- Email: [email protected]
Contribution of the foetal uro-MRI in the prenatal diagnosis of uronephropathies
+Model
ARTICLE IN PRESS
DIII-427; No. of Pages 6
Diagnostic and Interventional Imaging (2014) xxx, xxx—xxx
ORIGINAL ARTICLE / Genitourinary imaging
Contribution of the foetal uro-MRI in the prenatal diagnosis of uronephropathies H. Pico a,∗, A. Dabadie a, B. Bourliere-Najean a, N. Philip b, M. Capelle c, A. Aschero a, E. Quarello d, J.-M. Guys e, G. Hery e, P. Petit a, G. Gorincour a a
Service d’imagerie pédiatrique et prénatale, hôpital de la Timone, 264, rue Saint-Pierre, 13385 Marseille cedex 5, France b Département de génétique médicale, hôpital de la Timone, 264, rue Saint-Pierre, 13385 Marseille cedex 5, France c Centre de diagnostic prénatal, hôpital de la Timone, 264, rue Saint-Pierre, 13385 Marseille cedex 5, France d Service de gynécologie obstétrique, hôpital Saint-Joseph, 26, boulevard de Louvain, 13285 Marseille cedex 08, France e Service de chirurgie infantile, hôpital de la Timone, 264, rue Saint-Pierre, 13385 Marseille cedex 5, France
KEYWORDS Pregnant; Urogenital abnormalities; Prenatal ultrasonography; Magnetic resonance imaging
∗
Abstract Purpose: To study the complementary diagnostic value and role in the perinatal management of foetal MRI in the prenatal diagnosis of abnormalities of the urinary tract. Patients and methods: Retrospective monocentric study from November 2002 to June 2011 of foetuses benefiting from an MRI after ultrasound diagnosis of uronephropathy abnormalities. Ultrasound and MRI data were compared with postnatal radiological and/or surgical data or with the foetopathology. The MRI analysis focused on the diagnostic concordance with the ultrasound, the complementary diagnostic contribution and/or a change in perinatal care. Results: Of the 154 MRI examined, a follow-up was obtained for 108 cases. The indications for MRI were classified into six groups: suspected renal agenesis (n = 20, 18.5%), posterior urethral valve (n = 20, 18.5%), reflux or megaureter (n = 14, 13%), uretropelvic junction syndrome (n = 24, 22.5%), enlarged kidneys (n = 7, 6.5%) and others (n = 23, 21%). The information supplied by ultrasound was confirmed by MRI in 72 patients (67%). MRI provided additional data for 36 patients (33%) and changed the perinatal care for 16 patients (15%). Conclusion: Foetal uro-MRI is a useful complementary tool in the prenatal diagnosis of some uropathy abnormalities. © 2014 Published by Elsevier Masson SAS on behalf of the Éditions françaises de radiologie.
Corresponding author. E-mail address: [email protected] (H. Pico).
2211-5684/$ — see front matter © 2014 Published by Elsevier Masson SAS on behalf of the Éditions françaises de radiologie. http://dx.doi.org/10.1016/j.diii.2014.02.011
Please cite this article in press as: Pico H, et al. Contribution of the foetal uro-MRI in the prenatal diagnosis of uronephropathies. Diagnostic and Interventional Imaging (2014), http://dx.doi.org/10.1016/j.diii.2014.02.011
+Model DIII-427; No. of Pages 6
ARTICLE IN PRESS
2
H. Pico et al.
Malformations in the foetal urinary tract are fairly common, found in 0.1 to 1% of all pregnancies and account for about 30 to 50% of the abnormalities found at birth [1]. They are most often detected by obstectrical ultrasound, the examination that remains the screening reference [2]. The spectrum of malformation is wide and the greater the reduction in amniotic fluid and the more the malformation is bilateral, the more unfavourable the prognosis. The ultrasound may be unable to provide an exact diagnosis and prognosis of the uronephropathy, especially when the conditions are unfavourable (maternal obesity, unfavourable position of the foetus, oligohydramnios). In this situation, magnetic resonance imaging (MRI) is of value. With the increasingly fast sequences, it helps assess the foetal anatomy without requiring maternal sedation, and without being disturbed by the aforementioned factors. In this context, MRI has been validated as an effective technique to assess foetuses suspected of malformations (in particular neurological malformations), although its contribution to the diagnosis of foetal uronephropathies has only been demonstrated in studies carried out with a very limited number of subjects [9—12]. The purpose of this study is to assess the complementary diagnostic contribution and the role in the perinatal care of foetal MRI in the prenatal diagnosis of uronephropathies.
classify the patients into two groups according whether the foetal MRI confirmed the data of the obstetric ultrasound or whether it specified them (contribution of complementary or contradictory data, verified in the follow-up) into six sub-groups according to the initial ultrasound suspicion: suspected renal agenesis, posterior urethral valve in case of bilateral ureteropyelocalyceal dilatation in the male foetus, possibly associated with bladder anomalies (Fig. 1), bilateral nephromegaly with a renal length exceeding + 2 DS (Fig. 2), suspicion of vesicoureteral reflux or stenotic megaureter in case of unilateral or bilateral ureteropyelocalyceal dilatation or bilateral by very asymmetric dilatation without bladder anomaly, suspicion of a uretropelvic junction syndrome in case of pyelocalyceal dilatation without ureteral dilatation, and other. The ‘‘other’’ category includes atypical suspicion of multi-cystic dysplasia (in particular due to their size and/or compressive nature), renal hypotrophy, bladder exstrophy (bladder not seen, parietal sub umbilical irregularities) or hypoperistaltic megabladder/microcolon syndrome. By consensus, we considered that the MRI had an effect on the management of the rest of the pregnancy or birth when it helped modify the obstetric or perinatal care.
