Pediatr Radiol (2014) 44:768–786 DOI 10.1007/s00247-014-2892-5

REVIEW

Bladder exstrophy: current management and postoperative imaging Ketsia Pierre & Joseph Borer & Andrew Phelps & Jeanne S. Chow

Received: 19 June 2013 / Revised: 1 December 2013 / Accepted: 20 January 2014 # Springer-Verlag Berlin Heidelberg 2014

Abstract Bladder exstrophy is a rare malformation characterized by an infra-umbilical abdominal wall defect, incomplete closure of the bladder with mucosa continuous with the abdominal wall, epispadias, and alterations in the pelvic bones and muscles. It is part of the exstrophy–epispadias complex, with cloacal exstrophy on the severe and epispadias on the mild ends of the spectrum. Bladder exstrophy is the most common of these entities and is more common in boys. The goal of this paper is to describe common methods of repair and to provide an imaging review of the postoperative appearances. Keywords Bladder exstrophy . Exstrophy–epispadias complex . Voiding cystourethrogram . Ultrasound . Infants . Children . MRI Introduction Embryology The normal embryology of the cloacal membrane and defects that lead to bladder exstrophy are under investigation and

CME activity This article has been selected as the CME activity for the current month. Please visit the SPR Web site at www.pedrad.org on the Education page and follow the instructions to complete this CME activity. K. Pierre (*) : J. S. Chow Department of Radiology, Boston Children’s Hospital, 300 Longwood Ave., Boston, MA 02115, USA e-mail: [email protected] J. Borer : J. S. Chow Department of Urology, Boston Children’s Hospital, Boston, MA, USA A. Phelps Department of Pediatric Radiology, University of California, San Francisco, San Francisco, CA, USA

understanding is evolving [1–4]. Normally the cloaca begins as the common end of the rectal tube and urogenital tract. Division of the cloaca has traditionally been thought to occur by caudal migration of the upper urorectal septum and inward migration of the lower lateral Rathke folds. The cloacal membrane lies below the umbilical cord. Mesenchymal ingrowth shifts the cloacal membrane caudally, separating it from the umbilicus, and results in the formation of the lower abdominal muscles and pelvic bones. This is accompanied by medial migration of paired genital tubercles, which fuse in the midline cephalad to the cloacal membrane. The urorectal septum then fuses with the cloacal membrane, dividing it into the urogenital membrane anteriorly and the anal membrane posteriorly. The membrane eventually perforates, forming the urogenital and anal openings (Fig. 1) [5]. The most popular theory explaining the exstrophy– epispadias defect [6] describes an overgrowth of the cloacal membrane that prevents medial migration of the mesenchymal tissue. This prevents fusion of midline structures below the umbilicus. Depending on the extent of the abdominal wall defect, the cloacal membrane ruptures prematurely, resulting in the spectrum of the exstrophy–epispadias complex. If rupture occurs after the separation of the genitourinary (GU) and gastrointestinal (GI) tracts, classic bladder exstrophy results, as opposed to cloacal exstrophy, which occurs if rupture occurs before separation of the GU and GI tracts. Anatomical defects Children with bladder exstrophy have an everted bladder, epispadias, wide diastasis of the pubic symphysis, and pelvic muscular defects that result in anterior displacement of the anus and occasionally rectal prolapse. In boys the penis is short with wide separation of the corporal attachments. There

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Fig. 1 Diagram of the normal embryology of the cloaca and cloacal membrane. a Caudal growth of the urorectal septum divides the cloaca. b, c Downward shift of the cloacal membrane, fusion with the urorectal septum and subsequent perforation give rise to the anterior urogenital and posterior anal openings

is a cephalad (dorsal) curvature of the penis (Fig. 2). In girls the clitoris is bifid (Fig. 3) [7]. The defects result in an open book configuration of the pelvis in which the pubic bone is 30% deficient and the pelvic bones are externally rotated, resulting in an average diastasis of the pubic symphysis of 4 cm (Fig. 4) [8]. The pelvic floor anatomy is also altered. The puborectal sling is flatter (compared to its more normal conical shape)

Fig. 2 Clinical photograph of bladder exstrophy in a male neonate

Fig. 3 Clinical photograph of bladder exstrophy in a female neonate

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Fig. 4 Anteroposterior radiograph of a 5-year-old boy with bladder exstrophy. Note the open book configuration of the pelvis, with deficient pubic bones and outward rotation of the pelvic bones

and wider with divergence of the levator ani muscles. Compared to the normally centered position of the rectum within the levator muscles, the rectum is positioned in the anterior third of the pelvic floor (Fig. 5) [9]. The ureters insert low into the bladder and have a J-shape configuration because of the enlarged pouch of Douglas, which forces the distal ureters downward and laterally. These children invariably have vesicoureteral reflux following exstrophy closure unless ureteral re-implantation is performed (Fig. 6) [10].

Initial surgical repair of bladder exstrophy Despite several modifications over the years, currently there are two main approaches to bladder exstrophy repair: modern staged repair of exstrophy (MSRE) and complete primary repair of exstrophy (CPRE).

Fig. 5 Sagittal proton-density MRI of the pelvis in a 22-month-old boy following bladder exstrophy repair shows the anteriorly positioned rectum (wavy arrow) and thin puborectalis sling (arrowhead). Note the bladder (straight arrow)

Fig. 6 J-shape configuration of ureters in bladder exstrophy. Voiding cystourethrogram (VCUG) performed in a 2-month-old boy shows vesicoureteral reflux via J-shape ureter (arrow). In children with bladder exstrophy, the distal ureters are pushed downward and laterally as a result of mass effect by the enlarged pouch of Douglas. Note the bladder (arrowhead)

