Time course of recovery following poor-grade SAH: the incidence of delayed improvement and implications for SAH outcome study design

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  • Division of Neurological Surgery, Barrow Neurological Institute, St. Joseph's Hospital and Medical Center, Phoenix, Arizona
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Object

Data regarding the time course of recovery after poor-grade subarachnoid hemorrhage (SAH) is lacking. Most SAH studies assess outcome at a single time point, often as early as 3 or 6 months following SAH. The authors hypothesized that recovery following poor-grade SAH is a dynamic process and that early outcomes may not always approximate long-term outcomes. To test this hypothesis, they analyzed long-term outcome data from a cohort of patients with poor-grade aneurysmal SAH to determine the incidence and predictors of early and delayed neurological improvement.

Methods

The authors reviewed outcome data from 88 poor-grade SAH patients enrolled in a prospective SAH treatment trial (the Barrow Ruptured Aneurysm Trial). They assessed modified Rankin Scale (mRS) scores at discharge, 6 months, 12 months, and 36 months after treatment to determine the incidence and predictors of neurological improvement during each interval.

Results

The mean aggregate mRS scores at 6 months (3.31 ± 2.1), 12 months (3.28 ± 2.2), and 36 months (3.17 ± 2.3) improved significantly compared with the mean score at hospital discharge (4.33 ± 1.3, p < 0.001), but they did not differ significantly among themselves. Between discharge and 6 months, 61% of patients improved on the mRS. The incidence of improvement between 6–12 months and 12–36 months was 18% and 19%, respectively. Hunt and Hess Grade IV versus V (OR 6.20, 95% CI 2.11–18.25, p < 0.001) and the absence of large (> 4 cm) (OR 2.76, 95% CI 1.02–7.55, p = 0.05) or eloquent (OR 5.17, 95% CI 1.89–14.10, p < 0.01) stroke were associated with improvement up to 6 months. Age ≤ 65 years (OR 5.56, 95% CI 1.17–26.42, p = 0.02), Hunt and Hess Grade IV versus V (OR 4.17, 95% CI 1.10–15.85, p = 0.03), and absence of a large (OR 8.97, 95% CI 2.65–30.40, p < 0.001) or eloquent (OR 4.54, 95% CI 1.46–14.08, p = 0.01) stroke were associated with improvement beyond 6 months. Improvement beyond 1 year was most strongly predicted by the absence of a large stroke (OR 7.62, 95% CI 1.55–37.30, p < 0.01).

Conclusions

A substantial minority of poor-grade SAH patients will experience delayed recovery beyond the point at which most studies assess outcome. Younger patients, those presenting in better clinical condition, and those without CT evidence of large or eloquent stroke demonstrated the highest capacity for delayed recovery.

Abbreviations used in this paper:BRAT = Barrow Ruptured Aneurysm Trial; mRS = modified Rankin Scale; SAH = subarachnoid hemorrhage.

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Contributor Notes

Address correspondence to: Robert F. Spetzler, M.D., Neuroscience Publications, Barrow Neurological Institute, St. Joseph's Hospital and Medical Center, 350 West Thomas Road, Phoenix, Arizona 85013. email: neuropub@dignityhealth.org.

Please include this information when citing this paper: published online May 31, 2013; DOI: 10.3171/2013.4.JNS121287.

  • 1

    Bach y Rita P: Central nervous system lesions: sprouting and unmasking in rehabilitation. Arch Phys Med Rehabil 62:413417, 1981

  • 2

    Chiang VL, , Claus EB, & Awad IA: Toward more rational prediction of outcome in patients with high-grade subarachnoid hemorrhage. Neurosurgery 46:2836, 2000

    • Search Google Scholar
    • Export Citation
  • 3

    Dimyan MA, & Cohen LG: Neuroplasticity in the context of motor rehabilitation after stroke. Nat Rev Neurol 7:7685, 2011

  • 4

    Duke BJ, , Kindt GW, & Breeze RE: Outcome after urgent surgery for grade IV subarachnoid hemorrhage. Surg Neurol 50:169173, 1998