Results Patients and methods This retrospective, monocentric study was carried out on pregnant women benefiting from a foetal MRI for suspicion of uropathy or nephropathy abnormalities. A foetal MRI was carried out on all of the patients included, between November 2002 and June 2011, at hôpital de la Timone in Marseille. This MRI followed a so-called diagnostic obstetric ultrasound examination by referring sonographers from a multi-disciplinary prenatal diagnosis centre. The ultrasound examinations were carried out using several successive sonographs: EUB alpha (Hitashi, Tokyo, Japon), IU 22 (Philips, Amsterdam, Pays-Bas) and Voluson E8 (General Electrics, Milwaukee, USA) by means of a convex 4—8 MHz sound, by a referring obstetrician-gynaecologist or radiologist at the prenatal diagnostic centre. The foetal MRI was indicated in a multi-disciplinary staff meeting in order to better characterize the urinary anomaly, assess the state of the renal parenchyma, as well as in case of technical ultrasound difficulties (oligohydranamnios, maternal obesity, etc.). All of the MRI was carried out on a 1.5 T machine (Philips Symphony, Erlangen, Germany). The MRI study began with location sequences and continued with HASTE T2 weighted sequences, then TRUFISP sequences, and T1weighted sequences in the three planes in space [3—5]. Maternal sedation or injection of contract agent was not used in this examination. The MRI was interpreted by two radiologists experienced in this field. The results of the foetal MRI were compared with those of the obstetric ultrasound as well as the ‘‘gold standard’’ grouping postnatal imaging (kidney-bladder ultrasound, cystography, uro-MRI), the surgical findings, or the results of autopsy (in case of uterine foetal death or medical interruption of pregnancy). The analysis of the MRI was used to
Between November 2002 and June 2011, 150 single pregnancies and four twin pregnancies with suspicion of an uronephropathic twin benefited from a complementary MRI. When the foetal MRI was carried out, the age of gestation varied from 21 to 38 weeks of amenorrhoea (WA) with a mean assessed at 30 WA. The MRI examinations were well tolerated by the patients and the foetal movements did not alter the quality of the image, even without maternal sedation. The postnatal data, considered as the gold standard, was only found in 108 of the foetuses (70%). The results were put into several categories according to the initial ultrasound suspicion: suspicion of renal agenesis (20 foetuses or 18.5% including 15 suspicions of unilateral renal agnesis and five suspicions of bilateral agenesis), suspicion of posterior urethral valve (20 foetuses or 18.5%), bilateral nephromegaly (7 foetuses or 6.5%), suspicion of vesicoureteral reflux or stenotic megaureter (14 foetuses or 13%), suspicion of uretro pelvic junction syndrome (24 foetuses or 22.5%), and other (23 foetuses or 21%). The renal anomalies were bilateral in 56 cases (52%) and unilateral in 52 cases (48%). The results of the foetal MRI (combined with the ultrasound follow-up) complied with the neonatal data in 105 of the 108 foetuses, that is, in 97% of the cases, as opposed to 60 out of 108 foetuses, that is, 56% of the cases, with the ultrasound examination alone (Table 1). For three foetuses, the MRI and ultrasound were faulty, finding similar data, and invalidated by the post-natal examinations. As regards the first foetus, the obstetric ultrasound found a dilatation of the pyelocalyceal and bilateral urethral cavities and the MRI confirmed this bilateral but asymmetric dilatation uretheropyelocalyceal dilatation, with a posterior ureter visible without distinct appearance of dilatation. This latter examination concluded as to the possibility of a minor form of posterior urethral valve, a vesicoureteral reflux or stenotic megaureter. The ultrasound carried out at birth was
Please cite this article in press as: Pico H, et al. Contribution of the foetal uro-MRI in the prenatal diagnosis of uronephropathies. Diagnostic and Interventional Imaging (2014), http://dx.doi.org/10.1016/j.diii.2014.02.011
+Model DIII-427; No. of Pages 6
ARTICLE IN PRESS
Contribution of the foetal uro-MRI in the prenatal diagnosis of uronephropathies
3
Figure 1. Male foetus with a posterior urethral valve by ultrasound at 30 WA (a, b) and MRI at 32 WA (c): a: parasagittal section revealing dilatation of the pyelocalyceal cavities and megabladder with thick walls; b: coronal view showing pyelocalyceal dilatation and bilateral ureteral dilatation; c: sagittal section showing dilatation of the posterior urethra (arrow) and megabladder with thick, irregular and notched walls.
within the limits of the norm and only found slight bilateral pyelectasis. In the second foetus, the obstetric ultrasound revealed bilateral pyelocalyceal and ureteral dilatation, the MRI found a similar aspect with dilatation of the posterior urethra without bladder dilatation and suggesting a minor form of posterior urethral valve. The post-natal ultrasound and cystography detected left ureterocele with bilateral uretheropyelocalyceal dilatation indicating stenotic megaureter. The third foetus was also suspected of posterior urethral valve in the obstetric ultrasound. The MRI found a vesicoureteral distension, without dilatation of the pyelocalyceal cavities, with open bladder neck and overly good visibility of the posterior and anterior ureter to suspect an anterior urethral valve. The post-natal diagnosis (ultrasound and retrograde cystography) displayed a bilateral ureteral dilatation and left pyelectasis, associated with a large bladder, a bilateral vesicoureteral reflex predominant on the left and a diverticulum of the anterior ureter. These elements suggested a neuromuscular disorder and, associated with the clinical data, helped diagnose a Prune Belly syndrome. In 72 of the 108 foetuses, the MRI and the obstetric ultrasound provided concordant results (67%), confirmed in 69 foetuses by post-natal assessment. In 17 patients who developed an oligoamniosis (appeared on the average after 27.8 WA), the MRI confirmed the ultrasound diagnosis in 13 cases (76%).
Table 1
In 36 of the 108 foetuses, the MRI provided contradictory or complementary data (33%). It was able to specify the ultrasound diagnosis in four out of 17 foetuses (24%) within a context of oligoamniosis. The care was modified in 16 of these foetuses (15%). The MRI helped invalidate the diagnosis of posterior urethral valve in seven foetuses, mainly by the absence of dilatation of the posterior urethra and the bladder and thereby reassure the parents, allow for a level 1 or 2 delivery in a maternity ward and postpone a post-natal imaging assessment. In four foetuses, the information provided by the MRI led the multi-disciplinary team to propose a medical abortion. This decision was based on a suspicion of dysgenesis of the caudal pole, cloacal dysgenesis, bilateral renal agenesis and severe bilateral renal hypodysplasia. In six foetuses, the MRI detected renal parenchymateous dysplastic lesions, not seen in the ultrasound examination (two foetuses with diffuse bilateral, three with diffuse unilateral and one with focal unilateral dysplastic lesions), in which a post-natal assessment of renal function (kidneybladder ultrasound, blood) was carried out early. Three of the foetuses, two with a suspicion of bilateral uretropelvic junction syndrome, the other with stenotic megaureter or bilateral vesicoureteral reflux, actually had a posterior urethral valve. MRI rectified the diagnosis and thereby early surgical care and a level 3 delivery were indicated. The results of the concordance between MRI and ultrasound for each sub-group are summed up in Table 1.
