Prenatal unilateral cerebellar hypoplasia in a series of 26 cases

Transcription

Ultrasound Obstet Gynecol 2014; 44: 447–454
Published online in Wiley Online Library (wileyonlinelibrary.com). DOI: 10.1002/uog.13217
Prenatal unilateral cerebellar hypoplasia in a series of 26
cases: significance and implications for prenatal diagnosis
M. MASSOUD*, M. CAGNEAUX*†, C. GAREL‡§, N. VARENE§, M.-L. MOUTARD‡,
T. BILLETTE‡, A. BENEZIT¶, C. ROUGEOT¶, J.-M. JOUANNIC**, J. MASSARDIER*,
P. GAUCHERAND*, V. DESPORTES‡¶ and L. GUIBAUD*†‡
*Centre Pluridisciplinaire de Diagnostic Prénatal, Hôpital Femme Mère Enfant, Université Claude Bernard Lyon I, Lyon, France;
†Département d’Imagerie Pédiatrique et Fœtale, Hôpital Femme Mère Enfant, Université Claude Bernard Lyon I, Lyon, France; ‡Centre de
Référence des Malformations du Cervelet, Hôpital Femme Mère Enfant, Lyon et Hôpital Armand Trousseau, Paris, France; §Service de
Radiologie, Hôpital d’Enfants Armand-Trousseau, Paris, France; ¶Département de Neuropédiatrie, Hôpital Femme Mère Enfant, Université
Claude Bernard Lyon I, Lyon, France; **Service d’Obstétrique, Hôpital Armand Trousseau, Paris, France
K E Y W O R D S: cerebellum; clastic lesion; PHACE syndrome; posterior fossa; ultrasound
ABSTRACT
Objective To define imaging patterns of unilateral cerebellar hypoplasia (UCH), discuss possible pathophysiological mechanisms and underline the etiology and
prognosis associated with these lesions.
Methods In this retrospective study we reviewed the
charts of 26 fetuses diagnosed between 2003 and
2011 with UCH, defined by asymmetrical cerebellar
hemispheres with or without decreased transverse
cerebellar diameter. The review included analysis of
the anatomy of the cerebellar hemispheres, including
foliation, borders and parenchymal echogenicity, and of
the severity of the hypoplasia. Data from clinical and
biological work-up and follow-up were obtained.
Results Our series could be divided into two groups
according to whether imaging features changed progressively or remained constant during follow-up. In Group
1 (n = 8), the progression of imaging features, echogenic
cerebellar changes and/or hyposignal in T2*-weighted MR
images were highly suggestive of ischemic/hemorrhagic
insult. In Group 2 (n = 18), imaging features remained
constant during follow-up; UCH was associated with
abnormal foliation in three proven cases of clastic lesions,
a cystic lesion was noted in three cases of PHACE (posterior fossa anomalies, hemangioma, arterial anomalies,
cardiac abnormalities/aortic coarctation, eye abnormalities) syndrome and, in the remaining cases, UCH remained
unchanged, with no imaging pattern typical of hemorrhage. In 24 cases the infant was liveborn and follow-up
was continued in 23, for a mean period of 3 years. Among
these, neurological complications were identified in seven
(in one of seven (at a mean of 46 months) in Group
1 and in six of 16 (at a mean of 35 months) in Group
2). The surface loss of cerebellar hemisphere was > 50%
in 19/24 fetuses and the vermis was clearly normal in
appearance in 19/24. Predisposing factors for fetal vascular insult were identified in eight cases: these included
maternal alcohol addiction, diabetes mellitus, congenital
cytomegalovirus infection and pathological placenta with
thrombotic vasculopathy and infarctions.
Conclusion UCH is defined as a focal lesion of the
cerebellum that may be secondary to hemorrhage and/or
ischemic insult, suggesting a clastic origin, particularly
when imaging follow-up reveals changes over time. UCH
may also be a clue for the prenatal diagnosis of PHACE
syndrome. The amount of surface loss of cerebellar
hemisphere does not correlate with poor prognosis. UCH
with normal vermis is often associated with normal
outcome. Copyright © 2013 ISUOG. Published by John
Wiley & Sons Ltd.
INTRODUCTION
Unilateral cerebellar hypoplasia (UCH) is defined as a loss
of volume of one cerebellar hemisphere. The sonographic
