1. E-Mail karger@karger.com
Original Paper
Fetal Diagn Ther
DOI: 10.1159/000365353
Fetal Myelomeningocele Repair:
The Post-MOMS Experience at the
Children’s Hospital of Philadelphia
Julie S. Moldenhauer Shelly Soni Natalie E. Rintoul Susan S. Spinner
Nahla Khalek Juan Martinez-Poyer Alan W. Flake Holly L. Hedrick
William H. Peranteau Norma Rendon Jamie Koh Lori J. Howell
Gregory G. Heuer Leslie N. Sutton Mark P. Johnson N. Scott Adzick
Center for Fetal Diagnosis and Treatment, Children’s Hospital of Philadelphia, Philadelphia, Pa., USA
demises); 90.8% of women delivered at the Children’s Hos-
pital of Philadelphia and 3.4% received transfusions. With re-
gard to the neonates, 2 received ventriculoperitoneal shunts
prior to discharge; 71.1% of neonates had no evidence of
hindbrain herniation on MRI. Of the 80 neonates evaluated,
55% were assigned a functional level of one or more better
than the prenatal anatomic level. Conclusion: In an experi-
enced program, maternal and neonatal outcomes for pa-
tients undergoing fMMC repair are comparable to results of
the MOMS trial. © 2014 S. Karger AG, Basel
Introduction
Each year in the USA, approximately 1,500 babies are
born with spina bifida [1]. Although 75% of the affected
individuals survive to adulthood, the 1-year survival rate
among infants with open spina bifida remains at 88–96%
[2, 3]. Significant lifelong disabilities and morbidity are
associated with this common birth defect that is amena-
ble to prenatal diagnosis through routine screening [4–6].
Key Words
Fetal surgery · Myelomeningocele · Myeloschisis · Neural
tube defect · Spina bifida
Abstract
Background: Fetal myelomeningocele (fMMC) repair has
become accepted as a standard of care option in selected
circumstances. We reviewed our outcomes for fMMC repair
from referral and evaluation through surgery, delivery and
neonatal discharge. Material and Methods: All patients re-
ferred for potential fMMC repair were reviewed from January
1, 2011 through March 7, 2014. Maternal and neonatal data
were collected on the 100 patients who underwent surgery.
Results: 29% of those evaluated met the criteria and under-
went fMMC repair (100 cases). The average gestational age
was 21.9 weeks at evaluation and 23.4 weeks at fMMC repair.
Complications included membrane separation (22.9%), pre-
term premature rupture of membranes (32.3%) and preterm
labor (37.5%). Average gestational age at delivery was 34.3
weeks and 54.2% delivered at ≥35 weeks. The perinatal loss
rate was 6.1% (2 intrauterine fetal demises and 4 neonatal
Received: May 21, 2014
Accepted: June 18, 2014
Published online: August 15, 2014
Julie S. Moldenhauer, MD
Center for Fetal Diagnosis and Treatment, Children’s Hospital of Philadelphia
34th Street and Civic Center Boulevard
Philadelphia, PA 19104 (USA)
E-Mail moldenhauerj @ email.chop.edu
© 2014 S. Karger AG, Basel
1015–3837/14/0000–0000$39.50/0
www.karger.com/fdt
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2. Moldenhauer et al.Fetal Diagn Ther
DOI: 10.1159/000365353
2
With the ability to make a prenatal diagnosis and a known
clinical course, the concept of in utero repair of myelome-
ningocele (MMC) to improve outcomes came to fruition
with the initial failure of fetoscopic coverage of MMC fol-
lowed by the development of definitive successful open
fetal MMC (fMMC) repair [7–9].
The benefits and risks of fMMC repair were uncertain
until the results of the multicenter prospective random-
ized Management of Myelomeningocele Study (MOMS)
were published [10]. The trial compared fMMC repair to
standard neonatal repair and demonstrated that fMMC
repair led to decreased rate of shunting at 12 months of
age, reversal of hindbrain herniation and improved out-
comes, including the ability to walk at 30 months of age.
