In utero MRI diagnosis of fetal malformations in ...scholar.cu.edu.eg/?q=sahars/files/oligo_ejrnm_2016.pdf · volume (oligohydramnios), are often associated with con-genital anomalies,

The Egyptian Journal of Radiology and Nuclear Medicine xxx (2016) xxx–xxx

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The Egyptian Journal of Radiology and Nuclear Medicine

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Original Article

In utero MRI diagnosis of fetal malformations inoligohydramnios pregnancies

http://dx.doi.org/10.1016/j.ejrnm.2016.06.0040378-603X/� 2016 The Egyptian Society of Radiology and Nuclear Medicine. Production and hosting by Elsevier.This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).

Abbreviations: Abd, abdominal; ACC, agenesis of corpus callosum; ARPKD, autosomal recessive polycystic kidney; bilat, bilateral; BV, born vicerebellar hypoplasia; CMV, cytomegalovirus; CT, computed tomography; DWM, Dandy-Walker malformation; GA, gestational age; JSRD, Joubert sand related cerebellar disorders; L, left; LH, left heart; MCDK, multi-cystic dysplastic kidney; MKS, Meckel Gruber syndrome; MMH, megacystis mhypoperistalsis; MRI, magnetic resonance imaging; MRU, magnetic resonance urography; MTS, molar tooth sign; Obst, obstruction; PC,cephalocele; PM, post-mortem; Post, posterior; PUJ, pelvi-ureteric junction; PUV, posterior urethral valve; RH, right heart; SA, spontaneous abortherapeutic abortion; UB, urinary bladder; Unilat, unilateral; US, ultrasonography; UV, uretero-vesical; VCUG, voiding cysto-urethrograventriculomegaly; VSD, ventricular septal defect.

Peer review under responsibility of The Egyptian Society of Radiology and Nuclear Medicine.⇑ Corresponding author at: 32 Falaki Street, Bab El-Louq square, Apartment #16, Cairo 11111, Egypt. Fax: +20 2 27940102.

E-mail addresses: [email protected] (A.H. Said), [email protected] (E. El-Kattan), [email protected] (A.K. [email protected] (S. Saleem).

Please cite this article in press as: Said AH et al. In utero MRI diagnosis of fetal malformations in oligohydramnios pregnancies.Radiol Nucl Med (2016), http://dx.doi.org/10.1016/j.ejrnm.2016.06.004

Ahmed Hesham Said a,⇑, Eman El-Kattan b, Ahmed K. Abdel-Hakeem c, Sahar Saleemd

aRadiology Department, Faculty of Medicine, Beni Suef University, Beni Suef, EgyptbObstetrics and Gynaecology Department, Kasr Al-Ainy Faculty of Medicine - Cairo University, Cairo, EgyptcObstetrics and Gynaecology Department, Faculty of Medicine - Minia University, Minia, EgyptdRadiology Department, Kasr Al-Ainy Faculty of Medicine, Cairo University, Cairo, Egypt

a r t i c l e i n f o

Article history:Received 24 April 2016Accepted 6 June 2016Available online xxxx

Keywords:OligohydramniosFetal MRIFetal malformations

a b s t r a c t

Objective: To evaluate the role of MRI in assessing Ultrasonographically (US)-suspectedfetal malformations associated with oligohydramnios.Methods: We performed MRI in 43 oligohydramnios pregnancies referred withUS-suspected fetal malformations at a mean of 25.5 weeks’ gestation. MRI findings werecorrelated with US data and outcome measures.Results: MRI correctly diagnosed one normal fetus suspected to have posterior cephalocele.In the remaining 42 fetuses who had malformations involving their urinary systems(n = 36), brains (n = 23), bones (n = 4), hearts (n = 3), and hepatobiliary (n = 3), MRI con-firmed US diagnosis in 25 fetuses (58.1%), and added US-occult findings in 14 (32.5%) thatwere mainly related to the brain, urinary and hepatobiliary system. In 2 fetuses (4.7%), MRIadded findings but missed data correctly detected by US in another 2 fetuses. MRI missedfetal skeletal and cardiac function abnormalities correctly detected by US. MRI accuratelydetected multiple body system abnormalities that aided prenatal correct diagnosis ofsyndromes including Meckel Gruber (n = 15) and Joubert syndrome and related cerebellardisorders (n = 1).Conclusion: MRI is valuable in evaluating suspected fetal malformations especiallythose related to brain and urinary system when ultrasound is inconclusive owing tooligohydramnios. Fetal MRI can add findings that may modify prenatal diagnosis.� 2016 The Egyptian Society of Radiology and Nuclear Medicine. Production and hosting byElsevier. This is an open access article under the CC BY-NC-ND license (http://creativecom-

mons.org/licenses/by-nc-nd/4.0/).

