Fetal Magnetic Resonance Imaging of Congenital Renal Anomalies: A Pictorial Review
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1 J Radiol Sci 2014; 39: Fetal Magnetic Resonance Imaging of Congenital Renal Anomalies: A Pictorial Review Yu-Peng Liu 1,3 Su-Chiu Chen 2,3 Department of Radiology 1, Mackay Memorial Hospital, Hsinchu, Taiwan Department of Radiology 2, Mackay Memorial Hospital, Taipei, Taiwan Department of Radiological Technology 3, Yuanpei University, Hsinchu, Taiwan Abstract Congenital renal anomalies comprise a vast spectrum of pathologies and are often associated with oligohydramnios, which can make prenatal ultrasonography (US) evaluation difficult. However, fetal magnetic resonance imaging (MRI) is less affected by the diminished amniotic fluid and can provide superior image quality. Understanding of fetal renal anomalies and associated malformations is essential for patient counseling and appropriate pregnancy, delivery, and neonatal management. MRI is a well-established and effective diagnostic tool complementing US due to its superior tissue contrast, large field of view, enhanced anatomic evaluation, and more detailed rendering of renal malformations when US findings are equivocal or inconclusive, especially when oligohydramnios is present. Ultrasonography (US) is a modality of choice to evaluate the fetal renal anomalies, but making a precise prenatal diagnosis may be difficult or impossible, especially during the early second trimester due to fetal position, maternal obesity, superimposed bone, and in particular, oligohydramnios. Magnetic resonance imaging (MRI) is gaining more and more popularity as a complementary modality because it images the fetus in multiple planes, a large field of view, using excellent tissue contrast, and irrespective of fetal position [1-6]. Congenital renal anomalies include renal dysgenesis (agenesis and hypoplasia), congenital cystic renal disease, cystic renal disease associated with other syndromes, hydronephrosis, congenital renal positional anomalies, and congenital renal morphological anomalies [2, 5-7]. In this review, fetal renal MRI technique is discussed, and the congenital renal anomalies observed on MRI are illustrated. MRI Technique MRI was performed using a 1.5 T MR scanner (Twinspeed, GE Medical Systems, Milwaukee, WI) with a torso phased-array coil, and images were sequenced at a singleshot fast-spin echo (SSFSE) and thick-slab T2-weighted sequences. The imaging protocol comprised SSFSE sequences in the axial, coronal, and sagittal planes of the fetal kidneys (TE: 90 ms, TR: minimum, field of view: mm, matrix: , slice thickness: 4 or 5 mm, scan time: 34 s/19 slices) and thick-slab T2-weighted sequences in the coronal and sagittal planes (TE: minimum, TR: 4000 ms, field of view: mm, matrix: , slice thickness: 60 mm, scan time: 33 s/9 slices). If necessary, one could serially repeat scans of multiple sections (axial, coronal or sagittal), which might be expected to improve the rate of detection of the tiny or complicated lesions. All sequences were performed without or with maternal breathholding. The entire examination remained within 30 min. Normal fetal kidneys on T2-weighted images The renal parenchyma is brighter than fetal liver, spleen, or muscle, but less bright than maternal fat on SSFSE T2-weighted images. The renal pelvis appears Correspondence Author to: Su-Chiu Chen Department of Radiology, Mackay Memorial Hospital, Taipei, Taiwan No. 92, Sec. 2, Chung-Shan N. Road, Taipei 104, Taiwan J Radiol Sci September 2014 Vol.39 No.3 77
2 bright but is isointense to maternal fat, and represents fetal urine. Occasionally, a long-t2 rim surrounds the kidney, suggesting perirenal fat (Fig. 1). On thick-slab T2-weighted images, a topographic view of the normal bulk fluids within the spinal canal, lungs, stomach, intestines, and urinary tract, including bilateral renal pelves and urinary bladder, is visible (Fig. 2). Types of fetal renal anomalies Renal agenesis Renal agenesis, congenital absence of one or both kidneys, possibly results from a failure of the ureteral bud to induce development of the metanephrogenic blastema. Bilateral renal agenesis is a rare and devastating anomaly, occurring in only one or two per 10,000 births; the condition is usually associated with severe