As such, in the time since the trial concluded, fMMC re-
pair has become a standard of care option for prenatally
diagnosed spina bifida in appropriately selected fetal
surgery candidates [11]. Optimal care guidelines have
been developed, but the reproducibility of these results
have been questioned outside the setting of a rigorous tri-
al [12, 13]. Therefore, we sought to review our outcomes
for fMMC repair after the MOMS trial from referral and
evaluation through surgery, delivery and neonatal dis-
charge.
Material and Methods
The fetal therapy database of the Center for Fetal Diagnosis and
Treatment at the Children’s Hospital of Philadelphia (CHOP) was
queried for all women referred for the indication of fMMC from
January 1, 2011 through March 7, 2014. The disposition of those
referrals was reviewed. Women who presented for an on-site eval-
uation underwent a thorough screening and evaluation process
consistent with the protocol used in the MOMS trial. Patients were
prospectively enrolled in an fMMC repair database. Maternal de-
mographics, prenatal diagnostic criteria, fetal surgery, delivery and
neonatal outcomes were collected. Perioperative care and postop-
erative follow-up were consistent with the MOMS trial protocol.
Alterations in the hysterotomy surgical technique from the MOMS
trial were developed to avoid jamming of the uterine stapling de-
vice (Poly CS 57 mm stapler; Covidien, Mansfield, Mass., USA) in
thick uterine tissue. With this approach, the following method is
used: (1) two monofilament stay sutures are placed through the
full-thickness uterine wall under sonographic guidance, (2) the
cautery is used to incise between these two sutures through the
myometrium and membranes to create a precisely made 1-cm hys-
terotomy and (3) an atraumatic Glassman intestinal clamp (V.
Mueller, San Diego, Calif., USA) is placed to compress the uterine
tissue in the line of the planned stapler deployment, followed by
removal of the Glassman clamp and placement of the uterine sta-
pler which is then fired. We also pretreat the staple line in the sta-
pler with sterile mineral oil to facilitate staple disengagement from
the uterine stapler after it is deployed. In our study, if the patients
remained stable without complication, and their referring physi-
cians were willing to care for them, the patients returned to their
home institution for delivery as determined on a case-by-case ba-
sis, which was an alteration from the MOMS trial. IRB approval
for prospective data collection was granted for this study.
Results
During the study period a total of 587 women were re-
ferred to our center for an indication of fMMC with the
disposition presented in table 1. Of these, 348 women pre-
sented for prenatal evaluation at CHOP; 101 were candi-
dates (29%) and were taken to the operating room for
fMMC repair during the study period; 1 fMMC repair
could not be performed due to maternal hemodynamic in-
stability as a consequence of anesthetic sensitivity. In that
case, the maternal laparotomy was performed, a hysterot-
omy was not undertaken and the laparotomy was closed.
The woman delivered at term by cesarean section, and the
babyunderwentpostnatalMMCrepair.Afurther38wom-
en were fetal surgery candidates but chose either postnatal
surgery (n = 13) or TOP (n = 25) instead of fMMC repair.
A total of 100 women underwent fMMC repair during
this time period. Maternal demographics are presented in
table 2. The average gestational age at evaluation was 21
Table 1. Disposition of patients referred for fMMC repair
Total
(n = 587)
%
On-site evaluations 348 59.3
Disposition of fMMC repair candidates 139 23.7
Open fetal surgery 101 17.2
Postnatal care 13 2.2
Termination of pregnancy 25 4.3
Exclusions for noncandidates 209 35.6
BMI >35 12 2.0
Additional anomalies on imaging 66 11.2
Genetic diagnosis in fetus 8 1.4
Gestational age >26 weeks 5 0.9
Preexisting maternal medical condition 65 11.1
Multiple pregnancy 10 1.7
No hindbrain herniation on MRI 43 7.3
Disposition of referral-only patients 239 40.7
Declined appointment 67 11.4
Information call only 57 9.7
Insurance issues 1 0.2
International patient 22 3.7
Not a candidate based on basic information 77 13.1
Opted for termination of pregnancy 15 2.6
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3. Fetal Myelomeningocele Repair at CHOP Fetal Diagn Ther
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6/7 weeks. MMC or myeloschisis was present in 67 and
33%, respectively. L3/L4 (66%) was the most common
bony lesion level, and the lesion was L3 or as low as S1 in
73% of fetuses that underwent fMMC repair. Fetal and
pregnancy characteristics are presented in table 3.
