Fetal MRI of cloacal exstrophy - Springer Link

4 downloads 0 Views 789KB Size Report
Nov 27, 2012 - Maria A. Calvo-Garcia & Beth M. Kline-Fath & Eva I. Rubio &. Arnold C. ...... Saguintaah M, Couture A, Veyrac C et al (2002) MRI of the fetal.
Pediatr Radiol (2013) 43:593–604 DOI 10.1007/s00247-012-2571-3

ORIGINAL ARTICLE

Fetal MRI of cloacal exstrophy Maria A. Calvo-Garcia & Beth M. Kline-Fath & Eva I. Rubio & Arnold C. Merrow & Carolina V. Guimaraes & Foong-Yen Lim

Received: 22 June 2012 / Revised: 21 September 2012 / Accepted: 27 September 2012 / Published online: 27 November 2012 # Springer-Verlag Berlin Heidelberg 2012

Abstract Background Prenatal ultrasonographic (US) diagnosis of cloacal exstrophy (CE) is challenging. Objective To define the fetal MRI findings in CE. Materials and methods We performed a retrospective review of eight patients with CE. Imaging was performed between 22 weeks and 36 weeks of gestation with US in four and MRI in eight fetuses. Abdominal wall, gastrointestinal/genitourinary, and spine and limb abnormalities detected were compared with postnatal evaluation. Results US failed to display CE in one of the four fetuses. Fetal MRI confirmed CE in all eight fetuses by demonstrating absence of a normal bladder and lack of meconium-filled rectum/colon, associated with protuberant pelvic contour and omphalocele. These findings correlated postnatally with CE, atretic hindgut and omphalocele. One fetus had imaging before rupture of the cloacal membrane, showing a protruding pelvic cyst. Absent bladder was noted in the remaining seven fetuses. Confirmed skin-covered spinal defects were noted in seven fetuses, low conus/tethered cord in one and clubfoot in three. Six fetuses had renal M. A. Calvo-Garcia (*) : B. M. Kline-Fath : A. C. Merrow Department of Radiology, Cincinnati Children’s Hospital Medical Center, 3333 Burnet Ave., MLC 5031, Cincinnati, OH 45229-3039, USA e-mail: [email protected] E. I. Rubio Department of Radiology, Children’s National Medical Center, Washington, DC, USA C. V. Guimaraes Department of Radiology, Nemours Children’s Hospital, Orlando, FL, USA F.-Y. Lim Pediatric Surgery and Fetal Care Center of Cincinnati, Cincinnati Children’s Hospital Medical Center, Cincinnati, OH, USA

anomalies, two had hydrocolpos and one had ambiguous genitalia. Conclusion Fetal MRI provides a confident diagnosis of CE when a normal bladder is not identified, there is a protuberant abdominopelvic contour and there is absence of meconiumfilled rectum and colon. Genitourinary and spinal malformations are common associations. Keywords Cloacal exstrophy . OEIS . Prenatal diagnosis . Fetal MRI . Anorectal malformation

Introduction Cloacal exstrophy, also known as the OEIS complex (omphalocele, cloacal exstrophy, imperforate anus, spinal defects), is one of the rarest and most complex anorectal and urogenital malformations with a reported incidence of one in 200,000 to 400,000 births [1]. The entity includes the persistence and exstrophy of a common cloaca that receives ureters, ileum and a rudimentary blind-ending hindgut (Fig. 1). It is commonly associated with omphalocele, spinal dysraphism and incompletely formed external genitalia, and is always associated with imperforate anus [2]. This entity is different from bladder exstrophy (Fig. 2), in which imperforate anus and spinal anomalies are rare [3, 4]. In the past, various authors have confused the nomenclature as they have used the term OEIS complex to describe cases of what most likely represented limb–body wall complex or bladder exstrophy [3, 5, 6]. Carey [6] clarified that cloacal exstrophy and the OEIS complex are the same process and should therefore be used synonymously. A prenatal diagnosis of cloacal exstrophy with ultrasonography (US) is challenging, as cases are often misdiagnosed as omphalocele or gastroschisis and in some instances a differential diagnosis of bladder exstrophy or cloacal exstrophy is

594

Pediatr Radiol (2013) 43:593–604

Fig. 1 Diagrams of typical anatomical appearances of cloacal exstrophy without (a) and with (b) prolapsed terminal ileum. The cecum is located between two hemibladders and is open, as are the exstrophied hemibladders. The terminal ileum enters the back of the cecal wall and can prolapse. The rudimentary colon extends from the cecal plate and ends blindly in the abdomen or pelvis

provided [7–9]. Because survival and outcome are different for each of these malformations, a confident prenatal diagnosis is essential as it allows improved parental counseling in the presence of colorectal surgeons and pediatric urologists and may guide the selection of site for delivery. The literature on prenatal diagnosis of cloacal exstrophy is limited and only a few cases have been described with the aid of fetal MRI, though they lack detailed descriptions of the appearance of the gastrointestinal tract or of the complete spectrum of encompassing malformations [9–12]. The purpose of this paper is to define the fetal MRI findings in cloacal exstrophy to improve its detection so that a confident prenatal diagnosis can be provided.

Materials and methods This study was approved by the internal review board at our institution and patient written consent was waived.