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Egypt J

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http://dx.doi.org/10.1016/j.ejrnm.2016.06.004


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2 A.H. Said et al. / The Egyptian Journal of Radiology and Nuclear Medicine xxx (2016) xxx–xxx

1. Introduction

The amniotic fluid that surrounds the fetus is necessaryfor its proper development. Fetal urine is themain source ofamniotic fluid in the last two-thirds of pregnancy [1].Pregnancies associated with inadequacy of amniotic fluidvolume (oligohydramnios), are often associated with con-genital anomalies, both deformations and malformations[2]. Deformation is the process of disfiguring a pre-existing part of the body, while malformation is the processof disrupting the original stages of organ development [3].In oligohydramnios sequence, the decrease in fluid causesintrauterine mechanical constraints that result in fetaldeformations of flat facial profile (Potter’s facies), limbdeformities, chest compression and pulmonary hypoplasia[1], while fetal malformations associated with oligohy-dramnios are mainly urinary, musculoskeletal, digestiveand cardiac in nature [2]. Oligohydramnios has a high peri-natal mortality rate and requires careful fetal examination[4].

Although ultrasonography (US) remains the primaryimaging technique for evaluating the developing fetus,oligohydramnios implies significant limitations to USassessment of fetal anatomy and suspected malformations[1,5]. MR imaging does not suffer from oligohydramniosrestraints and has proved to be a useful prenatal imagingmodality of fetal abnormalities [6,7].

The aim of this study was to assess the role of MRI inassessing ultrasonographically suspected fetal malforma-tions associated with oligohydramnios.

2. Materials and methods

We performed MRI for 43 consecutive oligohydramniossingleton pregnancies referred with US-suspected fetalmalformations, in this institutional-approved study. The

Fig. 1. Megacystis at 30 weeks gestation. Oligohydramnios pregnancy referred wSagittal 2D-US image of the lower fetal abdomen and pelvis shows the lower partkeyhole appearance. The findings suggest obstruction by a posterior urethral valvdue to the limited field of view of US image. Right: Sagittal T2-weighted SSFP imurinary bladder (arrowheads) and confirmed the dilated posterior urethra (arro

Please cite this article in press as: Said AH et al. In utero MRI diagnosiRadiol Nucl Med (2016), http://dx.doi.org/10.1016/j.ejrnm.2016.06.004

mean maternal age was 25 years (SD 5.2, range 18–40).The mothers gave no history of ruptured membranes,hypertension, diabetes mellitus, or intake of medicationsduring the current pregnancy. Twenty-one pregnancieswere the result of consanguineous marriages. Thirteenpatients gave past history of 19 pregnancies with anoma-lous fetuses that included autosomal recessive polycystickidney disease (ARPKD) (n = 7), Meckel Gruber syndrome(MKS) (n = 9), anencephaly (n = 1), and posterior cephalo-cele (PC) (n = 2) (see Figs. 1 and 2).

All examined pregnancies were singleton at an averageof 25.5 weeks of gestation (SD 6) (range 17–39). Thegestational age (GA) was based on the last menstrual per-iod and/or the earliest US biometric measurements doneduring the pregnancy (see Figs. 3–5).

All pregnancies referred to MRI showed significantoligohydramnios (Amniotic Fluid Index was less than5 cm) and were associated with suspected fetal malforma-tion according to detailed prenatal 2D- and 3D-US studies.Only primary fetal malformations were included in ourstudy. Fetal deformations, such as pulmonary hypoplasiaand skeletal deformities that result from prolonged oligo-hydramnios were not studied.

US examination was performed at specialized obstetricUS imaging unit at our institution using 3.5–5 MHZ 3Dtransducer (Voluson 730 ProV, GE Healthcare, Milwaukee,WI, USA). An obstetric record was provided for each patientincluding fetal measurements, amount of amniotic fluid,and complete assessment for fetal anomalies. The staticand real-time digital images of all of the US studies werearchived.

Fetal MRI was performed in the same day or within3 days of the US examination (average 1.09 SD 1.1 days)using 1.5 T superconducting systems (Intera, Philips Medi-cal Systems, Best, Netherlands or Gyroscan Achieva, PhilipsMedical Systems, Best, Netherlands) using a phased-array

ith US findings of markedly enlarged urinary bladder (megacystis). Left:of a hugely dilated urinary bladder and a dilated posterior urethra giving ae (PUV). The full extent of the megacystis is not shown in the same imageage: the image shows the full extent of the hugely dilated thick-walled

w). The prenatal diagnosis of PUV was confirmed by postnatal imaging.

s of fetal malformations in oligohydramnios pregnancies. Egypt J


Fig. 2. Urinary tract obstruction at 31 weeks gestation 2. Oligohydramnios pregnancy referred with US findings of multiple variable sized abdominal andpelvic fluid-filled cysts and a suspected diagnosis of colon dilatation. Left: Coronal T2-SSFP of the fetal abdomen and pelvis identifies the fluid-filled cysts asmarkedly dilated left renal pelvicalyceal system (arrow) caused by pelviureteric junction obstruction, as well as a mildly dilated right pelvicalyceal systemand the visualized proximal part of the right ureter (arrowhead). Middle: Sagittal T2-weighted SSFP images shows dilated thick-walled urinary bladder anddilated posterior urethra (arrowhead) suggestive of a posterior urethral valve (PUV). The left hydronephrotic kidney is also seen (arrow). Right: SagittalT1-weighted MR image of the abdomen and pelvis documents normal size of meconium-filled distal colon and rectum (arrows). Fetal MRI changedUS-diagnosis of colonic dilatation to obstructive hydropathy. A viable fetus was born and the diagnosis of left PUJ obstruction and PUV was confirmed bypostnatal imaging.