oligohydramnios and is one causative agent of Potter sequence [8]. Unilateral renal agenesis is much more common and usually found incidentally along with compensatory hypertrophy of the contralateral kidney, or may be associated with ipsilateral urogenital anomalies or adrenal agenesis [8, 9]. On MRI, anhydramnios or oligohydramnios, bowel loops in place of normal kidney in the expected renal fossa, and a small or signal void of the urinary bladder [5] suggest bilateral renal agenesis (Fig. 3). In a fetus with unilateral agenesis, absence of the bright urine signal from the involved renal pelvis, contralateral renal hypertrophy, normal visualization of the urinary bladder and a normal amniotic fluid volume are observed (Fig. 4) [3, 5, 10, 11]. Renal hypoplasia Renal hypoplasia refers to a small kidney containing essentially normal residual parenchyma with intact, but fewer nephrons, whereas a dysplastic kidney contains disorganized and maldifferentiated tissue [12]. In practice, the diagnosis of congenital renal hypoplasia is favored under the following conditions: the renal size is decreased by two standard deviations from the mean size according to age and the contralateral kidney shows compensatory hypertrophy; renal scarring is excluded using postnatal Doppler US as an initial renal screen or 99mTc dimercaptosuccinic acid radionuclide scan [12]. Renal hypoplasia is not generally associated with urinary tract malformations but may be a component of a larger genetic syndrome such as renal coloboma and branchio-oto-renal syndromes, though it may be an isolated finding [13]. On MRI, the abnormal small kidney maintains a normal renal pelvis (Fig. 5). Congenital cystic renal diseases Congenital cystic renal disease can develop in the fetus but more typically develops after birth. The condition has two MRI patterns, frank cysts and long-t2 renal parenchyma, which can be associated with each other. The cysts can be miniscule or large, and can develop anywhere in one or both kidneys. Long T2 of the renal parenchyma suggests microscopic cysts and/or dilated tubules. The Potter Figure 1 Figure 2 Figure 1. Axial fetal MRI at 22 weeks of gestation. The renal parenchyma (arrows) appears less bright than the maternal fat (F). The renal pelvis is bright and isointense to the maternal fat, indicating fetal urine. The bright signal surrounding the kidney suggests perirenal fat (arrowheads). Figure 2. Thick-slab fetal MRI at 27 weeks of gestation. A global view reveals the normal static fluids in the spinal canal, lung (L), stomach (S), bowel loops (arrows), renal pelvis (arrowhead), and urinary bladder (B). 78 J Radiol Sci September 2014 Vol.39 No.3
3 classification of cystic renal disease [14, 15] comprises four types: type 1, infantile polycystic kidney disease (autosomal recessive polycystic kidney disease [ARPKD]); type 2, cystic dysplastic kidney disease (multicystic dysplastic kidney disease [MCDK]); type 3, adult polycystic kidney disease (autosomal dominant polycystic kidney disease [ADPKD]); and type 4, obstructive cystic renal dysplasia. Type 1: Autosomal recessive polycystic kidney disease ARPKD is the most common heritable cystic renal disease in infant and children, occurring at a frequency between one in 6,000 to 55,000 births [16, 17]. The disorder Figure 3 3a 3b Figure 3. Bilateral renal agenesis in a 34-week-old fetus. a. Axial and b. coronal MRI shows oligohydramnios, a signal void at the urinary bladder (arrowhead), and neither kidney is visible in the expected renal fossa, instead replaced by small bowel (arrows) and colon loops (C). Figure 4 Figure 5 Figure 4. Right renal agenesis in a 25-week-old fetus. Coronal MRI shows an absent urine signal in the right renal pelvis, normal left renal contour, visible urinary bladder (not shown), normal lung development, and normal amniotic fluid volume. Figure 5. Right renal hypoplasia in a 23-week-old fetus. Axial MRI shows a small right kidney (arrows) compared to left kidney and a normal bright urine signal in the bilateral renal pelves. J Radiol Sci September 2014 Vol.39 No.3 79
