Development of a prenatal clinical care pathway for uncomplicated gastroschisis and literature review

Abstract

BACKGROUND:

Gastroschisis is an abdominal wall defect wherein the bowel is herniated into the amniotic fluid. Controversy exists regarding optimal prenatal surveillance strategies that predict fetal well-being and help guide timing of delivery. Our objective was to develop a clinical care pathway for prenatal management of uncomplicated gastroschisis at our institution.

METHODS:

We performed a review of literature from January 1996 to May 2017 to evaluate prenatal ultrasound (US) markers and surveillance strategies that help determine timing of delivery and optimize outcomes in fetal gastroschisis.

RESULTS:

A total 63 relevant articles were identified. We found that among the US markers, intraabdominal bowel dilatation, polyhydramnios, and gastric dilatation are potentially associated with postnatal complications. Prenatal surveillance strategy with monthly US starting at 28weeks of gestational age (wGA) and twice weekly non-stress testing beginning at 32wGA is recommended to optimize fetal wellbeing. Timing of delivery should be based on obstetric indications and elective preterm delivery prior to 37wGA is not indicated.

CONCLUSIONS:

Close prenatal surveillance of fetal gastroschisis is necessary due to the high risk for adverse outcomes including intrauterine fetal demise in the third trimester. Decisions regarding the timing of delivery should take into consideration the additional prematurity-associated morbidity.

Keywords

Gastroschisis simple complex evidence-informed guidelines prenatal management clinical standard work clinical care pathway ultrasound markers

Abbreviations

Ultrasound

IABD

intraabdominal bowel dilatation

EABD

extra-abdominal bowel dilatation

gastric dilatation

BWT

bowel wall thickness

IUGR

intrauterine growth retardation

IUFD

intrauterine fetal demise

NND

neonatal death

bowel atresia

TFEF

time to full enteral feeds

TPN

total parenteral nutrition

LOS

length of stay

1 Introduction

Gastroschisis is a birth defect with a current reported incidence of 3.73 per 10,000 live births in United States [1], although this has increased 2- to 4-fold over the last 30 years [2, 3]. It can either be simple (uncomplicated) or complex if associated with bowel atresia (BA), volvulus or perforation. Gastroschisis both uncomplicated or complicated are associated with greater length of stay and health care costs while later having worse survival rates [4], the average LOS being 41 days and hospital charges ranging from 172k to 216k dollars [5, 6].

Fetal gastroschisis is easily diagnosed in the second trimester by ultrasound (US) which plays a key role in management of prenatal gastroschisis. Elective preterm delivery and increased prenatal surveillance have been proposed as strategies to reduce intrauterine fetal demise (IUFD) [7]. Postnatal gut dysfunction due to ongoing bowel injury secondary to prolonged exposure of the bowel to amniotic fluid has been suggested as another reason to consider elective preterm delivery [8]. The challenge in management of uncomplicated gastroschisis is balancing prematurity-associated risks with potential benefits of continued fetal maturation with a term delivery. However, there is a lack of consensus for surveillance strategies of fetal gastroschisis and of studies comparing neonatal outcomes following planned delivery rather than actual deliveries based on fetal/obstetrical indications. Consequently, in spite of early diagnosis with ample time for delivery planning, there is little guidance regarding optimal prenatal surveillance strategies to determine the optimal time of delivery.

This review is the result of a clinical standard work initiative in our institution to develop a standardized clinical care pathway (prenatal, neonatal, surgical and post-surgical) for uncomplicated gastroschisis. The objective of the our prenatal subgroup was to explore the literature to identify US markers and surveillance strategies that help predict fetal health with a goal to develop an evidence-informed clinical care pathway for best-practices in prenatal management of uncomplicated fetal gastroschisis. The US markers used to determine fetal well-being and the timing of delivery were intraabdominal bowel dilatation (IABD), extra-abdominal bowel dilatation (EABD), gastric dilatation (GD), bowel wall thickness (BWT), polyhydramnios, and intrauterine growth restriction (IUGR). The associated outcomes analyzed were IUFD, neonatal death (NND), bowel atresia (BA), time to full enteral feeds (TFEF), total parenteral nutrition (TPN) days, and LOS. Our overall objective was to evaluate the optimal timing of delivery that would help reduce neonatal morbidity and mortality and improve postnatal outcomes.

2 Methods

A multidisciplinary working group comprising of physicians and nursing providers from maternal fetal medicine (MFM), neonatology, pediatric surgery, pediatric outcomes research, and members from library science were directed to design a clinical care pathway for the continuum of care for uncomplicated gastroschisis in the state of Washington. The group defined the relevant questions about the prenatal, neonatal, surgical, and post-surgical care of uncomplicated gastroschisis. We received guidance in the search methods, development of questions, assessment of literature quality, and pathway development from our team members in the disciplines of outcomes research, evidence-based medicine specialty, and health science library. Each subgroup then directed its search and developed its review strategies and guidelines. The entire group met on a scheduled basis to report on the progress of the work, to elicit feedback, and to confirm continued alignment of the clinical care pathway. The prenatal subgroup consisted of one neonatologist (SC) and two maternal fetal medicine subspecialists (SP, EC). We identified three areas that could affect prenatal management: (1) Prenatal US indicators that predict fetal health in gastroschisis; (2) Ideal fetal surveillance strategy for gastroschisis; and (3) Optimal timing of delivery for gastroschisis.