Fig. 3. Meckel Gruber syndrome (MKS) at 24 weeks’ gestation. Oligohydramnios pregnancy referred with US diagnosis of bilateral autosomal recessivepolycystic kidneys (ARPCK). Left: 2D US image of the fetal abdomen identifies bilaterally enlarged, echogenic kidneys with multiple tiny cystic spaces.Middle: Sagittal T2-weighted image shows markedly enlarged kidneys with mottled high signal appearance resulted from innumerable small cysts(arrowhead) and confirms the US diagnosis of ARPKD. Fetal MRI identifies a small posterior cephalocele (PC) (arrow) and modifies the diagnosis to MekelGruber syndrome (MKS). The pregnancy was terminated 2 days after the prenatal MRI. Right: Postmortem coronal T2-weighted image of the abortusconfirmed the diagnosis. Arrows point to ARPKD; PC is not shown in this image.

A.H. Said et al. / The Egyptian Journal of Radiology and Nuclear Medicine xxx (2016) xxx–xxx 3

surface coil. No patients were excluded because of con-traindication to MRI or claustrophobia. Most patients werepositioned supine and head first into the gantry. Patientswho could not lie supine were put in the left lateraldecubitus. MR imaging was obtained along fetal bodyplanes using T2-weighted single shot fast spin echo (SSh)(TTR/TE 10,000/100 ms, 4-mm slice thickness, matrix196 � 256 or 256 � 256) and steady state free precessionsequence (TR/TE 3.5–4 ms/1.7–2 ms, FA 60–90, 1–2 signalsacquired, 256 � 256 matrix, and 4 mm slice thickness withno inter-slice gap). Additional T1-weighted MR imageswere obtained using a breath-hold spoiled gradient echosequence (100–140/4.2) (repetition time TR msec/echotime TE msec), 70–90� flip angle (FA), 256 � 160–256matrix, one signal acquired, slice thickness between 4


and 6 mm with an inter-slice gap of 0.2–0.4 mm. No con-trast agent, sedative, or fetal paralysis were used.

All fetal MRI examinations and MR images in this studywere approved at the time of acquisition by attending radi-ologist experienced in MRI and obstetrics imaging. Dataobtained at the time of MRI included the following: gesta-tional age, history of fetal anomalies in previous pregnan-cies if present, and the US diagnosis given upon referral.

MRI studies were reviewed by the radiologists in thisstudy for the presence of fetal malformations and diagnosiswas given by consensus. US images were analyzed in corre-lation with prenatal MRI and postnatal imaging findings.For statistical purpose, urinary abnormalities were groupedinto the following: Renal (including ureters) and vesico-urethral. Bilateral findings were counted separately. Brain



Fig. 4. Joubert syndrome and related cerebellar disorder (JSRD) at 28 weeks’ gestation. Oligohydramnios pregnancy referred with US finding of bilateralautosomal recessive polycystic kidneys (ARPKD). Left: Sagittal T2-SSFP of the fetal abdomen confirms the US referral diagnosis of renal enlargementconsistent of ARPKD (arrowhead). The posterior fossa (arrow) shows subtle findings in the form of prominent cisterna magna and mild deformity of thefourth ventricle. Middle: Axial T2-SSFP of the fetal posterior fossa identifies molar tooth sign (MTS) deformity pathognomonic for JSRD (arrow). Fetal MRImodifies the US diagnosis from isolated ARPKD to syndromal (JSRD). The pregnancy continued to term and resulted in a viable newborn. Right: Postnatalaxial T2-weighted MR image of the brain of the newborn identifies MTS and confirms the prenatal diagnosis of JSRD.

Fig. 5. Craniocervical stenosis at 33 weeks’ gestation. Oligohydramnios pregnancy referred with US diagnosis of micromelia and achondroplasia; SagittalT2-SSFP of the head and neck added US-occult craniocervical stenosis compressing medulla oblongata (arrow), mega cisterna magna, and defective inferiorvermis. US identified micromelic limbs more clearly than MRI did.


abnormalities were grouped into the following: posteriorfossa, ventricular, callosal and cerebral anomalies. Otheranomalies were counted per organ.

We prospectively studied the impact of the informationobtained by fetal MRI on prenatal diagnosis in consultationwith the referring physicians.


2.1. The reference standards

Follow-up was done for all of the studied cases. Inviable babies, the diagnosis was confirmed with clinicalexamination and postnatal imaging. In cases of termina-tion of pregnancy, we offered autopsy. If the parents did




not permit autopsy, we offered gross pathological exami-nation of the abortus and postmortem MRI. Retrospec-tively, we correlated fetal MRI findings with prenatal USfindings and final diagnoses.

For statistical analysis, data were described in terms ofrange, mean, frequency, percentages, sensitivity and speci-ficity when appropriate. McNemar test was used to com-pare proportion of abnormal findings by US and MRI asrelated to total abnormalities at final diagnosis.

All statistical calculations were done using the com-puter program SPSS (Statistical Package For The SocialScience: SPSS Inc., Chicago, IL, USA) version 16 for Micro-soft Windows.

3. Results

3.1. Prenatal imaging findings

We reported prenatal US and MRI findings in the stud-ied 43 oligohydramnios singleton pregnancies in correla-tion with the final diagnosis as per the outcome measures.

