Abstract
Objective
Evaluate the association of a small third-trimester abdominal circumference (AC < 10th percentile) in the setting of a normal estimated fetal weight (EFW ≥ 10th percentile) with gestational age at delivery, indication for delivery and neonatal outcomes.
Methods
Retrospective cohort study at an academic hospital of women with singleton pregnancy seen for ultrasound from 28+0-33+6 weeks of gestation during 2009-2011. Outcomes were compared between two groups: normal AC (AC and EFW ≥ 10th percentile) and small AC (AC < 10th percentile and EFW ≥ 10th percentile).
Results
Among 592 pregnancies, fetuses in the small AC group (n = 55) experienced a higher incidence of overall preterm delivery (RR: 2.2, 95% Cl: 1.3–3.7) and provider-initiated preterm delivery (RR: 3.7, Cl: 1.8–7.5) compared to those in the normal AC group (n = 537). Neonates in the small AC group had a lower median birth weight whether delivered at term (p < 0.001) or preterm (p = 0.04), but were not more likely to experience intensive care unit admission or respiratory distress syndrome (all p ≥ 0.35).
Conclusions
Small AC, even in the setting of an EFW ≥ 10th percentile, was associated with a higher incidence of overall and provider-initiated preterm delivery despite similar neonatal outcomes. Further investigation is warranted to determine whether these preterm deliveries could be prevented.
Keywords: Abdominal circumference, fetal surveillance, obstetrics, preterm delivery, third-trimester ultrasound
Introduction
Small for gestational age neonates, defined as infants with birth weight <10th percentile, account for a significant proportion of neonatal morbidity and mortality. Data showing a small estimated fetal weight as the best predictor of small for gestational age neonates motivates many primary obstetrical providers to obtain a sonographic estimated fetal weight in the third trimester, even in those at low risk for intrauterine growth restriction [1-6]. Additionally, some research findings support the use of a small (<10th percentile) abdominal circumference as a sensitive predictor of small for gestational age [7-10]. However, small abdominal circumference alone, in the absence of growth restriction has not been associated with adverse neonatal outcomes [1-5,7,8,11-17].
Studies evaluating the impact of a small abdominal circumference in the setting of a normal estimated fetal weight in a population at low risk for intrauterine growth restriction are few. In a population of fetuses at risk for intrauterine growth restriction, Chauhan and colleagues found that after third-trimester ultrasound, fetuses in which a small abdominal circumference was identified were delivered sooner after ultrasound than normal abdominal circumference fetuses but went on to experience similar neonatal outcomes, including similar incidence of small for gestational age diagnosis [15]. This finding suggests that a small abdominal circumference may motivate earlier delivery and in this way contribute to provider-initiated preterm delivery, defined as the induction of labor or elective cesarean section for maternal or fetal indications prior to 37 weeks of gestation [18-20].
The aim of this investigation was to evaluate the association of small third-trimester abdominal circumference in fetuses with no prior evidence of intrauterine growth restriction with gestational age at delivery, indication for delivery and neonatal outcomes.
Methods
All women obtaining a third-trimester ultrasound for biometry from 1 January 2009 through 30 November 2011 at a large university-based hospital were screened for inclusion in this retrospective cohort study. Inclusion criteria were women aged 18–45 years with singleton pregnancy who had a third-trimester ultrasound from 28+0 through 33+6 weeks of gestation and delivered at our institution. Pregnancies with previously documented fetal growth abnormalities, including concern for intrauterine growth restriction, and those complicated by major placental or fetal anomalies affecting fetal growth (placenta previa, vasa previa, gastroschisis, diaphragmatic hernia, duodenal atresia and posterior urethral valves) were excluded. The study was approved by the Committee on Clinical Investigations at Beth Israel Deaconess Medical Center.