diagnosis is based on asymmetry of the cerebellar
hemispheres and/or a decrease in the transverse cerebellar
diameter (TCD)1 . UCH is a rare pathological condition
and its underlying etiopathogenesis is unclear2 . According
to Barkovich in 19983 , UCH is suggestive of a primary
disorder of cerebellar formation; however, advances in
prenatal imaging, as reported in a few prenatal case
reports4 – 9 and postnatal short series10,11 , have led us to
Correspondence: Dr L. Guibaud, Université Claude Bernard Lyon 1, Imagerie Pédiatrique et Fœtale, Hôpital Femme Mère Enfant,
59, Boulevard Pinel, 69677 Lyon, Bron, France (e-mail: [email protected])
Accepted: 16 September 2013
Copyright © 2013 ISUOG. Published by John Wiley & Sons Ltd.
ORIGINAL PAPER
448
conclude that occurrence of UCH prenatally is probably
caused by vascular insult secondary to multiple etiologies
and leading to a disruption in cerebellar development11,12 .
The resulting clastic lesions of the cerebellar hemispheres
can mimic cerebellar malformations3,8,12,13 ; however, the
pathogenesis and consequent prognosis may differ. Based
on our prenatal series of UCH, to our knowledge the
largest to date, our objective was to define the imaging
patterns of these cerebellar lesions, discuss their possible
pathophysiological mechanisms (clastic vs malformative
origin) and determine their etiology and associated
prognosis.
SUBJECTS AND METHODS
In the database of our national referral center for
cerebellar malformations (Hospital Femme-MèreEnfants,
Lyon and Hopital Armand Trousseau, Paris), we identified
and reviewed retrospectively the charts of 26 fetuses
diagnosed between 2003 and 2011 with UCH, defined
by asymmetrical cerebellar hemispheres with/without
decreased TCD. According to the anatomical approach
proposed by Guibaud and des Portes1 , the posterior fossa
had been assessed in an axial plane by measuring the TCD
and the depth of the cisterna magna, and by analyzing
cerebellar anatomy, which normally includes a distinct
vermis surrounded by two well-defined symmetrical
hemispheres, with no communication between the
fourth ventricle anteriorly and the cisterna magna
posteriorly. The ultrasound and magnetic resonance
imaging (MRI) data of these 26 patients were reviewed
by two experienced pediatric neuroradiologists (L.G.
and C.G.). This included analysis of the anatomy of
the cerebellar hemispheres, including foliation, borders
and parenchymal echogenicity. The severity of the
cerebellar hypoplasia was assessed on the MRI axial
views by comparing the surface of the reduced cerebellar
hemisphere relative to that of the normal contralateral
hemisphere; this surface estimation was calculated by
measuring the orthogonal diameters of each hemisphere.
Data from clinical and biological work-up and follow-up
were provided by the corresponding physicians.
RESULTS
Our series included 26 fetuses with UCH, referred at a
mean gestational age of 26 (range, 21–35) gestational
weeks; the diagnosis was made between 21 and 26
weeks in 18 (72%) patients, between 28 and 32 weeks
in six (20%) patients and after 32 weeks in two (8%)
patients. The second-trimester ultrasound examination
was reported as normal in all cases diagnosed at or after
26 weeks, with the exception of two: Case 16, which had
no follow-up during pregnancy, and Case 22, in which
there was a conotruncal anomaly. UCH was observed in
the left cerebellar hemisphere in 17 patients and in the
right hemisphere in nine.
Our series could be divided into two groups according to imaging follow-up: Group 1 (n = 8, Cases 1–8)
Massoud et al.
showed a progressive change of imaging features during
follow-up and in Group 2 (n = 18, Cases 9–26) lesions
appeared unchanged over time. In Group 1 (Table S1),
the progression during follow-up of imaging features,
as well as echogenic cerebellar changes and/or hyposignal in T2*-weighted images, were highly suggestive of
ischemic/hemorrhagic insult. In Group 2 (Table S2), with
