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Metaanalysis of the prevalence of intrauterine fetal death in gastroschisis

Published:April 29, 2013DOI:https://doi.org/10.1016/j.ajog.2013.04.032

      Objective

      The objective of this study was to review the medical literature that has reported the risk for intrauterine fetal death (IUFD) in pregnancies with gastroschisis.

      Study Design

      We systematically searched the literature to identify all published studies of IUFD and gastroschisis through June 2011 that were archived in MEDLINE, PubMed, or referenced in published manuscripts. The MESH terms gastroschisis or abdominal wall defect were used.

      Results

      Fifty-four articles were included in the metaanalysis. There were 3276 pregnancies in the study and a pooled prevalence of IUFD of 4.48 per 100. Those articles that included gestational age of IUFD had a pooled prevalence of IUFD of 1.28 per 100 births at ≥36 weeks' gestation. The prevalence did not appear to increase at >35 weeks' gestation.

      Conclusion

      The overall incidence of IUFD in gastroschisis is much lower than previously reported. The largest risk of IUFD occurs before routine and elective early delivery would be acceptable. Risk for IUFD should not be the primary indication for routine elective preterm delivery in pregnancies that are affected by gastroschisis.

      Key words

      For Editors' Commentary, see Contents
      Gastroschisis is an abdominal wall defect of unclear cause and increasing incidence worldwide; current estimates are near 5 per 10,000 births.
      • Castilla E.E.
      • Mastroiacovo P.
      • Orioli I.M.
      Gastroschisis: international epidemiology and public health perspectives.
      There have been great improvements in survival in this patient population because >95% of infants survive from birth to initial hospital discharge.
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      • et al.
      Gastroschisis: one year outcomes from national cohort study.
      However, there remain many questions about perinatal management and, in particular, about the optimal gestational age at delivery. Intrauterine fetal death (IUFD) is more common in pregnancies that are affected by congenital anomalies. Among all major congenital anomalies, 2% of pregnancies result in stillbirth,
      • Dolk H.
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      The prevalence of congenital anomalies in Europe.
      which is much higher than the 0.6% baseline rate in the general population.
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      Fetal and perinatal mortality, United States, 2005.

      Centers for Disease Control and Prevention. National Center for Health Statistics. VitalStats. Available at: http://www.cdc.gov/nchs/vitalstats.htm. Accessed Aug. 21, 2012.

      This higher risk of stillbirth results in a higher frequency and level of antenatal monitoring and, in some cases, elective delivery at <39 weeks' gestation.
      • Craigo S.D.
      Indicated preterm birth for fetal anomalies.
      Decisions regarding obstetric management must be based on accurate knowledge of the risk for fetal death.
      The mean age of spontaneous labor in pregnancies that are affected by gastroschisis is between 36 and 37 weeks' gestation,
      • Lausman A.Y.
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      • Tai M.
      • et al.
      Gastroschisis: what is the average gestational age of spontaneous delivery?.
      yet the average age of delivery is approximately 1 week earlier. This discrepancy leads to the conclusion that infants with gastroschisis deliver early either for fetal/maternal indications or electively.
      • Barseghyan K.
      • Aghajanian P.
      • Miller D.A.
      The prevalence of preterm births in pregnancies complicated with fetal gastroschisis.
      Although some clinicians advocate for early delivery to improve postnatal clinical outcomes (such as earlier initiation of enteral feeds and shorter hospitalization time), the literature does not document a consistent benefit.
      • Simmons M.
      • Georgeson K.E.
      The effect of gestational age at birth on morbidity in patients with gastroschisis.
      • Ergün O.
      • Barksdale E.
      • Ergün F.S.
      • et al.
      The timing of delivery of infants with gastroschisis influences outcome.
      • Garne E.
      • Loane M.
      • Dolk H.
      Gastrointestinal malformations: impact of prenatal diagnosis on gestational age at birth.
      Therefore, the primary rationale for elective delivery before the onset of labor may be the prevention of IUFD.
      • Burge D.M.
      • Ade-Ajayi N.
      Adverse outcome after prenatal diagnosis of gastroschisis: the role of fetal monitoring.
      The reported incidence of IUFD in pregnancies that are affected by gastroschisis is as high as 12.5%.
      • Crawford R.A.
      • Ryan G.
      • Wright V.M.
      • Rodeck C.H.
      The importance of serial biophysical assessment of fetal wellbeing in gastroschisis.
      Although the cause for the increased risk of IUFD is unknown, hypotheses include umbilical cord compression after acute intestinal dilation,
      • Kalache K.D.
      • Bierlich A.
      • Hammer H.
      • Bollmann R.
      Is unexplained third trimester intrauterine death of fetuses with gastroschisis caused by umbilical cord compression due to acute extra-abdominal bowel dilatation?.
      oligohydramnios,
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      • Borgnon J.
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      • Sagot P.
      Transabdominal amnioinfusion to avoid fetal demise and intestinal damage in fetuses with gastroschisis and severe oligohydramnios.
      cardiovascular compromise that is related to high protein loss through the defect and subsequent hypovolemia,
      • Carroll S.G.
      • Kuo P.Y.
      • Kyle P.M.
      • Soothill P.W.
      Fetal protein loss in gastroschisis as an explanation of associated morbidity.
      and cytokine-mediated inflammation.
      • Luton D.
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      • Guibourdenche J.
      • et al.
      Prognostic factors of prenatally diagnosed gastroschisis.
      • Guibourdenche J.
      • Berrebi D.
      • Vuillard E.
      • et al.
      Biochemical investigations of bowel inflammation in gastroschisis.
      Additionally, there is increased risk for volvulus and vascular compromise that could lead to fetal death.
      • Bhatia A.M.
      • Musemeche C.A.
      • Crino J.P.
      Gastroschisis complicated by midgut atresia and closure of the defect in utero.
      Studies that have documented high rates of IUFD are limited by small numbers, and many were conducted at a time when prenatal diagnosis of gastroschisis was uncommon. These studies found that most IUFDs occurred late in the third trimester. Obstetricians developed the practice of early elective delivery based on these studies. Additional studies that have suggested lower rates of IUFD are also limited by sample sizes and evaluations of single institutions or populations. Our own experience suggests a much lower rate of IUFD than 10-12%. The limitations of individual studies compromise ascertainment of the true incidence of IUFDs with gastroschisis.
      We present a metaanalysis to generate a more accurate representation of the prevalence of IUFD among infants with prenatal diagnosis of gastroschisis. We hypothesize that the prevalence of IUFD is less than previously reported and that the risk of IUFD does not vary with gestational age.

      Materials and Methods

      We conducted a metaanalysis of the published, English-language literature that is related to gastroschisis.

