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Prenatal Risk Factors and Outcomes

in Gastroschisis: A Meta-Analysis
Francesco DAntonio, MD, PhDa, Calogero Virgone, MDb, Giuseppe Rizzo, MDc, Asma Khalil, MDa, David Baud, MD, PhDd,
Titia E. Cohen-Overbeek, MD, PhDe, Marina Kuleva, MDf, Laurent J. Salomon, MD, PhDf, Maria Elena Flacco, MDg,h,
Lamberto Manzoli, MD, PhDg,h, Stefano Giuliani, MD, PhDb

BACKGROUND AND OBJECTIVE: Gastroschisis is a congenital anomaly with increasing incidence, easy prenatal abstract
diagnosis and extremely variable postnatal outcomes. Our objective was to systematically review the
evidence regarding the association between prenatal ultrasound signs (intraabdominal bowel dilatation
[IABD], extraabdominal bowel dilatation, gastric dilatation [GD], bowel wall thickness, polyhydramnios, and
small for gestational age) and perinatal outcomes in gastroschisis (bowel atresia, intra uterine death,
neonatal death, time to full enteral feeding, length of total parenteral nutrition and length of in hospital stay).
METHODS: Medline, Embase, and Cochrane databases were searched electronically. Studies exploring the
association between antenatal ultrasound signs and outcomes in gastroschisis were considered suitable
for inclusion. Two reviewers independently extracted relevant data regarding study characteristics and
pregnancy outcome. All meta-analyses were computed using individual data random-effect logistic
regression, with single study as the cluster unit.
RESULTS: Twenty-six studies, including 2023 fetuses, were included. We found signicant positive associations
between IABD and bowel atresia (odds ratio [OR]: 5.48, 95% condence interval [CI] 3.19.8), polyhydramnios
and bowel atresia (OR: 3.76, 95% CI 1.78.3), and GD and neonatal death (OR: 5.58, 95% CI 1.324.1). No other
ultrasound sign was signicantly related to any other outcome.
CONCLUSIONS: IABD, polyhydramnios, and GD can be used to an extent to identify a subgroup of neonates
with a prenatal diagnosis of gastroschisis at higher risk to develop postnatal complications. Data are still
inconclusive on the predictive ability of several signs combined, and large prospective studies are needed
to improve the quality of prenatal counseling and the neonatal care for this condition.

a
Fetal Medicine Unit, Division of Developmental Sciences, St Georges University of London, London, United Kingdom; bDepartment of Paediatric and Neonatal Surgery, St Georges Healthcare
National Health Service Trust and University of London, London, United Kingdom; cDepartment of Obstetrics and Gynecology, Universit di Roma Tor Vergata, Roma, Italy; dMaterno-Fetal and
Obstetrics Research Unit, Department of Obstetrics and Gynaecology, University Hospital, Lausanne, Switzerland; eDepartment of Obstetrics and Gynaecology, Division of Obstetrics and
Prenatal Medicine, Erasmus MC, Rotterdam, The Netherlands; fMaternit, Hpital Necker-Enfants Malades, Assistance Publique des Hpitaux de Paris, Universit Paris Descartes, Paris, France;
g
Department of Medicine and Aging Sciences, University of Chieti-Pescara, Chieti, Italy; and hEMISAC (Epidemiologia e Management dellInvecchiamento, e Salubrit degli Ambienti Connati),
CeSI Biotech, Chieti, Italy

Drs DAntonio and Giuliani designed and conceptualized the study, extracted the data, performed the statistical analysis, wrote the manuscript, and reviewed and revised the
manuscript; Dr Virgone designed and conceptualized the study, extracted the data, performed the statistical analysis, wrote the manuscript, and reviewed and revised the
manuscript; Drs Rizzo, Khalil, Cohen-Overbeeck, Baud, Kuleva, and Salomon designed the study, contributed to data extraction, and reviewed and revised the manuscript;
Drs Flacco and Manzoli designed the study, performed statistical analysis, and reviewed the manuscript; and all authors approved the nal manuscript as submitted.
www.pediatrics.org/cgi/doi/10.1542/peds.2015-0017
DOI: 10.1542/peds.2015-0017
Accepted for publication Apr 14, 2015
Address correspondence to Stefano Giuliani, MD, PhD, Department of Paediatric and Neonatal Surgery, St Georges Healthcare NHS Trust and University of London,
Blackshaw Rd, London SW17 0QT, United Kingdom. E-mail: Stefano.giuliani@nhs.net
PEDIATRICS (ISSN Numbers: Print, 0031-4005; Online, 1098-4275).
Copyright 2015 by the American Academy of Pediatrics
FINANCIAL DISCLOSURE: The authors have indicated they have no nancial relationships relevant to this article to disclose.
FUNDING: No external funding.
POTENTIAL CONFLICT OF INTEREST: The authors have indicated they have no potential conicts of interest to disclose.

