+ MODEL
Journal of Pediatric Urology (xxxx) xxx xxx
a
Division of Pediatric Urology,
Nicklaus Children’s Hospital,
Miami, FL, USA
b
Division of Pediatric Urology,
Joe DiMaggio Children’s
Hospital, Hollywood, FL, USA
* Corresponding author. Division
of Pediatric Urology, Nicklaus
Children’s Hospital, 3200 SW
60th Court, Suite 104, Miami,
FL, 33155, USA. Tel.: þ1 (305)
669 6448.
moscardi.paulo@gmail.com
(P.R.M. Moscardi)
Keywords
Epispadias; Small intestinal
submucosa; Penile curvature
Received 29 December 2018
Accepted 18 May 2019
Available online xxx
https://doi.org/10.1016/j.jpurol.2019.05.024
1477-5131/ª 2019 Journal of Pediatric Urology Company. Published by Elsevier Ltd. All rights reserved.
Please cite this article as: Ballesteros N et al., Use of small intestinal submucosa for corporal body grafting in cases of epispadias and
epispadias/exstrophy complex, Journal of Pediatric Urology, https://doi.org/10.1016/j.jpurol.2019.05.024
Use of small intestinal submucosa for
corporal body grafting in cases of
epispadias and epispadias/exstrophy
complex
N. Ballesteros a, P.R.M. Moscardi a,*, R. Blachman-Braun a,
M. Salvitti a,b, A. Alam a,b, M. Castellan a,b, K. Kozakowski a,b,
R. Gosalbez a,b, A. Labbie a,b
Summary
Background
Male epispadias is a rare congenital urogenital
anomaly in which the meatus is ectopically located
along the dorsal midline of the penile shaft. In cases
associated with severe curvature, functional and
cosmetic outcomes could be accomplished by
lengthening the shorter dorsal surface with the use
of corporal grafting. Various graft materials have
been used in the past for hypospadias repair
including tunica vaginalis, dermis, and small intes-
tinal submucosa (SIS). The use of SIS grafting for
corporoplasty during epispadias repair has rarely
been described in the literature.
Objective
To report the experience in the management of
dorsal corporal body grafting using SIS in children
with severe penile curvature due to epispadias.
Study design
The authors retrospectively reviewed the charts of
all patients with epispadias or bladder exstrophy/
epispadias complex and severe dorsal chordee
(>40 ) who underwent epispadias repair with single-
layer SIS for corporal body grafting. Clinical vari-
ables, surgical technique, and outcomes were
analyzed.
Results
A total of nine consecutive patients underwent
staged epispadias repair with dorsal corporal single-
layer SIS grafting (summary figure). Of these, four
(44.4%) had primary penopubic epispadias, one
(11.1%) had mid-shaft epispadias, and four (44.4%)
had bladder exstrophy/epispadias complex. The
mean age at surgery was 13.4  6 months. After
phalloplasty with SIS grafting, there were no re-
ported complications related to the graft during the
post-operative period or follow-up visits.
Discussion
Although traditional techniques for epispadias repair
allow some degree of corporal lengthening, they
also result in abrupt medial rotation of the corporal
bodies leading to torqueing and potential unsatis-
factory cosmetic results. In contrast, the authors use
single-layer SIS for corporal body grafting, and this
study technique results in a more gradual inward
rotation thus allowing more anatomical accuracy.
Furthermore, an advantage of the use of SIS over
other grafting materials is that there is no need to
harvest an autologous graft such as tunica vaginalis
or dermis.
Conclusion
Epispadias repair using single-layer SIS corporal body
grafting is an effective, safe, and feasible method,
which provides satisfactory cosmesis and correction
of dorsal curvature in congenital epispadias in chil-
dren. Furthermore, a more normal penis appear-
ance, without a decrease in the corporal length or
diameter, is achieved with this technique.
 + MODEL
1.e2
Summary Fig. Dorsal transverse corporotomies at the area of maximum chordee (white arrows). The defects are then grafted
with single-layer SIS.
Introduction
Male epispadias is a rare congenital urogenital anomaly in
which the meatus is ectopically located along the dorsal
midline of the penile shaft. It may be seen as an isolated
defect or as part of the bladder exstrophyeepispadias
complex (BEEC). Several anatomical factors contribute to
the complexity of surgical reconstruction including dorsal
penile curvature, ventral hooded prepuce, and deficient
skin dorsally. In cases of BEEC, extragenital anomalies such
as poor pelvic musculature, pubic diastasis, bladder neck
abnormalities, and vesicoureteral reflux are also seen [1,2].
