Semin Neurol 2024; 44(03): 298-307
DOI: 10.1055/s-0044-1787104
Review Article

Outcome Trajectories after Intracerebral Hemorrhage

Lourdes Carhuapoma
1   Division of Neurosciences Critical Care, The Johns Hopkins Hospital, Baltimore, Maryland
,
Santosh Murthy
2   Department of Neurology, Weil Cornell Medical College, New York
,
Vishank A. Shah
3   Division of Neurosciences Critical Care, Departments of Neurology, Anesthesiology and Critical Care Medicine, The Johns Hopkins University School of Medicine, Baltimore, Maryland
› Author Affiliations

Abstract

Spontaneous intracerebral hemorrhage (ICH) is the most morbid of all stroke types with a high early mortality and significant early disability burden. Traditionally, outcome assessments after ICH have mirrored those of acute ischemic stroke, with 3 months post-ICH being considered a standard time point in most clinical trials, observational studies, and clinical practice. At this time point, the majority of ICH survivors remain with moderate to severe functional disability. However, emerging data suggest that recovery after ICH occurs over a more protracted course and requires longer periods of follow-up, with more than 40% of ICH survivors with initial severe disability improving to partial or complete functional independence over 1 year. Multiple other domains of recovery impact ICH survivors including cognition, mood, and health-related quality of life, all of which remain under studied in ICH. To further complicate the picture, the most important driver of mortality after ICH is early withdrawal of life-sustaining therapies, before initiation of treatment and evaluating effects of prolonged supportive care, influenced by early pessimistic prognostication based on baseline severity factors and prognostication biases. Thus, our understanding of the true natural history of ICH recovery remains limited. This review summarizes the existing literature on outcome trajectories in functional and nonfunctional domains, describes limitations in current prognostication practices, and highlights areas of uncertainty that warrant further research.



Publication History

Article published online:
24 May 2024

© 2024. Thieme. All rights reserved.

Thieme Medical Publishers, Inc.
333 Seventh Avenue, 18th Floor, New York, NY 10001, USA