cerebellar lesions remaining constant on prenatal imaging
follow-up, there were three cases of proven clastic lesions,
four cases of PHACE (posterior fossa anomalies, hemangioma, arterial anomalies, cardiac abnormalities/aortic
coarctation, eye abnormalities) syndrome, one case of
congenital cytomegalovirus (CMV) infection and 10 cases
of possible clastic lesions of undetermined origin.
UCH was associated with both central nervous system
(CNS) and non-CNS lesions. Associated CNS lesions
included abnormal foliation, which was noted in eight
cases (Cases 1, 9, 10, 11, 17, 18, 21 and 23) on
prenatal imaging and confirmed in two cases on
postnatal MRI (Cases 17 and 23) and one case on
pathological examination of the cerebellar hemisphere
(Case 9). Abnormal foliation was also noted on
postnatal MRI in two additional cases (Cases 16 and
24). Contralateral asymmetrical brainstem suggestive
of Wallerian degeneration was noted in two cases
prenatally (Cases 24 and 25) and four additional cases
on postnatal MRI (Cases 2, 5, 14 and 25). Anomalies of
the supratentorial level were found in two cases: severe
ventriculomegaly in a case of congenital CMV infection
(Case 16) and a cystic lesion close to the splenium in a
case of PHACE syndrome (Case 12). A cystic lesion of
the posterior fossa was associated with UCH in four cases
(Cases 12–15), including three cases of PHACE syndrome
and one case of clastic insult with a porencephalic cyst
(Case 7). Typically, the diagnosis of PHACE syndrome is
made in the postnatal period on the basis of facial infantile
hemangioma associated with arterial anomalies.
Associated non-CNS findings were found in three cases:
there was echogenicity of the left colon in one case (Case
23), conotruncal heart malformation in one case (Case 22)
and severely restricted growth in a fetus of a twin pregnancy complicated by twin-to-twin transfusion syndrome
(TTTS) which benefited from selective laser photocoagulation of chorionic vessels at 23 gestational weeks (Case 11).
Fetal karyotyping was performed in 11 cases, with normal results (Cases 1, 3, 4, 5, 7, 9, 10, 12, 19, 22 and 25).
There were predisposing maternal factors for fetal vascular insult in eight cases; these included alcohol addiction
in one case (Case 2), diabetes mellitus in two cases (Cases
2 and 19), congenital CMV infection in one case (Case
16), abnormal coagulopathy in three cases involving a
heterozygous mutation in the methylene tetrahydrofolate
reductase gene (MTHFR) in both parents in one case (Case
9), antiphospholipid syndrome in one case (Case 7) and
positive platelet cross-matching in one case (Case 6), and
a mother with hypertension treated by calcium inhibitor
in one case (Case 24). A pathological placenta with
thrombotic vasculopathy and infarctions was identified on
pathological examination in two cases (Cases 7 and 10).
Ultrasound Obstet Gynecol 2014; 44: 447–454.
Prenatal unilateral cerebellar hypoplasia
449
Figure 1 Case 2. (a) Ultrasound image in a patient with medical history of alcohol addiction referred at 23 gestational weeks for abnormal
echogenicity of the left cerebellar hemisphere, which was confirmed in our department. (b) Ultrasound follow-up at 25 weeks showed partial
absence of the left cerebellar hemisphere, as well as echogenic thickening of the meninges facing the abnormal hemisphere (arrow). Dotted
line indicates transcerebellar diameter. (c,d) Axial fetal magnetic resonance images confirmed both focal decrease of volume of the left
cerebellar hemisphere and thickening of adjacent meninges, which demonstrated hypo- and hyperintensity (arrows) on T2-weighted (c) and
T1-weighted (d) sequences, respectively, suggestive of ischemohemorrhagic insult.
Regarding prenatal counseling, postnatal prognosis was
characterized, as suggested in the literature11,12 , on the
basis of extension of the clastic process to the vermis and
the severity of surface loss of the affected hemisphere. The