Summary of the results of the contribution of MRI in the diagnosis of uronephropathies.
Obstetric ultrasound
MRI Specifies
Renal agnesis Posterior urethral valve Nephromegaly RVU or megaureter Uretropelvic junction syndrome Other
7 10 1 6 8 4 36
(35%) (50%) (14%) (43%) (33%) (20%) (33%)
Confirms 13 10 6 8 16 19 72
(65%) (50%) (86%) (57%) (67%) (80%) (67%)
Total 20 20 7 14 24 23 108
Please cite this article in press as: Pico H, et al. Contribution of the foetal uro-MRI in the prenatal diagnosis of uronephropathies. Diagnostic and Interventional Imaging (2014), http://dx.doi.org/10.1016/j.diii.2014.02.011
+Model DIII-427; No. of Pages 6
ARTICLE IN PRESS
4
H. Pico et al. renal vein, which was confirmed by the foetopathology (in utero foetal death). For foetuses with a suspicion of posterior urethral valve, megaureter, vesicoureteral reflux or uretropelvic junction syndrome, the MRI better assessed the ureteral dilatation as well as that of the posterior urethra, thereby helping distinguish these three disorders. It also helped display the renal dysplastic lesions of obstructive origin. In the ‘‘other’’ sub-group, the MRI was in favor of cloacal dysgenesis in one female foetus presenting multiple malformations (renal dysplasia, hydrocolpos, microcolon) and helped detect duplicity with ureterocel and pyelic dilatation of the upper pole in a foetus initially suspected of atypical dysplasia.
Discussion
Figure 2. Foetus at 27 WA. Bilateral and symmetrical nephromegaly with appearance in T2 hypersignal (ssh) of the renal parenchyma (renal polycystitis). Oligohyamnios.
In the category ‘‘suspicion of renal agenesis’’, the MRI revealed ectopic, horse-shaped or hypotrophic kidneys. In the ‘‘nephromegaly’’ category, the MRI found, in one foetus, a heterogeneous appearance in T2 hyposignal of the right kidney parenchyma suggesting thrombosis of the right
Ultrasound is the first type of imaging to assess the foetus. The performance, improved by technical progress (better apparatus, high frequency sound) and availability, make it the ideal method of screening for low risk populations. The foetal MRI is also a safe and effective technique in case of ambiguous signs. Congenital kidney anomalies are often associated with oligohydramnios, which may render the ultrasound evaluation difficult, whereas the foetal MRI is not significantly affected by a reduction in amniotic fluid [6]. In this study, the MRI has, in this situation, confirmed the diagnosis of uronephropathy in 76% of the cases and has provided complementary information in 24% (renal dysplasia, renal agenesis, posterior urethral valve) (Fig. 3). MRI is currently a technique that has been validated for foetal imaging, although it also has its limits (morbid obesity, movement artefacts). Currently, no harmful effects have
Figure 3. Female foetus at 32 WA. Double system with bilateral pyelo-ureteral dilatation predominant at the level of the upper left calyceal group, and left ureterocele (arrow).
Please cite this article in press as: Pico H, et al. Contribution of the foetal uro-MRI in the prenatal diagnosis of uronephropathies. Diagnostic and Interventional Imaging (2014), http://dx.doi.org/10.1016/j.diii.2014.02.011
+Model DIII-427; No. of Pages 6
ARTICLE IN PRESS
Contribution of the foetal uro-MRI in the prenatal diagnosis of uronephropathies been demonstrated. Several studies have been published on the role of MRI in the detection and care of anomalies of the central nervous system and thoracic anomalies, although only a small number of series of cases have been published on the use of MRI in the assessment of foetal uronephropathies [7,8]. However, the MRI has been found able to suspect the aetiology in most hydronephroses. In this study, the MRI helped better analyse the renal parenchyma, the posterior urethra in the foetus of the male phenotype, ureteral dilatations and concomitantly explore the digestive tract. In case of difficulty in seeing the ureters or the renal parenchyma by ultrasound, the MRI is able to do this efficiently. In an identical manner, it is difficult to analyse the foetal ureter by ultrasound (pelvic situation, bone interposition of the pelvis), whereas the MRI eliminates these limits. Similar to the study by Poutamo et al. [9] which noted that urinary tract anomalies were properly diagnosed in 15 out of 22 foetuses by ultrasound and in 20 out of 22 foetuses by MRI, this study also found a better concordance in the diagnoses with MRI than with ultrasound examination (97% concordance with MRI versus 56% with ultrasound). In this study, the MRI changed the obstetric care or postnatal care for 12 foetuses, and recommended a medical abortion for four foetuses [10]. Among these foetuses, 13 presented bilateral renal anomalies detected by ultrasound (81%) [11]. In addition, Cassart’s team [12] demonstrated that MRI may provide more precise information than ultrasound, and influence the obstetric decision. They thereby recommended a medical abortion for three foetuses (renal polycystitis, bilateral renal agenesis and Jeune syndrome) and helped reassure the parents and obstetricians by eliminating a diagnosis of megabladdermicrocolon, and thereby continue the pregnancy in one case. The study by Alamo et al. [13] found similar results with a modification in the care for five foetuses. This information justifies a foetal MRI in the case of bilateral renal anomalies or megabladder while its contribution is more debatable in unilateral disorders (uretopelvic junction syndrome, stenotic megaureter, vesicoureteric reflux and unilateral renal agenesis) especially when the bladder and the quantity of amniotic fluid are normal. In the study by Domenech-Fontenel et al. [14], MRI also helped distinguish dysplastic lesions and dilatation of the pyelocalyceal cavities, as in our study, showing a better analysis of the renal parenchyma by MRI (Fig. 4). The antenatal evaluation of the foetal renal function by puncture of the amniotic fluid of foetal blood [15] was little used in our study due to the risk of inducing major prematurity. Non-invasive methods were preferred (repeated ultrasound, foetal MRI) analyzing the appearance of the renal parenchyma and the quantity of amniotic fluid. Certain methods are being developed and assessed, such as functional imaging by magnetic resonance [16]. This study comprises a number of biases inherent in a retrospective study over a long period of time: multiplicity of sonographers and ultrasounds in particular. In addition, until the recommendations by the technical committee for prenatal ultrasound screening, there has been little codification of the so-called diagnostic ultrasound examination, in particular for the analysis of the foetal urinary tract. This study, due to its retrospective nature, was not carried out in blind conditions. In fact, the radiologists
5
Figure 4. Male foetus with bilateral renal dysplasia associated with dilatation of the pyelocalyceal cavities and an oligohyamnios in MRI at 35 WA, in coronal (a) and parasagittal sections (b).
