|Moderate||844 (34.0)||461 (54.6)||383 (45.34)|
|Most deprived||863 (34.8)||439 (50.9)||424 (49.1)|
|Missing||1 (0.1)||2 (66.7)||1 (33.3)|
| Pre-gestational diabetes*** |
|Yes||40 (1.6)||20 (50.0)||20 (50.0)||0.623|
|No||2443 (98.4)||1317 (53.9)||1126 (46.1)|
| Multiple pregnancy*** |
|Yes||131 (5.3)||53 (40.5)||78 (59.5)||0.002|
|No||2352 (94.7)||1284 (54.6)||1068 (45.3)|
| Birth outcomes*** |
|Late miscarriage||30 (1.2)||14 (46.7)||16 (53.3)||<0.001|
|Termination of pregnancy||361 (14.5)||0||360 (100.0)|
|Antepartum stillbirth||35 (1.4)||9 (25.7)||26 (74.3)|
|Intrapartum stillbirth||2 (0.1)||0 (0)||2 (100.0)|
|Early neonatal death||47 (1.9)||11 (23.4)||36 (76.6)|
|Late neonatal death||26 (1.1)||14 (53.9)||12 (46.2)|
|Post-neonatal death||38 (1.5)||19 (50.0)||19 (50.0)|
|Live birth||1940 (78.1)||1270 (65.5)||670 (34.5)|
|Missing||4 (0.1)||0||4 (100.0)|
| Sex*** |
|Male||1304||705 (54.1)||599 (45.9)||0.470|
|Female||1131||628 (55.5)||503 (44.5)|
|Unknown||48||4 (8.3)||44 (91.7)|
| Year of delivery |
|2006||648 (26.1)||358 (55.3)||290 (44.8)||0.718****|
|2007||620 (25.0)||337 (54.4)||283 (45.7)|
|2008||650 (26.2)||350 (53.5)||301 (46.5)|
|2009||565 (22.8)||297 (52.0)||271 (48.0)|
| Gestational age at delivery** , ***** (weeks) ||38 (35–40)||39 (37–40)||36 (21–39)||<0.001|
| Gestation at booking** , ***** (weeks) ||9 (8–12)||9 (7–12)||10 (8–12)||0.201|
| Gestation at diagnosis of anomaly**,***** (weeks) ||20 (18–22)||N/A||20 (18–22)|| N/A|
Cardiovascular anomalies were the most common congenital anomaly group notified to NorCAS (945 cases; 38.1%; Table S1), but were the least commonly suspected antenatally (11.5%; Table S1). Urinary anomalies, nervous system anomalies, orofacial clefts and digestive system anomalies were specifically suspected antenatally in 88.4, 84.7, 44.4 and 35.1% of cases, respectively (Table S1).
Excluding women with missing maternal BMI, 67 (4.0%) anomalies occurred in women who were underweight, 793 (47.0%) in women who were of recommended BMI, 468 (27.8%) in women who were overweight and 358 (21.2%) in women who were obese (Table 1). An anomaly of any system was detected antenatally in 40 (59.7%), 417 (52.6%), 225 (48.1%) and 164 (45.8%) cases in women who were underweight, of recommended BMI, overweight and obese, respectively (Figure 1). Detection rates decreased significantly with increasing BMI category (test for trend: P = 0.007). Cases in women with missing BMI were significantly less likely to have been detected antenatally (300/797 = 37.6%) than those in women with a recorded BMI (846/1686 = 50.2%; test of proportions: P < 0.001). There was no evidence of a difference in the distribution of gestational age at final antenatal detection of anomaly or gestational age at first antenatal visit across BMI categories (Kruskal–Wallis test: P = 0.688 and P = 0.430, respectively).
Figure 1. Trends in the percentage of suspected cases and the percentage of cases ending in termination of pregnancy across body mass index (BMI) categories (chromosomal and teratogenic syndromes were excluded). P values calculated using Cuzick’s test for trend.