Fig. 2 Diagram of the typical anatomical appearance of bladder exstrophy. The posterior bladder wall mucosa, which can have variable size, is exposed through a lower abdominal wall defect. The umbilical cord insertion is lower than normal and located close to the superior margin of the exstrophic bladder

We performed a retrospective review in eight patients with cloacal exstrophy prenatally evaluated and subsequently treated at our institution. All pregnancies were referred for evaluation of abnormalities detected by level II prenatal US at other centers with their reports available. Nine fetal MRI scans were performed in eight fetuses between 22 and 36 weeks’ gestational age (mean: 28 weeks). One fetus with giant omphalocele and complete extracorporeal liver had a second MRI scan at 33 weeks for reassessment of lung volumes. Four patients also had a level II US scan on the same day as the fetal MRI scan. MRI studies were obtained utilizing a phase array body coil in a 1.5-T scanner (Horizon; GE Healthcare, Milwaukee, WI) with a matrix of 224×192 or 256×256, a field-of-view of 30 cm or less when possible and 3- or 4-mm thick contiguous slices (5 mm for T1-W FSPGR). The following sequences were obtained in three orthogonal planes for each fetus: T2-W, single-shot fast spin-echo (SSFSE), 2-D fast imaging employing steady-state acquisition (FIESTA) and fast gradient echo T1-W FSPGR. In two fetuses (cases 6 and 7), a heavily T2-W hydrography sequence (MR fetography) was also utilized. No maternal or fetal sedation was required. US examinations were performed using a GE Voluson E8 (General Electric Medical Systems, Milwaukee, WI). The analysis focused on the anterior abdominal and pelvic wall (including the size and position of the omphalocele and the appearance of the region of exstrophy), the gastrointestinal and genitourinary tracts, spine/CNS defects, lower limb deformities and external genitalia. The number of vessels in the umbilical cord and amniotic fluid index were also recorded. The fetal MRI findings were compared with postnatal clinical, radiological (plain films, sonograms and spine MRI) and surgical evaluations. Imaging findings on the four cases with a same-day US scan were reviewed and compared to assess concordance and potential impact on clinical care. Chromosome analysis was available at the time of the work-up in six of the pregnancies (unknown in cases 2 and 6) and repeated at birth (confirming six children as 46,XX and two children as 46,XY karyotype). The presumed diagnosis at the time of referral and after the fetal MRI, as well as the gestational age at the time of imaging and delivery, were also recorded. These data are summarized in Table 1.

Pediatr Radiol (2013) 43:593–604

595

Table 1 Fetal MRI findings in eight fetuses with cloacal exstrophy with postnatal correlation Case no.

1

Karyotype

46,XX

Gestational age (weeks) At imaging

At birth

23

34

Prenatal findings

Covered exstrophy: protruding pelvic cyst with debris No prolapsed terminal ileum Absent meconium in rectum/colon Small and low omphalocele

2

3

46,XY

46,XX

31

27

33

36

Two neural tube defects, normal posterior fossa, clubfoot Right kidney duplex, bilateral hydroureteronephrosis Septated hydrocolpos, suggested female phenotype Absent bladder Protuberant anterior pelvic contour, no prolapsed terminal ileum Absent meconium in rectum/colon Small and low omphalocele No neural tube defect but low conus, normal posterior fossa +feet Normal kidneys Ambiguous genitalia (bifid scrotum) Absent bladder Prolapsed terminal ileum (±T2/T1) and bladder plates Absent meconium in rectum/colon Small and low omphalocele

4

46,XX

22

36

One neural tube defect, normal posterior fossa, clubfeet Pelvic/duplex left kidney, bilateral hydroureteronephrosis Suggested female phenotype Absent bladder Protuberant anterior pelvic contour, no prolapsed terminal ileum Absent meconium in rectum/colon Small and low omphalocele

5

46,XX

36

36

Two neural tube defects, normal posterior fossa +feet Left hydroureteronephrosis (prominent megaureter) Suggested female phenotype Absent bladder Prolapsed terminal ileum (±T2,↑T1), absent meconium in rectum/colon

Postnatal correlation

Omphalocele, exposed exstrophy +prolapsed terminal ileum Atretic blind-ending hindgut (11 cm length) Two skin-covered neural tube defects, normal posterior fossa, clubfoot Right kidney duplex, bilateral hydroureteronephrosis (bilateral distal ureteral stenosis) Two hemiuteri/vaginas, no hydrocolpos

Omphalocele +prolapsed terminal ileum Atretic blind-ending hindgut (7 cm length) Tethered cord with intradural lipoma, normal posterior fossa +feet Normal kidneys Ambiguous genitalia (phallus between bladder plates)

Omphalocele, no prolapsed terminal ileum (blind ending) Atretic blind-ending hindgut (8 cm length) One skin-covered neural tube defect, normal posterior fossa, clubfeet Pelvic/duplex left kidney, bilateral hydroureteronephrosis (ectopic +obstructive distal left ureter) Two hemiuteri +two vaginas (right obstructed distally), no hydrocolpos

Omphalocele, minimal terminal ileum mucosal prolapse Short atretic blind-ending hindgut (length not reported) Two skin-covered neural tube defects, normal posterior fossa, congenital right pes planus Left kidney cystic dysplasia +megaureter (left distal ureteral stenosis at surgery) Two hemiuteri +two vaginas (right not patent), no hydrocolpos

Omphalocele, prolapsed terminal ileum Short atretic blind-ending hindgut (length not reported)

596

Pediatr Radiol (2013) 43:593–604

Table 1 (continued) Case no.

