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Prenatal intraabdominal bowel dilation is associated with postnatal gastrointestinal complications in fetuses with gastroschisis
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Prenatal intraabdominal bowel dilation is associated with postnatal gastrointestinal complications in fetuses with gastroschisis Nancy G. Huh, MD; Shinjiro Hirose, MD; Ruth B. Goldstein, MD OBJECTIVE: The purpose of this study was to determine whether pre-
natal intraabdominal bowel dilation (IBD) is associated with increased postnatal complications in fetuses with gastroschisis. STUDY DESIGN: A retrospective review was performed on all maternalfetus pairs with prenatally diagnosed gastroschisis that was treated at the University of California San Francisco from 2002-2008. Postnatal outcomes were compared between fetuses with and without IBD.
as opposed to a single loop (n ⫽ 10) was associated highly with bowel complications and increased time to full enteral feeding and length of hospital stay (100% vs 0% [P ⫽ .001]; 44 vs 23 days [P ⫽ .034]; 69 vs 27 days [P ⫽ .001], respectively). CONCLUSION: IBD is associated with increased postnatal complica-
RESULTS: Forty-three of 61 maternal-fetal pairs met the criteria for in-
tions in infants with prenatally diagnosed gastroschisis; however, this association seems to be limited to those with multiple loops of dilated intraabdominal bowel.
clusion. Sixteen fetuses (37%) had evidence of IBD. Fetuses with IBD were significantly more likely to have postnatal bowel complications (38% vs 7%; P ⫽ .037). The presence of multiple loops of IBD (n ⫽ 6)
Key words: bowel complication, fetus, gastroschisis, intraabdominal bowel dilation, postnatal outcome, ultrasound
Cite this article as: Huh NG, Hirose S, Goldstein RB. Prenatal intraabdominal bowel dilation is associated with postnatal gastrointestinal complications in fetuses with gastroschisis. Am J Obstet Gynecol 2010;202:396.e1-6.
G
astroschisis is a congenital anomaly that is characterized by the herniation of fetal intestine through a fullthickness defect in the abdominal wall. The incidence of gastroschisis ranges from 0.5-1 per 10,000 births.1,2 Prenatal detection of gastroschisis is facilitated by the combination of maternal serum alpha fetoprotein measurement and widespread use of routine prenatal ultrasound. The apparent increase in incidence of prenatally detected gastroschisis over the past 2 decades has been From the Department of Radiology, University of California at San Francisco School of Medicine, San Francisco, CA. Received March 26, 2009; revised Aug. 13, 2009; accepted Oct. 29, 2009. Reprints: Ruth B. Goldstein, MD, Department of Radiology, University of California at San Francisco, 505 Parnassus Ave, San Francisco, CA 94143. Authorship and contribution to the article is limited to the 3 authors indicated. There was no outside funding or technical assistance with the production of this article. 0002-9378/$36.00 © 2010 Mosby, Inc. All rights reserved. doi: 10.1016/j.ajog.2009.10.888
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attributed to these advancements in screening and detection.3-6 Although the overall survival rate for neonates with gastroschisis is very good (range, 90 –97%7-10) both morbidity and mortality rates are highly correlated with the degree of bowel disease at birth. Gastrointestinal complications such as perforation or atresia occur in 10-20% of cases.11 Presence of gastrointestinal complications is associated with mortality rates as high as 28%, longer hospitalization, and prolonged parenteral nutrition with its accompanying risks of infection, growth restriction, metabolic disturbances, and severe liver disease.1,2,5,12 Identification of prenatal prognostic factors would help identify which patients would benefit from intensive fetal surveillance and potentially early intervention or delivery and more informed parental counseling. Identification of discriminating prenatal indicators of outcome has not been very successful. Dilation of extraabdominal bowel loops has been studied but has not been proved to be a useful predictor of postnatal outcome.1,3-5 The differences in definition of dilation and
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small sample sizes of previous studies limit the consensus on which measurements are consistently predictive of poor outcome.1,3-5 Furthermore, externalized bowel seems to dilate as “normal” phenomenon in many gastroschisis fetuses in the third trimester who do very well after birth (Figure 1). The development of intraabdominal bowel dilation (IBD) in these fetuses is much less common, with an estimated report in the limited published literature on this topic that ranges from 8-17%.1,11 In a recent study, Nick et al1 suggested that the presence of IBD in fetuses with gastroschisis may have important prognostic value. The purpose of this study was to evaluate whether IBD in fetuses with gastroschisis is associated with increased postnatal complications.
M ETHODS A retrospective review was conducted on all cases of gastroschisis who were delivered at our institution, the University of California San Francisco (UCSF), between May 2002 and June 2008. The study population included those mater-
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Differences between fetal groups with and without IBD were determined by use of the Fisher’s exact test or the Student t test, when appropriate. Data are presented as the average ⫾ SD. Probability values were 2-tailed and considered statistically significant if ⬍ .05.
FIGURE 1
Fetus at 16 and 22 weeks of gestation
R ESULTS
Ultrasound images of a fetus at A and B, 16 and 22 weeks of gestational age with normal external bowel (arrows). C, At 36 weeks, external bowel appears dilated (arrows). This fetus underwent uneventful primary closure of the gastroschisis without any complications and left the hospital on day 25 of life. Huh. Prenatal intraabdominal bowel dilation. Am J Obstet Gynecol 2010.
nal-fetus pairs with a prenatal diagnosis of gastroschisis, with at least 1 prenatal ultrasound examination performed at the UCSF Medical Center and delivery at or transported to UCSF as newborn infants for postnatal care. Pregnancies that were complicated by terminations of pregnancy were excluded. Maternal-fetus pairs were also excluded if medical records were incomplete or unavailable. Approval for this study was obtained from the institutional review board at the UCSF Medical Center. All digital images of the prenatal ultrasound studies were reviewed retrospectively by the senior author (R.B.G.) for the following findings: fetal growth parameters, amniotic fluid volume, abdominal wall defect size, and the presence and degree of IBD. If a dilated intraabdominal loop of bowel was identified, the diameter of the loop was measured with electronic calipers from inner wall to inner wall at the region of maximal observed dilation. If IBD was not noted, there was no measurement because IBD was defined as a clinical diagnosis that then can be measured subsequently. As for the comparison of the
degree of IBD among the fetuses, an average diameter was calculated for each trimester in cases in which ⬎1 ultrasound showed IBD. Presence of abnormally dilated extraabdominal bowel loops that was determined by the qualitative descriptions reported by 2 independent sonologists was also recorded. However, exteriorized loops were not remeasured. Maternal charts were reviewed for maternal age and parity, gestational age at evaluation, prenatal care, and the presence of other fetal abnormalities. In addition, the estimated gestational age at the time of delivery, birthweight, the indication for delivery, and the type of delivery were recorded. Postnatal charts were reviewed for method of abdominal wall closure, time to complete abdominal wall defect closure, time to initial and full enteral feeding, frequency of bowelrelated and nonbowel complications, number of days on ventilation, and length of hospital stay. The following bowel complications were considered severe: atresia, perforation, obstruction, necrosis, and volvulus with and without death.
