Predictive factors for shunt dependency in patients with spontaneous intraventricular hemorrhage | Scientific Reports

Nov 13, 2024

Scientific Reports volume 14, Article number: 26462 (2024) Cite this article

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Intraventricular hemorrhage (IVH) occurs in approximately 30–50% patients with spontaneous intracerebral hemorrhage (ICH), with a high 30-day mortality rate. Excess accumulation of parenchymal or ventricular blood associated with the development of acute hydrocephalus leads to poor outcomes. The prediction of shunt dependency is important to identify patients susceptible to requiring permanent shunt placement and benefit from the diversion. This retrospective analytical study aimed to establish a predictive model of shunt dependency in patients with IVH. This study included 179 patients with primary IVH with supratentorial origin or spontaneous ICH with extension into the ventricles between 2015 and 2021. Patients were grouped into “shunt required” and “shunt not required” groups. Variables, including age, sex, preexisting hypertension and diabetes, initial Glasgow Coma Scale scores, ICH location and volume, urokinase administration, modified Graeb score (mGraeb score), and bicaudate index, were analyzed. The shunt required group had significantly higher mGraeb scores (12.0 (6.5–15.0) vs. 7.0 (4.0–12.0), p = 0.001) and higher bicaudate index (0.20 (0.17–0.23) vs. 0.16 (0.13–0.18), P < 0.001) than the shunt not required group. The receiver operating characteristic curve (ROC curve) analysis revealed that a cut-off value of 0.16 of the bicaudate index was significantly related to shunt dependency. The subgroup statistical analysis revealed that neither urokinase administration (p = 0.533) nor urokinase dosage (p = 0.117) showed significant relevance in shunt dependency in patients who received external ventricular drainage. In logistic regression adjusted for the confounders, thalamic ICH (odds ratio (OR) 3.55; 95% confidence interval [(95%CI), 1.13–11.18], an mGraeb score greater than 8 (OR, 3.93; 95%CI, 1.84–8.38), and a bicaudate index greater than 0.16 (OR, 9.87; 95%CI, 3.79–25.73) were factors associated with a higher tendency for shunting. The findings of this study may help identify patients at risk for a permanent shunt after IVH.

Spontaneous intracerebral hemorrhage (ICH) is a cerebrovascular accident (CVA) with high morbidity and mortality, accounting for approximately 10–15% of all CVAs1, 7–20% of all CVAs in Western countries2,3, and 23–30% of all CVAs in Asia4,5. Approximately 30–50% of patients with spontaneous ICH encountered intraventricular hemorrhage (IVH) with a high 30-day mortality rate of 43–68%6,7. Excess accumulation of parenchymal or ventricular blood associated with the development of acute hydrocephalus leads to poor outcomes8. Furthermore, IVH-related acute hydrocephalus accounts for 45% of all hydrocephalus cases9.

External ventricular drainage (EVD) is a commonly used lifesaving procedure for the management of raised intracranial pressure (ICP) due to acute hydrocephalus. As a consequence of the disturbance of normal cerebral spinal fluid (CSF) flow, approximately 7–30% of these cases require permanent CSF diversion10,11. However, prolonged EVD drainage increases the risks of infection. Thus, a permanent CSF diversion modality with shunt placement may be required.

The prediction of shunt dependency is important to identify patients who are likely to require permanent shunt placement and benefit from the diversion. Previous studies have demonstrated multiple predictors of shunt-dependent hydrocephalus, such as thalamic ICH, posterior fossa ICH, IVH presentation, IVH volume, elevated ICP, old age, or craniectomy surgery12,13,14. This study aimed to establish a predictive model of shunt dependency in patients with IVH.

This was a retrospective analytical study. A total of 382 patients with primary IVH with supratentorial origin or spontaneous ICH with extension into the ventricles between 2015 and 2021 were enrolled. Patients eligible for EVD placement in our study were those presenting with severe IVH, or acute hydrocephalus accompanied by raised ICP signs such as coma or pupil dilation, necessitating ICP monitoring. Exclusion criteria included patients younger than 18 years, those with ICH that resulted from vascular malformation, cerebral aneurysm, trauma, previous thrombolysis-related hemorrhage, or drug-related hemorrhage, those with a history of preexisting brain diseases such as brain tumors, meningitis, or brain abscess, and those who did not survive to discharge after EVD placement or received palliative care. In addition, patient with a final pathologic diagnosis with amyloid angiopathy was excluded as well. This study was approved by the Institutional Review Board of Taichung Veterans General Hospital.