Modern staged repair of bladder exstrophy (MSRE) MSRE is a three-stage repair in boys and two-stage repair in girls. For stage I, performed within 48–72 h after birth, the bladder and the abdominal wall defect are closed in both boys and girls, with concomitant epispadias repair in girls only. Iliac osteotomies can be performed at this time. Stage II, closure of the urethra in boys (epispadias repair), is typically performed when children are 6– 12 months of age. Stage III (boys and girls) consists of bladder neck reconstruction, typically with bilateral ureteral reimplantation, and is performed when the child can participate in a voiding program, most commonly 4–5 years of age [10]. In stage I of MSRE, the umbilicus, bladder plate and urethral plate (to the level of the midshaft of the penis in males and vaginal os in females) is dissected off the anterior abdominal wall en bloc. A plane of dissection is carried inferiorly between the rectus fascia and bladder, and the urogenital diaphragm is taken down to the pelvic floor and detached from the pubis. If ureteral stents are in place, they are brought out through the urethra or bladder wall and a cystostomy catheter is used to drain the bladder. The urethral opening can be calibrated to an appropriate size using a urethral sound, and the bladder, bladder neck and urethral tissues are approximated in the midline. Pressure over the greater trochanters, with or without iliac osteotomies, potentiates near-approximation of the pubic bones, which are then sutured together. The suprapubic cystostomy catheter and ureteral stents can be brought out

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Fig. 7 Diagram shows stage I of MSRE. a Incision is made along the bladder plate and carried down to the urethral plate. b The bladder is dissected off the abdominal wall. c Ureteral stents are placed through the bladder wall and a suprapubic cystostomy catheter is used to drain the bladder. The urethra is calibrated to an appropriate size. The bladder,

bladder neck and urethral tissue are approximated in the midline. The rectus fascia and abdominal wall are closed. d, e Suprapubic cystostomy catheter and ureteral stents can be brought out through the neoumbilicus. MSRE modern staged repair of exstrophy

through the neoumbilicus (Fig. 7) [10]. The rectus fascia is then approximated and the abdominal wall closed. Stage II of MSRE is an epispadias repair in boys, typically the modified Cantwell–Ransley repair. The urethral plate is dissected off the paired corpora cavernosa after the foreskin is dissected along the ventral surface of the penis down to the

scrotum. The urethral plate is tubularized, typically over a stent or soft tube. The corporal bodies are then approximated in the midline dorsally, over the neourethra. In some instances, the surgeon advances the urethra to the tip of the penis if there is insufficient length. The ventral skin is then sutured to cover the corporal bodies (Fig. 8) [10].

Fig. 8 Stage II of MSRE, the modified Cantwell-Ramsey repair. a The urethral plate is dissected off the paired corpora cavernosa. b The urethral plate is tubularized over a stent. c The corporal bodies are approximated

in the midline dorsally, over the neourethra, moving the urethra to a more ventral position. d The ventral skin is then re-approximated over the corporal bodies. MSRE modern staged repair of exstrophy

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The Young–Dees–Leadbetter technique for bladder neck reconstruction forms a neourethra using a posterior median strip of mucosa that extends from the mid bladder trigone to the posterior urethra. Bladder muscle lateral to the median strip is denuded from underlying bladder mucosa to create flaps. The mucosal strip is tubularized and the raised muscle flaps are overlapped and sutured over the neourethra to reinforce the bladder neck. The bladder wall is closed and the bladder neck repair is suspended to the rectus fascia (Fig. 10) [10]. Bladder neck reconstruction results in an elevated bladder base.

Complete primary repair of exstrophy (CPRE) Fig. 9 Stage III of MSRE, bladder neck repair with cephalotrigonal ureteral reimplantation. Diagram shows how the distal ureters are dissected and reimplantated on or above the bladder trigone. MSRE modern staged repair of exstrophy

Stage III of MSRE includes bladder neck reconstruction, typically with ureteral reimplantation. Paired, bilateral longitudinal incisions are made at the level of the proximal urethra/ bladder neck and are carried cephalad. If ureteral reimplantation is performed, the ureters are reimplantated on or above the bladder trigone (cephalotrigonal) (Fig. 9).

Fig. 10 Bladder neck reconstruction using the Young–Dees–Leadbetter technique. a A posterior median strip is incised. Bladder muscle lateral to the median mucosal strip is denuded from underlying bladder mucosa to create mucosal flaps. b, c The mucosal strip is tubularized. d, e The raised

The objective of CPRE is to combine bladder closure and formal epispadias repair at the initial reconstruction. CPRE uses a slightly modified version of the bladder and abdominal wall closure described under stage I of MRSE, the main difference being that the initial incision in CPRE is carried onto the urethral plate as part of the planned concomitant epispadias repair. The urethral plate is separated from the corporal bodies and the urogenital diaphragm, as described for epispadias repair in stage II of MSRE. The epispadias repair follows the Mitchell technique or one of several of its modifications. The penis is disassembled into the right and left

muscle flaps are overlapped and sutured over the neourethra to reinforce the bladder neck. f The bladder wall is closed and the bladder neck repair is suspended to the rectus fascia

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corpora and the urethral plate. After the bladder is closed, the urethra is tubularized. If the urethra cannot be brought to the tip of the penis, it is placed in a hypospadiac position (Fig. 11) [11, 12]. One potential benefit of the CPRE approach is that of attaining earlier appropriate bladder outlet resistance, facilitating bladder cycling at a younger age and optimizing potential for bladder growth and development [13]. The CPRE approach has traditionally been performed within 72 h after birth; however there has been a recent shift in this practice by some surgeons, with repair now delayed until 2–3 months of age. Potential benefits of a delayed repair include somatic growth and organ system development, which reduces the risks associated with general anesthesia. Another benefit is the observed penile growth in boys secondary to the endogenous testosterone surge present in the first several months of life (Joseph Borer, personal communication). A planned delayed repair also allows the most experienced surgical team to preside, thus permitting the best possible surgical outcome. Potential downsides of delaying initial repair are the need for posterior iliac osteotomies in all infants and the potential for irritation of the bladder mucosa with development of squamous metaplasia. However, squamous metaplasia can be minimized with proper protection of the bladder plate. Although it was initially thought that children undergoing CPRE required only a single-stage reconstruction, many remain incontinent and later require bladder neck reconstruction [12, 14], at which time ureteral reimplantation can also be performed.

