REVIEW ARTICLE

Neurosurgery

doi: 10.25005/2074-0581-2025-27-1-107-122
INTRACRANIAL HEMORRHAGE: EPIDEMIOLOGY, PREVENTION, ETIOLOGY, CLINICAL FEATURES AND PROGNOSIS

N.O. RAKHIMOV¹,², KH.D. RAKHMONOV¹,², D.R. SANGINOV¹, S.SH. BAKHODUROV², M.V. DAVLATOV¹

1Avicenna Tajik State Medical University, Dushanbe, Republic of Tajikistan
2National Medical Center of the Republic of Tajikistan "Shifobakhsh", Dushanbe, Republic of Tajikistan

The literature review explores various aspects of non-traumatic intracranial hemorrhages (NTIH), including epidemiology, prevention, etiological factors, and clinical features. The search for relevant literature was conducted using databases such as PubMed, Web of Science, Scopus, and eLibrary, covering the period from 2010 to 2023. A total of 1,100 sources were identified, and 68 articles were selected after analysis, reflecting the core topics of interest. The search utilized keywords such as "non-traumatic intracranial hemorrhage", "epidemiology", "prevention", "etiology", "prognostic factors", "outcome", and "clinical signs".

Keywords: Intracranial hemorrhage, epidemiology, prevention, etiology, prognostic factors, outcome, clinical signs.

Download file:


References
  1. Gusev EI, Konovalov AN, Skvortsova VI (red). Nevrologiya: natsional'noe rukovodstvo: v 2-kh t. 2-e izd., pererab. i dop. [Neurology: National Manual]. Moscow, RF: GEOTAR-Media; 2022. T. 1. 880 p.
  2. Grabovski A, Alekseenko YuV (red). Neotlozhnaya nevrologiya [Emergency neurology]. Moscow, RF: Izdatel'stvo Panfilova; 2016. 592 p.
  3. Gusev EI, Gekht AB, Martynov MYu. Mezhdunarodnyy kongress, posvyashchyonnyy Vsemirnomu Dnyu insul'ta. Materialy [International Congress dedicated to World Stroke Day]. Moscow, RF: OOO «Buki – Vedi»; 2017. 760 p.
  4. Frisoli FA. Spetzler-Martin grade III arteriovenous malformations: A comparison of modified and supplemented Spetzler-Martin grading systems. Neurosurgery. 2021;88(6):1103-10. https://doi.org/10.1093/neuros/nyab020
  5. Krylov VV. Dashyan VG, Danilov VA, Godkov IM. Khirurgicheskoe lechenie gipertenzivnykh vnutrimozgovykh gematom (klinicheskie rekomendatsii) [Surgical treatment of hypertensive intracerebral hematomas]. Nevrologicheskiy zhurnal. 2016;21(3):146-51. https://doi.org/10.18821/1560-2016-23-3-146-151
  6. Dashyan VG, Korshikova AN, Godkov IM, Krylov VV. Endoskopicheskaya khirurgiya gemorragicheskogo insul'ta [Endoscopic surgery for hemorrhagic stroke]. Zhurnal nevrologii i psikhiatrii im. S.S. Korsakova. Spetsvypuski. 2014;114(3- 2):7-13.
  7. Krylov VV, Dashyan, Levchenko OV, Prirodov AV, Godkov IM, Dmitriev Ayu, i dr. Novye tekhnologii v khirurgii netravmaticheskikh vnutricherepnykh krovoizliyaniy [New technologies in the surgery of non-traumatic intracranial hemorrhages]. Neotlozhnaya meditsinskaya pomoshch. 2013;3:48-54.
  8. Babi MA, James ML. Spontaneous intracerebral hemorrhage: Should we operate? Front Neurol. 2017;8:645. https://doi.org/10.3389/fneur.2017.00645
  9. Krylov VV. Dashyan VG, Shesterikov YaA, Sytnik AV, Godkov IM, i dr. Endoskopicheskaya khirurgiya gemorragicheskogo insul'ta v regional'nykh sosudistykh tsentrakh [Endoscopic surgery of hemorrhagic stroke in regional vascular centers]. Neyrokhirurgiya. 2019;21(1):35-44. https://doi.org/10.17650/1683- 3295-2019-21-1-35-44
  10. Krylov VV, Dash'yan VG, Godkov IM. Endoskopicheskaya khirurgiya gemorragicheskogo insul'ta [Endoscopic surgery of hemorrhagic stroke]. Moscow, RF: Binom; 2014. p. 24-5.
  11. Yarikov AV, Balyabin AV. Analiz prichin letal'nosti i prognosticheski neblagopriyatnykh faktorov operativnogo lecheniya gemorragicheskogo insul'ta [Analysis of the causes of mortality and prognostically unfavorable factors in the surgical treatment of hemorrhagic]. Medial'. 2015;3:148-51.
  12. Yarikov AV, Balyabin AV. Varianty khirurgicheskogo lecheniya gemorragicheskogo insul'ta v Nizhegorodskom neyrokhirurgicheskom tsentre [Options for surgical treatment of hemorrhagic stroke at the Nizhny Novgorod Neurosurgical Center]. Meditsinskiy al'manakh. 2015;4:139-42.
  13. Mendelow AD, Mendelow AD, Gregson BA, Rowan EN, Murray GD, et al. STICH II Investigators. Early surgery versus initial conservative treatment in patients with spontaneous supratentorial lobar intracerebral haematomas (STICH II) a randomised trial. Lancet. 2013;382(9890):397-408. https://doi.org/10.1016/ S0140-6736(13)60986-1
  14. Zhou XX, Chen J, Li Q, Ren G, Yao G, Liu M, et al. A minimally invasive surgery for spontaneous supratentorial intracerebral hemorrhage / meta-analysis of randomized controlled trials. Stroke. 2014;43(11):2923-30. https://doi. org/10.1161/STROKEAHA.112.667535
  15. Xu X, Zheng Y, Chen X. Comparison of endoscopic evacuation, stereotactic aspiration and craniotomy for the treatment of supratentorial hypertensive intracerebral haemorrhage study protocol for a randomised controlled trial. Trials. 2017;18(1):296.
  16. Gaab MR. Intracerebral hemorrhages from cerebral arteriovenous malformations: Prognostic grading. World Neurosurgery. 2016;93:471-3. https://doi.org/10.1016/j.wneu.2016.05.068
  17. Van Asch CJ, Luitse MJ, Rinkel GJ. Incidence, case fatality, and functional outcome of intracerebral haemorrhage over time, according to age, sex, and ethnic origin: A systematic review and meta-analysis. Lancet Neurology. 2010;9(2):167176. https://doi.org/10.1016/S1474-4422(09)70340-0
  18. Strahle J, Garton JL, Maher CO. Mechanisms of hydrocephalus after neonatal and adult intraventricular hemorrhage. Transl Stroke Res. 2012;3:25-38. https://doi.org/10.1007/s12975-012-0182-9