A total of 61 maternal-fetus pairs were identified with prenatal gastroschisis and evaluated at our center. Forty-three maternal-fetus pairs met the criteria for inclusion in our study. Eighteen maternalfetus pairs were excluded for the following reasons: incomplete data such as no maternal identification information (n ⫽ 14), termination of pregnancy (n ⫽ 2), and not yet delivered (n ⫽ 2). The mean maternal age was 23.3 ⫾ 4.7 years. Patients had an average of 3 scans at our institution during their pregnancy; 77% of the patients had at least 1 second- and third-trimester ultrasound available for review. Eight fetuses (19%) were born by cesarean delivery, with indications in 6 cases because of nonreassuring fetal heart tracing, concerning change in bowel status or both; in 1 case because of breech presentation, and in 1 case because of a planned repeat cesarean delivery. Three of the 43 newborns had been born at an outside facility and transferred to our hospital. Forty newborns (93%) underwent staged reduction with a silo, and 3 newborns had primary closure of the abdominal wall defect. Overall, 27 newborns (63%) demonstrated morbidity; the most common bowel complication was atresia, and nonbowel complication was sepsis. Four newborns (9%) had an atresia, 1 of whom also had an intestinal perforation and another who had midgut volvulus, bowel necrosis, and perforation. One patient (2%) had isolated bowel necrosis with associated short gut syndrome and was total parenteral nutrition (TPN)dependent at time of discharge. Four of the 5 newborn infants with severe bowelrelated complications required bowel resection (2 on the first day of life, and the other 2 at approximately 1 month of age).
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TABLE 1
Demographics of the study population Characteristic
All (n ⴝ 43)
No IBD (n ⴝ 27)
Any IBD (n ⴝ 16)
P valuea
Maternal age, y
23.3 ⫾ 4.7
23.2 ⫾ 4.9
23.4 ⫾ 4.5
.92
Vaginal delivery, n (%)
35 (81)
23 (85)
11 (69)
.26
6 (14)
8 (30)
11 (69)
.025
................................................................................................................................................................................................................................................................................................................................................................................ ................................................................................................................................................................................................................................................................................................................................................................................
Delivery indication
................................................................................................................................................................................................................................................................................................................................................................................
35.4 ⫾ 2.2
EGA at delivery, wk
36 ⫾ 1.8
34.2 ⫾ 2.3
.006
................................................................................................................................................................................................................................................................................................................................................................................
Birthweight, g
2433 ⫾ 542
2514 ⫾ 557
2298 ⫾ 505
.21
................................................................................................................................................................................................................................................................................................................................................................................
Defect closure, d
4.3 ⫾ 3.7
3.9 ⫾ 2.6
4.6 ⫾ 5.3
.56
Time on ventilator, d
7 ⫾ 4.6
7.6 ⫾ 5.3
5.9 ⫾ 3.1
.26
Days to initial enteral feeding
15.8 ⫾ 8.2
16.8 ⫾ 9.1
14.1 ⫾ 6.6
.33
Days to full enteral feeding
29.8 ⫾ 18.3
30 ⫾ 19
29.6 ⫾ 17.7
.95
Length of hospitalization, d
36.8 ⫾ 23.2
34.4 ⫾ 20.3
40.9 ⫾ 27.8
.39
................................................................................................................................................................................................................................................................................................................................................................................ ................................................................................................................................................................................................................................................................................................................................................................................ ................................................................................................................................................................................................................................................................................................................................................................................ ................................................................................................................................................................................................................................................................................................................................................................................ ................................................................................................................................................................................................................................................................................................................................................................................
Neonatal death
2 (5%)
1 (4%)
1 (6%)
1.00
Bowel complications
8 (19%)
2 (7%)
6 (38%)
.037
Bowel resections
4 (2%)
1 (4%)
3 (19%)
.14
................................................................................................................................................................................................................................................................................................................................................................................ ................................................................................................................................................................................................................................................................................................................................................................................ ................................................................................................................................................................................................................................................................................................................................................................................
EGA at diagnosis of IBD, wk
—
—
29 ⫾ 5.13
—
IBD diameter, mm
—
—
17.8 ⫾ 6.29
—
................................................................................................................................................................................................................................................................................................................................................................................ ................................................................................................................................................................................................................................................................................................................................................................................
EGA, estimated gestational age; IBD, intraabdominal bowel dilation. a
P value calculated for no IBD vs any IBD groups.
Huh. Prenatal intraabdominal bowel dilation. Am J Obstet Gynecol 2010.
Of the 43 maternal-fetus pairs, 16 fetuses (37%) had some degree of IBD on prenatal ultrasound. These fetuses were delivered earlier, compared with those fetuses without IBD (34.2 ⫾ 2.26 wks vs 36 ⫾ 1.75 wks, respectively; P ⫽ .006). This difference in delivery timing may be due to the more aggressive delivery and treatment for these fetuses who were diagnosed with IBD at our institution. There were no statistically significant differences in maternal age, birthweight, incidence of polyhydramnios, size of abdominal wall defect, or delivery mode between the fetuses with and without IBD. The postnatal outcomes of fetuses with and without IBD are summarized in Table 1. Fetuses with IBD were significantly more likely to have bowel-related complications vs those fetuses without IBD (38% vs 7%; P ⫽ .037). The death rates were similar and low for both the IBD and non-IBD groups: 1 neonatal death (fetus with IBD) was due to bowelrelated complications, and 1 neonatal death (fetus had no IBD) was due to significant liver injury that resulted in coagulopathy and multisystem organ 396.e3
failure. There were no statistically significant differences in estimated gestational age at diagnosis of IBD or interval from detection of dilation to delivery between the fetuses with and without bowel complications. Thirteen of the 16 fetuses with IBD had at least 1 second-trimester ultrasound available for review, and 15 of the 16 fetuses had at least 1 third-trimester ultrasound. Among fetuses with IBD, there was no statistically significant difference in mean diameter of internalized bowel in the fetuses with bowel complications, compared with those infants without complications (P ⫽ .0838; Table 2). When bowel diameter was analyzed by trimesters in those fetuses with IBD, a significantly larger bowel diameter during the third trimester was found in the neonates with bowel complications, compared with those without complications (20.9 ⫾ 8.17 mm vs 12.1 ⫾ 3.46 mm; P ⫽ .0311). The presence of multiple loops of IBD was even more discriminating (Figure 2). Of the 6 fetuses with multiple loops of IBD (14% of all gastroschisis fetuses, 38% of fetuses with IBD), all fetuses had
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postnatal bowel complications. This is in distinct contrast to the group of fetuses without postnatal bowel complications (n ⫽ 10) among whom none of the fetuses demonstrated multiple loops of IBD (P ⫽ .001). Multiple loops of dilated bowel showed a sensitivity of 75%, a negative predictive value 95%, a specificity and positive predictive value of 100% for predicting bowel complications. Furthermore, all fetuses with sustained multiple loops of IBD on subsequent ultrasound examinations had associated bowel obstruction at birth (n ⫽ 4). Early resolution of the multiple dilated loops of IBD was seen in the remaining 2 fetuses, of whom 1 fetus had necrotizing enterocolitis and the other fetus had duodeno-jejuno megaly that required surgical plication (Table 2). A single loop of IBD, however, was not predictive of postnatal bowel complications (Figure 3). None of the fetuses with a single loop of IBD (n ⫽ 10) had postnatal bowel complications (23% of all gastroschisis fetuses, 62% of fetuses with IBD). Dilation of the rectosigmoid and exteriorization of dilated bowel through the abdominal wall defect were common
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TABLE 2
Cases of fetuses with intraabdominal bowel dilation Loop characteristic
EGA at diagnosis of IBD (EGA of prior sonogram)
1
Multiple
18.3 (NP)
2
Multiple
3 4
Case
2nd trimester IBD, mm
3rd trimester IBD, mm
Bowel complication
Surgery
4
Dilation resolved
Nectrotizing enterocolitis
—
23.6 (NP)
12
Dilation resolved
Duodeno-jejuno megaly
Plication
Multiple
24.9 (NP)
16
33
Atresia
Resection
Multiple
25.9 (21.7)
18.5
Small bowel obstruction, bowel necrosis
Resection
Volvulus, perforation of atresia, bowel necrosis
Resection —
................................................................................................................................................................................................................................................................................................................................................................................ ................................................................................................................................................................................................................................................................................................................................................................................ ................................................................................................................................................................................................................................................................................................................................................................................