      Literature search

      A systematic search was done independently by 2 of the authors (A.S., K.S.) who reviewed the literature to identify all published studies through June 2011 that were archived in MEDLINE and PubMed or were referenced in published articles. The MESH terms gastroschisis or abdominal wall defect were used. Abstracts were reviewed initially and excluded based on predetermined criteria that included non-English language, nonhuman subjects, or no relation to gastroschisis. The remaining articles were selected for full text review, which led to further exclusion of articles that did not report the number of IUFDs, case reports, studies with small sample sizes (n <10), and datasets that did not represent the total population (eg, case series of live births with gastroschisis or if the total number of pregnancies with gastroschisis was not disclosed). When there were multiple studies that used the same dataset, we included only 1 article and prioritized the article that reported the gestational age of IUFD. If both articles reported gestational age at IUFD, the article with the larger number of infants was included. The included articles were divided into those with a stated gestational age at IUFD and those without.

      Data extraction

      Data regarding all reported pregnancies, including termination of pregnancy, were extracted independently from all included studies by 2 authors (A.S., K.S.). Extracted data included gestational age at delivery, gestational age at IUFD, country of origin, year the study was published, presence of comorbidities in addition to gastroschisis, and obstetric delivery plan. IUFD was defined as an unplanned fetal death or stillbirth at any gestational age. The mean or median gestational age at delivery was extracted for each study. Early delivery plan was defined as systematic elective delivery at any predefined gestational age, compared with awaiting the onset of spontaneous labor or delivery because of maternal or fetal indications.

      Quality assessment

      A scoring system that was based on a previous metaanalysis was used to create a grading scale for the articles.
      • Luppa M.
      • Sikorski C.
      • Luck T.
      • et al.
      Age- and gender-specific prevalence of depression in latest-life: systematic review and meta-analysis.
      Studies were independently graded (A.S., K.S.) with the use of a standardized evaluation form that had been developed for the purpose of this metaanalysis. Each study was assigned a grade of 1-5 according to the quality of reporting of 5 factors. Variables were chosen to represent the factors that we believed to be essential for contributing valid data (population-based data, prospective data collection) or essential for understanding results (identified obstetric delivery plan, reported gestational age at birth, and reported gestational age at the time of IUFD). Differences between reviewers' grades were resolved by consensus among all 3 authors. The quality markers that were chosen for this study were identified before the start of data abstraction. The rate of IUFD was compared among studies on the basis of the assigned quality assessment scores.

      Statistical analysis

      The rate of IUFD was calculated for each study with the number of IUFDs reported in the numerator and the number of live births plus IUFDs in the denominator. Pregnancies that were terminated electively were not included in the numerator or denominator, because these pregnancies were considered not at risk for an IUFD. A random-effects model was used to aggregate individual effect sizes to create a pooled prevalence of IUFD. Random-effects models are based on the assumption that the studies that were selected for analysis are a sample of all potential studies by incorporating between-study variability in the overall pooled estimation.
      • Hedges L.
      • Vevea J.
      Fixed- and random-effects models in meta-analysis.
      Pooled prevalence estimates of IUFD with 95% confidence intervals were reported from these models with the use of the Der Simonian-Laird random-effects method.
      • DerSimonian R.
      • Laird N.
      Meta-analysis in clinical trials.
      All rates were calculated as deaths per 100 total births, with total births being the summation of live births and fetal deaths. Subgroup analyses were performed for the prevalence of IUFD with the following stratifications: gestational age, early delivery plan, study site (within US vs international), study grading, and years in which the study occurred.
      Homogeneity across studies was tested with the I2 index, which provides a measure (or percentage) of the variation in prevalence attributable to between-study heterogeneity.
      • Higgins J.P.
      • Thompson S.G.
      Quantifying heterogeneity in a meta-analysis.
      • Higgins J.P.
      • Thompson S.G.
      • Deeks J.J.
      • Altman D.G.
      Measuring inconsistency in meta-analyses.
      An I2 value of >75% is interpreted as high heterogeneity.
      • Higgins J.P.
      • Thompson S.G.
      • Deeks J.J.
      • Altman D.G.
      Measuring inconsistency in meta-analyses.
      Post-hoc sensitivity analyses were conducted to investigate the potential sources of heterogeneity from specific studies that may have biased the analyses. Studies that potentially influenced heterogeneity were removed from analyses, and the results were compared with the original findings. A forest plot was created to illustrate the prevalence of each study, with 95% confidence intervals, that contributed to the analysis along with the pooled prevalence estimate. Finally, all studies that reported mean/median gestational ages of the live births of gastroschisis were divided into 3 time periods: before 1990, 1990-1999, and after 2000. The mean/median birth rates of gastroschisis were described for each time period to determine trends in timing of delivery.

