Metaanalysis of the prevalence of intrauterine fetal death in gastroschisis

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OBSTETRICS

Metaanalysis of the prevalence of intrauterine fetal death in gastroschisis Andrew P. South, MD, MPH; Kevin M. Stutey, MD; Jareen Meinzen-Derr, PhD, MPH 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.

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.

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.

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.

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

Key words: abdominal wall defect, fetal death, gastroschisis, IUFD, stillbirth

Cite this article as: South AP, Stutey KM, Meinzen-Derr J. Metaanalysis of the prevalence of intrauterine fetal death in gastroschisis. Am J Obstet Gynecol 2013;209:114.e1-13.

G

astroschisis is an abdominal wall defect of unclear cause and increasing incidence worldwide; current estimates are near 5 per 10,000 births.1 There have been great improvements in survival in this patient population

From the Divisions of Neonatology (Drs South and Stutey) and Biostatistics and Epidemiology (Dr Meinzen-Derr), Department of Pediatrics, Cincinnati Children’s Hospital Medical Center, University of Cincinnati College of Medicine, Cincinnati, OH. Received Jan. 30, 2013; revised April 2, 2013; accepted April 24, 2013. This study was supported by the Perinatal Institute at Cincinnati Children’s Hospital Medical Center, Cincinnati, OH. The authors report no conflict of interest. Presented at the annual meeting of the Pediatric Academic Societies, Boston, MA, April 28-May 1, 2012. Reprints: Andrew P. South, MD, MPH, 3333 Burnet Ave., Cincinnati, OH 45229. [email protected]. 0002-9378/free ª 2013 Mosby, Inc. All rights reserved. http://dx.doi.org/10.1016/j.ajog.2013.04.032

For Editors’ Commentary, see Contents

because >95% of infants survive from birth to initial hospital discharge.2 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,3 which is much higher than the 0.6% baseline rate in the general population.4,5 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.6 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,7 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.8 Although some clinicians advocate for early delivery to improve

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postnatal clinical outcomes (such as earlier initiation of enteral feeds and shorter hospitalization time), the literature does not document a consistent benefit.9-11 Therefore, the primary rationale for elective delivery before the onset of labor may be the prevention of IUFD.12 The reported incidence of IUFD in pregnancies that are affected by gastroschisis is as high as 12.5%.13 Although the cause for the increased risk of IUFD is unknown, hypotheses include umbilical cord compression after acute intestinal dilation,14 oligohydramnios,15 cardiovascular compromise that is related to high protein loss through the defect and subsequent hypovolemia,16 and cytokine-mediated inflammation.17,18 Additionally, there is increased risk for volvulus and vascular compromise that could lead to fetal death.19 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

Obstetrics

www.AJOG.org 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.

M ATERIALS

AND

M ETHODS

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.20 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 (populationbased 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

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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.21 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.22 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 betweenstudy heterogeneity.23,24 An I2 value of >75% is interpreted as high heterogeneity.24 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.

R ESULTS Study and patient characteristics Our search produced 1123 results. Review of these abstracts resulted in 100

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Obstetrics

articles for further review (Figure 1). Six articles25-30 were excluded because of use of overlapping datasets with articles that were included in the analysis.13,31-34 Three articles were removed for having <10 subjects.35-37 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,16 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. 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, 18e41 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, 34e37 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).

Metaanalysis The pooled prevalence of IUFD for all studies was 4.48 per 100 gastroschisis pregnancies (live births þ IUFD; 95% confidence interval [CI], 3.48e5.76). There was no significant difference in IUFD rate between centers with and without an early delivery plan in place (prevalence, 4.09; 95% CI, 2.39e6.91 vs 4.64; 95% CI, 3.47e6.17 per 100 births,

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FIGURE 1

Process 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.

respectively; P ¼ .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 ¼ .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, 2.26e5.84 vs 4.89; 95% CI, 3.63e6.56; P ¼ .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 8.33e15.38 per 100 births. These studies also had study years beginning in the 1980s; therefore, rates may reflect the practices of that region and time.

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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 ¼ .8, with the use of a simple regression model). Thirty-five articles described gestational age at the time of IUFD, which totaled 37% (n ¼ 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, 0.72e2.26). The weekly prevalence of IUFD did not appear to increase at >35 weeks’ gestation. The difference between this graph of crude

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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 ¼.63). The pooled prevalence of IUFD among studies with elective termination was 4.21 (95% CI, 2.93e6.03), compared with 4.77 (95% CI, 3.32e6.81) 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 ¼ .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.