Study selection for the development of the prenatal clinical pathway: Literature search was conducted in MEDLINE and EMBASE to capture items published from January 1996 to May 2017. Controlled subject headings and keywords for the following concepts were used: gastroschisis, fetal monitoring, antenatal surveillance, delivery timing, prenatal US markers. Articles were selected based on relevancy to the specified three questions of interest and items published in English. Relevant articles were then assessed based on quality of the study, relevance to clinical care, fetal and neonatal outcomes, and impact on clinical decision making. Studies about the management of omphalocele were excluded. No statistical or quantitative analysis was performed due to the heterogeneity of data and complexity involving the timing of delivery with prenatal US markers and surveillance. The articles were initially screened by abstract by two (EC, SC) of the three authors in the prenatal subgroup for quality of studies. Both reviewers, independently graded the abstracts to be either included for full text review or excluded and submitted the grades to the research coordinator. Articles that both EC and SC rejected were excluded; articles with discordant grades were reviewed by SP for inclusion or exclusion. All accepted articles were reviewed by the prenatal group, with each article always having full independent grading by two of the three members of the prenatal group. We developed a standardized evaluation tool with a grading system to assess the quality of the study design, data, and conclusions, and whether the article addressed the clinical question or contained bias. Each article was summarized, critiqued, and discussed by the two reviewers in the presence of the entire working group in order to reduce bias and reach consensus. For development of the clinical care pathway continuum, findings related to fetal surveillance strategies and timing of delivery approaches were prioritized for discussion. Studies evaluating US markers to predict postnatal outcomes (i.e. bowel dilation, BWT, GD, IUGR, amniotic fluid index (AFI) were included in our overall analysis. An evidence-based medicine specialist from the clinical effectiveness team of a tertiary care academic hospital facilitated these discussions.

3 Results

The literature search identified 212 citations through the initial database search. The initial title and abstract screening excluded 140, leaving the remaining 72 articles that met inclusion criteria to undergo a full text review. Of these articles, 33 were further excluded upon full text review, leaving 39 articles for the qualitative synthesis. Due to the time lag between the completion of the pathway and the completion of this manuscript, the prenatal subgroup updated the initial search with another 83 articles (last search performed 5/16/2017) and added another 24 articles resulting in a total 63 relevant articles for discussion. The following sections summarize the results of our literature investigation of the three prenatal questions in the management of fetal gastroschisis. Using this information, we developed an evidence-informed clinical care pathway and a US checklist for the prenatal management of uncomplicated gastroschisis at our institution. The pathway has been implemented through the introduction of a decision-making algorithm (accessible for use on our institutional intranet homepage), linked through an electronic order set. Information on the pathway was disseminated to the provider groups via lectures and provider grand rounds locally and regionally along with reminders to utilize the pathway via electronic mail.

4 Discussion

4.1 Prenatal ultrasound markers for fetal health in gastroschisis

The most common US findings used to evaluate fetal gastroschisis were IABD, EABD, GD, BWT, polyhydramnios, and IUGR. Interestingly, although serial surveillance of the bowel may be useful in predicting complications thereby helping guide the timing of delivery, studies have been inconsistent in describing the measurement of bowel diameter (i.e. inner wall to inner wall vs. outer wall to outer wall) or whether they are referring to small or large bowel. Also, the threshold at which prenatal bowel dilation is considered pathologic is yet to be defined. The following is a summary of US findings and their association with perinatal and neonatal outcomes such as IUFD, NND, BA, TFEF, TPN days, and LOS in gastroschisis.

4.1.1 Intra-abdominal bowel dilatation

The intra-abdominal bowel diameter is defined as the segment of maximal dilation measured from the inner wall to inner wall and prenatal IABD is considered to be an indirect sign of BA, as shown by a recent meta-analysis along with several other studies [9 –21]. The exact bowel measurements used to define IABD are variable in studies: IABD of >6 mm was associated with a fourfold risk for bowel obstruction [19] and IABD of > 14 mm was associated with BA and increased LOS [13]. IABD has, however, not been shown to be associated with an increased risk of NND, TPN days or TFEF [9 , 20]. The presence of multiple loops of dilated bowel are associated with increased postnatal complications, however, absence of bowel dilation (either intra-abdominal or extra-abdominal) was associated with an uncomplicated postnatal course [22]. The significance of the gestational age at which IABD is first seen or the timing of bowel dilatation is unclear; one study found second trimester IABD to be strong predictor of postnatal BA although the measurement used to define bowel dilation was not provided [10]. In another study, third trimester IABD at 12 mm was considered a strong predictor for complex gastroschisis [23].

