Log in

Single and simultaneous multiple intracerebral hemorrhages: a radiological review

  • Review article
  • Published:
Acta Neurologica Belgica Aims and scope Submit manuscript

Abstract

Simultaneous multiple intracerebral hemorrhage (SMICH) is defined as ICH in two or more discrete noncontiguous acute intraparenchymal locations on initial CT. About 5% of ICH patients present with SMICH. ICH/SMICH etiology is classically divided into disorders of primary or secondary origin. About half of primary SMICH cases are caused by cerebral amyloid angiopathy or hypertensive arteriopathy. In this review, we will discuss the radiological features associated with the different causes of primary and secondary ICH and SMICH. Due to its rarity and the associated high morbidity and mortality, we will focus in particular on SMICH.

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

Access this article

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  1. Wu TY, Yassi N, Shah DG et al (2017) Simultaneous Multiple Intracerebral Hemorrhages (SMICH). Stroke 48:581–586

    PubMed  Google Scholar 

  2. Stemer A, Ouyang B, Lee VH et al (2010) Prevalence and risk factors for multiple simultaneous intracerebral hemorrhages. Cerebrovasc Dis 30:302–307

    PubMed  Google Scholar 

  3. Laiwattana D, Sangsawang B, Sangsawang N (2014) Primary Multiple Simultaneous Intracerebral Hemorrhages between 1950 and 2013: analysis of Data on Age, Sex and Outcome. Cerebrovasc Dis Extra 4:102–114

    PubMed  PubMed Central  Google Scholar 

  4. Seo JS, Nam TK, Kwon JT et al (2014) Multiple spontaneous simultaneous intracerebral hemorrhages. J Cerebrovasc Endovasc Neurosurg 16:104–111

    PubMed  PubMed Central  Google Scholar 

  5. Chen Y, Hénon H, Bombois S et al (2016) Multiple simultaneous spontaneous intracerebral hemorrhages: a rare entity. Cerebrovasc Dis 41:74–79

    PubMed  Google Scholar 

  6. Yamaguchi Y, Takeda R, Kikkawa Y et al (2017) Multiple simultaneous intracerebral hemorrhages: clinical presentations and risk factors. J Neurol Sci 383:35–38

    PubMed  Google Scholar 

  7. Meretoja A, Strbian D, Putaala J et al (2012) SMASH-U: a proposal for etiologic classification of intracerebral hemorrhage. Stroke 43:2592–2597

    PubMed  Google Scholar 

  8. Yeh SJ, Tang SC, Tsai LK et al (2014) Pathogenetical subtypes of recurrent intracerebral hemorrhage: designations by SMASH-U classification system. Stroke 45:2636–2642

    PubMed  Google Scholar 

  9. Kumral E, Polat F, Uzunköprü C et al (2012) The clinical spectrum of intracerebral hematoma, hemorrhagic infarct, non-hemorrhagic infarct, and non-lesional venous stroke in patients with cerebral sinus-venous thrombosis. Eur J Neurol 19:537–543

    CAS  PubMed  Google Scholar 

  10. Zhou G, Li M, Zhu Y et al (2016) Cerebral venous sinus thrombosis involving the straight sinus may result in infarction and/or hemorrhage. Eur Neurol 75:257–262

    PubMed  Google Scholar 

  11. Louis N, Marsh R (2016) Simultaneous and sequential hemorrhage of multiple cerebral cavernous malformations: a case report. J Med Case Rep 10:36

    PubMed  PubMed Central  Google Scholar 

  12. Havakeshian S, Bozinov O, Burkhardt JK (2013) Simultaneous rupture of two middle cerebral artery aneurysms presented with two aneurysm-associated intracerebral hemorrhages. J Neurol Surg A Cent Eur Neurosurg 74(Suppl 1):e233–e236

    PubMed  Google Scholar 

  13. Rogers LR (2008) Handbook of neuro-oncology neuroimaging. Academic Press, New York, pp 72–73

    Google Scholar 

  14. Zwicker JI, Karp Leaf R, Carrier M (2016) A meta-analysis of intracranial hemorrhage in patients with brain tumors receiving therapeutic anticoagulation. J Thromb Haemost 14:1736–1740

