evaluation of intraventricular hemorrhage assessment...

J Neurosurg / October 14, 2011

DOI: 10.3171/2011.9.JNS10850

1

IntraventrIcular extension occurs in 30%–45% of patients with ICH and is an independent predictor of poor outcome.1,3,25,26 The presence of IVH significantly

increases the risk of death and IVH volume directly cor-responds to the likelihood of death.27 Recent reports have demonstrated that early expansion of IVH worsens out-come25 and intraventricular clot removal reduces inflam-mation, hydrocephalus, and long-term functional deficits in the setting of ICH.12,18,23,28 Thus, the accurate assessment of IVH volume and severity is critical, particularly to de-termine the efficacy of novel treatments that aim to remove

Evaluation of intraventricular hemorrhage assessment methods for predicting outcome following intracerebral hemorrhage

Clinical articleBrian 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., anD e. 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 independent predictor of poor outcome. Clinical methods for evaluating IVH, however, are not well established. This study sought to determine the best IVH grading scale by evaluating the predictive accuracies of IVH, Graeb, and LeRoux scores in an 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 University Medical 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 for ICH location, hematoma volume, and presence of IVH. Intraventricular hemorrhage was categorized according to IVH, 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 modified Rankin Scale (mRS). Receiver operating characteristic analysis 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 scores were 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 the receiver operating characteristic curve were similar among the IVH, Graeb, and LeRoux scores (0.745, 0.743, and 0.744, respectively) and within 6 days postictus (0.765, 0.722, 0.723, respectively). Moreover, the IVH, Graeb, and LeRoux scores had similar maximum Youden Indices both at admission (0.515 vs 0.477 vs 0.440, respectively) and within 6 days postictus (0.515 vs 0.339 vs 0.365, respectively). Patients who received EVDs had higher mean IVH volumes (23 ± 26 ml vs 9 ± 11 ml, p = 0.003) and increased incidence of Glasgow Coma Scale scores < 8 (67% vs 38%, p = 0.015) and hydrocephalus (82% vs 50%, p = 0.004) at admission but had similar outcome as those who did not receive an EVD.

Conclusions. The IVH, Graeb, and LeRoux scores predict outcome well with similarly good accuracy in ICH patients with IVH when assessed at admission and within 6 days after hemorrhage. Therefore, any of one of the scores 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 beneficial for patients with severe IVH, who have particularly poor prognosis 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 ROC curve; EVD = external ventricular drain; GCS = Glasgow Coma Scale; ICH = intracerebral hemorrhage; IVH = intraventricular hem-orrhage; mRS = modified Rankin scale; ROC = receiver operating characteristic; tPA = tissue plasminogen activator.

B. Y. Hwang et al.

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 hemorrhage size and the presence of dilation within each ventricle (Fig. 1). The scores are useful for IVH evaluation at admission and have been used to define IVH severity20 or to select patients for studies;21 however, their clinical effectiveness to assess IVH or to predict outcome after ICH remains un-clear. The aim of this study was to prospectively evaluate the predictive accuracies of the IVH, Graeb, and LeRoux scores for functional outcome at discharge in a single-center, consecutive series of ICH patients with IVH. We also sought to investigate the subacute IVH dynamic, as well as the impact of EVD placement on IVH severity and outcome.

Methods

Patient Selection and Data Collection

All patients with spontaneous ICH admitted to the neurological intensive care unit of Columbia University Medical Center between February 2009 and February 2011 were offered participation in the Columbia University In-tracerebral Hemorrhage Outcomes Project. The study was approved by the hospital’s institutional review board, and in all cases, informed consent was obtained from the pa-tient or surrogate. The diagnosis of ICH was established by CT scan. Patients were included in the analysis if they had spontaneous nontraumatic ICH with evidence of IVH on CT scans upon admission and within 24 hours of onset.11 Patients 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 ManagementAll patients received standard neurological intensive

care 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 daily amount of drained CSF became less than 100 ml and no ventriculomegaly or increased intracranial pressure was recorded after 48 hours of clamping. Surgical hematoma evacuation was strongly considered for patients with cere-bellar hemorrhage with clinical deterioration or those with brainstem compression and/or hydrocephalus. Surgery was also considered for patients with lobar clots greater than 30 ml and within 1 cm of the cortical surface. The decision to administer intrathecal tPA was based on the preference of the treating neurosurgeon. The protocol consisted of re-moval of approximately 3 ml of CSF followed by 1 mg of tPA delivered in 1 ml of saline, and a 2-ml saline flush. Patients received intrathecal tPA twice daily until the deci-sion was made to discontinue the therapy, based on nearly complete clearance of blood from the ventricles. Further details regarding the clinical management of the patients have been described separately.7 Baseline demographics, medical history, clinical presentation, and clinical course, including EVD insertions, were prospectively recorded.