4.1.2 Extra-abdominal bowel dilatation

Although the clinical significance of EABD is unclear, it does not appear to be associated with an increased risk of bowel atresia, or NND [9 , 23– 30]. One study reported that EABD > 25 mm in the third trimester of pregnancy was associated with an increased risk of fetal distress or IUFD [22], however, another study that found the same association defined dilated extra-abdominal small bowel as any loop measured from the inner margin of the bowel wall > 10 mm in diameter [24]. With regards to postnatal outcomes, some studies have found EABD to be associated with increased LOS and prolonged TFEF while other studies have not [9 , 28].

4.1.3 Bowel wall thickness

There are very few studies reporting the significance of BWT. One study demonstrated BWT > 3 mm to be associated with increased LOS; however it was not associated with prolonged TFEF or prolonged TPN days [13]. Another study found that BWT of more than 2.5 mm was strongly associated with adverse condition of the bowel wall (massive peel, edema, livid color of bowel) and the need for reoperation because of bowel complications [24]. Other studies have found no association between BWT and bowel atresia, IUFD or NND [8 , 30].

4.1.4 Polyhydramnios

Polyhydramnios in fetal gastroschisis was associated with a significantly high risk of bowel atresia with one study demonstrating a high likelihood for severe neonatal bowel compromise (perforation, necrotic segments) [9, 28]. Another study reported polyhydramnios to be predictive of fetal bowel dilation and was strongly associated with bowel atresia [15]. More importantly, normal amniotic fluid volume and absence of internal or external bowel dilation was a strong predictor for absence of bowel atresia [15]. Polyhydramnios was, however, not associated with longer LOS, prolonged TPN days, IUFD or NND [9 , 31– 33].

4.1.5 Gastric dilatation

GD (defined as greater than 2 standard deviations above the normal in anteroposterior or transverse diameter per gestational age based nomogram) was not associated with longer LOS, delayed TFEF or IUFD, however, this was associated with NND within the first 28 days of life [9 , 34– 36]. One study found an association between recent herniation of the fetal stomach (within one week prior to delivery) and IUFD or non-reassuring feta heart tones [37]. Another single center study has reported an association between GD or subjective malposition of the stomach and perinatal death [38].

4.1.6 Fetal growth restriction

Ultrasound diagnosis of poor fetal growth is not uncommon in gastroschisis. IUGR, defined as expected fetal weight < 10^th percentile (with severe IUGR as fetal weight < 3^rd percentile) and small for gestational age (SGA), defined as birth weight (BW)<10^th percentile are known to be associated with IUFD in pregnancies with or without fetal gastroschisis. This diagnosis of a growth restriction in fetal gastroschisis is, however, confounded by the use of the abdominal wall circumference in determining fetal growth, which is generally always small in gastroschisis due to herniated bowel loops. Consequently, it may not be appropriate to interpret fetal growth in gastroschisis using abdominal circumference growth curves established from non-anomalous fetuses. This is supported by a fetal gastroschsis study estimating fetal weight using Hadlock [39] formulas which demonstrated that BW was underestimated by an average of 5.6% and IUGR was actually present in only 52% of babies, although it was predicted in 72% of pregnancies [40]. Another study reported that the formulas of Shepard and Siemer best predicted neonatal weight [41]. However, regardless of the fetal growth formula used, there is a higher incidence of poor fetal growth reported in gastroschisis. A retrospective study of prenatal surveillance of gastroschisis identified growth restriction in 38% of the fetuses with half being born with a BW < 3^rd percentile [42]. Another study reported that the pattern of symmetric intrauterine growth restriction was consistent with early development of growth delay with 44% having a BW < 5^th percentile and 61% having a BW < 10^th percentile for gestational age [43].

4.1.7 Summary

In summary, gastroschisis has been reported to have poor fetal growth as defined by ultrasound. Due to the variable definitions of ultrasound markers, lack of normative data, and small numbers in each series, it is difficult to determine the discriminatory values that predict impending fetal compromise or significant neonatal morbidity. There was however, a trend towards multiple abnormalities increasing the risk for fetal compromise and/or neonatal complications. Further studies are needed for a more standardized and multisystem approach to assessing the bowel and fetal health in gastroschisis.

4.2 Fetal surveillance

Non-reassuring fetal status and sudden fetal death are more frequent in fetuses with gastroschisis. The incidence of IUFD in fetal gastroschisis is reported to range from 5.2% to 12.5% [44 –46]; however, a recent meta-analysis of IUFD risk reported a much lower pooled prevalence of 4.48 per 100 births [47]. Another study from the National Center for Health Statistics database reported the risk of IUFD in fetal gastroschisis to be seven times that of non-anomalous fetus when controlling for GA (4.5% compared to 0.6% in non-anomalous fetuses for gastroschisis) [48]. These studies, however, do not stratify for the severity of gastroschisis or the reasons for stillbirth. While most studies suggest that IUFD in fetal gastroschisis occur in the third trimester [47], the lack of understanding of the developmental evolution of fetal gastroschisis and the underlying mechanisms for fetal death, makes it difficult to define the optimal prenatal surveillance strategy that would help reduce its risk while limiting the prematurity-associated morbidity and mortality.

