Impact of global cerebral atrophy on clinical outcome after subarachnoid hemorrhage

Clinical article

View More View Less
  • 1 Division of Neurosurgery, St. Michael's Hospital, Labatt Family Centre of Excellence in Brain Injury and Trauma Research, Keenan Research Centre of the Li Ka Shing Knowledge Institute of St. Michael's Hospital; and
  • | 2 Department of Surgery, University of Toronto, Ontario, Canada
Restricted access

Purchase Now

USD  $45.00

JNS + Pediatrics - 1 year subscription bundle (Individuals Only)

USD  $515.00

JNS + Pediatrics + Spine - 1 year subscription bundle (Individuals Only)

USD  $612.00
Print or Print + Online

Object

Atrophy in specific brain areas correlates with poor neuropsychological outcome after subarachnoid hemorrhage (SAH). Few studies have compared global atrophy in SAH with outcome. The authors examined the relationship between global brain atrophy, clinical factors, and outcome after SAH.

Methods

This study was a post hoc exploratory analysis of the Clazosentan to Overcome Neurological Ischemia and Infarction Occurring After Subarachnoid Hemorrhage (CONSCIOUS-1) trial, a randomized, double-blind, placebo-controlled trial of 413 patients with aneurysmal SAH. Patients with infarctions or areas of encephalomalacia on CT, and those with large clip/coil artifacts, were excluded. The 97 remaining patients underwent CT at baseline and 6 weeks, which was analyzed using voxel-based volumetric measurements. The percentage difference in volume between time points was compared against clinical variables. The relationship with clinical outcome was modeled using univariate and multivariate analysis.

Results

Older age, male sex, and systemic inflammatory response syndrome (SIRS) during intensive care stay were significantly associated with brain atrophy. Greater brain atrophy was significantly associated with poor outcome on the modified Rankin scale (mRS), severity of deficits on the National Institutes of Health Stroke Scale (NIHSS), worse executive functioning, and lower EuroQol Group–5D (EQ-5D) score. Adjusted for confounders, brain atrophy was not significantly associated with Mini-Mental State Examination and Functional Status Examination scores. Brain atrophy was not associated with angiographic vasospasm or delayed ischemic neurological deficit.

Conclusions

Worse mRS score, NIHSS score, executive functioning, and EQ-5D scores were associated with greater brain atrophy and older age, male sex, and SIRS burden. These data suggest outcome is associated with factors that cause global brain injury independent of focal brain injury.

Abbreviations used in this paper:

CONSCIOUS-1 = Clazosentan to Overcome Neurological Ischemia and Infarction Occurring After Subarachnoid Hemorrhage; CPP = cerebral perfusion pressure; DIND = delayed ischemic neurological deficit; EQ-5D = EuroQol Group–5 Dimension; FSE = Functional Status Examination; GOS = Glasgow Outcome Scale; MMSE = Mini-Mental State Examination; mRS = modified Rankin Scale; NIHSS = National Institutes of Health Stroke Scale; ROI = region of interest; SAH = subarachnoid hemorrhage; SIRS = systemic inflammatory response syndrome; WFNS = World Federation of Neurological Surgeons.

JNS + Pediatrics - 1 year subscription bundle (Individuals Only)

USD  $515.00

JNS + Pediatrics + Spine - 1 year subscription bundle (Individuals Only)

USD  $612.00
  • 1

    Bell BA, , Miller JD, , Neto NG, , O'Neill P, & Laughton LM: Effect of naloxone on deficits after aneurysmal subarachnoid hemorrhage. Neurosurgery 16:498501, 1985

    • Search Google Scholar
    • Export Citation
  • 2

    Bendel P, , Koivisto T, , Aikiä M, , Niskanen E, , Könönen M, & Hänninen T, et al.: Atrophic enlargement of CSF volume after subarachnoid hemorrhage: correlation with neuropsychological outcome. AJNR Am J Neuroradiol 31:370376, 2010

    • Search Google Scholar
    • Export Citation
  • 3

    Bendel P, , Koivisto T, , Hänninen T, , Kolehmainen A, , Könönen M, & Hurskainen H, et al.: Subarachnoid hemorrhage is followed by temporomesial volume loss: MRI volumetric study. Neurology 67:575582, 2006

    • Search Google Scholar
    • Export Citation
  • 4

    Bendel P, , Koivisto T, , Niskanen E, , Könönen M, , Aikiä M, & Hänninen T, et al.: Brain atrophy and neuropsychological outcome after treatment of ruptured anterior cerebral artery aneurysms: a voxel-based morphometric study. Neuroradiology 51:711722, 2009

    • Search Google Scholar
    • Export Citation
  • 5

    Biessels GJ, , Koffeman A, & Scheltens P: Diabetes and cognitive impairment. Clinical diagnosis and brain imaging in patients attending a memory clinic. J Neurol 253:477482, 2006