The possible factors affecting the development of shunt-dependent hydrocephalus were estimated. Data, including age, sex, preexisting hypertension and diabetes, ICH location and volume, and IVH presentation, were collected (Table 1). Post-operatively, we conducted brain CT scans within 12–24 h following the surgery to assess the need for intraventricular fibrinolysis. This evaluation was specifically focused on the extent of IVH reduction after a minimum of 12 h of drainage. If the IVH exhibited no significant decrease in volume, we then considered the administration of further fibrinolytic therapy. The use of urokinase for blood clot thrombolysis for patients who underwent EVD insertion was recorded, including dosage.

The hemorrhage location were divided into several categories: primary IVH, lobar ICH (located in cortical or subcortical areas), thalamus ICH, caudate/putamen ICH, pons ICH and cerebellar hemorrhage. The ICH volume was calculated using the following formula mentioned in Eq. (1).

where A is the maximum length (in cm), B is the width perpendicular to A on the same brain computed tomography (CT) slice, and C is the number of slices multiplied by the slice thickness) on brain CT scans. The bicaudate index was recorded from the initial brain CT upon emergency department arrival for hydrocephalus assessment. The IVH severity was assessed using the modified Graeb score (mGraeb score)15. The score demonstrated a maximum score of 32, quantifying the accumulation of blood within each ventricle: the fourth ventricle (maximum score 4), the third ventricle (maximum score 4), the right and left lateral ventricles (maximum score 4 for each), the right and left occipital horns (maximum score 2 for each), and the right and left temporal horns (maximum score 2 for each). Any blood clot that expanded beyond the normal anatomic boundary was given a score of + 1 in each compartment.

In our study, the process to assess the need for shunt placement, particularly in patients with an EVD, was carefully structured. The EVD challenge was typically initiated no sooner than one week following the initial EVD insertion. This challenge involved gradually elevating the EVD setting level and eventually clamping the EVD, provided the patient did not exhibit signs of sustained increased ICP or evidence of ongoing hydrocephalus. EVD challenge failure, indicating a potential need for shunt placement, was defined by specific clinical markers: a decline in the patient’s consciousness level that resolved upon cessation of the challenge, or a sustained ICP level exceeding 20 mmHg. In most cases, we conducted at least two attempts at weaning off the EVD, usually spaced about a week apart. As a result, shunt surgeries were indicated for patients who showed progressively enlarged ventricles with neurologic state deterioration or who failed to tolerate a gradual reduction in the EVD drainage amount.

Categorical variables were analyzed using the chi-square test, and continuous variables were analyzed using the Mann–Whitney U tests. Patients were grouped into “shunt required” (n = 46) and “shunt not required” (n = 133) groups. Shunt-related factors were compared between these two groups. The independent effects of risk factors on shunt occurrence were analyzed using multivariable regression analysis, with P < 0.05 indicating statistical significance. Additional subgroup analysis for urokinase administration was performed in patients receiving EVD insertion. The receiver operating characteristic curve (ROC curve) analysis was performed with an acceptable area under the ROC curve (AUC) value between 0.6 and 1 to access various threshold settings.

Of the 382 patients, 203 were excluded due to having ICH resulting from vascular malformation or trauma, having brain diseases, early death, palliative strategy implementation, or incomplete clinical data. Thus, a total of 179 patients were included in this study.

A total of 46 patients (26%) needed permanent CSF diversion, and the median time to shunting was 17.0 days (interquartile range (IQR): 13.25–28.5). The mean age of the patients was 68.7 ± 13.5 years in the shunt required group versus 64.8 ± 15.1 in the shunt not required group (p = 0.123). The shunt required group showed a poor Glasgow Coma Scale (GCS) score at arrival (median: 11.5; IQR: 8.0–15.0) compared with the “shunt not required” group (median 14.0; IQR: 10.0–15.0). No statistical differences in age and sex were observed between both groups. Comorbidities of hypertension (83.5% in the shunt not required group vs. 89.1% in the shunt required group, p = 0.354) and diabetes (21.1% in the shunt not required group vs. 23.9% in the shunt required group, p = 0.685) were similar among patients with and without shunts.