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PEDIATRICS Volume 136, number 1, July 2015 REVIEW ARTICLE
Gastroschisis is an abdominal wall However, these studies were often gestational age at examination, and
defect located on the right side of the based on small sample sizes, and the ultrasound signs explored. Two authors
umbilicus that allows herniation of the results did not reach good evidence (FD, CV) reviewed all abstracts
abdominal content and its direct examining single data sets in isolation. independently. Agreement about
exposure to the amniotic uid for the The aim of this study was to dene potential relevance was reached by
majority of the pregnancy. The which prenatal ultrasound markers consensus, and full-text copies of those
incidence of gastroschisis has risen were associated with postnatal articles were obtained. Two reviewers
worldwide in recent decades to reach outcome in gastroschisis. A meta- (FD, CV) independently extracted
2 to 5 per 10 000 live births.1 The analysis was conducted to pool any relevant data regarding study
postnatal outcome is favorable in cases relative risk estimates from the characteristics and pregnancy outcome.
of simple gastroschisis (continuous existing literature on the association Inconsistencies were discussed by the
and uncompromised intestine) with between various ultrasound signs and reviewers and consensus reached. If
a survival rate .95% and low the occurrence of atresia, intrauterine .1 study was published for the same
morbidity.1,2 In contrast, complex death (IUD), and neonatal death cohort with identical end points, the
gastroschisis (intestinal atresia, (NND); LOS, time to full enteral feeding report containing the most
necrosis, or perforation) is associated (TFEF), and length of TPN (LTPN) in comprehensive information on the
with worse survival rate (70%80%), an attempt to determine if there was population was included to avoid
longer hospital stay, and higher long- an association and, if so, its magnitude. overlapping populations. For those
term morbidity.2,3 The highly variable articles in which information was not
return to functional bowel (due to reported but the methodology was
METHODS
chronic intestinal inammation) and such that this information would have
the occurrence of bowel atresia (BA; Protocol, Eligibility Criteria, been recorded initially, the authors
requiring intestinal surgery in Information Sources and Search were contacted.
10%20% of cases) are the main This review was performed according Quality assessment of the included
factors affecting length of hospital stay to an a priori designed protocol and studies was performed using the
(LOS) as well as total parenteral recommended for systematic reviews Newcastle-Ottawa Scale (NOS) for
nutrition (TPN) dependence and and meta-analysis.1214 Medline, cohort studies (Supplement 3).16
associated neonatal complications (ie, Embase, the Cochrane Library
recurrent sepsis, TPN cholestasis, including the Cochrane Database of Summary Measures, Synthesis of the
adhesive bowel obstruction).2,46 Systematic Reviews, Database of Results, and Risk of Bias
Different surgical techniques (primary Abstracts of Reviews of Effects, and The ultrasound signs analyzed in this
vs staged closure) to repair this the Cochrane Central Register of review were as follows:
abdominal wall defect did not show Controlled Trials were searched
signicant differences in outcomes.2 Intraabdominal bowel dilatation
electronically in June 2014 using
(IABD)
In developed countries, prenatal combinations of the relevant medical
diagnosis allows a 90% detection rate subject heading terms, key words, Extraabdominal bowel dilatation
of gastroschisis within the second and word variants for gastroschisis (EABD)
trimester of pregnancy.7 A regular and outcome (Supplement 1). The Gastric dilatation (GD)
ultrasound monitoring of the fetus search and selection criteria were BWT
with gastroschisis aims to dene size restricted to English language.
Polyhydramnios
and quality of the herniated intestine Reference lists of relevant articles
(bowel dilatation or thickening), and reviews were hand searched for Small for gestational age (SGA)
amount of amniotic uid, and fetal additional reports. The PRISMA The outcomes analyzed in this
growth. Prenatal denition of simple (Preferred Reporting Items for systematic review were as follows:
and complex gastroschisis is important Systematic Reviews and Meta- BA
to establish accurate prenatal Analyses) guidelines15 were followed
counseling and to plan delivery site (Supplementary Fig 2, Supplement 2). IUD
and postnatal medical and surgical The study was registered with the NND
treatments. Recently, several PROSPERO database (registration LOS
ultrasound signs, such as bowel number: CRD42014007640). TFEF
dilatation, polyhydramnios, and bowel
wall thickness (BWT), have been Study Selection, Data Collection, and LTPN
reported to be associated with the Data Items IABD was dened as the dilatation of the
occurrence of unfavorable outcomes Studies were assessed according to the bowel inside the abdomen irrespective
and, in particular, with BA.5,811 following criteria: population, outcome, of the presence of EABD. EABD was

