Objective
We sought to compare fundal height and handheld ultrasound–measured fetal abdominal circumference (HHAC) for the prediction of fetal growth restriction (FGR) or large for gestational age.
Study Design
This was a diagnostic accuracy study in nonanomalous singleton pregnancies between 24 and 40 weeks’ gestation. Patients underwent HHAC and fundal height measurement prior to formal growth ultrasound. FGR was defined as estimated fetal weight less than 10%, whereas large for gestational age was defined as estimated fetal weight greater than 90%. Sensitivity and specificity were calculated and compared using methods described elsewhere.
Results
There were 251 patients included in this study. HHAC had superior sensitivity and specificity for the detection of FGR (sensitivity, 100% vs 42.86%) and (specificity, 92.62% vs 85.24%). HHAC had higher specificity but lower sensitivity when screening for LGA (specificity, 85.66% vs 66.39%) and (sensitivity, 57.14% vs 71.43%).
Conclusion
HHAC could prove to be a valuable screening tool in the detection of FGR. Further studies are needed in a larger population.
Identification of abnormal fetal growth is a critical component of prenatal care and failure of antenatal diagnosis can result in increased perinatal morbidity and mortality as well as affect the long-term health of the neonate. As such, reliable screening methods to detect fetuses with potential fetal growth restriction (FGR) and large for gestational age (LGA) are essential to prevent poor perinatal outcomes.
FGR refers to a weight below the 10th percentile for gestational age, although other definitions using a variety of criteria have been advocated. Inadequate fetal growth affects up to 10% of all pregnancies. Growth-restricted fetuses have an increased risk for meconium aspiration syndrome, neurological injury, acidosis, and fetal demise during the peripartum period with subsequent risks of hypertension, diabetes, coronary artery disease, and stroke in adulthood. Studies show that FGR is often undetected antenatally by current methods, and in recent studies up to 50-90% of these fetuses are not diagnosed until delivery.
At the other end of the spectrum is fetal macrosomia, defined as a birthweight greater than 4000-4500 g. Antenatally, these fetuses are classified as LGA with an estimated fetal weight (EFW) greater than the 90th percentile for gestational age. Approximately 10% of all live-born infants in the United States weigh more than 4000 g, putting these infants at risk for shoulder dystocia and resulting injuries and increased admissions to neonatal intensive care units. Maternal morbidity is also increased because of the higher rates of cesarean delivery and severe perineal lacerations. Unfortunately, an accurate diagnosis of LGA or macrosomia can be made only after weighing the infant at birth because clinical estimates and ultrasonography have proven to be unreliable.
Clinical estimation of fetal weight is most commonly performed using symphysis–fundal height measurement. Numerous studies have shown that fundal height (FH) has a poor positive predictive value for identifying abnormally grown fetuses, and the increasing incidence of maternal obesity further confounds this clinical estimation. Current literature supports the theory that measurement of the abdominal circumference (AC) in the fetus is the most sensitive single indicator of fetal growth abnormalities.
Our study investigates the ability of portable handheld ultrasound measurements of fetal AC to more accurately screen for fetal growth abnormalities compared with FH measurement. Our group hypothesized that height and handheld ultrasound–measured fetal abdominal circumference (HHAC) would be a superior screening modality for the detection of abnormal EFW and birthweight (BW) compared with FH.
Materials and Methods
Study design
This study is a diagnostic accuracy study as defined by the Standards for Reporting of Diagnostic Accuracy statement comparing the diagnostic accuracy of FH measurements with fetal AC measurements obtained by handheld ultrasound to identify fetal growth abnormalities. In addition, the abdominal circumference obtained from the formal ultrasound (USAC) was also included in our investigation of screening modalities. All ultrasounds and measurements were performed at the American Institute of Ultrasound in Medicine–certified Prenatal Wellness Center at the Medical University of South Carolina.
Following institutional review board approval and informed consent, patients were eligible for the study if they were between 24 and 40 weeks’ gestational age with a singleton pregnancy and undergoing a scheduled ultrasound to assess fetal growth. Gestational age was based on the last menstrual period confirmed by dating ultrasound done at less than 20 weeks’ gestational age.
Patients were excluded if their fetus had known congenital anomalies, aneuploidy, or an unsure estimated date of conception. Data abstracted from patient charts included maternal demographics, maternal indication for ultrasound, maternal weight, and maternal comorbidities including hypertension, tobacco use, and pregestational diabetes.
Prior to undergoing their formal growth ultrasound by registered diagnostic medical sonographers, an obstetrics and gynecology resident or maternal-fetal medicine specialist measured both FH and fetal AC using the portable handheld ultrasound device (GE Vscan, version 1.1; GE Healthcare, Indianapolis, IN).
FH was measured from the pubis symphysis to the top of the uterine fundus using a paper measuring tape in centimeters. Size greater than dates was recorded if the measurement was 3 cm or greater above the patient’s gestational age. Similarly, size less than dates was recorded if the measurement was 3 cm or less below the patient’s gestational age.
