Factors affecting feasibility and quality of second-trimester ultrasound scans in obese pregnant women
Correspondence to: Dr F. Fuchs, Hôpital Bicêtre, Service de Gynécologie-Obstétrique, 78 rue du Général Leclerc, 94275 Le Kremlin-Bicêtre cedex, France (e-mail: firstname.lastname@example.org)
To evaluate the feasibility of completing in one session a second-trimester ultrasound scan in obese pregnant women, to compare the quality of images obtained with those of non-obese women and to analyze factors that can improve the completion rate.
This prospective study, from 2009 to 2011, included all obese pregnant women (prepregnancy body mass index (BMI) > 30 kg/m2) who had an ultrasound examination at 20–24 weeks in our department, and a control group of pregnant women with normal BMI (20–24.9 kg/m2) who had the same examination. A single operator reviewed the standardized ultrasound images (three biometric and six to assess key anatomical features) required under French guidelines, to assess their presence, evaluate the quality of all images and score the quality of the six anatomical images. Each image was assessed according to between four and six criteria, each worth one point. We sought excellent quality, defined as the frequency of maximum points for a given image type. The factors associated with completing the scan in one session were evaluated with multivariate logistic regression.
The obese group included 223 women and the control group 60; a complete scan in one session was achieved in 70.4% and 81.7% of these, respectively (P = 0.08). The completion rate for each image type was at least 95% in the control group and 90% in the obese group, except for diaphragm and right outflow tract images. Significant factors associated with completing the scan in the multivariate model were: having 10 additional minutes for the scan (P = 0.03), moving the fetus so that the back was in posterior or lateral position (P = 0.01), more experienced sonographer (P = 0.03) and thinner maternal abdominal wall thickness (P = 0.01). Overall, the excellence rate varied from 35% to 92% in the normal BMI group and from 18% to 58% in the obese group, and was significantly lower in the latter for all images except abdominal circumference (P = 0.26) and spine (P = 0.06). Anatomical quality scores were also significantly lower in the obese group (22.3 vs 27.2; P = 0.001).
Although ultrasound scans of obese pregnant women are feasible, image quality and global anatomical scores are significantly lower among obese than normal-weight women. However, certain simple improvements may increase fetal visualization.
Obesity, defined by the World Health Organization as a body mass index (BMI) of 30 kg/m2 or greater, has become one of the most common medical problems worldwide. Its prevalence has increased dramatically over the past 20 years in western countries and is also growing in developing countries. More than 400 million people were obese in 2005, and the prediction for 2015 is 700 million. The number of pregnant women who are obese has also increased; estimates for the obesity rate among pregnant women in the USA range from 18 to 38%. In France, the rate is almost 10%, according to the last national perinatal study.
Numerous studies have reported that maternal obesity during pregnancy is associated not only with maternal and fetal complications but also with substantial limitations in the ability to evaluate fetal anatomy. Absorption of ultrasound beams by subcutaneous tissue makes ultrasound scans of the obese more difficult and decreases the detection rate of structural anomalies in fetuses of obese mothers. Nonetheless, although the rates of suboptimal visualization and incomplete scans on the first attempt have increased as maternal BMI has risen, completion rate of the basic anatomical survey does not differ significantly between women with normal BMI and those with Class I obesity (BMI, 30–34.9 kg/m2). However, previous studies dealing with second-trimester scan feasibility among obese patients have mainly been retrospective, used older ultrasound equipment[5, 9, 10] and did not attempt to identify factors that might improve visualization. The next step to improve prenatal diagnosis in obese women is to look at the quality of images obtained during prenatal ultrasound screening and determine whether this differs from the quality of images in a normal-BMI population. Despite the widespread use of diagnostic ultrasound in pregnancy, no study has compared the quality of ultrasound images obtained in obese and non-obese women.