Traditional prenatal surveillance includes non-stress testing (NST) which currently remains critical to the antenatal surveillance paradigms for the fetus. There are only a few studies that address the role of NST or a surveillance program in decreasing IUFD. One case series of sixty gastroschisis fetuses who underwent weekly ultrasound surveillance and daily NST (or every other day) from 34– 36 weeks until delivery reported one IUFD at 35 weeks and 4 days in the setting of maternal moderate pre-eclampsia [11]. In another study of forty gastroschisis fetuses which used routine ultrasound and fetal arterial Doppler for surveillance instead of NST, there were two IUFDs (18 and 22 weeks) and the remaining fetuses were liveborn at a mean gestational age of 37 wGA [49]. Interestingly, a recent study reported that IUGR and oligohydramnios were not associated with adverse neonatal outcomes and do not portend worse prognosis in gastroschisis pregnancies [50]. Another retrospective study of fetal gastroschisis evaluating perinatal and neonatal outcomes of SGA neonates concluded that SGA was associated with a fourfold increase in odds for prolonged LOS, independent of GA [51]. There are no studies that address the continuum of ultrasound characteristics or their role in predicting fetal/neonatal mortality or morbidity.

4.3 Timing of delivery

Elective preterm delivery in fetal gastroschisis has been suggested as a solution to decrease the incidence of IUFD. Other support for early delivery is the hypothesis that gut injury is related to the duration of bowel exposure to amniotic fluid leading to decreased postnatal gut function, morbidity, increased LOS, and other complications [45 –47]. There are lack of studies that address antenatal monitoring surveillance strategies that balance IUFD reduction while limiting prematurity-related neonatal morbidity. A retrospective cohort study using United States birth and death linked certificate data, prospectively determined the risks of IUFD and NND in fetal gastroschisis for each gestational age week from 24 0/7 to 39 6/7 wGA and found that the risk of IUFD and postnatal mortality can be minimized with delivery at 37 wGA [44]. Several small retrospective studies also reported that preterm delivery was associated with longer LOS and TFEF [52 , 54– 60], increased risk of sepsis [53 , 57], increased ventilator days [61], and NND [62]. Other single center, large retrospective studies also reported that preterm birth (34– 36 wGA) of fetuses with gastroschisis was associated with increased TFEF, LOS, and sepsis compared to infants born at≥37 wGA suggesting that elective PT delivery (prior to 37 wGA) is not beneficial [55, 56]. Interestingly, few retrospective cohort studies of fetal gastroschisis have reported a benefit to early elective delivery (at 35 wGA) with reduced time to initiation of oral feeds [63 –67], LOS [65, 67], and decreased time on ventilator [66]. However, in a RCT, where participants were either randomized to elective delivery at 36 weeks or to await the onset of spontaneous delivery, no differences in TFEF and LOS were observed suggesting no significant benefit from elective preterm delivery [68]. Another study evaluating the risks of prematurity-related morbidity versus the risk of IUFD in ongoing pregnancy, reported that delivery at 39 wGA was associated with increased risk of IUFD, however, delivery at 37– 38 wGA was associated with decreased risk of IUFD (and only minimal increase in risk of RDS), thereby concluding that 38 wGA was the most cost-effective time to deliver fetal gastroschisis [69]. A large retrospective cost analysis study, comparing preterm (<34wGA) to early term (37– 38 wGA) deliveries in fetal gastroschisis reported improved perinatal outcomes with lower hospital costs among those delivered at 37– 38 wGA and increased LOS (56 versus 37 days), hospital costs ($79,129 versus $51,574) and NND (3.8 versus 1.5%) in the preterm group [70].

The recommendation for elective delivery at 37 wGA in fetal gastroschisis is also supported by a large study which reported that induction of labor at 37 wGA was associated with reduced sepsis, bowel damage, and NND compared with pregnancies managed expectantly beyond 37 weeks GA [71]. The Canadian Pediatric Surgery Network cohort found no difference in neonatal outcomes between planned induction with vaginal delivery at 36– 37wGA or planned vaginal delivery after spontaneous onset of labor at≥38 weeks’ gestation and reported that vaginal deliveries after spontaneous labor at > 38wGA was acceptable [72]. A recent retrospective cohort study evaluating the prospective risk of IUFD and risk of NND with each additional week of expectant management reported an increasing IUFD risk beginning at 35 wGA and rising to 13.9 per 1000 pregnancies at 39 wGA [44]. Also, the relative risk of NND was significantly greater with expectant management between 37– 39 weeks, and the study concluded that the risk of prenatal and postnatal mortality for fetal gastroschisis can be minimized with delivery at 37 wGA [44].