The average gestational age at the time of fetal surgery
was 23.4 weeks. Overall, 1 patient required a blood trans-
fusion at the time of fetal surgery. Fetal resuscitation was
successfully performed in 5 cases, as defined by the need
for intraoperative cardiac compressions and/or adminis-
tration of atropine, epinephrine or blood products via the
umbilical vein [14]. In the immediate postoperative pe-
riod, 2 women required treatment with furosemide for
pulmonary edema. The average total operative time from
maternal skin incision to closure was 78.5 min. Periop-
erative outcomes are presented in table 4.
The average gestational age at delivery was 34.3 weeks
and the average birthweight was 2,416 g (table 5); 9.4%
delivered at less than 30 weeks and 54.2% delivered at 35
weeks or more; 2 women have not yet delivered. Chorio-
amniotic membrane separation was detected by postop-
erative ultrasonography in 22.9%. Preterm premature
rupture of membranes (PPROM) occurred in 32.3%
(31/96) and preterm labor (PTL) occurred in 37.5%
(36/96). Of these, 16 had PPROM with PTL. The perina-
tal loss rate was 6.1% (6/98), which included 2 intrauter-
ine fetal demises (IUFD) and 4 neonatal demises (NND);
1 IUFD was diagnosed at the conclusion of fMMC repair
prior to maternal emergence from anesthesia – there had
been transient fetal bradycardia that resolved spontane-
ously during the operation. The other IUFD was diag-
nosed by ultrasound on postoperative day 1. The 4 NND
occurred in women who had PPROM or PTL within 2
weeks of fMMC at 22 1/7, 23 2/7, 24 4/7 and 24 4/7 weeks.
Of these, 2 were previable, comfort care was provided per
parental decision in another case, and support was with-
drawn in 1 case due to severe prematurity.
Clinical chorioamnionitis was diagnosed in 4 women,
all of whom experienced PPROM. A further 6 women
were diagnosed with persistent oligohydramnios without
PPROM, and 1 woman was diagnosed with preeclampsia/
gestational hypertension. Placental abruption was diag-
nosed in 2 women, and 1 woman was diagnosed with
Table 2. fMMC repair patient characteristics (100 patients)
Maternal age, years 29.7 (18–41)
Multiparous 65 (65%)
Nulliparous 35 (35%)
Ethnicity
Caucasian 88 (88%)
African American 4 (4%)
Hispanic 6 (6%)
Native American 1 (1%)
Asian 1 (1%)
BMI 26.3 (18.7–35)
Family history of spina bifida
Yes 12 (12%)
No 88 (88%)
Gestational age at evaluation, weeks 21 6/7 (18 1/7–25 4/7)
Table 3. Fetal and pregnancy characteristics (100 patients)
Fetal gender
Female 52 (52%)
Male 48 (48%)
Placenta location
Anterior 46 (46%)
Posterior 51 (51%)
Fundal 2 (2%)
Right lateral 1 (1%)
Lesion level
T11/T12 6 (6%)
L1/L2 21 (21%)
L3/L4 66 (66%)
L5/S1 7 (7%)
Type of lesion
Myeloschisis 33 (33%)
MMC 67 (67%)
Lateral ventricle measurements, mm
Right 10.0 (4–18)
Left 10.6 (3.1–18)
Talipes present 15 (15%)
Poor or decreased lower extremity movement 9 (9%)
Table 4. Operative characteristics (100 patients)
Gestational age at fetal surgery, weeks 23.3 (20 2/7–25 6/7)
Intraoperative cephalic version
Yes 40 (40%)
No 60 (60%)
Maternal transfusion, U 1 (1%)
Estimated blood loss, ml 131.8 (50–500)
Patch required
Yes 20 (20%)
No 80 (80%)
Fetal resuscitation
Yes 5 (5%)
No 95 (95%)
Total operative time, min 78.5 (54–106)
Pulmonary edema 2 (2%)
Postoperative length of stay, days 4.2 (3–8)
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4. Moldenhauer et al.Fetal Diagn Ther
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acute appendicitis and underwent uncomplicated laparo-
scopic appendectomy between fMMC repair and delivery.