  • 5

    Greebe P, , Rinkel GJ, & Algra A: Long-term outcome of patients discharged to a nursing home after aneurysmal subarachnoid hemorrhage. Arch Phys Med Rehabil 91:247251, 2010

    • Search Google Scholar
    • Export Citation
  • 6

    Greebe P, , Rinkel GJ, , Hop JW, , Visser-Meily JM, & Algra A: Functional outcome and quality of life 5 and 12.5 years after aneurysmal subarachnoid haemorrhage. J Neurol 257:20592064, 2010

    • Search Google Scholar
    • Export Citation
  • 7

    Haley EC Jr, , Kassell NF, & Torner JC: The International Cooperative Study on the Timing of Aneurysm Surgery. The North American experience. Stroke 23:205214, 1992

    • Search Google Scholar
    • Export Citation
  • 8

    Haug T, , Sorteberg A, , Sorteberg W, , Lindegaard KF, , Lundar T, & Finset A: Cognitive outcome after aneurysmal subarachnoid hemorrhage: time course of recovery and relationship to clinical, radiological, and management parameters. Neurosurgery 60:649657, 2007

    • Search Google Scholar
    • Export Citation
  • 9

    Hutchinson PJ, , Power DM, , Tripathi P, & Kirkpatrick PJ: Outcome from poor grade aneurysmal subarachnoid haemorrhage—which poor grade subarachnoid haemorrhage patients benefit from aneurysm clipping?. Br J Neurosurg 14:105109, 2000

    • Search Google Scholar
    • Export Citation
  • 10

    Hütter BO, , Kreitschmann-Andermahr I, & Gilsbach JM: Healthrelated quality of life after aneurysmal subarachnoid hemorrhage: impacts of bleeding severity, computerized tomography findings, surgery, vasospasm, and neurological grade. J Neurosurg 94:241251, 2001

    • Search Google Scholar
    • Export Citation
  • 11

    Hütter BO, , Kreitschmann-Andermahr I, , Mayfrank L, , Rohde V, , Spetzger U, & Gilsbach JM: Functional outcome after aneurysmal subarachnoid hemorrhage. Acta Neurochir Suppl 72:157174, 1999

    • Search Google Scholar
    • Export Citation
  • 12

    Kassell NF, , Torner JC, , Haley EC Jr, , Jane JA, , Adams HP, & Kongable GL: The International Cooperative Study on the Timing of Aneurysm Surgery. Part 1: Overall management results. J Neurosurg 73:1836, 1990

    • Search Google Scholar
    • Export Citation
  • 13

    Laidlaw JD, & Siu KH: Poor-grade aneurysmal subarachnoid hemorrhage: outcome after treatment with urgent surgery. Neurosurgery 53:12751282, 2003

    • Search Google Scholar
    • Export Citation
  • 14

    Lanzino G, , Kassell NF, , Germanson TP, , Kongable GL, , Truskowski LL, & Torner JC, : Age and outcome after aneurysmal subarachnoid hemorrhage: why do older patients fare worse?. J Neurosurg 85:410418, 1996

    • Search Google Scholar
    • Export Citation
  • 15

    Le Roux PD, , Elliott JP, , Newell DW, , Grady MS, & Winn HR: Predicting outcome in poor-grade patients with subarachnoid hemorrhage: a retrospective review of 159 aggressively managed cases. J Neurosurg 85:3949, 1996

    • Search Google Scholar
    • Export Citation
  • 16

    Leung CH, , Poon WS, , Yu LM, , Wong GK, & Ng HK: Apolipoprotein E genotype and outcome in aneurysmal subarachnoid hemorrhage. Stroke 33:548552, 2002

    • Search Google Scholar
    • Export Citation
  • 17

    Longstreth WT Jr, , Nelson LM, , Koepsell TD, & van Belle G: Clinical course of spontaneous subarachnoid hemorrhage: a population-based study in King County, Washington. Neurology 43:712718, 1993