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e160 DANTONIO et al
dened as the occurrence of the led to a huge improvements in the We included observational cohort
dilatation of the extruded part of the diagnosis and denition of prenatal studies in which
bowel only. This choice was based on the structural anomalies. Furthermore,
assumption that EABD is almost a recent systematic review exploring (a) many comparisons reported
invariably present in fetuses with the association between EABD and 0 events in 1 group,
gastroschisis, most likely representing several adverse perinatal outcomes
(b) several comparisons reported
the consequence of bowel exposure to included studies published before
0 events in both groups, and
the amniotic uid, whereas IABD is only 2000.17
occasionally described in this condition. Case reports, conference abstracts, (c) exposed and unexposed group
GD was dened as the enlargement of and case series with ,3 cases, sizes were frequently severely
the stomach, and BWT was the irrespective of whether the anomalies unbalanced.
measurement of the wall of the bowel were isolated, were also excluded to Many of the most commonly used
inside or outside the defect. SGA was avoid publication bias. meta-analytical methods, including
dened as an estimated fetal weight
those using risk difference (which
#5th or 10th percentile according to the
Statistical Analysis could be used to handle total zero-
cutoff adopted. In view of the multitude
Overall, we evaluated separately the event studies), can produce biased
of cutoffs reported for all these
association between 6 potential estimates when events are rare.18,19
ultrasound measurements, a subanalysis
predictors (IABD, EABD, GD, When many studies are also
according to the threshold chosen to
polyhydramnios, SGA) and 6 adverse substantially imbalanced, the best
dene an ultrasound sign as abnormal
clinical outcomes (IUD, NND, BA, performing methods are the Mantel-
was carried out when possible. BA was
TFEF, LTPN, LOS). A sufcient Haenszel odds ratio (OR) without zero-
dened as a congenital obstruction of
number of studies with comparable cell continuity corrections, logistic
the bowel lumen. IUD was dened as
outcomes were available for only 3 regression, and an exact method.20,21
fetal loss in the second and third
outcomes (IUD, NND, and BA), and Mantel-Haenszel ORs cannot be
trimester of pregnancy, and NND as the
a total of 6 3 3 = 18 separate meta- computed in studies reporting 0 events
occurrence of a death in the neonatal in both groups, the exclusion of which
period, up to 28 days of life. LOS was analyses were thus carried out. For
the other outcomes (LOS, LTPN, and may, however, cause a relevant loss of
dened as the time from birth to information and the potential ination
discharge home. TFEF was dened as TFEF), heterogeneity in the data did
not allow to perform a meta- of the magnitude of the pooled
the time necessary to achieve full exposure effect.18 To keep all studies
enteral nutrition and LTPN as the time analysis.
into the analyses, we thus performed
of full dependency on parenteral The units of the meta-analysis were all meta-analyses using individual data
nutrition. single comparisons of subjects random-effect logistic regression, with
with abnormal versus normal single study as the cluster unit. The
Only studies reporting prenatal
ultrasound signs in predicting each pooled data sets with individual data
ultrasound data of fetuses with
of the selected clinical outcomes were reconstructed using published 2
gastroschisis were considered
during the scheduled follow-up. 3 2 tables. When 1 of the overall
suitable for the inclusion in the
Accordingly, when a study reported pooled arms showed no events, we
current systematic review; postnatal
separate relative risks for different used exact logistic regression including
studies or studies from which cases
patient characteristics (ie, levels individual studies as dummy variables.
diagnosed prenatally could not be
of dilation), all subgroups were The assessment of the potential
extracted were excluded. Autopsy-
grouped, and a single estimate of publication bias was performed with
based studies were excluded on the
risk was calculated for the study. Eggers regression asymmetry test.22
basis that fetuses undergoing
Unfortunately, the scarce number of
termination of pregnancy are more All analyses were performed using
studies did not permit meaningful
likely to show associated major Stata version 13.0 (Stata Corp, College
stratied meta-analyses to explore
structural and chromosomal Station, TX).
the test performance in subgroups
anomalies. Studies not reporting the
of patients who may be less or
site of the dilatation (intra or extra-
more susceptible to bias. For the
abdominal) were not considered RESULTS
purpose of this analysis, when
eligible for the inclusion.
multiple cutoffs were reported, that A total of 869 articles were identied,
Studies published before 2000 were showing the highest degree of 73 were assessed with respect to
not included in the current association, as reported by the their eligibility for inclusion
systematic review because advances authors, was selected to calculate (Supplementary Table 8). Twenty-six
in prenatal imaging techniques has the ORs. studies were included in the

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PEDIATRICS Volume 136, number 1, July 2015 e161
systematic review (Fig 1). These 26 assessment of antenatal imaging in machine setting, type of scan) and
studies included 2023 fetuses with relation to the outcome explored, when a given sign was assessed was
a prenatal diagnosis of gastroschisis. different thresholds adopted to missing (Table 3).
The general characteristics of the dened an ultrasound sign as The assessment of the potential
studies included in the systematic abnormal, and lack of a standardized publication bias was problematic
review are reported in Table 1. outcome measure. because of the scarce number of
Quality assessment of the included The denitions of the ultrasound studies and sparse events. The
studies was performed using signs used in each study are shown in formal tests for funnel plot
Newcastle-Ottawa Scale for cohort Table 3. Several cutoffs were used asymmetry cannot be used when the
studies. Almost all the included among the studies to dene a scan as total number of publications
studies showed an overall good rate abnormal; furthermore, most of the included for each outcome is ,10
with regard to the selection and included studies did not assess the because its power is too low to
comparability of the study groups and reproducibility, interobserver, and distinguish chance from real
to the ascertainment outcome of intraobserver variability of a given asymmetry.20 Furthermore, in 2 of
interest (Table 2).16 The major sign. Finally, for most of the the 3 comparisons including 10
weaknesses of these studies were ultrasound signs explored, an studies, the number of events was
represented by their retrospective objective explanation in terms on too scarce to allow formal testing
design, with the lack of a blind how (ie, imaging plane, ultrasound (n , 15 overall). We were thus able

FIGURE 1
Flow chart of studies included in the meta-analysis.