Karyotype

Gestational age (weeks) At imaging

Prenatal findings

Postnatal correlation

At birth Small and low omphalocele

6

46,XX

24+33

36

Two neural tube defects, normal posterior fossa +feet Pelvic left kidney, right hydroureteronephrosis Suggested female phenotype Absent bladder Prolapsed terminal ileum (±T2,↑T1 rim of fluid) +bladder plates Absent meconium in rectum/colon Giant omphalocele

7

46,XX

25

32

Two large neural tube defects, hindbrain herniation (at 33 weeks) +normal feet Left hydroureteronephrosis Suggested female phenotype Absent bladder Prolapsed terminal ileum (↓T2,↑T1) + bladder plates Absent meconium in rectum/colon Small and low omphalocele

8

46,XY

31

34

One neural tube defect, normal posterior fossa +feet Right hydroureteronephrosis, cystic dysplasia left kidney Suggested female phenotype Absent bladder Prolapsed terminal ileum (±T2,↑T1 +rim of fluid) +bladder plates Absent meconium in rectum/colon

Small and low omphalocele One large neural tube defect, hindbrain herniation +clubfeet Normal kidneys External genitalia not well defined

Two skin-covered neural tube defects, normal posterior fossa +feet Pelvic left kidney, right hydroureteronephrosis Two hemiuteri +vaginas with stenotic orifices, small left hydrocolpos Omphalocele, prolapsed terminal ileum Short +duplicated atretic blind-ending hindgut (length not reported) Left hydroureteronephrosis (left distal ureteral stenosis at surgery) Demise prior to postnatal spine imaging. On physical examination: skin-covered lesion. Low 4th ventricle (head US) Two hemiuteri +vaginas, no hydrocolpos

Omphalocele +prolapsed terminal ileum Atretic blind-ending hindgut (8 cm length) One skin-covered neural tube defect, normal posterior fossa +feet Right hydroureteronephrosis, cystic dysplasia left kidney Two hemiuteri +vaginas (atretic right müllerian structures), no hydrocolpos

Omphalocele +prolapsed terminal ileum Atretic blind-ending hindgut (4 cm length) One large skin-covered neural tube defect, hindbrain herniation +development of hydrocephalus +clubfeet Normal kidneys Two small hemipenises

± Intermediate, ↑ high, ↓ low.

Results Anterior abdominal and pelvic wall assessment All fetuses had an omphalocele, which was small and low in seven and giant (with complete extracorporeal liver) in one. They all had a protuberant anterior pelvic

contour, correlating with the exstrophy and widely spaced pubic symphysis after birth (Figs. 3 and 4). Four of seven cases presenting with a prolapsed terminal ileum at birth demonstrated on fetal MRI an infraumbilical cord-like midline segment of soft tissue (cases 5, 6, 7 and 8). This tubular structure had varied signal (Table 1) and was protruding within the amniotic fluid from the area of abnormal

Pediatr Radiol (2013) 43:593–604

597

Fig. 3 Case 7, 25 weeks’ gestational age. a US axial image at the most inferior pelvis. There is a cord-like mass of echogenic soft tissue protruding from the anterior pelvic wall (short, dashed white arrow) resembling the trunk of an elephant and representing the prolapsed terminal ileum. Sagittal fetography (b) and T1-W (c) MRI sequences. There is a

protuberant anterior pelvic contour with a low omphalocele (white arrow), prolapsed terminal ileum (short, dashed white arrow) and absent meconium in the rectum/colon (long, white dashed arrow). Distal dysraphic defect (black arrow) and normal posterior fossa (short black arrow) are noted. The lower leg is denoted (asterisk) for orientation

anterior pelvic contour, as the equivalent of the elephant trunk-like finding seen on the US image (Fig. 3). Case 6 had the prolapsed loop on both the 24-week and 33-week examinations. The prolapsed bowel was not identified prospectively in case 2. On retrospective review of the MR images, there was a redundant umbilical cord in the expected location of the prolapsed loop, which prevented prenatal diagnosis. Case 4 had only minimal prolapse of the terminal

ileum mucosa, correlating in utero with an abnormal protuberant contour at the level of the exstrophy but no defined prolapsed loop (Fig. 5). Case 1 presented with a covered cloacal exstrophy at the time of work-up, but the exstrophy was exposed with a prolapsed terminal ileum at birth, supporting delayed rupture of the cloacal membrane. In this special situation, there was a large, thin-walled pelvic cyst, which represented the cloaca protruding caudal to the

Fig. 4 Case 7, postnatal findings. Frontal (a) and cross-table abdominal (b) radiographs. There is pubic symphysis diastasis (asterisks), low omphalocele (white arrow) and dysraphic defect (black arrow). c Sagittal T2-W lumbar spine MR image. The skin-covered lesion shows

mixed features between terminal myelocystocele and lipomyelomeningocele. There is central canal dilatation with distal trumpeting (asterisk) and the neural placode is tethered to subcutaneous fat (white dashed arrow)