The shunt required group had significantly higher mGraeb scores (12.0 (6.5–15.0) vs. 7.0 (4.0–12.0), p = 0.001) and higher bicaudate index (0.20 (0.17–0.23) vs. 0.16 (0.13–0.18), P < 0.001). The ROC curve analysis (Table 2) revealed that a cut-off value of 0.16 of the bicaudate index was significantly related to shunt dependency (AUC = 0.804, P < 0.001) (Fig. 1), and the trend of mGraeb scores higher than 8 was correlated with shunt requirement, but the AUC value was only 0.66 (Fig. 2).

Receiver operating characteristic curve (ROC curve) analysis of the bicaudate index for the shunt dependency prediction. The sensitivity and specificity of the bicaudate index in predicting shunt dependency were 87.0% and 59.4%, respectively, at the cut-off value of 0.16 of the bicaudate index (AUC = 0.804, P < 0.001).

ROC curve analysis of the mGraeb score for the shunt dependency prediction. The sensitivity and specificity of the mGraeb score in predicting shunt dependency were 71.7% and 57.1%, respectively, at the cut-off value of 8 of the mGraeb score (AUC = 0.660, P < 0.001).

The hematoma volume (12.4 (5.8–20.9) mL vs. 9.1 (4.5–29.5) mL, p = 0.625) was not significantly different between the two groups. However, the hematoma location showed statistical significance in shunt dependency (p = 0.039). Regarding the ICH location, the shunt required group was most frequently associated with thalamic ICH (60.9%), followed by cerebellar hemorrhage (10.9%), primary IVH (8.7%), lobar ICH (8.7%), pons ICH (6.5%), and caudate/putamen ICH (4.3%), whereas the shunt not required group was most frequently associated with thalamic ICH (42.1%), followed by primary IVH (21.1%), caudate/putamen ICH (16.5%), lobar ICH (11.3%), cerebellar hemorrhage (6.0%), and pons ICH (3.0%).

A total of 135 patients received EVD insertion. Of the 135 patients, 75 (55.6%) received intraventricular urokinase. The subgroup statistical analysis revealed that neither urokinase administration (p = 0.533) nor urokinase dosage (p = 0.117) showed significant relevance in shunt dependency (Table 3). In the logistic regression adjusted for the confounders (Table 3), thalamic ICH (odds ratio (OR) 3.55; 95% confidence interval (95%CI) 1.13–11.18), an mGraeb score > 8 (OR 3.93; CI 1.84–8.38), and a bicaudate index > 0.16 (OR 9.87; CI 3.79–25.73) were the factors associated with a higher tendency for shunting.

Our study found that higher mGraeb scores and increased bicaudate index values are associated with an elevated risk of needing permanent CSF diversion. ROC curve analysis highlighted significant cutoff values for these parameters as potential indicators of shunt dependency. Subgroup analysis revealed that urokinase treatment in intraventricular fibrinolysis did not significantly affect shunt dependency in patients with external ventricular drainage. Additionally, logistic regression analysis identified thalamic ICH as a predictive factor for increased shunt dependency, aligning with findings from previous research10.

It is generally accepted that patients with non-subarachnoid hemorrhagic ICH have a lower incidence of developing chronic hydrocephalus than patients with aneurysmal subarachnoid hemorrhage16,17. For patients with aneurysmal subarachnoid hemorrhage, the disturbance of normal CSF drainage to the venous sinuses resulted from subarachnoid blood clots or an inflammatory environment causing excess accumulation of CSF in the ventricles. However, a more intricate interaction of factors, such as hematoma-related CSF flow obstruction, deteriorative ventricular compliance, impaired CSF reabsorption, and post-hemorrhagic inflammation, may be associated with shunt dependency in patients with non-subarachnoid hemorrhagic ICH.