      Results

      Study and patient characteristics

      Our search produced 1123 results. Review of these abstracts resulted in 100 articles for further review (Figure 1). Six articles
      • Byron-Scott R.
      • Haan E.
      • Chan A.
      • Bower C.
      • Scott H.
      • Clark K.
      A population-based study of abdominal wall defects in South Australia and Western Australia.
      • Sharp M.
      • Bulsara M.
      • Gollow I.
      • Pemberton P.
      Gastroschisis: early enteral feeds may improve outcome.
      • Contro E.
      • Fratelli N.
      • Okoye B.
      • Papageorghiou A.
      • Thilaganathan B.
      • Bhide A.
      Prenatal ultrasound in the prediction of bowel obstruction in infants with gastroschisis.
      • Fisher R.
      • Attah A.
      • Partington A.
      • Dykes E.
      Impact of antenatal diagnosis on incidence and prognosis in abdominal wall defects.
      • Grundy H.
      • Anderson R.L.
      • Filly R.A.
      • et al.
      Gastroschisis: prenatal diagnosis and management.
      • Garne E.
      • Rasmussen L.
      • Husby S.
      Gastrointestinal malformations in Funen county, Denmark: epidemiology, associated malformations, surgery and mortality.
      were excluded because of use of overlapping datasets with articles that were included in the analysis.
      • Crawford R.A.
      • Ryan G.
      • Wright V.M.
      • Rodeck C.H.
      The importance of serial biophysical assessment of fetal wellbeing in gastroschisis.
      • Reid K.P.
      • Dickinson J.E.
      • Doherty D.A.
      The epidemiologic incidence of congenital gastroschisis in Western Australia.
      • Fratelli N.
      • Papageorghiou A.T.
      • Bhide A.
      • Sharma A.
      • Okoye B.
      • Thilaganathan B.
      Outcome of antenatally diagnosed abdominal wall defects.
      • Bond S.J.
      • Harrison M.R.
      • Filly R.A.
      • Callen P.W.
      • Anderson R.A.
      • Golbus M.S.
      Severity of intestinal damage in gastroschisis: correlation with prenatal sonographic findings.
      • Bugge M.
      • Holm N.V.
      Abdominal wall defects in Denmark, 1970-89.
      Three articles were removed for having <10 subjects.
      • Arnaoutoglou C.
      • Keivanidou A.
      • Arnaoutoglou M.
      • et al.
      Outcome of antenatally diagnosed fetal anterior abdominal wall defects from a single tertiary centre.
      • Cedergren M.
      • Selbing A.
      Detection of fetal structural abnormalities by an 11-14-week ultrasound dating scan in an unselected Swedish population.
      • Redford D.H.
      • McNay M.B.
      • Whittle M.J.
      Gastroschisis and exomphalos: precise diagnosis by midpregnancy ultrasound.
      One article was removed because it did not appear to study consecutive cases of pregnancies that were affected by gastroschisis and thus did not reflect the total population at risk,
      • Carroll S.G.
      • Kuo P.Y.
      • Kyle P.M.
      • Soothill P.W.
      Fetal protein loss in gastroschisis as an explanation of associated morbidity.
      and 3 additional articles were excluded for being case reports. We included 54 eligible studies in the final statistical analysis (Figure 2). Thirty-five studies reported information regarding gestational ages at the time of the IUFD and/or a mean or median gestational age at delivery. Nineteen articles included the total number of IUFDs but did not provide the gestational age of each IUFD.
      Figure thumbnail gr1
      Figure 1Process of study selection
      Flow diagram shows the number of citations that were identified, the exclusions with indications, and the total articles for further analysis that are separated into those citations that included gestational age (GA) for intrauterine fetal death (IUFD) and those without.
      South. Risk of IUFD in gastroschisis. Am J Obstet Gynecol 2013.
      Figure thumbnail gr2
      Figure 2Forest plot shows odds ratios (random effect model)
      South. Risk of IUFD in gastroschisis. Am J Obstet Gynecol 2013.
      Final eligible studies included 3276 total pregnancies that were affected by gastroschisis (IUFD plus live births) and 177 IUFDs. Of the 54 studies that were included, 12 studies (22%) reported no IUFDs (Table 1). Sixteen studies (30%) reported a planned elective delivery before onset of labor. Seventeen studies (32%) took place in the United States. The median gestational age of 48 IUFDs for which information was available was 33 weeks (range, 18–41 weeks). For those studies that reported a mean or median gestational age, the average reported mean or median gestational age at delivery for included studies was 35.7 weeks (median, 36 weeks; range of medians, 34–37 weeks). Only 4 studies (7.4%) had a quality grade of 5 (the highest quality). Twenty-two studies (40.7%) had a grade of 4; 14 studies (25.9%) had a grade of 3; 11 studies (20.4%) had a grade of 2, and only 3 studies had the lowest grade of 1 (Table 2).
      Table 1Characteristics of the studies that were included in the systematic review
      StudyOriginStudy designStudy yearsTotal, nSpontaneous abortion, nTermination of pregnancy, nIntrauterine fetal death, n/N (%)Delivery planGestational age at birth, wk + dGestational age of intrauterine fetal death, wkQuality assessment score
      Abuhamad et al, 1997
      • Abuhamad A.Z.
      • Mari G.
      • Cortina R.M.
      • Croitoru D.P.
      • Evans A.T.
      Superior mesenteric artery Doppler velocimetry and ultrasonographic assessment of fetal bowel in gastroschisis: a prospective longitudinal study.
      VAPRNR17NR01/17 (6)No standard delivery plan35.8
      Data were reported as mean ± SD
      ± 2.74
      284
      Adair et al, 1996
      • Adair C.D.
      • Rosnes J.
      • Frye A.H.
      • Burrus D.R.
      • Nelson L.H.
      • Veille J.C.
      The role of antepartum surveillance in the management of gastroschisis.
      NCRR1985-199429NR04/29 (13.8)No standard delivery planNR28-412
      Adra et al, 1996
      • Adra A.M.
      • Landy H.J.
      • Nahmias J.
      • Gómez-Marín O.
      The fetus with gastroschisis: impact of route of delivery and prenatal ultrasonography.
      FLRR1986-199447NR32/44 (4.5)No standard delivery plan36.0
      Data were reported as mean ± SD
      ± 2.4
      28, 364
      Ajayi et al, 2011
      • Ajayi F.A.
      • Carroll P.D.
      • Shellhaas C.
      • et al.
      Ultrasound prediction of growth abnormalities in fetuses with gastroschisis.
      OHRR2000-200874NR00/74Elective delivery at 36-37 wks' gestation35.2
      Data were reported as mean (range)
      (26.3–38.1)
      N/A3
      Alfaraj et al, 2011
      • Alfaraj M.A.
      • Ryan G.
      • Langer J.C.
      • Windrim R.
      • Seaward P.G.
      • Kingdom J.
      Does gastric dilation predict adverse perinatal or surgical outcome in fetuses with gastroschisis?.
      CanadaRR2001-201098NR01/98 (1.0)NRNRNR2
      Alsulyman et al, 1996
      • Alsulyman O.M.