598

Pediatr Radiol (2013) 43:593–604

Fig. 5 Case 4. Coronal (a) and sagittal (b) 2-D FIESTA MR images. There is an abnormal infraumbilical protuberant contour (black arrows). Note the mild extension of the liver into the low omphalocele (white arrowhead) as well as the left kidney (LK) hydroureteronephrosis

(dashed white arrow). c Photograph of the wall defect at birth. There is a small and low omphalocele (O); caudal to it on each side lie the two everted lateral bladder plates (h). There is a very subtle prolapse of the terminal ileum mucosa (black arrowhead). UC umbilical cord

abdominal cord insertion in the intact cloacal membrane. That cystic structure was outlined by the umbilical arteries and contained layering dark T2-weighted signal intensity content, as expected for meconium (Fig. 6). Case 3 had a short protruding tubular midline structure through the area of the exstrophy (Fig. 7) consistent with a prolapsed terminal ileum. However, this structure was not identified prior to referral or after birth, which is likely explained by its potentially intermittent nature. The exposed bladder plates were defined in four fetuses (cases 3, 6, 7 and 8) as two small, lateral soft tissue protuberances lying on either side of the prolapsed ileum. The ipsilateral distal ureter was visualized extending into its respective bladder plate in cases 3 and 6 (Fig. 7).

Gastrointestinal tract assessment

Fig. 6 Case 1. Cloacal exstrophy detected before rupture of the cloacal membrane. a US axial image through the pelvis. Axial SSFSE (b) and sagittal 2-D FIESTA (c) MR images. There is a thin-walled protruding anterior pelvic cyst (long white arrow) outlined by the umbilical arteries (UA) and with a small amount

of echogenic (a)/low T2-weighted signal intensity (b) layering content (white arrowhead). There is hydrocolpos (short white arrow in c) with right hydroureter (white dashed arrow) posterior to it. Distal neural tube defect (black arrowhead) is noted. UC umbilical cord

Meconium-filled bowel was only seen in the omphalocele and in the anterior mid to lower abdomen (Figs. 3 and 7). None of the fetuses had a normal meconium-filled colon and rectum, including both examinations performed at 24 and 33 weeks’ gestational age for case 6. This observation correlated with surgical findings of a blind-ending atretic hindgut extending from the area of the exstrophy, which contained mucous but no meconium. The hindgut length ranged from 4 cm to 11 cm. One fetus (case 3) had a dilated bowel at the level of the omphalocele and a prolapsed loop, and after birth, an obstructed blind-ending terminal ileum was found (Fig. 7).

Pediatr Radiol (2013) 43:593–604

599

Fig. 7 Case 3. Axial consecutive 2-D FIESTA images at the level of the exstrophy (a, b) and right (c) and left (d) sagittal 2-D FIESTA and sagittal midline T1-W (e) MR images. Distal ureters (dashed white arrows) are seen extending to the everted lateral bladder plates (short black arrows). There is a prolapsed midline loop (white arrow) caudal to an omphalocele (black asterisks). Also apparent are a distal neural tube defect (arrowhead), pelvic duplex left kidney (LK) and lower limb (white asterisk). UC umbilical cord

Genitourinary tract and external genitalia All of the pregnancies had normal amniotic fluid volumes. However, there was failure to visualize a normal bladder in all fetuses, making note of the case of cloacal exstrophy with delayed rupture of the cloacal membrane, in which a protruding infraumbilical pelvic cyst was identified. Hydronephrosis was detected in six fetuses and in four of these six, the distal ureters extended toward the ipsilateral anterior pelvic wall (cases 3, 4, 5 and 6; Figs. 5 and 7). Distal ureteral stenosis was found during surgery in three of these four cases (cases 3, 4 and 6), and one of the three (case 3) had ectopic ureteral insertion into ipsilateral müllerian structures. Renal ectopia was noted in three fetuses (cases 1, 3 and 5), renal duplication in two (cases 1 and 3) and unilateral cystic renal dysplasia in one (case 7). After birth, incipient cystic renal dysplasia was noted in one additional case (case 4). Normal

bilateral kidneys were present in only two cases (cases 2 and 8). The uterus was not detected in any of the six female fetuses. Hydrocolpos was present in cases 1 and 5 (Figs. 6 and 8). In one fetus (case 1), bilateral hydrocolpos was seen posterior to the covered exstrophy. In the other case, left hydrocolpos was seen protruding into the anterior pelvic contour. After birth, hydrocolpos only persisted in one neonate (case 5), remaining stable in size (Fig. 8). Overall, the sexual phenotype was difficult to define (Fig. 9). Only the most caudal portion of what resembled the labia majora could be defined in the six girls. After birth, the cleft clitoris and widely divided labia were present. In one boy (case 2), ambiguous genitalia was noted in conjunction with a bifid scrotum. In this case, the penis was found between the bladder plates at the time of surgery. The external genitalia could not be defined in the other boy, and postnatal examination revealed a widely divided scrotum with two small hemipenises.