    • Search Google Scholar
    • Export Citation
  • 18

    Macdonald RL, , Hunsche E, , Schüler R, , Wlodarczyk J, & Mayer SA: Quality of life and healthcare resource use associated with angiographic vasospasm after aneurysmal subarachnoid hemorrhage. Stroke 43:10821088, 2012

    • Search Google Scholar
    • Export Citation
  • 19

    McDougall CG, , Spetzler RF, , Zabramski JM, , Partovi S, , Hills NK, & Nakaji P, : The Barrow Ruptured Aneurysm Trial. Clinical article. J Neurosurg 116:135144, 2012

    • Search Google Scholar
    • Export Citation
  • 20

    Mocco J, , Ransom ER, , Komotar RJ, , Schmidt JM, , Sciacca RR, & Mayer SA, : Preoperative prediction of long-term outcome in poor-grade aneurysmal subarachnoid hemorrhage. Neurosurgery 59:529538, 2006

    • Search Google Scholar
    • Export Citation
  • 21

    Mocco J, , Ransom ER, , Komotar RJ, , Sergot PB, , Ostapkovich N, & Schmidt JM, : Long-term domain-specific improvement following poor grade aneurysmal subarachnoid hemorrhage. J Neurol 253:12781284, 2006

    • Search Google Scholar
    • Export Citation
  • 22

    Naidech AM, , Bendok BR, , Bassin SL, , Bernstein RA, , Batjer HH, & Bleck TP: Classification of cerebral infarction after subarachnoid hemorrhage impacts outcome. Neurosurgery 64:10521058, 2009

    • Search Google Scholar
    • Export Citation
  • 23

    Niskakangas T, , Ohman J, , Niemelä M, , Ilveskoski E, , Kunnas TA, & Karhunen PJ: Association of apolipoprotein E polymorphism with outcome after aneurysmal subarachnoid hemorrhage: a preliminary study. Stroke 32:11811184, 2001

    • Search Google Scholar
    • Export Citation
  • 24

    Ogilvy CS, & Carter BS: A proposed comprehensive grading system to predict outcome for surgical management of intracranial aneurysms. Neurosurgery 42:959970, 1998

    • Search Google Scholar
    • Export Citation
  • 25

    O'Sullivan MG, , Sellar R, , Statham PF, & Whittle IR: Management of poor grade patients after subarachnoid haemorrhage: the importance of neuroradiological findings on clinical outcome. Br J Neurosurg 10:445452, 1996

    • Search Google Scholar
    • Export Citation
  • 26

    Pearl JD, & Macdonald RL: Vasospasm after aneurysmal subarachnoid hemorrhage: need for further study. Acta Neurochir Suppl 105:207210, 2008

    • Search Google Scholar
    • Export Citation
  • 27

    Quinn TJ, , Dawson J, , Walters MR, & Lees KR: Reliability of the modified Rankin Scale: a systematic review. Stroke 40:33933395, 2009

  • 28

    Rabinstein AA, , Friedman JA, , Weigand SD, , McClelland RL, , Fulgham JR, & Manno EM, : Predictors of cerebral infarction in aneurysmal subarachnoid hemorrhage. Stroke 35:18621866, 2004

    • Search Google Scholar
    • Export Citation
  • 29

    Roos YB, , de Haan RJ, , Beenen LF, , Groen RJ, , Albrecht KW, & Vermeulen M: Complications and outcome in patients with aneurysmal subarachnoid haemorrhage: a prospective hospital based cohort study in the Netherlands. J Neurol Neurosurg Psychiatry 68:337341, 2000

    • Search Google Scholar
    • Export Citation
  • 30

    Rosen DS, & Macdonald RL: Grading of subarachnoid hemorrhage: modification of the World Federation of Neurosurgical Societies scale on the basis of data for a large series of patients. Neurosurgery 54:566576, 2004

    • Search Google Scholar
    • Export Citation
  • 31

    Rosengart AJ, , Schultheiss KE, , Tolentino J, & Macdonald RL: Prognostic factors for outcome in patients with aneurysmal subarachnoid hemorrhage. Stroke 38:23152321, 2007