Iliac osteotomy

Fig. 11 The Mitchell epispadias repair method used in the complete primary repair of exstrophy (CPRE) approach. Diagram depicts axial (top row) and frontal views. a Initial appearance of the epispadiac urethra. b The urethral plate is separated from the corporal bodies. The penis is

disassembled into the right corpora, left corpora and the urethral plate. c The urethra is tubularized. d The penis is reassembled. If the urethra cannot be brought to the tip of the penis, it is placed in a hypospadiac position proximal to the glans

Several types of pelvic osteotomies have been developed. The first described was the bilateral posterior iliac osteotomy. Newer variations include bilateral superior pubic rami osteotomies, combined transverse innominate and vertical iliac osteotomy or anterior (transverse) innominate osteotomy alone [15, 16]. Pelvic osteotomies reduce pubic diastasis, which has many benefits. The decreased tension on the surgical repair reduces the incidence of bladder dehiscence. The bladder neck can be placed deep within the pelvis, improving bladder outlet resistance. The pelvic floor muscles are allowed to approach midline, where they can support the bladder neck and aid urinary continence [10]. In some cases iliac osteotomy is not performed, typically in infants younger than 72 h with pubic diastasis less than 4 cm. Sacroiliac ligament laxity at this age allows near approximation of the pubic bones with medial rotation of the greater trochanters.

Adjunct procedures Augmentation cystoplasty Augmentation cystoplasty can be considered in children who are not appropriate candidates for bladder neck reconstruction on the basis of poor bladder capacity or poor bladder compliance, and in those who fail to achieve continence or safe

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bladder storage characteristics following bladder neck reconstruction [10, 14]. Continence is defined as dry intervals of 3 h or more [17]. Augmentation cystoplasty can be combined with a catheterizable conduit. Options for bladder augmentation include enterocystoplasty (ileocystoplasty, sigmoidocystoplasty, right colocystoplasty, Mainz ileocecocystoplasty and gastrocystoplasty) as well as ureterocystoplasty [18]. Ileocystoplasty is by far the most popular option. Gastrocystoplasty is not commonly used secondary to metabolic complications such as hypochloremic metabolic alkalosis [19]. Ureterocystoplasty is only ideally suited for children with a markedly dilated ureter draining a poorly functioning or non-functioning kidney. The methods for small and large bowel enterocystoplasty are similar. The section of bowel is detubularized along its antimesenteric border, folded into a U, S or W shape and sutured to form a cup. The bladder is opened at the dome and a wide-mouth anastomosis is created between the bladder dome and the bowel segment [20]. Gastrocystoplasty is carried out by bringing a flap of isolated anterior and posterior stomach along with a gastroepiploic artery to the prepared bladder with subsequent anastomosis [20].

Catheterizable conduits Mitrofanoff Catheterizable conduits allow the bladder to be emptied independently from the urethra, offering children continence and easy access for catheterization. Appendicovesicostomy (Mitrofanoff) is the most commonly used channel. Other options include Yang–Monti ileovesicostomy (described below) and ureterovesicostomy. An appendicovesicostomy is created by first detaching the appendix from the cecum. The appendix forms a conduit through a submucosal bladder tunnel with the terminal end of the appendix attached to the bladder hiatus and the cecal end to a fascial opening at the stoma on the skin [21].

Yang–Monti ileovesicostomy If a suitable appendix is not present, the Yang-Monti ileovesicostomy is an ideal alternative. If performed at the time of bladder augmentation, a 3-cm segment of ileum is harvested from the distal end of the bowel used for augmentation. The segment is detubularized and then retubularized in an orthogonal plane. The technique for subsequent bladder and stomal anastomosis is similar to that used for appendicovesicostomy [21].

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Historical procedures for bladder exstrophy treatment Ureterosigmoidostomy was the first method of diversion used for patients with bladder exstrophy [22]. The ureters are divided at or below the common iliac arteries and each ureter is reimplanted into the teniae coli of the sigmoid colon using an antireflux technique [23]. This method has fallen out of favor because of complications including stone formation and increased risk of malignancy [24]. It does remain a surgical option in children for whom modern repair is not an option (e.g., those with bladder plates too small for closure) and in those who have had a failed exstrophy repair [10].

Clinical outcomes following exstrophy repair Continence, defined as dry intervals of 3 or more hours, is one of the primary goals of repair. Clinical outcomes in children following exstrophy repair vary across institutions depending on a number of factors including institution volume, surgeon experience, type of repair and definition of continence, making accurate comparison of clinical outcomes in these children challenging. A complete discussion of this topic is beyond the scope of this paper, but many authors have reviewed clinical outcomes following exstrophy repair and report on their clinical experience [25]. A review of the literature on this subject revealed a large variability in the achievement of continence among authors, with 10–80% of patients requiring bladder augmentation with or without intermittent catheterization following staged repair in order to achieve continence [25]. The same review reported 70–90% of patients undergoing complete primary repair achieving continence; however 15–90% of these patients required bladder neck reconstruction and up to 10% required bladder augmentation to achieve this goal [25].

Imaging the reconstructed urinary tract Because so few children are born with bladder exstrophy, guidelines for preoperative and postoperative imaging are not standardized. After the child is born, preoperative imaging can include a radiograph of the kidneys, ureters and bladder to assess the diastasis of the pubic symphysis and renal US examination to assess the kidneys, which are typically normal. It is not crucial to image the bladder plate because the surgical repair is based on the appearance of the bladder as seen on physical examination. After primary repair, voiding cystourethrograms (VCUGs) assess for reflux and complications of surgery. Ultrasonography is useful immediately after surgery and at 6-month and 1-

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Fig. 12 Pre- and postoperative appearances of the pelvis in a 19-monthold boy with bladder exstrophy. a Preoperative anteroposterior radiograph shows a wide pubic diastasis (straight arrows) and open book configuration of the pelvis. b Bladder exstrophy repair with anterior iliac

osteotomy. Anteroposterior radiograph shows the right diagonal innominate osteotomy (arrowhead). The pubic diastasis is decreased (straight arrows). Also note the suprapubic cystostomy catheter exiting through the neoumbilicus (short arrow)

year follow-up examinations to monitor for significant upper tract dilatation. 99mTc-dimercaptosuccinic acid (DMSA) scans are the gold standard to assess scarring, a dreaded complication of reflux and infections. MRI is useful for further definition of anatomy both preoperatively and postoperatively, and it is used experimentally in measuring pelvic angles to predict continence. Urodynamic testing at 3 years of age is useful for assessing bladder capacity and compliance. If there is concern for bladder perforation, US can first detect free fluid and then the defect is best visualized by CT or conventional cystograms. This section focuses on the normal post-operative findings for each of these modalities.