Radiological AssessmentAll CT scans were assessed using identical techniques.

Two authors (G.A. and C.P.K.) analyzed the scans while blinded to radiologists’ reports and patient outcomes. Con-sensus was then reached for each scan. Admission CT scans performed within 24 hours of onset were reviewed for ICH location, ICH volume, and presence of intraven-tricular extension. Intraventricular hemorrhage severity was 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 volume was measured as previously described, using a computer-based planimetric analysis program, Medical Image Pro-cessing, Analysis and Visualization (NIH).11 Scans were evaluated for the presence of hydrocephalus and the offi-cial radiology reports were consulted in questionable cases. Intraventricular hemorrhage was scored and ICH and IVH volumes were assessed based on the last scan performed during this period.

Fig. 1. Grading scales for assessing IVH severity. A: The IVH score (range 0–23). The IVH score is calculated using the following equation: 3 × (right lateral ventricle score + left lateral ventricle score + hydrocephalus score) + third ventricle score + fourth ventricle score. B: The Graeb score (range 0–12). C: The LeRoux score (range 0–16).


Intraventricular extension assessment in intracerebral hemorrhage

3

Outcome AssessmentSurvival and functional outcomes at discharge were as-

sessed using the mRS, and patients were routinely followed up after discharge by the study neurosurgeon (E.S.C.). Poor outcome was defined as mRS scores ≥ 3.

Statistical AnalysisContinuous variables were dichotomized based on

clinical cutoff points or median values if they were not normally distributed. The chi-square or Fisher exact tests were used to find significant associations between categor-ical or dichotomized variables. The 2-sided Student t-test or the Mann-Whitney U-test was used for normally and nonnormally distributed continuous variables, respective-ly. Receiver operating characteristic analysis was used to determine the predictive accuracies of the LeRoux, Graeb, and IVH scores with regard to discharge poor outcome, as measured by the AUROC. The ROC analysis measures the ability of a scale to discriminate patients with a higher probability of poor outcome from those with a lower prob-ability of poor outcome by assigning the former a higher score, and has been used to determine a clinical grading scale’s predictive accuracy for outcome.4,5,9 An AUROC greater than 0.7 is generally considered useful, and an AUROC between 0.8 and 0.9 indicates excellent accura-cy.8 Dependent AUROCs were compared nonparametri-cally,13 and the maximum Youden Index was identified for each scale to assess their prognostic performance. The maximum Youden Index is the optimization of a func- tion that gives equal weight to sensitivity and specific-ity. It is a method of ROC analysis that offers an alter-native measure to AUROC; whereas AUROC concerns a variable’s discriminative utility at all cutoff points, the maximum Youden Index concerns only the cutoff point at which the combination of sensitivity and specificity is maximal. A probability value ≤ 0.05 was considered sta-tistically significant. Data analysis was performed with SPSS version 17.

ResultsBaseline Characteristics

Of the 142 primary ICH patients enrolled during the study period, 73 (51.4%) met the inclusion criteria and were included in the analysis. Baseline demographic and admis-sion characteristics are outlined in Table 1. Patient charac-teristics were similar to previously reported larger cohorts with ICH.14,15,29,31,32 The mean age of the entire cohort was 62.6 years, 47% were women, and 80% had a history of hypertension. Fifty percent of patients had GCS scores < 8 at admission. Overall, 8% of patients received intrathe-cal tPA, and 53% and 15% underwent EVD placement and hematoma evacuation, respectively.

Radiographic CharacteristicsTable 1 lists radiographic characteristics of the study

cohort. Mean ICH and IVH volumes were 27 ± 33 ml and 17 ± 22 ml, respectively. Sixty-seven percent had radio-graphic evidence of hydrocephalus at admission. Median IVH, Graeb, and LeRoux scores were 13, 8, and 6, respec-

tively. Within 6 days, the incidence of hydrocephalus de-creased to 28% (p = 0.016). Median IVH, Graeb, and Le-Roux scores significantly decreased to 9 (p = 0.005), 4 (p = 0.002), and 4 (p = 0.003), respectively. Thirty-four patients (46.5%) had an increase in their IVH severity according to IVH, Graeb, and LeRoux scores.