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The odds of detection of an anomaly (in any system) were significantly lower in obese women than in women of recommended BMI (aOR = 0.77; 95% CI: 0.60–0.99; P = 0.046; Table 2). There were no significant differences in the odds of detection in underweight (P = 0.414) or overweight (P = 0.157) women compared with women of recommended BMI. Increasing maternal age was significantly associated with decreasing odds of antenatal detection (aOR = 0.97; 95% CI: 0.96–0.99; P < 0.001). The odds of detection were also increased in women with multiple pregnancies (aOR = 1.55; 95% CI: 1.06–2.26; P = 0.024). There were no significant associations with IMD (P = 0.889 and P = 0.698 for least and most deprived, respectively) or pre-gestational diabetes (P = 0.766).
Table 2. Association between maternal body mass index (BMI) and the odds of antenatal detection of congenital anomaly (overall and in most common anomaly groups*), as estimated by logistic regression
|Postnatal diagnosis||BMI category**||Total, n (%)||Detected antenatally***, n (% in BMI category)||Unadjusted||Adjusted****|
|OR (95% CI)|| P ||aOR (95% CI)|| P |
|Any congenital anomaly||Underweight||67 (2.7)||40 (59.7)||1.34 (0.80–2.22)||0.264||1.24 (0.74–2.06)||0.414|
|Recommended||793 (31.9)||417 (52.6)||1 (Reference)||–||1 (Reference)|| |
|Overweight||468 (18.9)||225 (48.1)||0.83 (0.66–1.05)||0.122||0.85 (0.67–1.07)||0.157|
|Obese||358 (14.4)||164 (45.8)||0.76 (0.59–0.98)||0.034||0.77 (0.60–0.99)||0.046|
|Missing||797 (32.1)||300 (37.6)|| || || || |
|Cardiovascular anomaly||Underweight||25 (2.7)||7 (28.0)||2.56 (1.00–6.56)||0.050||2.95 (1.13–7.70)||0.027|
|Recommended||273 (28.9)||36 (13.2)||1 (Reference)||–||1 (Reference)|| |
|Overweight||177 (18.7)||27 (15.3)||1.19 (0.69. 2.03)||0.537||1.18 (0.68–2.04)||0.557|
|Obese||144 (15.2)||18 (12.5)||0.94 (0.51–1.72)||0.843||0.84 (0.45–1.56)||0.575|
|Missing||326 (34.5)||21 (6.4)|| || || || |
|Urinary system anomaly||Underweight||7 (2.3)||7 (100.0)||–||–||–|| |
|Recommended||112 (37.1)||103 (92.0)||1 (Reference)||–||1 (Reference)|| |
|Overweight||61 (20.2)||52 (85.3)||0.57 (0.22–1.48)||0.246||0.58 (0.22–1.56)||0.284|
|Obese||37 (12.3)||34 (91.9)||0.81 (0.24–2.75)||0.734||0.84 (0.24–2.96)||0.815|
|Missing||84 (28.2)||73 (85.9)|| || || || |
|Nervous system anomaly||Underweight||8 (3.1)||8 (100.0)||–||–||–|| |
|Recommended||93 (35.5)||85 (91.4)||1 (Reference)||–||1 (Reference)|| |
|Overweight||51 (19.5)||45 (88.2)||1.01 (0.35–2.90)||0.991||1.06 (0.36–3.14)||0.914|
|Obese||41 (15.7)||38 (92.7)||1.24 (0.37–4.15)||0.726||1.47 (0.43–5.07)||0.540|
|Missing||69 (26.3)||51 (73.9)|| || || || |
|Orofacial cleft||Underweight||3 (2.1)||0 (0.0)||–||–||–|| |
|Recommended||58 (40.9)||30 (51.7)||1 (Reference)||–||1 (Reference)|| |
|Overweight||32 (22.5)||15 (46.9)||0.88 (0.37–2.09)||0.777||0.92 (0.38–2.20)||0.846|
|Obese||17 (12.0)||9 (52.9)||0.89 (0.30–2.62)||0.831||0.68 (0.21–2.16)||0.508|
|Missing||32 (22.5)||11 (34.4)|| || || || |
|Digestive system anomaly||Underweight||5 (4.5)||3 (60.0)||1.62 (0.23–11.26)||0.628||1.95 (0.26–14.86)||0.519|
|Recommended||27 (28.8)||13 (48.2)||1 (Reference)||–||1 (Reference)|| |
|Overweight||13 (11.7)||4 (30.8)||0.48 (0.12–1.94)||0.302||0.59 (0.13–2.74)||0.503|
|Obese||17 (15.3)||7 (41.2)||0.75 (0.22–2.57)||0.651||0.67 (0.17–2.61)||0.564|
|Missing||49 (44.1)||13 (26.5)|| || || || |
There was no evidence that the influence of BMI on the odds of antenatal detection was significantly different in multiple relative to singleton pregnancies or in women with pre-gestational diabetes relative to those without. One significant interaction was observed between overweight BMI and maternal age (P = 0.017). In women aged 35 years or more, the odds of an anomaly being detected antenatally was significantly lower in overweight women (aOR = 0.46; 95% CI: 0.25–0.84; P = 0.012) than in women of recommended BMI. No such effect was observed in women under the age of 35 years (overweight versus recommended BMI: aOR = 0.95; 95% CI: 0.74–1.22; P = 0.663).