      • Monteiro H.
      • Ouzounian J.G.
      • Barton L.
      • Songster G.S.
      • Kovacs B.W.
      Clinical significance of prenatal ultrasonographic intestinal dilatation in fetuses with gastroschisis.
      LARR1988-199523NR10/22NR34.3
      Data were reported as mean ± SD
      ± 6.3
      N/A4
      Axt et al, 1999
      • Axt R.
      • Quijano F.
      • Boos R.
      • et al.
      Omphalocele and gastroschisis: prenatal diagnosis and peripartal management: a case analysis of the years 1989-1997 at the Department of Obstetrics and Gynecology, University of Homburg/Saar.
      GermanyRR1989-199718NR30/15NR36.1
      Data were reported as mean ± SD
      ± 3.1
      N/A4
      Badillo et al, 2008
      • Badillo A.T.
      • Hedrick H.L.
      • Wilson R.D.
      • et al.
      Prenatal ultrasonographic gastrointestinal abnormalities in fetuses with gastroschisis do not correlate with postnatal outcomes.
      PARR2000-200764NR12/63 (3.2)NRNRNR2
      Barisic et al, 2001
      • Barisic I.
      • Clementi M.
      • Häusler M.
      • et al.
      Evaluation of prenatal ultrasound diagnosis of fetal abdominal wall defects by 19 European registries.
      11 European nationsRR1996-1998106NR3113/75 (17.3)NR36.3
      Data were reported as mean ± SD
      ± 2.2
      NR3
      Bond et al, 1988
      • Bond S.J.
      • Harrison M.R.
      • Filly R.A.
      • Callen P.W.
      • Anderson R.A.
      • Golbus M.S.
      Severity of intestinal damage in gastroschisis: correlation with prenatal sonographic findings.
      CARR1982-198615NR30/11NRNRN/A2
      Boyd et al, 1998
      • Boyd P.A.
      • Bhattacharjee A.
      • Gould S.
      • Manning N.
      • Chamberlain P.
      Outcome of prenatally diagnosed anterior abdominal wall defects.
      UKRR1985-199541NR70/34NR37
      Data were reported as median (range).
      N/A3
      Brantberg et al, 2004
      • Brantberg A.
      • Blaas H.G.
      • Salvesen K.A.
      • Haugen S.E.
      • Eik-Nes S.H.
      Surveillance and outcome of fetuses with gastroschisis.
      NorwayPR1988-200264NR31/61 (1.6)C/S at 37-39 wks' gestation36 + 1 (28–39)
      Data were reported as mean (range)
      35 + 55
      Bugge and Holm, 2002
      • Bugge M.
      • Holm N.V.
      Abdominal wall defects in Denmark, 1970-89.
      DenmarkRR1970-1989166NRNR9/166 (3.3)NRNRNR2
      Burge and Ade-Ajayi, 1997
      • Burge D.M.
      • Ade-Ajayi N.
      Adverse outcome after prenatal diagnosis of gastroschisis: the role of fetal monitoring.
      UKRR1982-199557NR03/54 (5.6)Spontaneous labor36
      Data were reported as mean ± SD
      32, 36, 394
      Calzolari et al, 1995
      • Calzolari E.
      • Bianchi F.
      • Dolk H.
      • Milan M.
      Omphalocele and gastroschisis in Europe: a survey of 3 million births 1980-1990. EUROCAT Working Group.
      ItalyPR1980-1990274NRNR40/274 (14.6)NRNR20-27 (n = 18) NR (n = 22)3
      Chen et al, 1996
      • Chen C.P.
      • Liu F.F.
      • Jan S.W.
      • Sheu J.C.
      • Huang S.H.
      • Lan C.C.
      Prenatal diagnosis and perinatal aspects of abdominal wall defects.
      ChinaRR1/1987-9/199415NR22/13 (15.4)NRNRNR2
      Chescheir et al, 1991
      • Chescheir N.C.
      • Azizkhan R.G.
      • Seeds J.W.
      • Lacey S.R.
      • Watson W.J.
      Counseling and care for the pregnancy complicated by gastroschisis.
      NCRR1986-199019NR01/19 (5.3)NRNR283
      Cohen-Overbeek et al, 2008
      • Cohen-Overbeek T.E.
      • Hatzmann T.R.
      • Steegers E.A.
      • Hop W.C.
      • Wladimiroff J.W.
      • Tibboel D.
      The outcome of gastroschisis after a prenatal diagnosis or a diagnosis only at birth: recommendations for prenatal surveillance.
      The NetherlandsRR1/1991-6/200333NR23/31 (9.7)Induction at 37 wks' gestationNR19, 33, 363
      Crawford et al, 1992
      • Crawford R.A.
      • Ryan G.
      • Wright V.M.
      • Rodeck C.H.
      The importance of serial biophysical assessment of fetal wellbeing in gastroschisis.
      UKRR1986-199126NR23/24 (12.5)No standard delivery planNR34, 35, 374
      Dillon and Renwick, 1995
      • Dillon E.
      • Renwick M.
      The antenatal diagnosis and management of abdominal wall defects: the northern region experience.
      UKPR1988-199256323/51 (5.9)No standard delivery planNR32, 32, 374
      Durfee et al, 2002
      • Durfee S.M.
      • Downard C.D.
      • Benson C.B.
      • Wilson J.M.
      Postnatal outcome of fetuses with the prenatal diagnosis of gastroschisis.
      MARR4/1990-12/200026NR20/24NRNRN/A2
      Eurenius and Axelsson, 1994
      • Eurenius K.
      • Axelsson O.
      Outcome for fetuses with abdominal wall defects detected by routine second trimester ultrasound.
      SwedenRR1983-199024NR41/20 (5.0)NRNRNR2
      Feldkamp et al, 2008
      • Feldkamp M.L.
      • Alder S.C.
      • Carey J.C.
      A case control population-based study investigating smoking as a risk factor for gastroschisis in Utah, 1997-2005.
      UTPR1/1997-12/2005189NR311/186 (5.9)NRNRNR2
      Fillingham and Rankin, 2008
      • Fillingham A.
      • Rankin J.
      Prevalence, prenatal diagnosis and survival of gastroschisis.
      UKRR1/97-12/06143NR32/140 (1.4)NRNRNR2
      Fitzsimmons et al, 1988
      • Fitzsimmons J.
      • Nyberg D.A.
      • Cyr D.R.
      • Hatch E.
      Perinatal management of gastroschisis.
      WARR1/1980-12/198615NR01/15 (6.7)C/S at 36 wks' gestation35.9
      Data were reported as mean (range)
      (31–37)
      413
      Forrester and Merz, 1999
      • Forrester M.B.
      • Merz R.D.
      Epidemiology of abdominal wall defects, Hawaii, 1986-1997.
      HIRR1986-199774NR67/68 (10.3)NRNRNR1
      Fratelli et al, 2007
      • Fratelli N.
      • Papageorghiou A.T.
      • Bhide A.
      • Sharma A.
      • Okoye B.
      • Thilaganathan B.
      Outcome of antenatally diagnosed abdominal wall defects.
      UKRR1/1997-4/200640NR22/38 (5.3)Induction at 38-39 wks' gestation37 + 1 (36 + 0 to 38 + 1)
      Data were reported as median (range).
      18, 224
      Garcia et al, 2010
      • Garcia L.
      • Brizot M.
      • Liao A.
      • Silva M.M.
      • Tannuri A.C.
      • Zugaib M.
      Bowel dilation as a predictor of adverse outcome in isolated fetal gastroschisis.
      BrazilRR1/1997-8/200994NRNR5/94 (5.3)Elective C/S at 37 wks' gestation36.5 ± 1.4
      Data were reported as mean ± SD
      32, 34, 35, 36, 374
      Garne et al, 2007
      • Garne E.
      • Loane M.
      • Dolk H.
      Gastrointestinal malformations: impact of prenatal diagnosis on gestational age at birth.
      Denmark and UKRR1997-2002216NR399/177 (5.1)NR36
      Data were reported as median (range).
      NR3
      Goldkrand et al, 2004
      • Goldkrand J.W.
      • Causey T.N.
      • Hull E.E.
      The changing face of gastroschisis and omphalocele in southeast Georgia.
      GARR1/1994-9/200234NRNR2/34 (5.8)Planned delivery at >37 wks' gestationNR32.7, 363
      Heinig et al, 2008