Abdominal circumference, measured using the ellipse region-of-interest method [21], and estimated fetal weight were converted into percentiles based on gestational age at the time of ultrasound as calculated by Williams’ nomogram [21], Exposure groups were assigned using the smallest observed measurement for fetal abdominal circumference obtained on third-trimester ultrasound and corresponding estimated fetal weight. Fetuses were classified into three groups: abdominal circumference and estimated fetal weight ≥10th percentile (normal abdominal circumference group, “ normal AC” ), abdominal circumference <10th percentile and estimated fetal weight ≥10th percentile (small abdominal circumference group, “ small AC” ), and both abdominal circumference and estimated fetal weight <10th percentile (intrauterine growth restricted group).
Data on patient demographics, pregnancy and neonatal outcomes were abstracted from the ultrasound database, electronic birth registry and medical records. Gestational age at delivery was calculated using the date of delivery from the medical record and the estimated date of confinement, which was derived according to standard obstetric dating parameters and previously recorded in the ultrasound database for clinical purposes [22]. For all preterm deliveries, indication for delivery was determined from delivery and operative records by two independent reviewers (LKH, WTS) and classified as spontaneous or provider-initiated. Spontaneous preterm deliveries included premature rupture of membranes, preterm labor and other clinical scenarios where delivery was imminent or unavoidable. Provider-initiated preterm deliveries indicated deliveries performed for maternal or fetal indication, such as pre-eclampsia or concern for general fetal growth. Though reviewers had access to the complete medical record when determining indication for delivery, they did not access biometric reports, which are located in a separate portion of the medical record, and reviewed only labor and delivery notes to remain blinded to exposure group. Another investigator (AMM) independently assigned exposure groups. Neonatal outcomes included intensive care unit admission, clinical diagnosis of respiratory distress syndrome and low birth weight (<2500 g).
Statistical Analysis Software 9.3 (SAS Institute Inc. 2011, Cary, NC) was used for all data analysis. Data are reported as median (interquartile range) or n (%). Group comparisons were made using Chi-square, Fisher’s exact or the Wilcoxon rank-sum test as indicated. Log-binomial regression generated risk ratios (RR) and 95% confidence intervals (Cl). Potential confounders were assessed using univariate analysis and were considered for addition to the final model if they changed the risk ratio by more than 10%. All tests were two-sided and statistical significance was assumed for p < 0.05.
Results
A total of 597 pregnancies met inclusion criteria. There were 537 (90.0%) pregnancies in the normal AC group, 55 (9.2%) in the small AC group and 5 (0.8%) in the intrauterine growth restricted group. To isolate a population of fetuses at low-risk for intrauterine growth restriction by established criteria and due to the inability to draw meaningful conclusions from a small sample size, fetuses in the intrauterine growth restricted group were excluded from subsequent analyses. Thus, 592 pregnancies were retained for analysis. Among eligible pregnancies, the median gestational age at ultrasound was 32.0 weeks (30.7–33.0) and the median maternal age at delivery was 32.8 years (28.8–36.7). An AC < 10th percentile was present in 10.1% of the initial cohort and, after exclusion of fetuses with an EFW < 10th percentile, 9.3% of the final cohort. Women with fetuses in the small AC group were younger, had an earlier gestational age at ultrasound, and were more likely to be African-American than women with fetuses in the normal AC group (all p ≤ 0.04; Table 1).
Table 1.
Demographic characteristics of 592 women receiving third-trimester growth scan.
| Small abdominal circumference n = 55 (9.3%) | Normal abdominal circumference n = 537 (90.7%) | P | |
|---|---|---|---|
| Gestational age at ultrasound (wks) | 30.9 (29.3–32.4) | 32.0 (30.9–33.0) | <0.001 |
| Maternal age at estimated date of confinement (yrs) | 31.3 (26.2–35.3) | 33.1 (29.0–36.8) | 0.04 |
| Parity | 0.08 | ||
| Nulliparous | 28 (50.9) | 209 (38.9) | |
| Parous | 27 (49.1) | 328 (61.1) | |
| Race/ethnicity | 0.01 | ||
| Caucasian | 24 (43.6) | 259 (48.2) | |
| African-American | 19 (34.6) | 82 (15.3) | |
| Hispanic | 6 (10.9) | 85 (15.8) | |
| Asian | 5 (9.1) | 77 (14.3) | |
| Other/Unknown | 1 (1.8) | 34 (6.3) |
Data are presented as n (%) or median (interquartile range).