surface loss of cerebellar hemisphere was below 25% in
one case, between 25 and 50% in five cases and above
50% in 19 cases; in one case this information was not
available. The vermis appeared normal in 19 cases and
abnormal in four cases, and was difficult to evaluate in
three cases. Among the 19 fetuses with normal vermis
on prenatal imaging, normal vermis was also reported on
postnatal MRI for 18 infants and focal hypoplasia of the
vermis was noted in one case with normal development
(Case 2). Among the four fetuses with abnormal vermis,
termination of pregnancy was performed in one case
(Case 9) and a stillbirth occurred in another (Case
10); the vermian lesion was confirmed on pathological
examination in these two cases. In the remaining two
cases, postnatal MRI was not performed; in one case
(Case 6), the infant demonstrated normal development at
20 months, while in the other case (Case 1), follow-up was
not possible. Among the three fetuses in which the analysis
of the vermis was limited during the prenatal period,
postnatal imaging showed normal vermis in two cases
(Cases 24 and 25) and confirmed the suspicion of a caudal
lesion of the vermis in the other (Case 7). Twenty-four
cases were live-born; the parents elected for termination of
pregnancy in one case in which UCH was associated with
a vermian lesion (Case 9) and a stillbirth was diagnosed
at 32 gestational weeks in another case (Case 10).
The mean gestational age at delivery was 38 (range,
34–41) weeks. One fetus (Case 11), the ex-donor
of a monochorionic twin pregnancy treated by laser,
had presented with restricted growth and had a birth
weight of 930 g at 35 weeks; all other newborns were
appropriate-for-gestational age.
Based on the collected data, UCH was likely to
have been associated with primitive hemorrhagic or
ischemic/hemorrhagic insults in 11 cases (Cases 1–11),
PHACE syndrome in four cases (Cases 12–15) and a congenital CMV infection in one case (Case 16). Regarding
clinical follow-up, among the 24 living infants, 16 had
normal neurological outcome and seven had abnormal
outcome (including mild speech delay (n = 2; Cases 5,
20), serious delay in developmental milestones (n = 3;
Cases 11, 12, 16), oculomotor disorders (n = 1; Case 25)
450
Massoud et al.
Figure 2 Case 8. Patient referred at 31 gestational weeks for anatomical disorganization of the left cerebellar hemisphere. (a,b) Axial
ultrasound images focusing on the left cerebellar hemisphere showed both focal decrease of volume and abnormal parenchymal echogenicity
(arrow) of the upper part of the hemisphere (a), as well as a cystic lesion (arrow) on its inferior part (b), suggestive of a porencephalic lesion.
(c) T2-weighted axial magnetic resonance (MR) image demonstrated large parenchymal dysgenesis of the inferior part of the cerebellar
hemisphere, which was replaced by a cystic lesion (arrow). (d) T2*-weighted axial MR image, at the same level as that in (c), showed
hypointensity of the residual parenchyma, which confirmed hemosiderin deposits (arrow) related to an ischemohemorrhagic insult. Neonatal
axial (e), coronal (f) and sagittal (g) T2-weighted MR images confirmed reduction of volume of the left cerebellar hemisphere associated with
porencephalic cyst (e), replacing the inferior part of the hemisphere, with hypointensity at the junction between the cyst and the residual
cerebellar parenchyma (arrow) on coronal image (f), suggestive of hemosiderin deposits. Note that the vermis was confirmed to be
anatomically intact (g).
and dyspraxia (n = 1; Case 17)); regular follow-up visits
were not possible for one infant. The mean follow-up
period was 3 years, ranging from 2 months to 9 years.
DISCUSSION
Among lesions of the posterior fossa, UCH is rare and the
pathophysiological mechanisms are unclear2 . Cerebellar
injuries have been described mainly as a complication
of low birth weight and extreme prematurity9 – 11 ;
however, similar lesions have been reported throughout