      • Heinig J.
      • Müller V.
      • Schmitz R.
      • Lohse K.
      • Klockenbusch W.
      • Steinhard J.
      Sonographic assessment of the extra-abdominal fetal small bowel in gastroschisis: a retrospective longitudinal study in relation to prenatal complications.
      GermanyRR10/2001-9/200514NRNR2/14 (14.3)C/S at 37-39 wks' gestation33 + 6 to 36 + 633 + 6, 35 + 34
      Hidaka et al, 2009
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      • et al.
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      JapanRR1990-200611NRNR1/11 (9.1)C/S at 37-38 wks' gestationNR354
      Horton et al, 2010
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      • Powell M.S.
      • Wolfe H.M.
      Intrauterine growth patterns in fetal gastroschisis.
      NCRR1/2000- 1/290771NRNR2/71 (2.8)Spontaneous labor35 + 4 ± 2.4
      Data were reported as mean ± SD
      27, 334
      Huang et al, 2002
      • Huang J.
      • Kurkchubasche A.G.
      • Carr S.R.
      • Wesselhoeft Jr., C.W.
      • Tracy Jr., T.F.
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      Benefits of term delivery in infants with antenatally diagnosed gastroschisis.
      RIRR1991-200160NRNR3/60 (5.0)NRNRNR1
      Japaraj et al, 2003
      • Japaraj R.P.
      • Hockey R.
      • Chan F.Y.
      Gastroschisis: can prenatal sonography predict neonatal outcome?.
      AustraliaRR1/1993-5/200145NRNR0/45NR35.6
      Data were reported as mean (range)
      (24–39)
      N/A3
      Kamata et al, 1996
      • Kamata S.
      • Ishikawa S.
      • Usui N.
      • et al.
      Prenatal diagnosis of abdominal wall defects and their prognosis.
      JapanRR1982-199412NRNR1/12 (8.3)Spontaneous labor35.4
      Data were reported as mean ± SD
      ± 3.7
      314
      Lafferty et al, 1989
      • Lafferty P.M.
      • Emmerson A.J.
      • Fleming P.J.
      • Frank J.D.
      • Noblett H.R.
      Anterior abdominal wall defects.
      UKRR1981-198627NR41/23 (4.3)Spontaneous labor37.2
      Data were reported as mean (range)
      (33.5–40.0)
      373
      Lausman et al, 2007
      • Lausman A.Y.
      • Langer J.C.
      • Tai M.
      • et al.
      Gastroschisis: what is the average gestational age of spontaneous delivery?.
      CanadaRR1/1980- 12/2001158132/154 (1.3)Eighty-six women had spontaneous labor; 66 women had planned delivery36.6 ± 2
      Data were reported as mean ± SD
      24, 354
      Logghe et al, 2005
      • Logghe H.L.
      • Mason G.C.
      • Thornton J.G.
      • Stringer M.D.
      A randomized controlled trial of elective preterm delivery of fetuses with gastroschisis.
      UKRCT5/1995- 9/199942NRNR1/42 (2.4)Two groups of 21 women randomly assigned to induction at 36 wks' gestation or spontaneous deliveryInduction: 35.8 ± 0.7
      Data were reported as mean ± SD
      ; spontaneous: 36.7 ± 1.5
      Data were reported as mean ± SD
      315
      Mears et al, 2010
      • Mears A.L.
      • Sadiq J.M.
      • Impey L.
      • Lakhoo K.
      Antenatal bowel dilatation in gastroschisis: a bad sign?.
      UKRR2004-200860NR03/60 (5.0)Induction at 37 wks' gestation36
      Data were reported as mean ± SD
      NR3
      Moir et al, 2004
      • Moir C.R.
      • Ramsey P.S.
      • Ogburn P.L.
      • Johnson R.V.
      • Ramin K.D.
      A prospective trial of elective preterm delivery for fetal gastroschisis.
      MNPRNR27NR00/27Deliver at >29 wks' gestation and 3/4 criteria: (1) maximum bowel diameter >10 mm, (2) wall thickness >2 mm, (3) lack of peristalsis, (4) intestinal mattingDelivery plan: 34.2 ± 2.4
      Data were reported as mean ± SD
      ; controlled trial: 37.7 ± 1.8
      Data were reported as mean ± SD
      N/A5
      Morrow et al, 1993
      • Morrow R.J.
      • Whittle M.J.
      • McNay M.B.
      • Raine P.A.
      • Gibson A.A.
      • Crossley J.
      Prenatal diagnosis and management of anterior abdominal wall defects in the west of Scotland.
      ScotlandRR1983-1989476112/30 (6.7)NR36
      Data were reported as mean (range)
      (31–38)
      >28 (n = 2)2
      Nicholas et al, 2009
      • Nicholas S.S.
      • Stamilio D.M.
      • Dicke J.M.
      • Gray D.L.
      • Macones G.A.
      • Odibo A.O.
      Predicting adverse neonatal outcomes in fetuses with abdominal wall defects using prenatal risk factors.
      WARR1991-200680NR42/76 (2.6)Spontaneous laborNRNR2
      Rankin et al, 1999
      • Rankin J.
      • Dillon E.
      • Wright C.
      Congenital anterior abdominal wall defects in the north of England, 1986-1996: occurrence and outcome.
      UKRR1986-1996126NR124/108 (3.7)NRNRNR3
      Reid et al, 2003
      • Reid K.P.
      • Dickinson J.E.
      • Doherty D.A.
      The epidemiologic incidence of congenital gastroschisis in Western Australia.
      AustraliaPR1980-2001122NRNR12/122 (9.8)Elective delivery at 38 wks' gestation37
      Data were reported as median (range).
      (24–41)
      34
      Data were reported as median (range).
      (24–39)
      5
      Reigstad et al, 2011
      • Reigstad I.
      • Reigstad H.
      • Kiserud T.
      • Berstad T.
      Preterm elective caesarean section and early enteral feeding in gastroschisis.
      NorwayRR1993-200836NR06/36 (17)Two groups: (1) spontaneous labor (n = 10); (2) elective C/S at 36-37 wks' gestation (n = 20)Group 1: 36.5 (34–40)
      Data were reported as median (range).
      ; group 2: 35.0 (34–37)
      Data were reported as median (range).
      <20 (n = 3) 28, 29, 394
      Rinehart et al, 1999
      • Rinehart B.K.
      • Terrone D.A.
      • Isler C.M.
      • Larmon J.E.
      • Perry Jr., K.G.
      • Roberts W.E.
      Modern obstetric management and outcome of infants with gastroschisis.
      MSRR9/1992-6/199833NR10/32NROutside center: 35.3 ± 2.2
      Data were reported as mean ± SD
      ; tertiary center: 35.6 ± 1.4
      Data were reported as mean ± SD
      N/A3
      Salomon et al, 2004
      • Salomon L.J.
      • Mahieu-Caputo D.
      • Jouvet P.
      • et al.
      Fetal home monitoring for the prenatal management of gastroschisis.
      FrancePR3/1998-7/200131NR1/31 (3.2)NRLow risk (n = 20 women): 35.5 (32–38)
      Data were reported as median (range).
      ; high risk (n = 11 women: 34.5 (32–36)
      Data were reported as median (range).
      NR3
      Santiago-Munoz et al, 2007
      • Santiago-Munoz P.C.
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      • Barber R.G.
      • Megison S.M.
      • Twickler D.M.
      • Dashe J.S.
      Outcomes of pregnancies with fetal gastroschisis.
      USRR1/1998-6/200666NR03/66 (4.5)Spontaneous labor37.1 ± 1.9
      Data were reported as mean ± SD
      33, 38, 404
      Serra et al, 2008
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      • König I.R.
      • Roesner D.
      Preliminary report on elective preterm delivery at 34 weeks and primary abdominal closure for the management of gastroschisis.
      GermanyRR1999-200423NR0/23Two groups: (1)