A total of 90.8% of the patients delivered at CHOP.
The remaining patients returned to their home institu-
tion for local delivery. Delivery outcomes, including the
status of the hysterotomy for those delivering at CHOP,
are presented in table 6. The estimated blood loss aver-
aged 754.5 ml and 3 women (3.4%) required blood trans-
fusion. Cesarean hysterectomy was performed in 1 case
and the patient had an uneventful postoperative course.
Neonatal outcomes are presented in table 7 for the 83
live-born patients cared for at CHOP. Dehiscence of the
fetal repair was noted in 3 neonates. There were 2 skin
wound dehiscences that required dressing changes after
preterm delivery at 25 3/7 and 35 weeks, respectively, and
1 who had received an AlloDerm (LifeCell Corporation,
Bridgewater, N.J.) patch skin closure required wound re-
vision after delivery at 36 4/7 weeks. Hindbrain hernia-
tion was reversed in 71.1%. In addition, 1 neonate was
diagnosed with aspiration pneumonia, 1 had necrotizing
enterocolitis and required a bowel resection and 1 was
diagnosed with 22q11 deletion syndrome. Functional lev-
el was improved compared to prenatal sonographic bony
lesion level in 44 of 80 (55%) neonates who were assessed.
Discussion
Our experience with fMMC at CHOP since the con-
clusion of the MOMS trial is similar to the results of the
published MOMS trial in the New England Journal of
Medicine [10]. In that trial, 1,087 women underwent pre-
liminary screening, with 183 (16.8%) of those undergoing
randomization. Of 299 patients referred to a study center
for further screening and evaluation, 183 (61%) were
deemed appropriate candidates and accepted randomiza-
tion. At CHOP after the MOMS trial, of the 587 referrals
for MMC evaluation, 104 (17.7%) ultimately underwent
fetal surgery. Of the 348 on-site evaluations performed,
29% underwent fMMC repair. Although it is difficult to
compare the proportion of women inquiring about fetal
MMC repair to those who are deemed candidates and opt
Table 5. Maternal and perinatal outcomes (96 patients)
Membrane separation 22/96 (22.9%)
PPROM 31/96 (32.3%)
Preterm labor 36/96 (37.5%)
Oligohydramnios 6/96 (6.3%)
Average gestational age at delivery weeks 34.3 (22 1/7–37 4/7)
Gestational age
<30 weeks 9/96 (9.4%)
30–34 weeks 35/96 (36.4%)
35–36 weeks 26/96 (27.1%)
>37 weeks 26/96 (27.1%)
Birthweight, g 2,415.5 (501–3,636)
Perinatal death 6/98 (6.1%)
2 IUFD
4 NND
Table 6. Delivery outcomes at CHOP (89 delivered)
Delivery at CHOP 89/98 (90.8%)
Estimated blood loss at delivery, ml 754.5 (400–2,000)
Transfusion 3/89 (3.4%)
Postoperative length of stay, days 3.1 (2–4)
Hysterotomy at delivery
Intact 44/87 (50.6%)
Thin 36/87 (41.4%)
Focal dehiscence 6/87 (6.9%)
Dehiscence 1/87 (1.1%)
Hysterotomy: the 2 IUFD cases that occurred within 24 h of
surgery were omitted from the hysterotomy assessment.
