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Moyamoya Syndrome Associated With Congenital Heart Disease

Joel Lutterman, MD*§; Michael Scott, MD‡i; Ruth Nass, MD¶; and Tal Geva, MD*§

ABSTRACT. Objective. To describe the association between moyamoya syndrome and congenital heart dis-ease and to discuss its clinical implications.

Study Design. Retrospective analysis of a case series from two institutions.

Results. Five patients with moyamoya syndrome and structural congenital heart disease were identified. Co-arctation of the aorta was present in 3 patients, in asso-ciation with a ventricular septal defect (1 patient), aortic and mitral valve stenoses (1 patient), and tetralogy of Fallot (1 patient). Tetralogy of Fallot and a large paramembranous ventricular septal defect were found in the other 2 patients. Four patients underwent surgical repair of their congenital heart disease during the first year of life and 1 patient had balloon dilation of aortic coarctation at 5 years of age. In all patients, moyamoya syndrome was diagnosed after surgical intervention for congenital heart disease—at 6 months of age in 1 patient, at 2 years of age in 3 patients, and at 6 years in 1 patient. Strokes were the most common presenting sign (3 pa-tients) followed by seizures (2 papa-tients). By the age of 33 months, 4 of 5 patients had undergone cerebral revascu-larization surgery to halt the clinical progression of moyamoya syndrome.

Conclusions. Moyamoya syndrome should be consid-ered in the differential diagnosis of seizures and stroke in patients with structural congenital heart disease. Prompt diagnosis and surgical management of the occlu-sive cerebral angiopathy should lead to improved neuro-logical outcome in these patients.Pediatrics1998;101:57– 60; congenital heart disease, moyamoya syndrome, neurosurgery, seizure, stroke.

M

oyamoya is a chronic cerebrovascular dis-ease of unknown etiology characterized by progressive stenosis and occlusion of the arteries comprising the circle of Willis and its branches, especially the internal carotid arteries.1,2

Due to the slow progression of the disease and in response to progressive cerebral ischemia, a large network of collateral vessels is formed from the ex-ternal carotid arteries, the vertebral-basilar system, and other vessels.2,3Cerebral angiography reveals an

extensive network of collateral vessels formed from enlarged penetrating vessels from the apex of the internal carotid artery that ordinarily supply the op-tic system, hypothalamus, and anterior-perforated

substance. These dilated vessles form a cloud of hy-pervascularity around the internal carotid artery on cerebral angiography, hence the name for the syn-drome of “moyamoya”—a Japanese phrase meaning “puff of smoke.”1–3Although moyamoya syndrome

can present in both adults and children, clinical man-ifestations are thought to be age-dependent. Adults more often present with subarachnoid or intracere-bral hemorrhage and children more often present with seizures and transient, often alternating, hemi-plegia.2,3 Intellectual impairment is often worse in

childhood presentation.3 Patients presenting as

young as 4 months old have been reported.3

Several studies have suggested a genetic predispo-sition for moyamoya syndrome4,5 and associations

with neurofibromatosis and the syndromes of Down, Turner, Alagille, and Williams have been report-ed.6 –14 To our knowledge, the coexistence of

moya-moya syndrome and congenital heart disease has not been documented. This report describes 5 such pa-tients and discusses the diagnostic and management implications of the coexistence of the two conditions.

METHODS Patients

The computerized databases of the Cardiovascular Program and the Department of Neurosurgery at Children’s Hospital in Boston were searched for patients diagnosed with moyamoya and congenital heart disease from January 1, 1983 through December 31, 1995. All clinical, echocardiographic, catheterization, and op-erative diagnoses were scanned. During that period, 65 patients with moyamoya syndrome were seen in the Department of Neu-rosurgery at Children’s Hospital. An additional case diagnosed at New York University Medical Center in New York is included in this report. The records of the 5 patients identified as having moyamoya syndrome and congenital heart disease were retro-spectively reviewed.

Diagnostic Criteria

Patients were diagnosed with moyamoya when cerebral an-giography demonstrated bilateral stenosis or occlusion of the in-ternal carotid artery at its intracranial bifurcation accompanied by the presence of enlarged penetrating vessels at or near the site of the obstruction which were partially collateralizing vasculature distal to the arterial stenosis (Fig 1A).

Patients with a patent foramen ovale were not included in this study. Similarly, premature and newborn infants with an isolated patent ductus arteriosus and physiological peripheral branch pul-monary artery stenosis were excluded.