pregnancy12 – 14 . To our knowledge, to date this is the
largest prenatal series of focal reduction of one cerebellar
hemisphere, referred to as UCH according to the anatomical approach proposed by Guibaud and des Portes1 .
Cerebellar clastic lesions have been described as early
as 17 gestational weeks4 . In our series, as a result of the
timing of ultrasound imaging, the mean gestational age
at diagnosis was 26 weeks. Between 24 and 32 weeks,
the cerebellum exhibits asymptotic growth related to high
proliferation of neuroblasts and differentiation of the
adult cerebellar cortex14 – 16 , which leads to significant
susceptibility to vascular insults and abnormalities.
Our series could be divided into two groups according
to imaging follow-up. In the eight patients of Group 1
(Table S1), the progression of imaging features, as well
as of echogenic cerebellar changes and/or hyposignal in
T2*-weighted images (Figure 1, Case 2), were highly
suggestive of hemorrhagic insult. Cerebellar hemorrhage
is generally visualized as an echogenic cerebellar hemisphere, or a mixed echogenic lesion within the cerebellum,
with subsequent liquefaction leading to a porencephalic
lesion5,6 , as typically shown in Case 8 (Figure 2). In Case
7, UCH was associated with a cystic lesion, reported
at 25 gestational weeks as an arachnoid cyst with a
mass effect on the vermis, suggestive of malformative
origin. However, repeat imaging at 33 weeks revealed a
porencephalic cyst associated with destruction of the left
CH and presence of a clastic lesion, which was confirmed
by postnatal MRI. Yuksel and Batukan8 described a similar case, which was misdiagnosed as a Dandy–Walker
malformation. Although ultrasound examination can
depict changes in parenchymal echogenicity, suggestive
of clastic lesions, over time, MRI can confirm more
accurately the presence of hemorrhage, especially when
using T2*-gradient echo sequences (Cases 2, 6 and 8).
However, it is not possible to assess whether these lesions
are inherently hemorrhagic or related to hemorrhagic
changes due to an underlying ischemic insult17 .
In the 18 patients of Group 2 (Table S2), the lesion
remained unchanged on prenatal imaging follow-up.
In two cases, clastic origin was confirmed, associated
with abnormal vermis (Cases 9 and 10) which led to
termination of pregnancy in one (Case 9) (Figure 3)
and stillbirth in the other (Case 10). Pathological
examination showed important ischemic/hemorrhagic
lesions in both cases. In a third case (Case 11), UCH was
encountered in a severely growth-restricted ex-donor of a
monochorionic twin pregnancy, which had been treated
451
by laser coagulation at 23 weeks for TTTS. Postnatal
MRI demonstrated hemosiderin deposition suggestive of
clastic infarction, secondary to TTTS.
Interestingly, in Group 2, there were four cases of
PHACE syndrome (Figure 4), a vascular neurocutaneous
disorder of undetermined origin18 . A spectrum of
congenital malformations of the posterior fossa has been
described for PHACE syndrome, ranging from Dandy–
Walker malformation to focal dysplasia–hypoplasia of
the cerebellum. In such cases, it is hypothesized that
UCH is related to underdevelopment of the cerebellar
hemisphere, as a consequence of arterial anomalies,
resulting in reduction of cerebellar arterial supply. UCH
was associated with a cystic lesion in three of our four
cases (Cases 13–15). Only three prenatal cases suggestive
of PHACE syndrome have been described previously19,20 ;
in one of these, UCH was reported.
Congenital CMV infection was associated with UCH
in one case (Case 16). Initial ultrasound examination
performed at 34 weeks, immediately before premature
delivery, demonstrated right UCH associated with severe
ventriculomegaly. Postnatal MRI confirmed prenatal
findings and showed a pattern typical of CMV fetopathy,
which was confirmed by serological testing. Vermian
hypoplasia has been reported in congenital CMV