 
  • References

  • 1 Sheth KN. Spontaneous intracerebral hemorrhage. N Engl J Med 2022; 387 (17) 1589-1596
  • 2 van Asch CJ, Luitse MJ, Rinkel GJ, van der Tweel I, Algra A, Klijn CJ. 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 Neurol 2010; 9 (02) 167-176
  • 3 Qureshi AI, Giles WH, Croft JB. Racial differences in the incidence of intracerebral hemorrhage: effects of blood pressure and education. Neurology 1999; 52 (08) 1617-1621
  • 4 Kittner SJ, Sekar P, Comeau ME. et al. Ethnic and racial variation in intracerebral hemorrhage risk factors and risk factor burden. JAMA Netw Open 2021; 4 (08) e2121921
  • 5 Zahuranec DB, Brown DL, Lisabeth LD. et al. Early care limitations independently predict mortality after intracerebral hemorrhage. Neurology 2007; 68 (20) 1651-1657
  • 6 Øie LR, Madsbu MA, Solheim O. et al. Functional outcome and survival following spontaneous intracerebral hemorrhage: a retrospective population-based study. Brain Behav 2018; 8 (10) e01113
  • 7 Fernando SM, Qureshi D, Talarico R. et al. Intracerebral hemorrhage incidence, mortality, and association with oral anticoagulation use: a population study. Stroke (1970) 2021; 52 (05) 1673-1681
  • 8 Pinho J, Costa AS, Araújo JM, Amorim JM, Ferreira C. Intracerebral hemorrhage outcome: a comprehensive update. J Neurol Sci 2019; 398: 54-66
  • 9 Ayala C, Greenlund KJ, Croft JB. et al. Racial/ethnic disparities in mortality by stroke subtype in the United States, 1995-1998. Am J Epidemiol 2001; 154 (11) 1057-1063
  • 10 Su CM, Warren A, Kraus C. et al. Lack of racial and ethnic-based differences in acute care delivery in intracerebral hemorrhage. Int J Emerg Med 2021; 14 (01) 6
  • 11 Zurasky JA, Aiyagari V, Zazulia AR, Shackelford A, Diringer MN. Early mortality following spontaneous intracerebral hemorrhage. Neurology 2005; 64 (04) 725-727
  • 12 Hemphill III JC, Bonovich DC, Besmertis L, Manley GT, Johnston SC. The ICH score: a simple, reliable grading scale for intracerebral hemorrhage. Stroke (1970) 2001; 32 (04) 891-897
  • 13 Abulhasan YB, Teitelbaum J, Al-Ramadhani K, Morrison KT, Angle MR. Functional outcomes and mortality in patients with intracerebral hemorrhage after intensive medical and surgical support. Neurology 2023; 100 (19) e1985-e1995
  • 14 Becker KJ, Baxter AB, Cohen WA. et al. Withdrawal of support in intracerebral hemorrhage may lead to self-fulfilling prophecies. Neurology 2001; 56 (06) 766-772
  • 15 Shah VA, Radzik B, Weingart J, Suarez J, Rivera-Lara L. Remarkable recovery after a large thalamic-midbrain intracerebral and intraventricular hemorrhage. Neurol Clin Pract 2021; 11 (01) 85-87
  • 16 Melmed KR, Lewis A, Kuohn L. et al. Association of neighborhood socioeconomic status with withdrawal of life-sustaining therapies after intracerebral hemorrhage. Neurology 2024; 102 (03) e208039
  • 17 Fraser SM, Torres GL, Cai C, Choi HA, Sharrief A, Chang TR. Race is a predictor of withdrawal of life support in patients with intracerebral hemorrhage. J Stroke Cerebrovasc Dis 2018; 27 (11) 3108-3114
  • 18 Shah VA, Thompson RE, Yenokyan G. et al. One-year outcome trajectories and factors associated with functional recovery among survivors of intracerebral and intraventricular hemorrhage with initial severe disability. JAMA Neurol 2022; 79 (09) 856-868
  • 19 Carlsson M, Wilsgaard T, Johnsen SH. et al. Long-term survival, causes of death, and trends in 5-year mortality after intracerebral hemorrhage: the TROMSØ study. Stroke (1970) 2021; 52 (12) 3883-3890
  • 20 Kuohn LR, Leasure AC, Acosta JN. et al. Cause of death in spontaneous intracerebral hemorrhage survivors: multistate longitudinal study. Neurology 2020; 95 (20) e2736-e2745
  • 21 Anderson CS, Heeley E, Huang Y. et al; INTERACT2 Investigators. Rapid blood-pressure lowering in patients with acute intracerebral hemorrhage. N Engl J Med 2013; 368 (25) 2355-2365