  19. Hanley DF, Lane K, Mc Bee N, Ziai W, Tuhrim S, et al. Thrombolytic removal of intraventricular hemorrhage in treatment of severe stroke: Results of the randomized, multicenter, multiregional, placebo-controlled CLEAR III trial. Lancet. 2017;389(10069):603-11. https://doi:10.1016/S0140-6736(16)32410-233
  20. Herrick DB, Ullman N, Nekoovaght-Tak S. Determinants of external ventricular drain placement and associated outcomes in patients with spontaneous intraventricular hemorrhage. Neurocrit Care. 2016;110-8. https://doi.org/10.1007/ s12028-014-9959-x
  21. Romero JM, Heit JJ, Delgado Almandoz JE. Spot sign score predicts rapid bleeding in spontaneous intracerebral hemorrhage. Emergency Radiology. 2012;19(3):195-202. https://doi.org/10.1007/s10140-012-1020-9
  22. Brown RD, Broderick JP. Unruptured intracranial aneurysms: Epidemiology, natural history, management options, and familial screening. Lancet Neurol. 2014;13(4):393-404. http://doi.org/10.1016/S1474-4422(14)70015-8
  23. Uricchio M, Gupta S, Jakowenko N, Levito M, Vu N, Doucette J, et al. Computed tomography angiography versus digital subtraction angiography for postclipping aneurysm obliteration detection. Stroke. 2019;50(2):381-8. https://doi. org/10.1161/STROKEAHA.118.023614/
  24. Brown MA, Parish J, Guandique CF, Payner TD, Horner T, Leipzig T, et al. A longterm study of durability and risk factors for aneurysm recurrence after microsurgical clip ligation. Journal of Neurosurgery. 2017;126(3):819-24. https://doi. org/10.3171/2016.2.JNS152059
  25. Thompson BG, Brown RD Jr, Amin-Hanjani S, Broderick JP, Cockroft KM, Connolly ES Jr, Duckwiler GR, Harris CC, Howard VJ, Johnston SC, Meyers PM, Molyneux A, Ogilvy CS, Ringer AJ, Torner J; American Heart Association Stroke Council, Council on Cardiovascular and Stroke Nursing, and Council on Epidemiology and Prevention; American Heart Association; American Stroke Association. Guidelines for the Management of Patients with Unruptured Intracranial Aneurysms: A Guideline for Healthcare Professionals from the American Heart Association/American Stroke Association. Guidelines for the Management of Patients with Unruptured Intracranial Aneurysms: A Guideline for Healthcare Professionals from the American Heart Association/American Stroke Association. Stroke. 2015;46(8):2368-400. https://doi.org/10.1161/ STR.0000000000000070
  26. Vlak MH, Rinkel GJ, Greebe P, van der Bom J, Algra A. Trigger factors for rupture of intracranial aneurysms in relation to patient and aneurysm characteristics. J Neurol. 2012;259(7):1298-1302. https://doi.org/10.1007/s00415-011-6341-1
  27. Hemphill JC 3rd, Greenberg SM, Anderson CS, Becker K, Bendok BR, Cushman M, Fung GL, Goldstein JN, Macdonald RL, Mitchell PH, Scott PA, Selim MH, Woo D; American Heart Association Stroke Council; Council on Cardiovascular and Stroke Nursing; Council on Clinical Cardiology. Guidelines for the Management of Spontaneous Intracerebral Hemorrhage: A Guideline for Healthcare Professionals from the American Heart Association/American Stroke Association. Stroke. 2015;46(7):2032-60. https://doi.org/10.1161/ STR.00000000000000069
  28. Steiner T, Al-Shahi Salman R, Beer R, Christensen H, Cordonnier C, Csiba L, Forsting M, Harnof S, Klijn CJ, Krieger D, Mendelow AD, Molina C, Montaner J, Overgaard K, Petersson J, Roine RO, Schmutzhard E, Schwerdtfeger K, Stapf C, Tatlisumak T, Thomas BM, Toni D, Unterberg A, Wagner M; European Stroke Organisation. European Stroke Organisation (ESO) guidelines for the management of spontaneous intracerebral hemorrhage. Int J Stroke. 2014;9(7):840-55. https://doi.org/10.1111/ijs.12309
  29. Gaab MR. Intracerebral hemorrhages from cerebral arteriovenous malformations: Prognostic grading. World Neurosurgery. 2016;93:471-3. https://doi. org/10.1016/j.wneu.2016.05.068
  30. Solomon RA, Connolly ES. Arteriovenous malformations of the Brain. N Engl J Med. 2017;376:1859-66. https://doi.org/10.1056/NEJMra1607407
  31. Kaplunova OA. Chaplygina EV, Dombrovskiy VI, Sukhanova OP, Blinov IM. Razvitie vnutrimozgovykh sosudov i arteriovenoznye mal'formatsii [Development of intracerebral vessels and arteriovenous malformations]. Zhurnal anatomii i gistopatologii. 2015;4(4):18-25. https://doi.org/10.18499/2225-7357-2015- 4-4-18-25
  32. Aoun SG, Bendok BR, Batjer HH. Acute management of ruptured arteriovenous malformations and dural arteriovenous fistulas. Neurosurgery Clinics. 2012;23(1):87-103. https://doi.org/10.1016/j.nec.2011.09.013