FIGURE 2

Forest plot shows odds ratios (random effect model)

South. Risk of IUFD in gastroschisis. Am J Obstet Gynecol 2013.

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

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add to the differences in the 2 point estimates. 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

Sensitivity analysis A pooled prevalence was calculated that included only those studies (n ¼ 35) that reported a gestational age at the time of the IUFD. Among the 35 articles, there were 1483 infants (births þ IUFDs) and 60 IUFDs. The pooled prevalence among these studies was 3.80 (95% CI, 2.68e5.35), 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 ¼ 1411 IUFD þ live births), the pooled prevalence was 5.6 per 100 births (95% CI, 4.01e7.89). Among the 14 studies with lowest quality grades of 1 or 2, the pooled prevalence rate was 4.49 (95% CI, 2.81e7.08; Table 2). None of the 5 quality assessment variables were related independently to risk for IUFD.

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Characteristics of the studies that were included in the systematic review Intrauterine Total, Spontaneous Termination of fetal death, n abortion, n pregnancy, n n/N (%)

Gestational age at birth, wk D d

Gestational age Quality of intrauterine assessment fetal death, wk score

Abuhamad et al, 199754

VA

PR

NR

17

NR

0

1/17 (6)

No standard delivery plan

35.8a  2.74

28

4

Adair et al, 199655

NC

RR

1985-1994

29

NR

0

4/29 (13.8)

No standard delivery plan

NR

28-41

2

Adra et al, 199656

FL

RR

1986-1994

47

NR

3

2/44 (4.5)

No standard delivery plan

36.0a  2.4

28, 36

4

Ajayi et al, 201157

OH

RR

2000-2008

74

NR

0

0/74

Elective delivery at 36-37 wks’ gestation

35.2b (26.3e38.1)

N/A

3

Alfaraj et al, 201158

Canada

RR

2001-2010

98

NR

0

1/98 (1.0)

NR

NR

NR

2

Alsulyman et al, 199659

LA

RR

1988-1995

23

NR

1

0/22

NR

34.3a  6.3

N/A

4

Axt et al, 199960

Germany

RR

1989-1997

18

NR

3

0/15

NR

36.1a  3.1

N/A

4

Badillo et al, 200861

PA

RR

2000-2007

64

NR

1

2/63 (3.2)

NR

NR

NR

2

Barisic et al, 200162

11 European RR nations

1996-1998

106

NR

31

13/75 (17.3)

NR

36.3a  2.2

NR

3

Bond et al, 198833

CA

RR

1982-1986

15

NR

3

0/11

NR

NR

N/A

2

Boyd et al, 199845

UK

RR

1985-1995

41

NR

7

0/34

NR

37c

N/A

3

Brantberg et al, 200463

Norway

PR

1988-2002

64

NR

3

1/61 (1.6)

C/S at 37-39 wks’ gestation

36 þ 1 (28e39)b

35 þ 5

5

Bugge and Holm, 200234

Denmark

RR

1970-1989

166

NR

NR

9/166 (3.3)

NR

NR

NR

2

Burge and Ade-Ajayi, 199712

UK

RR

1982-1995

57

NR

0

3/54 (5.6)

Spontaneous labor

36a

32, 36, 39

4

Calzolari et al, 199538

Italy

PR

1980-1990

274

NR

NR

NR

20-27 (n = 18) NR (n = 22)

3

South. Risk of IUFD in gastroschisis. Am J Obstet Gynecol 2013.

Delivery plan

40/274 (14.6) NR

(continued)

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Study

Study Study design years

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TABLE 1

Characteristics of the studies that were included in the systematic review (continued) Intrauterine Total, Spontaneous Termination of fetal death, n abortion, n pregnancy, n n/N (%)

Delivery plan

Gestational age at birth, wk D d

Gestational age Quality of intrauterine assessment fetal death, wk score

Chen et al, 199664

China

RR

1/1987-9/1994

15

NR

2

2/13 (15.4)

NR

NR

NR

2

Chescheir et al, 199165

NC

RR

1986-1990

19

NR

0

1/19 (5.3)

NR

NR

28

3

Cohen-Overbeek The RR et al, 200866 Netherlands

1/1991-6/2003

33

NR

2

3/31 (9.7)

Induction at 37 wks’ gestation

NR

19, 33, 36

3

Crawford et al, 199213

UK

RR

1986-1991

26

NR

2

3/24 (12.5)

No standard delivery plan

NR

34, 35, 37

4

Dillon and Renwick, 199567

UK

PR

1988-1992

56

3

2

3/51 (5.9)

