Child’s Nervous System
https://doi.org/10.1007/s00381-021-05265-x

CASE REPORT

Cerebrofacial vascular metameric syndrome associated
with Moyamoya syndrome: a rare case report
Aldo José F da Silva1 · Ana Carolina de Carvalho Ruela Pires2
Carla Roberta Vieira da Silva3

· Lara Cansanção Lopes de Farias3

·

Received: 7 April 2021 / Accepted: 12 June 2021
© The Author(s), under exclusive licence to Springer-Verlag GmbH Germany, part of Springer Nature 2021

Abstract
Introduction Neural crest and mesoderm cell dysfunction of certain metameric level result in vascular malformations, i.e.,
cerebrofacial arteriovenous metameric syndrome (CAMS) and cerebrofacial venous metameric syndrome (CVMS). Moyamoya disease is a progressive steno-occlusive disease in the terminal portions of the bilateral internal carotid artery. The
patient in this case report was a child with cerebrofacial vascular metameric syndrome, associated with moyamoya syndrome.
Case report Child, 7 months old, female, admitted to the emergency department with seizures, hemangioma on the right
half of the face (forehead, upper eyelid, and upper lip), and left hemiparesis. The magnetic resonance imaging of the skull
indicated increased myelination in the right hemisphere (T2) and atrophy compatible with Sturge-Weber syndrome. Cerebral
angiography indicated vasculopathy with bilateral moyamoya pattern, associated with other arteriovenous malformations
compatible with cerebrofacial vascular metameric syndrome. Moyamoya syndrome was treated with indirect revascularization (pial synangiosis) achieving good outcomes.
Discussion Vascular malformations can involve the orbits, face, and brain simultaneously. CAMS with forebrain or hindbrain involvement can be classified into subgroups: I, II, and III. On the other hand, venous malformations in Sturge-Weber
syndrome or encephalotrigeminal angiomatosis can be considered CVMS. Moyamoya disease is called syndrome when
related to another clinical condition, such as the present case, i.e., neurocutaneous Sturge-Weber syndrome. The association
of chronic moyamoya vasculopathy with cerebrofacial vascular metameric syndrome is rare. Further studies are required to
establish the best treatment approach.
Keywords Vascular malformations · Hemangioma · Moyamoya · Arteriovenous

Introduction
* Aldo José F da Silva
neuroajfs@yahoo.com.br
Ana Carolina de Carvalho Ruela Pires
anacarolinaruelapires@gmail.com
Lara Cansanção Lopes de Farias
lara_farias07@hotmail.com
Carla Roberta Vieira da Silva
craves.2020@gmail.com
1

Pediatric Neurosurgery, General State Hospital
and at the Pediatric Neurosurgery Division of the Santa
Mônica Teaching Maternity - Alagoas State University
of Health Sciences, Maceió, Alagoas, Brazil

2

Pediatric Division, General State Hospital (GSH)
and CESMAC University Center, Maceió, Alagoas, Brazil

3

Graduated in Medicine, CESMAC University Center,
Maceió, Alagoas, Brazil

Studies have pointed out that the cells of the neural crest
and mesoderm of certain transversal or metameric level will
occupy the same territory in the face and in the brain and
will also help in myogenesis and vasogenesis. The early dysfunction of these cells during migration and differentiation
results in vascular malformations, which can be a genetic
defect or somatic mutation [1, 2]. This way, the names “cerebrofacial arteriovenous metameric syndrome” (CAMS) and
“cerebrofacial venous metameric syndrome” (CVMS) have
been suggested, corresponding to arterial and venous malformations, respectively, involving the face and the brain at
the same time [3].
In turn, Moyamoya disease is considered a progressive
steno-occlusive disease occurring in the terminal portions of
the bilateral internal carotid artery, with the development of

13

Vol.:(0123456789)

Child’s Nervous System

collaterals, called “moyamoya vessels,” to ensure the circulation channels. When associated with other pathological conditions, it is called syndrome [4]. The present report describes
the case of a child with cerebrofacial vascular metameric
syndrome, rarely associated with moyamoya syndrome.

Case report
This is the case of a 7-month-old girl, daughter of nonconsanguineous parents, admitted to the emergency department with convulsions and weakness on the left side of the
body. Upon examination, she exhibited hemangioma on the
Fig. 1  a Hemangioma on
the right half of the face:
forehead,upper eyelid, and
upper lip (blackarrows); b
brainmagnetic resonance imaging, axial T2 showing hypointensity with atrophy in theright
cerebral hemisphere (whitearrow); c arteriovenousmalformations involving cisterns at the
base of the brain and hypothalamicregion (black arrow)
with extension to the right orbit
(whitearrow); and d angiogram
showing arteriovenous malformations in the right orbit (black
arrow) supplied by branches of
the facial artery(white arrow)