To measure the HHAC, the fetal abdomen was visualized in a cross-sectional view using the handheld ultrasound at the level of the stomach and umbilical vein. Figures 1 and 2 depict the image quality obtained with HHAC compared with USAC. The fetal AC was obtained by placing the ultrasound cursor directly in the middle of the fetal abdomen and expanding a circle to encompass the entire abdominal circumference using the radius feature on the device. The radius measurement obtained from the handheld ultrasound device was then used to calculate the total abdominal circumference using the following formula: circumference = 2πr, with r meaning the radius.
A positive screen for FGR was recorded as an HHAC less than the 5th percentile and a positive screen for LGA was an HHAC greater than the 95th percentile. This cutoff was chosen to avoid an overestimation of FGR and LGA and to support the data showing an AC less than the 5th percentile is more closely associated with an increased perinatal morbidity and mortality.
For the current study, FGR was defined as an EFW less than the 90th percentile, and LGA was defined as an EFW greater than the 90th percentile because macrosomia cannot be diagnosed until a fetus reaches greater than 4000 g. Therefore, LGA will refer to both an EFW greater than the 90th percentile and a BW greater than the 90th percentile.
After completion of the formal growth scan, measurements from this study were recorded into the patient’s research chart. EFW and percentiles were calculated automatically by the GE Voluson machines in our office using the formula of Hadlock et al. Fetal AC measurement percentiles using the handheld ultrasound device were also calculated using the Hadlock formula for consistency.
A total of 251 patients were consecutively enrolled throughout the study period. The patients were subsequently scheduled for follow-up growth ultrasound at intervals determined by their primary provider. After delivery, the sex of the infant, gestational age at delivery, and BW were recorded. Birthweight percentiles were then calculated using the growth curves of Olsen et al and recorded into the patient’s research chart. Small for gestational age (SGA) at the time of delivery was defined as a BW less than the 10th percentile, and LGA was defined as a BW greater than the 90th percentile.
Sensitivity and specificity of the screening tests were then calculated using a Fisher exact test using SAS 9.3 statistical software (SAS Institutes, Carey, NC) with the EFW and BW as the gold standard for which these were compared. These values were then analyzed using methods previously described by Hawass and McNemar. Statistical significance was established based on a value of P < .05.
Results
A total of 251 patients were enrolled in our study between April 2013 and October 2013. Table 1 describes the demographic and obstetric characteristics of our study population. The average gestational age at enrollment was approximately 32 weeks’ gestation and ranged from 24 weeks’ gestation to 40 weeks’ gestation. As shown, a high proportion of our patients had significant comorbidities including diabetes, hypertension, and tobacco use, making our population relatively high risk for fetal growth abnormalities. Of the patients enrolled, 145 of 151 (96%) had a body mass index greater than 30 kg/m 2 .
| Demographic | Average | Range or % |
|---|---|---|
| Age, y | 28.3 | 18–41 |
| Gestational age, wks | 31 6/7 | 24 0/7–40 0/7 |
| Parity | 1 | 0–4 |
| BMI | 33.9 | 18.1–71.6 |
| EFW, g | 1961.3 | 600–4732 |
| Race | ||
| Black | 113 | 45% |
| White | 131 | 52% |
| Other | 7 | 3% |
| Prevalence of conditions | ||
| Hypertension | n = 65 | 25.9% |
| Diabetes | n = 52 | 20.7% |
| Smoking | n = 29 | 11.5% |
To validate the handheld ultrasound device used in our study, a correlation between HHAC and AC measurement from the formal growth scan is presented in Figure 3 . There is a highly significant correlation between HHAC and AC determined at the time of a formal ultrasound (R = 0.939; P < .001), leading us to accept that the AC measurements made by the clinicians using the handheld ultrasound device were overall comparable with those measurements performed by the registered diagnostic medical sonographer–certified ultrasonographers.
In our study population, we found that antenatally we had 7 fetuses (2.79%) that met criteria for FGR, defined as an EFW less than the 10th percentile on the scheduled growth scan. Similarly, we found that 7 fetuses (2.79%) met criteria for LGA, measuring greater than the 90th percentile at the time of the scheduled ultrasound screening. However, once the BWs were collected and the percentiles calculated using gestational age at delivery and sex of the infant by the method of Olsen et al, we found that 27 infants (10.76%) were considered SGA, defined as a BW below the 10th percentile. On the other hand, 24 infants (9.56%) were found to be LGA, or a BW greater than the 90th percentile.