No standard delivery plan

NR

32, 32, 37

4

Durfee et al, 200268

MA

RR

4/1990-12/2000

26

NR

2

0/24

NR

NR

N/A

2

Eurenius and Axelsson, 199469

Sweden

RR

1983-1990

24

NR

4

1/20 (5.0)

NR

NR

NR

2

Feldkamp et al, 200870

UT

PR

1/1997-12/2005 189

NR

3

11/186 (5.9)

NR

NR

NR

2

Fillingham and Rankin, 200871

UK

RR

1/97-12/06

143

NR

3

2/140 (1.4)

NR

NR

NR

2

Fitzsimmons et al, 198872

WA

RR

1/1980-12/1986

15

NR

0

1/15 (6.7)

C/S at 36 wks’ gestation

35.9b (31e37)

41

3

Forrester and Merz, 199973

HI

RR

1986-1997

74

NR

6

7/68 (10.3)

NR

NR

NR

1

Fratelli et al, 200732

UK

RR

1/1997-4/2006

40

NR

2

2/38 (5.3)

Induction at 38-39 wks’ gestation

37 þ 1 (36 þ 0 to 38 þ 1)c

18, 22

4

Garcia et al, 201074

Brazil

RR

1/1997-8/2009

94

NR

NR

5/94 (5.3)

Elective C/S at 37 wks’ gestation

36.5  1.4a

32, 34, 35, 36, 37

4

Garne et al, 200711

Denmark and UK

RR

1997-2002

216

NR

39

9/177 (5.1)

NR

36c

NR

3

Goldkrand et al, 200475

GA

RR

1/1994-9/2002

34

NR

NR

2/34 (5.8)

Planned delivery at >37 wks’ gestation

NR

32.7, 36

3

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(continued)

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Study Study design years

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TABLE 1

Characteristics of the studies that were included in the systematic review (continued) Intrauterine Total, Spontaneous Termination of fetal death, n abortion, n pregnancy, n n/N (%)

Gestational age at birth, wk D d

Gestational age Quality of intrauterine assessment fetal death, wk score

Heinig et al, 200876

Germany

RR

10/2001-9/2005

14

NR

NR

2/14 (14.3)

C/S at 37-39 wks’ gestation

33 þ 6 to 36 þ 6

33 þ 6, 35 þ 3 4

Hidaka et al, 200977

Japan

RR

1990-2006

11

NR

NR

1/11 (9.1)

C/S at 37-38 wks’ gestation

NR

35

4

Horton et al, 201078

NC

RR

1/2000- 1/2907

71

NR

NR

2/71 (2.8)

Spontaneous labor

35 þ 4  2.4a

27, 33

4

Huang et al, 200279

RI

RR

1991-2001

60

NR

NR

3/60 (5.0)

NR

NR

NR

1

Japaraj et al, 200380

Australia

RR

1/1993-5/2001

45

NR

NR

0/45

NR

35.6b (24e39)

N/A

3

Kamata et al, 199681

Japan

RR

1982-1994

12

NR

NR

1/12 (8.3)

Spontaneous labor

35.4a  3.7

31

4

Lafferty et al, 198982

UK

RR

1981-1986

27

NR

4

1/23 (4.3)

Spontaneous labor

37.2b (33.5e40.0)

37

3

Lausman et al, 20077

Canada

RR

1/1980- 12/2001 158

1

3

2/154 (1.3)

Eighty-six women 36.6  2a had spontaneous labor; 66 women had planned delivery

24, 35

4

Logghe et al, 200550

UK

RCT

5/1995- 9/1999

42

NR

NR

1/42 (2.4)

Two groups of 21 women randomly assigned to induction at 36 wks’ gestation or spontaneous delivery

31

5

Mears et al, 201083

UK

RR

2004-2008

60

NR

0

3/60 (5.0)

Induction at 37 wks’ 36a gestation

NR

3

Moir et al, 200484

MN

PR

NR

27

NR

0

0/27

Deliver 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 matting

Delivery plan: 34.2  2.4a; controlled trial: 37.7  1.8a

N/A

5

Morrow et al, 199385

Scotland

RR

1983-1989

47

6

11

2/30 (6.7)

NR

36b (31e38)

>28 (n = 2)

2

South. Risk of IUFD in gastroschisis. Am J Obstet Gynecol 2013.