who interpreted the foetal MRI assisted the prenatal diagnosis staff and/or themselves carried out the obstetric ultrasound examinations. Therefore, this work continues in a prospective manner by protocoling the ultrasound and MRI analysis of the foetal urinary tract.
Conclusion The obstetric ultrasound examination is the first choice method of screening to assess renal foetal anomalies and appears to be sufficient in most cases. This study shows, in a large number of cases, that MRI can help better characterize anomalies of the urinary tract in certain selected cases (bilateral anomalies of the urinary tract, oligohydramnios, technical difficulties, etc.) or in certain indications (suspicion of cloaque or megabladder-microcolon). MRI combined with ultrasound can provide a more precise diagnosis, in particular due to the complementary analysis of the renal parenchyma, ureters and posterior urethra, and better determine the prognosis or even modify the perinatal care. Although high frequency ultrasound has a full role to play, MRI seems to be unavoidable when the technical ultrasound conditions are poor and for the concomitant analysis of the foetal digestive tract.
Disclosure of interest The authors declare that there are no conflicts of interest with respect to this article.
References [1] Martín C, Darnell A, Durán C, Bermúdez P, Mellado F, Rigol S. Magnetic resonance imaging of the intrauterine fetal genitourinary tract: normal anatomy and pathology. Abdom Imaging 2004;29(3):286—302.
Please cite this article in press as: Pico H, et al. Contribution of the foetal uro-MRI in the prenatal diagnosis of uronephropathies. Diagnostic and Interventional Imaging (2014), http://dx.doi.org/10.1016/j.diii.2014.02.011
+Model DIII-427; No. of Pages 6
ARTICLE IN PRESS
6
H. Pico et al.
[2] Greig JD, Raine PA, Young DG, Azmy AF, MacKenzie JR, Danskin F, et al. Value of antenatal diagnosis of abnormalities of the urinary tract. BMJ 1989;298(6685):1417—9. [3] Huppert BJ, Brandt KR, Ramin KD, King BF. Single-shot fast spinecho MR imaging of the fetus: a pictorial essay. Radiographics 1999;19SpecNo:S215—27. [4] Hubbard AM, Harty MP. MRI for the assessment of the malformed fetus. Baillieres Best Pract Res Clin Obstet Gynaecol 2000;14(4):629—50. [5] Amin RS, Nikolaidis P, Kawashima A, Kramer LA, Ernst RD. Normal anatomy of the fetus at MR imaging. Radiographics 1999;19 SpecNo:S201—14. [6] Abdelazim IA, Abdelrazak KM, Ramy AR, Mounib AM. Complementary roles of prenatal sonography and magnetic resonance imaging in diagnosis of fetal renalanomalies. Aust N Z J Obstet Gynaecol 2010;50(3):237—41, http://dx.doi.org/10.1111/j.1479-828X. 2010.01153.x. [7] 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(3):209—12, http://dx.doi.org/10.1016/j.ijgo.2010.07.024. Epub 2010 Sep 25. [8] Hawkins JS, Dashe JS, Twickler DM. Magnetic resonance imaging diagnosis of severe fetal renal anomalies. Am J Obstet Gynecol 2008;198(3):328.e1—5. Epub 2007 Nov 26. [9] 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(1): 65—71.
[10] 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(11):1563—9. [11] Maugey-Laulom B, Chateil JF. Diagnostic anténatal des uronéphropathies malformatives. EMC - radiologie et imagerie médicale : génito-urinaire - gynéco-obstétricale - mammaire 2011:1—17 [Article 34-760-A-25]. [12] Cassart M, Massez A, Metens T, Rypens F, Lambot MA, Hall M, et al. Complementary role of MRI after sonography in assessing bilateral urinary tract anomalies in the fetus. AJR Am J Roentgenol 2004;182(3):689—95. [13] Alamo L, Laswad T, Schnyder P, Meuli R, Vial Y, Osterheld MC, et al. Fetal MRI as complement to US in the diagnosis and characterization of anomalies of the genito-urinary tract. Eur J Radiol 2010;76(2):258—64, http://dx.doi.org/10.1016/j.ejrad.2009.06.030. Epub 2009 Jul 29. [14] Domenech-Fontenel C, Baunin C, Domenech B, Sarramon MF, Guitard J, Rolland M, et al. Value of MR imaging of the fetal kidney. J Radiol 2002;83(9 Pt 1):1073—7. [15] Nicolini U, Spelzini F. Invasive assessment of fetal renal abnormalities: urinalysis, fetal blood sampling and biopsy. Prenat Diagn 2001;21:964—9. [16] Chaumoitre K, Colavolpe N, Shojai R, Sarran A, D’ Ercole C, Panuel M. Diffusion-weighted magnetic resonance imaging with apparent diffusion coefficient (ADC) determination in normal and pathological fetal kidneys. Ultrasound Obstet Gynecol 2007;29(1):22—31.