In cases associated with severe curvature, functional
and cosmetic outcomes could be accomplished by length-
ening the shorter dorsal surface with the use of corporal
grafting. Various graft materials have been used in the past
for hypospadias repair including tunica vaginalis, dermis,
and small intestinal submucosa (SIS) [3]. SIS is an acellular
extracellular matrix biomaterial that is mechanically
derived from porcine small intestine and has been shown to
improve wound healing by creating a scaffold that allows
adherence, migration, proliferation, and differentiation of
numerous cell types, leading to tissue-specific regeneration
[4]. In 2002, Kropp et al. initially reported the use of SIS
grafting for surgical correction of severe ventral curvature
Please cite this article as: Ballesteros N et al., Use of small intestinal submucosa for corporal body grafting in cases of epispadias and
epispadias/exstrophy complex, Journal of Pediatric Urology, https://doi.org/10.1016/j.jpurol.2019.05.024
N. Ballesteros et al.
in patients with hypospadias [5]. Since then, other authors
have described their experience, with overall studies
showing satisfactory outcomes [3,6] and few complications
[7,8].
The use of SIS grafting for corporoplasty during epis-
padias repair has rarely been described in the literature,
with only two previously reported cases of patients with
BEEC that underwent surgical correction at the age of 16
and 17 years [5]. Owing to the successful results in the
management of hypospadias with SIS grafting, one pediatric
urologist at the authors institution has been performing
epispadias reconstruction using SIS grafting for 10 years.
Thus, in this article, the authors aim to present their
experience and outcomes in the management of epispadias
with SIS grafting. To the authors knowledge, this is the first
report of this surgical technique in young children.
Materials and methods
Patients selection and clinical assessment
After IRB approval, a retrospective chart review was per-
formed including all patients with isolated epispadias or
BEEC and severe dorsal chordee (>40 ) who underwent
epispadias repair with single-layer SIS (SURGISIS; Cook
Biotech, US) corporal body grafting at the authors institu-
tion from January 2008 to July 2018. Data regarding patient
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Epispadias: use of small intestinal submucosa 1.e3

characteristics included age at surgery, surgical technique,
duration of follow-up, post-operative cosmesis, erectile
function, and post-operative complications. Information
regarding penile erections was obtained from parents dur-
ing follow-up visits. All of the patients were operated on by
one of two pediatric urologists. Descriptive statistics were
obtained with the program, SPSS version 24 (Chicago). For
continuous variables, the mean and standard deviation was
reported, and categorical variables were presented as ab-
solute values and frequencies.
Surgical technique
A ventral circumcising incision was made and carried
dorsally around the urethral plate, preserving it, to just
cephalad to the meatal opening on the pubic region. The
penis was degloved, and the corpora were completely
dissected to Bucks fascia with care to identify and protect
the neurovascular bundles (NVBs). The urethral plate with
its spongiosal tissue was then elevated. Artificial erections
were performed noticing the degree of dorsal chordee and
its point of maximal curvature, which usually is greater
than 90 and with significant tethering by the short urethral
plate (Supplementary Fig. 1). The urethral plate was
divided distally and mobilized back. Both corpora were
further mobilized and separated in the midline raphe,
without total disassembly of the glans and distalmost
corpora cavernosa. Lateral mobilization of the NVB was
carefully performed as needed. At this point, there was
sufficient space on the dorsal shafts for corporotomy and
SIS grafting. A dorsal transverse incision was made at the
area of maximum chordee on each corpora that was
approximately 180 degrees of their circumference, reach-
ing the most lateral and medial points of each tunica
albuginea (Fig. 1a). Note that this results in penile
straightening with two long elliptical defects. The defects
were measured, and two elliptical pieces of single-layer SIS
graft, 20% greater than the measured defect, were sized
and sutured with 7-0 PDS (Fig. 1b). The tourniquet was then
released revealing hemostasis of the grafted site (Fig. 1c).
Artificial erections demonstrated a straight penis in a
dependent position, with significant elongation, and
pointing about 90 from the abdominal wall. The corpora
were then sutured together with 6-0 PDS. The distal ure-
thral plate was tubularized over an 8 Fr catheter with 5-
0 PDS, and the urethra was transposed ventrally to allow for
reconstruction in the next stage. The IPGAM procedure was
done to fashion the meatus. The deep glans closure was
done dorsally with 6-0 PDS, and the cuticular layer was
approximated with 6-0 monocryl, including a circumcision
collar. The proximal urethra was mobilized, dropped
ventrally, spatulated, and fixed to the underlying corpora
cavernosa with 5-0 PDS. In cases of previous exstrophy
closure, scar tissue was dissected, and when needed, deep
fascial closure of the lower abdominal wall was done with
2-0 PDS. The skin was tailored for dorsal midline closure
with reversed Byars flaps and sutured with 6-0 Monocryl.