The incidence of preterm delivery in the cohort was 12.2%. Compared to fetuses in the normal AC group, fetuses in the small AC group were twice as likely to experience preterm delivery (RR: 2.2, Cl: 1.3–3.7, p = 0.006) and nearly four times as likely to experience provider-initiated preterm delivery (RR: 3.7, Cl: 1.8–7.5, p = 0.002). Fetuses in the small AC group were also more likely than fetuses in the normal AC group to experience spontaneous preterm delivery, though the difference was not statistically significant (Table 2). The addition of potential confounders (maternal age at delivery, estimated gestational age at ultrasound and maternal ethnicity, Table 1) did not appreciably alter risk ratios.
Table 2.
Risks of preterm delivery among 592 women by third-trimester abdominal circumference.
| Type of preterm delivery | Small abdominal circumference n = 55 (9.3%) | Normal abdominal circumference n = 537 (90.7%) | p | Risk ratio (95% Confidence Interval) |
|---|---|---|---|---|
| All | 13 (23.6) | 59 (11.0) | 0.006 | 2.2 (1.3–3.7) |
| Spontaneous | 4 (7.3) | 35 (4.7) | 0.78 | 1.1 (0.4–3.0) |
| Provider-initiated | 9 (16.4) | 24 (4.5) | 0.002 | 3.7 (1.8–75) |
Adverse neonatal outcomes stratified by timing of delivery are presented in Table 3. The median gestational age at delivery did not differ between groups within term deliveries (small AC: 39.4 weeks, normal AC: 39.1 weeks; p = 0.94) or within preterm deliveries (small AC: 34.6 weeks, normal AC: 34.7 weeks; p = 0.93). Among term deliveries, neonates in the small AC group experienced a similar incidence of intensive care unit admission and respiratory distress syndrome despite having a lower median birth weight (small AC: 2977.5 g, normal AC: 3350.0 g; p < 0.001) and an increased risk of low birth weight (RR: 4.6, Cl: 1.5–13.9) when compared to neonates in the normal AC group (Table 3). Among preterm deliveries, the median birth weight was lower in the small AC group (small AC: 2040.0 g, normal AC: 2385.0 g, p = 0.04) but incidences of low birth weight, intensive care unit admission, and respiratory distress syn-drome were similar compared to the normal AC group (all p ≥ 0.35; Table 3).
Table 3.
Neonatal outcomes among 592 women stratified by third-trimester abdominal circumference and timing of delivery.
| Term delivery
|
Preterm delivery
|
|||||||
|---|---|---|---|---|---|---|---|---|
| Small abdominal circumference n = 42 (8.1%) | Normal abdominal circumference n = 478 (91.9%) | p | Risk ratio (95% Confidence Interval) | Small abdominal circumference n = 13 (18.1%) | Normal abdominal circumference n = 59 (81.9%) | p | Risk ratio (95% Confidence Interval) | |
| Neonatal intensive care admission | 3 (7.1) | 53 (11.1) | 0.60 | 0.64 (0.2–2.0) | 11 (84.6) | 44 (74.6) | 0.72 | 1.1 (0.9–1.5) |
| Respiratory distress syndrome | 0 (0.0) | 1 (0.2) | 1.0 | – | 4 (30.8) | 15 (25.4) | 0.73 | 1.2 (0.5–3.1) |
| Low birth weight | 4 (9.5) | 10 (2.1) | 0.02 | 4.6 (1.5–13.9) | 10 (76.9) | 36 (61.0) | 0.35 | 1.3 (0.9–1.8) |
Discussion
The present work assessed the impact of a small third-trimester abdominal circumference on delivery and neonatal outcomes. The major finding of this work shows that a small third-trimester abdominal circumference, even in the setting of an estimated fetal weight ≥ 10th percentile, was associated with a lower median birth weight and an increased risk of overall and provider-initiated preterm delivery despite similar neonatal outcomes. These findings suggest that the label of small abdominal circumference in fetuses with a normal estimated weight might contribute to an increase in provider concern and intervention.