      C/S at 34 wks' gestation; (2)

      spontaneous labor
      Group 1: 243 (226–264) days
      Data were reported as median (range).
      ; group 2: 257 (235–282) days
      Data were reported as median (range).
      N/A4
      Sipes et al, 1990
      • Sipes S.L.
      • Weiner C.P.
      • Sipes 2nd, D.R.
      • Grant S.S.
      • Williamson R.A.
      Gastroschisis and omphalocele: does either antenatal diagnosis or route of delivery make a difference in perinatal outcome?.
      IA, WIRR12/1979-1/198933NR10/32Spontaneous labor36.3 ± 2.4
      Data were reported as mean ± SD
      N/A3
      Skarsgard et al, 2008
      • Skarsgard E.D.
      • Claydon J.
      • Bouchard S.
      • et al.
      Canadian Pediatric Surgical Network: a population-based pediatric surgery network and database for analyzing surgical birth defects: the first 100 cases of gastroschisis.
      CanadaRR2005-2006114NR3 (4 lost to follow up)1/107 (0.9)NR35.9 ± 2.3
      Data were reported as mean ± SD
      NR2
      Towers and Carr, 2008
      • Towers C.V.
      • Carr M.H.
      Antenatal fetal surveillance in pregnancies complicated by fetal gastroschisis.
      USRR1/1986-12/200385NR02/84 (2.4)Spontaneous laborNR29 + 4, 31 + 34
      Vegunta et al, 2005
      • Vegunta R.K.
      • Wallace L.J.
      • Leonardi M.R.
      • et al.
      Perinatal management of gastroschisis: analysis of a newly established clinical pathway.
      ILRR6/1998-8/200230NR00/30C/S 36-38 wks' gestation35.7 (28.4–38.6)
      Data were reported as median (range).
      N/A3
      C/S, cesarean section delivery; N/A, not applicable; NR, not reported; PR, prospective observational review; RCT, randomized controlled trial; RR, retrospective review.
      South. Risk of IUFD in gastroschisis. Am J Obstet Gynecol 2013.
      a Data were reported as mean ± SD
      b Data were reported as mean (range)
      c Data were reported as median (range).
      Table 2Pooled prevalence of intrauterine fetal death by graded quality of study
      GradeStudies, nPregnancies, nPooled prevalence per 100 births95% CI
      1, 21412624.492.81–7.08
      3146032.501.29–4.78
      4, 52614115.654.01–7.89
      CI, confidence interval.
      South. Risk of IUFD in gastroschisis. Am J Obstet Gynecol 2013.

      Metaanalysis

      The pooled prevalence of IUFD for all studies was 4.48 per 100 gastroschisis pregnancies (live births + IUFD; 95% confidence interval [CI], 3.48–5.76). There was no significant difference in IUFD rate between centers with and without an early delivery plan in place (prevalence, 4.09; 95% CI, 2.39–6.91 vs 4.64; 95% CI, 3.47–6.17 per 100 births, respectively; P = .7). The mean gestational age at delivery for those studies that reported an early delivery plan was not different from those studies in which there was no delivery plan (prevalence, 35.5 ± 0.83 (SD) vs 35.8 ± 0.85; P = .22). There was also no difference in IUFD rate between studies conducted in the United States vs outside the United States (prevalence, 3.65; 95% CI, 2.26–5.84 vs 4.89; 95% CI, 3.63–6.56; P = .30). Twenty-two of the 54 publications (40.7%) reported on study populations or study sites within the United States while 3 were from Canada. Three studies were from Asia (2 Japan, 1 China), and 1 study was from South America (Brazil). The remaining studies were from the United Kingdom, Europe, or Australia. The 3 studies from Asia had relatively high rates of IUFD that ranged from 8.33–15.38 per 100 births. These studies also had study years beginning in the 1980s; therefore, rates may reflect the practices of that region and time. The prevalence of IUFD across the publication years was quite variable, with a range from 0 (2000 and 2004) to 13.8 per 100 births (2010). The highest rates occurred in 1986 (13.3 per 100 births), 1990 (13.4 per 100 births), and 2010. No significant trends were seen among other years (P = .8, with the use of a simple regression model).
      Thirty-five articles described gestational age at the time of IUFD, which totaled 37% (n = 66) of all identified IUFDs. Fourteen of 66 IUFDs (21%) occurred at ≥36 weeks' gestation. Figure 3 shows the prevalence of IUFD at each gestational age and cumulative prevalence of IUFD across each gestational age. Nineteen percent of IUFDs occurred at ≤30 weeks' gestation. The pooled prevalence of IUFD that occurred at ≥36 weeks' gestation was 1.28 per 100 births (95% CI, 0.72–2.26). The weekly prevalence of IUFD did not appear to increase at >35 weeks' gestation. The difference between this graph of crude prevalence estimates and the pooled prevalence estimates for gestational age of ≥36 weeks is that the metaanalysis included all IUFDs that occurred at ≥36 weeks, although the graph only includes IUFDs up to 38 weeks' gestation. In addition, the metaanalysis weights the prevalence calculations based on sample size of the studies, which can also add to the differences in the 2 point estimates.
      Figure thumbnail gr3
      Figure 3Prevalence of intrauterine fetal death by gestational age
      Cumulative and weekly prevalence of intrauterine fetal death per 100 pregnancies. Blue lines indicate weekly prevalence of intrauterine fetal death; red lines indicate cumulative prevalence of intrauterine fetal death.
      South. Risk of IUFD in gastroschisis. Am J Obstet Gynecol 2013.
      Thirty-seven studies reported a mean/median gestational age for live births. The proportion of deliveries that occurred at 37 weeks' gestation was no different between the 90s and 2000s (2 decades, 14% and 15.8%, respectively). The proportions that occurred at 36 weeks' gestation were 50% and 37%, respectively. The proportions that occurred at 35 weeks were 21.4% and 42%, respectively. This temporal pattern did not vary significantly when alternative grouping strategies were used.
      Twenty-eight studies reported at least 1 termination of pregnancy. There was no difference in the prevalence of IUFD among studies that reported a termination of pregnancy and studies that had none or were not reported (P = .63). The pooled prevalence of IUFD among studies with elective termination was 4.21 (95% CI, 2.93–6.03), compared with 4.77 (95% CI, 3.32–6.81) among studies without a case of elective termination.
      The 12 studies in which there were no reported fetal death included a total of 369 cases. These studies, which represent 11% of the total number of cases that were included in the metaanalysis, appeared to have a slightly lower gestational age at delivery (35.1 ± 0.99 weeks), compared with studies that reported at least 1 IUFD (35.9 ± 0.70 weeks; P = .01). We were unable to identify a pattern of differences in management or study methods between those studies with and those without reported IUFDs in terms of quality score, geographic location, or reporting of an obstetric delivery plan.