Please cite this article in press as: Pico H, et al. Contribution of the foetal uro-MRI in the prenatal diagnosis of uronephropathies. Diagnostic and Interventional Imaging (2014), http://dx.doi.org/10.1016/j.diii.2014.02.011
ARTICLE IN PRESS
DIII-427; No. of Pages 6
Diagnostic and Interventional Imaging (2014) xxx, xxx—xxx
ORIGINAL ARTICLE / Genitourinary imaging
Contribution of the foetal uro-MRI in the prenatal diagnosis of uronephropathies H. Pico a,∗, A. Dabadie a, B. Bourliere-Najean a, N. Philip b, M. Capelle c, A. Aschero a, E. Quarello d, J.-M. Guys e, G. Hery e, P. Petit a, G. Gorincour a a
Service d’imagerie pédiatrique et prénatale, hôpital de la Timone, 264, rue Saint-Pierre, 13385 Marseille cedex 5, France b Département de génétique médicale, hôpital de la Timone, 264, rue Saint-Pierre, 13385 Marseille cedex 5, France c Centre de diagnostic prénatal, hôpital de la Timone, 264, rue Saint-Pierre, 13385 Marseille cedex 5, France d Service de gynécologie obstétrique, hôpital Saint-Joseph, 26, boulevard de Louvain, 13285 Marseille cedex 08, France e Service de chirurgie infantile, hôpital de la Timone, 264, rue Saint-Pierre, 13385 Marseille cedex 5, France
KEYWORDS Pregnant; Urogenital abnormalities; Prenatal ultrasonography; Magnetic resonance imaging
∗
Abstract Purpose: To study the complementary diagnostic value and role in the perinatal management of foetal MRI in the prenatal diagnosis of abnormalities of the urinary tract. Patients and methods: Retrospective monocentric study from November 2002 to June 2011 of foetuses benefiting from an MRI after ultrasound diagnosis of uronephropathy abnormalities. Ultrasound and MRI data were compared with postnatal radiological and/or surgical data or with the foetopathology. The MRI analysis focused on the diagnostic concordance with the ultrasound, the complementary diagnostic contribution and/or a change in perinatal care. Results: Of the 154 MRI examined, a follow-up was obtained for 108 cases. The indications for MRI were classified into six groups: suspected renal agenesis (n = 20, 18.5%), posterior urethral valve (n = 20, 18.5%), reflux or megaureter (n = 14, 13%), uretropelvic junction syndrome (n = 24, 22.5%), enlarged kidneys (n = 7, 6.5%) and others (n = 23, 21%). The information supplied by ultrasound was confirmed by MRI in 72 patients (67%). MRI provided additional data for 36 patients (33%) and changed the perinatal care for 16 patients (15%). Conclusion: Foetal uro-MRI is a useful complementary tool in the prenatal diagnosis of some uropathy abnormalities. © 2014 Published by Elsevier Masson SAS on behalf of the Éditions françaises de radiologie.
Corresponding author. E-mail address: [email protected] (H. Pico).
2211-5684/$ — see front matter © 2014 Published by Elsevier Masson SAS on behalf of the Éditions françaises de radiologie. http://dx.doi.org/10.1016/j.diii.2014.02.011
Please cite this article in press as: Pico H, et al. Contribution of the foetal uro-MRI in the prenatal diagnosis of uronephropathies. Diagnostic and Interventional Imaging (2014), http://dx.doi.org/10.1016/j.diii.2014.02.011
+Model DIII-427; No. of Pages 6
ARTICLE IN PRESS
2
H. Pico et al.
Malformations in the foetal urinary tract are fairly common, found in 0.1 to 1% of all pregnancies and account for about 30 to 50% of the abnormalities found at birth [1]. They are most often detected by obstectrical ultrasound, the examination that remains the screening reference [2]. The spectrum of malformation is wide and the greater the reduction in amniotic fluid and the more the malformation is bilateral, the more unfavourable the prognosis. The ultrasound may be unable to provide an exact diagnosis and prognosis of the uronephropathy, especially when the conditions are unfavourable (maternal obesity, unfavourable position of the foetus, oligohydramnios). In this situation, magnetic resonance imaging (MRI) is of value. With the increasingly fast sequences, it helps assess the foetal anatomy without requiring maternal sedation, and without being disturbed by the aforementioned factors. In this context, MRI has been validated as an effective technique to assess foetuses suspected of malformations (in particular neurological malformations), although its contribution to the diagnosis of foetal uronephropathies has only been demonstrated in studies carried out with a very limited number of subjects [9—12]. The purpose of this study is to assess the complementary diagnostic contribution and the role in the perinatal care of foetal MRI in the prenatal diagnosis of uronephropathies.
classify the patients into two groups according whether the foetal MRI confirmed the data of the obstetric ultrasound or whether it specified them (contribution of complementary or contradictory data, verified in the follow-up) into six sub-groups according to the initial ultrasound suspicion: suspected renal agenesis, posterior urethral valve in case of bilateral ureteropyelocalyceal dilatation in the male foetus, possibly associated with bladder anomalies (Fig. 1), bilateral nephromegaly with a renal length exceeding + 2 DS (Fig. 2), suspicion of vesicoureteral reflux or stenotic megaureter in case of unilateral or bilateral ureteropyelocalyceal dilatation or bilateral by very asymmetric dilatation without bladder anomaly, suspicion of a uretropelvic junction syndrome in case of pyelocalyceal dilatation without ureteral dilatation, and other. The ‘‘other’’ category includes atypical suspicion of multi-cystic dysplasia (in particular due to their size and/or compressive nature), renal hypotrophy, bladder exstrophy (bladder not seen, parietal sub umbilical irregularities) or hypoperistaltic megabladder/microcolon syndrome. By consensus, we considered that the MRI had an effect on the management of the rest of the pregnancy or birth when it helped modify the obstetric or perinatal care.
