Prediction of clinical outcome in subacute subarachnoid hemorrhage using diffusion tensor imaging

Restricted access

OBJECTIVE

Clinical outcome in nontraumatic subarachnoid hemorrhage (SAH) is multifactorial and difficult to predict. Diffusion tensor imaging (DTI) findings are a prognostic marker in some diseases such as traumatic brain injury. The authors hypothesized that DTI parameters measured in the subacute phase of SAH can be associated with a poor clinical outcome.

METHODS

Diffusion tensor imaging was prospectively performed in 54 patients at 8–10 days after nontraumatic SAH. Logistic regression analysis was performed to evaluate the association of fractional anisotropy (FA) and apparent diffusion coefficient (ADC) values with a poor clinical outcome (modified Rankin Scale score ≥ 3) at 3 months.

RESULTS

At 8–10 days post-SAH, after adjusting for other variables associated with a poor outcome, an increased ADC at the frontal centrum semiovale was associated with a poor prognosis (OR estimate 1.29, 95% CI 1.04–1.60, p = 0.020). Moreover, an increase of 0.1 in the FA value at the corpus callosum at 8–10 days after SAH corresponded to 66% lower odds of having a poor outcome (p = 0.002).

CONCLUSIONS

Decreased FA and increased ADC values in specific brain regions were independently associated with a poor clinical outcome after SAH. This preliminary exploratory study supports a potential role for DTI in predicting the outcome of SAH.

ABBREVIATIONS ADC = apparent diffusion coefficient; AUC = area under the ROC curve; DCI = delayed cerebral ischemia; DTI = diffusion tensor imaging; DWI = diffusion-weighted imaging; FA = fractional anisotropy; GCS = Glasgow Coma Scale; HH = Hunt and Hess; MRI = magnetic resonance imaging; mRS = modified Rankin Scale; PLIC = posterior limb of internal capsule; ROC = receiver operating characteristic; ROI = region of interest; SAH = subarachnoid hemorrhage; WFNS = World Federation of Neurosurgical Societies.

Article Information

Correspondence Isabel Fragata: Centro Hospitalar Lisboa Central, Lisbon, Portugal. isabelfragata@gmail.com.

INCLUDE WHEN CITING Published online April 13, 2018; DOI: 10.3171/2017.10.JNS171793.

Disclosures The authors report no conflict of interest concerning the materials or methods used in this study or the findings specified in this paper.

© AANS, except where prohibited by US copyright law.

Headings

Figures

  • View in gallery

    Transverse FA and ADC maps show ROIs drawn bilaterally in the brain parenchyma. Upper and lower left: Regions of interest in the pons and cerebellar white matter. Upper and lower center: Regions of interest in the lentiform nucleus, thalamus, PLIC, and splenium and genu of corpus callosum. Upper and lower right: Regions of interest in the frontal and parietal centrum semiovale. From Neuroradiology, Evolution of diffusion tensor imaging parameters after acute subarachnoid haemorrhage: a prospective cohort study, 59, 2017, 13–21, Fragata I, Canhão P, Alves M, Papoila AL, Canto-Moreira N. With permission from Springer. Figure is available in color online only.

  • View in gallery

    Flowchart with the number of patients admitted, excluded, and enrolled in the present study. h = hours; IV = intravenous.

  • View in gallery

    Influence of age on outcome at 3 months (solid curve) and corresponding 95% confidence intervals (dashed curves), showing a nonlinear association that led to a dichotomization into 2 categories: age 42–67 years and ages < 42/> 67 years.

  • View in gallery

    Odds ratio estimates and corresponding 95% confidence intervals obtained by logistic regression models for a poor clinical outcome in each ROI. A: Fractional anisotropy at 8–10 days post-SAH. B: Apparent diffusion coefficient at 8–10 days post-SAH. C = cerebellum; FCSO = frontal centrum semiovale; GSCC = genu and splenium of corpus callosum; L = lentiform nucleus; P = pons; PCSO = parietal centrum semiovale; T = thalamus.