infection20,21 . The immune inflammatory response and the
direct cytopathic effect of CMV on precursor cells of the
neuroepithelium are responsible for brain damage22,23 .
However, in our case, UCH was most likely due to
inflammatory vasculopathy rather than direct cytotoxicity
of CMV, since the lesion was unilateral.
In our 10 remaining patients (Cases 17–26), the
imaging pattern of UCH remained constant during
follow-up, without any features to suggest the presence
of hemorrhage. Imaging findings were confirmed in the
postnatal period in only seven cases, since MRI was not
performed in one infant (Case 20). Postnatal outcome
was normal in all cases, with the exception of Case 17
(Figure 5); thus genetic or syndromic entities, in which
UCH has occasionally been reported24 – 27 , were excluded.
Defective foliation was associated with UCH in eight
cases. The possible vascular injury in these cases may
have caused abnormal migration and misorientation of
Purkinje cells, and subsequent disorganization of external
granular cells, leading to abnormal foliation, as described
in mutant rats28 .
Contralateral asymmetrical brainstem, suggestive of
Wallerian degeneration, was seen in two of our series
prenatally (Cases 24 and 25) and four cases postnatally
(Cases 2, 5, 14 and 25); this has also been noted in
association with clastic lesions of the cerebellum29 .
Since risk factors for clastic lesions have been described
previously17 and were also identified in eight cases
of our series, we recommend, in accordance with
Malinger et al.6 , that in cases of UCH it is important
to investigate the possibility of any maternal drug
use, alcohol consumption or recent trauma, as well as
thrombocytopenia and coagulation disorders (including
factor VII and X deficiencies17 , platelet cross-matching
452
Massoud et al.
Figure 3 Case 9. Patient referred at 28.5 gestational weeks for focal decreased cerebellar biometry. Axial ultrasound (a) and T2-weighted
magnetic resonance (MR) (b) images showed focal volume loss (arrows) of the left cerebellar hemisphere, without any anomaly of
echogenicity or intensity, respectively. (c) Sagittal ultrasound imaging showed both a reduction of volume and a lack of foliation (arrow) of
the left cerebellar hemisphere, compared with normal volume and foliation (d, arrow) of the contralateral right cerebellar hemisphere.
(e) Mid-sagittal ultrasound image demonstrated decreased height of the vermis (arrow) (height, 11–12 mm) with an abnormally distal fourth
ventricle, compared with the normal appearance of the fourth ventricle and vermis (height, 16 mm) at the same gestational age in a control
fetus (f). These imaging findings, demonstrated also in mid-sagittal T2-weighted MR image (g), were suggestive of clastic lesion extending to
the cranial part of the vermis, which was confirmed in the pathological specimen (h). Double-headed arrow in (h) indicates height of vermis.
453
Figure 4 Case 13. Patient referred at 27 gestational weeks for anatomical disorganization of the posterior fossa. (a) Axial ultrasound image
showed focal decrease of volume of the left cerebellar hemisphere and a cystic lesion facing the left cerebellar hemisphere (arrow),
demonstrating mass effect on the adjacent vault of the skull. (b) T2-weighted axial magnetic resonance image showed discrete focal low
signal (arrow) of the left cerebellar hemisphere, suggestive of a clastic lesion. (c) Postnatal clinical follow-up demonstrated development of
segmental hemangioma on the left part of the face, which led to a diagnosis of PHACE syndrome.
Figure 5 Case 17. Patient referred at 35 gestational weeks for focal decreased cerebellar biometry (transcerebellar diameter, 41 mm;
50th percentile, 46 mm). Axial ultrasound image confirmed abnormal cerebellar biometry and showed focal volume loss and increased
echogenicity (arrow) of the left cerebellar hemisphere. Axial (b), mid-sagittal (c) and coronal (d) T2-weighted fetal magnetic resonance