Of the cases that were confirmed postnatally as having isolated cardiovascular anomalies, there was an approximate three-fold increased odds of detecting a cardiovascular anomaly in underweight women than in women of recommended BMI (aOR = 2.95; 95% CI: 1.13–7.70; P = 0.027; Table 2). There were no significant differences in the antenatal detection of cardiovascular anomalies in overweight and obese women compared with women of recommended BMI (Table 2).
There were no significant associations between BMI (of any category) and antenatal detection of congenital anomalies in any other organ system (the most commonly affected organ systems are shown in Table 2).
Overall, 361 (14.5%) of all cases ended in termination of pregnancy, with seven (10.5%), 134 (17.0%), 84 (18.0%) and 56 (15.7%) cases occurring in underweight, recommended BMI, overweight and obese women, respectively (Figure 1). There was no trend in termination of pregnancy rates over increasing BMI categories (test for trend: P = 0.835). Of those cases that were suspected antenatally, 17.5, 32.4, 37.3 and 34.4% ended in a termination of pregnancy in underweight, recommended BMI, overweight and obese women, respectively (test for trend: P = 0.112). After adjusting for maternal age, IMD, diabetes and multiple pregnancies, there was no significant association between termination and BMI (logistic regression: P = 0.075, P = 0.182 and P = 0.431 in underweight, overweight and obese women, respectively). There was no association with IMD (P = 0.335 and P = 0.081 for least and most deprived, respectively) or diabetes (P = 0.408), but there was some evidence that the odds of termination decreased with increasing maternal age (aOR = 0.98; 95% CI: 0.96–1.00; P = 0.051) and in multiple relative to singleton pregnancies (aOR = 0.43; 95% CI: 0.23–0.80; P = 0.008).
Termination of pregnancy occurred in 28 (3.0%) confirmed cases of cardiovascular anomaly. There was no association between BMI categories and termination of pregnancy among cardiovascular cases (P = 0.876 and P = 0.201 for overweight and obese women, respectively).
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This study found a significant decreasing trend in the antenatal ultrasound detection of congenital anomalies across all BMI categories. In addition, there was a significantly increased odds of detecting an anomaly of the cardiovascular system in underweight women relative to women of recommended BMI. There was no significant association between BMI and antenatal detection of congenital anomalies in any other organ system, or between BMI and termination of pregnancy for fetal anomaly.
This study is the largest to examine the effect of maternal BMI on the antenatal detection of congenital anomalies. The primary strength of the study is that information on cases was extracted from a high-quality, population-based congenital anomaly register. Consistent methods of identifying and notifying cases are used to ensure a high case ascertainment. In addition, NorCAS is an active register that follows cases to age 12 years to maximise ascertainment of anomalies, such as those of the cardiovascular system, which may not be diagnosed until well into childhood. NorCAS records data on up to six congenital anomalies per case; thus, we were able to classify each case as isolated, associated or chromosomal, and to examine antenatal detection rates by organ system, which has not been performed previously.