References

  • 1

    Bendel PKoivisto TAikiä MNiskanen EKönönen MHänninen T: Atrophic enlargement of CSF volume after subarachnoid hemorrhage: correlation with neuropsychological outcome. AJNR Am J Neuroradiol 31:3703762010

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 2

    Bonita RBeaglehole R: Modification of Rankin Scale: Recovery of motor function after stroke. Stroke 19:149715001988

  • 3

    Brander AKataja ASaastamoinen ARyymin PHuhtala HOhman J: Diffusion tensor imaging of the brain in a healthy adult population: Normative values and measurement reproducibility at 3 T and 1.5 T. Acta Radiol 51:8008072010

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 4

    Condette-Auliac SBracard SAnxionnat RSchmitt ELacour JCBraun M: Vasospasm after subarachnoid hemorrhage: interest in diffusion-weighted MR imaging. Stroke 32:181818242001

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 5

    De Marchis GMFilippi CGGuo XPugin DGaffney CDDangayach NS: Brain injury visible on early MRI after subarachnoid hemorrhage might predict neurological impairment and functional outcome. Neurocrit Care 22:74812015

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 6

    Drake CG: Report of World Federation of Neurological Surgeons Committee on a Universal Subarachnoid Hemorrhage Grading Scale. J Neurosurg 68:9859861988 (Letter)

    • Search Google Scholar
    • Export Citation
  • 7

    Ebisu TNaruse SHorikawa YUeda STanaka CUto M: Discrimination between different types of white matter edema with diffusion-weighted MR imaging. J Magn Reson Imaging 3:8638681993

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 8

    Fisher CMKistler JPDavis JM: Relation of cerebral vasospasm to subarachnoid hemorrhage visualized by computerized tomographic scanning. Neurosurgery 6:191980

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 9

    Fragata IAlves MPapoila ALNunes APFerreira PCanto-Moreira N: Early prediction of delayed ischemia and functional outcome in acute subarachnoid hemorrhage. Stroke 48:209120972017

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 10

    Fragata ICanhão PAlves MPapoila ALCanto-Moreira N: Evolution of diffusion tensor imaging parameters after acute subarachnoid haemorrhage: a prospective cohort study. Neuroradiology 59:13212017

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 11

    Frontera JAAhmed WZach VJovine MTanenbaum LSehba F: Acute ischaemia after subarachnoid haemorrhage, relationship with early brain injury and impact on outcome: a prospective quantitative MRI study. J Neurol Neurosurg Psychiatry 86:71782015

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 12

    Frontera JAClaassen JSchmidt JMWartenberg KETemes RConnolly ESJ Jr: Prediction of symptomatic vasospasm after subarachnoid hemorrhage: the modified fisher scale. Neurosurgery 59:21272006

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 13

    Frontera JAFernandez ASchmidt JMClaassen JWartenberg KEBadjatia N: Defining vasospasm after subarachnoid hemorrhage: what is the most clinically relevant definition? Stroke 40:196319682009

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 14

    Germanò Ad’Avella DImperatore CCaruso GTomasello F: Time-course of blood-brain barrier permeability changes after experimental subarachnoid haemorrhage. Acta Neurochir (Wien) 142:5755812000

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 15

    Hackett MLAnderson CS: Health outcomes 1 year after subarachnoid hemorrhage: an international population-based study. Neurology 55:6586622000

  • 16

    Heiss WD: Malignant MCA infarction: pathophysiology and imaging for early diagnosis and management decisions. Cerebrovasc Dis 41:172016

  • 17

    Helbok RKurtz PVibbert MSchmidt MJFernandez LLantigua H: Early neurological deterioration after subarachnoid haemorrhage: risk factors and impact on outcome. J Neurol Neurosurg Psychiatry 84:2662702013

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 18

    Hijdra ABrouwers PJVermeulen Mvan Gijn J: Grading the amount of blood on computed tomograms after subarachnoid hemorrhage. Stroke 21:115611611990

  • 19

    Hop JWRinkel GJEAlgra Avan Gijn J: Case-fatality rates and functional outcome after subarachnoid hemorrhage: a systematic review. Stroke 28:6606641997

  • 20

    Hunt WEHess RM: Surgical risk as related to time of intervention in the repair of intracranial aneurysms. J Neurosurg 28:14201968

  • 21

    Janssen PMVisser NADorhout Mees SM, Klijn CJM, Algra A, Rinkel GJE: Comparison of telephone and face-to-face assessment of the modified Rankin Scale. Cerebrovasc Dis 29:1371392010