When visible, a linear band of sclerosis at the site of healing is most commonly appreciated (Fig. 13), though the osteotomy defect can be seen early on. In children who do not undergo iliac osteotomy, a lesser reduction in pubic diastasis is noted (Fig. 14).

Fluoroscopy VCUG is the mainstay of post-operative evaluation following bladder exstrophy repair. VCUG allows the assessment and surveillance of bladder capacity, the evaluation of complications and, in conjunction with a retrograde urethrogram, the evaluation of urethral integrity and patency. The grade of vesicoureteral reflux can also be assessed. The expected postoperative findings include iliac osteotomy defects with reduction in pubic diastasis, smallcapacity bladder, irregular bladder contour in most patients, elevation of the bladder base following bladder neck reconstruction and reflux through J-shape ureters (unless ureteral re-implantation has been performed).

Normal VCUG findings following bladder closure and bladder neck reconstruction Immediately following exstrophy repair, the typical findings are a small-capacity bladder with an irregular contour (Fig. 15) and vesicoureteral reflux into J-shape ureters (Fig. 16). Over time the bladder contour may become smooth (Fig. 17). The bladder capacity is typically smaller than age-predicted capacity. Therefore in the assessment of bladder capacity in these children the focus is on measuring growth in comparison to the child’s previous measurements. Most children who are

Osseous structures When iliac osteotomy is performed, the most striking observation should be the reduction in pubic diastasis. On a frontal radiograph of the pelvis, the transverse or diagonal innominate osteotomies are most clearly visible (Fig. 12). The vertical iliac osteotomy is more subtle.

Fig. 13 Postoperative appearance of the pelvis following bladder exstrophy repair with posterior iliac osteotomy in a 5-year-old boy, same child as in Fig. 4. Anteroposterior radiograph shows the significantly reduced pubic diastasis (white arrow). The healed posterior iliac osteotomies are subtle but can be seen as linear bands of sclerosis (black arrows)

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Fig. 14 Exstrophy repair in a 1-day-old boy without iliac osteotomy. a Preoperative frontal radiograph of the pelvis shows a wide pubic diastasis. b The pubic bones are slightly more approximated post-repair, which was accomplished by inward rotation of the pelvis. This position was held with sutures through the pubic bones

candidates for bladder neck reconstruction have a bladder capacity of about 100 cc. Immediately following bladder neck reconstruction, the expected postoperative findings are a temporary reduction in bladder capacity and elevated bladder base (Fig. 17).

conduit and bladder can result in an hourglass configuration of the neobladder (Fig. 20). The augmented segment often retains the appearance of the native bowel, with valvulae conniventes seen in ileocystoplasty, haustra in colocystoplasty (Fig. 21) and rugae in gastrocystoplasty (Fig. 22).

Urethra following epispadias repair Ultrasound The urethra is tubularized in both the Mitchell and the modified Cantwell–Ransley methods of epispadias repair. Therefore some irregularity of the urethral contour is normal as long as the urinary stream is normal (Fig. 18.) In some cases of Mitchell epispadias repair the urethra is brought into a hypospadiac position, so this is an expected postoperative appearance (Fig. 19).

Kidneys

Following augmentation cystoplasty, the urinary reservoir may no longer be spherical. Tapering between the augmented

Although congenital renal anomalies are more frequent in children with bladder exstrophy than in the general population (2.8% vs. 0.8%) [26], their overall occurrence is uncommon. Following exstrophy closure, children do, however, have vesicoureteral reflux that can lead to renal scarring as a result of recurrent pyelonephritis or obstructive uropathy following bladder neck reconstruction. Symmetrical, normal-appearing kidneys are the expected postoperative finding; however hydronephrosis can develop in some children following closure.

Fig. 15 Normal postoperative appearance of the bladder following exstrophy repair. VCUG in a 5-year-old boy following bladder exstrophy repair demonstrates a small-capacity bladder (wavy arrow) with an irregular contour. Bilateral vesicoureteral reflux is demonstrated (arrowheads). The suprapubic cystostomy catheter (arrow) was used for contrast agent administration. This is the same boy as in Figs. 4 and 13. VCUG voiding cystourethrogram

Fig. 16 Vesicoureteral reflux following exstrophy repair. VCUG in a 1month-old boy following exstrophy repair demonstrates bilateral grade II reflux (arrowheads) through J-shape ureters (arrows). Note the low insertion of the distal ureters near the bladder neck. VCUG voiding cystourethrogram

Normal postoperative VCUG findings following adjunct procedures

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Fig. 19 Urethral hypospadias in a 15-year-old boy post bladder exstrophy repair. Epispadias repair was performed using the complete penile disassembly technique. In this case, the urethra was brought into a hypospadiac position. VCUG shows the ventral position of the urethra (curved arrow). The urethra is short and thin with areas of irregularity (straight arrow). Also note the air-filled anteriorly positioned rectum, which partially courses beneath the bladder base (arrowhead). VCUG voiding cystourethrogram

Bladder

Fig. 17 Urinary bladder pre- and post-bladder neck reconstruction in a 6year-old boy who underwent CPRE at 1 day of age combined with ureteral reimplantation. Iliac osteotomies were not performed. a VCUG demonstrates a smooth bladder contour with a small bladder capacity of 130 cc (age-predicted bladder capacity 285 cc). There is free leakage through the urethra (arrow). No vesicoureteral reflux is demonstrated in this case because of the ureteral reimplantation. b Following bladder neck reconstruction, note the reduction in bladder volume and elevation of the bladder base (arrow). CPRE complete primary repair of exstrophy, VCUG voiding cystourethrogram