The aim of this study was to conduct a prospective assessment of the feasibility of completing a second-trimester ultrasound scan in obese pregnant women in a single session, to analyze factors that might improve the completion rate, and to compare the quality of each second-trimester ultrasound image obtained with those obtained in non-obese pregnant women.
Subjects and methods
This prospective study included all obese pregnant women (prepregnancy BMI > 30 kg/m2) and a control group of normal-weight women (prepregnancy BMI 20–24.9 kg/m2) who underwent routine second-trimester ultrasound examination in our tertiary care center between November 2009 and May 2011. Exclusion criteria were multiple gestation and a scan performed before 20 or after 24 weeks' gestation.
The six sonographers in our unit performed all the ultrasound examinations, using a GE E8 or a GE Voluson 730 (GE Medical Systems, Piscataway, NJ, USA) ultrasound unit, equipped with real-time 4D abdominal transducers supporting a bandwidth of 2–8 MHz and two-dimensional abdominal transducers supporting a bandwidth of 2–5 MHz. After completion of the examination, each sonographer completed a detailed form including maternal data (age, prepregnancy and second-trimester BMI, history of prepregnancy diabetes and previous Cesarean delivery) and ultrasound data (gestational age at ultrasound, duration of scan, fetal position, placental placement and maternal abdominal wall thickness, defined as the maximum subcutaneous thickness from skin surface to uterine serosa measured by ultrasound).
A single trained operator, who had performed none of the scans, reviewed each one to evaluate the presence or absence of the nine images recommended by French guidelines and thus to evaluate feasibility. These images included three biometric images (head and abdominal circumferences, femur length measurement) and six images to assess key anatomical features (four-chamber view, right outflow tract, kidneys, diaphragm, spine and face). The reviewer was blinded to the sonographers' names. The reviewer's evaluations of the scans were used for the analysis. Feasibility of completion was defined as the ability to obtain a complete scan on the first attempt, i.e. at the first session. When the scan was incomplete on the first try, the number of additional scans needed to obtain a complete examination as well as the gestational age at which they were performed was reported.
The quality of each scan was determined on two complementary scales. The first scale used the criteria described by Salomon et al.[12, 13] to score the quality of each of these nine images (Table 1). These criteria were specific for each type of image and were designed to apply established standards for fetal examination[11, 14-16]. Each criterion was worth 1 point, and each image could yield a maximum score of 4, 5 or 6 points, depending on the specific image. Excellence was defined as the maximum score for that image and was measured as the frequency of maximum scores for that type of image. The second scale was a global anatomical score for the scan, computed by adding the points for the six anatomical images. The maximum global score was 32 points.
Table 1. Criteria for score-based evaluation of the nine images recommended by French guidelines for the second-trimester scan, according to Salomon et al[12, 13]
|Symmetrical plane||Symmetrical plane||Both ends of bone clearly visible||Upper lip visible||Four chambers visible||Pulmonary artery bifurcation visible||Heart visible||Circular view of first kidney||Dorsal spine visible|
|Plane showing thalami||Plane showing stomach bubble||< 45° angle to horizontal||Two nostrils visible||Apex of heart visible||Ascending aorta visible||Stomach visible||Circular view of second kidney||Sacrum visible|
|Plane showing cavum septi pellucidi||Plane showing portal sinus||—||Two lip angles visible||Heart crux visible||Right ventricle visible||Spine not visible||Posterior kidney clear from spine acoustic shadow||Alignment of vertebrae visible from dorsal level to sacrum|
|Cerebellum not visible||Kidneys not visible||—||—||One pulmonary vein visible||Pulmonary artery curling up aorta||Diaphragmatic interface visible from back to front||Corticomedullary differentiation or pyelic cavity visible||Continuity of skin|
|Calipers and dotted ellipse placed correctly||Calipers and dotted ellipse placed correctly||Calipers and dotted ellipse placed correctly||—||Descending thoracic aorta visible||—||Thigh and neck visible||—||Amniotic fluid visible beyond skin|
|Head plane occupying more than half of total image size||Abdominal plane occupying more than half of total image size||Femoral plane occupying more than half of total image size||ROI occupying more than half of total image size||ROI occupying more than half of total image size||ROI occupying more than half of total image size||ROI occupying more than half of total image size||ROI occupying more than half of total image size||ROI occupying more than half of total image size|
The control group (women with a prepregnancy BMI between 20 and 24.9 kg/m2) was selected and their ultrasound images were evaluated according to the same procedure. Women included in this group were examined by the same operators, during the same study period, and were the next woman with a normal BMI examined after an obese woman. As the obese sample included 223 women, the control group required 60 women to be able to detect a 4-point difference in the anatomical score with a statistical power of 80% and a two-tailed 0.05 significance level.