  33. Karbe AG, Vajkoczy P. Postoperative management and follow-up after resection of arteriovenous malformations. Journal of Neurosurgical Sciences. 2018;62(4):484-9. https://doi.org/10.23736/S0390-5616.18.04417-X
  34. Gabriel RA, Kim H, Sidney S, McCulloch CE, Singh V, Johnston SC, et al. Ten-year detection rate of brain arteriovenous malformations in a large, multiethnic, defined population. Stroke. 2010;41(1):21-6. https://doi.org/10.1161/STROKEAHA.109.566018
  35. Cho WS, Kim JE, Park SQ, Ko JK, Kim DW, Park JC, Yeon JY, Chung SY, Chung J, Joo SP, Hwang G, Kim DY, Chang WH, Choi KS, Lee SH, Sheen SH, Kang HS, Kim BM, Bae HJ, Oh CW, Park HS; Quality Control Committees from the Korean Society of Cerebrovascular Surgeons; Society of Korean Endovascular Neurosurgeons; Korean Society of Interventional Neuroradiology; Korean Stroke Society and Korean Academy of Rehabilitation Medicine. Korean Clinical Practice Guidelines for Aneurysmal Subarachnoid Hemorrhage. J Korean Neurosurg Soc. 2018;61(2):127-66. https://doi.org/10.3340/jkns.2017.0404.005
  36. Bor AS, Rinkel GJ, van Norden J, Wermer MJ. Long-term, serial screening for intracranial aneurysms in individuals with a family history of aneurysmal subarachnoid hemorrhage: A cohort study. Lancet Neurol. 2014;13:385-92. https://doi.org/10.1016/S1474-4422(14)70021-3
  37. Palm F, Henschke N, Wolf J, Zimmer K, Safer A, Schröder RJ, et al. Intracerebral haemorrhage in a population-based stroke registry (LuSSt): Incidence, aetiology, functional outcome and mortality. J Neurol. 2013;260:2541-50. https://doi. org/ 10.1007/s00415-013-7013-0
  38. Yamashiro S, Hitoshi Y, Yoshida A, Kuratsu J. Effectiveness of endoscopic surgery for comatose patients with large supratentorial intracerebral hemorrhages. Neurol Med Chir. 2015;55(2):810-23. https://doi.org/10.2176/nmc.oa.2014- 0136
  39. Golanov AV, Kostyuchenko VV. Neyroradiokhirurgiya na Gamma-nozhe [Neuoradiosurgery using Gamma]. Moscow, RF: Izdatel'stvo IP «T.A. Alekseeva»; 2018. 960 p.
  40. Graffeo CS. Stereotactic radiosurgery for Spetzler-Martin grade I and II arteriovenous malformations: International Society of Stereotactic Radiosurgery (ISRS) practice guideline. Neurosurgery. 2020;87(3):442-52. https://doi. org/10.1093/neuros/nyaa004
  41. Kimura Y, Mikami T, Miyata K, Suzuki H, Hirano T, Komatsu K, Mikuni N. Vascular assessment after clipping surgery using four-dimensional CT angiography. Neurosurgical Review. 2019;42(1):107-14. https://doi.org/10.1007/s10143- 018-0962-0
  42. Deng X. Comparison of language cortex reorganization patterns between cerebral arteriovenous malformations and gliomas: A functional MRI study. Journal of Neurosurgery. 2015;122(5):996-1003. https://doi.org/10.3171/2014.12. JNS14629
  43. Meshkova KS, Gudkova VV, Stakhovskaya LV. Zavisimost' razvitiya insul'ta ot arterial'noy gipertenzii i voprosy vybora antigipertenzivnoy terapii [Dependence of stroke development on arterial hypertension and issues of choice of antihypertensive therapy]. Farmateka. 2014;13:8-13. https://doi.org/10.26442/207 51753.2019.9.190626
  44. Krylov VV, Dashyan VG, Danilov VA, Godkov IM. Khirurgicheskoe lechenie gipertenzivnykh vnutrimozgovykh gematom (klinicheskiye rekomendatsii) [Surgical treatment of hypertensive intracerebral hematomas]. Nevrologicheskiy zhurnal. 2016;21(3):146-51. https://doi.org/10.18821/1560-9545-2016- 21-3-146-151
  45. Torné R, Rodríguez-Hernández A, Lawton MT. Intraoperative arteriovenous malformation rupture: Causes, management techniques, outcomes, and the effect of neurosurgeon experience. Neurosurgical Focus. 2014;37(3):E12. https://doi.org/10.3171/2014.6.FOCUS14218
  46. Graeb DA, Robertson WD, Lapointe JS, Nugent RA, Harrison PB. Computed tomographic diagnosis of intraventricular hemorrhage. Etiology and prognosis. Radiology. 1982;143(1):91-6. https://doi.org/10.1148/radiology.143.1.6977795
  47. Specogna AV, Turin TC, Patten SB, Hill MD. Factors associated with early deterioration after spontaneous intracerebral hemorrhage: A systematic review and meta-analysis. PLoS One. 2014;9(5):e96743. https://doi.org/10.1371/journal. pone.0096743
  48. Nishida T. Brain arteriovenous malformations associated with hereditary hemorrhagic telangiectasia: Gene – phenotype correlations. American Journal of Medical Genetics Part A. 2014;158(11):2829-34. https://doi.org/10.1002/ ajmg.a.35622