Table 7. Neonatal outcomes at CHOP (83 patients)
Apgar (1 min) 7.5 (1–10)
Apgar (5 min) 8.4 (3–10)
Dehiscence at repair site 3/83 (3.6%)
Shunt prior to discharge 2/83 (2.4%)
Hindbrain herniation on MRI
None 59/83 (71.1%)
Yes 13/83 (15.7%)
Mild/minimal 7/83 (8.4%)
Not imaged 4/83 (4.8%)
Respiratory distress syndrome 43/83 (51.8%)
Apnea 48/83 (57.8%)
Caffeine therapy 43/83 (51.8%)
Pneumothorax 3/83 (3.6%)
Length of stay, days 24.5 (3–133)
Foot deformity 32/83 (38.6%)
Functional vs. prenatal lesion level (n = 80)
2 levels worse 1 (1.25%)
1 level worse 9 (11.25%)
No difference 26 (32.5%)
1 level better 20 (25%)
2 levels better 12 (15%)
3 levels better 6 (7.5%)
4 levels better 5 (6.25%)
5 levels better 1 (1.25%)
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5. Fetal Myelomeningocele Repair at CHOP Fetal Diagn Ther
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to have the procedure after the MOMS trial, it is clear
from the process utilized in the MOMS trial that only a
small proportion of those initially interested will be ap-
propriate candidates and commit to surgery.
The average maternal age, race or ethnic group distri-
bution, maternal BMI, placental location, and gender dis-
tribution were very similar between the study cohort and
the MOMS trial. The number of patients with an L3 or
lower lesion in the prenatal surgery limb of the MOMS
trial was 68 compared to 73% in our cohort. L3 and L4
lesions made up 66 of our cohort compared to 38% of the
prenatal cohort in the MOMS trial. Our cohort saw only
15% of talipes prenatally in comparison to the MOMS
cohort of 26%. Some of these factors may be associated
with self-selected patients knowledgeable about the trial,
who presented for fMMC repair in order to preserve nor-
mal function seen prenatally and their hopes for improve-
ment of long-term motor function.
Rates of PTL and membrane separation were similar
between our cohort and the MOMS trial. We did see a low-
er rate of PPROM of 32.3% compared to 46% in the trial.
Modifications in our perioperative management of fluids
decreased the rate of pulmonary edema in our cohort (2 vs.
6% in the trial). Patients were encouraged to maintain a
robust oral intake of water the night before surgery; post-
operatively, intravenous fluids were highly restricted while
fluid intake and output were monitored very closely. We
believe that this has resulted in the decreased rate of pul-
monary edema requiring diuretic treatment.
Similar to the trial, the majority (50.6%) of our patients
had an intact hysterotomy at the time of delivery. Our rate
of transfusion at the time of delivery was 3.4% compared
to 9% in the trial. This, again, is partly due to modifica-
tions in technique and continuity of delivery team mem-
bers who are very experienced with delivery of women
who have undergone fMMC repair. In all cases, the pa-
tient is typed and crossed preoperatively with blood avail-
able should the need arise. The average blood loss at the
time of cesarean delivery after fMMC repair was 754.5 ml,
which is well above the average blood loss that has been
reported with cesarean delivery in general – in the range
of 128–608 ml [15]. Of the 3 women who received a blood
transfusion, 1 required a cesarean hysterectomy. This was
probably due in part to 2 prior cesarean deliveries with
significant intra-abdominal scarring and very friable tis-
sue at delivery. This risk after multiple prior cesarean de-
liveries should be part of the counseling process. In the
trial, prior uterine surgery was defined as full myometrial
thickness or incision in the fundal region, while prior low
transverse cesarean scars were not an exclusion factor.