3.2. Fate and outcome measures

We followed the fate of All of the 43 studied cases:twenty-one viable fetuses were born, three cases hadspontaneous abortion shortly after MRI, and 19 cases hadtherapeutic abortion. Mortality rate in our study reached51.1%. In cases of terminated pregnancies, the outcomemeasures included autopsy (n = 18), and postmortem MRI(n = 4). The outcome measures for viable 21 babiesincluded clinical examination of the newborn as well asone or more of the following: postnatal abdomino-pelvicUS (n = 18), abdomino-pelvic MRI and magnetic resonanceurography (MRU) (n = 2), CT abdomen (n = 1), voidingcysto-urethrogram (VCUG) (n = 3), brain CT (n = 1), brainMRI (N = 16), and X-rays for the skeletal system (n = 1).

Chromosome analysis showed two cases with Trisomy13, and the remainder cases had normal karyotype.

3.3. Final diagnoses

Outcome measures identified one normal subject and42 malformed ones. Final diagnoses of the 43 cases – asper the involved body systems – included abnormalitiesof the urinary system in 36 fetuses (83.7%), brain malfor-mations in 23 (53.5%), skeletal system in 4 (9.3%), heartsin 3 (7%), and hepatobiliary in 3 (7%). The numbers ofabnormal findings per body systems at both US and fetal

Table 1Number of findings in different body systems as depicted by US and MRI – total n

Body system No. of affected fetuses No of findings No. of abnor

Urinary 36 75 69 (92.0%)Brain 23 41 33 (80.5%)Skeletal 4 5 1 (20%)Cardiac 3 6 6 (100%)Hepatic 3 3 2 (66.7%)

* P value 6 0.05 is significant (Bold), it is two tailed.


MRI, as well as at final diagnosis are summarized atTable 1.

3.3.1. Correlation of prenatal imaging findings of each fetalbody system with the final diagnosis3.3.1.1. Urinary system. Final diagnoses of the urinary mal-formations in the 36 cases included 75 abnormal findings,distributed as bilateral renal agenesis (n = 5), bilateralrenal hypoplasia (n = 1), bilateral autosomal recessivepolycystic kidney diseases (ARPKD) (n = 20), bilateralmulticystic-dysplastic kidneys (MCDK) (n = 1), and bilat-eral renal enlargement associated with intrauterine cyto-megalovirus (CMV) infection (n = 1), posterior urethralvalve with secondary bilateral collecting system dilatation(n = 4), unilateral (n = 1) or bilateral (n = 3) urinary collect-ing system dilatation due to other causes.

Both prenatal US and MRI correctly diagnosed urinarymalformations in 32 out of 36 fetuses. Both prenatal USand MRI correctly diagnosed: six fetuses with bilateralrenal agenesis/ hypoplasia by documenting the absence/diminished renal tissues respectively and non-filling ofthe urinary bladder; 20 fetuses with bilateral ARPKDappeared as enlarged kidneys with high signal intensityon T2-weighted MR images and high echogenicity on US;a fetus with bilateral renal enlargement related to CMVinfection; four fetuses with posterior urethral valve (PUV)causing secondary bilateral hydroureter-hydronephrosis,as well as dilated thick walled urinary bladder, and dilatedposterior urethra appearing as ’key-hole sign’; and a fetuswith unilateral dilated collecting system caused by ipsilat-eral uretero-vesical obstruction.

The remaining four fetuses were missed by US, whileMRI correctly added bilateral obstructive uropathy in twofetuses, and modified the diagnosis from unilateral tobilateral in another two fetuses.

The sensitivity and specificity for prenatal imaging indiagnosing urinary system malformations in the 43 oligo-hydramnios pregnancies were 92% and 100% for US and100% and 100% for MRI respectively.

3.3.1.2. Brain malformations. Outcome measures identifiedbrain malformations in 23 fetuses that included combina-tions of 41 findings: Dandy Walker Malformation complex(DWM) (n = 12), cerebellar hypoplasia (n = 1); posteriorcephaloceles (n = 11), ventriculomegaly (n = 9), hydro-cephalus with obstruction at aqueduct of Sylvius (n = 1),agenesis of corpus callosum (n = 2), alobar holoprosen-cephaly (n = 1), semilobar holoprosencephaly (n = 1), molartooth sign (n = 1), anencephaly (n = 1), and compressed

umber of fetuses = 43.

mal findings at US No. of findings at fetal MRI p value*

75 (100%) 0.01841 (100%) 0.0081 (20%) 1.003 (50%) 0.503 (100%) 1.00



Table 2Agreement/disagreements of US and fetal MRI findings – Per fetus.

Results of MRI in reference to US findings Number of fetuses

Agreeda 25Modifiedb 14Missedc 2Mixedd 2

a MRI confirmed prenatal US diagnosis without additional findings.b MRI added US-occult findings.c MRI missed data detected by US.d MRI added US-occult findings but missed other data detected by US.


medulla oblongata caused by cranio-cervical stenosis(n = 1).