5 Conclusions

Gastroschisis pregnancies are considered high-risk and require close antenatal surveillance due to the potential for adverse pregnancy outcomes including IUFD in the third trimester. Lacking clear directions for fetal gastroschisis, we developed our prenatal surveillance pathway based first on empiric constructs for fetal surveillance of simple pregnancies. We then prospectively included the longitudinal surveillance of ultrasound markers for fetal gastroschisis to test their role in informing prenatal management. We acknowledge the limitation of our clinical pathway as it is based on a retrospective review, however, the literature search was rigorous and comprehensive. Since we are a referral site, our team also had to construct a surveillance pathway that was realistic for patient compliance and could be adapted by regional clinics in our state. Several US markers have been used to predict bowel health and fetal well-being, but no single antenatal sonographic marker or groups of markers have been shown to determine timing of delivery to decrease the risk of IUFD and/or postnatal morbidity. The current literature suggests that the complications of prematurity do not support routine preterm delivery in fetal gastroschisis to prevent IUFD.

5.1 Recommendations

We recommend close fetal monitoring of a pregnancy with gastroschisis. At the time of diagnosis, counseling about the embryologic etiology, prenatal surveillance, delivery, and postnatal management should be completed by a multidisciplinary team including MFM, Neonatology, Pediatric Surgery, Social Work, and nursing specialists. Based on our retrospective and comprehensive review of the literature, we propose the following prenatal clinical care pathway for simple/uncomplicated fetal gastroschisis:

Monthly fetal growth evaluations beginning at 24 wGA

Twice weekly NSTs with weekly ultrasound evaluations for bowel characteristics and amniotic fluid volume beginning at 32 wGA until delivery

Consideration for evaluation of US markers followed longitudinally in all fetuses:

Size of the abdominal wall defect

Fetal stomach measured as the antero-posterior diameter on axial view

Categorical confirmation of “No IABD or EABD” if none was seen on ultrasound

Intra-abdominal and extra-abdominal bowel lumen measurements obtained from inner wall to inner wall when progressive bowel dilation is suspected

Bowel wall thickness measurement

Identification of small bowel versus large bowel when following IABD/EABD

For uncomplicated gastroschisis, delivery to be scheduled for 37 ^0/7 to 38 ^0/7 wGA.

5.2 Summary points

Gastroschisis pregnancies are at high risk for poor fetal growth and intrauterine fetal demise (IUFD) in the third trimester. There are no antenatal sonographic markers with high predictive values to guide antenatal management, determine timing of delivery, or predict postnatal morbidity. The benefits of elective preterm delivery remain controversial

5.3 Additional points

Intra-abdominal bowel dilatation (IABD), polyhydramnios and gastric dilatation (GD), are the sonographic markers associated with potential postnatal complications. An antenatal surveillance strategy of close fetal monitoring involving ultrasound and antepartum fetal heart rate monitoring may help support continuation of pregnancy to early term. Plan for term delivery at 37 ^0/7– 38 ^0/7 weeks GA, unless indicated earlier by maternal or fetal status

Disclosure statement

Authors declare no conflict of interest

Funding statement

No funding sources

Footnotes

Acknowledgments

We thank Sue Groshong, MLS, Medical Librarian at Seattle Children’s Hospital, for her outstanding support in the literature search process. We also thank all of the members of the Clinical Standard Work Team of Seattle Children’s Hospital and the Gastroschisis Guideline Committee.

References

Canfield

, Honein

, Yuskiv

, Xing

, Mai

, Collins

, et al. National estimates and race/ethnic-specific variation of selected birth defects in the United States, 1999–2001. Birth Defects Res A Clin Mol Teratol. 2006;76(11):747–56.

, Nobuhara

, Laurent

, Shaw

. Increasing prevalence of gastroschisis: Population-based study in California. J Pediatr. 2008;152(6):807–11.

Chabra

, Gleason

, Seidel

, Williams

. Rising prevalence of gastroschisis in Washington State. J Toxicol Environ Health A. 2011;74(5):336–45.

Molik

, Gingalewski

, West

, Rescorla

, Scherer

, Engum

, et al. Gastroschisis: A plea for risk categorization. J Pediatr Surg. 2001;36(1):51–5.

Centers for Disease Control and Prevention. Hospital stays, hospital charges, and in-hospital deaths among infants with selected birth defect – United States, 2003. MMWR. 2007;56:25–48.

Banyard

, Ramones

, Phillips

, Leys

, Rauth

, Yang

. Method to our madness: An 18-year retrospective analysis on gastroschisis closure. 2010;45:579.

Landisch

, Yin

, Christensen

, Szabo

, Wagner

. Outcomes of gastroschisis early delivery: A systematic review and meta-analysis. J Pediatr Surg. 2017;52(12):1962–71.

Morrison

, Klein

, Chitty

, Kocjan

, Walshe

, Goulding

, et al. Intra-amniotic inflammation in human gastroschisis: Possible etiology of postnatal bowel dysfunction. Br J Obstet Gynaecol. 1998;105(11):1200–4.

D’Antonio

, Virgone

, Rizzo

, Khalil

, Baud

, Cohen-Overbeek

, et al. Prenatal risk factors and outcomes in gastroschisis: A meta-analysis. Pediatrics. 2015;136(1):e159–69.

10.