We first looked at FH, HHAC, and USAC as screening modalities to detect an EFW less than the 10th percentile. These data are broken down in Tables 2, 3, and 4 . Using FH as a screening test, 3 of 7 fetuses (42.86%) with an EFW less than the 10th percentile were detected using FH (size less than the dates). Using HHAC, all 7 fetuses (100%) with an EFW less than the 10th percentile had a positive screen using HHAC less than the 5th percentile. Finally, USAC less than the 5th percentile was tested as a screening tool for EFW less than the 10th percentile, with detection of 6 of 7 fetuses (85.71%).
| Variable | Size less than dates | Normal FH | Size greater than dates | Totals |
|---|---|---|---|---|
| EFW less than 10th percentile | 3 (1.2%) | 4 (1.59%) | 0 | 7 (2.79%) |
| Normal EFW | 18 (7.17%) | 137 (54.58%) | 82 (32.67%) | 237 (94.42%) |
| EFW greater than 90th percentile | 0 | 2 (0.8%) | 5 (1.99%) | 7 (2.79%) |
| Totals | 21 (8.37%) | 143 (56.97%) | 87 (34.66%) | 251 (100%) |
| BW less than 10th percentile | 10 (3.98%) | 13 (5.18%) | 4 (1.59%) | 27 (10.76%) |
| Normal BW | 11 (4.38%) | 118 (47.01%) | 71 (28.29%) | 200 (79.68%) |
| BW greater than 90th percentile | 0 | 12 (4.78%) | 12 (4.78%) | 24 (9.56%) |
| Totals | 21 (8.37%) | 143 (56.97%) | 87 (34.66%) | 251 (100%) |
| Variable | HHAC less than 5th percentile | Normal HHAC | HHAC greater than 95th percentile | Totals |
|---|---|---|---|---|
| EFW less than 10th percentile | 7 (2.79%) | 0 | 0 | 7 (2.79%) |
| Normal EFW | 35 (13.94%) | 167 (66.53%) | 35 (13.94%) | 237 (94.42%) |
| EFW greater than 90th percentile | 1 (0.4%) | 2 (0.8%) | 4 (1.59%) | 7 (2.79%) |
| Totals | 43 (17.13%) | 143 (56.97%) | 39 (15.54%) | 251 (100%) |
| BW less than 10th percentile | 20 (7.97%) | 7 (2.79%) | 0 | 27 (10.76%) |
| Normal BW | 22 (8.76%) | 155 (61.75%) | 23 (9.16%) | 200 (79.68%) |
| BW greater than 90th percentile | 1 (0.4%) | 7 (2.79%) | 16 (6.37%) | 24 (9.56%) |
| Totals | 43 (17.13%) | 143 (56.97%) | 39 (15.54%) | 251 (100%) |
| Variable | USAC less than 5th percentile | Normal USAC | USAC greater than 95th percentile | Totals |
|---|---|---|---|---|
| EFW less than 10th percentile | 6 (2.4%) | 1 (0.4%) | 0 | 7 (2.8%) |
| Normal EFW | 18 (7.2%) | 190 (75.7%) | 29 (11.5%) | 237 (94.4%) |
| EFW greater than 90th percentile | 0 | 0 | 7 (2.8%) | 7 (2.8%) |
| Totals | 24 (9.6%) | 191 (76.1%) | 36 (14.3%) | 251 (100%) |
| BW less than 10th percentile | 15 (6%) | 12 (4.8%) | 0 | |
| Normal BW | 9 (3.6%) | 173 (68.9%) | 18 (7.2%) | 200 (79.7%) |
| BW greater than 90th percentile | 0 | 6 (2.4%) | 18 (7.2%) | 24 (9.5%) |
| Totals | 24 (9.6%) | 191 (76.1%) | 36 (14.3%) | 251 (100%) |
We then looked at the ability of the same screening modalities to detect an EFW greater than the 90th percentile, which is again shown in Tables 2, 3, and 4 . Using FH as a screening test, 5 of 7 fetuses (71.42%) with an EFW greater than the 90th percentile were detected using FH (size greater than the dates).
Using HHAC, 4 of 7 fetuses (57.14%) with an EFW greater than the 90th percentile had a positive screen using a cutoff of HHAC greater than the 95th percentile. Finally, USAC greater than the 95th percentile was tested as a screening tool for EFW greater than the 90th percentile, with detection of 7 of 7 fetuses (100%).
Once BWs were collected, we then looked at our screening modalities with the addition of EFW obtained from the scheduled ultrasound to screen for SGA (BW less than the 10th percentile). These data are outlined in Tables 2, 3, 4, and 5 . Using FH as a screening test, 10 of 27 fetuses (37.04%) with a BW less than the 10th percentile were detected using FH (size less than the dates). Using HHAC, 20 of 27 SGA neonates (74.07%) had a positive screen using HHAC less than the 5th percentile. Next, USAC less than the 5th percentile was tested as a screening tool for SGA, with detection of 15 of 27 fetuses (55.56%). Finally, EFW was investigated as a screening modality to detect SGA. Of the neonates with a BW less than the 10th percentile, 6 of 27 (21.43%) were detected at the time of the scheduled ultrasound examination using EFW less than the 10th percentile as the screening modality.
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