Advertisement

European Radiology

, Volume 26, Issue 8, pp 2853–2862 | Cite as

Early-onset stroke with moyamoya-like syndrome and extraneurological signs: a first reported paediatric series

  • Bruno Law-ye
  • Guillaume Saliou
  • Frédérique Toulgoat
  • Marc Tardieu
  • Kumaran Deiva
  • Catherine AdamsbaumEmail author
  • Béatrice Husson
Paediatric

Abstract

Background

Moyamoya syndrome is characterised by an occlusion of the carotid terminations with the development of collateral vessels. Our objective is to describe a series of infants presenting early-onset moyamoya-like syndrome, which may constitute a distinct entity.

Methods

From a cohort of children with rare cerebral vascular pathologies, we studied eight infants (28 days–1 year) with early-onset moyamoya-like syndrome demonstrated by angiography. We retrospectively analysed the patterns on MRI and MRA, as well as all other available data.

Results

Median age at diagnosis was 7 months (IQR: 6–8) with arterial ischaemic stroke in the middle cerebral artery territory. All of the children experienced severe stroke recurrence within a median time of 11 months (IQR: 10–12), and all showed extraneurological symptoms. The anterior cerebral circulation was involved in all cases and the posterior circulation was involved in six. Two children died and all of the other children suffered permanent neurological deficits.

Conclusions

The presence of extraneurological signs in cases of early-onset moyamoya syndrome is suggestive of a newly described systemic vasculopathy with predominantly cerebrovascular expression. Given its rapid progression marked by severe recurrent strokes and poor clinical outcome, early diagnosis could help in the decision to institute aggressive therapy.

Keywords

Moyamoya syndrome Ischaemic stroke Digital subtraction angiography MRI MRA 

Abbreviations

ACA

Cerebral anterior artery

MCA

Middle cerebral artery

PCA

Posterior cerebral artery

ICA

Internal carotid artery

DSA

Digital subtraction angiography

MMS

Moyamoya syndrome

MMD

Moyamoya disease

MRA

Magnetic resonance angiography

mRS

Modified Rankin Scale

Notes

Acknowledgments

The scientific guarantor of this publication is Catherine Adamsbaum. The authors of this manuscript declare no relationships with any companies, whose products or services may be related to the subject matter of the article. The authors state that this work has not received any funding. No complex statistical methods were necessary for this paper. Institutional Review Board approval was not required in accordance with French and European ethical guidelines (standard care). Written informed consent was not required for this study because this was a non-interventional retrospective study. Methodology: retrospective, observational, multicentre study.