In our cohort, women with fetuses in the small AC group were younger, had an earlier gestational age at ultrasound, and were more likely to be African-American than women with fetuses in the normal AC group. Controlling for these characteristics did not appreciably alter the risk ratios. While we cannot comment on the origin of these baseline differences, we note that an earlier gestational age at ultrasound in the small AC group has been documented in a previous investigation [15].
In a similar study, Chauhan and colleagues assessed the value of third-trimester abdominal circumference and estimated fetal weight in predicting small for gestational age at delivery in a population at risk for intrauterine growth restriction [15]. Similar to our study, they found no significant differences among normal estimated weight fetuses (EFW ≥ 10th percentile) between small (n = 76) and normal (n = 33) abdominal circumference groups when comparing mean gestational age at delivery (p > 0.05), mean birth weight (p > 0.05), small for gestational age diagnosis (95% Cl: 0.56–2.94), intensive care unit admission (Cl: 0.47–2.58) and composite neonatal morbidity (Cl: 0.49–4.49). However, fetuses with a small abdominal circumference on third-trimester ultrasound were delivered sooner than fetuses with a normal abdominal circumference (small AC: 4.6 days, normal AC: 8.9 days; p < 0.01). The findings of the present work along with those of Chauhan and colleagues suggest that the finding of a small abdominal circumference may motivate delivery.
Strengths of our study include identification of an ideal population in which to evaluate this research question: normal estimated weight fetuses without previously documented growth abnormalities. Access to complete maternal records allowed for the isolation of a population at low-risk for intrauterine growth restriction. Access to neonatal medical records allowed for pairing of immediate neonatal outcomes. Indication for preterm delivery was determined by two independent reviewers who did not access biometric records at the time of record review to prevent knowledge of exposure group classification and to minimize bias. The general izability of study findings is supported by the finding that 10.1% of the fetuses in our population had an abdominal circumference <10th percentile and that preterm delivery occurred in 12.2% of our population, consistent with a national estimate from 2010 of 12% [23].
We lacked information on the indication for third-trimester ultrasound of fetuses at low-risk for intrauterine growth restriction. As such, it is possible ascertainment bias that may influence our findings, though all pregnancies with previously documented fetal growth abnormalities were excluded. We lacked data on additional potential confounders such as body mass index, alcohol intake and smoking during pregnancy [24-26], Data on the indication for preterm delivery was retrospectively collected from non-standardized provider documentation and thus was subject to interpretation by reviewers, though variability was minimized by independent reviews.
The major findings of this study are that in the setting of a normal estimated fetal weight, third-trimester small abdominal circumference is associated with an increased risk of both overall and provider-initiated preterm delivery, despite similar immediate neonatal outcomes. Further study of the factors that influence timing of delivery in fetuses with a small abdominal circumference may help identify a population that could be targeted to reduce provider-initiated preterm delivery.
Acknowledgments
Author Michele R. Hacker reports that her work was conducted with support from the Harvard Catalyst. The Harvard Clinical and Translational Science Center (National Center for Research Resources and the National Center for Advancing Translational Sciences, National Institutes of Health Award 8UL1TR000170-05 and financial contributions from Harvard University and its affiliated academic health care centers).
Footnotes
Declaration of interest
The other authors report no declarations of interest.
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