9.4
................................................................................................................................................................................................................................................................................................................................................................................ a
5
Multiple
31 (NP)
—
16
................................................................................................................................................................................................................................................................................................................................................................................
6
Multiple
35.4 (34.3)
—
16
Partial small bowel obstruction
1
Single
25.4 (NP)
7
—
—
2 3
Single
26.1 (NP)
7
Dilation resolved
—
Single
26.6 (NP)
8
Dilation resolved
—
4
Single
27.7 (NP)
7.4
14
—
5
Single
37 (NP)
—
18
—
6
Single
29 (24.3)
ND
8
—
7
Single
30.1 (26.6)
ND
14.1
—
8
Single
32.7 (21.7)
ND
11
—
9
Single
32.9 (31.9)
ND
9.5
—
10
Single
34.7 (32.7)
ND
10
—
................................................................................................................................................................................................................................................................................................................................................................................ ................................................................................................................................................................................................................................................................................................................................................................................ ................................................................................................................................................................................................................................................................................................................................................................................ ................................................................................................................................................................................................................................................................................................................................................................................ ................................................................................................................................................................................................................................................................................................................................................................................ ................................................................................................................................................................................................................................................................................................................................................................................ ................................................................................................................................................................................................................................................................................................................................................................................ ................................................................................................................................................................................................................................................................................................................................................................................ ................................................................................................................................................................................................................................................................................................................................................................................ ................................................................................................................................................................................................................................................................................................................................................................................ ................................................................................................................................................................................................................................................................................................................................................................................
EGA, estimated gestational age; IBD, intraabdominal bowel dilation; ND, no dilation; NP, no prior sonogram. a
Neonatal death.
Huh. Prenatal intraabdominal bowel dilation. Am J Obstet Gynecol 2010.
findings that were seen exclusively in fetuses with a single dilated loop of intraabdominal bowel. Among fetuses with any IBD (n ⫽ 16), a statistically significant increase in inci-
dence of bowel resections (P ⫽ .036), time to full enteral feeds (P ⫽ .034), and length of hospital stay (P ⫽ .001) was found in the group with multiple loops of dilated intraabdominal bowel (Table
FIGURE 2
Two fetuses at 33 weeks of gestation
3). There was no significant difference in the rate of polyhydramnios between the IBD groups with multiple vs single loop of dilated bowel (33% vs 20%; P ⫽ .60). The sonograms of 20 fetuses (47%) in our series were interpreted as having extraabdominal bowel dilation. There was a greater incidence of extraabdominal bowel dilation in fetuses with IBD (62% vs 37%; P ⫽ .127). There was no statistically significant difference in the incidence of extraabdominal bowel dilation between the groups with multiple loops vs single loop of IBD (67% vs 60%; P ⫽ 1.00).
C OMMENT
Ultrasound images of A and B, 2 fetuses at 33 weeks gestational age with multiple loops of dilated intraabdominal bowel. Postnatally, both fetuses had a small bowel obstruction that required surgical resection. Huh. Prenatal intraabdominal bowel dilation. Am J Obstet Gynecol 2010.
The attempt to establish sonographic criteria for the prediction of outcome in prenatally diagnosed fetuses with gastroschisis has focused mainly on extraabdominal bowel dilation. However, the published literature reflects no consensus as to whether extraabdominal bowel
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FIGURE 3
Ultrasound image
Ultrasound image of a fetus at 32 weeks gestational age with a single loop of dilated intraabdominal bowel (arrow). This fetus underwent uneventful staged reduction of the gastroschisis without complications and left the hospital on day of life 19. STOM, stomach; UB, urinary bladder. Huh. Prenatal intraabdominal bowel dilation. Am J Obstet Gynecol 2010.
dilation is a reliable predictor of poor outcome. In addition to the limitation of a small sample size for most of the studies, there is also significant variation among the different studies in their diagnostic criteria for dilation.3-5,8,9,12-15 Furthermore, in a study by Babcook et al,8 measurement differences between
www.AJOG.org examiners were large enough to shift 13% of fetuses between categories. Unlike extraabdominal bowel dilation, IBD has not received much attention. In a study by Brun et al16 that assessed various ultrasonographic patterns in correlation with postnatal outcome, 1 of the 34 fetuses was noted to have IBD without dilation of the external loops and postnatally was complicated by atresia, multiple surgeries, and an extended hospital stay. Badillo et al,5 however, was unable to demonstrate any association between IBD and neonatal outcome. Our series is the first study to report and investigate both the extent and presence of IBD in fetuses with gastroschisis. Interestingly, IBD in fetuses with gastroschisis was associated with a higher rate of postnatal complications, but only when multiple loops were dilated in the abdomen. This has not been reported previously. Six of the 8 fetuses with bowel-related complications in our series demonstrated multiple dilated loops of intraabdominal bowel, with the earliest detection at estimated gestational age of 18 weeks, whereas none of the 10 fetuses with only a single dilated loop of intraabdominal bowel had postnatal bowel complications. The presence of multiple discrete loops of dilated intra-
abdominal bowel was associated significantly with postnatal bowel complications and, consequently, greater morbidity in terms of number of days to full enteral feedings, bowel resections, and length of hospital stay. Similar cases have been reported by McMahon et al,17 in which sonographic evaluation of 2 pregnancies that were complicated by gastroschisis revealed polyhydramnios and IBD of 48 mm at 34 weeks and 30 mm at 31 weeks, respectively. Postnatally, both neonates had multiple atresias, in addition to bowel necrosis in 1 neonate, and midgut volvulus in the other. Brantberg et al11 also suggested that an increasing IBD in the third trimester may be a warning sign of severe bowel obstruction. Although morbidity was found to be greater in infants with IBD and bowel complications, there was only 1 neonatal death of the 6 neonates with IBD and bowel complications. Both Nick et al1 and Brantberg et al11 also reported that, although the immediate morbidity in terms of hospitalization and time to full enteral feeding was longer, survival rates were not lower for fetuses with intraabdominal dilation and postnatal bowel complications.