Results Patients and methods This retrospective, monocentric study was carried out on pregnant women benefiting from a foetal MRI for suspicion of uropathy or nephropathy abnormalities. A foetal MRI was carried out on all of the patients included, between November 2002 and June 2011, at hôpital de la Timone in Marseille. This MRI followed a so-called diagnostic obstetric ultrasound examination by referring sonographers from a multi-disciplinary prenatal diagnosis centre. The ultrasound examinations were carried out using several successive sonographs: EUB alpha (Hitashi, Tokyo, Japon), IU 22 (Philips, Amsterdam, Pays-Bas) and Voluson E8 (General Electrics, Milwaukee, USA) by means of a convex 4—8 MHz sound, by a referring obstetrician-gynaecologist or radiologist at the prenatal diagnostic centre. The foetal MRI was indicated in a multi-disciplinary staff meeting in order to better characterize the urinary anomaly, assess the state of the renal parenchyma, as well as in case of technical ultrasound difficulties (oligohydranamnios, maternal obesity, etc.). All of the MRI was carried out on a 1.5 T machine (Philips Symphony, Erlangen, Germany). The MRI study began with location sequences and continued with HASTE T2 weighted sequences, then TRUFISP sequences, and T1weighted sequences in the three planes in space [3—5]. Maternal sedation or injection of contract agent was not used in this examination. The MRI was interpreted by two radiologists experienced in this field. The results of the foetal MRI were compared with those of the obstetric ultrasound as well as the ‘‘gold standard’’ grouping postnatal imaging (kidney-bladder ultrasound, cystography, uro-MRI), the surgical findings, or the results of autopsy (in case of uterine foetal death or medical interruption of pregnancy). The analysis of the MRI was used to
Between November 2002 and June 2011, 150 single pregnancies and four twin pregnancies with suspicion of an uronephropathic twin benefited from a complementary MRI. When the foetal MRI was carried out, the age of gestation varied from 21 to 38 weeks of amenorrhoea (WA) with a mean assessed at 30 WA. The MRI examinations were well tolerated by the patients and the foetal movements did not alter the quality of the image, even without maternal sedation. The postnatal data, considered as the gold standard, was only found in 108 of the foetuses (70%). The results were put into several categories according to the initial ultrasound suspicion: suspicion of renal agenesis (20 foetuses or 18.5% including 15 suspicions of unilateral renal agnesis and five suspicions of bilateral agenesis), suspicion of posterior urethral valve (20 foetuses or 18.5%), bilateral nephromegaly (7 foetuses or 6.5%), suspicion of vesicoureteral reflux or stenotic megaureter (14 foetuses or 13%), suspicion of uretro pelvic junction syndrome (24 foetuses or 22.5%), and other (23 foetuses or 21%). The renal anomalies were bilateral in 56 cases (52%) and unilateral in 52 cases (48%). The results of the foetal MRI (combined with the ultrasound follow-up) complied with the neonatal data in 105 of the 108 foetuses, that is, in 97% of the cases, as opposed to 60 out of 108 foetuses, that is, 56% of the cases, with the ultrasound examination alone (Table 1). For three foetuses, the MRI and ultrasound were faulty, finding similar data, and invalidated by the post-natal examinations. As regards the first foetus, the obstetric ultrasound found a dilatation of the pyelocalyceal and bilateral urethral cavities and the MRI confirmed this bilateral but asymmetric dilatation uretheropyelocalyceal dilatation, with a posterior ureter visible without distinct appearance of dilatation. This latter examination concluded as to the possibility of a minor form of posterior urethral valve, a vesicoureteral reflux or stenotic megaureter. The ultrasound carried out at birth was
Please cite this article in press as: Pico H, et al. Contribution of the foetal uro-MRI in the prenatal diagnosis of uronephropathies. Diagnostic and Interventional Imaging (2014), http://dx.doi.org/10.1016/j.diii.2014.02.011
+Model DIII-427; No. of Pages 6
ARTICLE IN PRESS
Contribution of the foetal uro-MRI in the prenatal diagnosis of uronephropathies
3
Figure 1. Male foetus with a posterior urethral valve by ultrasound at 30 WA (a, b) and MRI at 32 WA (c): a: parasagittal section revealing dilatation of the pyelocalyceal cavities and megabladder with thick walls; b: coronal view showing pyelocalyceal dilatation and bilateral ureteral dilatation; c: sagittal section showing dilatation of the posterior urethra (arrow) and megabladder with thick, irregular and notched walls.
within the limits of the norm and only found slight bilateral pyelectasis. In the second foetus, the obstetric ultrasound revealed bilateral pyelocalyceal and ureteral dilatation, the MRI found a similar aspect with dilatation of the posterior urethra without bladder dilatation and suggesting a minor form of posterior urethral valve. The post-natal ultrasound and cystography detected left ureterocele with bilateral uretheropyelocalyceal dilatation indicating stenotic megaureter. The third foetus was also suspected of posterior urethral valve in the obstetric ultrasound. The MRI found a vesicoureteral distension, without dilatation of the pyelocalyceal cavities, with open bladder neck and overly good visibility of the posterior and anterior ureter to suspect an anterior urethral valve. The post-natal diagnosis (ultrasound and retrograde cystography) displayed a bilateral ureteral dilatation and left pyelectasis, associated with a large bladder, a bilateral vesicoureteral reflex predominant on the left and a diverticulum of the anterior ureter. These elements suggested a neuromuscular disorder and, associated with the clinical data, helped diagnose a Prune Belly syndrome. In 72 of the 108 foetuses, the MRI and the obstetric ultrasound provided concordant results (67%), confirmed in 69 foetuses by post-natal assessment. In 17 patients who developed an oligoamniosis (appeared on the average after 27.8 WA), the MRI confirmed the ultrasound diagnosis in 13 cases (76%).
Table 1
In 36 of the 108 foetuses, the MRI provided contradictory or complementary data (33%). It was able to specify the ultrasound diagnosis in four out of 17 foetuses (24%) within a context of oligoamniosis. The care was modified in 16 of these foetuses (15%). The MRI helped invalidate the diagnosis of posterior urethral valve in seven foetuses, mainly by the absence of dilatation of the posterior urethra and the bladder and thereby reassure the parents, allow for a level 1 or 2 delivery in a maternity ward and postpone a post-natal imaging assessment. In four foetuses, the information provided by the MRI led the multi-disciplinary team to propose a medical abortion. This decision was based on a suspicion of dysgenesis of the caudal pole, cloacal dysgenesis, bilateral renal agenesis and severe bilateral renal hypodysplasia. In six foetuses, the MRI detected renal parenchymateous dysplastic lesions, not seen in the ultrasound examination (two foetuses with diffuse bilateral, three with diffuse unilateral and one with focal unilateral dysplastic lesions), in which a post-natal assessment of renal function (kidneybladder ultrasound, blood) was carried out early. Three of the foetuses, two with a suspicion of bilateral uretropelvic junction syndrome, the other with stenotic megaureter or bilateral vesicoureteral reflux, actually had a posterior urethral valve. MRI rectified the diagnosis and thereby early surgical care and a level 3 delivery were indicated. The results of the concordance between MRI and ultrasound for each sub-group are summed up in Table 1.