4 manifests as nonobstructive dilatation of collecting tubule or renal medulla ectasia, and is typically bilaterally symmetric. In severe cases, these 1-2 mm diameter lesions may extend to the cortex. The kidneys are typically enlarged when numerous ducts are involved. Patients with ARPKD can also have hepatic anomalies, including numerous, dilated bile ducts, as well as enlarged and fibrotic portal Figure 6 Figure 6. ARPKD in a 23-week-old fetus. Coronal MRI shows enlarged well-delineated kidneys with high signal intensity (arrows), while the renal pelves and urinary bladder are not visible. Concurrent low signal hypoplastic lungs and oligohydramnios are also seen. tracts. On MRI, the enlarged well-delineated kidneys with high T2 signal intensity are indicative of numerous dilated collecting ducts in the renal parenchyma; the normally bright renal pelves may be obscured as well [3, 18, 19]. Concurrent pulmonary hypoplasia and oligohydramnios can be also seen (Fig. 6) [19]. The hyperintense medullary lesions help differentiate ARPKD from other causes of renal hyperechogenicity found on US, such as ADPKD, congenital nephrosis, Bardet Biedl syndrome, or cytomegalovirus infection [3]. Type 2: Multicystic dysplastic kidney disease MCDK is characterized by a disturbed nephrogenic tissue differentiation. The renal parenchyma is randomly replaced by variably sized non-communicating cysts resembling bunches of grapes; ultimately, the reniform shape of the kidney is completely lost [14]. Segmental MCDK may occur in one pole of a duplex kidney or within a crossed fused ectopic kidney. The abnormality may be unilateral (76%) or bilateral (24%) and occurs more frequently in males, at 2.4:1 [7, 20]. In unilateral cases, oligohydramnios is absent, and the bladder appears normal [21]. However, in bilateral cases, there is severe oligohydramnios, and the urinary bladder is not visible; Potter s sequence usually results [20]. The MRI shows an enlarged lobulated kidney with randomly scattered variably sized cysts [5] resembling bunches of grapes (Fig. 7). In severe cases, the kidneys appear as large abdominal cystic structures [22, 23]. Type 3: Autosomal dominant polycystic kidney disease ADPKD is a dominant heterogenetic systemic disease, Figure 7 7a 7b Figure 7. MCDK in a 25-week-old fetus. a. Coronal and b. thick-slab MRIs show an enlarged lobulated left kidney with randomly scattered variably sized cysts resembling bunches of grapes. 80 J Radiol Sci September 2014 Vol.39 No.3
5 affecting approximately one in births [24, 25]. It is characterized by focal and progressive enlargement of renal cysts, and as a systemic disorder, multiple organs are affected, resulting in extrarenal cysts in the liver, pancreas, spleen, thyroid, arachnoid membranes, and macrovessels. ADPKD is genetically heterogeneous and is attributed to mutations in PKD1 (chromosome 16), which is more associated with renal disease, and PKD2 (chromosome 4), which causes extrarenal manifestations such as intracranial aneurysms [15, 25, 26]. In utero, only the renal lesions can be detected by US [15] or MRI. Increased renal echogenicity is the most common US finding in ADPKD, and identification of simple cysts is rare in utero (1:1100 pregnancies). Although cysts are the diagnostic criteria for ADPKD, cystic changes seldom occur in fetus and are found predominantly in the cortex [15, 26]. In MRI, both ARPKD and ADPKD demonstrate high T2 signal intensity in utero; however, the kidney tends to be larger and have a brighter T2 signal in individuals with ARPKD compared to those with ADPKD. Besides ARPKD, other differential diagnoses include Bardet Biedl syndrome, Meckel Gruver syndrome, and Ivemark II syndrome [26]. Diagnosis of ADPKD is supported by the following findings: high T2 renal signal intensity with a normal renal pelvis and tiny subcapsular cysts [15]; the absence of concurrent malformations such as polydactyly, spinal abnormalities, hepatic fibrosis, and central nervous system anomalies; normal amniotic fluid volume; visible urinary bladder; and normal lung development (Fig. 8). Type 4: Obstructive cystic renal dysplasia This condition is defined as an abnormal nephronic and ductal development due to urinary tract obstruction during the early first trimester such as ureteropelvic junction obstruction, vesicoureteral junction obstruction, vesicoureteral reflux, urethral agenesis, and posterior urethral valves [14, 27]. In utero, obstruction during the first trimester causes cystic renal dysplasia, whereas obstruction