TABLE 3
Comparison of postnatal outcome variables between fetuses with multiple vs single dilated loop of intraabdominal bowel Outcome
No IBD (n ⴝ 27)
Bowel complications
Multiple loops of IBD (n ⴝ 6)
Single loop of IBD (n ⴝ 10) 0 (0%)
P valuea
2 (7%)
6 (100%)
Severe
2
3
—
—
.001
Other
—
3
—
—
....................................................................................................................................................................................................................................................................................................................................................................... ....................................................................................................................................................................................................................................................................................................................................................................... .......................................................................................................................................................................................................................................................................................................................................................................
Bowel resection
1 (4%)
3 (50%)
0 (0%)
.036
................................................................................................................................................................................................................................................................................................................................................................................
Extraabdominal bowel dilation
4 (67%)
6 (60%)
Days to complete defect closure
10 (37%)
3.9 ⫾ 2.6
7.5 ⫾ 9.1
3.4 ⫾ 2.7
1.00 .20
Days on ventilator
7.6 ⫾ 5.3
6.6 ⫾ 4
5.6 ⫾ 2.7
.57
Days to initial enteral feeding
16.8 ⫾ 9.1
17.4 ⫾ 9.8
12.5 ⫾ 4
.18
Days to full enteral feeding
23.2 ⫾ 6.9
.034
................................................................................................................................................................................................................................................................................................................................................................................ ................................................................................................................................................................................................................................................................................................................................................................................ ................................................................................................................................................................................................................................................................................................................................................................................ ................................................................................................................................................................................................................................................................................................................................................................................
30 ⫾ 19
44 ⫾ 26.9
TPN-dependent at time of discharge
0 (0%)
1 (17%)
Length of hospitalization
1 (4%)
................................................................................................................................................................................................................................................................................................................................................................................
0 (0%)
.375
................................................................................................................................................................................................................................................................................................................................................................................
69.4 ⫾ 31.3
26.7 ⫾ 9.6
.001
................................................................................................................................................................................................................................................................................................................................................................................
IBD, intraabdominal bowel dilation; TPN, total parenteral nutrition. a
P value calculated for multiple loops vs single loop of IBD groups.
Huh. Prenatal intraabdominal bowel dilation. Am J Obstet Gynecol 2010.
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www.AJOG.org The only reported study in the literature to date to focus on IBD as an important prognostic indicator is by Nick et al.1 In their study, 10 of the 58 fetuses (17%) had IBD, and all had bowel atresia at birth. Among the other 48 fetuses (without IBD), none had bowel atresia. Our series confirms the prognostic importance of fetal IBD in fetuses with gastroschisis. However, our data differed in that not all of the 16 fetuses with IBD had an atresia or other bowel-related complication at birth. Moreover, 2 of the fetuses without IBD also had atresias. Thus, the 100% predictive value of IBD for neonatal bowel atresia that was reported by Nick et al is not confirmed in our study. This difference may be due to the varying severity or sensitivity of detection of IBD in the 2 data groups (37% prevalence in our study; 17% in theirs). We considered any loop of visibly dilated loop in the abdomen to be abnormal. Increased severity in IBD marked by the presence of multiple bowel loops may be a prognostic factor for bowel atresia. This relationship will need further study in future investigations. Sustained dilation of multiple loops of IBD seems to be most important. A report by Brantberg et al11 suggests that sustained IBD was associated in 5 cases with obstruction of the bowel. In our series, all fetuses with sustained multiple loops of IBD (n ⫽ 4) had bowel obstruction at birth. In the 2 fetuses with early resolution of dilation, neither fetus had obstructive bowel complications. Nick et al1 did not specify whether the IBD persists or resolves on subsequent ultrasound examinations after initial diagnosis of dilation. In their study, Nick et al1 reported that IBD was noted by 29 weeks of gestation in all 10 cases and that, in 8 of the 10 cases, it was detected at ⬍25 weeks of gestation. In our data, IBD was detected as early as 18 weeks of gestation but was also not detected until 35 weeks of gesta-
tion in 1 fetus (with previous sonograms) who had a partial small bowel obstruction at birth. The presence of multiple loops of IBD, however, was detected by 25 weeks of gestation in all fetuses with associated severe bowel obstruction, except for 1 case in which an initial ultrasound was performed at 31 weeks of gestation. This suggests that, although IBD (single or multiple dilated loops) may develop in both the second and third trimesters, sustained multiple dilated loops that are detected initially in the second trimester may be a predictor of severe bowel obstruction. Long-term follow-up was not reviewed in this series, but our follow-up was, on average, ⬎1 month after delivery and observed with each neonate until the time of discharge. This suggests that our findings may be predictive not only during the acute hospitalization after delivery but also may carry prognostic significance for long-term outcomes. Our study is limited by the retrospective design of the study but is strengthened by the comprehensive and consecutive nature of the series of all patients who are treated at our institution. This study represents the largest review of fetuses with IBD in the setting of prenatally diagnosed gastroschisis to date. Multiple loops of IBD in the second trimester is an important observation in fetuses with gastroschisis and is associated with bowel complications and poorer outcomes. f REFERENCES 1. Nick AM, Bruner JP, Moses R, Yang EY, Scott TA. Second-trimester intra-abdominal bowel dilation in fetuses with gastroschisis predicts neonatal bowel atresia. Ultrasound Obstet Gynecol 2006;28:821-5. 2. Wilson RD, Johnson MP. Congenital abdominal wall defects: an update. Fetal Diagn Ther 2004;19:385-98. 3. Japaraj RP, Hockey R, Chan FY. Gastroschisis: can prenatal sonography predict neonatal outcome? Ultrasound Obstet Gynecol 2003;21: 329-33.