Clinical Outcome and Change in IVH SeverityTwenty-five patients (34%) died during initial admis-

sion. Poor outcome (mRS score ≥ 3) was noted in 55 pa-tients (75%). Increase or decrease in IVH severity within 6 postbleed days was not associated with outcome (p = 0.762 and p = 0.513, respectively).

Comparison of IVH Grading Scales in Predicting OutcomeFigure 2 left shows the ROC curves for the admission

IVH, Graeb, and LeRoux scores with regard to discharge functional outcome. The 3 scores demonstrated good ac-curacy for predicting outcome. The AUROCs of the IVH (0.745, 95% CI 0.589–0.900), Graeb (0.743, 95% CI 0.601–0.886) and LeRoux (0.744, 95% CI 0.604–0.884) scores were not statistically different (p = 0.646). The 3 scores were also good at predicting outcome when assessed again within 6 days of admission with similar AUROCs (0.765, 95% CI 0.640–0.891 [IVH] vs 0.722, 95% CI 0.596–0.848 [Graeb] vs 0.723, 95% CI 0.597–0.850 [LeRoux]; Fig. 2 right). Furthermore, the 3 scores had similar maximum Youden Indices and associated sensitivities and specifici-ties when assessed at admission and within 6 days postic-tus (Table 2). Admission IVH score of 9 (IVH volume of approximately 6.0 ml) and 7 (IVH volume of approximate-ly 3.3 ml) were associated with maximum Youden Index, and thus were identified as an optimal cutoff point for poor outcome.

Impact of EVD on IVH Severity and OutcomeAt admission, patients who received an EVD had sim-

ilar demographic characteristics as compared with those who did not (Table 3). The proportion of patients with a GCS score < 8 was significantly higher in the EVD group (p = 0.015). The EVD group also had significantly worse radiographic findings with higher mean IVH volumes compared with the non-EVD group (23 ± 26 ml vs 9 ± 11 ml, respectively; p = 0.003) and increased incidence of hydrocephalus (82% vs 50%, respectively; p = 0.004). In-traventricular hemorrhage severity, as assessed by IVH (17 vs 8, respectively; p < 0.001), Graeb (11 vs 3, respectively; p < 0.001) and LeRoux scores (7 vs 3, respectively; p < 0.001) were significantly worse in the EVD group as com-pared with the non-EVD group (Table 3). Within 6 days of admission, the median IVH (17 vs 10; p = 0.001), Graeb (7 vs 5; p < 0.001) and LeRoux scores (11 vs 5, p < 0.001) significantly decreased in the EVD group compared with the admission scores. During the same period, there was no significant change in median IVH (8 vs 9, p = 0.058), Graeb (3 vs 4, p = 0.182) or LeRoux scores (3 vs 4, p = 0.091) among patients who did not undergo EVD place-ment. The EVD and non-EVD groups had similar postad-mission IVH, Graeb, and LeRoux scores (Table 3). In ad-dition, there was no significant difference in the incidence

B. Y. Hwang et al.


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

DiscussionComparison of the IVH, Graeb, and LeRoux Scores

In this study, we have demonstrated that the admis-sion IVH, Graeb, and LeRoux scores predict functional outcome at discharge with good accuracy. The 3 scores retained their predictive accuracy when assessed within 6 days postictus, suggesting that they are robust against potentially confounding factors, such as discrepancies in medical or surgical management among patients. Although the scores were not intended for predicting outcome per se, their predictive accuracies reflect their ability to assess IVH severity and risk-stratify patients with regard to out-come. Therefore, any 1 of the 3 scores can be considered for IVH evaluation in the setting of ICH and assessment of hemorrhage progression and treatment response, as well as for incorporation into ICH grading scales for improved outcome prediction and risk-stratification.