RESULTS

Patient characteristics are summarized in the Ta-ble. Three patients had additional diseases: renal hypoplasia and congenital hip dysplasia in patient 2, neurofibromatosis in patient 3, and trisomy 21 in patient 5. All patients presented in the newborn pe-riod with signs of congenital heart disease, typically

From the Departments of *Cardiology and ‡Neurosurgery, Children’s Hos-pital, Boston, Massachusetts; the Departments of §Pediatrics andiSurgery, Harvard Medical School, Boston, Massachusetts; and the ¶Department of Neurology, New York University Medical Center, New York, New York. Received for publication Apr 10, 1997; accepted Jun 26, 1997.

Address correspondence to: Tal Geva, MD, Department of Cardiology, Children’s Hospital, 300 Longwood Ave, Boston, MA 02115.

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a prominent heart murmur. The specific cardiac diag-noses were subsequently confirmed by echocardiogra-phy. Coarctation of the aorta was present in 3 patients, 1 of whom had a ventricular septal defect and patent ductus arteriosus (patient 1), 1 had aortic and mitral valve stenoses (patient 2), and 1 (patient 4) had tetral-ogy of Fallot (Fig 2). Another patient also had tetraltetral-ogy of Fallot (patient 3) and one patient had a large paramembranous ventricular septal defect (patient 5). Four patients underwent surgical repair of their con-genital heart disease during the first year of life. Three patients required repeat interventions for residual or recurrent cardiac anomalies after the initial operation (Table). There was no cardiac-related mortality in this

series. At the time of most recent follow-up, the cardiac status of 4 patients was good. One patient died of complications after renal transplantation.

In all patients, moyamoya syndrome was diag-nosed after surgical intervention for congenital heart disease. Moyamoya syndrome was diagnosed at 6 months of age in 1 patient, at 2 years of age in 3 patients and at 6 years of age in 1 patient. Strokes were the most common presenting sign (3 patients) followed by seizures (2 patients). By age 33 months, 4 patients had undergone revascularization surgery to halt the clinical progression of moyamoya syn-drome (Fig 1). Cerebral revascularization was carried out in patient 2 at 6.7 years of age. To date, this

Fig 1. Selective cerebral angiograms in patient 5 before and after cerebral revascularization. A, Preoperative selective left internal carotid arteriogram in the anteroposterior projection shows tapering, near-total occlusion at the intracranial carotid bifurcation (arrow) with severe narrowing of the middle cerebral artery. The moyamoya vessels above the subtotal occlusion of the internal carotid artery partially reconstitutes the midline anterior cerebral artery. B, Postoperative left internal carotid arteriogram 1 year after pial synangiosis. The middle cerebral artery is occluded and the moyamoya vessels persist (straight arrow). The ophthalmic artery (curved arrow) collateralizes the left basal frontal lobe through transdural and calvarial vessels. C, Early-phase selective left external carotid arteriogram shows an enlarged superficial temporal artery (straight arrow) and middle meningeal artery (curved arrow) collateralizing the cerebral vascular area beneath the craniotomy area. D, Late phase of the same injection demonstrates revascularization of the posterior, frontal, and temporal lobe circulation.

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patient is the only one in the present series to have died, the result of postoperative complications after orthotopic renal transplantation.

The neurosurgical procedure carried out in pa-tients 2 through 5 was “pial synangiosis,” in which an intact scalp vessel (usually a branch of the super-ficial temporal artery) is sutured directly to the brain surface after the dura and arachnoid membranes have been opened.15 Patient 1 underwent bilateral

external carotid artery to internal carotid artery anas-tomosis (encephalodurosynangiosis). The neurologi-cal outcome of the 4 surviving patients has varied from severe impairment, including spastic

quadra-paresis and pseudobulbar palsy, to minimal motor delay (Table) and seems dependent on the patients’ neurological status at the time of neurosurgery.