images confirmed decreased volume (arrows) of the left hemisphere and showed focal low signal, suggestive of a clastic lesion. The vermis
was otherwise normal.
and CMV infection), and to perform pathological analysis
of the placenta17 .
Regarding prenatal counseling, postnatal prognosis
may be characterized, as suggested in the literature10,11 , on
the basis of extension of the clastic process to the vermis
and the severity of surface loss of the affected hemisphere.
The majority of our cases were liveborn (n = 24) and
showed normal development in infancy (n = 16), even
though cerebellar surface loss prenatally was > 50% in
the majority of cases (n = 19). The vermis was normal in
14 of these 16 normally developed cases, based on postnatal MRI. The three infants with severe developmental
Massoud et al.
454
delay (Cases 11, 12 and 16) had presented prenatally
with severely restricted growth, PHACE syndrome and
congenital CMV infection, respectively, with normal vermis on postnatal MRI. Of the remaining four patients with
abnormal outcome (speech delay, Cases 5 and 20; ocular
disorders (Case 25); dyspraxia (Case 17)), postnatal MRI
showed normal vermis in three (Cases 5, 17 and 25) and
asymmetrical brainstem in two (Cases 5 and 25). Postnatal
MRI was not performed in Case 20. Based on our collection of data, the surface loss of cerebellar hemisphere did
not correlate with poor prognosis, and UCH with normal
vermis was often associated with normal outcome in the
absence of associated pathologies. However, despite the
normal outcome of our two infants with abnormal vermis,
we believe that in these cases the prognosis is of concern,
as noted by Poretti et al.10 , since vermian lesion is often
associated with poor cognitive outcome.
REFERENCES
1. Guibaud L, Des Portes V. Plea for an anatomical approach
to abnormalities of the posterior fossa in prenatal diagnosis.
2. Baulhauser E. Cerebellum - small brain but large confusion:
a review of selected cerebellar malformations and disruptions.
Am J Med Genet A 2004; 126A: 376–385.
3. Barkovich AJ. Neuroimaging manifestations and classification
of congenital muscular dystrophies. AJNR Am J Neuroradiol
1998; 19: 1389–1396.
4. Mancini J, Lathel V, Hugonenq C, Charbol B. Brain injuries in
early foetal life: consequences for brain development. Dev Med
Child Neurol 2001; 43: 52–55.
5. Gorincour G, Rypens F, Lapierre C, Costa T, Audibert F,
Robitaille Y. Fetal magnetic resonance imaging in the prenatal
diagnosis of cerebellar hemorrhage. Ultrasound Obstet Gynecol
2006; 27: 78–80.
6. Malinger G, Zahalka N, Kidron D, Ben-Sira L, Lev D,
Lerman-Sagie T. Fatal outcome following foetal cerebellar
haemorrhage associated with placental thrombosis. Eur J
Paediatr Neurol 2006; 10: 93–96.
7. Sharony R, Kidron D, Aviram R, Beyth Y, Tepper R. Prenatal
diagnosis of fetal cerebellar lesions: a case report and review of
the literature. Prenat Diagn 1999; 19: 1077–1080.
8. Yuksel A, Batukan C. Foetal cerebellar haemorrhage in a
severely growth-restricted fetus: natural history and differential
diagnosis from Dandy–Walker malformation. Ultrasound
Obstet Gynecol 2003; 22: 178–181.
9. Ranzini AC, Shen-Schwarz S, Guzman ER, Fisher AJ, White
M, Vintzileos AM. Prenatal sonographic appearance of
haemorrhagic cerebellar infarction. J Ultrasound Med 1998;
17: 725–727.
10. Poretti A, Limperopoulos C, Roulet-Perez E, Wolf NI, Rauscher
C, Prayer D, Müller A, Weissert M, Kotzaeridou U, Du
Plessis AJ, Huisman TA, Boltshauser E. Outcome of severe
unilateral cerebellar hypoplasia. Dev Med Child Neurol 2010;
52: 718–724.
11. Benbir G, Kara S, Yalcinkaya BC, Karhkaya G, Tuysuz B, Kocer
N, Yalcinkaya C. Unilateral cerebellar hypoplasia with different
clinical features. Cerebellum 2011; 10: 49–60.
12. Boltshauser E, Steinlin M, Martin E, Deonna TH. Unilateral
cerebellar aplasia. Neropediatrics 1996; 27: 50–53.
13. Patel S, Barkovich AJ. Analysis and classification of cerebellar