During the MOMS trial, all the women remained in
close proximity to the centers performing the fMMC
repair for ongoing care and delivery. Since the trial,
women now have the option of returning to their refer-
ral centers for care and delivery if that is mutually ac-
ceptable between the performing center and the refer-
ring center. In our experience, 90.8% of our patients
opted to remain local and deliver with our group. The
average gestational age at delivery of 34.3 weeks was
similar to the 34.1 weeks seen in the MOMS trial. The
stratification of gestational age at delivery was very sim-
ilar, although we saw a slight decrease in the number of
deliveries before 30 weeks (9.4% at CHOP compared to
13% in the trial). Our average birthweight of 2,415.5 g
was comparable to the birthweight of 2,383 g in the tri-
al group.
The perinatal loss rate in our series of 6.1% was higher
than the prenatal repair group in the MOMS trial of 3%.
The 2 IUFD cases were not anticipated. In all 4 of the
NND cases, PPROM or PTL ensued within 2 weeks of
fMMC repair, which may, in part, be attributed to the
earlier gestational age at which the fMMC repair was per-
formed in our cohort. In the MOMS trial, randomization
occurred at an average gestational age of 23 6/7 weeks
with surgery thereafter at 24 weeks of gestation or more,
whereas the average gestational age at the time of surgery
in our group was 23 3/7 weeks. Therefore, any PPROM
or PTL in the more immediate postoperative period
would have occurred at a gestation of at least 24 weeks or
more on average in the trial, with a higher likelihood for
survival.
Although the distribution of gestational age at delivery
was similar in our cohort compared to the prenatal sur-
gery cohort in the MOMS trial, we saw a higher rate of
respiratory distress syndrome (52 vs. 21%) and apnea (58
vs. 36%) in our group. This has prompted the creation of
a clinical care pathway for these neonates to monitor
them closely for apnea. There were no neonates with cul-
ture-proven sepsis in our cohort, although 44/83 (53%)
underwent a work-up to rule out sepsis. Of the 83 neo-
nates, 2 (2.4%) underwent ventriculoperitoneal shunt
placement prior to discharge from the hospital. The lon-
ger-term shunt requirements are not reported in this
study, and the patients are being followed to determine
the overall shunt placement rate at 12 months of age; 3/83
neonates had dehiscence of the fetal repair site. This does
not seem to be related to the use of patch or gestational
age as the clinical picture associated with the skin break-
down was varied. Only 1 of the 3 required postnatal
wound revision, while 2 were managed with dressing
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6. Moldenhauer et al.Fetal Diagn Ther
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6
changes. It is important to counsel families that this is a
possibility and that all neonates are evaluated for this
complication.
Although talipes was diagnosed in 15% of fetuses pre-
natally, 38.6% of neonates were noted to have clubbing or
foot deformities. It has been documented that prenatal
function as assessed by leg movements on sonography
does not necessarily correlate with postnatal functional
level [16], which is determined through physical therapy
assessment in the neonatal period in our institution. In
comparison to prenatal anatomic lesion level by ultra-
sound, we saw an improvement in functional motor level
by at least one level in 55% of neonates. This needs to be
followed closely to determine how the longer-term out-
comes correlate with the neonatal assessment, and care
must be taken as to how this information is disseminated
during family counseling. The majority (71%) of neo-
nates in our cohort did not have evidence of hindbrain
herniation on neonatal MRI, 24% had some residual
hindbrain herniation and 5% were not imaged. In the
MOMS trial, 64% of the prenatal surgery group had hind-
brain herniation at 12 months. Our data includes only the
immediate neonatal imaging that is performed and not
outcomes at 12 months, so it will be important to deter-
mine if this rate of hindbrain herniation resolution re-
mains the same at 12 months.
Based on our data from 100 cases, we believe that
fMMC repair outside of the MOMS trial has similar out-
comes. In fact, with lessons learned and modifications in
perioperative technique, it is likely that we can improve
on those outcomes. Continued collaboration between
centers that are performing fMMC repair to track results
long-term and promote further research is essential to
optimize safety and outcomes.
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