Nick

, Bruner

, Moses

, Yang

, Scott

. Second-trimester intra-abdominal bowel dilation in fetuses with gastroschisis predicts neonatal bowel atresia. Ultrasound Obstet Gynecol. 2006;28(6):821–5.

11.

Brantberg

, Blaas

H-GK

, Salvesen

, Haugen

, Eik-Nes

. Surveillance and outcome of fetuses with gastroschisis. Ultrasound Obstet Gynecol. 2004;23(1):4–13.

12.

Brantberg

, Blaas

H-G

, Haugen

, Eik-Nes

. Re: Second-trimester intra-abdominal bowel dilation in fetuses with gastroschisis predicts neonatal bowel atresia. Ultrasound Obstet Gynecol. 2006;28(7):981.

13.

Goetzinger

, Tuuli

, Longman

, Huster

, Odibo

, Cahill

. Sonographic predictors of postnatal bowel atresia in fetal gastroschisis. Ultrasound Obstet Gynecol. 2014;43(4):420–5.

14.

Emil

, Canvasser

, Chen

, Friedrich

, Su

. Contemporary 2-year outcomes of complex gastroschisis. J Pediatr Surg. 2012;47(8):1521–8.

15.

Ghionzoli

, James

, David

, Shah

, Tan

, Iskaros

, et al. Gastroschisis with intestinal atresia–predictive value of antenatal diagnosis and outcome of postnatal treatment. J Pediatr Surg. 2012;47(2):322–8.

16.

Kuleva

, Khen-Dunlop

, Dumez

, Ville

, Salomon

. Is complex gastroschisis predictable by prenatal ultrasound? BJOG Int J Obstet Gynaecol. 2012;119(1):102–9.

17.

Alfaraj

, Ryan

, Langer

, Windrim

, Seaward

, Kingdom

. Does gastric dilation predict adverse perinatal or surgical outcome in fetuses with gastroschisis? Ultrasound Obstet Gynecol. 2011;37(2):202–6.

18.

Mears

, Sadiq

, Impey

, Lakhoo

. Antenatal bowel dilatation in gastroschisis: A bad sign? Pediatr Surg Int. 2010;26(6):581–8.

19.

Contro

, Fratelli

, Okoye

, Papageorghiou

, Thilaganathan

, Bhide

. Prenatal ultrasound in the prediction of bowel obstruction in infants with gastroschisis. Ultrasound Obstet Gynecol. 2010;35(6):702–7.

20.

Huh

, Hirose

, Goldstein

. Prenatal intraabdominal bowel dilation is associated with postnatal gastrointestinal complications in fetuses with gastroschisis. Am J Obstet Gynecol. 2010;202(4):396.e1–6.

21.

Cohen-Overbeek

, Hatzmann

, Steegers

EAP

, Hop

, Wladimiroff

, Tibboel

. The outcome of gastroschisis after a prenatal diagnosis or a diagnosis only at birth. Recommendations for prenatal surveillance. Eur J Obstet Gynecol Reprod Biol. 2008;139(1):21–7.

22.

Andrade

, Brizot

, Rodrigues

, Tannuri

, Krebs

, Nishie

, et al. Sonographic markers in the prediction of fetal complex gastroschisis. Fetal Diagn Ther. 2018;43(1):45–52.

23.

Martillotti

, Boucoiran

, Damphousse

, Grignon

, Dubé

, Moussa

, et al. Predicting perinatal outcome from prenatal ultrasound characteristics in pregnancies complicated by gastroschisis. Fetal Diagn Ther. 2016;39(4):279–86.

24.

Heinig

, Müller

, Schmitz

, Lohse

, Klockenbusch

, Steinhard

. Sonographic assessment of the extra-abdominal fetal small bowel in gastroschisis: A retrospective longitudinal study in relation to prenatal complications. Prenat Diagn. 2008;28(2):109–14.

25.

Long

A-M

, Court

, Morabito

, Gillham

. Antenatal diagnosis of bowel dilatation in gastroschisis is predictive of poor postnatal outcome. J Pediatr Surg. 2011;46(6):1070–5.

26.

Brown

, Nardi

, Greer

, Petersen

, Thomas

, Gardener

, et al. Prenatal extra-abdominal bowel dilatation is a risk factor for intrapartum fetal compromise for fetuses with gastroschisis. Prenat Diagn. 2015;35(6):529–33.

27.

Wilson

, Carroll

, Braun

, Walsh

, Pietsch

, Bennett

. Is preterm delivery indicated in fetuses with gastroschisis and antenatally detected bowel dilation? Fetal Diagn Ther. 2012;32(4):262–6.

28.

Japaraj

, Hockey

, Chan

. Gastroschisis: Can prenatal sonography predict neonatal outcome? Ultrasound Obstet Gynecol. 2003;21(4):329–33.

29.

Tower

, Ong

SSC

, Ewer

, Khan

, Kilby

. Prognosis in isolated gastroschisis with bowel dilatation: A systematic review. Arch Dis Child Fetal Neonatal Ed. 2009;94(4):F268–74.

30.