    CAS  PubMed  Google Scholar 

  15. Franceschi AM, Moschos SJ, Anders CK et al (2016) Use of susceptibility-weighted imaging (SWI) in the detection of brain hemorrhagic metastases from breast cancer and melanoma. J Comput Assist Tomogr 40:803–805

    PubMed  PubMed Central  Google Scholar 

  16. Yang L, Chen CJ, Guo XL et al (2018) Bevacizumab and risk of intracranial hemorrhage in patients with brain metastases: a meta-analysis. J Neurooncol 137:49–56

    CAS  PubMed  Google Scholar 

  17. Silver B, Behrouz R, Silliman S (2016) Bacterial endocarditis and cerebrovascular disease. Curr Neurol Neurosci Rep 16:104

    PubMed  Google Scholar 

  18. Asaithambi G, Adil MM, Qureshi AI (2013) Thrombolysis for ischemic stroke associated with infective endocarditis: results from the nationwide inpatient sample. Stroke 44:2917–2919

    PubMed  Google Scholar 

  19. Mader I, Wolff M, Niemann G et al (2004) Acute haemorrhagic encephalomyelitis (AHEM): MRI findings. Neuropediatrics 35:143–146

    CAS  PubMed  Google Scholar 

  20. Zhang J, Yang Y, Sun H et al (2014) Hemorrhagic transformation after cerebral infarction: current concepts and challenges. Ann Transl Med 2:81

    PubMed  PubMed Central  Google Scholar 

  21. Kalinin MN, Khasanova DR, Ibatullin MM (2017) The hemorrhagic transformation index score: a prediction tool in middle cerebral artery ischemic stroke. BMC Neurol 17:177

    PubMed  PubMed Central  Google Scholar 

  22. Kato E, Tahara K, Hayashi H et al (2018) Granulomatosis with polyangiitis complicated by hypertrophic pachymeningitis presenting with simultaneous multiple intracerebral hemorrhages. Intern Med 57:1167–1172

    PubMed  Google Scholar 

  23. Yu J, Yuan Y, Li W et al (2016) Moyamoya disease manifested as multiple simultaneous intracerebral hemorrhages: a case report and literature review. Exp Ther Med 12:1440–1444

    PubMed  PubMed Central  Google Scholar 

  24. Pfleger MJ, Hardee EP, Contant CF Jr et al (1994) Sensitivity and specificity of fluid-blood levels for coagulopathy in acute intracerebral hematomas. AJNR Am J Neuroradiol 15:217–223

    CAS  PubMed  Google Scholar 

  25. Prats-Sánchez L, Camps-Renom P, Sotoca-Fernández J, Catalan Stroke Code and Reperfusion Consortium (Cat-SCR) et al (2016) Remote intracerebral hemorrhage after intravenous thrombolysis: results from a multicenter study. Stroke 47:2003–2009

    PubMed  Google Scholar 

  26. Braemswig TB, Villringer K, Turc G et al (2019) Predictors of new remote cerebral microbleeds after IV thrombolysis for ischemic stroke. Neurology 92:e630–e638

    PubMed  Google Scholar 

  27. Prats-Sanchez L, Martínez-Domeño A, Camps-Renom P et al (2017) Risk factors are different for deep and lobar remote hemorrhages after intravenous thrombolysis. PLoS One 12:e0178284

    PubMed  PubMed Central  Google Scholar 

  28. Linn J, Halpin A, Demaerel P et al (2010) Prevalence of superficial siderosis in patients with cerebral amyloid angiopathy. Neurology 74:1346–1350

    CAS  PubMed  PubMed Central  Google Scholar 

  29. Charidimou A, Boulouis G, **ong L et al (2017) Cortical superficial siderosis and first-ever cerebral hemorrhage in cerebral amyloid angiopathy. Neurology 88:1607–1614

    PubMed  PubMed Central  Google Scholar 

  30. Charidimou A, Imaizumi T, Moulin S et al (2017) Brain hemorrhage recurrence, small vessel disease type, and cerebral microbleeds: a meta-analysis. Neurology 89:820–829

    PubMed  PubMed Central  Google Scholar 

  31. Charidimou A, Boulouis G, Roongpiboonsopit D et al (2017) Cortical superficial siderosis multifocality in cerebral amyloid angiopathy: a prospective study. Neurology 89:2128–2135

