Skip to main content

Advertisement

Log in

Ischaemic stroke after acute intracranial haemorrhage in patients with moyamoya disease: six new cases and a short literature review

  • Clinical Article
  • Published:
Acta Neurochirurgica Aims and scope Submit manuscript

Abstract

Background

We report six new cases of ischaemic stroke after cerebral haemorrhage in patients with moyamoya disease (MMD) and analyse their clinical and radiological characteristics, together with cases reported in the literature, to deduce the mechanism of cerebral infarct.

Methods

Six (2%) of 246 patients with MMD who were admitted to our hospitals between 1993 and 2009 suffered cerebral infarct after intracranial haemorrhage. Ten patients identified in the literature with the PubMed search engine were also included in this study. All the ischaemic lesions in these 16 patients were analysed according to their location, size, and number and were compared according to the spatial relationship between the haemorrhage and infarct, as follows: (1) anterior vs posterior involvement, (2) cortical vs subcortical involvement, (3) watershed vs non-watershed infarct, (4) small vs large infarct, (5) single vs multiple infarct, and (6) adjacent vs distant involvement.

Results

Acute synchronous multiple brain infarcts occurred in six (38%) patients and recurrent infarcts in three patients (19%). Cerebral infarcts had mainly cortical (72%), anterior (66%), and distant involvement (75%) and were large (69%) and non-watershed (66%). Adjacent infarct had significantly anterior involvement (P < 0.05), and distant infarcts tended to have cortical involvement. Non-watershed infarcts had significantly cortical involvement (P < 0.05). Watershed infarcts tended to be large. Vasospasm was confirmed either pathologically or angiographically in two patients with large cerebral infarcts.

Conclusions

We suggest that thromboembolism or vasospasm plays a crucial role in the pathogenesis of cerebral infarction after acute intracranial haemorrhage in patients with MMD.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  1. Adams HP Jr, Bendixen BH, Kappelle LJ, Biller J, Love BB, Gordon DL, Marsh EE 3rd (1993) Classification of subtype of acute ischemic stroke. Definitions for use in a multicenter clinical trial. TOAST. Trial of org 10172 in acute stroke treatment. Stroke 24:35–41

    PubMed  Google Scholar 

  2. Baird AE, Lovblad KO, Schlaug G, Edelman RR, Warach S (2000) Multiple acute stroke syndrome: marker of embolic disease? Neurology 54:674–678

    PubMed  CAS  Google Scholar 

  3. Bruno A, Yuh WT, Biller J, Adams HP Jr, Cornell SH (1988) Magnetic resonance imaging in young adults with cerebral infarction due to moyamoya. Arch Neurol 45:303–306

    PubMed  CAS  Google Scholar 

  4. Faraci FM, Heistad DD (1998) Regulation of the cerebral circulation: role of endothelium and potassium channels. Physiol Rev 78:53–97

    PubMed  CAS  Google Scholar 

  5. 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(2):S238–S240

    PubMed  Google Scholar 

  6. Hijdra A, Van Gijn J, Stefanko S, Van Dongen KJ, Vermeulen M, Van Crevel H (1986) Delayed cerebral ischemia after aneurysmal subarachnoid hemorrhage: clinicoanatomic correlations. Neurology 36:329–333

    PubMed  CAS  Google Scholar 

  7. Horn P, Bueltmann E, Buch CV, Schmiedek P (2005) Arterio-embolic ischemic stroke in children with moyamoya disease. Childs Nerv Syst 21:104–107

    Article  PubMed  Google Scholar 

  8. Iwama T, Kotani Y, Yamakawa H, Nagata I, Hashimoto N, Sakai N (2001) Cerebral ischemic complications following intracranial bleeding in patients with moyamoya disease–three case reports. Neurol Med chir 41:450–453

    Article  CAS  Google Scholar 

  9. Karnchanapandh K (2008) Effect of increased intracranial pressure on cerebral vasospasm in SAH. Acta Neurochir Suppl 102:307–310

    Article  PubMed  Google Scholar 

  10. Kim JM, Lee SH, Roh JK (2009) Changing ischaemic lesion patterns in adult moyamoya disease. J Neurol Neurosurg Psychiatry 80:36–40

    Article  PubMed  Google Scholar 

  11. Kivisaari RP, Salonen O, Servo A, Autti T, Hernesniemi J, Ohman J (2001) MR imaging after aneurysmal subarachnoid hemorrhage and surgery: a long-term follow-up study. AJNR Am J Neuroradiol 22:1143–1148

    PubMed  CAS  Google Scholar 

  12. Kobayashi M, Takayama H, Mihara B, Kawase T (2002) Severe vasospasm caused by repeated intraventricular haemorrhage from small arteriovenous malformation. Acta Neurochir (Wien) 144:405–406

    Article  CAS  Google Scholar 

  13. Kolominsky-Rabas PL, Weber M, Gefeller O, Neundoerfer B, Heuschmann PU (2001) Epidemiology of ischemic stroke subtypes according to TOAST criteria: incidence, recurrence, and long-term survival in ischemic stroke subtypes: a population-based study. Stroke 32:2735–2740