    • Search Google Scholar
    • Export Citation
  • 6

    Brott T, , Adams HP Jr, , Olinger CP, , Marler JR, , Barsan WG, & Biller J, et al.: Measurements of acute cerebral infarction: a clinical examination scale. Stroke 20:864870, 1989

    • Search Google Scholar
    • Export Citation
  • 7

    de Bresser J, , Vincken KL, , Kaspers AJ, , Rinkel GJ, , Viergever MA, & Biessels GJ: Quantification of cerebral volumes on MRI 6 months after aneurysmal subarachnoid hemorrhage. Stroke 43:27822784, 2012

    • Search Google Scholar
    • Export Citation
  • 8

    Dhar R, & Diringer MN: The burden of the systemic inflammatory response predicts vasospasm and outcome after subarachnoid hemorrhage. Neurocrit Care 8:404412, 2008

    • Search Google Scholar
    • Export Citation
  • 9

    Dikmen S, , Machamer J, , Miller B, , Doctor J, & Temkin N: Functional status examination: a new instrument for assessing outcome in traumatic brain injury. J Neurotrauma 18:127140, 2001

    • Search Google Scholar
    • Export Citation
  • 10

    Dumont AS, , Dumont RJ, , Chow MM, , Lin CL, , Calisaneller T, & Ley KF, et al.: Cerebral vasospasm after subarachnoid hemorrhage: putative role of inflammation. Neurosurgery 53:123135, 2003

    • Search Google Scholar
    • Export Citation
  • 11

    Fergusen S, & Macdonald RL: Predictors of cerebral infarction in patients with aneurysmal subarachnoid hemorrhage. Neurosurgery 60:658667, 2007

    • Search Google Scholar
    • Export Citation
  • 12

    Firbank MJ, , Wiseman RM, , Burton EJ, , Saxby BK, , O'Brien JT, & Ford GA: Brain atrophy and white matter hyperintensity change in older adults and relationship to blood pressure. Brain atrophy, WMH change and blood pressure. J Neurol 254:713721, 2007

    • Search Google Scholar
    • Export Citation
  • 13

    Fischer U, , Arnold M, , Nedeltchev K, , Brekenfeld C, , Ballinari P, & Remonda L, et al.: NIHSS score and arteriographic findings in acute ischemic stroke. Stroke 36:21212125, 2005

    • Search Google Scholar
    • Export Citation
  • 14

    Hadjivassiliou M, , Tooth CL, , Romanowski CA, , Byrne J, , Battersby RD, & Oxbury S, et al.: Aneurysmal SAH: cognitive outcome and structural damage after clipping or coiling. Neurology 56:16721677, 2001

    • Search Google Scholar
    • Export Citation
  • 15

    Hale PM, , McAllister JP II, , Katz SD, , Wright LC, , Lovely TJ, & Miller DW, et al.: Improvement of cortical morphology in infantile hydrocephalic animals after ventriculoperitoneal shunt placement. Neurosurgery 31:10851096, 1992

    • Search Google Scholar
    • Export Citation
  • 16

    Hudak AM, , Caesar RR, , Frol AB, , Krueger K, , Harper CR, & Temkin NR, et al.: Functional outcome scales in traumatic brain injury: a comparison of the Glasgow Outcome Scale (Extended) and the Functional Status Examination. J Neurotrauma 22:13191326, 2005

    • Search Google Scholar
    • Export Citation
  • 17

    Kassell NF, , Haley ECJ Jr, , Apperson-Hansen C, & Alves WM: Randomized, double-blind, vehicle-controlled trial of tirilazad mesylate in patients with aneurysmal subarachnoid hemorrhage: a cooperative study in Europe, Australia, and New Zealand. J Neurosurg 84:221228, 1996

    • Search Google Scholar
    • Export Citation
  • 18

    Lin X, & Blumhardt LD: Inflammation and atrophy in multiple sclerosis: MRI associations with disease course. J Neurol Sci 189:99104, 2001

    • Search Google Scholar
    • Export Citation
  • 19

    Lindegaard KF, , Sorteberg W, & Nornes H: Transcranial Doppler in neurosurgery. Adv Tech Stand Neurosurg 20:3980, 1993

  • 20

    Macdonald RL, , Kassell NF, , Mayer S, , Ruefenacht D, , Schmiedek P, & Weidauer S, et al.: Clazosentan to overcome neurological ischemia and infarction occurring after subarachnoid hemorrhage (CONSCIOUS-1): randomized, double-blind, placebo-controlled phase 2 dose-finding trial. Stroke 39:30153021, 2008

    • Search Google Scholar
    • Export Citation
  • 21

    Miklossy J: Chronic inflammation and amyloidogenesis in Alzheimer's disease—role of Spirochetes. J Alzheimers Dis 13:381391, 2008