We compared obese and control women using Student's and Mann–Whitney U-tests for quantitative and Fisher's exact or χ2 tests for qualitative data. Univariate comparison of successful scan completion used the same tests. Variables with P < 0.2 in the univariate analysis were entered into a multivariate model. Multiple logistic regression analysis was used to fit the model that best predicted a complete ultrasound scan in a single session. Results were considered significant when P < 0.05. Statistical analyses were performed with STATA software, v.11 (Stata Corporation, College Station, TX, USA).
All scans were stored in a database. This database and its use for research have been approved by the French Data Protection Authority (CNIL, Commission Nationale de l'Informatique et des Libertes) under notification number 1181076.
Characteristics of the 223 obese and 60 control women included in the study are summarized in Table 2. Pregnancy outcome was verified for all, and no fetal anomalies were found. In the obese group, prepregnancy BMI ranged from 30 to 54.3 kg/m2 and was distributed as follows: Class I obesity (30–34.9 kg/m2), 69%; Class II obesity (35–39.9 kg/m2), 22%; and Class III obesity (≥40 kg/m2), 9%. The obese women gained less weight during pregnancy than did the non-obese women (P = 0.04). In the obese group, 34 (16%) women had had diabetes before pregnancy, but only 3% had in the normal BMI group (P = 0.01). Maternal abdominal wall thickness differed significantly between the two groups, ranging from 16.7 to 68.2 mm in the obese group and from 12 to 34.6 mm in the normal BMI group (P < 0.001). Neither fetal presentation nor placental location, as assessed during the scan, differed between the groups. On the other hand, the fetal back was more frequently in a lateral position (left or right) in the control population than among the obese women (P = 0.006). The duration of the ultrasound scan was significantly longer for the obese women (P < 0.001).
Table 2. Patient and second-trimester ultrasound characteristics in obese and non-obese populations
|Age|| || ||0.1|
|< 25 years||27 (12.1)||12 (20)|| |
|25–34 years||128 (57.4)||36 (60)|| |
|> 34 years||68 (30.5)||12 (20)|| |
|Prepregnancy BMI (kg/m2)||33.1 (31.2; 36.2)||21.9 (20.8; 22.8)||< 0.001|
|BMI at US (kg/m2)||35.3 (33.3; 38.5)||24.5 (22.6; 26.0)||< 0.001|
|Weight gain* (kg)||5 (1; 9)||7 (4; 10)||0.04|
|GA at ultrasound (weeks)||22.6 (22.1; 23.2)||22.6 (22.1; 22.9)||0.5|
|Ultrasound unit|| || ||0.3|
|GE E8||189 (84.7)||54 (90)|| |
|GE Voluson 730||34 (15.3)||6 (10)|
|Maternal abdominal wall thickness (mm)||33.7 (28; 41)||20 (16; 23)||< 0.001|
|Maternal abdominal wall thickness|| || ||< 0.001|
|Min–24.9 mm||24 (11)||49 (82)|| |
|25–34.9 mm||98 (44)||11 (18)|
|> 35 mm||101 (45)||—|
|Duration of US exam (min)||24 (20; 33)||20 (17.5; 24.5)||< 0.001|
|Fetal presentation|| || ||0.2|
|Vertex||116 (52)||40 (67)|| |
|Breech||69 (31)||13 (22)|
|Transverse||38 (17)||7 (11)|