Fig. 18 Normal appearance of the urethra following CPRE. a VCUG in an 8-year-old boy shows voiding through the neourethra, with a short and narrow urethra but a good urine stream. b VCUG in an 11-month-old boy

The newly repaired exstrophied bladder can have varying appearances depending upon the degree of bladder distention. In most cases there is irregularity of the bladder wall as is seen on US imaging (Fig. 23). Areas of bladder wall thickening are also common (Fig. 24). Over-estimation of bladder wall thickening can occur when the bladder is under-distended. If new bladder wall thickening is a concern, for malignancy reassessment with a full bladder is recommended though challenging in these children, who are often incontinent. Cystoscopy is helpful when there is concern or when US imaging is equivocal. Bladder volume measurements can be estimated during sonography, although more precise measurement of full bladder capacity is obtained during urodynamics and VCUG. Bladder volume is measured by obtaining

following CPRE at 1 day of age with a diffusely irregular anterior urethra with good stream. Note the tip of the phallus (arrow). CPRE complete primary repair of exstrophy, VCUG voiding cystourethrogram

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Fig. 20 Ileocystoplasty. Cystogram in a 10-year-old boy following ileocystoplasty. The detubularized ileal segment is anastomosed to the dome of the urinary bladder. Note the wide communication between the bladder and the ileal segment (arrows), as well as the hourglass configuration of the neobladder

dimensions of the bladder in three planes and entering the numbers into the volume calculator on the US unit or using relatively reliable equations [27]. Comparison is made with the expected bladder capacity, which can be found in population-based charts [28]. Measurement of a post-void residual volume is useful, particularly if there is concern for bladder outlet obstruction or overflow incontinence. In children suspected of having bladder perforation, sonography easily demonstrates the presence of urinary ascites. The exact location of the perforation can then be evaluated by fluoroscopic or CT cystography.

Fig. 22 Gastrocystoplasty in a 10-year-old boy. a Note the gastric rugae (arrow), which are best appreciated prior to distention of the augmented segment of stomach on these cystogram images. b Gastrocystoplasty distended with contrast solution

Augmented bladder Children with augmented urinary bladders have a more lobulated bladder contour with characteristic gut signature (Fig. 25) of alternating mucosal and muscular layers.

Fig. 21 Colocystoplasty. Cystogram shows a normal postoperative appearance following bladder augmentation utilizing a colon conduit in a 15year-old girl. Note the wide communication between the native bladder and colon conduit (arrows.) The girl also has an appendicovesicostomy (Mitrofanoff) accessed via an umbilical stoma

Fig. 23 Bladder wall irregularity. Transverse gray-scale bladder US in a 13-year-old boy shows irregularity of the midline anterior bladder wall (arrow), attributed to the bladder exstrophy closure

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Fig. 24 Bladder wall thickening. Transverse gray-scale US image of the bladder in an 18-month-old girl demonstrates irregularity and thickening of the bladder wall, in this case more apparent along the posterior wall (arrow)

Debris or mucus can often be seen within the lumen (Fig. 26).

Fig. 26 Echogenic mucus. US shows augmented bladder containing echogenic mucus (arrow) in a 21-year-old woman

MRI

before and after bladder exstrophy repair and of those measurements obtained, a reduction in the iliac wing angle and increase in the ischial and obturator internus angles were seen following closure and were thought to be surrogate markers for improvement in the open book configuration of the pelvis and were suggestive in predicting which children would achieve continence following CPRE (Figs. 27, 28 and 29) [30]. Pelvic MRI also demonstrates the muscular redistribu-

MRI is not widely used clinically but has been studied in the preoperative and postoperative evaluation of children with bladder exstrophy to evalute the genitourinary tract, pelvic bones and pelvic floor muscles, though little has been written on this subject because the disease is rare and was until recently generally repaired within the first 72 h after birth, before a preoperative MRI could be obtained. MRI studies have shown that children with repaired bladder exstrophy have wider symphyseal diastasis, more divergent levator ani (greater puborectalis angle), a flatter pelvic floor and more anteriorly displaced anus [29] than age-matched controls. Multiple pelvic measurements have been studied in children

Fig. 25 Characteristic gut signature in ileocystoplasty. Transverse gray-scale US image of an augmented bladder in a 12-year-old boy shows an irregular bladder contour with characteristic gut signature. Note the inner hyperechoic mucosal layer (arrowhead) and the hypoechoic muscular layer (arrow)

Fig. 27 Preoperative and postoperative iliac wing angle measurements in a 3-month-old boy. a Axial proton-density MR image through the pelvis shows iliac wing measurements taken by placing lines across the flattest portion of the anterior cortex of the iliac wings at the inferior aspect of the sacroiliac joints. b Postoperative MR measurement shows a reduced iliac wing angle

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Fig. 28 Preoperative and postoperative ischial angle measurements in a 3-month-old boy. a Axial proton-density MR image through the pelvis shows ischial angle measurements taken by drawing lines along the medial cortex of the right and left ischium. b Postoperative MR measurement shows an increased ischial angle

tion of the pelvic floor following bladder exstrophy repair, which is similar in children whether CPRE was performed with or without iliac osteotomy [31]. Imaging of complications following bladder exstrophy repair Several complications can occur after bladder exstrophy repair. These include recurrent pyelonephritis, wound dehiscence, bladder rupture, urethrocutaneous fistula and urethral stricture [32]. Complications specific to augmented bladders include bladder rupture, stone formation, inadequate detubularization of the bowel segment resulting in augmented bladder spasm and, rarely, malignancy. After bladder diversion, children commonly develop stones and are at higher risk of developing malignancy [33]. Though complications following exstrophy repair are seen using many different imaging modalities, the following discussion is organized by the most common methods used. Fluoroscopy