Delivery plan

Induction: 35.8  0.7a; spontaneous: 36.7  1.5a

(continued)

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TABLE 1

Characteristics of the studies that were included in the systematic review (continued) Intrauterine Total, Spontaneous Termination of fetal death, n abortion, n pregnancy, n n/N (%)

Delivery plan

Gestational age at birth, wk D d

Gestational age Quality of intrauterine assessment fetal death, wk score

Nicholas et al, 200986

WA

RR

1991-2006

80

NR

4

2/76 (2.6)

Spontaneous labor

NR

NR

2

Rankin et al, 199987

UK

RR

1986-1996

126

NR

12

4/108 (3.7)

NR

NR

NR

3

Reid et al, 200331

Australia

PR

1980-2001

122

NR

NR

12/122 (9.8)

Elective delivery 37c (24e41) at 38 wks’ gestation

34c (24e39)

5

Reigstad et al, 201188

Norway

RR

1993-2008

36

NR

0

6/36 (17)

Two groups: (1) Group 1: 36.5 spontaneous labor (34e40)c; group 2: (n = 10); (2) 35.0 (34e37)c elective C/S at 36-37 wks’ gestation (n = 20)

<20 (n = 3) 28, 29, 39

4

Rinehart et al, 199989

MS

RR

9/1992-6/1998

33

NR

1

0/32

NR

Outside center: N/A 35.3  2.2a; tertiary center: 35.6  1.4a

3

Salomon et al, 200451

France

PR

3/1998-7/2001

31

NR

1/31 (3.2)

NR

Low risk (n ¼ 20 NR women): 35.5 (32e38)c; high risk (n ¼ 11 women: 34.5 (32e36)c

3

Santiago-Munoz US et al, 200790

RR

1/1998-6/2006

66

NR

3/66 (4.5)

Spontaneous labor

37.1  1.9a

33, 38, 40

4

Serra et al, 200848

Germany

RR

1999-2004

23

NR

0/23

Two groups: (1) C/S at 34 wks’ gestation; (2) spontaneous labor

Group 1: 243 (226e264) daysc; group 2: 257 (235e282) daysc

N/A

4

Sipes et al, 199091

IA, WI

RR

12/1979-1/1989

33

NR

0/32

Spontaneous labor

36.3  2.4a

N/A

3

Skarsgard et al, 200839

Canada

RR

2005-2006

114

NR

1/107 (0.9)

NR

35.9  2.3a

NR

2

Towers and Carr, 200892

US

RR

1/1986-12/2003

85

NR

0

2/84 (2.4)

Spontaneous labor

NR

29 þ 4, 31 þ 3

4

Vegunta et al, 200593

IL

RR

6/1998-8/2002

30

NR

0

0/30

C/S 36-38 wks’ gestation

35.7 (28.4e38.6)c

N/A

3

0

1 3 (4 lost to follow up)

C/S, cesarean section delivery; N/A, not applicable; NR, not reported; PR, prospective observational review; RCT, randomized controlled trial; RR, retrospective review.

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a

Data were reported as mean  SD; b Data were reported as mean (range); c Data were reported as median (range).

South. Risk of IUFD in gastroschisis. Am J Obstet Gynecol 2013.

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Origin

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Study

Study Study design years

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Heterogeneity We detected moderate heterogeneity across studies (I2 ¼ 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 al38 (prevalence, 14.6 per 100 births; 95% CI, 10.78e19.16) contributed the most to the I2 (pooled prevalence without the study of Calzolari et al, 4.47; 95% CI, 3.46e5.76; I2 ¼ 55%]. Skarsgard et al39 also contributed significantly to the heterogeneity (prevalence, 0.94 per 100 births; 95% CI, 0.05e4.56; pooled prevalence without Skarsgard, 4.40; 95% CI, 3.40e5.67; I2 ¼ 43%]. The removal of both of these studies decreased the I2 to 46%.

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TABLE 2

Pooled prevalence of intrauterine fetal death by graded quality of study Grade

Studies, n

Pregnancies, n

Pooled prevalence per 100 births

95% CI

1, 2

14

1262

4.49

2.81e7.08

3

14

603

2.50

1.29e4.78

4, 5

26

1411

5.65

4.01e7.89

CI, confidence interval. South. Risk of IUFD in gastroschisis. Am J Obstet Gynecol 2013.

infants without congenital anomalies, Young et al40 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.41 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.42 In

addition, late preterm birth has been associated with cerebral palsy, cognitive and developmental delay, and behavioral problems.43 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.44 The published literature on longterm developmental outcomes that are associated with gastroschisis is sparse, which leaves us with little data regarding the effect of gestational age on

FIGURE 3

Prevalence of intrauterine fetal death by gestational age

C OMMENT 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

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.