13

right half of the face (forehead, upper eyelid, and upper lip)
(Fig. 1a), irritability, and left hemiparesis. The other systems (cardiovascular and respiratory) had no alterations. The
child’s birth had been at term, with normal labor and no
complications. The progression was normal, and she was
immunized for her age. There was no family history of the
condition.
Magnetic resonance imaging (T2) indicatedsubcortical
white matter hypointensity (Fig.1b), with accentuation of
the myelination patternof the entire right cerebral hemisphere, and atrophy compatible withSturge-Weber syndrome
(Fig. 1a). In addition, there were arteriovenous malformationsin the cisterns at the base of the brain (Willis polygon),

Child’s Nervous System

with extension tothe right orbit through the optic nerve,
associated with multiple ectatic andtortuous vessels, thus
configuring a CAMS II-type lateral prosencephalicarteriovenous malformation (Fig. 1c, d).
Cerebral angiography indicated vasculopathy with bilateral moyamoya pattern (Fig. 2), associated with bilateral
orbital arteriovenous malformation and aneurysmatic formation with dysplastic vessels of the basilar artery and right
posterior communicating artery.
In view of the diagnosis of bilateral moyamoya syndrome,
with episodes of cerebral ischemia, it was decided to perform
surgical treatment. Indirect revascularization was performed
through bilateral pial synangiosis (Fig. 3a, c). The procedure
was performed without problems. Cerebral angiography was
performed 8 months after the surgery. It evidenced signs of
anastomosis between branches of the superficial temporal
artery, and cortical branches of the middle cerebral artery on
the left side (Fig. 3b). However, the procedure on the right
side did not present a favorable (Fig. 3d) result because we

could not say whether the ischemic suffering would be Moyamoya or Sturge-Weber syndrome. The child had no seizures
(using phenobarbital), with improvement in left hemiparesis
after rehabilitation by means of physiotherapy.

Fig. 2  a AP and b lateral view of cerebral angiography showing a
network of collateral vessels or Moyamoya vessels (black arrows) and
poor visualization of the terminal branches of the left internal carotid
artery (ICA): anterior cerebral and middle cerebral arteries (white
arrows); c lateral view of cerebral angiography showing preserved
left posterior circulation; d AP and e lateral view of cerebral angi-

ography showing stenosis of the supraclinoid segment of the right
internal carotid artery (white arrowhead), with steno-occlusive lesion
of the middle cerebral artery, presence of a network of collateral vessels (black arrows) with aneurysmatic formations and normal anterior
cerebral artery(white arrow); f lateral view of cerebral angiography
showing preserved right posterior circulation

Discussion
In 2001, Bhattacharya et al. observed evidence of metameric
craniofacial vascular malformations, with typical characteristics and revised embryology [2,5]. This way, a classification of three subgroups determined as CAMS was proposed
based on the involvement of the forebrain or rhombencephalon, namely, CAMS I—medial prosencephalic group involving the hypothalamus, pituitary, and nasal regions; CAMS
II—lateral prosencephalic group involving the occipital
lobe, thalamus, optic tract, retina, and maxilla; and CAMS
III—lateral rhombencephalon group involving the cerebellum, nasal bridge, and mandible [5, 6]. According to the

13

Child’s Nervous System
Fig. 3  a Left pial synangiosis—
branch of the left superficial
temporal artery sutured directly
to the pia mater (black arrows);
b postoperative with formation
of neovascularization (white
ring) between branches of the
superficial temporal artery and
cortical branches of the middle
cerebral artery; c right pial
synangiosis (black arrow) with
cerebral atrophy (curved black
arrow); d postoperative with
formation of mild neovascularization (white ring)

alterations in images of the present case, the CAMS II subgroup would be the most similar.
Sturge-Weber syndrome is a neurocutaneous syndrome
that, due to veno-lymphatic malformations on the face and
brain, is characterized by maxillofacial port-wine stains, cerebral atrophy, convulsions, cortical vessel and parenchymal
calcifications, maxillofacial and cranial bone hypertrophy,
ocular abnormalities (glaucoma and choroidal hemorrhage),
and leptomeningeal angiomatosis [7, 8]. Venous malformations observed in Sturge-Weber syndrome can be considered
CVMS. In the case presented, CVMS with port-wine stains
on the face and image alterations characteristic of SturgeWeber syndrome were evident.
Moyamoya disease is characterized by a progressive
steno-occlusive disease in the terminal portions of the internal carotid arteries and their main branches [9]. This disease is related to neural crest pathology or neurochristopathy
[10]. It is called syndrome when related to another clinical
condition, such as the present case, i.e., neurocutaneous
Sturge-Weber syndrome[11].