Fetal MRI correctly identified all of the brain malforma-tions findings in the 23 fetuses. US correctly identifiedbrain malformations in 15 fetuses, and missed findings in8 fetuses that included combinations of posterior cephalo-celes (n = 5), DWM (n = 3), cerebellar hypoplasia (n = 1),Molar tooth sign (MTS) (n = 1), compressed medulla oblon-gata (n = 1), and partially separated cerebral hemispheresin a fetus with US diagnosis of alobar holoprosencephalythat refined the diagnosis to semilobar holoprosencephaly.Fetal MRI correctly ruled out US-suspected posteriorcephalocele in a normal fetus and agenesis of corpus callo-sum in another. The sensitivity and specificity for prenatalimaging in diagnosing brain malformations in the 43 oligo-hydramnios pregnancies were 78% and 99% for US, and100% and 100% for MRI respectively.

3.3.1.3. Skeletal. Post-delivery/postmortem examinationsidentified skeletal malformations in 4 fetuses that includedaxial polydactyly as a component of Meckel Gruber syn-drome (MKS) in 3 fetuses, as well as micromelia, and cra-nial cervical stenosis in a fetus with achondroplasia. Postaxial polydactyly was not detected neither by prenatalUS nor by fetal MRI. In an achondroplastic fetus, FetalMRI identified the US-occult craniocervical stenosis, whileprenatal US detected and evaluated the micromelic bonesbetter than fetal MRI did.

3.3.1.4. Cardiac. Both fetal US and MRI identified cardiacmalformations in three fetuses: hypoplastic right heart,hypoplastic left heart, and a ventricular septal defect. Thecardiac abnormalities were documented by autopsy. FetalMRI diagnosed hypoplastic right heart and hypoplastic leftheart abnormalities by showing imbalanced four-chambersteady state free precession (SSFP) MR images, and diag-nosed ventricular septal defect (VSD) by showing a largedefect in the interventricular septum in four-chamber SSFPimage. However, unlike echocardiography, MRI could notassess the cardiac functions related to thesemalformations.

3.3.1.5. Hepatobiliary. Final diagnoses included hepatobil-iary lesions in 3 fetuses with proved MKS: dilated bileducts in two fetuses and hepatic cysts in one. Fetal MRIidentified the hepatobiliary abnormalities in the threefetuses as tubular and rounded hyperintense lesions onT2-weighted images. Prenatal US identified dilated bileducts in 2 fetuses, and missed hepatic cysts in one.

3.3.2. Correlation of prenatal imaging findings of multiple fetalbody system with the final diagnosis

Twenty-two cases in this study had malformations thatinvolved more than one fetal body system. These includedurinary, brain, skeletal, and hepatobiliary (n = 3); urinaryand brain (n = 14); urinary and cardiac (n = 2); brain andcardiac (n = 1); brain and skeletal (n = 1); as well as uri-nary, ascites, and pericardial effusion (n = 1). The associa-tion of anomalies in multiple fetal body systemssuggested the diagnosis of syndromes: Meckel Grubersyndrome (MKS) in 15 fetuses and Joubert syndrome and


related cerebellar disorders (JSRD) in one. Fetal MRIcorrectly confirmed prenatal US diagnosis of 8 out of the15 cases with proved MKS without adding findings. Inthe remaining 7 cases, fetal MRI correctly detectedUS-occult findings (PC, DWM, and hepatic cysts) that sug-gested/supported MKS diagnosis.

Of the 43 oligohydramnios pregnancies, correlation ofMRI diagnosis of fetal malformations with prenatal USfindings – in reference to final diagnoses- resulted in 4groups (Table 2):

1. ‘Agreed’ in 25 fetuses (58.1%): Fetal MRI correctlyconfirmed prenatal US diagnosis without additionalfindings. These cases included the following: PUV(n = 4), bilateral renal agenesis (n = 4), bilateral ARPKD(N = 4), MKS (N = 8), alobar holoprosencephaly-Trisomy 13 (n = 1), posterior cephalocele (n = 1), anen-cephaly (n = 1), intrauterine CMV infection (n = 1), andhydrocephalus due to aqueduct stenosis (n = 1).

2. ‘Modified’ in 14 fetuses (32.5%): Fetal MRI correctlyadded US-occult findings and modified prenataldiagnosis

3. ‘Missed’ in 2 fetuses (4.7%): Fetal MRI missed correctfindings detected by prenatal US.

4. ‘Mixed’ in 2 fetuses (4.7%): Fetal MRI correctly addedUS-occult findings but missed other findings that werecorrectly detected by prenatal US.

4. Discussion

Oligohydramnios refers to amniotic fluid volume that isless than expected for gestational age [8]. The condition iscommonly secondary to an excess loss of fluid due to pre-term rupture of membranes or reduced urine productioncaused by fetal anomalies and/or aneuploidy [2,8]. Therewas no history of preterm rupture of membranes in ourstudy; however, fetal MRI correctly described fetal malfor-mations in 42 fetuses while diagnosed a normal fetus withUS-suspected posterior cephalocele.

In their larger series of 224 cases of oligohydramnios-associated malformation and examined by US, Stoll andcolleagues found that the majority of fetal malformationsinvolved the urinary tract; other malformations were mus-culoskeletal, digestive and cardiac [2]. In our series, themajority of fetal malformations involved the urinary tractsin 36 fetuses (83.7%), followed by the brains in 23 fetuses(53.5%); other fetal body systems were less commonlyencountered, namely the skeletal system in 4 fetuses(9.3%), hearts in 3 (7%), and hepatobiliary in 3 (7%).




Because in the latter half of the pregnancy the amnioticfluid is primarily fetal urine, the absence of functioningrenal tissues or a blockage in the fetus’ urinary tract canresult in oligohydramnios [2]. In a study of 80 cases withPotter sequence caused by renal abnormalities, cystic dys-plasia consisted almost half of the cases (47.5%), whileobstructive uropathy (25%), and bilateral renal agenesis(21.25%) came next [9]. We had similar results in our studyof 36 oligohydramnios pregnancies with urinary malfor-mations as 58.3% had cystic kidneys, 22.2% had dilated uri-nary system caused by obstruction, 16.7% had bilateralrenal agenesis/hypoplasia, and one fetus (3%) had enlargedkidneys associated with intrauterine CMV infection. Sev-eral previous reports have described the successful use ofMRI in evaluating a broad spectrum of fetal urinary malfor-mations but without specifying the presence of oligohy-dramnios [7,10,11]. Thus the place of fetal MRI fordetermination of UT malformations in the presence ofoligohydramnios still needs to be defined. In our series,fetal MRI correctly identified all of the 75 urinary systemmalformations in 36 fetuses (100%) in contrast to 69 mal-formations in 32 fetuses (92%) by prenatal US, a significantdifference in favor of MRI. In other words, oligohydramnioscan significantly limit US assessment of fetal anatomy andmalformations [5,12].

In our study, MRI documented US findings of theabsence of both kidneys and non-filling of the urinarybladder in five fetuses. When bilateral, renal agenesis isincompatible with life. Prenatal documentation of bilateralrenal agenesis supported parents’ decision to terminatepregnancy [3].

Fetal abdominal cystic masses may result from obstruc-tion of the urinary system. The sites of obstruction can beat the pelviureteric junction (PUJ), uretero-vesical (U-V)junction, and/or urethra [7,10–12]. Fetal MRI correctlydiagnosed all of the 8 fetuses with urinary obstruction inthis study and accurately determined the obstruction level.Owed to its large field of view, MRI helped in accuratedelineation of the full extent of a hugely dilated urinarybladder (megacystis) in a fetus in this series; the presenceof dilated posterior urethra (Keyhole sign) along withthickening of the urinary bladder wall helped in establish-ing the prenatal diagnosis of PUV in this fetus. Prune-bellysyndrome can also result in hugely dilated urinary bladderthat can be confused with megacystis secondary to PUV.However, unlike in PUV, megacystis in Prune-belly syn-drome has thin wall and associated with stricture of theentire length of urethra and thus does not show keyholesign [13].

Prenatal US correctly diagnosed 5 fetuses with urinarytract obstruction and misdiagnosed/missed findings inthe other 3 fetuses. In a fetus, where US suspected unilat-eral hydronephrosis, MRI detected a dilated ureter andrefined the diagnosis to hydroureter-hydronephrosis. Intwo fetuses, prenatal US misdiagnosed cystic abdominalmasses caused by urinary obstruction as bowel obstruc-tion. Markedly dilated urinary system may sometimes bemisdiagnosed as bowel obstruction [14]. T1-weighted MRimages identified normal hyperintense meconium-filledcolon in these two cases that helped in ruling out the erro-neous US diagnosis.


Cystic kidneys were the most common urinary malfor-mations in this study encountered in one fetus with bilat-eral multicystic dysplastic kidneys and in 20 fetuses withbilateral autosomal recessive polycystic kidneys (ARPKD).Multicystic dysplastic kidney is characterized by replace-ment of renal parenchyma by multiple variable-sized cysts[15]. In a fetus with US diagnosis of unilateral multicysticdysplastic kidney (MCDK) in this study, MRI detected renalcysts in the other kidney and refined the diagnosis to abilateral disease. MCDK is a distinct entity that is not usu-ally mistaken for other renal cystic diseases [16,17]. Unlikein hydronephrosis where there is communication with thecentral renal pelvis, cystic changes in MCDK are non-communicating [15]. It is also important to distinguishbetween ARPKD and MCDK, as the recurrence risk is 25%in the former in contrast to 3% in the latter [18]. UnlikeMCDK, the cysts in ARPKD are smaller in size and usuallycause marked bilateral renal enlargement [19]. MRI docu-mented US diagnosis of bilateral ARPKD in 20 fetuses inthis study. Fetal MRI identified markedly enlarged kidneyswith mottled high signal appearance on T2-weightedimages. The innumerable small cysts are responsible forthe high signal intensity appearance of ARPKD onT2-weighted fetal MRI [7,10,11]. Classically in ARPKD, bothkidneys are symmetrically enlarged and equally affectedby the cystic changes [20]. The occurrence of bilateral renalanomalies and oligohydramnios should initiate a search forother fetal anomalies and syndromal affection such asMeckel Gruber syndrome (MKS) [21]. MKS is a lethal auto-somal recessive disorder characterized by a combination ofrenal cysts and variably associated anomalies of the brain,liver cysts, and polydactyly [22–31].

Previous reports have documented the association ofoligohydramnios pregnancies with fetal brain malforma-tions such as hydrocephalus, periventricular calcification,agenesis of corpus callosum, holoprosencephaly, andmicrocephaly [2,26,28]. Twenty-three fetuses (53.5%) inour study had brain malformations in association witholigohydramnios and included Dandy Walker Malforma-tion complex (DWM), posterior cephaloceles (PC), ventricu-lomegaly, hydrocephalus, agenesis of corpus callosum,holoprosencephaly, anencephaly, and molar tooth sign(MTS). MRI proved to be a valuable adjunct to US in diag-nosing fetal brain abnormalities [12,32]. Fetal MRI identi-fied correctly all of the brain malformations in 23 fetusesin this study and was significantly superior to prenatal USwhich correctly identified abnormalities in only 12 fetuses.Fetal MRI correctly identified US-occult findings in 11fetuses that were mainly related to the posterior fossa,and ruled out US-suspected posterior cephalocele in a nor-mal fetus and agenesis of corpus callosum in another.

Malformations of fetal organs other than urinary andbrain were much less encountered in association witholigohydramnios in this study and included hepatobiliaryabnormalities in three fetuses (7%), skeletal malformationsin four fetuses (9.3%), and cardiac malformations in threefetuses (7%).

Outcome measures revealed hepatobiliary malforma-tions in three fetuses with MKS: two fetuses had dilatedbile ducts, and one had multiple hepatic cysts. Hepato-biliary malformations have been reported with MKS and




included hepatomegaly with small cysts, absent gall blad-der, or dilated bile ducts [22]. Fetal MRI correctly diag-nosed hepatobiliary malformations in the 3 fetuses, whileprenatal US diagnosed dilated bile ducts in 2 fetuses andcould not detect the hepatic cysts in the third one.

Outcome measures revealed skeletal malformations infour fetuses in this study: polydactyly in three fetuses withMKS, and a fetus with achondroplasia. Prenatal US pro-vided detailed assessment of the skeletal system in a fetuswith achondroplasia. US is the method of choice for mea-suring fetal long bones and recognition of prenatal-onsetskeletal dysplasias using 2D and 3D imaging [33]. Unlikeprenatal US, fetal MRI could not provide detailed assess-ment or bony measurements of the micromelic bones,but added US-occult cranio-cervical stenosis. Recent reportindicated that echo planar MR imaging (EPI) can be used toimage fetal bones especially when it is difficult to assess allextremities sonographically in late gestation or if theamniotic fluid is severely reduced [34]. We did not useEPI sequence in this study, but this sequence will openthe door for future studies. Polydactyly was reported with55% of MKS being typically postaxial and bilateral [21].Polydactyly was missed by both prenatal US and MRI andwere proved only by autopsy. Prenatal US can miss subtleskeletal malformations such as polydactyly in the presenceof oligohydramnios likely because of the crowding effect ofoligohydramnios on fetal parts [31].

Recent preliminary reports indicated that fetal cardiacMRI is feasible in evaluation of the morphology of normaland abnormal fetal hearts using the anatomical segmentalapproach for congenital heart diseases [35,36]. Steady StateFree Precession (SSFP) MR images allowed documentationof echocardiographic findings of the structural malforma-tions in 3 fetuses in this study with hypoplastic right heart,hypoplastic left heart and a ventricular septal defect. How-ever, unlike echocardiography, the technique of fetal car-diac MRI in its current status could not assess cardiacfunction related to these malformations, as ECG-gated fetalMRI sequences are not yet available for clinical practice [36].

Twenty-two cases in this study had malformations thatinvolved more than one fetal body system. The associationof anomalies in multiple fetal body systems suggested pre-natal diagnosis of MKS in 15 fetuses, Joubert syndrome andrelated cerebellar disorders (JSRD) in one fetus, andintrauterine cytomegalovirus CMV infection in one fetus.

The association of ARPKDwith brain abnormalities, hep-atobiliary, and/or polydactyly suggests MKS diagnosis [22].Fetal MRI correctly suggested MKS diagnosis in 15 fetusesin this study. The incidence of MKS is estimated to be1/13,250 in USA live births, while it is much higher in NorthAfrica at 1/3500 [23]. The typical renal cystic pattern ofARPKD is characteristic ofMKS and the diagnosis of this dis-order cannot be made in the absence of these changes [24].AlthoughMKS has been described classically with posteriorcephalocele, many authors have expressed disagreementwith the idea of an obligatory cerebral abnormality due tothe wide phenotypic variation of the disorder [24–27]. Awide spectrum of brain pathology has been reported withMKS [28]. Posterior cephalocele (PC) was the most consis-tent malformation reported with MKS (60–90%) [29].DWM was also accepted as part of MKS syndrome [30].


Other reported brain abnormalities with MKS includedcerebral ventriculomegaly, agenesis of corpus callosum,absent olfactory bulb, fused thalami, holoprosencephaly,hypoplasia of optic nerves-chiasm, absent pituitary gland,and microcephaly [28]. Out of 15 fetuses with MKS diagno-sis in our study, fetal MRI correctly identified PC in 10fetuses (66.6%), DWM in 11 (73.3%), cerebral ventricu-lomegaly in 9 (60%), agenesis of corpus callosum in 2(13.3%), and hepatobiliary dilatation/cysts in 3 (20%). MRIcorrectly confirmed prenatal US diagnosis of MKS in 8 outof the 15 fetuses without adding findings. In the remaining7 fetuses, fetal MRI correctly detected US-occult findings(PC, DWM, and hepatic cysts) that suggested/supportedMKS diagnosis.