  49. Macmurdo CF, Teng С, Bernstein JM, Stevenson DA. RASA1 somatic mutation and variable expressivity in capillary malformation/arteriovenous malformation (CM/AVM) syndrome. Am J Med Genet. 2016;170:1450-4. https://doi. org/10.1002/ajmg.a.37613
  50. Morales-Valero SF, Carlo В, Carmelo S, Giuseppe L. Are parenchymal AVMs congenital lesions? Neurosurgical Focus. 2014;37(3):E2. https://doi. org/10.3171/2014.6.FOCUS14234
  51. de Oliveira Manoel AL. Surgery for spontaneous intracerebral hemorrhage. Crite Care. 2020;24(1):45. https://doi.org/10.1186/s13054-020-2749-2
  52. AlShardan MM, Mubasher M, Orz Y. Factors that predict hydrocephalus following intraventricular hemorrhage. Brit J Neurosurg. 2015;29(2):225-8. https:// doi.org/10.3109/02688697.2014.960365
  53. Saleh M. Brain arteriovenous malformations in patients with hereditary hemorrhagic telangiectasia: Clinical presentation and anatomical distribution. Pediatric Neurology. 2014;49(6):445-50. https://doi.org/10.1016/j.pediatrneurol.2013.07.021
  54. Moradiya Y, Murthy SB, Newman-Toker DE. Intraventricular thrombolysis in intracerebral hemorrhage requiring ventriculostomy: A decade-long real-world experience. Stroke. 2014;45(9):2629-35. https://doi.org/10.1161/STROKEAHA.114.006067
  55. Steiner TT, Steiner R, Al-S Salman, Beer R. European Stroke Organisation (ESO) guidelines for the management of spontaneous intracerebral hemorrhage. Int J Stroke. 2014;9(7):840-55. https://doi.org/ 10.1111/ijs.12309
  56. Xia, C, Cheng C, Li D. A new protocol to treat moderate to severe intraventricular hemorrhage with obstructive hydrocephalus. Neurol Res. 2014;36(11):955- 61. https://doi.org/10.1179/1743132814Y.0000000378
  57. Gao C, Du. H, Hua Y. Role of red blood cell lysis and iron in hydrocephalus after intraventricular hemorrhage. J Cerebr Blood F Met. 2014;34(6):1070-5. https:// doi.org/10.1038/jcbfm.2014.56
  58. del Zoppo GJ. Tissue plasminogen activator for acute ischemic stroke. The National Institute of Neurological Disorders and Stroke rt-PA Stroke Study Group. New Engl J Med. 1995;333(24):1581-7. https://doi.org/10.1056/ NEJM199512143332401
  59. Rutledge CW, Lawton MT. Basilar artery aneurysm: Role for open surgery. In: Veznedaroglu E, ed. Controversies in vascular neurosurgery. Cham: Springer International Publishing Switzerland; 2016. pp. 83-92.
  60. Bricout NL. Estrade L, Boustia F, Kalsoum E, Pruvo JP. Leclerc reduced-dose CT protocol for the assessment of cerebral vasospasm. Neuroradiology. 2015;5:1211-8. https://doi.org/10.1007/s00234-015-1585-6
  61. Yan Y, Zhu D, Tang H, Huang Q. Safety and efficacy of flow diverter treatment for aneurysm in small cerebral vessels: A systematic review and meta-analysis. World Neurosurg. 2018;115:54-64. https://doi.org/10.1016/j. wneu.2018.04.009
  62. Spetzler R F, Martin NA. A proposed grading system for arteriovenous malformations. Journal of Neurosurgery. 1986;65(4):476-83.
  63. Lawton MT; UCSF Brain Arteriovenous Malformation Study Project. Spetzler-Martin Grade III arteriovenous malformations: surgical results and a modification of the grading scale. Neurosurgery. 2003;52(4):740-8; discussion 748- 9. https://doi.org/10.1227/01.neu.0000053220.02268.9c
  64. Lawton MT, Kim H, McCulloch CE, Mikhak B, Young WL. A supplementary grading scale for selecting patients with brain arteriovenous malformations for surgery. Neurosurgery. 2010;66(4):702-13; discussion 713. https://doi. org/10.1227/01.NEU.0000367555.16733.E1
  65. Kim H, Abla AA, Nelson J, McCulloch CE, Bervini D, Morgan MK, et al. Validation of the supplemented Spetzler-Martin grading system for brain arteriovenous malformations in a multicenter cohort of 1009 surgical patients. Neurosurgery. 2015;76(1):25-31; discussion 31-2; quiz 32-3. https://doi.org/10.1227/ NEU.0000000000000556
  66. Beynon C, Schiebel P, Bösel J, Unterberg AW, Orakcioglu B. Minimally invasive endoscopic surgery for treatment of spontaneous intracerebral haematomas. Neurosurg Rev. 2015;38(3):421-8; discussion 428. https://doi.org/10.1007/ s10143-015-0606-6
  67. Orakcioglu B, Beynon C, Bösel J, Stock C, Unterberg AW. Minimally invasive endoscopic surgery for treatment of spontaneous intracerebral hematomas: a single-center analysis. Neurocrit Care. 2014;21(3):407-16. https://doi.org/ 10.1007/s12028-014-9987-6
  68. Spetzler RF, Kalani YS, Nakaji P. Neurovascular surgery. 2nd edition. NY, USA: Thieme Medical Publishers; 2015. 1238 р.