600

Pediatr Radiol (2013) 43:593–604

Fig. 8 Case 5. Left parasagittal (a) and axial (b) SSFSE T2-W MR images and (c) postnatal US image on the first day of life. There is a left hydrocolpos (white arrow). Also apparent are a distal neural tube defect (arrowhead), lower limb (asterisk), left kidney (LK) and hemiuterus (dashed white arrow)

Spine/CNS assessment Distal dorsal neural tube defects were present in seven fetuses, correlating with skin-covered lesions at birth. All of these fetuses had elongation of the cord into a dorsal cyst at the level of the dysraphic defect. Five of these fetuses had small dorsal cysts and normal posterior fossa imaging (Fig. 3). In two fetuses, the dorsal cyst was very large and associated with herniation of the cerebellar tonsils below the foramen magnum (Fig. 10). Surgery was performed in five cases after birth (cases 1, 3, 5, 7 and 8). In these patients, there was a dysmorphic neural placode tethered to subcutaneous fat (as seen with lipomyelomeningocele) with or without distal trumpeting and hydromyelia (as expected with a terminal myelocystocele). Mixed features of both types of defects were seen in three cases (Figs. 3 and 4) while more dominant features of lipomyelomeningocele or terminal myelocystocele were Fig. 9 a Case 3. Axial 2-D FIESTA MR image immediately caudal to the exstrophy with suggested female external genitalia. Also apparent are the caudal portion of the bladder plates (short black arrows) and the tip of a prolapsed terminal ileum (dashed white arrow). b Case 2. Axial SSFSE FIESTA MR image immediately caudal to the exstrophy displaying a bifid scrotum (arrowheads)

noted in one patient each (cases 1 and 8, respectively) (Fig. 10). In addition to the above-described distal spinal dysraphic defect, a second higher skin-covered lesion with focal tethering of the cord was seen in four fetuses (cases 1, 4, 5 and 6) and confirmed after birth (Fig. 11). Clubfoot was present in three fetuses (cases 1, 3 and 8) and was bilateral in two (cases 3 and 8). One patient had congenital vertical talus, not identified in utero. One fetus (case 2) had no spinal dysraphic defect but a very low conus at the lumbosacral junction. This appearance correlated with a tethered cord with an intradural lipoma found on postnatal imaging. Additional findings A two-vessel cord was noted in six of the eight fetuses. Despite the presence of normal amniotic fluid volumes, all pregnancies developed preterm labor.

Pediatr Radiol (2013) 43:593–604

601

Fig. 10 Case 8. Sagittal SSFSE MR images at 34 weeks’ gestational age (a, b) and postnatal SSFSE MR image of the spine on the fourth day of life (c). There is a very large neural tube defect/dorsal cyst with dominant features of terminal myelocystocele. The caudal central canal

forms an expansile sac (asterisk) that herniates into an outer sac (arrowheads). There is an area of tethering into dorsal fatty tissue (black arrow) and associated hindbrain herniation below the foramen magnum (white arrow)

Change in diagnosis Prenatal diagnosis of cloacal exstrophy was considered only in four patients at the time of referral (cases 1, 5, 7 and 8). In the other four cases, the proposed diagnoses were omphalocele (case 2), giant omphalocele and spinal defect (case 6), omphalocele with renal and spinal anomalies (case 3) and sacrococcygeal teratoma (case 4). After the fetal MRI scan, cloacal exstrophy was prospectively considered in all of the cases, leading to improved multidisciplinary parental counseling. Cases 1, 3, 7 and 8 also had a repeat US scan at our institution on the same day as the fetal MRI scan. Case 3 was referred with a different diagnosis, and our US scan failed to

show the area of exstrophy. It was a challenging examination due to maternal body habitus and fetal positioning, but was clearly enhanced by the use of fetal MRI, providing a confident diagnosis and adequate counseling. The other three cases had the correct suspected diagnosis at the time of referral, and US and fetal MRI showed the elephant trunk-like image in cases 7 and 8 (Fig. 3) and a protruding cloaca/cloacal membrane in case 1 (Fig. 6). In case 7, the prolapsed terminal ileum was much easier to identify on MRI. In addition, fetal MRI provided improved evaluation of the gastrointestinal tract and a hydronephrotic pelvic kidney (case 3), allowed identification of a right megaureter as opposed to a fluid-filled rectum (case 1), and identified a

Fig. 11 Case 1. Coronal SSFSE (a) and axial 2-D FIESTA (b) MR images. There is a distal neural tube defect (arrowhead) and a second, upper level lesion with focal tethering of the cord (white arrow). c

Postnatal Axial T2-W MR image at the same level as (b) There is tethering of the cord and mild dilatation of the central canal just above it, consistent with abortive non-terminal myelocystocele

602

gallbladder contained in a low omphalocele that initially was thought to represent urachal anomaly or small bladder by US (case 7). In case 8, there was hindbrain herniation in association with a large dorsal dysraphic defect; MRI improved its assessment. Only fetal MRI allowed the identification of the hindgut anomaly in these patients.