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4. Alsulyman OM, Monteiro H, Ouzounian JG, Barton L, Songster GS, Kovacs BW. Clinical significance of prenatal ultrasonographic intestinal dilatation in fetuses with gastroschisis. Am J Obstet Gynecol 1996;175:982-4. 5. Badillo AT, Hedrick HL, Wilson RD, et al. Prenatal ultrasonographic gastrointestinal abnormalities in fetuses with gastroschisis do not correlate with postnatal outcomes. J Pediatr Surg 2008;43:647-53. 6. Torfs C, Curry C, Roeper P. Gastroschisis. J Pediatr 1990;116:1-6. 7. Aina-Mumuney AJ, Fischer AC, Blakemore KJ, et al. A dilated fetal stomach predicts a complicated postnatal course in cases of prenatally diagnosed gastroschisis. Am J Obstet Gynecol 2004;190:1326-30. 8. Babcook CJ, Hedrick MH, Goldstein RB, et al. Gastroschisis: can sonography of the fetal bowel accurately predict postnatal outcome? J Ultrasound Med 1994;13:701-6. 9. Bond SJ, Harrison MR, Filly RA, Callen PW, Anderson RA, Golbus MS. Severity of intestinal damage in gastroschisis: correlation with prenatal sonographic findings. J Pediatr Surg 1988;23:520-5. 10. Molik KA, Gingalewski CA, West KW, et al. Gastroschisis: a plea for risk categorization. J Pediatr Surg 2001;36:51-5. 11. Brantberg A, Blaas HG, Salvesen KA, Haugen SE, Eik-Nes SH. Surveillance and outcome of fetuses with gastroschisis. Ultrasound Obstet Gynecol 2004;23:4-13. 12. Langer JC, Khanna J, Caco C, Dykes EH, Nicolaides KH. Prenatal diagnosis of gastroschisis: development of objective sonographic criteria for predicting outcome. Obstet Gynecol 1993;81:53-6. 13. Lenke RR, Persutte WH, Nemes J. Ultrasonographic assessment of intestinal damage in fetuses with gastroschisis: is it of clinical value? Am J Obstet Gynecol 1990;163:995-8. 14. Pryde PG, Bardicef M, Treadwell MC, Klein M, Isada NB, Evans MI. Gastroschisis: can antenatal ultrasound predict infant outcomes? Obstet Gynecol 1994;84:505-10. 15. Sipes SL, Weiner CP, Williamson RA, Pringle KC, Kimura K. Fetal gastroschisis complicated by bowel dilation: an indication for imminent delivery? Fetal Diagn Ther 1990;5:100-3. 16. Brun M, Grignon A, Guibaud L, Garel L, Saint-Vil D. Gastroschisis: are prenatal ultrasonographic findings useful for assessing the prognosis? Pediatr Radiol 1996;26:723-6. 17. McMahon MJ, Kuller JA, Chescheir NC. Prenatal ultrasonographic findings associated with short bowel syndrome in two fetuses with gastroschisis. Obstet Gynecol 1996;88:676-8.
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www. AJOG.org
IMAGING
Prenatal intraabdominal bowel dilation is associated with postnatal gastrointestinal complications in fetuses with gastroschisis Nancy G. Huh, MD; Shinjiro Hirose, MD; Ruth B. Goldstein, MD OBJECTIVE: The purpose of this study was to determine whether pre-
natal intraabdominal bowel dilation (IBD) is associated with increased postnatal complications in fetuses with gastroschisis. STUDY DESIGN: A retrospective review was performed on all maternalfetus pairs with prenatally diagnosed gastroschisis that was treated at the University of California San Francisco from 2002-2008. Postnatal outcomes were compared between fetuses with and without IBD.
as opposed to a single loop (n ⫽ 10) was associated highly with bowel complications and increased time to full enteral feeding and length of hospital stay (100% vs 0% [P ⫽ .001]; 44 vs 23 days [P ⫽ .034]; 69 vs 27 days [P ⫽ .001], respectively). CONCLUSION: IBD is associated with increased postnatal complica-
RESULTS: Forty-three of 61 maternal-fetal pairs met the criteria for in-
tions in infants with prenatally diagnosed gastroschisis; however, this association seems to be limited to those with multiple loops of dilated intraabdominal bowel.
clusion. Sixteen fetuses (37%) had evidence of IBD. Fetuses with IBD were significantly more likely to have postnatal bowel complications (38% vs 7%; P ⫽ .037). The presence of multiple loops of IBD (n ⫽ 6)
Key words: bowel complication, fetus, gastroschisis, intraabdominal bowel dilation, postnatal outcome, ultrasound
Cite this article as: Huh NG, Hirose S, Goldstein RB. Prenatal intraabdominal bowel dilation is associated with postnatal gastrointestinal complications in fetuses with gastroschisis. Am J Obstet Gynecol 2010;202:396.e1-6.
G
astroschisis is a congenital anomaly that is characterized by the herniation of fetal intestine through a fullthickness defect in the abdominal wall. The incidence of gastroschisis ranges from 0.5-1 per 10,000 births.1,2 Prenatal detection of gastroschisis is facilitated by the combination of maternal serum alpha fetoprotein measurement and widespread use of routine prenatal ultrasound. The apparent increase in incidence of prenatally detected gastroschisis over the past 2 decades has been From the Department of Radiology, University of California at San Francisco School of Medicine, San Francisco, CA. Received March 26, 2009; revised Aug. 13, 2009; accepted Oct. 29, 2009. Reprints: Ruth B. Goldstein, MD, Department of Radiology, University of California at San Francisco, 505 Parnassus Ave, San Francisco, CA 94143. Authorship and contribution to the article is limited to the 3 authors indicated. There was no outside funding or technical assistance with the production of this article. 0002-9378/$36.00 © 2010 Mosby, Inc. All rights reserved. doi: 10.1016/j.ajog.2009.10.888
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attributed to these advancements in screening and detection.3-6 Although the overall survival rate for neonates with gastroschisis is very good (range, 90 –97%7-10) both morbidity and mortality rates are highly correlated with the degree of bowel disease at birth. Gastrointestinal complications such as perforation or atresia occur in 10-20% of cases.11 Presence of gastrointestinal complications is associated with mortality rates as high as 28%, longer hospitalization, and prolonged parenteral nutrition with its accompanying risks of infection, growth restriction, metabolic disturbances, and severe liver disease.1,2,5,12 Identification of prenatal prognostic factors would help identify which patients would benefit from intensive fetal surveillance and potentially early intervention or delivery and more informed parental counseling. Identification of discriminating prenatal indicators of outcome has not been very successful. Dilation of extraabdominal bowel loops has been studied but has not been proved to be a useful predictor of postnatal outcome.1,3-5 The differences in definition of dilation and
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small sample sizes of previous studies limit the consensus on which measurements are consistently predictive of poor outcome.1,3-5 Furthermore, externalized bowel seems to dilate as “normal” phenomenon in many gastroschisis fetuses in the third trimester who do very well after birth (Figure 1). The development of intraabdominal bowel dilation (IBD) in these fetuses is much less common, with an estimated report in the limited published literature on this topic that ranges from 8-17%.1,11 In a recent study, Nick et al1 suggested that the presence of IBD in fetuses with gastroschisis may have important prognostic value. The purpose of this study was to evaluate whether IBD in fetuses with gastroschisis is associated with increased postnatal complications.
M ETHODS A retrospective review was conducted on all cases of gastroschisis who were delivered at our institution, the University of California San Francisco (UCSF), between May 2002 and June 2008. The study population included those mater-
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Differences between fetal groups with and without IBD were determined by use of the Fisher’s exact test or the Student t test, when appropriate. Data are presented as the average ⫾ SD. Probability values were 2-tailed and considered statistically significant if ⬍ .05.