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e162 DANTONIO et al
TABLE 1 General Characteristics of the Included Studies
Author Year Country Study Design GA at Scan Fetuses (n) Prenatal Ultrasound Signs Explored Outcome(s) Explored
a
Overcash 2014 United States Retrospective 1 wk before delivery 191 SGA BA, NND
Goetzinger 2014 United States Retrospective 33.7 6 2.6 wk 94 IABD, EABD, BWT BA, NND, LOS, LTPN, TFEF
Janoo 2013 United States Retrospective 23 wk from delivery 25 SGA, polyhydramnios IUD, NND
Durfee 2013 United States Retrospective 7.6 d (069) before delivery 84 EABD, BWT, SGA IUD
Emila 2012 Canada Retrospective Third trimester 83 IABD, EABD, GD, SGA, polyhydramnios BA
Ghionzolia 2012 United Kingdom Retrospective From 30 wk 130 IABD, EABD, GD, polyhydramnios BA
Overton 2012 United Kingdom Retrospective Secondthird trimester 217 Polyhydramnios, SGA IUD, NND
Kulevaa 2011 France Retrospective Third trimester 105 IABD, EABD, GD, SGA, BWT BA, IUD, NND
Ajayi 2011 United States Retrospective Secondthird trimester 74 SGA, polyhydramnios IUD, NND

PEDIATRICS Volume 136, number 1, July 2015


Alfaraja 2011 Canada Retrospective Within 2 wk of delivery 98 IABD,a GD, polyhydramnios BA, IUD, NND, LOS TFEF, LTPN
Mearsa 2010 United Kingdom Retrospective Secondthird trimester 47 IABD, EABD BA,a NND, LTPN
Controa 2010 United Kingdom Retrospective From 32 wk 48 IABD, EABD, polyhydramnios BA, IUD, NND
Garciaa 2010 Brazil Retrospective 35.6 6 1.6 wk 94 EABD BA, IUD, NND, LOS, TFEF
Huh 2010 United States Retrospective Secondthird trimester 43 IABD BA, IUD, NND, LOS, TFEF
Hidaka 2009 Japan Retrospective Secondthird trimester 11 Polyhydramnios IUD, NND
Payne 2009 United States Retrospective Within 4 wk of delivery 155 Polyhydramnios LOS
Towers 2008 United States Retrospective Not stated 75 Polyhydramnios IUD
Heinig 2008 Germany Retrospective Not stated 14 EABD, BWT IUD, BA
Cohen-Overbeeka 2008 The Netherlands Retrospective Secondthird trimester 24 IABD,a EABD, SGA, polyhydramnios BA, IUD, NND
Santiago-Munoz 2007 United States Retrospective Secondthird trimester 58 SGA, GD IUD
Brantberga 2006 Norway Prospective From 3436 wk 60 IABD BA, IUD, NND
Nick 2006 United States Retrospective Secondthird trimester 58 IABD, SGA BA, IUD, LOS, NND
Puliglandaa 2004 Canada Retrospective Secondthird trimester 96 SGA BA
Aina-Mumuney 2004 United States Retrospective 2836 wk 34 GD BA, IUD, NND, LOS, TFEF
Strauss 2003 United States Retrospective Not stated 60 EABD, SGA BA, IUD, NND
Japaraj 2003 Australia Retrospective Within 23 wk of delivery 45 EABD, BWT, polyhydramnios, SGA IUD, NND, LOS
a Additional information provided by the authors.

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IABD

EABD
occurrence of BA.

with the LTPN (Table 7).


(Supplemental Figure 2).

dilated bowel (80.5 days,

Two studies24,34 explored the


a signicant prolonged LOS

of hospitalization (Table 5).


used different thresholds of
individual studies versus the

fetuses without IABD (Table 4).


BA): we displayed the ORs of

compared with those with less


95% condence interval [CI] =

regarding this outcome (Table 6).

the occurrence of bowel atresia.


Both did not report any signicant
.02). Likewise, Nick,41 using GA-

with 26.5 days in those without,


dilatation to dene the bowel as
abnormal; in the largest study,24

fetuses with dilatation compared


vs 47.5 days, IQR 31.078.0, P ,
Fetuses with ultrasound evidence of

Three studies24,34,41 explored the


IABD, irrespective of the presence of
1.290532 to 1.001958, P = .779)

the association between EABD and


whereas Huh34 could not nd any
association between IABD and the

Ten studies (659 fetuses) explored


found to be signicantly associated
Nine studies (673 fetuses) explored

fetuses with an IABD .14 mm had


NND was not signicantly higher than
logarithm of their SE22 (0.144287,

CI 3.19.8), whereas the risk of IUD or

overall postnatal LOS. These studies

increased risk in fetuses showing IABD


EABD, had a signicantly higher risk of

interquartile range [IQR], 34.5136.5

reported a median LOS of 84 days in


BA diagnosed at surgery (OR: 5.48, 95%

corrected cutoff for bowel dilatation,

Finally, the presence of IABD was not


association between IABD and length
analysis only (IABD as a predictor of
to assess publication bias in 1 meta-

e163
the association between IABD and the

association between IABD and the TFEF.