Discussion Cloacal exstrophy is a severe and rare malformation thought to be a developmental field defect affecting the mesoderm that later will contribute to infraumbilical mesenchyme, urorectal septum and caudal vertebrae during early embryogenesis. This defect results in persistance and subsequent rupture of the cloacal membrane with prevention of normal anterior abdominal wall closure in combination with lack of septation of the primitive cloaca [3, 7]. This multisystem malformation represents the most severe form of the exstrophy-epispadias sequence ranging in severity from epispadias to bladder exstrophy to cloacal exstrophy. The underlying cause remains unknown, but genetic and environmental factors likely are contributory. It is thought that the earlier the presentation of the offending factor, the more severe the resulting malformation [4, 13, 14]. Cloacal exstrophy presents as an anterior abdominal wall defect with an opened and everted cecum between two everted hemibladders (Fig. 1). The terminal ileum enters the back of the cecal wall and can prolapse. There is a second opening from the exposed cecal plate for the rudimentary colon, which always ends blindly in the abdomen or pelvis as an associated imperforate anus. The distal ureters enter each bladder plate. Girls usually have two vaginal openings entering each hemibladder, near the ureteral orifices. The symphysis pubis is widely separated and the external genitalia incompletely formed. Penile or clitoral halves with the adjacent scrotal or labial components can be located separately inferior to the bladder plates. Apendiceal duplication inserting in the cecal wall is also frequently noted. The anomaly is commonly associated with omphalocele and spinal defects [1]. Bladder exstrophy is a less severe defect in which the posterior bladder wall is exposed through a midline defect of the abdominal wall (Fig. 2). The umbilicus has a low insertion located close to the superior margin of the exstrophic bladder. External genitalia abnormalities are common in boys and girls, presenting epispadias and a small, dorsally curved split phallus in a boy or a split clitoris in a girl. There is also diastasis of the pubic symphysis [3]. Small to medium sized omphalocele, imperforate anus and spinal defects have been described with this malformation, but are very rare, when compared to cloacal exstrophy [3, 15, 16]. In isolated epispadias, there is nonclosure of the urethral plate with an abnormal dorsal location and low-set

Pediatr Radiol (2013) 43:593–604

umbilicus but no lower anterior abdominal bulge. Boys have a short, broad penis and girls have a variable cleft of the urethra and a split clitoris. A minor symphysis gap is possible. Children with epispadias may be incontinent due to an inadequate bladder neck mechanism [17]. Any of these three types of malformations could present in utero as a persistently absent bladder with normal amniotic fluid volume. However, only the first two, cloacal exstrophy and bladder exstrophy, are associated with an anterior abdominal wall mass [4, 17, 18]. A special presentation of cloacal exstrophy was displayed by one of our cases, in which the cloacal membrane was still intact at the time of work-up. This created a characteristic protruding infraumbilical abdominopelvic cyst. Although on a quick inspection, it could simulate an abnormally enlarged bladder, it had a more anterior position and bulged through a very thin anterior wall. It contained layering debris following the expected signal characteristics of meconium, supporting communication with the gastrointestinal system, and the cyst was outlined by the umbilical arteries [19]. The exstrophy was exposed at birth, supporting delayed rupture of the cloacal membrane. Other forms of wall defects such as omphalocele, gastroschisis and limb–body wall complex are different from cloacal exstrophy. An omphalocele is a ventral wall defect in which a portion of the abdominal organs herniates into the base of the umbilical cord and is covered by a membrane. Gastroschisis is a small paraumbilical wall defect, to the right of the abdominal cord insertion, with herniation of abdominal contents into the amniotic cavity without a covering membrane [20]. Both defects should have a normal bladder. Limb–body wall complex is another type of body wall defect with multiple malformations, the major findings of which include a large, usually left-sided, thoracoabdominal wall defect, limb reduction anomalies, scoliosis and fusion of the body with the placenta in association with a short or absent umbilical cord [21]. This entity is not only morphologically different from cloacal exstrophy but also differs significantly in prognosis as it is universally fatal [20]. An accurate and confident prenatal diagnosis of cloacal exstrophy is essential for adequate parental counseling with a multidisciplinary team, including colorectal surgeons, pediatric urologists, pediatric neurosurgeons and neonatologists [4]. Several authors have stressed the importance of a correct unified surgical management plan instituted from birth to optimize functional outcomes for the patient [1, 22, 23]. As this is an uncommon diagnosis, these patients are expected to benefit from centralized pre- and postnatal management in centers with experience in treating cloacal exstrophy, which may influence the chosen site of delivery and postnatal care [24, 25].

Pediatr Radiol (2013) 43:593–604

603

Prenatal diagnosis of cloacal exstrophy with US has been suggested with the following criteria: failure to visualize the bladder without anhydramnios or severe oligohydramnios, large midline infraumbilical anterior wall defect, infraumbilical cystic anterior wall structure (persistent cloacal membrane) and/or lumbar myelomeningocele [7]. However, this alone will not provide a confident diagnosis. In 1999, Hamada et al. [26] reported the elephant trunk-like US finding as a new criterion for the prenatal diagnosis. This finding represents the prolapse of the terminal ileum through the exstrophy seen as a wavy cord-like mass of soft tissue protruding from the infraumbilical anterior wall. It is the most specific US finding but may be inconstantly found as the prolapse can be intermittent or even potentially obscured by the omphalocele, fetal limbs or redundant umbilical cord [27]. In the absence of this sign, a confident prenatal US diagnosis of cloacal exstrophy could be difficult and a differential diagnosis with bladder exstrophy is frequently provided [13, 28]. Sometimes, the findings are difficult to understand and the entertained prenatal diagnosis is gastroschisis, omphalocele or sacrococcygeal teratoma [8, 29, 30]. For example, it could be possible that a prolapsed terminal ileum may be misinterpreted as gastroschisis during a technically difficult US scan, particularly if a persistently absent bladder goes unrecognized. By our review, clues to US diagnosis of cloacal exstrophy should include an abdominal wall defect with persistently absent bladder despite normal amniotic fluid volume. Additional malformations, such as spinal defects, would make our level of concern even greater. In those situations, further evaluation with MRI may be helpful. Fetal MRI can provide a confident diagnosis of cloacal exstrophy and allow its differentiation from other forms of wall defects. In this paper, we define the spectrum of fetal MRI findings in cloacal exstrophy, including before and after rupture of the cloacal membrane. The findings include absence of a normal bladder despite normal amniotic fluid volume (in the form of persistently absent bladder or thinwalled protruding anterior pelvic cyst), protuberant anterior