DISCUSSION

The association of moyamoya syndrome and con-genital heart disease has two important implications. From a clinical standpoint, moyamoya syndrome has not been considered in the traditional differential diagnosis of neurological complications in patients with congenital heart disease. From the standpoint of etiology, the findings reported in this series raise the

TABLE. Patient Characteristics and Interventions

Patient 1 2 3 4 5

Gender M F F F M

Age at diagnosis of congenital heart disease

Birth Birth Birth 3 days Birth

Congenital heart disease

CoA, PDA, VSD CoA, AS, MS TOF TOF, RAA, ALSCA,

CoA

Paramembranous VSD

Cardiac 15 days: CoA repair; 5 years: CoA balloon 7 months: BTS; 5 days: CoA repair, 10 months: VSD

interventions 14 months: PDA ligation, aortic

angioplasty 2 years: TOF repair 3 months: vascular ring repair;

repair

augmentation 14 months: TOF

repair;

8 years: CoA balloon angioplasty Age at diagnosis of

moyamoya disease

6 months 6 years 2.2 years 2 years 2 years

Neurological signs Seizures, bilateral hemiparesis and serial strokes

Hemorrhagic strokes Seizures, strokes Multiple strokes Right hemiparesis, multiple strokes

Neurosurgical interventions

1.5 years: bilateral EDAS

6.7 years: left pial synangiosis

2.5 years: bilateral pial synangiosis

2.7 years: bilateral pial synangiosis

2.5 years: bilateral pial synangiosis Associated

anomalies

None Renal hypoplasia,

congenital hip dysplasia

Neurofibromatosis None Trisomy 21

Outcome 7 years: pseudo-bulbar

palsy, spastic quadra-paresis, mute, mildly retarded

7.3 years: died after renal transplant

10.5 years: mild speech delay, mild left hemiparesis

9 years: mild speech delay

4.5 years: mild motor delay

Abbreviations: ALSCA, anomalous origin of the left subclavian artery; AS, aortic stenosis; BTS, Blalock-Taussig shunt; CoA, coarctation of the aorta; EDAS, encephaloduroarteriosynangiosis; F, female; MS, mitral stenosis; M, male; PDA, patent ductus arteriosus; RAA, right aortic arch; TOF, tetralogy of Fallot; VSD, ventricular septal defect.

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possibility that the link between the two disease processes may not be incidental.

The incidence of congenital heart disease in the gen-eral population varies from 8 to 10 cases per 1000 live births.16 Among the 65 patients with moyamoya

syn-drome followed at Children’s Hospital in Boston, 4 (6.1%) were diagnosed with significant congenital heart disease. The incidence of moyamoya syndrome among all patients with congenital heart disease is not known. Because moyamoya syndrome is relatively rare with a reported incidence of 0.07%,17it is not surprising that

the association of moyamoya syndrome and congenital heart disease has not been widely appreciated.

The higher prevalence of the disease in Japan7and

its increased occurrence in some families4 have

prompted consideration of a genetic component of the disease.5,9The number of affected patients,

how-ever, is small and a clear link has not been estab-lished. Four of the 5 patients reported in this series had either conotruncal or obstructive aortic arch anomalies. These anomalies may be linked via de-fects of the embryonic neural crest, which has been associated with anomalies of chromosome 22.19,20

Normal migration and function of neural crest cells are essential for normal development of the conus, truncus arteriosus, and aortic arches.21 Among the

patients reported in this series, only patient 3 under-went genetic testing of chromosome 22 and no mi-crodeletions were found. Further investigation into the etiology and mechanism of moyamoya syndrome and congenital heart disease is needed.

From a clinical standpoint, seizures and strokes can complicate the course of infants and children before and after repair of congenital heart disease.22

Among frequently considered etiologies are throm-boembolism, ischemic insults, hemorrhage, and in situ thrombosis.22Some patients are found ultimately

to have a primary seizure disorder. The cases pre-sented here illustrate the need to consider moya-moya syndrome in the differential diagnosis of sei-zures and other neurological symptoms in patients with congenital heart disease. The typical clinical course observed in the current series is characterized by the development of seizures or strokes months to years after repair of congenital heart disease. Al-though it is common to relate the neurological symp-toms to the heart disease, its sequelae, or its treat-ment, the possibility of moyamoya syndrome should be investigated. Vascular changes typical of this con-dition are almost always recognizable on axial mag-netic resonance imaging studies, with reduced or absent caliber of the flow-voids in the internal ca-rotid and proximal middle cerebral arteries. In ad-vanced cases, multiple flow-voids representing the moyamoya collaterals are seen as these vessels course upward through the basal ganglia. Magnetic resonance angiography is also useful in delineating vascular abnormalities.4Prompt diagnosis and

treat-ment of moyamoya syndrome is important in these children to prevent progressive neurologic deterio-ration. The ischemic brain of these children shows a remarkable propensity to attract new blood supply and cerebral angiography 1 year after pial synangio-sis has invariably demonstrated striking new

collat-eral flow to the cerebral vessels distal to areas of stenosis or occlusion with a stable subsequent clini-cal course. The authors believe that aggressive eval-uation of children with congenital heart disease and symptoms of cerebral ischemia is warranted to detect the presence of moyamoya syndrome.