TABLE 2 Quality Assessment of the Included Studies According to Newcastle-Ottawa Scale Two studies33,45 analyzed the
Author Year Selection Comparability Outcome association between EABD and LOS.
Overcash23 2014
In the study by Garcia et al,34 the
Goetzinger24 2013 authors found that fetuses with
Janoo25 2013 ultrasound evidence of EABD .25 mm
Durfee26 2013 had a signicantly longer LOS
Emil27 2012 (42.4 6 19.7 days) compared with
Ghionzoli6 2012
Overton28 2012
those without (33.3 6 22.3 days, P =
Kuleva3 2011 .04), whereas Japarai, using
Ajayi29 2011 a different threshold of dilatation
Alfaraj30 2011 (17 mm), did not nd any association
Mears31 2010 between EABD and LOS (Table 5).
Contro32 2010
Garcia33 2010 Only 1 study34 explored the association
Huh34 2010 between EABD and TFEF and found that
Hidaka35 2009
fetuses with EABD .25 mm had
Payne10 2009
Towers36 2008 signicantly longer times to reach the
Heinig37 2008 full enteral feeding (25.7 6 12.8 vs 18.2
Cohen-Overbeek38 2008 6 9.9 days, P = .02) compared with
Santiago-Munoz39 2007 those without EABD (Table 6).
Brantberg40 2006
Nick41 2006 Finally, the only study31 exploring the
Puligandla42 2004 association between EABD and LTPN
Aina-Mumuney43 2004 could not nd any signicant association
Strauss44 2003
between this ultrasound sign and the
Japaraj45 2003
observed outcome (Table 7).
A study can be awarded a maximum of 1 star for each numbered item within the Selection and Outcome categories. A
maximum of 2 stars can be given for comparability. See Supplement 2.
GD
Fetuses showing evidence of EABD in those fetuses was not signicantly Five studies (449 fetuses) explored
were not at increased risk of having higher than that of the control the association between GD and
BA. Likewise, the risk of IUD and NND population (Table 4). outcome. Fetuses with GD diagnosed
TABLE 3 Description of Ultrasound Signs Used Among the Studies Included
Author Year IABD EABD GD BWT SGA (Percentile)
Overcash23 2014 ,10th
Goetzinger24 2014 .6, .10, .14,a .18 mm .6, .10, .14, .18 mm .3 mm
Janoo25 2013 Not stated
Durfee26 2013 .8 mm .1 mm
Emil27 2012 Not stated Not stated Not stated ,10th
Ghionzoli6 2012 .18 mm .18 mm Not stated
Overton28 2012 Not stated
Kuleva3 2011 .6 mm .6 mm .2 SD .3 mm ,10th
Ajayi29 2011 ,10th
Alfaraj30 2011 .2 SD
Mears31 2010 .10 mm .10 mm
Contro32 2010 .6 mm .6 mm
Garcia33 2010 .15, .20, .25, .30 mm
Huh34 2010 Not stated
Hidaka35 2009
Payne10 2009
Towers36 2008
Heinig37 2008 .15, .20, .25 mm .3 mm
Cohen-Overbeek38 2008 .10 mm ,10th
Santiago-Munoz39 2007 GA dependent
Brantberg40 2006 Not stated
Nick41 2006 GA dependent ,10th
Puligandla42 2004 ,5th
Aina-Mumuney43 2004 GA dependent
Strauss44 2003 2942 mm Not stated
Japaraj45 2003 .17 mm .3 mm ,10th
a Most predictive cutoff in this study.

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e164 DANTONIO et al
prenatally were not at signicantly outcome. BWT was not associated with

(0.914.7) 25,28,29, 30,32,35, 45

Number of events / Total n of subjects in the exposed group (ie, bowel thickness) versus Number of events / Total n of subjects in the unexposed group (ie, normal bowel). The total sample of the meta-analyses does not exactly match the total
8,24,31, 32,34,40, 41
8,31,32, 33,38,44, 45

8,23,28, 29,45
higher risk of BA or IUD compared atresia, IUD, or NND (Table 4).

8,30,43

8,24,45
with those without. However, GD was
Ref.

sample derived from the sum of individual studies as reported in Table 1 because for some outcomes/signs, the number of subjects included in each study slightly varied. All raw datasets are available on request from the authors.
Only 1 study24 explored the
signicantly associated with the association between BWT and LOS. In
occurrence of NND within the rst 28 this study, fetuses with a BWT
(1.324.1)b days of life (OR: 5.58, 95% CI .3 mm had signicantly longer stay
(0.43.9)
(0.21.2)

(0.06.3)
(0.43.5)
1.324.1).
Pooled OR
(95% CI)

in the hospital (100.5 median days,


C. NND

Two studies30,43 explored the IQR 82.0196.0) compared with those


1.31
0.47
5.58
3.98
0.83
1.12

association between GD and LOS. The without (48.5 median days, IQR,
study by Aina-Mumuney43 included 31.081.5) (Table 5). In the same
(452) 5/126 vs 10/326
(378) 6/164 vs 16/214

(576) 5/155 vs 10/421


(234)b 5/57 vs. 3/177b
3/34 vs 14/426
0/29 vs 11/215

study, the authors did not nd any


a

34 fetuses with a prenatal diagnosis of


Raw Data

gastroschisis of whom 13 showed association between BWT and TFEF


ultrasound evidence of GD. The authors (Table 6) or LTPN (Table 7).
found a signicantly longer LOS in
Sample)
Studies,
n (Total