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 22

    Jellison BJField ASMedow JLazar MSalamat MSAlexander AL: Diffusion tensor imaging of cerebral white matter: a pictorial review of physics, fiber tract anatomy, and tumor imaging patterns. AJNR Am J Neuroradiol 25:3563692004

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 23

    Kistler JPCrowell RMDavis KRHeros ROjemann RGZervas T: The relation of cerebral vasospasm to the extent and location of subarachnoid blood visualized by CT scan: a prospective study. Neurology 33:4244361983

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 24

    Lindegaard KFNornes HBakke SJSorteberg WNakstad P: Cerebral vasospasm diagnosis by means of angiography and blood velocity measurements. Acta Neurochir (Wien) 100:12241989

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 25

    Liu YSoppi VMustonen TKönönen MKoivisto TKoskela A: Subarachnoid hemorrhage in the subacute stage: elevated apparent diffusion coefficient in normal-appearing brain tissue after treatment. Radiology 242:5185252007

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 26

    Mori SZhang J: Principles of diffusion tensor imaging and its applications to basic neuroscience research. Neuron 51:5275392006

  • 27

    Nitkunan ABarrick TRCharlton RAClark CAMarkus HS: Multimodal MRI in cerebral small vessel disease: its relationship with cognition and sensitivity to change over time. Stroke 39:199920052008

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 28

    Nucifora PGPVerma RLee SKMelhem ER: Diffusion-tensor MR imaging and tractography: exploring brain microstructure and connectivity. Radiology 245:3673842007

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 29

    Pegoli MMandrekar JRabinstein AALanzino G: Predictors of excellent functional outcome in aneurysmal subarachnoid hemorrhage. J Neurosurg 122:4144182015

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 30

    Rinkel GJEAlgra A: Long-term outcomes of patients with aneurysmal subarachnoid haemorrhage. Lancet Neurol 10:3493562011

  • 31

    Rosengart AJSchultheiss KETolentino JMacdonald RL: Prognostic factors for outcome in patients with aneurysmal subarachnoid hemorrhage. Stroke 38:231523212007

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 32

    Sehba FAPluta RMZhang JH: Metamorphosis of subarachnoid hemorrhage research: from delayed vasospasm to early brain injury. Mol Neurobiol 43:27402011

  • 33

    Sener SVan Hecke WFeyen BFEVan der Steen GPullens PVan de Hauwe L: Diffusion tensor imaging: a possible biomarker in severe traumatic brain injury and aneurysmal subarachnoid hemorrhage? Neurosurgery 79:7867932016

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 34

    Teasdale GJennett B: Assessment of coma and impaired consciousness. A practical scale. Lancet 2:81841974

  • 35

    van Gijn JHijdra AWijdicks EFVermeulen Mvan Crevel H: Acute hydrocephalus after aneurysmal subarachnoid hemorrhage. J Neurosurg 63:3553621985

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 36

    Vergouwen MDIVermeulen Mvan Gijn JRinkel GJWijdicks EFMuizelaar JP: Definition of delayed cerebral ischemia after aneurysmal subarachnoid hemorrhage as an outcome event in clinical trials and observational studies: proposal of a multidisciplinary research group. Stroke 41:239123952010

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 37

    Wartenberg KESheth SJMichael Schmidt JFrontera JARincon FOstapkovich N: Acute ischemic injury on diffusion-weighted magnetic resonance imaging after poor grade subarachnoid hemorrhage. Neurocrit Care 14:4074152011

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 38

    Weimer JMJones SEFrontera JA: Acute cytotoxic and vasogenic edema after subarachnoid hemorrhage: a quantitative MRI study. AJNR Am J Neuroradiol 38:9289342017

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 39

    Witsch JFrey HPPatel SPark SLahiri SSchmidt JM: Prognostication of long-term outcomes after subarachnoid hemorrhage: the FRESH score. Ann Neurol 80:46582016

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 40

    Yuh ELCooper SRMukherjee PYue JKLingsma HFGordon WA: Diffusion tensor imaging for outcome prediction in mild traumatic brain injury: a TRACK-TBI study. J Neurotrauma 31:145714772014

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation

TrendMD

Metrics

Metrics

All Time Past Year Past 30 Days
Abstract Views 130 130 12
Full Text Views 176 176 0
PDF Downloads 72 72 0
EPUB Downloads 0 0 0

PubMed

Google Scholar