  • 22 Qureshi AI, Palesch YY, Barsan WG. et al; ATACH-2 Trial Investigators and the Neurological Emergency Treatment Trials Network. Intensive blood-pressure lowering in patients with acute cerebral hemorrhage. N Engl J Med 2016; 375 (11) 1033-1043
  • 23 Mayer SA, Brun NC, Begtrup K. et al; FAST Trial Investigators. Efficacy and safety of recombinant activated factor VII for acute intracerebral hemorrhage. N Engl J Med 2008; 358 (20) 2127-2137
  • 24 Sreekrishnan A, Leasure AC, Shi FD. et al. Functional improvement among intracerebral hemorrhage (ICH) survivors up to 12 months post-injury. Neurocrit Care 2017; 27 (03) 326-333
  • 25 Rost NS, Smith EE, Chang Y. et al. Prediction of functional outcome in patients with primary intracerebral hemorrhage: the FUNC score. Stroke 2008; 39 (08) 2304-2309
  • 26 Weimar C, Benemann J, Diener HC. German Stroke Study Collaboration. Development and validation of the Essen intracerebral haemorrhage score. J Neurol Neurosurg Psychiatry 2006; 77 (05) 601-605
  • 27 Gregório T, Pipa S, Cavaleiro P. et al. Prognostic models for intracerebral hemorrhage: systematic review and meta-analysis. BMC Med Res Methodol 2018; 18 (01) 145
  • 28 Jakobsson J, Redebrandt HN, Tobieson L. et al. Long-term functional outcome and quality of life after surgical evacuation of spontaneous supratentorial intracerebral hemorrhage: results from a Swedish nationwide cohort. World Neurosurg 2023; 170: e351-e363
  • 29 Greenberg SM, Ziai WC, Cordonnier C. et al; American Heart Association/American Stroke Association. 2022 guideline for the management of patients with spontaneous intracerebral hemorrhage: a guideline from the American Heart Association/American Stroke Association. Stroke (1970) 2022; 53 (07) e282-e361
  • 30 Potter T, Lioutas VA, Tano M. et al. Cognitive impairment after intracerebral hemorrhage: a systematic review of current evidence and knowledge gaps. Front Neurol 2021; 12: 716632
  • 31 Banerjee G, Summers M, Chan E. et al. Domain-specific characterisation of early cognitive impairment following spontaneous intracerebral haemorrhage. J Neurol Sci 2018; 391: 25-30
  • 32 Gong L, Gu Y, Yu Q. et al. Prognostic factors for cognitive recovery beyond early poststroke cognitive impairment (PSCI): a prospective cohort study of spontaneous intracerebral hemorrhage. Front Neurol 2020; 11: 278
  • 33 You S, Wang X, Lindley RI. et al. Early cognitive impairment after intracerebral hemorrhage in the INTERACT1 study. Cerebrovasc Dis 2017; 44 (5-6): 320-324
  • 34 Griauzde J, Lisabeth LD, Li C. et al. A population-based study of intracerebral hemorrhage survivors' outcomes. J Stroke Cerebrovasc Dis 2019; 28 (01) 49-55
  • 35 Garcia PY, Roussel M, Bugnicourt JM. et al. Cognitive impairment and dementia after intracerebral hemorrhage: a cross-sectional study of a hospital-based series. J Stroke Cerebrovasc Dis 2013; 22 (01) 80-86
  • 36 Biffi A, Bailey D, Anderson CD. et al. Risk factors associated with early vs delayed dementia after intracerebral hemorrhage. JAMA Neurol 2016; 73 (08) 969-976
  • 37 Keins S, Abramson JR, Castello JP. et al. Latent profile analysis of cognitive decline and depressive symptoms after intracerebral hemorrhage. BMC Neurol 2021; 21 (01) 481
  • 38 Kokubo K, Suzuki K, Hattori N, Miyai I, Mori E. Executive dysfunction in patients with putaminal hemorrhage. J Stroke Cerebrovasc Dis 2015; 24 (09) 1978-1985
  • 39 Skidmore ER, Eskes G, Brodtmann A. Executive function poststroke: concepts, recovery, and interventions. Stroke (1970) 2023; 54 (01) 20-29
  • 40 Bosma MS, Nijboer TCW, Caljouw MAA, Achterberg WP. Impact of visuospatial neglect post-stroke on daily activities, participation and informal caregiver burden: a systematic review. Ann Phys Rehabil Med 2020; 63 (04) 344-358
  • 41 Zeng YY, Cheng HR, Cheng L. et al. Comparison of poststroke depression between acute ischemic and hemorrhagic stroke patients. Int J Geriatr Psychiatry 2021; 36 (04) 493-499
  • 42 Avadhani R, Thompson RE, Carhuapoma L. et al. Post-stroke depression in patients with large spontaneous intracerebral hemorrhage. J Stroke Cerebrovasc Dis 2021; 30 (11) 106082