    Article  PubMed  CAS  Google Scholar 

  14. Kothbauer K, Schroth G, Seiler RW, Do DD (1995) Severe symptomatic vasospasm after rupture of an arteriovenous malformation. AJNR Am J Neuroradiol 16:1073–1075

    PubMed  CAS  Google Scholar 

  15. Maeda K, Kurita H, Nakamura T, Usui M, Tsutsumi K, Morimoto T, Kirino T (1997) Occurrence of severe vasospasm following intraventricular hemorrhage from an arteriovenous malformation. Report of two cases. J Neurosurg 87:436–439

    Article  PubMed  CAS  Google Scholar 

  16. Mugikura S, Takahashi S, Higano S, Shirane R, Kurihara N, Furuta S, Ezura M, Takahashi A (1999) The relationship between cerebral infarction and angiographic characteristics in childhood moyamoya disease. AJNR Am J Neuroradiol 20:336–343

    PubMed  CAS  Google Scholar 

  17. Nagasaka T, Hayashi S, Naito T, Okamoto T, Ikeda H, Inao S (2007) Concomitant cerebral infarction and intraventricular hemorrhage in moyamoya disease. Case report. J Neurosurg 106:388–390

    Article  PubMed  Google Scholar 

  18. Nakai Y, Hyodo A, Yanaka K, Nose T (2002) Fatal cerebral infarction after intraventricular hemorrhage in a pregnant patient with moyamoya disease. J Clin Neurosci 9:456–458

    Article  PubMed  Google Scholar 

  19. Rabinstein AA, Weigand S, Atkinson JL, Wijdicks EF (2005) Patterns of cerebral infarction in aneurysmal subarachnoid hemorrhage. Stroke 36:992–997

    Article  PubMed  Google Scholar 

  20. Rafay MF, Smith SE, Dirks P, Armstrong D, deVeber GA (2006) Hemorrhage predisposing to cerebral infarction in children with moyamoya disease. Pediatr Neurol 34:400–404

    Article  PubMed  Google Scholar 

  21. Roh JK, Kang DW, Lee SH, Yoon BW, Chang KH (2000) Significance of acute multiple brain infarction on diffusion-weighted imaging. Stroke 31:688–694

    PubMed  CAS  Google Scholar 

  22. Rovira A, Grive E, Alvarez-Sabin J (2005) Distribution territories and causative mechanisms of ischemic stroke. Eur Radiol 15:416–426

    Article  PubMed  CAS  Google Scholar 

  23. Shimoda M, Takeuchi M, Tominaga J, Oda S, Kumasaka A, Tsugane R (2001) Asymptomatic versus symptomatic infarcts from vasospasm in patients with subarachnoid hemorrhage: serial magnetic resonance imaging. Neurosurgery 49:1341–1348, Discussion 1348–1350

    Article  PubMed  CAS  Google Scholar 

  24. Su IC, Yang CC, Wang WH, Lee JE, Tu YK, Wang KC (2008) Acute cerebral ischemia following intraventricular hemorrhage in moyamoya disease: early perfusion computed tomography findings. J Neurosurg 109:1049–1051

    Article  PubMed  Google Scholar 

  25. Suyama K, Yoshida K, Takahata H, Toda K, Baba H, Ishikawa Y, Hirose M, Nagata I (2008) Pediatric moyamoya disease presenting with intracerebral hemorrhage—report of three cases and review of the literature. Clin Neurol Neurosurg 110:270–275

    Article  PubMed  Google Scholar 

  26. Suzuki J, Takaku A (1969) Cerebrovascular "moyamoya" disease. Disease showing abnormal net-like vessels in base of brain. Arch Neurol 20:288–299

    PubMed  CAS  Google Scholar 

  27. Vergouwen MD, Vermeulen M, Coert BA, Stroes ES, Roos YB (2008) Microthrombosis after aneurysmal subarachnoid hemorrhage: an additional explanation for delayed cerebral ischemia. J Cerb Blood Metab 28:1761–1770

    Article  Google Scholar 

  28. Wang X, Lam WW, Fan YH, Graham CA, Rainer TH, Wong KS (2006) Topographic patterns of small subcortical infarcts associated with MCA stenosis: a diffusion-weighted MRI study. J Neuroimaging 16:266–271

    Article  PubMed  Google Scholar 

  29. Yanaka K, Hyodo A, Tsuchida Y, Yoshii Y, Nose T (1992) Symptomatic cerebral vasospasm after intraventricular hemorrhage from ruptured arteriovenous malformation. Surg Neurol 38:63–67

    Article  PubMed  CAS  Google Scholar 

Download references

Conflicts of interest

None.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Dong-Kyu Jang.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Kim, DS., Jang, DK., Huh, PW. et al. Ischaemic stroke after acute intracranial haemorrhage in patients with moyamoya disease: six new cases and a short literature review. Acta Neurochir 153, 1253–1261 (2011). https://doi.org/10.1007/s00701-010-0926-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00701-010-0926-9

Keywords

Navigation