|Fetal back position|| || ||0.006|
|Lateral (left or right)||127 (57)||41 (68)|| |
|Posterior||39 (17)||15 (25)|
|Anterior||57 (26)||4 (7)|
|Placental location|| || ||0.1|
|Posterior||98 (44)||33 (55)|| |
|Anterior||125 (56)||27 (45)|
The scan was completed on the first attempt in 70.4% of the obese group and 81.7% of the controls (P = 0.08) (Table 3). In the obese sample, 24.2% of women needed one additional scan to have a complete examination, and 5.4% needed two additional scans. The median gestational age at the second and third scans was 26.5 and 30.4 weeks, respectively. Thus, all obese patients had a complete evaluation, with a maximum of three scans. In the non-obese group, only 18% needed a second scan to have a complete evaluation. Indeed, in that group, the first-try completion rate was 100% for five of the nine types of images (head and abdominal circumferences, femur length, face and four-chamber view) and 95% for the other four (right outflow tract, diaphragm, kidneys and spine). In the obese group, the first-try completion rate was over 95% for six images: head and abdominal circumferences, femur length, face, four-chamber view and spine; it was 90% for kidneys and 87% for right outflow tract and diaphragm. No image type showed a statistical difference in first-time completion rate between obese and non-obese women.
Table 3. Feasibility of second-trimester ultrasound examination in obese and non-obese populations
|Complete scan on first attempt (9 images)||157 (70.4)||49 (81.7)||0.08|
|Additional scans needed for completion|| || ||0.2|
|One scan||54 (24.2)||11 (18)|| |
|Two scans||12 (5.4)||—|
|Biometric images|| || || |
|Anatomical images|| || || |
|Right outflow tract||87||95||0.11|
Comparing a successful complete scan and an incomplete scan by univariate analysis showed that increased duration (P = 0.02), newer equipment (GE E8 vs GE Voluson 730) (P = 0.01), fetal back in either lateral or posterior (vs anterior) position (P = 0.03) and a more experienced sonographer (P = 0.02) were all factors that increased the probability of a complete scan in a single session. More severe obesity and increased maternal abdominal wall thickness also increased the probability that the complete scan would not be performed in a single session, but not to a statistically significant extent: Class I obesity, 28%; Class II obesity, 30%; Class III obesity, 41%; P = 0.16 and minimum thickness 24.9 mm, 17%; minimum thickness 25–34.9 mm, 26.5%; minimum thickness ≥35 mm, 36%; P = 0.12. Because these two indicators were highly correlated, we chose to keep only maternal abdominal wall thickness in the model for the multiple regression analysis.
Multivariate analysis (Table 4) showed that four independent factors of improvement significantly increased the probability of a complete scan in obese women during a single session: an additional 10 min for the scan; a posterior fetal back position; more experienced sonographer; and thinner maternal abdominal wall thickness.