(460)
(244)

fetuses with (75 6 57days) compared SGA


with those without (43 6 30) gastric
7
7
3
7
3
5

Ten studies (700 fetuses) included


(0.215.7) 25,28,29, 30,32,35, 36,38,39, 45

8,25,26, 28,29,38, 39,41,44, 45

dilatation, whereas Alfaray,30 in a larger analyzed the association between SGA


8,26,32, 33,37,38, 44,45

study including 98 fetuses, did not nd and postnatal outcome in


8,32,34, 38,40,41

8,30,39, 43

8,26,30, 37

any signicant difference among the gastroschisis. SGA fetuses were not at
TABLE 4 Results of the Meta-Analyses Evaluating the Association Between Selected Ultrasound Signs and Various Clinical Outcomes

Ref.

2 groups (Table 5). Furthermore, no increased risk of either bowel atresia


signicant association was found in or IUD or NND compared with
term of TFEF in fetuses with or without controls (Table 5). There were no
GD (Table 6). Finally, none of the studies exploring the association
studies included in this systematic between SGA diagnosed at the scan
(0.05.7)
(0.12.9)
(0.05.7)

(0.07.5)
(0.22.9)
B. IUD

Pooled OR
(95% CI)

review analyzed the relationship and LOS, TFEF, and LTPN.


between GD and LTPN.
0.42
0.56
0.74
1.77
0.86
0.75

Polyhydramnios DISCUSSION
(0.82.3) 5,8,24,27, 31,32,33, 37,38,44 8 (434) 3/220 vs 7/214

10 (700) 3/220 vs 9/480


10 (602) 1/45 vs 10/557
6 (331) 1/94 vs 4/237

4 (295) 0/62 vs 6/233

4 (237) 0/83 vs 4/154


a
Raw Data

Ten studies (602 fetuses) analyzed Main Findings


the association between
The ndings from this systematic
polyhydramnios and postnatal
review showed that IABD and
Sample)
Studies,
n (Total

outcomes. Fetuses with


polyhydramnios are associated with an
polyhydramnios were at signicantly
increased risk of BA (OR 5.48 and 3.76,
high risk of BA compared with those
(3.19.8)b 5,8,24,27, 31,32,34, 40,41

respectively). Fetuses with GD are at


with normal amniotic uid at the scan
8,23,27, 38,41,42

high risk of NND (OR 5.58). In view of


b Indicates the signs associated with an increased risk of a specic adverse outcome.
5,27,30, 32,38
5,8,27, 30,43

(OR: 3.76, 95% CI 1.78.3) (Table 5).


8,24,37

the small sample size of the studies


Ref.

However, polyhydramnios was not


included, heterogeneity in outcome
signicantly associated with either
denition, and the data displayed, it
IUD or NND (Table 5).
was not possible to draw any robust
Two studies10,30 explored the conclusion regarding the association
(1.78.3)b
(0.62.6)

(0.66.2)
(0.62.2)
Pooled OR

relationship between polyhydramnios between prenatal ultrasound markers


(95% CI)
A. BA

and LOS but failed to nd a signicant and LOS, TFEF, and LTPN.
5.48
1.34
1.23
3.76
1.94
1.15

association (Table 5). There was no


study analyzing the association Limitations
9 (673)b 44/203 vs 30/470b

Polyhydramnios 5 (380)b 11/36 vs. 36/344b


10 (659) 26/226 vs 40/433

6 (495) 14/118 vs 40/377


10/76 vs 41/373

5/34 vs 17/179

between polyhydramnios and TFEF.


a
Raw Data

Limitations and bias derive from the


Finally, the only study30 investigating features of the studies included in this
the association between review. The main weaknesses of these
polyhydramnios and time on TPN did studies were represented by their
not nd any signicant result
Sample)
Studies,
n (Total

5 (449)

3 (213)

retrospective design, small sample size,


(Table 7). different thresholds used to dene an
ultrasound sign as abnormal, and by
Ultrasound

BWT the fact that most of the outcomes


Sign

Three studies (244 fetuses) analyzed the were explored only by a limited
EABD
IABD