The distal aspect of the closure was anastomosed to the
tubularized urethral plate. Proximally, the skin was anas-
tomosed to the spatulated urethra, leaving a proximal
hypospadic meatus. A sterile dressing was applied, and
proximally, an 8 Fr tube was secured with 5-0 prolene and
left for bladder drainage to double diaper technique. The
tubularized distal urethra was stented with a 5 Fr tube tied
with a knot for maintenance of post-operative patency
(Fig. 2).
Results
A total of nine consecutive patients underwent epispadias
repair with dorsal corporal SIS grafting (Supplementary
Table 1). Of these, four (44.4%) had primary penopubic
epispadias, one (11.1%) had penile shaft epispadias, and
four (44.4%) had bladder exstrophy/epispadias complex,
with the bladder closure performed previously in infancy
(two as neonates and one each at 4 and 10 months old). The
mean age at surgery was 13.4  6 months, with a range of
7e22 months. All patients, except for one, received 1 or 2
intramuscular testosterone cypionate injections (2 mg/kg)
depending on penile growth response. The surgical tech-
nique was done as described above, except for one patient
who underwent a one-stage Mitchell-type technique of
total penile disassembly although still underwent SIS cor-
poroplasty and ventral urethral tube transposition (after

Fig. 1 Corporoplasty. (A) Dorsal transverse corporotomies are performed at the area of maximum chordee. (B) The defects are
grafted with single-layer SIS. (C) Hemostatic grafted corpora after tourniquet release.

Please cite this article as: Ballesteros N et al., Use of small intestinal submucosa for corporal body grafting in cases of epispadias and
epispadias/exstrophy complex, Journal of Pediatric Urology, https://doi.org/10.1016/j.jpurol.2019.05.024
 + MODEL
1.e4 N. Ballesteros et al.

Fig. 2 Final cosmesis. (A and B) Patient 4 at his 73rd month of follow-up. C and D, patient 2 after 62 months of follow-up.

Table 1 Clinical variables and outcomes. patient with a history of BEEC underwent concomitant
Clinical variable Patients bladder neck reconstruction. Post-operative outcomes are
n Z 9 (%) summarized in Table 1. There were no reported complica-
tions related to the graft during the immediate post-oper-
Clinical presentation
ative period or follow-up visits. For all patients, there were
Primary penopubic epispadias 4 (44.4)
no complications from the first stage including no shaft
Bladder exstrophy epispadias complex 4 (44.4)
hourglass appearance, no bumps, no aneurysmal dilatations
Penile shaft epispadias 1 (11.1)
of the tunica, nor changes in consistency of the area where
Mean age at surgery in months (range) 13.4  6 (7e22)
the graft was placed. Likewise, all patients were reported
Graft-related complications (1st stage) 0
to have satisfactory cosmetic results (Fig. 2). During follow-
Post-operative complications (2nd stage) 4
up, six patients were reported by their parents to have
Clinical straight erectiona 6 (75)
straight penile erections, two whose parents had not
Satisfactory cosmetic results 9 (100)
monitored for erections, and one patient had only been
Mean follow-up in months 57.3  42.4
seen once to remove dressings after his first stage. All pa-
Mean  standard deviations. tients had eventual second-stage urethroplasty except for
a
On two patient parents had not noticed any erections during the one who had a single stage procedure and the last pa-
follow-up and 1 patient had only been seen once to remove
tient who had recently undergone his first stage. Overall,
dressings after his first stage.
the mean follow-up was 57.3  42.4 months, with patient
age at the last office visit ranging from 19 to 120 months.
graft corporoplasty, the residual urethral plate is usually There were four patients with subsequent complications
too short and reconstructed at a subsequent stage; how- after urethroplasty. Three of them underwent surgical
ever, this patient had adequate urethral length despite correction: two urethral diverticulectomies and an epis-
corporoplasty that was amenable for a single-stage pro- padias revision with redo Byars flaps for dorsal skin
cedure). He did not require subsequent operations. Another contracture that was causing mild distal penile shaft to tilt

Please cite this article as: Ballesteros N et al., Use of small intestinal submucosa for corporal body grafting in cases of epispadias and
epispadias/exstrophy complex, Journal of Pediatric Urology, https://doi.org/10.1016/j.jpurol.2019.05.024
 + MODEL
Epispadias: use of small intestinal submucosa
upward. For the latter, an artificial erection was performed
after the skin was fully degloved revealing completely
straight corpora. The fourth patient developed dorsal
glandular urethrocutaneous fistula as well as urethral
diverticulum and will undergo surgical correction in the
future.