To our knowledge, this is the first study to directly compare the 3 most commonly used IVH grading scales for 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 and clinical efficacy of treatments. However, there is currently no widely accepted, standardized method for measuring IVH severity or volume. The recently developed IVH score is different from the Graeb and LeRoux scores in several aspects. First, unlike the Graeb and LeRoux scores, the IVH score was specifically developed in a cohort of ICH patients with IVH, and hence, may better account for the characteristics of IVH in this specific population. Further-more, the IVH score may be more sensitive to the differ-ences in severity as it assesses hemorrhage size in thirds rather than halves. The score also considers hydrocephalus, an independent predictor of outcome after ICH,6 separately from IVH volume in each ventricle. This may enable the IVH 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 necessarily always go hand-in-hand. Nevertheless, in our cohort, the difference in how hydrocephalus is evaluated by each scale did not translate into improved predictive accuracy for the IVH score. Also in our cohort, the potential advantages of the 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 <3 mRS Score ≥3 p Value

no. of patients 73 18 55demographic characteristics mean age (yrs) ± SD 62.6 ± 16.6 50.6 ± 16.4 65.4 ± 15.4 0.002† female 31 (42.5) 6 (33.3) 28 (50.9) 0.756 hx of HTN 58 (79.5) 10 (55.6) 48 (87.3) 0.467admission characteristics median GCS score (IQR) 7 (4–13) 15 (14–15) 6 (4–11) <0.001† median ICH score (IQR) 3 (2–3.5) 7 (3–10) 14 (7–17) <0.001† mean ICH volume (ml) ± SD 27.35 ± 32.96 13.37 ± 23.79 30.67 ± 34.10 0.077 mean IVH volume (ml) ± SD 16.92 ± 21.84 4.41 ± 5.15 19.94 ± 23.25 <0.001† bleeding in lt lateral ventricle 61 (83.6) 8 (44.4) 53 (96.4) 0.008† bleeding in rt lateral ventricle 59 (80.8) 10 (55.6) 49 (89.1) 0.449 bleeding in 3rd ventricle 53 (72.6) 6 (33.3) 47 (85.5) 0.016† bleeding in 4th ventricle 44 (60.3) 5 (27.8) 39 (70.9) 0.037† hydrocephalus 49 (67.1) 5 (27.8) 44 (80.0) 0.005† infratentorial ICH 13 (17.8) 1 (5.6) 12 (21.8) 0.440 mean midline shift (mm) ± SD 3.65 ± 4.97 2.07 ± 3.37 4.03 ± 5.23 0.188 median IVH score (IQR) 13 (6–17) 7 (3–10) 14 (7–17) 0.004† median LeRoux score (IQR) 8 (3–12) 3 (2–6) 9 (4–12) 0.005† median Graeb score (IQR) 6 (3–8) 3 (2–4) 6 (4–9) 0.005†hospital course surgical hematoma evacuation 11 (15.1) 1 (5.6) 10 (18.2) 0.679 EVD placement 39 (53.4) 4 (22.2) 35 (63.6) 0.071 intrathecal tPA 6 (8.2) 0 (0) 6 (10.9) 0.588

* HTN = hypertension; IQR = interquartile range.† Statistically significant.



5

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

Effects of Alterations in IVH Severity and Volume on Outcome

Intraventricular hemorrhage volume is directly related to 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 signifi-cant increase in the likelihood of poor functional outcome. This suggests that even relatively small IVH can lead to clinically significant ventricular dysfunction, intracranial hypertension, reduced cerebral perfusion, and secondary cerebral injuries.11 The lower threshold for poor outcome at postadmission may be due to the prolonged exposure of the

ventricles to blood, which worsens IVH-mediated injuries and neurological outcome.22,23

Intraventricular hemorrhage is a dynamic condition and its course depends on many factors, including mean arterial pressure, baseline ICH volume, and treatment.25 Nearly half of our cohort experienced an increase in their IVH severity, suggesting that IVH progression is common beyond the first 24 hours despite standard neurocritical management. Although hydrocephalus resolved and IVH grades improved in a significant number of patients, the overall mean IVH volume did not significantly change. Furthermore, increase or decrease in IVH severity with-in 6 days of hemorrhage was not significantly associated with outcome. This suggests that subacute worsening in IVH volume may not significantly worsen outcome once patients are medically stabilized and hydrocephalus and intracranial pressure are optimally managed. Surprisingly, a decrease in IVH severity also did not have significant influence on outcome. It is possible that IVH either causes a considerable amount of its damage in the early periods, or IVH severity within the first 24 hours determines the ex-tent of cerebral injuries to come. Studies have reported that early changes in IVH severity may significantly influence outcome. Steiner et al.25 have reported that 17% of ICH patients had IVH expansion within 24 hours of symptom onset and that the growth was associated with severe dis-ability and death. We did not investigate the incidence or degree of IVH growth in the first 24 hours. Further studies are needed to determine the IVH dynamics and its clinical impact 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 IVHCurrent treatment for IVH in ICH patients is EVD-as-

sisted drainage but its usefulness remains controversial.21 In our cohort, patients who underwent EVD placement had significantly higher IVH volume and incidence of hy-drocephalus at admission with significantly worse IVH, as assessed 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, and LeRoux scores as predictors of discharge poor functional outcome (mRS score ≥ 3).

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

Score Youden Index Sensitivity Specificity

admission IVH 0.515 0.729 0.786 Graeb 0.477 0.763 0.643 LeRoux 0.440 0.797 0.714w/in 6 days postictus IVH 0.515 0.729 0.786 Graeb 0.339 0.339 1 LeRoux 0.365 0.508 0.857

B. Y. Hwang et al.


hydrocephalus in the EVD group were symptomatic from ventricular expansion. Interestingly, patients who under-went EVD placement and those who did not had similar IVH severity within 6 days of hemorrhage, suggesting that an EVD was effective at alleviating IVH and ventricular obstruction. Although EVD insertion was not associated with outcome, it is important to recognize that the EVD group had similar mortality rates and functional outcome as those who did not receive an EVD, despite having a significantly worse prognosis at admission, which is con-sistent with previous reports.6,30 Although this prospective observational study was not designed to isolate the impact of EVD on outcome, our results suggest EVD placement, in conjunction with neurocritical care and appropriate surgical and medical interventions, may be beneficial in a subset of ICH patients with IVH with particularly dismal prognosis based on admission characteristics. A random-ized clinical trial is needed to determine whether EVD insertion improves outcome in ICH patients with IVH.

Study LimitationsThis study has several limitations. First, only the ad-

mission scans and the last scan performed within 6 days were used for our study. All the patients received at least 1 scan during this time period but they were not performed on 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 IVH score. Although this method has been shown to be accu-rate,11 it is novel and is yet to be conclusively validated. In addition, this study may have been underpowered for dif-ferentiating the predictive accuracies of the scales, as well as detecting small difference among subgroups of patients. Our results must be validated in future studies with larger cohorts and longer follow-up periods that are sufficiently powered to control for the heterogeneity of the study popu-lation and treatments.

ConclusionsThe IVH score, Graeb score, and LeRoux score as-

sessed at admission predict discharge functional outcome in 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 progression is common after the first 24 hours even with standard optimal neurocritical care, its impact on clinical outcome needs to be further elucidated. Future research is also needed to better understand IVH pathophysiology, which may help define optimal timing and degree of interven-tion. Although EVD placement remains one of the main treatments 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 39demographic 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) 0.556admission characteristics GCS score <8 (%) 13 (38.2) 26 (66.7) 0.015* infratentorial ICH (%) 5 (14.7) 8 (20.5) 0.518 mean ICH volume (ml) ± SD 31.38 ± 36.79 23.85 ± 29.25 0.334 mean IVH volume (ml) ± SD 9.21 ± 11.30 23.44 ± 26.24 0.003* hydrocephalus (%) 17 (50.0) 32 (82.1) 0.004* median IVH score (IQR) 8 (4–14) 17 (10–17) <0.001* median LeRoux score (IQR) 3 (2–9) 11 (5–14) <0.001* median Graeb score (IQR) 3 (2–6) 7 (5–10) <0.001*postadmission characteristics (within 6 days postictus) median IVH score (IQR) 9 (6–16) 10 (6–17) 0.701 median LeRoux score (IQR) 4 (2–10) 5 (2–10) 0.446 median Graeb score (IQR) 4 (2–8) 5 (2–7) 0.668clinical course and outcome (%) intrathecal tPA 0 6 (15.4) 0.027* hematoma evacuation 3 (8.8) 8 (20.5) 0.202 in-hospital deaths 10 (29.4) 15 (38.5) 0.416 in-hospital poor outcome (mRS score ≥3) 24 (70.6) 31 (79.5) 0.251

* Statistically significant.



7

on clinical outcome remains controversial. Although an EVD was associated with improvement in outcome in patients with severe IVH with particularly poor progno-sis at admission, a randomized clinical trial is needed to conclusively demonstrate its therapeutic benefits in ICH patients with IVH.

Disclosure

Brian Y. Hwang was supported by a Doris Duke Clinical Research Fellowship.

Author contributions to the study and manuscript preparation include the following. Conception and design: Appelboom, Hwang, Carpenter, CP Kellner, Ducruet, Meyers, Connolly. Acquisition of data: Bruce, Piazza, Carpenter, Deb-Sen, Vaughan. Analysis and interpretation of data: Appelboom, Hwang, Bruce, Piazza, Carpenter, Gigante, CP Kellner, Deb-Sen, Vaughan. Drafting the article: Appelboom, Hwang, Bruce, Carpenter, Gigante, CP Kellner, M Kellner, Deb-Sen, Vaughan, Connolly. Critically revising the article: all authors. Reviewed submitted version of manuscript: all authors. Approved the final version of the manuscript on behalf of all authors: 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.

References

1. Bhattathiri PS, Gregson B, Prasad KS, Mendelow AD: Intra-ventricular hemorrhage and hydrocephalus after spontaneous intracerebral hemorrhage: results from the STICH trial. Acta Neurochir Suppl 96:65–68, 2006

2. Broderick J, Connolly S, Feldmann E, Hanley D, Kase C, Krieger D, et al: Guidelines for the management of spontaneous intracerebral hemorrhage in adults: 2007 update: a guideline from the American Heart Association/American Stroke Asso-ciation Stroke Council, High Blood Pressure Research Council, and the Quality of Care and Outcomes in Research Interdisci-plinary Working Group. Stroke 38:2001–2023, 2007

3. Broderick JP, Brott T, Tomsick T, Miller R, Huster G: Intrace-rebral hemorrhage more than twice as common as subarach-noid hemorrhage. J Neurosurg 78:188–191, 1993

4. Cheung RT, Zou LY: Use of the original, modified, or new intracerebral hemorrhage score to predict mortality and mor-bidity after intracerebral hemorrhage. Stroke 34:1717–1722, 2003

5. Chuang YC, Chen YM, Peng SK, Peng SY: Risk stratification for predicting 30-day mortality of intracerebral hemorrhage. Int J Qual Health Care 21:441–447, 2009

6. Diringer MN, Edwards DF, Zazulia AR: Hydrocephalus: a previously unrecognized predictor of poor outcome from su-pratentorial intracerebral hemorrhage. Stroke 29:1352–1357, 1998

7. Ducruet AF, Hickman ZL, Zacharia BE, Grobelny BT, Narula R, Guo KH, et al: Exacerbation of perihematomal edema and sterile meningitis with intraventricular administration of tis-sue plasminogen activator in patients with intracerebral hem-orrhage. Neurosurgery 66:648–655, 2010

8. Giannini EG, Zaman A, Kreil A, Floreani A, Dulbecco P, Tes-ta E, et al: Platelet count/spleen diameter ratio for the noninva-sive diagnosis of esophageal varices: results of a multicenter, prospective, validation study. Am J Gastroenterol 101: 2511–2519, 2006

9. Godoy DA, Piñero G, Di Napoli M: Predicting mortality in spontaneous intracerebral hemorrhage: can modification to original score improve the prediction? Stroke 37:1038–1044, 2006

10. Graeb DA, Robertson WD, Lapointe JS, Nugent RA, Harrison

PB: Computed tomographic diagnosis of intraventricular hem-orrhage. Etiology and prognosis. Radiology 143:91–96, 1982

11. Hallevi H, Dar NS, Barreto AD, Morales MM, Martin-Schild S, Abraham AT, et al: The IVH score: a novel tool for estimat-ing intraventricular hemorrhage volume: clinical and research implications. Crit Care Med 37:969–974, e1, 2009

12. Hanley DF: Intraventricular hemorrhage: severity factor and treatment target in spontaneous intracerebral hemorrhage. Stroke 40:1533–1538, 2009

13. Hanley JA, McNeil BJ: A method of comparing the areas under receiver operating characteristic curves derived from the same cases. Radiology 148:839–843, 1983

14. Hemphill JC III, Bonovich DC, Besmertis L, Manley GT, Johnston SC: The ICH score: a simple, reliable grading scale for intracerebral hemorrhage. Stroke 32:891–897, 2001

15. Hemphill JC III, Farrant M, Neill TA Jr: Prospective validation of the ICH Score for 12-month functional outcome. Neurology 73:1088–1094, 2009

16. Kothari RU, Brott T, Broderick JP, Barsan WG, Sauerbeck LR, Zuccarello M, et al: The ABCs of measuring intracerebral hemorrhage volumes. Stroke 27:1304–1305, 1996

17. LeRoux PD, Haglund MM, Newell DW, Grady MS, Winn HR: Intraventricular hemorrhage in blunt head trauma: an analysis of 43 cases. Neurosurgery 31:678–685, 1992

18. Mayfrank L, Kim Y, Kissler J, Delsing P, Gilsbach JM, Schröder JM, et al: Morphological changes following exper-imental intraventricular haemorrhage and intraventricular fibrinolytic treatment with recombinant tissue plasminogen act iv ator. Acta Neuropathol 100:561–567, 2000

19. Morgenstern LB, Hemphill JC III, Anderson C, Becker K, Broderick JP, Connolly ES Jr, et al: Guidelines for the man-agement of spontaneous intracerebral hemorrhage: a guide-line for healthcare professionals from the American Heart Association/American Stroke Association. Stroke 41:2108–2129, 2010

20. Nieuwkamp DJ, de Gans K, Rinkel GJ, Algra A: Treatment and outcome of severe intraventricular extension in patients with subarachnoid or intracerebral hemorrhage: a systematic review of the literature. J Neurol 247:117–121, 2000

21. Nishikawa T, Ueba T, Kajiwara M, Miyamatsu N, Yamashita K: A priority treatment of the intraventricular hemorrhage (IVH) should be performed in the patients suffering intracerebral hemorrhage with large IVH. Clin Neurol Neurosurg 111: 450–453, 2009

22. Pang D, Sclabassi RJ, Horton JA: Lysis of intraventricular blood clot with urokinase in a canine model: Part 2. In vivo safety study of intraventricular urokinase. Neurosurgery 19: 547–552, 1986

23. Pang D, Sclabassi RJ, Horton JA: Lysis of intraventricular blood clot with urokinase in a canine model: Part 3. Effects of intraventricular urokinase on clot lysis and posthemorrhagic hydrocephalus. Neurosurgery 19:553–572, 1986

24. Ruscalleda J, Peiró A: Prognostic factors in intraparenchyma-tous hematoma with ventricular hemorrhage. Neuroradiology 28:34–37, 1986

25. Steiner T, Diringer MN, Schneider D, Mayer SA, Begtrup K, Broderick J, et al: Dynamics of intraventricular hemorrhage in patients with spontaneous intracerebral hemorrhage: risk factors, clinical impact, and effect of hemostatic therapy with recombinant activated factor VII. Neurosurgery 59:767–774, 2006

26. Tuhrim S, Dambrosia JM, Price TR, Mohr JP, Wolf PA, Hier DB, et al: Intracerebral hemorrhage: external validation and extension of a model for prediction of 30-day survival. Ann Neurol 29:658–663, 1991

27. Tuhrim S, Horowitz DR, Sacher M, Godbold JH: Volume of ventricular blood is an important determinant of outcome in supratentorial intracerebral hemorrhage. Crit Care Med 27: 617–621, 1999

B. Y. Hwang et al.


28. Wagner KR, Xi G, Hua Y, Zuccarello M, de Courten-Myers GM, Broderick JP, et al: Ultra-early clot aspiration after ly-sis with tissue plasminogen activator in a porcine model of intracerebral hemorrhage: edema reduction and blood-brain bar rier protection. J Neurosurg 90:491–498, 1999

29. Weimar C, Benemann J, Diener HC: Development and valida-tion of the Essen Intracerebral Haemorrhage Score. J Neurol Neurosurg Psychiatry 77:601–605, 2006

30. Young WB, Lee KP, Pessin MS, Kwan ES, Rand WM, Caplan LR: Prognostic significance of ventricular blood in supratento-rial hemorrhage: a volumetric study. Neurology 40:616–619, 1990

31. Zahuranec DB, Gonzales NR, Brown DL, Lisabeth LD, Lon-gwell PJ, Eden SV, et al: Presentation of intracerebral haemor-rhage in a community. J Neurol Neurosurg Psychiatry 77: 340–344, 2006

32. Zahuranec DB, Morgenstern LB, Sánchez BN, Resnicow K, White DB, Hemphill JC III: Do-not-resuscitate orders and pre-dictive models after intracerebral hemorrhage. Neurology 75: 626–633, 2010

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].

evaluation of intraventricular hemorrhage assessment...

Documents