      Sensitivity analysis

      A pooled prevalence was calculated that included only those studies (n = 35) that reported a gestational age at the time of the IUFD. Among the 35 articles, there were 1483 infants (births + IUFDs) and 60 IUFDs. The pooled prevalence among these studies was 3.80 (95% CI, 2.68–5.35), which is consistent with findings of all included studies. When we restricted the analysis only to the 26 studies that had a quality grade of 4 or 5 (n = 1411 IUFD + live births), the pooled prevalence was 5.6 per 100 births (95% CI, 4.01–7.89). Among the 14 studies with lowest quality grades of 1 or 2, the pooled prevalence rate was 4.49 (95% CI, 2.81–7.08; Table 2). None of the 5 quality assessment variables were related independently to risk for IUFD.

      Heterogeneity

      We detected moderate heterogeneity across studies (I2 = 63%), which indicated moderate between-studies variability. This likely is due to differences in the definition of IUFD (gestational age cutoff for spontaneous abortion vs IUFD) and practice variability in the management of gastroschisis pregnancies. Because 12 studies reported no cases of IUFD, these 12 studies were not included in the initial assessment of heterogeneity (they provided no estimates of variances for prevalence rates). To estimate their contribution if they had reported IUFDs, we assumed 1 case occurred in each study and then recalculated the I2, which decreased slightly from 63% to 56%. We investigated each study's individual contribution to the heterogeneity by removing each study individually from the analysis and recalculating the pooled results, which included the assessment of the 12 studies that had the largest sample sizes (n > 100). Results indicated that the article by Calzolari et al
      • Calzolari E.
      • Bianchi F.
      • Dolk H.
      • Milan M.
      Omphalocele and gastroschisis in Europe: a survey of 3 million births 1980-1990. EUROCAT Working Group.
      (prevalence, 14.6 per 100 births; 95% CI, 10.78–19.16) contributed the most to the I2 (pooled prevalence without the study of Calzolari et al, 4.47; 95% CI, 3.46–5.76; I2 = 55%]. Skarsgard et al
      • Skarsgard E.D.
      • Claydon J.
      • Bouchard S.
      • et al.
      Canadian Pediatric Surgical Network: a population-based pediatric surgery network and database for analyzing surgical birth defects: the first 100 cases of gastroschisis.
      also contributed significantly to the heterogeneity (prevalence, 0.94 per 100 births; 95% CI, 0.05–4.56; pooled prevalence without Skarsgard, 4.40; 95% CI, 3.40–5.67; I2 = 43%]. The removal of both of these studies decreased the I2 to 46%.