Summary of the results of the contribution of MRI in the diagnosis of uronephropathies.
Obstetric ultrasound
MRI Specifies
Renal agnesis Posterior urethral valve Nephromegaly RVU or megaureter Uretropelvic junction syndrome Other
7 10 1 6 8 4 36
(35%) (50%) (14%) (43%) (33%) (20%) (33%)
Confirms 13 10 6 8 16 19 72
(65%) (50%) (86%) (57%) (67%) (80%) (67%)
Total 20 20 7 14 24 23 108
Please cite this article in press as: Pico H, et al. Contribution of the foetal uro-MRI in the prenatal diagnosis of uronephropathies. Diagnostic and Interventional Imaging (2014), http://dx.doi.org/10.1016/j.diii.2014.02.011
+Model DIII-427; No. of Pages 6
ARTICLE IN PRESS
4
H. Pico et al. renal vein, which was confirmed by the foetopathology (in utero foetal death). For foetuses with a suspicion of posterior urethral valve, megaureter, vesicoureteral reflux or uretropelvic junction syndrome, the MRI better assessed the ureteral dilatation as well as that of the posterior urethra, thereby helping distinguish these three disorders. It also helped display the renal dysplastic lesions of obstructive origin. In the ‘‘other’’ sub-group, the MRI was in favor of cloacal dysgenesis in one female foetus presenting multiple malformations (renal dysplasia, hydrocolpos, microcolon) and helped detect duplicity with ureterocel and pyelic dilatation of the upper pole in a foetus initially suspected of atypical dysplasia.
Discussion
Figure 2. Foetus at 27 WA. Bilateral and symmetrical nephromegaly with appearance in T2 hypersignal (ssh) of the renal parenchyma (renal polycystitis). Oligohyamnios.
In the category ‘‘suspicion of renal agenesis’’, the MRI revealed ectopic, horse-shaped or hypotrophic kidneys. In the ‘‘nephromegaly’’ category, the MRI found, in one foetus, a heterogeneous appearance in T2 hyposignal of the right kidney parenchyma suggesting thrombosis of the right
Ultrasound is the first type of imaging to assess the foetus. The performance, improved by technical progress (better apparatus, high frequency sound) and availability, make it the ideal method of screening for low risk populations. The foetal MRI is also a safe and effective technique in case of ambiguous signs. Congenital kidney anomalies are often associated with oligohydramnios, which may render the ultrasound evaluation difficult, whereas the foetal MRI is not significantly affected by a reduction in amniotic fluid [6]. In this study, the MRI has, in this situation, confirmed the diagnosis of uronephropathy in 76% of the cases and has provided complementary information in 24% (renal dysplasia, renal agenesis, posterior urethral valve) (Fig. 3). MRI is currently a technique that has been validated for foetal imaging, although it also has its limits (morbid obesity, movement artefacts). Currently, no harmful effects have
Figure 3. Female foetus at 32 WA. Double system with bilateral pyelo-ureteral dilatation predominant at the level of the upper left calyceal group, and left ureterocele (arrow).
Please cite this article in press as: Pico H, et al. Contribution of the foetal uro-MRI in the prenatal diagnosis of uronephropathies. Diagnostic and Interventional Imaging (2014), http://dx.doi.org/10.1016/j.diii.2014.02.011
+Model DIII-427; No. of Pages 6
ARTICLE IN PRESS
Contribution of the foetal uro-MRI in the prenatal diagnosis of uronephropathies been demonstrated. Several studies have been published on the role of MRI in the detection and care of anomalies of the central nervous system and thoracic anomalies, although only a small number of series of cases have been published on the use of MRI in the assessment of foetal uronephropathies [7,8]. However, the MRI has been found able to suspect the aetiology in most hydronephroses. In this study, the MRI helped better analyse the renal parenchyma, the posterior urethra in the foetus of the male phenotype, ureteral dilatations and concomitantly explore the digestive tract. In case of difficulty in seeing the ureters or the renal parenchyma by ultrasound, the MRI is able to do this efficiently. In an identical manner, it is difficult to analyse the foetal ureter by ultrasound (pelvic situation, bone interposition of the pelvis), whereas the MRI eliminates these limits. Similar to the study by Poutamo et al. [9] which noted that urinary tract anomalies were properly diagnosed in 15 out of 22 foetuses by ultrasound and in 20 out of 22 foetuses by MRI, this study also found a better concordance in the diagnoses with MRI than with ultrasound examination (97% concordance with MRI versus 56% with ultrasound). In this study, the MRI changed the obstetric care or postnatal care for 12 foetuses, and recommended a medical abortion for four foetuses [10]. Among these foetuses, 13 presented bilateral renal anomalies detected by ultrasound (81%) [11]. In addition, Cassart’s team [12] demonstrated that MRI may provide more precise information than ultrasound, and influence the obstetric decision. They thereby recommended a medical abortion for three foetuses (renal polycystitis, bilateral renal agenesis and Jeune syndrome) and helped reassure the parents and obstetricians by eliminating a diagnosis of megabladdermicrocolon, and thereby continue the pregnancy in one case. The study by Alamo et al. [13] found similar results with a modification in the care for five foetuses. This information justifies a foetal MRI in the case of bilateral renal anomalies or megabladder while its contribution is more debatable in unilateral disorders (uretopelvic junction syndrome, stenotic megaureter, vesicoureteric reflux and unilateral renal agenesis) especially when the bladder and the quantity of amniotic fluid are normal. In the study by Domenech-Fontenel et al. [14], MRI also helped distinguish dysplastic lesions and dilatation of the pyelocalyceal cavities, as in our study, showing a better analysis of the renal parenchyma by MRI (Fig. 4). The antenatal evaluation of the foetal renal function by puncture of the amniotic fluid of foetal blood [15] was little used in our study due to the risk of inducing major prematurity. Non-invasive methods were preferred (repeated ultrasound, foetal MRI) analyzing the appearance of the renal parenchyma and the quantity of amniotic fluid. Certain methods are being developed and assessed, such as functional imaging by magnetic resonance [16]. This study comprises a number of biases inherent in a retrospective study over a long period of time: multiplicity of sonographers and ultrasounds in particular. In addition, until the recommendations by the technical committee for prenatal ultrasound screening, there has been little codification of the so-called diagnostic ultrasound examination, in particular for the analysis of the foetal urinary tract. This study, due to its retrospective nature, was not carried out in blind conditions. In fact, the radiologists
5
Figure 4. Male foetus with bilateral renal dysplasia associated with dilatation of the pyelocalyceal cavities and an oligohyamnios in MRI at 35 WA, in coronal (a) and parasagittal sections (b).