pelvic contour representing the exstrophy, lack of meconium in the rectum and colon supporting a primitive blind-ending hindgut, and omphalocele, usually small and low. Additional findings would include potential visualization of the prolapsed terminal ileum and the lateral bladder plates, distal ureters extending to the anterior abdominal wall, closed neural tube defects and genitourinary abnormalities. The external genitalia are incompletely formed in this type of malformation accounting for their difficult characterization [10]. In addition, other external genitalia anomalies are possible and one of the two boys in our series had a bifid scrotum and ambiguous genitalia at birth with a small penis found between the bladder plates during surgery. This type of genital arrangement is rare but has been previously described in two reports of cloacal exstrophy [22, 25]. The evaluation of the colon and rectum is extremely important to establish this diagnosis and the findings are different from those in bladder exstrophy and persistent cloaca (Table 2). Fetal MRI allows excellent depiction of the large bowel once it is filled with meconium, displaying characteristic bright T1-weighted signal in a predictable chronological pattern. Starting around 21 weeks’ gestation, meconium is expected to fill the rectum. By 22 to 23 weeks’ gestation, the left colonic flexure is recognized. Usually by 26 weeks’ gestation, the entire colon is visualized [31, 32]. Therefore, imaging prior to 21 weeks may not provide the desired information about the colon. In our series, there was absent meconium-filled rectum and colon in its expected anatomical distribution by gestational age. This appearance supported a diagnosis of imperforate anus and a primitive hindgut, which are features of cloacal exstrophy that allow differentiation from bladder exstrophy (in which a normal rectum and colon is expected) [4, 33]. This is also different from cloacal malformation, where the most distal segment of the bowel is focally dilated and is not associated with an infraumbilical wall defect [34]. Bowel dilatation was only seen in one case in our series, affecting the portion of small bowel contained in the omphalocele rather than the distal

Table 2 Imaging characteristics to differentiate cloacal exstrophy, bladder exstrophy and cloacal malformation

Bladder

Anterior pelvic wall mass Omphalocele Abdominal cord insertion Meconium-filled rectum/colon (↑T1-W signal)

Spinal anomalies

Cloacal exstrophy

Bladder exstrophy

Cloacal malformation

Absent (uncommonly: anterior protruding pelvic cyst if presentation prior to cloacal membrane rupture) Yes Frequent, usually small and low Low Absent

Absent

Variable size (megacystis/normal size/decompressed)

Yes Rare Low Usually normal

Frequent (closed dysraphism)

Rare

No Rare Normal Short and dilated rectum (cloaca with long common channel) Variable signal: it could have fluid (↓T1) or meconium (↑T1) Possible

604

bowel. This finding correlated at birth with a blind-ending terminal ileum as a form of intestinal atresia. Other gastrointestinal malformations, such as duplication, have also been described in the setting of cloacal exstrophy and were found at surgery in one of our patients [4, 14]. Besides attention for expected genitourinary malformations, we recommend meticulous evaluation of the spine, as these patients typically demonstrate complex closed dysraphism in the spectrum of terminal myelocystocele and lipomyelomeningocele. There is also potential involvement at several spinal levels in the same patient, which has not been previously reported.

Conclusion Fetal MRI provides a confident diagnosis of cloacal exstrophy when a normal bladder is not identified, there is a protuberant abdominopelvic contour, and there is absence of meconium-filled rectum and colon. Genitourinary and spinal malformations are common associations. In the case of presentation prior to rupture of the cloacal membrane, a thin-walled anterior cyst can be seen protruding through the infraumbilical pelvic wall. Confident detection of the hindgut anomaly is achieved when fetal MRI scan is performed after 21 weeks’ gestation, the time of expected physiological distention of the rectum with meconium. Conflicts of interest None

