Volumetric analysis of subarachnoid hemorrhage: assessment of the reliability of two computerized methods and their comparison with other radiographic scales

Clinical article

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Object

There were two main purposes to this study: first, to assess the feasibility and reliability of 2 quantitative methods to assess bleeding volume in patients who suffered spontaneous subarachnoid hemorrhage (SAH), and second, to compare these methods to other qualitative and semiquantitative scales in terms of reliability and accuracy in predicting delayed cerebral ischemia (DCI) and outcome.

Methods

A prospective series of 150 patients consecutively admitted to the Hospital 12 de Octubre over a 4-year period were included in the study. All of these patients had a diagnosis of SAH, and diagnostic CT was able to be performed in the first 24 hours after the onset of the symptoms. All CT scans were evaluated by 2 independent observers in a blinded fashion, using 2 different quantitative methods to estimate the aneurysmal bleeding volume: region of interest (ROI) volume and the Cavalieri method. The images were also graded using the Fisher scale, modified Fisher scale, Claasen scale, and the semiquantitative Hijdra scale. Weighted κ coefficients were calculated for assessing the interobserver reliability of qualitative scales and the Hijdra scores. For assessing the intermethod and interrater reliability of volumetric measurements, intraclass correlation coefficients (ICCs) were used as well as the methodology proposed by Bland and Altman. Finally, weighted κ coefficients were calculated for the different quartiles of the volumetric measurements to make comparison with qualitative scales easier. Patients surviving more than 48 hours were included in the analysis of DCI predisposing factors and analyzed using the chi-square or the Mann-Whitney U-tests. Logistic regression analysis was used for predicting DCI and outcome in the different quartiles of bleeding volume to obtain adjusted ORs. The diagnostic accuracy of each scale was obtained by calculating the area under the receiver operating characteristic curve (AUC).

Results

Qualitative scores showed a moderate interobserver reproducibility (weighted κ indexes were always < 0.65), whereas the semiquantitative and quantitative scores had a very strong interobserver reproducibility. Reliability was very high for all quantitative measures as expressed by the ICCs for intermethod and interobserver agreement. Poor outcome and DCI occurred in 49% and 31% of patients, respectively. Larger bleeding volumes were related to a poorer outcome and a higher risk of developing DCI, and the proportion of patients suffering DCI or a poor outcome increased with each quartile, maintaining this relationship after adjusting for the main clinical factors related to outcome. Quantitative analysis of total bleeding volume achieved the highest AUC, and had a greater discriminative ability than the qualitative scales for predicting the development of DCI and outcome.

Conclusions

The use of quantitative measures may reduce interobserver variability in comparison with categorical scales. These measures are feasible using dedicated software and show a better prognostic capability in relation to outcome and DCI than conventional categorical scales.

Abbreviations used in this paper:AUC = area under the curve; DCI = delayed cerebral ischemia; ICC = intraclass correlation coefficient; ROI = region of interest; SAH = subarachnoid hemorrhage; WFNS = World Federation of Neurological Surgeons.

Article Information

Address correspondence to: Alfonso Lagares, M.D, Ph.D., Department of Neurosurgery, Hospital 12 de Octubre, Universidad Complutense de Madrid, Avda de Cordoba s/n, Madrid, Spain 28041. email: algadoc@yahoo.com.

Please include this information when citing this paper: published online September 21, 2012; DOI: 10.3171/2012.8.JNS12100.

© AANS, except where prohibited by US copyright law.

Headings

Figures

  • View in gallery

    Analysis of the intermethod agreement (Cavalieri-ROI) both for cisternal bleeding volume (A–C) and total bleeding volume (D–F). cc = milliliters; CV = Cavalieri; Cv = cisternal bleeding volume; TV = total bleeding volume.

  • View in gallery

    Analysis of interobserver agreement for cisternal bleeding volume for the ROI method (A–C), Cavalieri method (D–F), and semiquantitative cisternal Hijdra score (G–I). CH = cisternal Hijdra score.

  • View in gallery

    Analysis of interobserver agreement for total bleeding volume for the ROI method (A–C), Cavalieri method (D–F), and semiquantitative total Hijdra score (G–I). TH = total Hijdra score.

  • View in gallery

    Receiver operating characteristic curves for the different qualitative, semiquantitative, and quantitative measures used for determining poor outcome (left) or the development of DCI (right).

References

1

Bland JMAltman DG: Statistical methods for assessing agreement between two methods of clinical measurement. Lancet 1:3073101986

2

Broderick JPBrott TGDuldner JETomsick TLeach A: Initial and recurrent bleeding are the major causes of death following subarachnoid hemorrhage. Stroke 25:134213471994

3

Claassen JBernardini GLKreiter KBates JDu YECopeland D: Effect of cisternal and ventricular blood on risk of delayed cerebral ischemia after subarachnoid hemorrhage: the Fisher scale revisited. Stroke 32:201220202001

4

Drake CGHunt WESano KKassell NPertuiset BSano K: Report of the World Federation of Neurological Surgeons Committee on a universal subarachnoid hemorrhage grading scale. J Neurosurg 68:9859861988

5

Fergusen SMacdonald RL: Predictors of cerebral infarction in patients with aneurysmal subarachnoid hemorrhage. Neurosurgery 60:6586672007

6

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

7

Friedman JAGoerss SJMeyer FBPiepgras DGPichelmann MAMcIver JI: Volumetric quantification of Fisher Grade 3 aneurysmal subarachnoid hemorrhage: a novel method to predict symptomatic vasospasm on admission computerized tomography scans. J Neurosurg 97:4014072002