Durfee

, Benson

, Adams

, Ecker

, House

, Jennings

, et al. Postnatal outcome of fetuses with the prenatal diagnosis of gastroschisis. J Ultrasound Med Off J Am Inst Ultrasound Med. 2013;32(3):407–12.

31.

Janoo

, Cunningham

, Hobbs

, O’Bringer

, Merzouk

. Can antenatal ultrasounds help predict postnatal outcomes in babies born with gastrochisis? The West Virginia experience. W V Med J. 2013;109(2):22–7.

32.

Overton

, Pierce

, Gao

, Kurinczuk

, Spark

, Draper

, et al. Antenatal management and outcomes of gastroschisis in the U. K. Prenat Diagn. 2012;32(13):1256–62.

33.

Ajayi

, Carroll

, Shellhaas

, Foy

, Corbitt

, Osawe

, et al. Ultrasound prediction of growth abnormalities in fetuses with gastroschisis. J Matern-Fetal Neonatal Med. 2011;24(3):489–92.

34.

Babcook

, Hedrick

, Goldstein

, Callen

, Harrison

, Adzick

, et al.

Gastroschisis: Can sonography of the fetal bowel accurately predict postnatal outcome?

J Ultrasound Med. 1994;13(9):701–6.

35.

Aina-Mumuney

, Fischer

, Blakemore

, Crino

, Costigan

, Swenson

, et al. A dilated fetal stomach predicts a complicated postnatal course in cases of prenatally diagnosed gastroschisis. Am J Obstet Gynecol. 2004;190(5):1326–30.

36.

Santiago-Munoz

, McIntire

, Barber

, Megison

, Twickler

, Dashe

. Outcomes of pregnancies with fetal gastroschisis. Obstet Gynecol. 2007;110(3):663–8.

37.

Kanda

, Ogawa

, Sugibayashi

, Sumie

, Matsui

, Wada

, et al. Stomach herniation predicts fetal death or non-reassuring fetal status in gastroschisis at late pregnancy. Prenat Diagn. 2013;33(13):1302–4.

38.

Sinkey

, Habli

, South

, Gibler

, Burns

, Eschenbacher

, et al. Sonographic markers associated with adverse neonatal outcomes among fetuses with gastroschisis: An 11-year, single-center review. Am J Obstet Gynecol. 2016;214(2):275.e1–7.

39.

Hadlock

, Harrist

, Sharman

, Deter

, Park

. Estimation of fetal weight with the use of head, body, and femur measurements–a prospective study. Am J Obstet Gynecol. 1985;151(3):333–7.

40.

Adams

, Durfee

, Pettigrew

, Katz

, Jennings

, Ecker

, et al. Accuracy of sonography to predict estimated weight in fetuses with gastroschisis. J Ultrasound Med. 2012;31(11):1753–8.

41.

Chaudhury

, Haeri

, Horton

, Wolfe

, Goodnight

. Ultrasound prediction of birthweight and growth restriction in fetal gastroschisis. Am J Obstet Gynecol. 2010;203(4):395.e1–5.

42.

Towers

, Carr

. Antenatal fetal surveillance in pregnancies complicated by fetal gastroschisis. Am J Obstet Gynecol. 2008;198(6):686.e1-5; discussion 686.e5.

43.

Netta

, Wilson

, Visintainer

, Johnson

, Hedrick

, Flake

, et al. Gastroschisis: Growth patterns and a proposed prenatal surveillance protocol. Fetal Diagn Ther. 2007;22(5):352–7.

44.

Sparks

, Shaffer

, Page

, Caughey

. Gastroschisis: mortality risks with each additional week of expectant management. Am J Obstet Gynecol. 2017;216(1):66.e1–7.

45.

Burge

, Ade-Ajayi

. Adverse outcome after prenatal diagnosis of gastroschisis: The role of fetal monitoring. J Pediatr Surg. 1997;32(3):441–4.

46.

Crawford

, Ryan

, Wright

, Rodeck

. The importance of serial biophysical assessment of fetal wellbeing in gastroschisis. Br J Obstet Gynaecol. 1992;99(11):899–902.

47.

South

, Stutey

, Meinzen-Derr

. Metaanalysis of the prevalence of intrauterine fetal death in gastroschisis. Am J Obstet Gynecol. 2013;209(2):114.e1–13.

48.

Meyer

, Shaffer

, Doss

, Cahill

AG3

, Snowden

JM2

, Caughey

. Prospective risk of fetal death with gastroschisis. J Matern-Fetal Neonatal Med. 2015;28(17):2126–9.

49.

Fratelli

, Papageorghiou

, Bhide

, Sharma

, Okoye

, Thilaganathan

. Outcome of antenatally diagnosed abdominal wall defects. Ultrasound Obstet Gynecol. 2007;30(3):266–70.

50.

Johnston

, Haeri

. Oligohydramnios and growth restriction do not portend worse prognosis in gastroschisis pregnancies. J Matern-Fetal Neonatal Med. 2016;1-4.

51.

Girsen

, Do

, Davis

, Hintz

, Desai

, Mansour

, et al. Peripartum and neonatal outcomes of small-for-gestational-age infants with gastroschisis. Prenat Diagn. 2015;35(5):477–82.