References

  1. 1.
    Fukui M (1997) Guidelines for the diagnosis and treatment of spontaneous occlusion of the circle of Willis (’moyamoya’ disease). Research Committee on Spontaneous Occlusion of the Circle of Willis (Moyamoya Disease) of the Ministry of Health and Welfare, Japan. Clin Neurol Neurosurg 99:S238–S240CrossRefPubMedGoogle Scholar
  2. 2.
    Fukui M, Kono S, Sueishi K, Ikezaki K (2000) Moyamoya disease. Neuropathol Off J Jpn Soc Neuropathol 20:S61–S64CrossRefGoogle Scholar
  3. 3.
    Kataoka H, Miyamoto S, Nagata I, Hatano T, Kano H, Hashimoto N (1999) Moyamoya disease showing atypical angiographic findings—two case reports. Neurol Med Chir (Tokyo) 39:294–298CrossRefGoogle Scholar
  4. 4.
    Guey S, Tournier-Lasserve E, Hervé D, Kossorotoff M (2015) Moyamoya disease and syndromes: from genetics to clinical management. Appl Clin Genet 8:49–68PubMedPubMedCentralGoogle Scholar
  5. 5.
    Horn P, Pfister S, Bueltmann E, Vajkoczy P, Schmiedek P (2004) Moyamoya-like vasculopathy (moyamoya syndrome) in children. Childs Nerv Syst ChNS Off J Int Soc Pediatr Neurosurg 20:382–391CrossRefGoogle Scholar
  6. 6.
    Sasaki T, Nogawa S, Amano T (2006) Co-morbidity of moyamoya disease with Graves’ disease. report of three cases and a review of the literature. Intern Med Tokyo Jpn 45:649–653CrossRefGoogle Scholar
  7. 7.
    Tokimura H, Tajitsu K, Takashima H, Hirayama T, Tsuchiya M, Takayama K et al (2010) Familial moyamoya disease associated with Graves’ disease in a mother and daughter. Two case reports. Neurol Med Chir (Tokyo) 50:668–674CrossRefGoogle Scholar
  8. 8.
    Houkin K, Yoshimoto T, Kuroda S, Ishikawa T, Takahashi A, Abe H (1996) Angiographic analysis of moyamoya disease--how does moyamoya disease progress? Neurol Med Chir (Tokyo) 36:783–787, discussion 788CrossRefGoogle Scholar
  9. 9.
    Amlie-Lefond C, Zaidat OO, Lew SM (2011) Moyamoya disease in early infancy: case report and literature review. Pediatr Neurol 44:299–302CrossRefPubMedGoogle Scholar
  10. 10.
    Harrison JK, McArthur KS, Quinn TJ (2013) Assessment scales in stroke: clinimetric and clinical considerations. Clin Interv Aging 8:201–211PubMedPubMedCentralGoogle Scholar
  11. 11.
    Nassaf M, Draiss G, Rada N, Bourrous M, Bouskraoui M (2012) Moyamoya disease in children: a case report. Arch Pédiatrie Organe Off Sociéte Fr Pédiatrie 19:493–496CrossRefGoogle Scholar
  12. 12.
    Ahmed R, Ahsan H (1997) Imaging of Moya Moya disease. JPMA J Pak Med Assoc 47:181–185PubMedGoogle Scholar
  13. 13.
    Manceau E, Giroud M, Dumas R (1997) Moyamoya disease in children. A review of the clinical and radiological features and current treatment. Childs Nerv Syst ChNS Off J Int Soc Pediatr Neurosurg 13:595–600CrossRefGoogle Scholar
  14. 14.
    Funaki T, Takahashi JC, Takagi Y, Yoshida K, Araki Y, Kikuchi T et al (2013) Impact of posterior cerebral artery involvement on long-term clinical and social outcome of pediatric moyamoya disease. J Neurosurg Pediatr 12:626–632CrossRefPubMedGoogle Scholar
  15. 15.
    Kuroda S, Ishikawa T, Houkin K, Iwasaki Y (2002) Clinical significance of posterior cerebral artery stenosis/occlusion in moyamoya disease. No Shinkei Geka 30:1295–1300PubMedGoogle Scholar
  16. 16.
    Miyamoto S, Kikuchi H, Karasawa J, Nagata I, Ikota T, Takeuchi S (1984) Study of the posterior circulation in moyamoya disease. Clinical and neuroradiological evaluation. J Neurosurg 61:1032–1037CrossRefPubMedGoogle Scholar
  17. 17.
    Tamogami R, Oi S, Nonaka Y, Miwa T, Abe T (2010) Clinical prognosis and therapeutic aspects in management of pediatric moyamoya disease. Nihon Rinsho Jpn J Clin Med 68:45–52Google Scholar
  18. 18.
    Currie S, Raghavan A, Batty R, Connolly DJA, Griffiths PD (2011) Childhood moyamoya disease and moyamoya syndrome: a pictorial review. Pediatr Neurol 44:401–413CrossRefPubMedGoogle Scholar
  19. 19.
    Kamada F, Aoki Y, Narisawa A, Abe Y, Komatsuzaki S, Kikuchi A et al (2011) A genome-wide association study identifies RNF213 as the first Moyamoya disease gene. J Hum Genet 56:34–40CrossRefPubMedGoogle Scholar
  20. 20.
    Liu W, Morito D, Takashima S, Mineharu Y, Kobayashi H, Hitomi T et al (2011) Identification of RNF213 as a susceptibility gene for moyamoya disease and its possible role in vascular development. PLoS One 6, e22542CrossRefPubMedPubMedCentralGoogle Scholar
  21. 21.
    Wu Z, Jiang H, Zhang L, Xu X, Zhang X, Kang Z et al (2012) Molecular analysis of RNF213 gene for moyamoya disease in the Chinese Han population. PLoS One 7, e48179CrossRefPubMedPubMedCentralGoogle Scholar
  22. 22.
    Miyatake S, Miyake N, Touho H, Nishimura-Tadaki A, Kondo Y, Okada I et al (2012) Homozygous c.14576G > A variant of RNF213 predicts early-onset and severe form of moyamoya disease. Neurology 78:803–810CrossRefPubMedGoogle Scholar
  23. 23.
    Mineharu Y, Takagi Y, Takahashi JC, Hashikata H, Liu W, Hitomi T et al (2013) Rapid progression of unilateral moyamoya disease in a patient with a family history and an RNF213 risk variant. Cerebrovasc Dis Basel Switz 36:155–157CrossRefGoogle Scholar
  24. 24.
    Morito D, Nishikawa K, Hoseki J, Kitamura A, Kotani Y, Kiso K et al (2014) Moyamoya disease-associated protein mysterin/RNF213 is a novel AAA+ ATPase, which dynamically changes its oligomeric state. Sci Rep 4:4442CrossRefPubMedPubMedCentralGoogle Scholar
  25. 25.
    Buerki S, Steinlin M (2013) Coexistent childhood renovascular and cerebrovascular disease. Dev Med Child Neurol 55:297–298CrossRefPubMedGoogle Scholar
  26. 26.
    Willsher A, Roebuck DJ, Ng J, Ganesan V (2013) How commonly do children with complex cerebral arteriopathy have renovascular disease? Dev Med Child Neurol 55:335–340CrossRefPubMedGoogle Scholar
  27. 27.
    Richard MA, Grob JJ, Durand JM, Noë C, Basseres N, Bonerandi JJ (1994) Sneddon syndrome. Ann Dermatol Vénéréologie 121:331–337Google Scholar
  28. 28.
    Scott IA, Boyle RS (1986) Sneddon’s syndrome. Aust N Z J Med 16:799–802CrossRefPubMedGoogle Scholar
  29. 29.
    Legierse CM, Canninga-Van Dijk MR, Bruijnzeel-Koomen CAFM, Kuck-Koot VCM (2008) Sneddon syndrome and the diagnostic value of skin biopsies - three young patients with intracerebral lesions and livedo racemosa. Eur J Dermatol EJD 18:322–328PubMedGoogle Scholar
  30. 30.
    Zaccariotti VA, Martins LF, da Costa V, Silva NA, da Casas AA, de Melo-Souza SE (1995) Sneddon syndrome. Report of 3 cases. Arq Neuropsiquiatr 53:82–87CrossRefPubMedGoogle Scholar
  31. 31.
    Maamar M, Rahmani M, Aidi S, Benabdeljlil M, El Hassani My R, Jiddane M et al (2007) Sneddon’s syndrome: 15 cases with cerebral angiography. Rev Neurol (Paris) 163:809–816CrossRefGoogle Scholar
  32. 32.
    Provenzale JM, Barboriak DP, Allen NB, Ortel TL (1998) Antiphospholipid antibodies: findings at arteriography. AJNR Am J Neuroradiol 19:611–616PubMedGoogle Scholar
  33. 33.
    Pomper MG, Miller TJ, Stone JH, Tidmore WC, Hellmann DB (1999) CNS vasculitis in autoimmune disease: MR imaging findings and correlation with angiography. AJNR Am J Neuroradiol 20:75–85PubMedGoogle Scholar
  34. 34.
    Zhou Q, Yang D, Ombrello AK, Zavialov AV, Toro C, Zavialov AV et al (2014) Early-onset stroke and vasculopathy associated with mutations in ADA2. N Engl J Med 370:911–920CrossRefPubMedPubMedCentralGoogle Scholar
  35. 35.
    Kotagal S, Peterson PL, Martens ME, Lee CP, Nigro M, Archer CR (1988) Impaired NADH-CoQ reductase activity in a child with moyamoya syndrome. Pediatr Neurol 4:241–244CrossRefPubMedGoogle Scholar
  36. 36.
    Cullu N, Karakas E, Karakas O, Deveer M, Calik M, Boyaci FN (2013) Childhood moyamoya disease accompanying Leigh syndrome. JPMA J Pak Med Assoc 63:1538–1540PubMedGoogle Scholar
  37. 37.
    Marcinkevicius E, Liutkus D, Gvazdaitis A (2006) Experience of treatment of moyamoya disease at the Clinic of Neurosurgery of Kaunas University of Medicine. Med Kaunas Lith 42:130–136Google Scholar
  38. 38.
    Kim S-K, Seol HJ, Cho B-K, Hwang Y-S, Lee DS, Wang K-C (2004) Moyamoya disease among young patients: its aggressive clinical course and the role of active surgical treatment. Neurosurgery 54:840–844, discussion 844–846CrossRefPubMedGoogle Scholar
  39. 39.
    Imaizumi T, Hayashi K, Saito K, Osawa M, Fukuyama Y (1998) Long-term outcomes of pediatric moyamoya disease monitored to adulthood. Pediatr Neurol 18:321–325CrossRefPubMedGoogle Scholar
  40. 40.
    Jackson EM, Lin N, Manjila S, Scott RM, Smith ER (2014) Pial synangiosis in patients with moyamoya younger than 2 years of age. J Neurosurg Pediatr 13:420–425CrossRefPubMedGoogle Scholar