  • 43 Christensen MC, Mayer SA, Ferran JM, Kissela B. Depressed mood after intracerebral hemorrhage: the FAST trial. Cerebrovasc Dis 2009; 27 (04) 353-360
  • 44 Stern-Nezer S, Eyngorn I, Mlynash M. et al. Depression one year after hemorrhagic stroke is associated with late worsening of outcomes. NeuroRehabilitation 2017; 41 (01) 179-187
  • 45 Sallinen H, Sairanen T, Strbian D. Quality of life and depression 3 months after intracerebral hemorrhage. Brain Behav 2019; 9 (05) e01270
  • 46 Koivunen RJ, Harno H, Tatlisumak T, Putaala J. Depression, anxiety, and cognitive functioning after intracerebral hemorrhage. Acta Neurol Scand 2015; 132 (03) 179-184
  • 47 Scopelliti G, Casolla B, Boulouis G. et al. Long-term anxiety in spontaneous intracerebral hemorrhage survivors. Int J Stroke 2022; 17 (10) 1093-1099
  • 48 Francis BA, Beaumont J, Maas MB. et al. Depressive symptom prevalence after intracerebral hemorrhage: a multi-center study. J Patient Rep Outcomes 2018; 2 (01) 55
  • 49 Karamchandani RR, Vahidy F, Bajgur S. et al. Early depression screening is feasible in hospitalized stroke patients. PLoS One 2015; 10 (06) e0128246
  • 50 Syed MJ, Farooq S, Siddiqui S, Awan S, Wasay M. Depression and the use of selective serotonin reuptake inhibitors in patients with acute intracerebral hemorrhage. Cureus 2019; 11 (10) e5975
  • 51 Kubiszewski P, Sugita L, Kourkoulis C. et al. Association of selective serotonin reuptake inhibitor use after intracerebral hemorrhage with hemorrhage recurrence and depression severity. JAMA Neurol 2020; 78 (01) 1-8
  • 52 U.S. Department of Health and Human Services FDA Center for Drug Evaluation and Research, U.S. Department of Health and Human Services FDA Center for Biologics Evaluation and Research, U.S. Department of Health and Human Services FDA Center for Devices and Radiological Health. Guidance for industry: patient-reported outcome measures: use in medical product development to support labeling claims: draft guidance. Health Qual Life Outcomes 2006; 4 (01) 79
  • 53 Tengs TO, Yu M, Luistro E. Health-related quality of life after stroke a comprehensive review. Stroke 2001; 32 (04) 964-972
  • 54 Lin C, Martin K, Arevalo YA, Harvey RL, Prabhakaran S. Association of proportional recovery after stroke with health-related quality of life. Stroke (1970) 2021; 52 (09) 2968-2971
  • 55 Rimmele DL, Lebherz L, Frese M. et al. Health-related quality of life 90 days after stroke assessed by the International Consortium for Health Outcome Measurement standard set. Eur J Neurol 2020; 27 (12) 2508-2516
  • 56 Christensen MC, Mayer S, Ferran JM. Quality of life after intracerebral hemorrhage: results of the Factor Seven for Acute Hemorrhagic Stroke (FAST) trial. Stroke 2009; 40 (05) 1677-1682
  • 57 Delcourt C, Zheng D, Chen X. et al; INTERACT Investigators. Associations with health-related quality of life after intracerebral haemorrhage: pooled analysis of INTERACT studies. J Neurol Neurosurg Psychiatry 2017; 88 (01) 70-75
  • 58 Slaughter KB, Meyer EG, Bambhroliya AB. et al. Direct assessment of health utilities using the standard gamble among patients with primary intracerebral hemorrhage. Circ Cardiovasc Qual Outcomes 2019; 12 (09) e005606
  • 59 Arnold D, Girling A, Stevens A, Lilford R. Comparison of direct and indirect methods of estimating health state utilities for resource allocation: review and empirical analysis. BMJ 2009; 339 (7717) 385-388
  • 60 Dorman PJ, Waddell F, Slattery J, Dennis M, Sandercock P. Are proxy assessments of health status after stroke with the EuroQoL questionnaire feasible, accurate, and unbiased?. Stroke 1997; 28 (10) 1883-1887
  • 61 Pickard AS, Johnson JA, Feeny DH, Shuaib A, Carriere KC, Nasser AM. Agreement between patient and proxy assessments of health-related quality of life after stroke using the EQ-5D and Health Utilities Index. Stroke 2004; 35 (02) 607-612