  • 22

    Ohman J, , Servo A, & Heiskanen O: Risks factors for cerebral infarction in good-grade patients after aneurysmal subarachnoid hemorrhage and surgery: a prospective study. J Neurosurg 74:1420, 1991

    • Search Google Scholar
    • Export Citation
  • 23

    Pendlebury ST, , Cuthbertson FC, , Welch SJ, , Mehta Z, & Rothwell PM: Underestimation of cognitive impairment by Mini-Mental State Examination versus the Montreal Cognitive Assessment in patients with transient ischemic attack and stroke: a population-based study. Stroke 41:12901293, 2010

    • Search Google Scholar
    • Export Citation
  • 24

    Risselada R, , Lingsma HF, , Bauer-Mehren A, , Friedrich CM, , Molyneux AJ, & Kerr RS, et al.: Prediction of 60 day case-fatality after aneurysmal subarachnoid haemorrhage: results from the International Subarachnoid Aneurysm Trial (ISAT). Eur J Epidemiol 25:261266, 2010

    • Search Google Scholar
    • Export Citation
  • 25

    Rosengart AJ, , Huo JD, , Tolentino J, , Novakovic RL, , Frank JI, & Goldenberg FD, et al.: Outcome in patients with subarachnoid hemorrhage treated with antiepileptic drugs. J Neurosurg 107:253260, 2007

    • Search Google Scholar
    • Export Citation
  • 26

    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
  • 27

    Salerno JA, , Murphy DG, , Horwitz B, , DeCarli C, , Haxby JV, & Rapoport SI, et al.: Brain atrophy in hypertension. A volumetric magnetic resonance imaging study. Hypertension 20:340348, 1992

    • Search Google Scholar
    • Export Citation
  • 28

    Scahill RI, , Frost C, , Jenkins R, , Whitwell JL, , Rossor MN, & Fox NC: A longitudinal study of brain volume changes in normal aging using serial registered magnetic resonance imaging. Arch Neurol 60:989994, 2003

    • Search Google Scholar
    • Export Citation
  • 29

    Soininen H, , Puranen M, , Helkala EL, , Laakso M, & Riekkinen PJ: Diabetes mellitus and brain atrophy: a computed tomography study in an elderly population. Neurobiol Aging 13:717721, 1992

    • Search Google Scholar
    • Export Citation
  • 30

    Staff RT, , Murray AD, , Ahearn T, , Salarirad S, , Mowat D, & Starr JM, et al.: Brain volume and survival from age 78 to 85: the contribution of Alzheimer-type magnetic resonance imaging findings. J Am Geriatr Soc 58:688695, 2010

    • Search Google Scholar
    • Export Citation
  • 31

    Tam AK, , Ilodigwe D, , Mocco J, , Mayer S, , Kassell N, & Ruefenacht D, et al.: Impact of systemic inflammatory response syndrome on vasospasm, cerebral infarction, and outcome after subarachnoid hemorrhage: exploratory analysis of CONSCIOUS-1 database. Neurocrit Care 13:182189, 2010

    • Search Google Scholar
    • Export Citation
  • 32

    Tombaugh TN, & McIntyre NJ: The mini-mental state examination: a comprehensive review. J Am Geriatr Soc 40:922935, 1992

  • 33

    van der Zanden BP, , Dijkgraaf MG, , Blanken P, , de Borgie CA, , van Ree JM, & van den Brink W: Validity of the EQ-5D as a generic health outcome instrument in a heroin-dependent population. Drug Alcohol Depend 82:111118, 2006

    • Search Google Scholar
    • Export Citation
  • 34

    van Swieten JC, , Koudstaal PJ, , Visser MC, , Schouten HJ, & van Gijn J: Interobserver agreement for the assessment of handicap in stroke patients. Stroke 19:604607, 1988

    • Search Google Scholar
    • Export Citation
  • 35

    Wilson JT, , Pettigrew LE, & Teasdale GM: Structured interviews for the Glasgow Outcome Scale and the extended Glasgow Outcome Scale: guidelines for their use. J Neurotrauma 15:573585, 1998

    • Search Google Scholar
    • Export Citation
  • 36

    Yoshimoto Y, , Tanaka Y, & Hoya K: Acute systemic inflammatory response syndrome in subarachnoid hemorrhage. Stroke 32:19891993, 2001

  • 37

    Zivadinov R, , Weinstock-Guttman B, , Hashmi K, , Abdelrahman N, , Stosic M, & Dwyer M, et al.: Smoking is associated with increased lesion volumes and brain atrophy in multiple sclerosis. Neurology 73:504510, 2009

    • Search Google Scholar
    • Export Citation

Metrics

All Time Past Year Past 30 Days
Abstract Views 848 212 12
Full Text Views 232 31 1
PDF Downloads 198 21 2
EPUB Downloads 0 0 0