ACKNOWLEDGMENTS

We thank Arthur A. Klein, MD, at New York Hospital-Cornell, New York, NY; Charles S. Kleinman, MD, at Yale University Hospital, Yale-New Haven, CT; and John C. Werner, MD, at Hasbro Children’s Hospital, Providence, RI, for information about the cardiac status of their patients.

REFERENCES

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2. Suzuki J, Kodama N. Moyamoya disease—a review.Stroke.1983;14: 104 –109

3. Fukuyama Y, Umezu R. Clinical and cerebral angiographic evolutions of idiopathic progressive occlusive disease of the circle of Willis (“Moyamoya” disease) in children.Brain Dev.1985;7:21–37

4. Kikuchi M, Hayakawa H, Takahashi I, et al. Moyamoya disease in three siblings—follow-up study with magnetic resonance angiography (MRA).Neuropediatrics.1995;26:33–36

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7. Fukushima Y, Kondo Y, Kuroki Y, et al. Are Down syndrome patients predisposed to moyamoya disease?Eur J Pediatr.1986;144:516 –517 8. Fukuyama Y, Osawa M, Kanai N. Moyamoya disease (syndrome) and

the Down syndrome.Brain Dev.1992;14:254 –256

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10. Schrager G, Cohen S, Vigman MP. Acute hemiplegia and cortical blind-ness due to moyamoya disease: report of a case in a child with Down’s syndrome.Pediatrics.1977;60:33–37

11. Ajimi Y, Uchida K, Kawase T, Toya S. A case of Turner’s syndrome associated with moyamoya disease.Neurol Surg.1992;20:1021–1024 12. Rachmel A, Zeharia A, Neuman-Levin M, Weitz R, Shamir R, Dinari G.

Alagille syndrome associated with moyamoya disease.Am J Med Genet.

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13. Kawai M, Nishikawa T, Tanaka M, et al. An autopsied case of Williams syndrome complicated by moyamoya disease.Acta Paediatr Jpn.1993; 35:63– 67

14. Woody RC, Perrot LJ, Beck SA. Neurofibromatosis cerebral vasculopa-thy in an infant: clinical, neuroradiographic, and neuropathologic stud-ies.Pediatr Pathol.1992;12:613– 619

15. Adelson PD, Scott RM. Pial synangiosis for moyamoya syndrome in children.Pediatr Neurosurg.1995;23:26 –33

16. Mitchell SC, Korones SB, Berendes HW. Congenital heart disease in 56,109 births.Circulation.1971;43:323–332

17. Goto Y, Yonekawa Y. Worldwide distribution of moyamoya disease.

Neurol Med Chir.1992;32:883– 886

18. Wilson DI, Burn J, Scrambler P, Goodship J. DiGeorge syndrome: part of catch 22.J Med Genet.1993;30:852– 856

19. Crifasi PA, Michels VV, Driscol DJ, Jalal SM, DeWald GD. DNA fluo-rescent probes for diagnosis of velocardiofacial and related syndromes.

Mayo Clin Proc.1995;70:1148 –1153

20. Gunthard J, Murdison KA, Wagner HR, Norwood WI. Tetralogy of Fallot and coarctation of the aorta: a rare combination and its clinical implications.Pediatr Cardiol.1992;13:37– 40

21. Waldo KL, Kirby ML. Cardiac neural crest contribution to the pulmo-nary artery and sixth aortic arch artery complex in chick embryos aged 6 to 18 days.Anat Rec.1993;237:385–399

22. Fishman MA, Parke JT. Neurologic issues of importance for the pedi-atric cardiologist. In: Garson AT, Bricker JT, McNamara DG, eds.The Science and Practice of Pediatric Cardiology. Philadelphia, PA: Lea & Febiger; 1990:2305–2327

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DOI: 10.1542/peds.101.1.57

1998;101;57

Pediatrics

Joel Lutterman, Michael Scott, Ruth Nass and Tal Geva

Moyamoya Syndrome Associated With Congenital Heart Disease

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DOI: 10.1542/peds.101.1.57

1998;101;57

Pediatrics

Joel Lutterman, Michael Scott, Ruth Nass and Tal Geva

Moyamoya Syndrome Associated With Congenital Heart Disease

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Figure

Fig 1. Selective cerebral angiograms in patient 5 before and after cerebral revascularization
TABLE.Patient Characteristics and Interventions

References

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