Table 4. Factors affecting success of complete second-trimester scan on first attempt in obese women
|Maternal abdominal wall thickness|| ||0.01|
|Min–24.9 mm||1|| |
|25–34.9 mm||0.5 (0.1; 1.7)|
|≥ 35 mm||0.3 (0.1; 0.8)|
|10 min additional time at US screening||1.5 (1.1; 2.0)||0.03|
|Ultrasound unit|| ||0.09|
|GE Voluson 730||1|| |
|GE E8||2.1 (0.9; 5.0)|
|Fetal back position|| || |
|Lateral (left or right)||1||0.01|
|Posterior||2.8 (1.1; 7.7)|
|Anterior||0.5 (0.3; 1.0)|
|More experienced sonographer||2.1 (1.1 ; 4.0)||0.03|
Table 5 reports the frequency of excellent quality for each of the nine types of image and compares it between the two groups. Excellence was always significantly less frequent in the obese sample, except for two types of image: abdominal circumference (P = 0.26) and the spine (P = 0.06). By looking at each image separately, we found that the significant difference in head circumference, face and kidney images was due to insufficient zoom in the obese group, with the region of interest occupying less than half the total image size (P < 0.001, Pearson χ2 test). Two femur length criteria were met significantly less often on obese patients' images: both ends of the bone were not clearly visible (P = 0.002, Fisher's exact test) and the femoral plane occupied less than half the total image (P < 0.001, Pearson's χ2 test). The quality of both heart images was also poorer among obese women: for the four-chamber image, the problem was due especially to the poor visibility of both the apex of the heart (P = 0.03, Pearson χ2 test) and the crux (P = 0.03, Pearson χ2 test) and to inadequate zooming (P < 0.001, Pearson χ2 test); for the right outflow tract image, the problem was because the pulmonary artery curling up the aorta was not visible (P < 0.001; Pearson χ2 test) and the zooming was inadequate (P < 0.001, Pearson χ2 test). The diaphragm image was also of poor quality for obese patients, with the diaphragm interface not visible from back to front (P < 0.001, Pearson χ2 test).
Table 5. Comparison of frequency of excellent quality for each image in second-trimester scan and global anatomical quality score among obese and normal body mass index (BMI) population
|Biometric images|| || || |
|HC – 6 points||129/223 (58)||47/60 (78)||0.004|
|AC – 6 points||96/221 (43)||31/60 (52)||0.26|
|Femur length – 4 points||114/222 (51)||55/60 (92)||< 0.001|
|Anatomical images|| || || |
|Face – 4 points||81/210 (39)||36/60 (60)||0.003|
|4CV – 6 points||89/215 (41)||38/60 (63)||0.003|
|ROT – 5 points||71/205 (35)||28/57 (49)||0.046|
|Diaphragm – 6 points||26/148 (18)||20/57 (35)||0.007|
|Kidneys – 5 points||84/194 (43)||46/57 (81)||< 0.001|
|Spine – 6 points||78/210 (37)||29/57 (51)||0.06|
|Global anatomical quality score||22.3 ± 5.6||27.2 ± 3.6||0.001|
Finally, the mean global anatomical score for all six anatomical images was significantly lower in the obese group than in the control group (22.3 ± 5.6 points vs 27.2 ± 3.6 points, P < 0.001) (Table 5). This score ranged from 4 to 32 points in the obese sample and from 17 to 32 points in the control group. The global anatomical score did not differ significantly between the three BMI obesity classes (Class I, II and III had 22.4, 22.4 and 20.9 points, respectively, P = 0.38), or between the three classes of maternal abdominal wall thickness (P = 0.06). More experienced sonographers had significantly better global anatomical scores for obese patients than did younger operators: 24.1 ± 5.4 points vs 21.7 ± 5.6 points (P = 0.008).
We found that a second-trimester ultrasound scan in an obese population is feasible, with a first-attempt scan success rate of 70.4%, which was not significantly different from the rate among non-obese patients. Moreover, this rate could be improved by spending more time scanning, by moving the fetus so that its back was in a posterior or lateral position and by using experienced sonographers. Nonetheless, the quality of images was significantly lower among the obese population.