Copyright information

© European Society of Radiology 2015

Authors and Affiliations

  • Bruno Law-ye
    • 1
  • Guillaume Saliou
    • 2
    • 3
    • 4
  • Frédérique Toulgoat
    • 5
  • Marc Tardieu
    • 6
    • 7
  • Kumaran Deiva
    • 7
  • Catherine Adamsbaum
    • 1
    • 6
    • 8
    Email author
  • Béatrice Husson
    • 1
    • 4
  1. 1.Pediatric Radiology DepartmentAP-HP, Bicêtre HospitalLe Kremlin Bicêtre CedexFrance
  2. 2.Neuroradiology DepartmentAP-HP, Bicêtre HospitalLe Kremlin Bicêtre CedexFrance
  3. 3.National Referral Center for Neurovascular Malformation in ChildrenAP-HP, Bicêtre HospitalLe Kremlin Bicêtre CedexFrance
  4. 4.French Center for Paediatric StrokeAP-HP, Bicêtre HospitalLe Kremlin Bicêtre CedexFrance
  5. 5.CHU Nantes, Nord Laennec Hospital, Diagnostic and Interventional NeuroradiologyNantes Cedex 1France
  6. 6.Faculty of MedicineParis Sud UniversityLe Kremlin Bicêtre CedexFrance
  7. 7.Neuropediatry DepartmentAP-HP, Bicêtre HospitalLe Kremlin Bicêtre CedexFrance
  8. 8.LTCI, CNRS, Télécom ParisTech, Université Paris-SaclayParisFrance

Personalised recommendations