BWT
SGA
GD

relationship between BWT and adverse number of studies. The variability in


a

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PEDIATRICS Volume 136, number 1, July 2015 e165
TABLE 5 Results of the Systematic Review Evaluating the Association Between Selected between IABD .14 mm and LOS (80
Ultrasound Signs and LOS vs 47 days) compared with fetuses
Ultrasound Sign Denition Exposed Group Unexposed Group P without intestinal dilatation. This was
n LOS n LOS explained by the higher risk of BA
associated with IABD and therefore
IABD
Nick41 (2006)a GA dependent 10 84.0 48 26.5 .0027
increased LOS.
Huh34 (2010)a Not stated 16 40.9 6 27.8 27 34.4 6 20.3 .39 A second systematic review46
Goetzinger24 (2014)b $14 mm 28 80.5 (34.5136.5) 66 47.5 (31.078.0) .02c
compared the postnatal outcome in
EABD
Japarai45 (2003)a $17 mm 19 46.7 26 58 .64 newborns with simple and complex
Garcia33 (2010)a $25 mm 16 42.4 6 19.7 78 33.3 6 22.3 .04c gastroschisis (atresia, necrosis,
GD perforation, or volvulus). The authors
Aina-Mumuney43 (2003)b GA dependent 13 75 6 57 21 43 6 30 .05c showed a signicantly higher mortality
Alfaraj30 (2011)a .2 SD 32 46.1 6 29.5 65 59.0 6 46.3 .15
rate in complex compared with
Polyhydramnios
Payne10 (2009)b 10 41 (2877) 31 (2638) 131 .402 simple gastroschisis (16.7% vs 2.2%,
Alfaraj30 (2011) 14 62.28 6 49.97 80 53.64 6 40.74 .481 respectively). Moreover, infants with
BWT complex gastroschisis showed worse
Goetzinger24 (2014)b .3 mm 6 100.5 (82.0196.0) 88 48.5 (31.081.5) .03c outcome in terms of later ability to feed
a Values expressed as median, median and range, or IQR or 95% CI. orally, longer time to reach full feeds,
b Values reported as mean or mean (6 SD).
c P , .05 is signicant.
longer time on parenteral nutrition,
and longer length of hospital stay.46
Because of high data heterogeneity, we
the thresholds used to dene an in 273 fetuses with isolated were not able to perform a meta-
ultrasound sign as abnormal did not gastroschisis. The authors analyzed 27 analysis for the following outcomes:
allow any meaningful subanalysis years (19802007) of published LOS, LTPN, and TFEF). Looking at
according to the cutoff used. literature on the topic without nding selected papers (Table 5 and 6) and
Gestational age at examination is any signicant correlation between assuming that IABD was a prenatal sign
another particular issue with most of bowel dilatation and risk of adverse of complex gastroschisis, we showed
the included studies not reporting the perinatal outcome. They also that in the 3 largest series, there was
time at scan. In this scenario, it is underlined the inconsistent denition a signicant association between
plausible that the relationship between of bowel dilatation used by different IABD/EABD and longer LOS.24,33,41
a given ultrasound sign and an authors and the lack of randomized
In a recent systematic review, our
outcome may change according to the control trials. In our systematic review,
group explored the role of prenatal
gestational age at scan. we analyzed a larger population with
ultrasound in detecting non-duodenal
EABD (659 cases) and found a longer
Comparison With Other Systematic small bowel atresia in otherwise
LOS (42.4 vs 33.3 days) compared
Reviews normal fetuses.47 We found that
with those without dilatation only
A previous systematic review17 considering an EABD cutoff .25 mm. ultrasound had a poor accuracy in
explored the prognostic value of EABD More signicant was the association detecting small bowel atresia either
using bowel dilatation or
polyhydramnios. In gastroschisis, we
TABLE 6 Results of the Systematic Review Evaluating the Association Between Selected could not dene the accuracy of
Ultrasound Signs and TFEF prenatal ultrasound in detecting BA
Ultrasound Sign Denition Exposed Group Unexposed Group P but we could calculate a four times
n TFEF n TFEF
increased risk when IABD was present.

IABD
Huh34 (2010)a Not stated 16 29.6 6 17.7 27 29.8 6 18.3 .95 Implication for Clinical Practice
Goetzinger24 (2014)b $14 mm 28 36.0 (25.052.0) 66 38.5 (21.565.5) .92
BA in fetuses with gastroschisis is
EABD
Garcia33 (2010)a $25 mm 16 25.7 6 12.8 78 18.2 6 9.9 .02 c likely to be the result of an ischemic
GD necrosis from a constriction/
Aina-Mumuney43 (2003)b GA dependent 13 71 6 58 21 38 6 29 .46 obstruction at the level of the
Alfaraj30 (2011)a .2 SD 32 33.1 6 22.7 65 43.3 6 35.1 .138 umbilical ring or a volvulus of the
BWT
herniated bowel producing a vascular
Goetzinger24 (2014)b .3 mm 6 16.5 (11.022.0) 88 17.0 (12.021.0) .9
a
compromise. Our results showed that
Values reported as mean or mean (6 SD).
b Values expressed as median, median and range or IQR, or 95% CI. both IABD and polyhydramnios were
c P , .05 is signicant. associated with the presence of BA.