  • 62 Satopää J, Mustanoja S, Meretoja A. et al. Comparison of all 19 published prognostic scores for intracerebral hemorrhage. J Neurol Sci 2017; 379: 103-108
  • 63 Hwang DY, Kim KS, Muehlschlegel S. et al. Guidelines for neuroprognostication in critically ill adults with intracerebral hemorrhage. Neurocrit Care 2024; 40 (02) 395-414
  • 64 Dowlatshahi D, Demchuk AM, Flaherty ML, Ali M, Lyden PL, Smith EE. VISTA Collaboration. Defining hematoma expansion in intracerebral hemorrhage: relationship with patient outcomes. Neurology 2011; 76 (14) 1238-1244
  • 65 Roh DJ, Asonye IS, Carvalho Poyraz F. et al. Intraventricular hemorrhage expansion in the CLEAR III trial: a post hoc exploratory analysis. Stroke 2022; 53 (06) 1847-1853
  • 66 Bhattathiri PS, Gregson B, Prasad KS, Mendelow AD. STICH Investigators. Intraventricular hemorrhage and hydrocephalus after spontaneous intracerebral hemorrhage: results from the STICH trial. Acta Neurochir Suppl (Wien) 2006; 96: 65-68
  • 67 Ziai WC, Siddiqui AA, Ullman N. et al. Early therapy intensity level (TIL) predicts mortality in spontaneous intracerebral hemorrhage. Neurocrit Care 2015; 23 (02) 188-197
  • 68 Hwang DY, Chu SY, Dell CA. et al. Factors considered by clinicians when prognosticating intracerebral hemorrhage outcomes. Neurocrit Care 2017; 27 (03) 316-325
  • 69 Gilbert DT, Wilson TD. Prospection: experiencing the future. Science 2007; 317 (5843) 1351-1354
  • 70 Wilson TD, Gilbert DT. Affective forecasting: knowing what to want. Current Directions in Psychological Science: A Journal of the American Psychological Society 2005; 14 (03) 131-134
  • 71 Bamford JM, Sandercock PA, Warlow CP, Slattery J. Interobserver agreement for the assessment of handicap in stroke patients. Stroke (1970) 1989; 20 (06) 828
  • 72 Mahoney FI, Barthel DW. Functional evaluation: the Barthel Index. Md State Med J 1965; 14: 61-65
  • 73 Folstein MF, Folstein SE, McHugh PR. “Mini-mental state”. A practical method for grading the cognitive state of patients for the clinician. J Psychiatr Res 1975; 12 (03) 189-198
  • 74 Nasreddine ZS, Phillips NA, Bédirian V. et al. The Montreal Cognitive Assessment, MoCA: a brief screening tool for mild cognitive impairment. J Am Geriatr Soc 2005; 53 (04) 695-699
  • 75 Jaywant A, Toglia J, Gunning FM, O'Dell MW. The clinical utility of a 30-minute neuropsychological assessment battery in inpatient stroke rehabilitation. J Neurol Sci 2018; 390: 54-62
  • 76 Hamilton M. A rating scale for depression. J Neurol Neurosurg Psychiatry 1960; 23 (01) 56-62
  • 77 Hamilton M. Assessment of change in psychiatric state by means of rating scales. Proc R Soc Med 1966; 59 Suppl 1(suppl): 10-13
  • 78 Hamilton M. Development of a rating scale for primary depressive illness. Br J Soc Clin Psychol 1967; 6 (04) 278-296
  • 79 Hamilton M. Standardised assessment and recording of depressive symptoms. Psychiatr Neurol Neurochir 1969; 72 (02) 201-205
  • 80 Hamilton M. Rating depressive patients. J Clin Psychiatry 1980; 41 (12, Pt 2): 21-24
  • 81 Radloff LS. The CES-D Scale: a self-report depression scale for research in the general population. Applied Psychological Measurement 1977; 1 (03) 385-401
  • 82 Attema AE, Edelaar-Peeters Y, Versteegh MM, Stolk EA. Time trade-off: one methodology, different methods. Eur J Health Econ 2013; 14 Suppl 1 (Suppl. 01) S53-S64
  • 83 Lugnér AK, Krabbe PFM. An overview of the time trade-off method: concept, foundation, and the evaluation of distorting factors in putting a value on health. Expert Rev Pharmacoecon Outcomes Res 2020; 20 (04) 331-342
  • 84 Oppe M, Rand-Hendriksen K, Shah K, Ramos-Goñi JM, Luo N. EuroQol protocols for time trade-off valuation of health outcomes. PharmacoEconomics 2016; 34 (10) 993-1004
  • 85 Gafni A. The standard gamble method: what is being measured and how it is interpreted. Health Serv Res 1994; 29 (02) 207-224
  • 86 van Osch SMC, Stiggelbout AM. The construction of standard gamble utilities. Health Econ 2008; 17 (01) 31-40