during the second trimester causes hydronephrosis or atrophy [27, 28]. The MRI shows a normal to small renal size, preserved reniform shape, and scattered small cysts associated with urinary tract obstruction (Fig. 9). Differential diagnoses include MCDK (usually enlarged lobulated kidney with larger cysts and no urinary tract obstruction) and Meckel Gruber syndrome (concurrent occipital encephalocoele and polydactyly). Cystic renal diseases within syndromes or sequences (glomerulocystic and medullary cystic dysplasia) Many syndromes or sequences are also associated with renal cysts. Distinguishing between glomerulocystic and medullary forms requires pathologic examination. In glomerulocystic kidney disease, the cysts result from dilation of the Bowman s space; subcapsular cysts are diagnostic on MRI or US. The disease is rare and may occur in otherwise normal infants or associated multiple malformations such as ADPKD glomerulocystic type, oral facial digital syndrome, short rib-polydactyly syndromes, Trisomy 13, Trisomy 18, tuberous sclerosis complex, Jeune syndrome (asphyxiating thoracic dysplasia), Zellweger syndrome Figure 8 Figure 9 Figure 8. ADPKD in a 33-week-old fetus. Coronal MRI shows a bilateral high renal signal intensity, normal renal pelvis brightness, tiny subcapsular cysts (arrows), normal amniotic fluid volume, and normal lung development. Figure 9. Obstructive cystic renal dysplasia in a 28-weekold fetus caused by vesicoureteral reflux. Coronal MRI shows a normal left renal contour (arrows) with hydronephrosis and several small cysts (arrowheads). J Radiol Sci September 2014 Vol.39 No.3 81
6 Figure 10 Figure 11 Figure 10. Ureteropelvic junction obstruction in a 27-weekold fetus. Coronal MRI shows moderate pelvicaliectasis with no ureteral dilatation, an ectopic ureterocele, and megaureter or posterior urethral dilatation (not shown). Figure 11. Left hydronephrosis caused by primary megaureter in a 33-week-old fetus. Thick-slab MRI shows a left hydronephrosis (arrows) and tortuous megaureter (U). The urinary bladder is displaced laterally (B). (cerebrohepatorenal syndrome), Ivemark II syndrome, and others [29]. Medullary cystic dysplasia is characterized by extensive medullary tubule dilation extending towards the cortex but primarily affecting the medulla. Associated diseases include Meckel Gruber, Bardet Biedl, and Beckwith Wiedemann syndromes [30, 31]. Similar to ARPKD, syndromes or sequences associated with glomerulocystic kidney disease and medullary cystic dysplasia may show nephromegaly with high T2 signal intensity [32] or small renal cysts [33]. Hydronephrosis Fetal hydronephrosis is a common finding and occurs in 0.5 to 1 percent of pregnancies [34]. Although typically a common and transient physiologic state in most cases, it can occasionally be caused by urinary tract obstructive uropathy (ureteropelvic junction obstruction, posterior urethral valve) and non-obstructive causes (vesicoureteral reflux, megaureter, prune-belly syndrome) [35]. The most common causes are transient hydronephrosis, ureteropelvic junction obstruction, and vesicoureteral reflux. However, ureteropelvic junction obstruction and vesicoureteral reflux may manifest initially as mild hydronephrosis. In severe cases, the normal renal morphology is lost, resulting in a large, lobulated cystic structure visibly that may be difficult to distinguish from other abdominal cystic masses. On MRI, the features of ureteropelvic junction obstruction include varying degrees of pelvicaliectasis without ureteral dilatation, ectopic ureterocele, megaureter, or posterior urethral dilatation (Fig. 10). MRI also provides superior anatomic details and a large field of view to detect complex urinary tract abnormalities (Fig. 11) [36]. Congenital renal positional anomalies An ectopic kidney may be pelvic, iliac, abdominal, thoracic, or crossed and is often associated with other abnormalities such as contralateral renal agenesis, vascular malformation, and genital anomalies [37]. Pelvic kidney is the most common type, while ectopic intrathoracic kidney is the least frequent, occurring in less than 1 in 10,000 births [38]. Most ectopic kidneys are clinically asymptomatic except for the vesicoureteral reflux development, hydronephrosis, urolithiasis, and increased susceptibility