initial repair in CPRE or MSRE, following epispadias repair in MSRE, or following bladder neck reconstruction, and is usually suspected clinically and then confirmed by VCUG. It is helpful to place a BB or radiopaque marker at the site of suspected leak. The fistula tract is often difficult to document and use of magnification, oblique position and short bursts of continuous fluoroscopy are helpful. The dorsal aspect of the proximal penile urethra or the penopubic junction is the most common location for a urethrocutaneous fistula (Fig. 30), which typically closes spontaneously with prolonged diversion of the urinary stream by a suprapubic catheter. Those that do not heal after a waiting period of up to 6 months require surgical repair. One pitfall is the simulation of a urethrocutaneous fistula by contrast pooling between the mons and base of the penis (Fig. 31). Because of the shortened phallus and recumbent position of the child during the exam, contrast agent pools in this location. This can be avoided by pointing the phallus downward and keeping this area dry during the exam. Careful, direct visual inspection and review of the images for lack of communication between the pooled contrast agent and the urethra should help exclude a urethrocutaneous fistula.

Urethrocutaneous fistula

Urethral stricture

A urethrocutaneous fistula is one of the most common complications after exstrophy repair. This can develop following the

Urethral stricture is another common complication following bladder exstrophy and epispadias repair and can present

Fig. 29 Preoperative and postoperative pubic diastasis measurements in a 3-month-old boy. Axial proton-density MR images of the pelvis before and after bladder exstrophy repair. a The degree of symphyseal diastasis is measured by drawing a line between the medial surface of the pubic bones. Preoperative bladder plate (white arrows); distal ureters (black arrows). b Note the reduced pubic diastasis from 47 mm to 14 mm

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Fig. 30 Urethrocutaneous fistula. a VCUG via suprapubic cystostomy catheter during the voiding phase in a 1-month-old boy. A radiopaque marker is placed at the dorsal aspect of the base of the penis at the site of the suspected leak. Note the extravasation of contrast agent from the dorsal aspect of the proximal penile urethra (straight arrow). The normal penile urethra is denoted by the arrowhead. Bilateral J-shape distal ureters

with vesicoureteral reflux (curved arrow) are present. b VCUG via suprapubic cystostomy catheter performed 3 weeks later following continued bladder decompression demonstrates resolution of the urethrocutaneous fistula. A smooth, normal-appearing urethra is seen (wavy arrow). Reflux into J-shape distal ureters is again noted (curved arrow). VCUG voiding cystourethrogram

at any time from early in the postoperative period to years later. Children typically present with obstructive symptoms such as reduced urinary stream, urinary retention or straining to void [32]. Children who perform clean intermittent catheterization (CIC) present with difficulty or inability to pass the catheter. Urethral strictures can be evaluated by VCUG and retrograde urethrogram. On VCUG, dilatation of the proximal urethra with an abrupt caliber change in the distal urethra is typical. During retrograde urethrography, care must be taken not to forcefully insert the catheter and disrupt the urethra if resistance from a stricture is encountered. Varying degrees of stricture formation can be seen after contrast agent is administered (Figs. 32 and 33). Complications of urethral stricture include urethral diverticula and subsequent stone formation (Fig. 34).

Bladder rupture/perforation

Fig. 31 Simulation of urethrocutaneous fistula, an imaging pitfall. VCUG during the voiding phase shows contrast material pooling at the base of the penis (arrow), simulating a fistula; however note the communication with contrast pooling along the glans from the tip of the penis and lack of communication with the urethra. This image was obtained during same examination as in Fig. 30b. VCUG voiding cystourethrogram

Fig. 32 Recurrent high-grade stricture involving the proximal portion of the anterior urethra. Oblique retrograde urethrogram image in a 20-yearold man with a small catheter positioned in the penile urethra. A tight stricture is demonstrated at the proximal portion of the anterior urethra (arrow). A retrograde urethrogram performed when the patient was 17 years old (not shown) had a similar appearance

Bladder rupture is a life-threatening emergency that can occur immediately or as a delayed complication in children with primary bladder exstrophy repair or augmentation cystoplasty. High bladder pressure is a risk factor for this complication and can result from bladder overdistention secondary to high bladder outlet resistance or in children who are noncompliant with a prescribed voiding or catheterization regimen. Spontaneous rupture occurs in 13% of children with an augmentation cystoplasty, and it is usually seen posteriorly along the anastomosis. Bladder perforation can also occur as a result of difficult self-catheterization in children with or without augmentation.

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The first imaging modality to assess for bladder perforation is sonography. New free fluid is ominous for bladder perforation, in the absence of other causes. Fluoroscopic or CT cystogram are useful for confirmation. In either modality, the bladder should be filled passively with contrast agent. During VCUG imaging should occur in the anterior and lateral positions followed by repeat imaging after the bladder has been emptied. Because the most common location of bladder perforation in an augmented bladder is posteriorly along the anastamosis, lateral imaging is crucial. Bladder perforation is well imaged with CT cystogram. A precontrast scan of the pelvis is performed followed by a scan of the pelvis after instillation of water-soluble contrast material into the bladder. Intra-peritoneal bladder rupture is seen as focal extravasation of contrast agent from the bladder or an increase in the attenuation of peritoneal fluid following contrast administration (Fig. 35). Some may choose to only use a post-contrast CT cystogram for the evaluation of extravasation. Complications of bladder augmentation

Fig. 33 High-grade stricture of the distal penile urethra in a 12-year-old boy. a A 5-French pediatric feeding tube could not be passed beyond the distal penile urethra. On retrograde urethrography, contrast medium opacifies only the distal-most 1.5 cm of the urethra. b A fistula tip then used to form a seal with the urethral meatus still fails to overcome the obstruction and results in intravasation (arrow) of contrast agent. Note: We prefer the use of a fistula tip rather than an inflated foley balloon in the urethral meatus but both serve the same purpose