52.

Charlesworth

, Njere

, Allotey

, Dimitrou

, Ade-Ajayi

, Devane

, et al. Postnatal outcome in gastroschisis: Effect of birth weight and gestational age. J Pediatr Surg. 2007;42(5):815–8.

53.

Kassa

A-M

, Lilja

. Predictors of postnatal outcome in neonates with gastroschisis. J Pediatr Surg. 2011;46(11):2108–14.

54.

Ergün

, Barksdale

, Ergün

, Prosen

, Qureshi

, Reblock

, et al. The timing of delivery of infants with gastroschisis influences outcome. J Pediatr Surg. 2005;40(2):424–8.

55.

Carnaghan

, Pereira

, James

, Charlesworth

PB4

, Ghionzoli

, Mohamed

, et al.

Is early delivery beneficial in gastroschisis?

J Pediatr Surg. 2014;49(6):928–933; discussion 933.

56.

Carnaghan

, Baud

, Lapidus-Krol

, Ryan

, Shah

PS5

, Pierro

, et al. Effect of gestational age at birth on neonatal outcomes in gastroschisis. J Pediatr Surg. 2016;51(5):734–8.

57.

Maramreddy

, Fisher

, Slim

, Lagamma

, Parvez

. Delivery of gastroschisis patients before 37 weeks of gestation is associated with increased morbidities. J Pediatr Surg. 2009;44(7):1360–6.

58.

Overcash

, DeUgarte

, Stephenson

, Gutkin

, Norton

, Parmar

, et al. Factors associated with gastroschisis outcomes. Obstet Gynecol. 2014;124(3):551–7.

59.

Huang

, Kurkchubasche

, Carr

, Wesselhoeft

Jr , Tracy

Jr , Luks

. Benefits of term delivery in infants with antenatally diagnosed gastroschisis. Obstet Gynecol. 2002;100(4):695–9.

60.

Snyder

, Synder

, Biggio

, Barnes

, Bartle

, Georgeson

, et al. Effects of multidisciplinary prenatal care and delivery mode on gastroschisis outcomes. J Pediatr Surg. 2011;46(1):86–9.

61.

Boutros

, Regier

, Skarsgard

; Canadian Pediatric Surgery Network. Is timing everything? The influence of gestational age, birth weight, route, and intent of delivery on outcome in gastroschisis. J Pediatr Surg. 2009;44(5):912–7.

62.

Salihu

, Emusu

, Aliyu

, Pierre-Louis

, Druschel

, Kirby

. Mode of delivery and neonatal survival of infants with isolated gastroschisis. Obstet Gynecol. 2004;104(4):678–83.

63.

Gelas

, Gorduza

, Devonec

, Gaucherand

, Downham

, Claris

, et al. Scheduled preterm delivery for gastroschisis improves postoperative outcome. Pediatr Surg Int. 2008;24(9):1023–9.

64.

Hadidi

, Subotic

, Goeppl

, Waag

. Early elective cesarean delivery before 36 weeks vs. late spontaneous delivery in infants with gastroschisis. J Pediatr Surg. 2008;43(7):1342–6.

65.

Moir

, Ramsey

, Ogburn

, Johnson

, Ramin

. A prospective trial of elective preterm delivery for fetal gastroschisis. Am J Perinatol. 2004;21(5):289–94.

66.

Correia-Pinto

, Estevão-Costa

. Prolonged intestinal exposure to amniotic fluid does not result in peel formation in gastroschisis. J Pediatr Surg. 2000;35(2):399.

67.

Serra

, Fitze

, Kamin

, Dinger

, König

, Roesner

. Preliminary report on elective preterm delivery at 34 weeks and primary abdominal closure for the management of gastroschisis. Eur J Pediatr Surg. 2008;18(1):32–7.

68.

Logghe

, Mason

, Thornton

, Stringer

. A randomized controlled trial of elective preterm delivery of fetuses with gastroschisis. J Pediatr Surg. 2005;40(11):1726–31.

69.

Harper

, Goetzinger

, Biggio

, Macones

. Timing of elective delivery in gastroschisis: a decision and cost-effectiveness analysis. Ultrasound Obstet Gynecol. 2015;46(2):227–32.

70.

Cain

, Salemi

, Paul Tanner

, Mogos

, Kirby

, Whiteman

, et al. Perinatal outcomes and hospital costs in gastroschisis based on gestational age at delivery. Obstet Gynecol. 2014;124(3):543–50.

71.

Baud

, Lausman

, Alfaraj

, Seaward

, Kingdom

, Windrim

, et al. Expectant management compared with elective delivery at 37 weeks for gastroschisis. Obstet Gynecol. 2013;121(5):990–8.

72.

Al-Kaff

, MacDonald

, Kent

, Burrows

, Skarsgard

ED3

, Hutcheon

; Canadian Pediatric Network. Delivery planning for pregnancies with gastroschisis: Findings from a prospective national registry. Am J Obstet Gynecol. 2015;213(4):557.e1–8.