Discussion
Penile epispadias has inherent anatomic deformities that
make its correction difficult and variable. These include
disproportional corpora cavernosa, inconsistent NVB
course, and variable skin deficiencies. Long-term studies on
adults who underwent epispadias repair during childhood
have shown that their main complaints relate to very short
penis, persistent or recurrent dorsal curvature, and difficult
or painful sexual intercourse [9]. Several techniques are
used for epispadias repair, none being the gold standard.
The more common ones are the Mitchell technique, which
involves complete penile disassembly [10], lateral rotation
of the corpora, and the Cantwell-Ransley technique, which
avoids glandular disassembly and involves corporotomies
for curvature correction [11]. In the latter, the corporoto-
mies are sutured together in the midline, dorsal to the
urethra, in a Heineke-Mikulicz fashion. Ventral curvature
correction during epispadias repair should be a priority as it
is strongly associated with sexual dysfunction and psycho-
logical burden during adulthood [12]. Although the
Cantwell-Ransley repair allows some degree of corporal
lengthening, it also results in an abrupt medial rotation of
the corporal bodies, which in the authors opinion, can lead
to some circumferential torque that might result in an
hourglass defect, thus causing unsatisfactory cosmetic re-
sults. In contrast, the study technique allows for a more
gradual inward rotation to the midline thus allowing more
anatomical accuracy, as well as the authors perception of
increased length.
The long-term focus of epispadias repair, besides having
an orthotopic urethra and meatus, is achieving a straight
phallus of adequate length and with acceptable cosmesis.
The use of single-layer SIS grafting has shown satisfactory
short-term outcomes in chordee repair during hypospadias
surgery [3]. Of note, the size of the graft is chosen to be
about 20% greater than the defect to account for a small
degree of contraction that is expected during the healing
process [3]. At the authors institution, they have incorpo-
rated this technique for the correction of dorsal chordee
during epispadias repair.
Kappa et al. used single-layer SIS grafts in rats showing
that it provides histologically an adequate scaffold that
fully incorporates into the corporal body and results in a
tunica albuginea that is virtually identical to the control
group [5]. The study results show no evidence of graft
fibrosis, contracture, shrinkage, or dilatation with the use
of single-layer SIS corporal grafting in children.
A surgical advantage of the use of SIS over other grafting
materials is that there is no need to harvest an autologous
graft such as tunica vaginalis or dermis [7]. Although these
tissues provide the inherent advantage of graft compati-
bility, conventional results regarding residual chordee and
satisfactory outcomes of the tunica vaginalis grafts might
Please cite this article as: Ballesteros N et al., Use of small intestinal submucosa for corporal body grafting in cases of epispadias and
epispadias/exstrophy complex, Journal of Pediatric Urology, https://doi.org/10.1016/j.jpurol.2019.05.024
1.e5
raise concerns [13,14]. Furthermore, dermal graft har-
vesting is a time-consuming endeavor not exempt of com-
plications, which will inevitably leave an additional scar
[7]. Therefore, the use of SIS graft avoids the inherent
complications of autologous grafting, while providing an
adequate biomaterial that creates a scaffold for tunica
albuginea healing.
Though the study results are encouraging, it is important
to address that because of the small sample size and the
relatively new approach of using single layer SIS graft for
the management of severe chordee in patients with epis-
padias, and the study outcomes still need to be further
assessed after puberty and need to be compared in ran-
domized trials against autologous grafts. Nonetheless, the
study’s early findings indicate that single-layer SIS graft is
another safe and useful option for the treatment of severe
chordee with satisfactory cosmetic and functional
outcomes.
Conclusion
The use of single-layer SIS corporal body grafting is an
effective method for the correction of dorsal curvature in
epispadias repair. The authors demonstrate that this tech-
nique is safe, feasible, and provides satisfactory cosmesis
without decreasing corporal length or diameter. To the
authors knowledge, this is the first report of this surgical
technique in young children.
Author statements
Acknowledgments
The authors are grateful to all the personnel that was
involved in the medical and surgical treatment of these
patients.
Ethical approval
IRB approval was obtained for this study.
Funding source
None.
Competing interest
The authors declare that they have no competing interests
regarding this article.
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Appendix A. Supplementary data
Supplementary data to this article can be found online at
https://doi.org/10.1016/j.jpurol.2019.05.024.