If the bowel segment used for augmentation is not detubularized, excessive contraction can occur, limiting its reserve capacity and in some cases producing painful spasms. Excessive contraction or delayed filling of the bladder segment can be seen using VCUG (Fig. 36). Ultrasound Renal scarring Nearly 100% of children with bladder exstrophy develop vesicoureteral reflux following closure. This can be

Fig. 34 Complications of urethral stricture, including urethral stricture, diverticula and urethroperineal fistula. a Antegrade VCUG in a 3-yearold boy with multiple prior urethral strictures. Note the lobulated contour of the urethra, with multiple saccular diverticula in the proximal urethra (arrowhead) and a more normal-caliber distal urethra (white arrow). A urethroperineal fistula is also present (black arrow). b The same boy, now 8 years of age and following repair of urethral stricture and

urethroperineal fistula. VCUG, performed with a catheter in the penile urethra because of inability to pass catheter into the bladder, shows that the posterior urethra has a lobulated contour with multiple urethral diverticula (arrowhead). A urethroperineal fistula (long arrow) is seen between a stone containing urethral diverticulum (short arrow) and the perineum. VCUG voiding cystourethrogram

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Fig. 35 Intraperitoneal bladder rupture. a Axial CT cystogram demonstrates an intraperitoneal bladder rupture in a 16-year-old boy following self-catheterization. Note the intraperitoneal contrast agent (black arrow). b There is a focal area of contrast extravasation from the bladder dome (white arrow) on coronal reconstruction

exacerbated by bladder outlet obstruction or urethral stricture. The increased bladder pressures are transmitted to the upper tracts and sonography shows relatively large post-void residual and worsening hydroureteronephrosis, which improves when the bladder is emptied. Clinically these children can have overflow incontinence, as well, which can be associated with a larger-than-expected bladder volume if longstanding. Reflux nephropathy or renal scarring can develop as a result of high-pressure reflux secondary to bladder outlet obstruction or recurrent pyelonephritis. This is seen as diffuse cortical thinning and loss of corticomedullary differentiation or focal areas of renal scarring (Fig. 37). Most children with

reflux are placed on prophylactic antibiotics and undergo surgical intervention if they continue to have breakthrough infections. 99mTc-dimercaptosuccinic acid single photon-emission computed tomography (DMSA SPECT) is a useful exam for confirming renal cortical damage by demonstrating focal cortical defects (Fig. 37).

Fig. 36 Augmentation colocystoplasty with a non-detubularized segment of bowel. This 21-year-old woman presented with recurrent crampy pelvic pain. a VCUG demonstrates opacification of the native bladder. Contrast agent within the bowel segment (arrows) is only faintly seen

secondary to dilution from retained urine. b Delayed image demonstrates a tight narrowing (wavy arrows) between the bladder and the colonic segment, which filled much more slowly. The colonic segment was acting more like a diverticulum than a reservoir

Stone formation Stone formation in augmented bladders can be seen at sonography as echogenic mobile masses with posterior acoustic shadowing (Fig. 38). They can be distinguised from mucous

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masses, which are non-shadowing, mobile and isoechoic. Plain films and CT also commonly demonstrate stones (Fig. 39).

MRI MRI is not commonly used to image postoperative complications of bladder exstrophy repair. Complications secondary to iliac osteotomy rarely occur. MRI, as stated in previous sections, is utilized primarily in a research capacity to evaluate pelvic anatomy changes following repair. Its clinical utility remains under investigation.

Miscellaneous complications Bladder malignancy

Fig. 37 Renal cortical scarring in a 15-year-old girl. a Sagittal gray-scale US image of the left kidney demonstrates a focal area of scarring in the upper to mid pole (arrow). b Posterior 99mTc-dimercaptosuccinic acid single photonemission computed tomography (DMSA SPECT) scan confirms a focal cortical defect in the upper to mid pole of the left kidney (arrow)

Fig. 38 Neobladder with stone formation in a 21-year-old woman with an ileocecocystoplasty. Neobladder containing an echogenic stone (black arrow) with posterior acoustic shadowing and adjacent mucus (white arrow). Calipers measure stone

Bladder malignancy, most commonly adenocarcinoma, in children with bladder exstrophy occurs rarely in the present day of early primary repair. Squamous cell carcinoma is the second most common pathology and is thought to occur on a background of squamous metaplasia. It is far more common for malignancy to occur in children with bladder diversion than in children with primary repair. Vigilance for changes that indicate the possibility of bladder malignancy in such children is required for early detection. These changes include the presence of new immobile bladder masses, bladder wall thickening in an adequately distended bladder and new unexplained hydronephrosis (Fig. 40).

Fig. 39 Neobladder with stone formation. Pelvic radiograph obtained in a 21-year-old woman (same patient in Fig. 28) demonstrates multiple radiopaque structures (arrows) projecting in the right hemipelvis. These were confirmed by US as bladder calculi

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Fig. 40 Bladder malignancy in an 18-year-old woman with history of bladder exstrophy repair in infancy. a US shows normal right kidney. b Routine surveillance US 6 months later shows new-onset right-side hydronephrosis. This was later determined to be caused by squamous cell carcinoma of the bladder. The urinary bladder (not shown) was non-distended and could not be adequately imaged. c Axial T2-W HASTE and (d) axial VIBE post-contrast MR images demonstrate a lobulated softtissue bladder mass with heterogeneous postcontrast enhancement (arrows) HASTE half-Fourier acquisition singleshot turbo spin-echo, VIBE volumetric interpolated breath hold examination

Conclusion Bladder exstrophy is a rare congenital abnormality with a complex surgical repair regardless of the approach. Imaging plays a key role in the follow-up of these patients. Therefore an understanding of the surgical techniques and the normal postoperative appearances of bladder exstrophy repair and familiarity with the imaging appearance of complications are essential for the pediatric radiologist and pediatric urologist.