    PubMed  PubMed Central  Google Scholar 

  32. Quinones-Hinojosa A, Gulati M, Singh V et al (2003) Spontaneous intracerebral hemorrhage due to coagulation disorders. Neurosurg Focus 15:E3

    PubMed  Google Scholar 

  33. Zhang Q, Li X, Wei Z et al (2017) Risk factors and clinical characteristics of non-promyelocytic acute myeloid leukemia of intracerebral hemorrhage: a single center study in China. J Clin Neurosci 44:203–206

    PubMed  Google Scholar 

  34. Owattanapanich W, Auewarakul CU (2016) Intracranial hemorrhage in patients with hematologic disorders: prevalence and predictive factors. J Med Assoc Thai 99:15–24

    PubMed  Google Scholar 

  35. Roininen S, Laine O, Kauppila M et al (2017) A minor role of asparaginase in predisposing to cerebral venous thromboses in adult acute lymphoblastic leukemia patients. Cancer Med 6:1275–1285

    CAS  PubMed  PubMed Central  Google Scholar 

  36. Kumar NS, Neeraja V, Raju CG et al (2015) Multiple spontaneous hypertensive intracerebral hemorrhages. J Stroke Cerebrovasc Dis 24:e25–e27

    PubMed  Google Scholar 

  37. Takeuchi S, Takasato Y, Masaoka H et al (2011) Simultaneous multiple hypertensive intracranial hemorrhages. J Clin Neurosci 18:1215–1218

    PubMed  Google Scholar 

  38. Pozzi M, Roccatagliata D, Sterzi R (2008) Drug abuse and intracranial hemorrhage. Neurol Sci 29(Suppl 2):S269–S270

    PubMed  Google Scholar 

  39. Fonseca AC, Ferro JM (2016) Drug abuse and stroke. Curr Neurol Neurosci Rep. 13:325

    Google Scholar 

  40. Sturiale CL, Rossetto M, Ermani M et al (2016) Remote cerebellar hemorrhage after supratentorial procedures (part 1): a systematic review. Neurosurg Rev 39:565–573

    PubMed  Google Scholar 

  41. Sturiale CL, Rossetto M, Ermani M et al (2016) Remote cerebellar hemorrhage after spinal procedures (part 2): a systematic review. Neurosurg Rev 39:369–376

    PubMed  Google Scholar 

  42. You SH, Son KR, Lee NJ et al (2012) Remote cerebral and cerebellar hemorrhage after massive cerebrospinal fluid leakage. J Korean Neurosurg Soc 51:240–243

    PubMed  PubMed Central  Google Scholar 

  43. Garcha M, Sivakumar K, El-Hunjul M et al (2018) Intracranial hemorrhage in the setting of posterior reversible encephalopathy syndrome: two case reports and a review. Hosp Pract 46:103–109

    Google Scholar 

  44. Babi MA, Gorman MJ, Cipolla MJ et al (2016) Ondansetron-related hemorrhagic posterior reversible encephalopathy syndrome (PRES) following gastric bypass. Springerplus 5:18

    PubMed  PubMed Central  Google Scholar 

  45. Martin RM, Wright MJ, Lutkenhoff ES et al (2017) Traumatic hemorrhagic brain injury: impact of location and resorption on cognitive outcome. J Neurosurg 126:796–804

    PubMed  Google Scholar 

Download references

Acknowledgements

We would like to thank Dr. Sarah Kabani (Service de Biostatistique, Epidémiologie Clinique, Santé Publique et Innovation en Méthodologie (BESPIM), CHU de Nîmes, 4 Rue du Professeur Debré, 30029 Nîmes Cedex 09) for proofreading our manuscript.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Dimitri Renard.

Ethics declarations

Conflict of interest

We have no conflict of interest to declare.

Ethical statement

The subject has given her informed consent to report data given. The manuscript was approved by the institute’s committee on human research.

Additional information

Publisher's Note

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

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Renard, D., Castelnovo, G., Ion, I. et al. Single and simultaneous multiple intracerebral hemorrhages: a radiological review. Acta Neurol Belg 120, 819–829 (2020). https://doi.org/10.1007/s13760-020-01385-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13760-020-01385-4

Keywords

Navigation