Authors' information:


Rakhimov Narzullo Odinaevich,
Candidate of Medical Sciences, Assistant of the Department of Neurosurgery and Polytrauma, Avicenna Tajik State Medical University; Neurosurgeon of the Department of Neurosurgery, National Medical Center of the Republic of Tajikistan “Shifobakhsh”
ORCID ID: 0000-0002-8471-1808
Е-mail: narzullorahimov91@gmail.com

Rakhmonov Khurshed Dzhamshedovich,
Doctor of Medical Sciences, Principal Researcher of the Department of Neurosurgery, National Medical Center of the Republic of Tajikistan “Shifobakhsh”; Associate Professor of the Department of Neurosurgery and Polytrauma, Avicenna Tajik State Medical University
ORCID ID: 0000-0002-6782-2979
Е-mail: doc-Rahmonov@mail.ru

Sanginov Dzhumaboy Rakhmatovich,
Doctor of Medical Sciences, Full Professor, Professor of the Department of Oncology and Diagnostic Imaging, Avicenna Tajik State Medical University
ORCID ID: 0000-0002-4804-1952
Е-mail: sanginov1952@gmail.ru

Bakhodurov Subkhoniddin Sharofiddinovich,
Neurosurgeon of the Department of Neurosurgery, National Medical Center of the Republic of Tajikistan “Shifobakhsh”
ORCID ID: 0000-0002-5501-19390
Е-mail: subhon-neuro@mail.ru

Davlatov Manuchekhr Valievich,
Candidate of Medical Sciences, Assistant of the Department of Neurosurgery and Polytrauma, Avicenna Tajik State Medical University
ORCID ID: 0000-0002-5504-19388
Е-mail: manuchehrd@mail.ru

Information about support in the form of grants, equipment, medications

The authors did not receive financial support from manufacturers of medi- cines and medical equipment

Conflicts of interest: No conflict

Address for correspondence:


Rakhimov Narzullo Odinaevich
Candidate of Medical Sciences, Assistant of the Department of Neurosurgery and Polytrauma, Avicenna Tajik State Medical University; Neurosurgeon of the Department of Neurosurgery, National Medical Center of the Republic of Tajikistan “Shifobakhsh”

734026, Republic of Tajikistan, Dushanbe, Sino str., 29-31

Tel.: +992 (918) 470304

Е-mail: narzullorahimov91@gmail.com


This work is licensed under a Creative Commons Attribution 4.0 International License.

Materials on the topic: