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J Neurosurg / October 14, 2011

DOI: 10.3171/2011.9.JNS10850

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IntraventrIcular extension occurs in 30%45% ofpatients with ICH and is an independent predictor ofpoor outcome.1,3,25,26 The presence of IVH signicantly

increases the risk of death and IVH volume directly cor-responds to the likelihood of death.27 Recent reports havedemonstrated that early expansion of IVH worsens out-come25 and intraventricular clot removal reduces inam-mation, hydrocephalus, and long-term functional decitsin the setting of ICH.12,18,23,28 Thus, the accurate assessmentof IVH volume and severity is critical, particularly to de-

termine the efcacy of novel treatments that aim to remove

Evaluation of intraventricular hemorrhage

assessment methods for predicting outcome followingintracerebral hemorrhage

Clinical article

Brian Y. Hwang, M.D.,SaMuel S. Bruce, B.a.,geoffreY appelBooM, M.D.,MattHew a. piazza, B.a.,aManDa M. carpenter, B.a.,paul r. gigante, M.D.,cHriStopHer p. Kellner, M.D.,anDrew f. Ducruet, M.D.,MicHael a. Kellner, B.S.,rajeev DeB-Sen,KerrY a. vaugHan, B.a.,pHilip M. MeYerS, M.D.,anDe. SanDer connollY jr., M.D.

Department of Neurological Surgery, Columbia University College of Physicians and Surgeons, New York,

New York

Object. Intraventricular hemorrhage (IVH) associated with intracerebral hemorrhage (ICH) is an independentpredictor of poor outcome. Clinical methods for evaluating IVH, however, are not well established. This study soughtto determine the best IVH grading scale by evaluating the predictive accuracies of IVH, Graeb, and LeRoux scores inan independent cohort of ICH patients with IVH. Subacute IVH dynamics as well as the impact of external ventricu-lar drain (EVD) placement on IVH and outcome were also investigated.

Methods. A consecutive cohort of 142 primary ICH patients with IVH was admitted to Columbia UniversityMedical Center between February 2009 and February 2011. Baseline demographics, clinical presentation, and hospi-tal course were prospectively recorded. Admission CT scans performed within 24 hours of onset were reviewed forICH location, hematoma volume, and presence of IVH. Intraventricular hemorrhage was categorized according toIVH, Graeb, and LeRoux scores. For each patient, the last scan performed within 6 days of ictus was similarly evalu-ated. Outcomes at discharge were assessed using the modied Rankin Scale (mRS). Receiver operating characteristicanalysis was used to determine the predictive accuracies of the grading scales for poor outcome (mRS score 3).

Results. Seventy-three primary ICH patients (51%) had IVH. Median admission IVH, Graeb, and LeRoux scoreswere 13, 6, and 8, respectively. Median IVH, Graeb and LeRoux scores decreased to 9 (p = 0.005), 4 (p = 0.002),and 4 (p = 0.003), respectively, within 6 days of ictus. Poor outcome was noted in 55 patients (75%). Areas under thereceiver operating characteristic curve were similar among the IVH, Graeb, and LeRoux scores (0.745, 0.743, and0.744, respectively) and within 6 days postictus (0.765, 0.722, 0.723, respectively). Moreover, the IVH, Graeb, andLeRoux scores had similar maximum Youden Indices both at admission (0.515 vs 0.477 vs 0.440, respectively) andwithin 6 days postictus (0.515 vs 0.339 vs 0.365, respectively). Patients who received EVDs had higher mean IVHvolumes (23 26 ml vs 9 11 ml, p = 0.003) and increased incidence of Glasgow Coma Scale scores < 8 (67% vs38%, p = 0.015) and hydrocephalus (82% vs 50%, p = 0.004) at admission but had similar outcome as those who didnot receive an EVD.

Conclusions. The IVH, Graeb, and LeRoux scores predict outcome well with similarly good accuracy in ICHpatients with IVH when assessed at admission and within 6 days after hemorrhage. Therefore, any of one of thescores would be equally useful for assessing IVH severity and risk-stratifying ICH patients with regard to outcome.These results suggest that EVD placement may be benecial for patients with severe IVH, who have particularly poorprognosis at admission, but a randomized clinical trial is needed to conclusively demonstrate its therapeutic value.

(DOI: 10.3171/2011.9.JNS10850)

KeY worDS intraventricular hemorrhage intracerebral hemorrhage

Graeb Score LeRoux Score IVH Score outcome vascular disorders

1

Abbreviations used in this paper: AUROC = area under the ROCcurve; EVD = external ventricular drain; GCS = Glasgow ComaScale; ICH = intracerebral hemorrhage; IVH = intraventricular hem-orrhage; mRS = modified Rankin scale; ROC = receiver operatingcharacteristic; tPA = tissue plasminogen activator.


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2 J Neurosurg / October 14, 2011

or reduce the effects of IVH. Methods to grade IVH sever-ity, however, are not well established.

The IVH,11 Graeb,10 and LeRoux scores17 were devel-oped to estimate IVH severity based on gross hemorrhagesize and the presence of dilation within each ventricle (Fig.1). The scores are useful for IVH evaluation at admissionand have been used to dene IVH severity20 or to selectpatients for studies;21 however, their clinical effectivenessto assess IVH or to predict outcome after ICH remains un-clear. The aim of this study was to prospectively evaluatethe predictive accuracies of the IVH, Graeb, and LeRouxscores for functional outcome at discharge in a single-center, consecutive series of ICH patients with IVH. Wealso sought to investigate the subacute IVH dynamic, aswell as the impact of EVD placement on IVH severity andoutcome.

Methods

Patient Selection and Data CollectionAll patients with spontaneous ICH admitted to the

neurological intensive care unit of Columbia UniversityMedical Center between February 2009 and February 2011were offered participation in the Columbia University In-tracerebral Hemorrhage Outcomes Project. The study wasapproved by the hospitals institutional review board, andin all cases, informed consent was obtained from the pa-tient or surrogate. The diagnosis of ICH was established byCT scan. Patients were included in the analysis if they hadspontaneous nontraumatic ICH with evidence of IVH onCT scans upon admission and within 24 hours of onset.11Patients were excluded if the ICH was due to secondary

causes such as trauma, aneurysm, or arteriovenous malfor-mation rupture, or hemorrhagic conversion of an infarct.

Clinical Assessment and Management

All patients received standard neurological intensivecare unit management according to our institutional pro-tocol, corresponding to the latest American Heart Asso-ciation guidelines.2,19 An EVD was placed in patients with

evidence of symptomatic hydrocephalus and a GCS score< 8. The catheters were left in place until the total dailyamount of drained CSF became less than 100 ml and noventriculomegaly or increased intracranial pressure wasrecorded after 48 hours of clamping. Surgical hematomaevacuation was strongly considered for patients with cere-bellar hemorrhage with clinical deterioration or those withbrainstem compression and/or hydrocephalus. Surgery wasalso considered for patients with lobar clots greater than 30ml and within 1 cm of the cortical surface. The decisionto administer intrathecal tPA was based on the preferenceof the treating neurosurgeon. The protocol consisted of re-moval of approximately 3 ml of CSF followed by 1 mg oftPA delivered in 1 ml of saline, and a 2-ml saline ush.Patients received intrathecal tPA twice daily until the deci-sion was made to discontinue the therapy, based on nearlycomplete clearance of blood from the ventricles. Furtherdetails regarding the clinical management of the patientshave been described separately.7 Baseline demographics,medical history, clinical presentation, and clinical course,

including EVD insertions, were prospectively recorded.

Radiological Assessment

All CT scans were assessed using identical techniques.Two authors (G.A. and C.P.K.) analyzed the scans whileblinded to radiologists reports and patient outcomes. Con-sensus was then reached for each scan. Admission CTscans performed within 24 hours of onset were reviewedfor ICH location, ICH volume, and presence of intraven-tricular extension. Intraventricular hemorrhage severitywas assessed by determining the IVH,11 Graeb,10 and Le-Roux scores17 according to previously published criteria.Intracerebral hemorrhage volume was determined using

the ABC/2 method.16 Intraventricular hemorrhage volumewas measured as previously described, using a computer-based planimetric analysis program, Medical Image Pro-cessing, Analysis and Visualization (NIH).11 Scans wereevaluated for the presence of hydrocephalus and the of-cial radiology reports were consulted in questionable cases.Intraventricular hemorrhage was scored and ICH and IVHvolumes were assessed based on the last scan performedduring this period.

Fig. 1. Grading scales for assessing IVH severity. A: The IVH score (range 023). The IVH score is calculated using thefollowing equation: 3 (right lateral ventricle score + left lateral ventricle score + hydrocephalus score) + third ventricle score +fourth ventricle score. B: The Graeb score (range 012). C: The LeRoux score (range 016).


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Intraventricular extension assessment in intracerebral hemorrhage

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Outcome Assessment

Survival and functional outcomes at discharge were as-sessed using the mRS, and patients were routinely followedup after discharge by the study neurosurgeon (E.S.C.). Pooroutcome was dened as mRS scores 3.

Statistical Analysis

Continuous variables were dichotomized based onclinical cutoff points or median values if they were notnormally distributed. The chi-square or Fisher exact testswere used to nd signicant associations between categor-ical or dichotomized variables. The 2-sided Student t-testor the Mann-Whitney U-test was used for normally andnonnormally distributed continuous variables, respective-ly. Receiver operating characteristic analysis was used todetermine the predictive accuracies of the LeRoux, Graeb,and IVH scores with regard to discharge poor outcome, asmeasured by the AUROC. The ROC analysis measuresthe ability of a scale to discriminate patients with a higherprobability of poor outcome from those with a lower prob-ability of poor outcome by assigning the former a higherscore, and has been used to determine a clinical gradingscales predictive accuracy for outcome.4,5,9 An AUROCgreater than 0.7 is generally considered useful, and anAUROC between 0.8 and 0.9 indicates excellent accura-cy.8 Dependent AUROCs were compared nonparametri-cally,13 and the maximum Youden Index was identiedfor each scale to assess their prognostic performance. Themaximum Youden Index is the optimization of a func-tion that gives equal weight to sensitivity and specic-ity. It is a method of ROC analysis that offers an alter-native measure to AUROC; whereas AUROC concernsa variables discriminative utility at all cutoff points, the

maximum Youden Index concerns only the cutoff pointat which the combination of sensitivity and specicity ismaximal. A probability value 0.05 was considered sta-tistically signicant. Data analysis was performed withSPSS version 17.

Results

Baseline Characteristics

Of the 142 primary ICH patients enrolled during thestudy period, 73 (51.4%) met the inclusion criteria and wereincluded in the analysis. Baseline demographic and admis-sion characteristics are outlined in Table 1. Patient charac-

teristics were similar to previously reported larger cohortswith ICH.14,15,29,31,32 The mean age of the entire cohort was62.6 years, 47% were women, and 80% had a history ofhypertension. Fifty percent of patients had GCS scores


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of poor outcome between the EVD and non-EVD groups(79.5% vs 70.6%, p = 0.251).

Discussion

Comparison of the IVH, Graeb, and LeRoux Scores

In this study, we have demonstrated that the admis-sion IVH, Graeb, and LeRoux scores predict functionaloutcome at discharge with good accuracy. The 3 scoresretained their predictive accuracy when assessed within

6 days postictus, suggesting that they are robust againstpotentially confounding factors, such as discrepancies inmedical or surgical management among patients. Althoughthe scores were not intended for predicting outcome perse, their predictive accuracies reect their ability to assessIVH severity and risk-stratify patients with regard to out-come. Therefore, any 1 of the 3 scores can be consideredfor IVH evaluation in the setting of ICH and assessmentof hemorrhage progression and treatment response, as wellas for incorporation into ICH grading scales for improvedoutcome prediction and risk-stratication.

To our knowledge, this is the rst study to directlycompare the 3 most commonly used IVH grading scalesfor their abilities to predict outcome after ICH with intra-

ventricular extension. With rapidly growing interest in nov-el therapies for IVH in the setting of ICH, simple and ac-curate assessment of IVH is becoming critical for system-atic evaluation and monitoring of disease progression andclinical efcacy of treatments. However, there is currentlyno widely accepted, standardized method for measuringIVH severity or volume. The recently developed IVH scoreis different from the Graeb and LeRoux scores in severalaspects. First, unlike the Graeb and LeRoux scores, theIVH score was specically developed in a cohort of ICHpatients with IVH, and hence, may better account for the

characteristics of IVH in this specic population. Further-more, the IVH score may be more sensitive to the differ-ences in severity as it assesses hemorrhage size in thirdsrather than halves. The score also considers hydrocephalus,an independent predictor of outcome after ICH,6 separatelyfrom IVH volume in each ventricle. This may enable theIVH score to evaluate the severity of IVH with better ac-curacy as compared with the other scales because hemor-rhage burden and ventricular expansion do not necessarilyalways go hand-in-hand. Nevertheless, in our cohort, thedifference in how hydrocephalus is evaluated by each scaledid not translate into improved predictive accuracy for theIVH score. Also in our cohort, the potential advantages ofthe IVH score failed to translate into improved predictive

TABLE 1: Demographic, admission, and radiographic data of the study population according to functional outcome

(mRS score) at discharge*

Parameter Overall mRS Score


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accuracy for outcome. Given the comparable performances

of the 3 scores, one important feature that distinguishes theIVH score from the others is its ability to rapidly estimateIVH volume without the need for time-consuming calcu-lations that often involve computer-assisted planimetricanalysis. This is important because, once validated as a re-liable and accurate volume estimation tool, the IVH scorewill allow quick and routine clinical assessment of IVHand total volume (IVH and ICH volume) at admission andduring treatment course. This will be useful to researchersas clinical trials move toward novel therapies that addressboth ICH and IVH volumes in recognition of their inde-pendent effects on outcome.12

Effects of Alterations in IVH Severity and Volume onOutcome

Intraventricular hemorrhage volume is directly relatedto the risk of poor outcome after ICH, with volumes of >20 ml often leading to death.24,25,30 In our cohort, admis-sion IVH volume of 6.0 ml was associated with a signi-cant increase in the likelihood of poor functional outcome.This suggests that even relatively small IVH can lead toclinically signicant ventricular dysfunction, intracranialhypertension, reduced cerebral perfusion, and secondarycerebral injuries.11 The lower threshold for poor outcome atpostadmission may be due to the prolonged exposure of the

ventricles to blood, which worsens IVH-mediated injuries

and neurological outcome.22,23Intraventricular hemorrhage is a dynamic condition

and its course depends on many factors, including meanarterial pressure, baseline ICH volume, and treatment.25Nearly half of our cohort experienced an increase in theirIVH severity, suggesting that IVH progression is commonbeyond the rst 24 hours despite standard neurocriticalmanagement. Although hydrocephalus resolved and IVHgrades improved in a signicant number of patients, theoverall mean IVH volume did not signicantly change.Furthermore, increase or decrease in IVH severity with-in 6 days of hemorrhage was not signicantly associatedwith outcome. This suggests that subacute worsening in

IVH volume may not signicantly worsen outcome oncepatients are medically stabilized and hydrocephalus andintracranial pressure are optimally managed. Surprisingly,a decrease in IVH severity also did not have signicantinuence on outcome. It is possible that IVH either causesa considerable amount of its damage in the early periods,or IVH severity within the rst 24 hours determines the ex-tent of cerebral injuries to come. Studies have reported thatearly changes in IVH severity may signicantly inuenceoutcome. Steiner et al.25 have reported that 17% of ICHpatients had IVH expansion within 24 hours of symptomonset and that the growth was associated with severe dis-ability and death. We did not investigate the incidence ordegree of IVH growth in the rst 24 hours. Further studiesare needed to determine the IVH dynamics and its clinicalimpact on hospital course and outcome. Continued inves-tigation into the IVH pathophysiology may also help iden-tify an optimal timing and degree of intervention.

Impact of an EVD on Outcome in ICH Patients With IVH

Current treatment for IVH in ICH patients is EVD-as-sisted drainage but its usefulness remains controversial.21In our cohort, patients who underwent EVD placementhad signicantly higher IVH volume and incidence of hy-drocephalus at admission with signicantly worse IVH, asassessed by the IVH grading scales. Based on our manage-ment protocol, it is likely that a majority of patients with

Fig. 2. Comparison of ROC curves and AUROCs of admission (left) and postadmission (right) IVH scores, Graeb scores, andLeRoux scores as predictors of discharge poor functional outcome (mRS score 3).

TABLE 2: Performance of the IVH, Graeb, and LeRoux scores forpredicting poor outcome (mRS score 3)

Score Youden Index Sensitivity Specifcity

admission

IVH 0.515 0.729 0.786

Graeb 0.477 0.763 0.643

LeRoux 0.440 0.797 0.714

w/in 6 days postictus

IVH 0.515 0.729 0.786

Graeb 0.339 0.339 1

LeRoux 0.365 0.508 0.857


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hydrocephalus in the EVD group were symptomatic fromventricular expansion. Interestingly, patients who under-went EVD placement and those who did not had similarIVH severity within 6 days of hemorrhage, suggesting thatan EVD was effective at alleviating IVH and ventricularobstruction. Although EVD insertion was not associatedwith outcome, it is important to recognize that the EVDgroup had similar mortality rates and functional outcomeas those who did not receive an EVD, despite having asignicantly worse prognosis at admission, which is con-sistent with previous reports.6,30 Although this prospectiveobservational study was not designed to isolate the impactof EVD on outcome, our results suggest EVD placement,in conjunction with neurocritical care and appropriate

surgical and medical interventions, may be benecial in asubset of ICH patients with IVH with particularly dismalprognosis based on admission characteristics. A random-ized clinical trial is needed to determine whether EVDinsertion improves outcome in ICH patients with IVH.

Study Limitations

This study has several limitations. First, only the ad-mission scans and the last scan performed within 6 dayswere used for our study. All the patients received at least 1scan during this time period but they were not performedon the same postbleed day. It is possible that not all wors-ening or improvement in IVH was included in our analysis.

Second, we estimated the IVH volume based on the IVHscore. Although this method has been shown to be accu-rate,11 it is novel and is yet to be conclusively validated. Inaddition, this study may have been underpowered for dif-ferentiating the predictive accuracies of the scales, as wellas detecting small difference among subgroups of patients.Our results must be validated in future studies with largercohorts and longer follow-up periods that are sufcientlypowered to control for the heterogeneity of the study popu-lation and treatments.

Conclusions

The IVH score, Graeb score, and LeRoux score as-sessed at admission predict discharge functional outcomein ICH patients with IVH with good accuracy. Therefore,any 1 of the 3 scores may be considered for IVH assess-ment in the setting of ICH or for improving the perfor-mance of ICH grading scales that incorporates IVH se-verity for outcome prediction. Although IVH progressionis common after the rst 24 hours even with standardoptimal neurocritical care, its impact on clinical outcomeneeds to be further elucidated. Future research is alsoneeded to better understand IVH pathophysiology, whichmay help dene optimal timing and degree of interven-tion. Although EVD placement remains one of the maintreatments of IVH and acute hydrocephalus, its impact

TABLE 3: Demographic, admission, and outcome data of study population according to EVD status

Parameter No EVD EVD p Value

no. of patients 34 39

demographic characteristics

mean age (yrs) SD 65.0 16.3 60.4 16.7 0.234

female (%) 14 (41.2) 20 (51.3) 0.388

hx of HTN (%) 26 (76.5) 32 (82.1) 0.556

admission characteristics

GCS score


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on clinical outcome remains controversial. Although anEVD was associated with improvement in outcome inpatients with severe IVH with particularly poor progno-sis at admission, a randomized clinical trial is needed toconclusively demonstrate its therapeutic benets in ICHpatients with IVH.

Disclosure

Brian Y. Hwang was supported by a Doris Duke ClinicalResearch Fellowship.

Author contributions to the study and manuscript preparationinclude the following. Conception and design: Appelboom, Hwang,Carpenter, CP Kellner, Ducruet, Meyers, Connolly. Acquisitionof data: Bruce, Piazza, Carpenter, Deb-Sen, Vaughan. Analysisand interpretation of data: Appelboom, Hwang, Bruce, Piazza,Carpenter, Gigante, CP Kellner, Deb-Sen, Vaughan. Drafting thearticle: Appelboom, Hwang, Bruce, Carpenter, Gigante, CP Kellner,M Kellner, Deb-Sen, Vaughan, Connolly. Critically revising thearticle: all authors. Reviewed submitted version of manuscript: allauthors. Approved the final version of the manuscript on behalf of allauthors: Appelboom. Statistical analysis: Appelboom, Bruce, Piazza.

Administrative/technical/material support: Appelboom, Hwang,Carpenter, CP Kellner, MA Kellner, Deb-Sen. Study supervision:Appelboom, Hwang, Carpenter, CP Kellner, Meyers, Connolly.

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Manuscript submitted May 31, 2010.

Accepted September 14, 2011.Current affiliation for Dr. Hwang: Department of Neurosurgery,

Johns Hopkins University School of Medicine, Baltimore, Maryland.

Please include this information when citing this paper: published

online October 14, 2011; DOI: 10.3171/2011.9.JNS10850.

Address correspondence to: Geoffrey Appelboom, M.D., Depart-

ment of Neurosurgical Surgery, Columbia University Medical Cen-

ter, New York, New York 10032. email: [email protected].

ivh.scoring.matt 4

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