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e166 DANTONIO et al
TABLE 7 Results of the Systematic Review Evaluating the Association Between Selected dene an ultrasound marker as
Ultrasound Signs and LTPN abnormal, gestational age at
Ultrasound Sign Denition Exposed Group Unexposed Group P assessment, and outcome denition,
n LTPN n LTPN large prospective studies are needed
to clarify the role of antenatal
IABD
Mears31 (2010)a $10 mm 5 24 9 23 .91
ultrasound in stratifying the perinatal
Goetzinger24 (2014)b $14 mm 28 33.0 (22.072.0) 66 36.0 (20.055.0) .52 risk in fetuses with gastroschisis.
EABD Ideally, these studies should take into
Mears31 (2010)a $10 mm 21 39 9 23 .09 account objectively dened
Polyhydramnios ultrasound signs and assess their
Alfaraj30 (2011)a 14 58.43 6 36.34 81 49.26 6 30.92 .320
BWT
reproducibility and association with
Goetzinger24 (2014)b .3 mm 6 45.5 (19.072.0) 88 35.5 (21.055.5) .91 a given outcome at a given gestational
P , .05 is signicant. age at examination. The association
a Values reported as mean or mean (6 SD). between an ultrasound sign and
b Values expressed as median, median and range or IQR, or 95% CI.
a given outcome may be due to other
cofactors. In this scenario, regression
This can be explained by an intestine.5153 The main surgical models should be used to nd those
obstruction and blockage at the level concerns in this situation are about signs independently associated with
of the small bowel with accumulation the degree of bowel inammation, a given outcome.
of amniotic uid (polyhydramnios) edema, necrosis, and the increased Furthermore, predicative models
and proximal bowel dilatation (IABD). abdominal pressure after the using different ultrasound signs, alone
However, EABD was not found to be abdominal wall closure that can all or in combination, should be
associated with BA, IUD, or NND. increase the risk of surgical constructed by including only those
EABD is a common nding during the complications. For this reason, being signs showing independent and
prenatal ultrasound of fetuses with able to predict the presence of BA in signicant association with a given
gastroschisis; it is usually the result of newborns with gastroschisis could outcome and the diagnostic
the prolonged exposure of the signicantly help the surgeon to plan performance of the different signs
extruded bowel to the amniotic uid the repair, either with an anastomosis should be explored by taking into
and may not necessarily imply the or with a diverting ileostomy at the account all the possible thresholds.
presence of bowel complications. time of the abdominal wall closure. The number of ultrasound signs
Although advances in the neonatal Parental counseling54 should take into needed to label a scan as suggestive
care have led to a dramatic reduction account the presence of IABD and for a given outcome represents
in mortality, infants with gastroschisis polyhydramnios and their association another particular problem; it might
are still at high risk of neonatal and with BA. These signs are suspicious of be hypothesized that reduction in the
long-term morbidity. It has been BA, and the possibility of postnatal number of sonographic criteria may
observed that most short- and long- and postsurgical complications should increase the sensitivity but is likely to
be disclosed with parents during the reduce the specicity of the test.
term complications occur in cases in
prenatal period. Conversely, an increase in the number
which an intestinal atresia is
of criteria needed to label a case as
present.4850 Furthermore, newborns GD was associated with the
positive would reduce sensitivity but
with gastroschisis and associated BA occurrence of NND in the current
would improve specicity. Finally, each
were found to be more TPN meta-analysis. GD may indicate the
ultrasound sign should be evaluated in
dependent, at higher risk of chronic presence of a proximal intestinal
relation to the optimal cutoff needed
liver damage (eg, cholestasis), and obstruction (midgut volvulus or
to more accurately predict a given
have severe infectious atresia), which has been reported to
outcome. In this scenario, large
complications.5,51 be associated with a higher risk of
prospective studies are needed to
Published series showed that only mortality. However, it was not
standardize the different ultrasound
60% of the time was possible to possible to rule out other
measurements and to provide
confounders, such as prematurity, the
conrm an atresia at birth or during gestational age dependent cutoffs for
size of the defect, or postnatal
the rst surgical procedure (primary each ultrasound sign.
medical complications.
closure or silo placement).49,51,52
Even if a BA is identied at birth, the Conclusions
surgeon is often facing the dilemma Implications for Research Antenatal ultrasound can be used at
whether performing an early or In view of the wide heterogeneity in some extent to identify a subgroup of
a delayed repair of the interrupted study design, thresholds adopted to neonates with a prenatal diagnosis of

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PEDIATRICS Volume 136, number 1, July 2015 e167
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PEDIATRICS Volume 136, number 1, July 2015 e169
Prenatal Risk Factors and Outcomes in Gastroschisis: A Meta-Analysis
Francesco D'Antonio, Calogero Virgone, Giuseppe Rizzo, Asma Khalil, David Baud,
Titia E. Cohen-Overbeek, Marina Kuleva, Laurent J. Salomon, Maria Elena Flacco,
Lamberto Manzoli and Stefano Giuliani
Pediatrics 2015;136;e159; originally published online June 29, 2015;
DOI: 10.1542/peds.2015-0017
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Prenatal Risk Factors and Outcomes in Gastroschisis: A Meta-Analysis
Francesco D'Antonio, Calogero Virgone, Giuseppe Rizzo, Asma Khalil, David Baud,
Titia E. Cohen-Overbeek, Marina Kuleva, Laurent J. Salomon, Maria Elena Flacco,
Lamberto Manzoli and Stefano Giuliani
Pediatrics 2015;136;e159; originally published online June 29, 2015;
DOI: 10.1542/peds.2015-0017

The online version of this article, along with updated information and services, is
located on the World Wide Web at:
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PEDIATRICS is the official journal of the American Academy of Pediatrics. A monthly


publication, it has been published continuously since 1948. PEDIATRICS is owned,
published, and trademarked by the American Academy of Pediatrics, 141 Northwest Point
Boulevard, Elk Grove Village, Illinois, 60007. Copyright 2015 by the American Academy
of Pediatrics. All rights reserved. Print ISSN: 0031-4005. Online ISSN: 1098-4275.

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