8

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

9

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

10

Hijdra Avan Gijn JNagelkerke NJVermeulen Mvan Crevel H: Prediction of delayed cerebral ischemia, rebleeding, and outcome after aneurysmal subarachnoid hemorrhage. Stroke 19:125012561988

11

Ibrahim GMWeidauer SMacdonald RL: Interobserver variability in the interpretation of computed tomography following aneurysmal subarachnoid hemorrhage. Clinical article. J Neurosurg 115:119111962011

12

Jennet BBond M: Assessment of outcome after severe brain damage. Lancet 1:4804841975

13

Klimo P JrSchmidt RH: Computed tomography grading schemes used to predict cerebral vasospasm after aneurysmal subarachnoid hemorrhage: a historical review. Neurosurg Focus 21:3E52006

14

Ko SBChoi HACarpenter AMHelbok RSchmidt JMBadjatia N: Quantitative analysis of hemorrhage volume for predicting delayed cerebral ischemia after subarachnoid hemorrhage. Stroke 42:6696742011

15

Kramer AHHehir MNathan BGress DDumont ASKassell NF: A comparison of 3 radiographic scales for the prediction of delayed ischemia and prognosis following subarachnoid hemorrhage. J Neurosurg 109:1992072008

16

Lagares ACicuendez MRamos ASalvador EAlén JFKaen A: Acute perfusion changes after spontaneous SAH: a perfusion CT study. Acta Neurochir (Wien) 154:4054122012

17

Lagares Ade Toledo PFernández-Alén JAIbánez JArikan FSarabia R: Spontaneous Subarachnoid Haemorrhage multicenter database from the Group for the Study of Vascular Pathology of the Spanish Society for Neurosurgery: presentation, inclusion criteria and development of an internet-based registry. Neurocirugia (Astur) 19:4054152008. (Span)

18

Lagares AGómez PAAlén JFArikan FSarabia RHorcajadas A: Aneurysmal subarachnoid hemorrhage: group of study of cerebrovascular pathology of the Spanish society of neurosurgery management guideline. Neurocirugia (Astur) 22:931152011. (Span)

19

Lagares AGómez PAAlén JFLobato RDRivas JJAlday R: A comparison of different grading scales for predicting outcome after subarachnoid haemorrhage. Acta Neurochir (Wien) 147:5162005

20

Lagares AGómez PALobato RDAlén JFAlday RCampollo J: Prognostic factors on hospital admission after spontaneous subarachnoid haemorrhage. Acta Neurochir (Wien) 143:6656722001

21

Luiz RRCosta AJKale PLWerneck GL: Assessment of agreement of a quantitative variable: a new graphical approach. J Clin Epidemiol 56:9639672003

22

Ogilvy CSCarter BS: A proposed comprehensive grading system to predict outcome for surgical management of intracranial aneurysms. Neurosurgery 42:9599701998

23

Reilly CAmidei CTolentino JJahromi BSMacdonald RL: Clot volume and clearance rate as independent predictors of vasospasm after aneurysmal subarachnoid hemorrhage. J Neurosurg 101:2552612004

24

Risselada RLingsma HFBauer-Mehren AFriedrich CMMolyneux AJKerr RS: Prediction of 60 day case-fatality after aneurysmal subarachnoid haemorrhage: results from the International Subarachnoid Aneurysm Trial (ISAT). Eur J Epidemiol 25:2612662010

25

Roda JMConesa GLobato RDGarcia Allut AGomez PAGonzalez Darder JM: Hemorragia subaranoidea aneurismática. Introducción a alguno de los aspectos más importantes de esta enfermedad. Neurocirugia (Astur) 11:1561682000

26

Rosen DSAmidei CTolentino JReilly CMacdonald RL: Subarachnoid clot volume correlates with age, neurological grade, and blood pressure. Neurosurgery 60:2592672007

27

Rosen DSMacdonald RLHuo DGoldenberg FDNovakovic RLFrank JI: Intraventricular hemorrhage from ruptured aneurysm: clinical characteristics, complications, and outcomes in a large, prospective, multicenter study population. J Neurosurg 107:2612652007

28

Rosengart AJHuo JDTolentino JNovakovic RLFrank JIGoldenberg FD: Outcome in patients with subarachnoid hemorrhage treated with antiepileptic drugs. J Neurosurg 107:2532602007

29

Sato TSasaki TSakuma JWatanabe TIchikawa MIto E: Quantification of subarachnoid hemorrhage by three-dimensional computed tomography: correlation between hematoma volume and symptomatic vasospasm. Neurol Med Chir (Tokyo) 51:1871942011

30

Stocchetti NCroci MSpagnoli DGilardoni FResta FColombo A: Mass volume measurement in severe head injury: accuracy and feasibility of two pragmatic methods. J Neurol Neurosurg Psychiatry 68:14172000

31

Teasdale GJennet B: Assessment of coma and impaired consciousness: a practical scale. Lancet 2:81841977

32

van der Jagt MHasan DBijvoet HWPieterman HKoudstaal PJAvezaat CJ: Interobserver variability of cisternal blood on CT after aneurysmal subarachnoid hemorrhage. Neurology 54:215621582000

33

van Norden AGvan Dijk GWvan Huizen MDAlgra ARinkel GJ: Interobserver agreement and predictive value for outcome of two rating scales for the amount of extravasated blood after aneurysmal subarachnoid haemorrhage. J Neurol 253:121712202006

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