FIGURE 1
Fetus at 16 and 22 weeks of gestation
R ESULTS
Ultrasound images of a fetus at A and B, 16 and 22 weeks of gestational age with normal external bowel (arrows). C, At 36 weeks, external bowel appears dilated (arrows). This fetus underwent uneventful primary closure of the gastroschisis without any complications and left the hospital on day 25 of life. Huh. Prenatal intraabdominal bowel dilation. Am J Obstet Gynecol 2010.
nal-fetus pairs with a prenatal diagnosis of gastroschisis, with at least 1 prenatal ultrasound examination performed at the UCSF Medical Center and delivery at or transported to UCSF as newborn infants for postnatal care. Pregnancies that were complicated by terminations of pregnancy were excluded. Maternal-fetus pairs were also excluded if medical records were incomplete or unavailable. Approval for this study was obtained from the institutional review board at the UCSF Medical Center. All digital images of the prenatal ultrasound studies were reviewed retrospectively by the senior author (R.B.G.) for the following findings: fetal growth parameters, amniotic fluid volume, abdominal wall defect size, and the presence and degree of IBD. If a dilated intraabdominal loop of bowel was identified, the diameter of the loop was measured with electronic calipers from inner wall to inner wall at the region of maximal observed dilation. If IBD was not noted, there was no measurement because IBD was defined as a clinical diagnosis that then can be measured subsequently. As for the comparison of the
degree of IBD among the fetuses, an average diameter was calculated for each trimester in cases in which ⬎1 ultrasound showed IBD. Presence of abnormally dilated extraabdominal bowel loops that was determined by the qualitative descriptions reported by 2 independent sonologists was also recorded. However, exteriorized loops were not remeasured. Maternal charts were reviewed for maternal age and parity, gestational age at evaluation, prenatal care, and the presence of other fetal abnormalities. In addition, the estimated gestational age at the time of delivery, birthweight, the indication for delivery, and the type of delivery were recorded. Postnatal charts were reviewed for method of abdominal wall closure, time to complete abdominal wall defect closure, time to initial and full enteral feeding, frequency of bowelrelated and nonbowel complications, number of days on ventilation, and length of hospital stay. The following bowel complications were considered severe: atresia, perforation, obstruction, necrosis, and volvulus with and without death.
A total of 61 maternal-fetus pairs were identified with prenatal gastroschisis and evaluated at our center. Forty-three maternal-fetus pairs met the criteria for inclusion in our study. Eighteen maternalfetus pairs were excluded for the following reasons: incomplete data such as no maternal identification information (n ⫽ 14), termination of pregnancy (n ⫽ 2), and not yet delivered (n ⫽ 2). The mean maternal age was 23.3 ⫾ 4.7 years. Patients had an average of 3 scans at our institution during their pregnancy; 77% of the patients had at least 1 second- and third-trimester ultrasound available for review. Eight fetuses (19%) were born by cesarean delivery, with indications in 6 cases because of nonreassuring fetal heart tracing, concerning change in bowel status or both; in 1 case because of breech presentation, and in 1 case because of a planned repeat cesarean delivery. Three of the 43 newborns had been born at an outside facility and transferred to our hospital. Forty newborns (93%) underwent staged reduction with a silo, and 3 newborns had primary closure of the abdominal wall defect. Overall, 27 newborns (63%) demonstrated morbidity; the most common bowel complication was atresia, and nonbowel complication was sepsis. Four newborns (9%) had an atresia, 1 of whom also had an intestinal perforation and another who had midgut volvulus, bowel necrosis, and perforation. One patient (2%) had isolated bowel necrosis with associated short gut syndrome and was total parenteral nutrition (TPN)dependent at time of discharge. Four of the 5 newborn infants with severe bowelrelated complications required bowel resection (2 on the first day of life, and the other 2 at approximately 1 month of age).
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TABLE 1
Demographics of the study population Characteristic
All (n ⴝ 43)
No IBD (n ⴝ 27)
Any IBD (n ⴝ 16)
P valuea
Maternal age, y
23.3 ⫾ 4.7
23.2 ⫾ 4.9
23.4 ⫾ 4.5
.92
Vaginal delivery, n (%)
35 (81)
23 (85)
11 (69)
.26
6 (14)
8 (30)
11 (69)
.025
................................................................................................................................................................................................................................................................................................................................................................................ ................................................................................................................................................................................................................................................................................................................................................................................
Delivery indication
................................................................................................................................................................................................................................................................................................................................................................................
35.4 ⫾ 2.2
EGA at delivery, wk
36 ⫾ 1.8
34.2 ⫾ 2.3
.006
................................................................................................................................................................................................................................................................................................................................................................................
Birthweight, g
2433 ⫾ 542
2514 ⫾ 557
2298 ⫾ 505
.21
................................................................................................................................................................................................................................................................................................................................................................................
Defect closure, d
4.3 ⫾ 3.7
3.9 ⫾ 2.6
4.6 ⫾ 5.3
.56
Time on ventilator, d
7 ⫾ 4.6
7.6 ⫾ 5.3
5.9 ⫾ 3.1
.26
Days to initial enteral feeding
15.8 ⫾ 8.2
16.8 ⫾ 9.1
14.1 ⫾ 6.6
.33
Days to full enteral feeding
29.8 ⫾ 18.3
30 ⫾ 19
29.6 ⫾ 17.7
.95
Length of hospitalization, d
36.8 ⫾ 23.2
34.4 ⫾ 20.3
40.9 ⫾ 27.8
.39
................................................................................................................................................................................................................................................................................................................................................................................ ................................................................................................................................................................................................................................................................................................................................................................................ ................................................................................................................................................................................................................................................................................................................................................................................ ................................................................................................................................................................................................................................................................................................................................................................................ ................................................................................................................................................................................................................................................................................................................................................................................
Neonatal death
2 (5%)
1 (4%)
1 (6%)
1.00
Bowel complications
8 (19%)
2 (7%)
6 (38%)
.037
Bowel resections
4 (2%)
1 (4%)
3 (19%)
.14
................................................................................................................................................................................................................................................................................................................................................................................ ................................................................................................................................................................................................................................................................................................................................................................................ ................................................................................................................................................................................................................................................................................................................................................................................
EGA at diagnosis of IBD, wk
—
—
29 ⫾ 5.13
—
IBD diameter, mm
—
—
17.8 ⫾ 6.29
—
................................................................................................................................................................................................................................................................................................................................................................................ ................................................................................................................................................................................................................................................................................................................................................................................
EGA, estimated gestational age; IBD, intraabdominal bowel dilation. a
P value calculated for no IBD vs any IBD groups.
Huh. Prenatal intraabdominal bowel dilation. Am J Obstet Gynecol 2010.