malformations. AJNR Am J Neuroradiol 2002; 23: 1074–1087.
14. Guibaud L, Garel C, Annie B, Pascal G, Francois V, Vavasseur
C, Oury JF, Pracros JP. Prenatal diagnosis of capillary
telangiectasia of the cerebellum - ultrasound and MRI features.
Prenat Diagn 2003; 23: 791–796.
15. Messerschmidt A, Brugger PC, Boltshauser E, Zoder G,
Sterniste W, Birnbacher R, Prayer D. Disruption of cerebellar
development: potential complication of extreme prematurity.
AJNR Am J Neuroradiol 2005; 26: 1659–1667.
16. Goldstein I, Reece EA, Pilu G, Bovicelli, Hobbins JC. Cerebellar
measurements with ultrasonography in the evaluation of fetal
growth and development. Am J Obstet Gynecol1987; 156:
1065–1069.
17. Govaert P. Prenatal stroke. Semin Fetal Neonatal Med 2009;
14: 250–266.
18. Metry D, Heyer G, Hess C, Garzon M, Haggstrom , Frommelt
P, Adams D, Siegel D, Hall K, Powell J, Frieden I, Drolet B.
PHACE Syndrome Research Conference. Consensus Statement
on Diagnostic Criteria for PHACE Syndrome. Pediatrics 2009;
124: 1447–1456.
19. Carles D, Pelluard F, Alberti EM, Maugey-Laulom B, Lin TY,
Saura R, Roux D, Lacombe D. Fetal presentation of PHACES
syndrome. Am J Med Genet A 2005; 132: 110.
20. Recio-Rodrı́guez M, Martı́n Fernández-Mayoralas D,
Jiménez-de-la-Peña M, Fernández-Jaén A. PHACES syndrome
(Pascual Castroviejo type II): prenatal and postnatal magnetic
resonance imaging. Radiologia 2013; 55: 537–540.
21. de Vries LS, Gunardi H, Barth PG, Bok LA, Verboon-Maciolek
MA, Groenendaal F. The spectrum of cranial ultrasound
and magnetic resonance imaging abnormalities in congenital cytomegalovirus infection. Neuropediatrics 2004; 35:
113–119.
22. Malinger G, Lev D, Zahalka N, Ben Aroia Z, Watemberg
N, Kidron D, Sira LB, Lerman-Sagie T. Fetal cytomegalovirus
infection of the brain: the spectrum of sonographic findings.
AJNR Am J Neuroradiol 2003; 24: 28–32.
23. Bissinger AL, Sinzger C, Kaiserling E, Jahn G. Human
cytomegalovirus as a direct pathogen: correlation of multiorgan
involvement and cell distribution with clinical and pathological
findings in a case of congenital inclusion disease. J Med Virol
2002; 67: 200–206.
24. Harbord MG, Finn JP, Hall-Craggs MA, Brett EM, Baraitser
M. Moebius’ syndrome with unilateral cerebellar hypoplasia. J
Med Genet 1989; 26: 579–582.
25. Martinelli P, Maruotti GM, Agangi A, Mazzarelli LL,
Bifulco G, Paladini D. Prenatal diagnosis of hemifacial
microsomia and ipsilateral cerebellar hypoplasia in a fetus with
oculoauriculovertebral spectrum. Ultrasound Obstet Gynecol
2004; 24: 199–201.
26. Titomanlio L, De Brasi D, Romano A, Genesio R, Diano AA,
Del Giudice E. Partial cerebellar hypoplasia in a patient with
Prader–Willi syndrome. Acta Paediatr 2006; 95: 861–863.
27. Serrano-Gonzalez C, Prats Vinas JM. [Unilateral aplasia of
the cerebellum in Aicardi’s syndrome]. Neurolgia 1998; 13:
254–256.
28. Conradi NG. Cerebellar foliation in rats. 1. Cortical changes
preceding the formation of a fissure. Acta Pathol Microbiol
Immunol Scand 1985; 93: 385–389.
29. Garel C. Posterior fossa malformations: main features and limits
in prenatal diagnosis. Pediatr Radiol 2010; 40: 1038–1045.
SUPPORTING INFORMATION ON THE INTERNET
Tables S1 and S2 Summary of clinical and imaging findings and neonatal outcome of fetuses with
asymmetrical cerebellar hemispheres which showed progressive changes in imaging features during follow-up
(Group 1, Table S1) or no change in imaging features during follow-up (Group 2, Table S2)

Prenatal unilateral cerebellar hypoplasia in a series of 26 cases

Transcription

Similar documents

Cerebellum (Small brain)

LOCALIZATION NEUROLOGY HEARING LOSS AND GAIT ATAXIA

could abnormal fetal movements be a clue to the prenatal diagnosis

Brothers - iCareAboutOrphans

radiology - Health Careers

Thomas - iCareAboutOrphans

Catastrophic Cerebellitis in an adolescent: A Case Report

PDF - Samsung Medison

ZONARE Vascular Radiology

Postinfectious Cerebellitis - LVHN Scholarly Works