13

The metameric arrangement of intracranial arteries suggests that the region of the brain (more specifically derived
from the prosencephalon and diencephalon), supplied by the
primitive internal carotid arteries, is more prone to intimal
thickening. Therefore, it is expected that the cerebral arteries
in Moyamoya disease have preexisting structural defects that
are not known and remain latent during vasculogenesis [12].
The gold standard image exam is cerebral angiography,
which will more accurately demonstrate the stenotic vessels, the network of collateral vessels, in addition to small
aneurysms that may be associated [11].
Due to the fact that this disease is characterized by progressive worsening in its evolution, the most appropriate
approach would be surgery. There are two surgical techniques, namely, (1) direct revascularization with intracranial-extracranial anastomoses. The great disadvantage of
this technique is children with small-sized vessels and (2)
indirect revascularization performed with the contact of
the vascularized tissue of the external carotid artery (dura
mater, temporal muscle, or even branches of the superficial

Child’s Nervous System

temporal artery) and the surface of the brain. Unfortunately,
this technique should not be used in an emergency, as a time
interval is required for neovascularization [11]. The case
described was treated with the technique of indirect revascularization by pial synangiosis. Neovascularization was only
observed after 8 months.
A rare association between chronic moyamoya vasculopathy and cerebrofacial vascular metameric syndrome was
observed in the present case report. They are severe vascular
malformations with few reports in the literature. Therefore,
further studies should be conducted with the goal of establishing the best treatment approach.

3.

4.
5.

6.
7.

Author contribution Conception and design: da Silva. Acquisition
of data: all authors. Analysis and interpretation of data: all authors.
Drafting the article: all authors. Critically revising the article: da Silva.
Reviewed submitted version of manuscript: all authors. Approved the
final version of the manuscript on behalf of all authors: da Silva

8.
9.

Declarations
Ethics approval This article does not contain any studies with animals
performed by any of the authors.
Consent to participate Informed consent was obtained from parents.

10.

11.

Conflict of interest On behalf of all authors, the corresponding author
states that there is no conflict of interest.

References
1. Brinjikji W, Nicholson P, Hilditch CA, Krings T, Pereira V, Agid
R (2020) Cerebrofacial venous metameric syndrome-spectrum of
imaging findings. Neuroradiology 62(4):417–425. https://d​ oi.o​ rg/​
10.​1007/​s00234-​020-​02362-7
2. Wong IY, Batista LL, Alvarez H, Lasjaunias PL (2003) Craniofacial arteriovenous metameric syndrome (CAMS) 3–a transitional
pattern between CAM 1 and 2 and spinal arteriovenous metameric

12.

syndromes. Neuroradiology 45(9):611–615. https://​doi.​org/​10.​
1007/​s00234-​003-​1041-x
Krings T, Geibprasert S, Luo CB, Bhattacharya JJ, Alvarez H,
Lasjaunias P (2007) Segmental neurovascular syndromes in children. Neuroimaging Clin N Am 17(2):245–258. https://​doi.​org/​
10.​1016/j.​nic.​2007.​02.​006
Janda PH, Bellew JG, Veerappan V (2009) Moyamoya disease: case report and literature review. J Am Osteopath Assoc
109(10):547–553
O’Loughlin L, Groves ML, Miller NR, Pearl MS (2017) Cerebrofacial arteriovenous metameric syndrome (CAMS): a spectrum
disorder of craniofacial vascular malformations. Childs Nerv Syst
33(3):513–516. https://​doi.​org/​10.​1007/​s00381-​016-​3277-x
Agid R, Terbrugge KG (2007) Cerebrofacial venous metameric
syndrome 2 plus 3: facial and cerebral manifestations. Interv Neuroradiol 13(1):55–58. https://​doi.​org/​10.​1177/​15910​19907​01300​107
Luo C, Bhattacharya J, Ferreira M, Alvarez H, Rodesch G, Lasjaunias
P (2003) Cerebrofacial vascular disease. Orbit 22(2):89–102. https://​
doi.​org/​10.​1076/​orbi.​22.2.​89.​14312
Hao Z, Lai X (2019) Sturge-Weber syndrome coexisting with
moyamoya disease in the fifth decade: a case report and literature
review. Neurologist 24(1):13–16
Currie S, Raghavan A, Batty R, Connolly DJ, Griffiths PD (2011)
Childhood Moyamoya disease and moyamoya syndrome: a pictorial review. Pediatr Neurol 44(6):401–413. https://​doi.​org/​10.​
1016/j.​pedia​trneu​rol.​2011.​02.​007
Komiyama M (2017) Moyamoya disease is a vascular form of
neurocristopathy: disease of the embryologic cephalic neural
crest. Childs Nerv Syst 33(4):567–568. https://​doi.​org/​10.​1007/​
s00381-​017-​3369-2
Tharayil AM, Ganaw AEA, Shaikh N, Prabhakaran SM, Chanda
AH, Praveen S, Choran AK, ul Haq QZ (2019) Moyamoya disease: a rare vascular disease of the CNS. In: Vascular malformations of the central nervous system. Bora Gürer Pinar Kuru
Bektaşoğlu. Available from: https://​w ww.​i ntec​h open.​c om/​
books/​vascu​lar-​malfo​r mati​ons-​of-​the-​centr​al-​nervo​us-​system/​
moyam​oya-​disea​se-a-​rare-​vascu​lar-​disea​se-​of-​the-​cns
Komiyama M (2003) Moyamoya disease is a progressive occlusive
arteriopathy of the primitive internal carotid artery. Interv Neuroradiol 9(1):39–45. https://​doi.​org/​10.​1177/​15910​19903​00900​105

Publisher’s Note Springer Nature remains neutral with regard to
jurisdictional claims in published maps and institutional affiliations.

13