Recent studies focusing on the ability to scan obese pregnant women have been mainly retrospective. The two largest studies[5, 9], which both included more than 1000 obese and non-obese patients, found that a complete scan was feasible in 57% and 65% of the obese groups and among 70% and 79% of the non-obese groups. These results, although they showed a significant difference, are fairly similar to ours and demonstrate that scanning obese patients is, albeit difficult, feasible a good proportion of the time. The same studies showed that the ability to scan fetuses of obese women decreased as the obesity class increased: Thornburg et al. found in Class I that this proportion was 72%, in Class II it was 61% and in Class III it was 49% while Dashe et al. reported values of 57%, 41% and 30%, respectively. We observed the same phenomenon, which we explain by the increased quantity of subcutaneous tissue that decreases beam penetration. Our results, however, were better for all three obesity classes. Several reasons may explain this discrepancy. The prospective nature of our study may have artificially increased the performance of each sonographer, and the difference in the distribution of obese patients among the three classes, with only 9% in Class III, might also have affected the results. In addition, we used low-frequency transducers, harmonic technology and recent specific tips that will have improved our results on what was possible a few years ago.
We also observed that BMI was highly correlated with maternal abdominal wall thickness, as expected: the higher the BMI is, the thicker the patient's abdomen. Nonetheless, sonographers have often faced difficult scanning situations for patients with only a moderately high BMI and sometimes found scanning easier for women with a much higher BMI. This apparent anomaly is due mainly to skin and subcutaneous thickness. Women with Class III obesity always have abdominal folds and it is therefore possible to scan through a relatively thin abdominal window above or below the panniculus. On the contrary, women with Class I obesity may have no folds and a very tense, hard abdomen that is quite hard to depress. Maternal abdominal wall thickness therefore seems to us to be more informative than BMI, which does not tell us about body fat distribution. Although this abdominal wall thickness is not predictable and cannot be considered at the time that the second-trimester scan appointment is made, the multivariate regression showed a high thickness to be strongly associated with failure to complete the scan in a single session. We believe that this characteristic, rather than BMI, is the main barrier to a complete scan among obese women, and we advise sonographers to record it.
Improving our ability to perform ultrasound scans on obese patients has a single overriding goal: to increase the sensitivity of fetal malformation detection and enable us to reassure pregnant women when the scan is normal. We found that additional scanning time and positioning the fetus so that its back was in a posterior or lateral view were both significant factors for enhancing feasibility. These results are new, for no study has ever looked at factors of improvement. Although one might suspect that more time is correlated with adjusting fetal position, these two factors were independently significant in multivariate logistic regression.
Recent improvements in ultrasound equipment, as previously reported by Hendler et al., might also improve visualization of some structures. Newer ultrasound equipment, with better resolution, sophisticated features and advanced signal processing modules, appeared to help improve feasibility, perhaps because they provide most benefit to obese patients, although this difference was not statistically significant in our study.
The literature about the effect of sonographers' experience is relatively sparse. Only Hendler et al. have suggested that greater sonographer experience is associated with higher rates of adequate visualization of fetal craniospinal structures in obese patients. Our study confirmed those results and showed that the completion rate for experienced sonographers was double that of new operators. Presumably, as they have faced many different situations, they are better able to obtain good images even under difficult conditions.
The strengths of our study are the prospective design over a short period, with no patients lost to follow-up, the good global completion rate of each image in both groups and the large number of obese patients included. The use of several sonographers with different levels of experience also enabled us to increase external validity. Using a single reviewer provided us with a consistency of viewpoint and impression for every image. Because the reviewer was blinded to the sonographer's name, knowledge of their experience could not affect his evaluation of image quality.
Some limitations must also be mentioned. Each operator was supposed to complete a case report form after each examination and list the images that were or were not seen. There are thus three possible explanations about why examinations were not completed: the sonographer was unable to record the image, they took an incorrect or inadequate image of the structure (according to the reviewer) or they forgot to image a structure. Even in a prospective study, some structures can be forgotten, such as the diaphragm. Thus, the prevalence of completion among non-obese patients might have been lowered and led to non-significant results. Another point is that we only had one reviewer and therefore could not study inter-reviewer reproducibility.
In conclusion, scanning the obese pregnant woman is feasible but the quality of the images is poor. Nonetheless, simple improvements may increase fetal visualization, which is the cornerstone for detecting fetal abnormalities.