Of the 43 maternal-fetus pairs, 16 fetuses (37%) had some degree of IBD on prenatal ultrasound. These fetuses were delivered earlier, compared with those fetuses without IBD (34.2 ⫾ 2.26 wks vs 36 ⫾ 1.75 wks, respectively; P ⫽ .006). This difference in delivery timing may be due to the more aggressive delivery and treatment for these fetuses who were diagnosed with IBD at our institution. There were no statistically significant differences in maternal age, birthweight, incidence of polyhydramnios, size of abdominal wall defect, or delivery mode between the fetuses with and without IBD. The postnatal outcomes of fetuses with and without IBD are summarized in Table 1. Fetuses with IBD were significantly more likely to have bowel-related complications vs those fetuses without IBD (38% vs 7%; P ⫽ .037). The death rates were similar and low for both the IBD and non-IBD groups: 1 neonatal death (fetus with IBD) was due to bowelrelated complications, and 1 neonatal death (fetus had no IBD) was due to significant liver injury that resulted in coagulopathy and multisystem organ 396.e3
failure. There were no statistically significant differences in estimated gestational age at diagnosis of IBD or interval from detection of dilation to delivery between the fetuses with and without bowel complications. Thirteen of the 16 fetuses with IBD had at least 1 second-trimester ultrasound available for review, and 15 of the 16 fetuses had at least 1 third-trimester ultrasound. Among fetuses with IBD, there was no statistically significant difference in mean diameter of internalized bowel in the fetuses with bowel complications, compared with those infants without complications (P ⫽ .0838; Table 2). When bowel diameter was analyzed by trimesters in those fetuses with IBD, a significantly larger bowel diameter during the third trimester was found in the neonates with bowel complications, compared with those without complications (20.9 ⫾ 8.17 mm vs 12.1 ⫾ 3.46 mm; P ⫽ .0311). The presence of multiple loops of IBD was even more discriminating (Figure 2). Of the 6 fetuses with multiple loops of IBD (14% of all gastroschisis fetuses, 38% of fetuses with IBD), all fetuses had
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postnatal bowel complications. This is in distinct contrast to the group of fetuses without postnatal bowel complications (n ⫽ 10) among whom none of the fetuses demonstrated multiple loops of IBD (P ⫽ .001). Multiple loops of dilated bowel showed a sensitivity of 75%, a negative predictive value 95%, a specificity and positive predictive value of 100% for predicting bowel complications. Furthermore, all fetuses with sustained multiple loops of IBD on subsequent ultrasound examinations had associated bowel obstruction at birth (n ⫽ 4). Early resolution of the multiple dilated loops of IBD was seen in the remaining 2 fetuses, of whom 1 fetus had necrotizing enterocolitis and the other fetus had duodeno-jejuno megaly that required surgical plication (Table 2). A single loop of IBD, however, was not predictive of postnatal bowel complications (Figure 3). None of the fetuses with a single loop of IBD (n ⫽ 10) had postnatal bowel complications (23% of all gastroschisis fetuses, 62% of fetuses with IBD). Dilation of the rectosigmoid and exteriorization of dilated bowel through the abdominal wall defect were common
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TABLE 2
Cases of fetuses with intraabdominal bowel dilation Loop characteristic
EGA at diagnosis of IBD (EGA of prior sonogram)
1
Multiple
18.3 (NP)
2
Multiple
3 4
Case
2nd trimester IBD, mm
3rd trimester IBD, mm
Bowel complication
Surgery
4
Dilation resolved
Nectrotizing enterocolitis
—
23.6 (NP)
12
Dilation resolved
Duodeno-jejuno megaly
Plication
Multiple
24.9 (NP)
16
33
Atresia
Resection
Multiple
25.9 (21.7)
18.5
Small bowel obstruction, bowel necrosis
Resection
Volvulus, perforation of atresia, bowel necrosis
Resection —
................................................................................................................................................................................................................................................................................................................................................................................ ................................................................................................................................................................................................................................................................................................................................................................................ ................................................................................................................................................................................................................................................................................................................................................................................
9.4
................................................................................................................................................................................................................................................................................................................................................................................ a
5
Multiple
31 (NP)
—
16
................................................................................................................................................................................................................................................................................................................................................................................
6
Multiple
35.4 (34.3)
—
16
Partial small bowel obstruction
1
Single
25.4 (NP)
7
—
—
2 3
Single
26.1 (NP)
7
Dilation resolved
—
Single
26.6 (NP)
8
Dilation resolved
—
4
Single
27.7 (NP)
7.4
14
—
5
Single
37 (NP)
—
18
—
6
Single
29 (24.3)
ND
8
—
7
Single
30.1 (26.6)
ND
14.1
—
8
Single
32.7 (21.7)
ND
11
—
9
Single
32.9 (31.9)
ND
9.5
—
10
Single
34.7 (32.7)
ND
10
—
................................................................................................................................................................................................................................................................................................................................................................................ ................................................................................................................................................................................................................................................................................................................................................................................ ................................................................................................................................................................................................................................................................................................................................................................................ ................................................................................................................................................................................................................................................................................................................................................................................ ................................................................................................................................................................................................................................................................................................................................................................................ ................................................................................................................................................................................................................................................................................................................................................................................ ................................................................................................................................................................................................................................................................................................................................................................................ ................................................................................................................................................................................................................................................................................................................................................................................ ................................................................................................................................................................................................................................................................................................................................................................................ ................................................................................................................................................................................................................................................................................................................................................................................ ................................................................................................................................................................................................................................................................................................................................................................................
EGA, estimated gestational age; IBD, intraabdominal bowel dilation; ND, no dilation; NP, no prior sonogram. a
Neonatal death.
Huh. Prenatal intraabdominal bowel dilation. Am J Obstet Gynecol 2010.
findings that were seen exclusively in fetuses with a single dilated loop of intraabdominal bowel. Among fetuses with any IBD (n ⫽ 16), a statistically significant increase in inci-
dence of bowel resections (P ⫽ .036), time to full enteral feeds (P ⫽ .034), and length of hospital stay (P ⫽ .001) was found in the group with multiple loops of dilated intraabdominal bowel (Table
FIGURE 2
Two fetuses at 33 weeks of gestation
3). There was no significant difference in the rate of polyhydramnios between the IBD groups with multiple vs single loop of dilated bowel (33% vs 20%; P ⫽ .60). The sonograms of 20 fetuses (47%) in our series were interpreted as having extraabdominal bowel dilation. There was a greater incidence of extraabdominal bowel dilation in fetuses with IBD (62% vs 37%; P ⫽ .127). There was no statistically significant difference in the incidence of extraabdominal bowel dilation between the groups with multiple loops vs single loop of IBD (67% vs 60%; P ⫽ 1.00).
C OMMENT
Ultrasound images of A and B, 2 fetuses at 33 weeks gestational age with multiple loops of dilated intraabdominal bowel. Postnatally, both fetuses had a small bowel obstruction that required surgical resection. Huh. Prenatal intraabdominal bowel dilation. Am J Obstet Gynecol 2010.
The attempt to establish sonographic criteria for the prediction of outcome in prenatally diagnosed fetuses with gastroschisis has focused mainly on extraabdominal bowel dilation. However, the published literature reflects no consensus as to whether extraabdominal bowel
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FIGURE 3
Ultrasound image
Ultrasound image of a fetus at 32 weeks gestational age with a single loop of dilated intraabdominal bowel (arrow). This fetus underwent uneventful staged reduction of the gastroschisis without complications and left the hospital on day of life 19. STOM, stomach; UB, urinary bladder. Huh. Prenatal intraabdominal bowel dilation. Am J Obstet Gynecol 2010.