In this study, fetal MRI identified US-occult malforma-tion of the posterior fossa consistent with molar tooth sign(MTS) in association with bilateral ARPKD. MTS is a pathog-nomonic sign for Joubert Syndrome and Related cerebellardisorders, and it consists of thick horizontally placed supe-rior cerebellar peduncles, associated with deepening of theinterpeduncular fossa and hypoplastic vermis. The possibil-ity to identify MTS by fetal MRI has been previouslyreported [37]. The association of MTS with cystic dysplastickidneys has been described with Joubert Syndrome withrenal involvement. Prenatal MRI diagnosis of MTS in associ-ation with bilateral ARPKD has been reported once in theliterature [38].

In association with intrauterine cytomegalovirus (CMV)infection, both prenatal US and MRI identified bilateralrenal enlargement associated with ascites and pericardialeffusion in a fetus at 23 weeks of gestation. CMV infectionis the most common cause of congenital infection with anannual frequency of 0.5–2.5% of live births. Oligohydram-nios and fetal ascites have been described in associationwith intrauterine CMV infection [39]. Choong and col-leagues described prenatal US findings of bilateral renalenlargement in association with intrauterine CMV infec-tion in a fetus at 28 weeks’ gestation [40].

We correlated the overall prenatal US and MRI diag-noses of fetal malformations in the 43 oligohydramniospregnancies with the final diagnosis.

Fetal MRI confirmed US diagnosis of fetal malforma-tions in 25 fetuses (58.1%) that included mainly the urinarysystem and brain.

Fetal MRI added US-occult findings that correctly chan-ged or modified prenatal US diagnosis in 14 fetuses(32.5%). Fetal MRI correctly diagnosed one normal fetuswith US-suspected posterior cephalocele and detected USoccult findings that were mostly related to the brainand/or urinary system in 13 fetuses. In two fetuses withobstructive uropathy, fetal MRI identified the dilated uri-nary systems and ruled out incorrect US diagnosis of colonabnormality. MRI changed US diagnosis fromhydronephrosis to hydroureteronephrosis in one fetusand from unilateral multicystic kidney to bilateral multi-cystic kidneys in another. Fetal MRI added cerebellarhypoplasia to a correct US diagnosis of bilateral renalagenesis in one fetus. Fetal MRI added findings of brainmalformation to US diagnosis of bilateral ARPKD that sug-gested/confirmed the diagnosis of MKS in 7 fetuses andJSRD in one fetus.




MRI missed fetal abnormalities that were detected byUS and involved cardiac function of heart anomalies in 2fetuses (4.7%). MRI missed data correctly detected by USwhile added US-occult findings in 2 fetuses (4.7%). In onefetus, fetal MRI identified partially separated cerebralhemispheres and modified US diagnosis of lobar holopros-encephaly to semilobar but could not assess cardiac func-tions related to an associated VSD. Unlike US, MRI couldnot fully assess the micromelic bones in a fetus withachondroplasia, but identified craniocervical stenosis andposterior fossa abnormalities that were US-occult.

Identification of fetal abnormalities and associatedconditions is important for fetal prognosis and geneticcounseling [1]. Knowledge of the fetal chromosome consti-tution in the setting of abnormal prenatal imaging findingshas important benefit on diagnosis and counseling inoligohydramnios pregnancies [2]. Among 224 oligohy-dramnios pregnancies associated with fetal malformationsstudied by Stoll and colleagues, 13.8% had a chromosomalabnormalities. Two out of the 42 oligohydramnios preg-nancies associated with fetal malformations in our studyhad chromosomal abnormalities. The use of fetal chromo-some analysis and careful imaging examination is advisedin every pregnancy complicated by oligohydramnios [2,5].

The degree of confidence required for prenatal diagnosisis clearly higher in cases where termination of pregnancy isconsidered. The results of fetal MR imaging in this study,whether excluding or confirming sonographically detectedabnormalities, or discovering additional abnormalities thatwere not apparent by US, have been shown to help reach amore confident prenatal diagnosis and support counselingof the referring physicians and parents. However, manage-ment decision is multi-factorial, including the gestationalage at diagnosis, the severity and type of the abnormality,the presence of multiple anomalies, as well as social andreligious views [8]. In addition, the decision in pregnancymanagement depends also on other oligohydramnios-related deformations such as pulmonary deformity/hypo-plasia which were out of the scope of this study.

A partial limitation of this study is the relatively smallsample size. However, this study opens the door for furtherprospective works to evaluate the diagnostic ability andaccuracy of MRI findings in fetal malformations associatedwith oligohydramnios pregnancies, a well-known USlimitation.

5. Conclusion

Fetal MRI is a valuable adjunct to US in evaluating sus-pected fetal malformations associated with oligohydram-nios specifically those related to the brain and urinarysystem. Fetal MRI may add findings that can modify prena-tal US diagnosis and support pregnancy counseling. On theother hand, US seems to excel MRI in detection of fetuseswith skeletal anomalies or cardiac functions related toheart anomalies.

Conflict of interest

Author states that there is no conflict of interest.


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