to injury from blunt trauma. Ectopic kidney is frequently first diagnosed on US, usually incidentally. Intrathoracic renal ectopia may be related to diaphragmatic eventration or hernia and is usually an associated finding (Fig. 12). Congenital renal morphological anomalies Horseshoe kidney is the most common renal fusion anomaly. Most cases of horseshoe kidneys are asymptomatic and found during autopsy. The condition may increase the risk of hydronephrosis, renal stones, infection, transitional cell carcinoma and other cancers, Wilms tumor, and carcinoid tumor; it may also accompany genitourinary and other congenital anomalies. A renal pelvic angle less than 140 on an axial US highly suggests horseshoe kidney [39]. 82 J Radiol Sci September 2014 Vol.39 No.3
7 Figure 12 Figure 12. Congenital diaphragmatic hernia in a 29-weekold fetus. On axial MRI, the liver (L), small bowel loops (arrows), and right kidney (arrowheads) are herniated into the right thorax, causing left displacement of the heart. Conclusions MRI is a useful complementary diagnostic tool to assess fetal renal anomalies diagnosed by US. It is essential for both prenatal counseling and peri- and postnatal management to selected patients when US findings are inconclusive or inadequate, especially if oligohydramnios is present.3. Acknowledgement The review study was approved by the Institutional Review Board of Mackay Memorial Hospital (IRB Number: 14MMHIS156). References 1. Abdelazim IA, Belal MM. The role of magnetic resonance imaging in refining the diagnosis of suspected fetal renal anomalies. J Turk Ger Gynecol Assoc 2013; 14: Barseghyan K, Jackson HA, Chmait R, De Filippo RE, Miller DA. Complementary roles of sonography and magnetic resonance imaging in the assessment of fetal urinary tract anomalies. J Ultrasound Med 2008; 27: Cassart M, Massez A, Metens T, et al. Complementary role of MRI after sonography in assessing bilateral urinary tract anomalies in the fetus. AJR Am J Roentgenol 2004; 182: Chaumoitre K, Wikberg E, Shojai R, et al. Fetal magnetic resonance hydrography: evaluation of a single-shot thick-slab RARE (rapid acquisition with relaxation enhancement) sequence in fetal thoracoabdominal pathology. Ultrasound Obstet Gynecol 2006; 27: Hawkins JS, Dashe JS, Twickler DM. Magnetic resonance imaging diagnosis of severe fetal renal anomalies. Am J Obstet Gynecol 2008; 198: 328e1-e5 6. Gupta P, Kumar S, Sharma R, Gadodia A, Roy KK, Sharma JB. The role of magnetic resonance imaging in fetal renal anomalies. Int J Gynaecol Obstet 2010; 111: Wellesley D, Howe DT. Fetal renal anomalies and genetic syndromes. Prenat Diagn 2001; 21: Whitehouse W, Mountrose U. Renal agenesis in nontwin siblings. Am J Obstet Gynecol 1973; 116: Cascio S, Paran S, Puri P. Associated urological anomalies in children with unilateral renal agenesis. J Urol 1999; 162: Caire JT, Ramus RM, Magee KP, Fullington BK, Ewalt DH, Twickler DM. MRI of fetal genitourinary anomalies. AJR Am J Roentgenol 2003; 181: Poutamo J, Vanninen R, Partanen K, Kirkinen P. Diagnosing fetal urinary tract abnormalities: benefits of MRI compared to ultrasonography. Acta Obstet Gynecol Scand 2000; 79: Sanna-Cherchi S, Caridi G, Weng PL, et al. Genetic approaches to human renal agenesis/hypoplasia and dysplasia. Pediatr Nephrol 2007; 22: Sanyanusin P, Schimmenti LA, McNoe LA, et al. Mutation of the PAX2 gene in a family with optic nerve colobomas, renal anomalies and vesicoureteral reflux. Nat Genet 1995; 9: Fong KW, Rahmani MR, Rose TH, Skidmore MB, Connor TP. Fetal renal cystic disease: sonographicpathologic correlation. AJR Am J Roentgenol 1986; 146: Avni FE, Garel C, Cassart M, D Haene N, Hall M, Riccabona M. Imaging and classification of congenital cystic renal diseases. AJR Am J Roentgenol 2012; 198: Lonergan GJ, Rice RR, Suarez ES. Autosomal recessive polycystic kidney disease: radiologic-pathologic correlation. Radiographics 2000; 20: Zerres K, Mücher G, Becker J, et al. Prenatal diagnosis of autosomal recessive polycystic kidney disease (ARPKD): molecular genetics, clinical experience, and fetal morphology. Am J Med Genet 1998; 76: Nishi T. Prenatal diagnosis of urinary tract abnormalities. Acta Obstet Gynecol Scand 1997; 76: J Radiol Sci September 2014 Vol.39 No.3 83
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