who interpreted the foetal MRI assisted the prenatal diagnosis staff and/or themselves carried out the obstetric ultrasound examinations. Therefore, this work continues in a prospective manner by protocoling the ultrasound and MRI analysis of the foetal urinary tract.
Conclusion The obstetric ultrasound examination is the first choice method of screening to assess renal foetal anomalies and appears to be sufficient in most cases. This study shows, in a large number of cases, that MRI can help better characterize anomalies of the urinary tract in certain selected cases (bilateral anomalies of the urinary tract, oligohydramnios, technical difficulties, etc.) or in certain indications (suspicion of cloaque or megabladder-microcolon). MRI combined with ultrasound can provide a more precise diagnosis, in particular due to the complementary analysis of the renal parenchyma, ureters and posterior urethra, and better determine the prognosis or even modify the perinatal care. Although high frequency ultrasound has a full role to play, MRI seems to be unavoidable when the technical ultrasound conditions are poor and for the concomitant analysis of the foetal digestive tract.
Disclosure of interest The authors declare that there are no conflicts of interest with respect to this article.
References [1] Martín C, Darnell A, Durán C, Bermúdez P, Mellado F, Rigol S. Magnetic resonance imaging of the intrauterine fetal genitourinary tract: normal anatomy and pathology. Abdom Imaging 2004;29(3):286—302.
Please cite this article in press as: Pico H, et al. Contribution of the foetal uro-MRI in the prenatal diagnosis of uronephropathies. Diagnostic and Interventional Imaging (2014), http://dx.doi.org/10.1016/j.diii.2014.02.011
+Model DIII-427; No. of Pages 6
ARTICLE IN PRESS
6
H. Pico et al.
[2] Greig JD, Raine PA, Young DG, Azmy AF, MacKenzie JR, Danskin F, et al. Value of antenatal diagnosis of abnormalities of the urinary tract. BMJ 1989;298(6685):1417—9. [3] Huppert BJ, Brandt KR, Ramin KD, King BF. Single-shot fast spinecho MR imaging of the fetus: a pictorial essay. Radiographics 1999;19SpecNo:S215—27. [4] Hubbard AM, Harty MP. MRI for the assessment of the malformed fetus. Baillieres Best Pract Res Clin Obstet Gynaecol 2000;14(4):629—50. [5] Amin RS, Nikolaidis P, Kawashima A, Kramer LA, Ernst RD. Normal anatomy of the fetus at MR imaging. Radiographics 1999;19 SpecNo:S201—14. [6] Abdelazim IA, Abdelrazak KM, Ramy AR, Mounib AM. Complementary roles of prenatal sonography and magnetic resonance imaging in diagnosis of fetal renalanomalies. Aust N Z J Obstet Gynaecol 2010;50(3):237—41, http://dx.doi.org/10.1111/j.1479-828X. 2010.01153.x. [7] 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(3):209—12, http://dx.doi.org/10.1016/j.ijgo.2010.07.024. Epub 2010 Sep 25. [8] Hawkins JS, Dashe JS, Twickler DM. Magnetic resonance imaging diagnosis of severe fetal renal anomalies. Am J Obstet Gynecol 2008;198(3):328.e1—5. Epub 2007 Nov 26. [9] 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(1): 65—71.
[10] 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(11):1563—9. [11] Maugey-Laulom B, Chateil JF. Diagnostic anténatal des uronéphropathies malformatives. EMC - radiologie et imagerie médicale : génito-urinaire - gynéco-obstétricale - mammaire 2011:1—17 [Article 34-760-A-25]. [12] Cassart M, Massez A, Metens T, Rypens F, Lambot MA, Hall M, et al. Complementary role of MRI after sonography in assessing bilateral urinary tract anomalies in the fetus. AJR Am J Roentgenol 2004;182(3):689—95. [13] Alamo L, Laswad T, Schnyder P, Meuli R, Vial Y, Osterheld MC, et al. Fetal MRI as complement to US in the diagnosis and characterization of anomalies of the genito-urinary tract. Eur J Radiol 2010;76(2):258—64, http://dx.doi.org/10.1016/j.ejrad.2009.06.030. Epub 2009 Jul 29. [14] Domenech-Fontenel C, Baunin C, Domenech B, Sarramon MF, Guitard J, Rolland M, et al. Value of MR imaging of the fetal kidney. J Radiol 2002;83(9 Pt 1):1073—7. [15] Nicolini U, Spelzini F. Invasive assessment of fetal renal abnormalities: urinalysis, fetal blood sampling and biopsy. Prenat Diagn 2001;21:964—9. [16] Chaumoitre K, Colavolpe N, Shojai R, Sarran A, D’ Ercole C, Panuel M. Diffusion-weighted magnetic resonance imaging with apparent diffusion coefficient (ADC) determination in normal and pathological fetal kidneys. Ultrasound Obstet Gynecol 2007;29(1):22—31.
Please cite this article in press as: Pico H, et al. Contribution of the foetal uro-MRI in the prenatal diagnosis of uronephropathies. Diagnostic and Interventional Imaging (2014), http://dx.doi.org/10.1016/j.diii.2014.02.011