NorCAS is held within the same database as two other high-quality population-based registers (NorDIP and NorSTAMP). As records are linked as cases are notified, we were able to accurately identify cases occurring in women with pre-gestational diabetes or multiple pregnancies. Therefore, we could adjust for these potentially confounding factors, which are both associated with an increased risk of congenital anomaly18,19 and increased antenatal surveillance.20,21
The study has some limitations. The maternal BMI data recorded at the first antenatal visit were mostly derived from self-reported height and weight. It has been suggested that around 20% of women underreport their weight at first attendance for antenatal care, leading to an underestimation of their BMI.2 Moreover, almost one-third of the BMI data were missing. Despite our best efforts to obtain these data, they were not recorded in the study years. Cases in women with missing BMI data were less likely to have been detected antenatally than those in women who had a BMI recorded. If overweight or obese women account for a higher proportion of the missing data, the strength of our association may be an underestimate.
Although we were able to account for pregnancies associated with pre-gestational diabetes, we could not account for those associated with gestational diabetes. Mothers with gestational diabetes are more likely to be overweight or obese22 and, because of the higher risks associated with their pregnancy, may receive additional antenatal scans. Thus, we may have underreported the size of the true association between antenatal detection and obesity.
The second-trimester ultrasound may have been too early to detect certain nervous system anomalies, such as posterior fossa or agenesis of the corpus callosum, which are not usually detectable until a later gestational age. However, a large proportion of nervous system anomalies were suspected antenatally (84.7%), and so this would not have had a major impact on the results.
As the purpose of the study was to investigate the sensitivity of routine antenatal ultrasound scanning to detect congenital anomalies, we excluded chromosomal anomalies. We could not distinguish between those anomalies identified via ultrasound examination and those detected by other means (e.g. genetic testing). Therefore, this study cannot describe the association between BMI and the odds of antenatal detection in this group of anomalies.
In addition, we could not adjust the logistic regression models for gestational age at scanning. Although gestational age at final antenatal diagnosis is recorded, this may correspond to a scan subsequent to that which caused the initial suspicion. Furthermore, this variable has a high proportion of missing values. Evidence suggests that scans occurring at later gestational ages may lead to better visualisation of the fetus,7,13 although not all studies support this finding.5,8 Nevertheless, we examined gestational age at final antenatal diagnosis, and at first antenatal visit, and found no significant difference across BMI categories, which suggests that the association between BMI and the odds of detection is not related to differences in gestational age at the time of the scan.
Considering all congenital anomalies, we found similar antenatal detection rates to those described by EUROCAT in the UK.4 However, we identified significantly lower detection rates of cardiovascular anomalies than did Boyd et al.23 in 2005–2006 in England and Wales. However, the study by Boyd et al.23 only included serious cardiac anomalies (defined as common arterial trunk, discordant ventriculoarterial connection, transposition of the great vessels, tetralogy of Fallot, Ebstein’s anomaly or coarctation of the aorta) that were amenable to detection, whereas we investigated all EUROCAT-defined major anomalies of the cardiovascular system.14 Garne et al.24 reported cardiovascular detection rates of 25% in Europe and 35% in England, which are slightly more consistent with ours, but this was an older study and detection rates may have since improved.
Apart from the cardiovascular system, there were a limited number of anomalies from other individual organ systems. As a result, this study may have been underpowered to detect associations between maternal BMI and the antenatal detection of anomalies within other organ systems. Nonsignificant associations should therefore not be interpreted as evidence of no effect. Further studies are needed with larger sample sizes.