Conflicts of interest None

References 1. Kluth D, Hillen M, Lambrecht W (1995) The principles of normal and abnormal hindgut development. J Pediatr Surg 30:1143–1147 2. Paidas CN, Morreale RF, Holoski KM et al (1999) Septation and differentiation of the embryonic human cloaca. J Pediatr Surg 34: 877–884 3. Penington EC, Hutson JM (2003) The absence of lateral fusion in cloacal partition. J Pediatr Surg 38:1287–1295 4. Wang C, Wang J, Borer JG et al (2013) Embryonic origin and remodeling of the urinary and digestive outlets. PLoS One 8:e55587 5. Ambrose SS, O’Brien DP 3rd (1974) Surgical embryology of the exstrophy–epispadias complex. Surg Clin N Am 54:1379–1390 6. Muecke EC (1964) The role of the cloacal membrane in exstrophy: the first successful experimental study. J Urol 92:659–667

7. Young RH (2008) Non-neoplastic disorders of the urinary bladder. In: Bostic DG, Cheng L (eds) Urologic surgical pathology. Mosby, China, pp 215–256 8. Sponseller PD, Bisson LJ, Gearhart JP et al (1995) The anatomy of the pelvis in the exstrophy complex. J Bone Joint Surg Am 77:177–189 9. Stec AA, Pannu HK, Tadros YE et al (2001) Pelvic floor anatomy in classic bladder exstrophy using 3-dimensional computerized tomography: initial insights. J Urol 166:1444–1449 10. Gearhart JP, Mathews RI (2011) Exstrophy–epispadias complex. In: Wein AJ, Kavoussi LR, Novick AC et al (eds) Campbell-Walsh urology. W. B. Saunders, Philadelphia, pp 3326–3378 11. Grady RW, Mitchell ME (1999) Complete primary repair of exstrophy. J Urol 162:1415–1420 12. Borer JG, Gargollo PC, Hendren WH et al (2005) Early outcome following complete primary repair of bladder exstrophy in the newborn. J Urol 174:1674–1678, discussion 1678–1679 13. Borer JG, Gargollo PC, Kinnamon DD et al (2005) Bladder growth and development after complete primary repair of bladder exstrophy in the newborn with comparison to staged approach. J Urol 174: 1553–1557, discussion 1557–1558 14. Gargollo P, Hendren WH, Diamond DA et al (2011) Bladder neck reconstruction is often necessary after complete primary repair of exstrophy. J Urol 185:2563–2571 15. Purves JT, Gearhart JP (2007) Pelvic osteotomy in the modern treatment of the exstrophy–epispadias complex. EAU-EBU Updat Ser 5:188–196 16. Wild AT, Sponseller PD, Stec AA et al (2011) The role of osteotomy in surgical repair of bladder exstrophy. Semin Pediatr Surg 20:71–78 17. Lloyd JC, Spano SM, Ross SS et al (2012) How dry is dry? A review of definitions of continence in the contemporary exstrophy/ epispadias literature. J Urol 188:1900–1904 18. Pohl HG (2010) Augmentation cystoplasty in children. In: Graham SD, Keane TE, Glenn JF (eds) Glenn’s urologic surgery. Lippincott Williams & Wilkins, Philadelphia, pp 784–792

786 19. Mingin GC, Stock JA, Hanna MK (1999) Gastrocystoplasty: longterm complications in 22 patients. J Urol 162:1122–1125 20. Rao PK, Iverson AJ, Sabanegh ES (2012) Augmentation cystoplasty technique. http://emedicine.medscape.com/article/443916-technique. Accessed 16 Dec 2013 21. Cain M (2010) The Mitrofanoff in pediatric urinary tract reconstruction. In: Graham SD, Keane TE, Glenn JF (eds) Glenn’s urologic surgery. Lippincott Williams & Wilkins, Philadelphia, pp 794–799 22. Simon J (1852) Ectopia vesicae (absence of the anterior walls of the bladder and pubic abdominal parietes): operation for diverting the orifices of the ureters into the rectum, temporary success, subsequent death, autopsy. Lancet 2:568–570 23. Kiarash M, deKernion JB (2002) Urinary diversions and continent reservoirs. In: Gillenwater JY, Howards SS, Grayhack JT, Duckett JW (eds) Adult and pediatric urology. Lippincott Williams & Wilkins, Philadelphia, pp 1363–1400 24. Pettersson L, Tranberg L, Abrahamsson K et al (2013) Half century of followup after ureterosigmoidostomy performed in early childhood. J Urol 189:1870–1875 25. Husmann DA (2006) Surgery insight: advantages and pitfalls of surgical techniques for the correction of bladder exstrophy. Nat Clin Pract Urol 3:95–100 26. Stec AA, Baradaran N, Gearhart JP (2012) Congenital renal anomalies in patients with classic bladder exstrophy. Urology 79:207–209

Pediatr Radiol (2014) 44:768–786 27. McGrath D. Bladder volume calculator. http://users.tpg.com.au/ mcgrath_/Calculators/Bladder_Volume_Calculator.html. Accessed 16 Dec 2013 28. Kaefer M, Zurakowski D, Bauer SB et al (1997) Estimating normal bladder capacity in children. J Urol 158:2261–2264 29. Halachmi S, Farhat W, Konen O et al (2003) Pelvic floor magnetic resonance imaging after neonatal single stage reconstruction in male patients with classic bladder exstrophy. J Urol 170:1505–1509 30. Gargollo PC, Borer JG, Retik AB et al (2005) Magnetic resonance imaging of pelvic musculoskeletal and genitourinary anatomy in patients before and after complete primary repair of bladder exstrophy. J Urol 174:1559–1566, discussion 1566 31. Stec AA, Tekes A, Ertan G et al (2012) Evaluation of pelvic floor muscular redistribution after primary closure of classic bladder exstrophy by 3-dimensional magnetic resonance imaging. J Urol 188:1535–1542 32. Borer JG, Retik AB (2007) Complications of exstrophy and epispadias surgery. In: Loughlin KR (ed) Complications of urologic surgery and practice: diagnosis, prevention and management. Informa Healthcare, New York, pp 295–300 33. Higuchi TT, Granberg CF, Fox JA et al (2010) Augmentation cystoplasty and risk of neoplasia: fact, fiction and controversy. J Urol 184:2492–2496