      Comment

      The optimal timing for delivery of infants with gastroschisis is unknown, because there are both risks and benefits associated with elective delivery before term. The possibility of fetal death is a major factor in the determination of appropriate obstetric management. The identification of an accurate risk profile for IUFD is essential for clinicians to assess risks and benefits appropriately and therefore develop an obstetrics management plan.
      In the general population, late preterm delivery (34-36 weeks' gestation) is associated with increased morbidity and mortality rates. Among a cohort of infants without congenital anomalies, Young et al
      • Young P.C.
      • Glasgow T.S.
      • Li X.
      • Guest-Warnick G.
      • Stoddard G.
      Mortality of late-preterm (near-term) newborns in Utah.
      showed decreasing mortality rates at 34, 35, and 36 weeks' gestation, compared with term infants (risk ratio, 10.5, 7.2, and 5.3, respectively). Neonatal intensive care unit admissions for respiratory issues were also more common among infants who were born late preterm.
      • Ramachandrappa A.
      • Jain L.
      Health issues of the late preterm infant.
      Longer-term complications have also been described. Late preterm infants were found to have increased intensive care admissions because of respiratory syncytial virus, with increased length of hospitalization, compared with term infants.
      • Kotecha S.J.
      • Dunstan F.D.
      • Kotecha S.
      Long term respiratory outcomes of late preterm-born infants.
      In addition, late preterm birth has been associated with cerebral palsy, cognitive and developmental delay, and behavioral problems.
      • Boyle J.D.
      • Boyle E.M.
      Born just a few weeks early: does it matter?.
      Because of these apparent risks that are associated with early delivery, the March of Dimes is leading an effort to reset the obstetric paradigm by advocating a decrease in the number of normal pregnancies electively delivered at <39 weeks' gestation.
      • Howse J.L.
      • Katz M.
      Conquering prematurity.
      The published literature on long-term developmental outcomes that are associated with gastroschisis is sparse, which leaves us with little data regarding the effect of gestational age on these outcomes. Although children with gastroschisis have been reported to have both normal
      • Boyd P.A.
      • Bhattacharjee A.
      • Gould S.
      • Manning N.
      • Chamberlain P.
      Outcome of prenatally diagnosed anterior abdominal wall defects.
      and delayed development,
      • Berseth C.L.
      • Malachowski N.
      • Cohn R.B.
      • Sunshine P.
      Longitudinal growth and late morbidity of survivors of gastroschisis and omphalocele.
      studies have been limited by small sample sizes, noncontemporary cohorts, and a lack of formal developmental testing. The most detailed contemporary formal developmental data suggests that preterm birth in infants with gastroschisis may influence both cognitive and motor development.
      • South A.P.
      • Marshall D.D.
      • Bose C.L.
      • Laughon M.M.
      Growth and neurodevelopment at 16 to 24 months of age for infants born with gastroschisis.
      Given the lack of definitive data, in addition to the lack of a compelling hypothesis that would suggest otherwise, we speculate that infants with gastroschisis who are born prematurely experience equal or worse outcomes, compared with preterm infants without this congenital anomaly. Thus, there is potential for benefit in delaying delivery in pregnancies that are affected by gastroschisis.
      The developmental benefits of delaying delivery must be balanced with all other known risks and benefits. Some clinicians theorize that prolonged exposure to amniotic fluid increases bowel damage and dysmotility and therefore advocate for routine early delivery in pregnancies that are complicated by gastroschisis. One small cohort study showed decreased time to the initiation of feeding and decreased length of stay with planned cesarean section delivery at 34 weeks' gestation.
      • Serra A.
      • Fitze G.
      • Kamin G.
      • Dinger J.
      • König I.R.
      • Roesner D.
      Preliminary report on elective preterm delivery at 34 weeks and primary abdominal closure for the management of gastroschisis.
      However, other retrospective studies report worse outcomes that are related to preterm delivery of neonates with gastroschisis, compared with term delivery. Boutros et al
      • Boutros J.
      • Regier M.
      • Skarsgard E.D.
      Is timing everything? The influence of gestational age, birth weight, route, and intent of delivery on outcome in gastroschisis.
      described an inverse relationship between gestational age and ventilator days, time on parenteral nutrition, and length of stay. An additional small randomized controlled trial showed no difference in outcomes between elective delivery at 36 weeks' gestation compared with spontaneous labor
      • Logghe H.L.
      • Mason G.C.
      • Thornton J.G.
      • Stringer M.D.
      A randomized controlled trial of elective preterm delivery of fetuses with gastroschisis.
      ; however, the sample size may not have been sufficient to detect a difference because many pregnancies with gastroschisis will deliver spontaneously before term.
      Results of this metaanalysis suggest a pooled prevalence of IUFD with gastroschisis of 4.48 per 100 births, which is much lower than previously cited but higher than the general population. The prevalence of IUFD did not increase during late gestation. The overall risk of IUFD is greatest at <36 weeks' gestation, which is earlier than many obstetricians would consider routine elective delivery. It appears that, once a fetus has completed 35 weeks' gestation, it already has assumed most of the risk of IUFD; therefore, fetal death should not weigh as heavily in the decision electively deliver early. However, we must point out that the methods used to generate our estimates of IUFD assume the denominator to be constant. Because of the high rate of early deliveries, this assumption limits our ability to calculate prospectively the risk for fetal death at advanced gestational ages. Furthermore, data regarding additional anomalies and comorbidities were provided only rarely in the reviewed articles. Therefore, we were unable to control for other extraneous factors that may have led to fetal death, such as abnormal karyotype, additional congenital anomalies, or other related factors such as intestinal dilation.
      Our objective in evaluating the presence of a delivery plan was to determine whether having a clearly stated delivery process decreased the likelihood of death. We did not intend to evaluate the merits of any individual plan. The reported delivery plans differed greatly in both the antenatal monitoring and proposed goal for gestational age at delivery. Our results suggest that having a delivery plan (1) does not alter the rate of IUFD and (2) does not change the gestational age at delivery. The reason the delivery plan may not influence outcomes is that either the delivery plan is not adhered to or the studies in which no delivery plan is reported have a practice of early, elective delivery. We suspect that both of these possibilities contributed to our observations. Additional study of antenatal risk factors and comprehensive delivery plans may allow for individualized approaches to planning the timing of delivery. Identification of those pregnancies that would benefit from early delivery would optimize outcomes without compromising those who would not benefit.
      We believe that multiple factors influence caregiver decisions regarding the timing of nonspontaneous deliveries that are affected by gastroschisis. The risk of ongoing visceral injury is a prominent concern. However, in the absence of specific compromise of bowel integrity (ie, dilation), there is not consistent evidence in the literature that supports the practice of routine early delivery to improve gut-related outcomes. In our experience, the risk for fetal death is the primary driver of early elective delivery. Misrepresentation of risk in the literature and anecdotal evidence play key roles in perpetuating this practice.
      Our study also suggests that the gestational age at delivery for pregnancies that are affected by gastroschisis is decreasing over time. We speculate that, as prenatal diagnosis has become more common, the opportunity for obstetric intervention in the timing of delivery has increased. This likely has led to either an increase in elective early deliveries or an increase in indicated early deliveries. The role of each is impossible to determine based on the current literature. The causal relationship between earlier delivery and fetal or postnatal death is not clear. The role of fetal monitoring in the prevention of IUFD in gastroschisis is not well established. Most accounts of antenatal management in the published literature describe the inclusion of increased antenatal monitoring, which includes increased frequency of ultrasound scanning, tococardiography, and other measures of fetal well-being. Despite this medical practice, there is little evidence to suggest that antenatal monitoring improves survival or other neonatal outcomes in this population.
      • Salomon L.J.
      • Mahieu-Caputo D.
      • Jouvet P.
      • et al.
      Fetal home monitoring for the prenatal management of gastroschisis.
      • Overton T.G.
      • Pierce M.R.
      • Gao H.
      • et al.
      Antenatal management and outcomes of gastroschisis in the U.K.
      This may be because fetal death in gastroschisis is an acute event without preceding indicators.
      Our study has certain limitations. First, our results may be influenced by early elective delivery that eliminated potential IUFDs. When we compared studies with and without an early elective delivery plan, we found no significant difference in outcomes of IUFD. However, this finding may be the result of improved prenatal monitoring practices. The use of ultrasound scanning and biophysical profiles to assess for the compromised fetus and the increased awareness of IUFD may contribute to overall fetal survival. Second, although the risk for IUFD has decreased, the postnatal mortality rate may have increased. We found a pooled prevalence of postnatal survival of 95%. These results are similar to those published by Vachharajani et al,
      • Vachharajani A.J.
      • Dillon P.A.
      • Mathur A.M.
      Outcomes in neonatal gastroschisis: an institutional experience.
      who reported a postnatal survival of approximately 90%. These improvements in postnatal survival most likely are related to the advances in total parental nutrition, surgical care, antibiotics, and tertiary neonatal intensive care units. Finally, our results may be influenced by ascertainment or referral bias. If referral bias were to be present, by concentrating the most severely affected pregnancies in tertiary care centers, our outcomes should be biased to overestimate the rate of IUFD. We attempted to limit this bias by including larger, population-based published cohorts. We cannot, however, account for gastroschisis cases that were not diagnosed before delivery.
      This metaanalysis seeks to provide more evidence to consider in decision-making for the timing of the delivery in gastroschisis. Normal neonates without congenital defects are at a higher risk of morbidity and death when they are delivered prematurely, which has resulted in a trend in the United States to delay the timing of elective deliveries to >39 weeks' gestation. The risk of IUFD in gastroschisis is lower than is cited commonly; however, the implications of even a single potentially preventable death are significant. Given the small incremental increase in risk for IUFD with advancing gestational age, we advocate for strategies to delay elective delivery before term in the stable patient with gastroschisis. Elective delivery at >36 completed weeks' gestation may be an appropriate balance of risks and benefits. Given the lack of data regarding fetal death in the setting of in utero growth restriction or bowel dilation, we cannot advocate for changes in current management strategies. Although there is no strong evidence that antenatal fetal monitoring prevents IUFD in gastroschisis,
      • Salomon L.J.
      • Mahieu-Caputo D.
      • Jouvet P.
      • et al.
      Fetal home monitoring for the prenatal management of gastroschisis.
      • Overton T.G.
      • Pierce M.R.
      • Gao H.
      • et al.
      Antenatal management and outcomes of gastroschisis in the U.K.
      there may be a benefit to increased monitoring at ≥36 weeks' gestation, with a plan to deliver at 37 weeks' gestation. Antenatal markers that include cytokine profiles, oligohydramnios, and bowel dilation have been evaluated yet have not been shown to be predictive of outcomes in gastroschisis.
      • Luton D.
      • De Lagausie P.
      • Guibourdenche J.
      • et al.
      Prognostic factors of prenatally diagnosed gastroschisis.
      Throughout pregnancy, the pooled prevalence of IUFD in gastroschisis is 7-fold higher (4.48%) than that of the general population (0.62%). Furthermore, at >36 weeks' gestation, our data suggest that the risk for IUFD is still significantly higher than the general obstetric population, thus making the question of antenatal monitoring pertinent. The current paucity of data does not allow for early identification of individual infants who are likely to experience bad outcomes. Despite this, ultrasound findings that are consistent with increasing intraabdominal size or dilation may warrant earlier delivery because of risks of postnatal morbidity. Large, prospective, multicenter evaluations of prenatal risk factors for IUFD are needed, along with randomized trials that are designed to determine optimal timing of delivery in pregnancies that are affected by IUFD.

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