dilation is a reliable predictor of poor outcome. In addition to the limitation of a small sample size for most of the studies, there is also significant variation among the different studies in their diagnostic criteria for dilation.3-5,8,9,12-15 Furthermore, in a study by Babcook et al,8 measurement differences between
www.AJOG.org examiners were large enough to shift 13% of fetuses between categories. Unlike extraabdominal bowel dilation, IBD has not received much attention. In a study by Brun et al16 that assessed various ultrasonographic patterns in correlation with postnatal outcome, 1 of the 34 fetuses was noted to have IBD without dilation of the external loops and postnatally was complicated by atresia, multiple surgeries, and an extended hospital stay. Badillo et al,5 however, was unable to demonstrate any association between IBD and neonatal outcome. Our series is the first study to report and investigate both the extent and presence of IBD in fetuses with gastroschisis. Interestingly, IBD in fetuses with gastroschisis was associated with a higher rate of postnatal complications, but only when multiple loops were dilated in the abdomen. This has not been reported previously. Six of the 8 fetuses with bowel-related complications in our series demonstrated multiple dilated loops of intraabdominal bowel, with the earliest detection at estimated gestational age of 18 weeks, whereas none of the 10 fetuses with only a single dilated loop of intraabdominal bowel had postnatal bowel complications. The presence of multiple discrete loops of dilated intra-
abdominal bowel was associated significantly with postnatal bowel complications and, consequently, greater morbidity in terms of number of days to full enteral feedings, bowel resections, and length of hospital stay. Similar cases have been reported by McMahon et al,17 in which sonographic evaluation of 2 pregnancies that were complicated by gastroschisis revealed polyhydramnios and IBD of 48 mm at 34 weeks and 30 mm at 31 weeks, respectively. Postnatally, both neonates had multiple atresias, in addition to bowel necrosis in 1 neonate, and midgut volvulus in the other. Brantberg et al11 also suggested that an increasing IBD in the third trimester may be a warning sign of severe bowel obstruction. Although morbidity was found to be greater in infants with IBD and bowel complications, there was only 1 neonatal death of the 6 neonates with IBD and bowel complications. Both Nick et al1 and Brantberg et al11 also reported that, although the immediate morbidity in terms of hospitalization and time to full enteral feeding was longer, survival rates were not lower for fetuses with intraabdominal dilation and postnatal bowel complications.
TABLE 3
Comparison of postnatal outcome variables between fetuses with multiple vs single dilated loop of intraabdominal bowel Outcome
No IBD (n ⴝ 27)
Bowel complications
Multiple loops of IBD (n ⴝ 6)
Single loop of IBD (n ⴝ 10) 0 (0%)
P valuea
2 (7%)
6 (100%)
Severe
2
3
—
—
.001
Other
—
3
—
—
....................................................................................................................................................................................................................................................................................................................................................................... ....................................................................................................................................................................................................................................................................................................................................................................... .......................................................................................................................................................................................................................................................................................................................................................................
Bowel resection
1 (4%)
3 (50%)
0 (0%)
.036
................................................................................................................................................................................................................................................................................................................................................................................
Extraabdominal bowel dilation
4 (67%)
6 (60%)
Days to complete defect closure
10 (37%)
3.9 ⫾ 2.6
7.5 ⫾ 9.1
3.4 ⫾ 2.7
1.00 .20
Days on ventilator
7.6 ⫾ 5.3
6.6 ⫾ 4
5.6 ⫾ 2.7
.57
Days to initial enteral feeding
16.8 ⫾ 9.1
17.4 ⫾ 9.8
12.5 ⫾ 4
.18
Days to full enteral feeding
23.2 ⫾ 6.9
.034
................................................................................................................................................................................................................................................................................................................................................................................ ................................................................................................................................................................................................................................................................................................................................................................................ ................................................................................................................................................................................................................................................................................................................................................................................ ................................................................................................................................................................................................................................................................................................................................................................................
30 ⫾ 19
44 ⫾ 26.9
TPN-dependent at time of discharge
0 (0%)
1 (17%)
Length of hospitalization
1 (4%)
................................................................................................................................................................................................................................................................................................................................................................................
0 (0%)
.375
................................................................................................................................................................................................................................................................................................................................................................................
69.4 ⫾ 31.3
26.7 ⫾ 9.6
.001
................................................................................................................................................................................................................................................................................................................................................................................
IBD, intraabdominal bowel dilation; TPN, total parenteral nutrition. a
P value calculated for multiple loops vs single loop of IBD groups.
Huh. Prenatal intraabdominal bowel dilation. Am J Obstet Gynecol 2010.
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www.AJOG.org The only reported study in the literature to date to focus on IBD as an important prognostic indicator is by Nick et al.1 In their study, 10 of the 58 fetuses (17%) had IBD, and all had bowel atresia at birth. Among the other 48 fetuses (without IBD), none had bowel atresia. Our series confirms the prognostic importance of fetal IBD in fetuses with gastroschisis. However, our data differed in that not all of the 16 fetuses with IBD had an atresia or other bowel-related complication at birth. Moreover, 2 of the fetuses without IBD also had atresias. Thus, the 100% predictive value of IBD for neonatal bowel atresia that was reported by Nick et al is not confirmed in our study. This difference may be due to the varying severity or sensitivity of detection of IBD in the 2 data groups (37% prevalence in our study; 17% in theirs). We considered any loop of visibly dilated loop in the abdomen to be abnormal. Increased severity in IBD marked by the presence of multiple bowel loops may be a prognostic factor for bowel atresia. This relationship will need further study in future investigations. Sustained dilation of multiple loops of IBD seems to be most important. A report by Brantberg et al11 suggests that sustained IBD was associated in 5 cases with obstruction of the bowel. In our series, all fetuses with sustained multiple loops of IBD (n ⫽ 4) had bowel obstruction at birth. In the 2 fetuses with early resolution of dilation, neither fetus had obstructive bowel complications. Nick et al1 did not specify whether the IBD persists or resolves on subsequent ultrasound examinations after initial diagnosis of dilation. In their study, Nick et al1 reported that IBD was noted by 29 weeks of gestation in all 10 cases and that, in 8 of the 10 cases, it was detected at ⬍25 weeks of gestation. In our data, IBD was detected as early as 18 weeks of gestation but was also not detected until 35 weeks of gesta-
tion in 1 fetus (with previous sonograms) who had a partial small bowel obstruction at birth. The presence of multiple loops of IBD, however, was detected by 25 weeks of gestation in all fetuses with associated severe bowel obstruction, except for 1 case in which an initial ultrasound was performed at 31 weeks of gestation. This suggests that, although IBD (single or multiple dilated loops) may develop in both the second and third trimesters, sustained multiple dilated loops that are detected initially in the second trimester may be a predictor of severe bowel obstruction. Long-term follow-up was not reviewed in this series, but our follow-up was, on average, ⬎1 month after delivery and observed with each neonate until the time of discharge. This suggests that our findings may be predictive not only during the acute hospitalization after delivery but also may carry prognostic significance for long-term outcomes. Our study is limited by the retrospective design of the study but is strengthened by the comprehensive and consecutive nature of the series of all patients who are treated at our institution. This study represents the largest review of fetuses with IBD in the setting of prenatally diagnosed gastroschisis to date. Multiple loops of IBD in the second trimester is an important observation in fetuses with gastroschisis and is associated with bowel complications and poorer outcomes. f REFERENCES 1. Nick AM, Bruner JP, Moses R, Yang EY, Scott TA. Second-trimester intra-abdominal bowel dilation in fetuses with gastroschisis predicts neonatal bowel atresia. Ultrasound Obstet Gynecol 2006;28:821-5. 2. Wilson RD, Johnson MP. Congenital abdominal wall defects: an update. Fetal Diagn Ther 2004;19:385-98. 3. Japaraj RP, Hockey R, Chan FY. Gastroschisis: can prenatal sonography predict neonatal outcome? Ultrasound Obstet Gynecol 2003;21: 329-33.
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