Few studies have investigated the association between maternal BMI and the detection of congenital anomalies, but those that have, show consistent findings to those reported here. In low-risk pregnancies, Dashe et al.6 identified a negative trend in the rates of detection as BMI increased, with rates of 66 and 48% in normal (BMI < 25 kg/m2) and class 1 obese (BMI = 30–34.9 kg/m2) women, respectively. These detection rates are higher than ours, possibly because the authors excluded cases associated with atrial septal defect, a cardiovascular anomaly which is difficult to detect antenatally [e.g. in our study, 2.9% (1/35) of isolated atrial septal defects were suspected antenatally]. In addition, Dashe et al.6 only recorded cases if they were diagnosed before hospital discharge or if they occurred in neonatal deaths, whereas NorCAS can receive notification of a case up to age 12 years. Similarly, Tabor et al.5 identified a difference in detection rates between women with BMI ≤ 25 kg/m2 and BMI > 25 kg/m2 (76.4 and 53.3%, respectively). These detection rates may also appear to be higher than in our study because of a more modest BMI categorisation and because the length of follow-up was shorter than ours (median of 22 months). Neither of these studies performed regression analyses, and so we cannot compare the adjusted odds of detection.5,6 A number of other studies showing greater suboptimal visualisation for increasing BMI7–10,12,25 also complement our findings.
In our study, obese BMI was not significantly associated with antenatal detection of cardiovascular anomalies. This contrasts with the studies by Hendler et al.7 and Khoury et al.,12 who both identified greater suboptimal visualisation of the fetal heart in obese women than in women of recommended BMI. This discrepancy may have occurred because of low study power. Although we found an overall effect in obese women, and cardiovascular anomalies were the largest congenital anomaly group, they also had the lowest rate of detection (11.5%), and therefore very few antenatally detected cases (n = 88). Hence, although our study had sufficient power to detect a large effect size for cardiovascular anomalies (as observed with underweight women), it may not have had sufficient power for a moderate effect, which potentially exists for obese women. To our knowledge, this is the first study to investigate the effect of maternal underweight on the ultrasound detection of congenital anomalies. We found an increased rate of antenatal detection in underweight women, which suggests that ultrasound visibility decreases continuously over all BMI categories.
Although obese women were less likely to have an anomaly suspected antenatally, they were not significantly less likely to have a termination of pregnancy, compared with women of recommended BMI. Termination of pregnancy was a relatively rare outcome and the effect of obesity on antenatal detection was moderate, and so it is possible that we did not have the power to identify a small effect. However, a recent systematic review found no evidence to support this, as the association between congenital anomaly and maternal obesity was similar irrespective of whether terminations of pregnancy for fetal anomaly were included.3 Thus, antenatal scanning for congenital anomalies is less effective as BMI increases, resulting in fewer cases detected antenatally, but this study provides no evidence that this has an impact on termination of pregnancy for fetal anomaly.
We found that cases occurring in a multiple pregnancy were more likely to be detected than cases occurring in a singleton pregnancy. Congenital anomalies may be more frequently suspected in multiple pregnancies because more scans are offered to these women or, potentially, more experienced sonographers might scan these women.21 Further research is required to investigate this association. There was no evidence that the effect of BMI on antenatal detection was different among multiple relative to singleton pregnancies, and so it was feasible to incorporate and adjust for multiple pregnancies in our analysis.
As the amount of abdominal adipose tissue increases, the depth travelled by the ultrasound waves during the mid-trimester scan becomes greater.25 Therefore, more waves are absorbed into the surrounding tissue, which causes the signal to weaken and, as a result, visualisation of the fetus and therefore any congenital anomalies diminishes.25 If BMI is considered as a marker for abdominal adipose tissue, this would explain why detection decreases over all BMI categories, and is not impaired in obese women alone. Furthermore, this might explain why we identified an interaction between overweight BMI and maternal age, if the older overweight mothers had more abdominal adipose tissue than their younger counterparts with the same BMI, as has been reported previously.26,27
The National Institute for Health and Clinical Excellence (NICE) suggests that pregnant women should be informed that antenatal detection rates may vary by maternal BMI.28 Recommendations should be directed to improving ultrasound sensitivity, for example by advising enhanced scanning for overweight and obese women. Paladini25 has described several methods to boost ultrasound image quality and therefore enhance visualisation of the fetal heart, which should be further evaluated in women of increased BMI.