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www.AJOG.org these outcomes. Although children with gastroschisis have been reported to have both normal45 and delayed development,46 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.47 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.48 However, other retrospective studies report worse outcomes that are related to preterm delivery of neonates with gastroschisis, compared with term delivery. Boutros et al49 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 labor50; 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

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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.51,52 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

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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,53 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 decisionmaking 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,51,52 there may be a benefit to increased monitoring at
36 weeks’

www.AJOG.org 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.17 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. REFERENCES 1. Castilla EE, Mastroiacovo P, Orioli IM. Gastroschisis: international epidemiology and public health perspectives. Am J Med Genet 2008;148C:162-79. 2. Bradnock TJ, Marven S, Owen A, et al. Gastroschisis: one year outcomes from national cohort study. BMJ 2011;343:d6749. 3. Dolk H, Loane M, Garne E. The prevalence of congenital anomalies in Europe. Adv Exp Med Biol 2010;686:349-64. 4. MacDorman MF, Kirmeyer S. Fetal and perinatal mortality, United States, 2005. Natl Vital Stat Rep 2009;57:1-19. 5. 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. 6. Craigo SD. Indicated preterm birth for fetal anomalies. Semin Perinatol 2011;35:270-6. 7. Lausman AY, Langer JC, Tai M, et al. Gastroschisis: what is the average gestational age of spontaneous delivery? J Pediatr Surg 2007;42: 1816-21. 8. Barseghyan K, Aghajanian P, Miller DA. The prevalence of preterm births in pregnancies complicated with fetal gastroschisis. Archives of gynecology and obstetrics 2012;286(4):889-92. 9. Simmons M, Georgeson KE. The effect of gestational age at birth on morbidity in patients

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www.AJOG.org Benefits of term delivery in infants with antenatally diagnosed gastroschisis. Obstet Gynecol 2002;100:695-9. 80. Japaraj RP, Hockey R, Chan FY. Gastroschisis: can prenatal sonography predict neonatal outcome? Ultrasound Obstet Gynecol 2003;21:329-33. 81. Kamata S, Ishikawa S, Usui N, et al. Prenatal diagnosis of abdominal wall defects and their prognosis. J Pediatr Surg 1996;31:267-71. 82. Lafferty PM, Emmerson AJ, Fleming PJ, Frank JD, Noblett HR. Anterior abdominal wall defects. Arch Dis Child 1989;64:1029-31. 83. Mears AL, Sadiq JM, Impey L, Lakhoo K. Antenatal bowel dilatation in gastroschisis: a bad sign? Pediatr Surg Int 2010;26:581-8. 84. Moir CR, Ramsey PS, Ogburn PL, Johnson RV, Ramin KD. A prospective trial of elective preterm delivery for fetal gastroschisis. Am J Perinatol 2004;1:289-94. 85. Morrow RJ, Whittle MJ, McNay MB, Raine PA, Gibson AA, Crossley J. Prenatal diagnosis and management of anterior abdominal wall defects in the west of Scotland. Prenatal Diagn 1993;13:111-5. 86. Nicholas SS, Stamilio DM, Dicke JM, Gray DL, Macones GA, Odibo AO. Predicting adverse neonatal outcomes in fetuses with abdominal wall defects using prenatal risk factors. Am J Obstet Gynecol 2009;201:383.e1-6.

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87. Rankin J, Dillon E, Wright C. Congenital anterior abdominal wall defects in the north of England, 1986-1996: occurrence and outcome. Prenatal Diagn 1999;19:662-8. 88. Reigstad I, Reigstad H, Kiserud T, Berstad T. Preterm elective caesarean section and early enteral feeding in gastroschisis. Acta Paediatr 2011;100:71-4. 89. Rinehart BK, Terrone DA, Isler CM, Larmon JE, Perry KG Jr, Roberts WE. Modern obstetric management and outcome of infants with gastroschisis. Obstet Gynecol 1999;94: 112-6. PC, McIntire DD, 90. Santiago-Munoz Barber RG, Megison SM, Twickler DM, Dashe JS. Outcomes of pregnancies with fetal gastroschisis. Obstet Gynecol 2007;110:663-8. 91. Sipes SL, Weiner CP, Sipes DR 2nd, Grant SS, Williamson RA. Gastroschisis and omphalocele: does either antenatal diagnosis or route of delivery make a difference in perinatal outcome? Obstet Gynecol 1990;76:195-9. 92. Towers CV, Carr MH. Antenatal fetal surveillance in pregnancies complicated by fetal gastroschisis. Am J Obstet Gynecol 2008;198: 686.e1-5. 93. Vegunta RK, Wallace LJ, Leonardi MR, et al. Perinatal management of gastroschisis: analysis of a newly established clinical pathway. J Pediatr Surg 2005;40:528-34.