    • Search Google Scholar
    • Export Citation
  • 32

    Sbordone RJ, , Liter JC, & Pettler-Jennings P: Recovery of function following severe traumatic brain injury: a retrospective 10-year follow-up. Brain Inj 9:285299, 1995

    • Search Google Scholar
    • Export Citation
  • 33

    Schievink WI, , Wijdicks EF, , Piepgras DG, , Chu CP, , O'Fallon WM, & Whisnant JP: The poor prognosis of ruptured intracranial aneurysms of the posterior circulation. J Neurosurg 82:791795, 1995

    • Search Google Scholar
    • Export Citation
  • 34

    Schmidt JM, , Ko SB, , Helbok R, , Kurtz P, , Stuart RM, & Presciutti M, : Cerebral perfusion pressure thresholds for brain tissue hypoxia and metabolic crisis after poor-grade subarachnoid hemorrhage. Stroke 42:13511356, 2011

    • Search Google Scholar
    • Export Citation
  • 35

    Siman R, , Giovannone N, , Toraskar N, , Frangos S, , Stein SC, & Levine JM, : Evidence that a panel of neurodegeneration biomarkers predicts vasospasm, infarction, and outcome in aneurysmal subarachnoid hemorrhage. PLoS ONE 6:e28938, 2011

    • Search Google Scholar
    • Export Citation
  • 36

    Skilbeck CE, , Wade DT, , Hewer RL, & Wood VA: Recovery after stroke. J Neurol Neurosurg Psychiatry 46:58, 1983

  • 37

    Spetzler RF, , McDougall CG, , Albuquerque FC, , Zabramski JM, , Hills NK, & Partovi S, : The Barrow Ruptured Aneurysm Trial: 3-year results. Clinical article. J Neurosurg 119:146157, 2013

    • Search Google Scholar
    • Export Citation
  • 38

    Starke RM, , Komotar RJ, , Otten ML, , Schmidt JM, , Fernandez LD, & Rincon F, : Predicting long-term outcome in poor grade aneurysmal subarachnoid haemorrhage patients utilising the Glasgow Coma Scale. J Clin Neurosci 16:2631, 2009

    • Search Google Scholar
    • Export Citation
  • 39

    Strong AJ, & Macdonald RL: Cortical spreading ischemia in the absence of proximal vasospasm after aneurysmal subarachnoid hemorrhage: evidence for a dual mechanism of delayed cerebral ischemia. J Cereb Blood Flow Metab 32:201202, 2012

    • Search Google Scholar
    • Export Citation
  • 40

    Taki W, , Sakai N, & Suzuki H: Determinants of poor outcome after aneurysmal subarachnoid hemorrhage when both clipping and coiling are available: Prospective Registry of Subarachnoid Aneurysms Treatment (PRESAT) in Japan. World Neurosurg 76:437445, 2011

    • Search Google Scholar
    • Export Citation
  • 41

    Taylor B, , Harries P, & Bullock R: Factors affecting outcome after surgery for intracranial aneurysm in Glasgow. Br J Neurosurg 5:591600, 1991

    • Search Google Scholar
    • Export Citation
  • 42

    Vergouwen MD, , Etminan N, , Ilodigwe D, & Macdonald RL: Lower incidence of cerebral infarction correlates with improved functional outcome after aneurysmal subarachnoid hemorrhage. J Cereb Blood Flow Metab 31:15451553, 2011

    • Search Google Scholar
    • Export Citation
  • 43

    Vergouwen MD, , Ilodigwe D, & Macdonald RL: Cerebral infarction after subarachnoid hemorrhage contributes to poor outcome by vasospasm-dependent and -independent effects. Stroke 42:924929, 2011

    • Search Google Scholar
    • Export Citation
  • 44

    Wagner AK, & Zitelli KT: A Rehabilomics focused perspective on molecular mechanisms underlying neurological injury, complications, and recovery after severe TBI. Pathophysiology [epub ahead of print] 2012

    • Search Google Scholar
    • Export Citation

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