References 1. Hendren WH (1996) Urogenital sinus and cloacal malformations. Semin Pediatr Surg 5:72–79 2. Carey JC, Greenbaum B, Hall BD (1978) The OEIS complex (omphalocele, exstrophy, imperforate anus, spinal defects). Birth Defects Orig Artic Ser 14:253–263 3. Martinez-Frias ML, Bermejo E, Rodriguez-Pinilla E et al (2001) Exstrophy of the cloaca and exstrophy of the bladder: two different expressions of a primary developmental field defect. Am J Med Genet 99:261–269 4. Ebert AK, Reutter H, Ludwig M et al (2009) The exstrophyepispadias complex. Orphanet J Rare Dis 4:23 5. Bohring A (2002) OEIS complex, VATER, and the ongoing difficulties in terminology and delineation. Am J Med Genet 107:72–76 6. Carey JC (2001) Exstrophy of the cloaca and the OEIS complex: one and the same. Am J Med Genet 99:270 7. Austin PF, Homsy YL, Gearhart JP et al (1998) The prenatal diagnosis of cloacal exstrophy. J Urol 160:1179–1181 8. Wu JL, Fang KH, Yeh GP et al (2004) Using color Doppler sonography to identify the perivesical umbilical arteries: a useful method in the prenatal diagnosis of omphalocele-exstrophy-imperforate anusspinal defects complex. J Ultrasound Med 23:1211–1215 9. Gobbi D, Fascetti Leon F, Tregnaghi A et al (2008) Early prenatal diagnosis of cloacal exstrophy with fetal magnetic resonance imaging. Fetal Diagn Ther 24:437–439

Pediatr Radiol (2013) 43:593–604 10. Caire JT, Ramus RM, Magee KP et al (2003) MRI of fetal genitourinary anomalies. AJR Am J Roentgenol 181:1381–1385 11. Chauvin NA, Epelman M, Victoria T et al (2012) Complex genitourinary abnormalities on fetal MRI: imaging findings and approach to diagnosis. AJR Am J Roentgenol 199:W222–W231 12. Chen CP, Chang TY, Liu YP et al (2008) Prenatal 3dimensional sonographic and MRI findings in omphaloceleexstrophy-imperforate anus-spinal defects complex. J Clin Ultrasound 36:308–311 13. Chen CP (2007) Syndromes and disorders associated with omphalocele (II): OEIS complex and Pentalogy of Cantrell. Taiwan J Obstet Gynecol 46:103–110 14. Phillips TM (2011) Spectrum of cloacal exstrophy. Semin Pediatr Surg 20:113–118 15. Pinette MG, Pan YQ, Pinette SG et al (1996) Prenatal diagnosis of fetal bladder and cloacal exstrophy by ultrasound. A report of three cases. J Reprod Med 41:132–134 16. Gearhart JP, Ben-Chaim J, Jeffs RD et al (1995) Criteria for the prenatal diagnosis of classic bladder exstrophy. Obstet Gynecol 85:961–964 17. Yiee J, Wilcox D (2008) Abnormalities of the fetal bladder. Semin Fetal Neonatal Med 13:164–170 18. Wilcox DT, Chitty LS (2001) Non-visualisations of the fetal bladder: aetiology and management. Prenat Diagn 21:977–983 19. Langer JC, Brennan B, Lappalainen RE et al (1992) Cloacal exstrophy: prenatal diagnosis before rupture of the cloacal membrane. J Pediatr Surg 27:1352–1355 20. Emanuel PG, Garcia GI, Angtuaco TL (1995) Prenatal detection of anterior abdominal wall defects with US. Radiographics 15:517–530 21. Chen CP (2008) Syndromes, disorders and maternal risk factors associated with neural tube defects (III). Taiwan J Obstet Gynecol 47:131–140 22. Carr MC, Benacerraf BR, Mandell J (1994) Prenatal diagnosis of an XY fetus with aphallia and cloacal exstrophy variant. J Ultrasound Med 13:323–325 23. Soffer SZ, Rosen NG, Hong AR et al (2000) Cloacal exstrophy: a unified management plan. J Pediatr Surg 35:932–937 24. Marvin T (2007) Cloacal exstrophy: a case study. Neonatal Netw 26:21–30 25. Tiblad E, Wilson RD, Carr M et al (2008) OEIS sequence – a rare congenital anomaly with prenatal evaluation and postnatal outcome in six cases. Prenat Diagn 28:141–147 26. Hamada H, Takano K, Shiina H et al (1999) New ultrasonographic criterion for the prenatal diagnosis of cloacal exstrophy: elephant trunk-like image. J Urol 162:2123–2124 27. Richards DS, Langham MR Jr, Mahaffey SM (1992) The prenatal ultrasonographic diagnosis of cloacal exstrophy. J Ultrasound Med 11:507–510 28. Keppler-Noreuil K, Gorton S, Foo F et al (2007) Prenatal ascertainment of OEIS complex/cloacal exstrophy – 15 new cases and literature review. Am J Med Genet A 143A:2122–2128 29. Kutzner DK, Wilson WG, Hogge WA (1988) OEIS complex (cloacal exstrophy): prenatal diagnosis in the second trimester. Prenat Diagn 8:247–253 30. Hyun SJ (2006) Cloacal exstrophy. Neonatal Netw 25:101– 115 31. Saguintaah M, Couture A, Veyrac C et al (2002) MRI of the fetal gastrointestinal tract. Pediatr Radiol 32:395–404 32. Brugger PC, Prayer D (2006) Fetal abdominal magnetic resonance imaging. Eur J Radiol 57:278–293 33. Hsieh K, O’Loughlin MT, Ferrer FA (2005) Bladder exstrophy and phenotypic gender determination on fetal magnetic resonance imaging. Urology 65:998–999 34. Calvo-Garcia MA, Kline-Fath BM, Levitt MA et al (2011) Fetal MRI clues to diagnose cloacal malformations. Pediatr Radiol 41:1117–1128