Several predictors of permanent hydrocephalus have been reported, including poor GCS score at admission18, thalamic ICH location10, elevated ICP level10,12,19,20,21, hypertension, and slow CSF circulation22. Furthermore, huge variability concerning the incidence of shunt-dependent hydrocephalus in patients with spontaneous IVH has been reported23. The CLEAR III trial in 2017 showed an incidence of long-term shunt placement of 18%24, whereas Gluski et al.25 reported an incidence of 1.6% in their study. Zacharia et al.10 and Miller et al.12 reported 20% and 28.3% shunt dependency rates, respectively. A similar result showing that an elevated ICP level and the presence of IVH on arrival are associated with higher rates of shunt-dependent hydrocephalus was observed in these studies. However, Gluski et al.25 reported that hemorrhage location surprisingly did not predict shunt dependency but did correlate with functional outcomes.

In this study, 46 patients (25.7%) required permanent CSF diversion resulting from chronic hydrocephalus status after a hemorrhagic event. GCS at arrival, ICH location, mGraeb scores, and bicaudate index were associated with permanent shunt dependency in patients with IVH. In the multivariable-adjusted model, GCS at arrival, thalamic ICH, mGraeb scores, and bicaudate index were significantly associated with shunt dependency after EVD placement. Previous studies have shown an association between infratentorial ICH and poor outcomes. However, strong evidence regarding the relationship between pons/cerebellar ICH and shunt dependency is still needed26,27. In this study, although pons and cerebellar ICH showed a higher OR than thalamic ICH (OR 4.52; 95%CI 0.95–21.64; p = 0.059 for cerebellar ICH and OR 5.38; 95%CI 0.85–34.02; p = 0.074 for pons ICH), these two factors did not reach statistical significance. Kuo et al. proposed that a hematoma in the third and fourth ventricles showed a more significant association with shunt dependency than that in the lateral ventricles14. Further studies and clinical evidence are needed to determine whether pons and cerebellar ICH-related third and fourth ventricle obstruction will result in a permanent shunt requirement in patients with ICH.

In discussing the radiologic evaluation of the modified Graeb (mGraeb) score, we propose that obstructive blood clots in IVH patients hinder CSF outflow, leading to acute hydrocephalus and ventriculomegaly. The extent of hemorrhage within the intraventricular space, due to its impact on CSF circulation and outflow, intuitively suggests a greater likelihood of requiring additional CSF drainage. Unlike ICH, the volume of IVH lacks a definitive measurement protocol, prompting us to utilize the mGraeb score for evaluation. Our ROC curve analysis identified a cutoff value of 8 as a predictor of shunt dependency.

The bicaudate index, a common clinical tool for hydrocephalus assessment, potentially indicates the risk of sustained CSF reabsorption or outflow blockage following ICH. Radiographic factors correlating with shunt placement were significant, with identified clinical cut-offs. Prior studies measuring the bicaudate index at admission suggested a ventriculoperitoneal shunt requirement in cases exceeding 0.228,29. Rubinos et al. examined the relationship between sequential bicaudate index measurements during hospitalization and shunt dependency30. Our analysis yielded a threshold of 0.16 (AUC 0.8) for assessing the association between the bicaudate index and shunt dependency. Previous research has indicated a positive correlation between the bicaudate index and age31,32,33, with Dhok et al. also noting significant sex-based differences34. Consequently, our multivariable logistic regression model was adjusted for age and sex, revealing that a bicaudate index value above 0.16 significantly predicts the need for permanent CSF diversion.

A subgroup statistical analysis was performed regarding intraventricular fibrinolysis (IVF) use in patients with IVH. The results showed that neither urokinase administration (p = 0.533) nor urokinase dosage (p = 0.117) showed significant relevance in shunt dependency prevention. Regarding IVF use, previous reviews have been cautiously optimistic35,36,37, with a lower risk of mortality and ventriculitis. Similar positive findings with lower mortality were proposed by van Solinge et al.38. However, the same study also found no significant difference in shunt dependency but an increase in symptomatic hemorrhages in patients receiving IVF. Covrig et al.39 conducted a retrospective study including 102 patients with IVH or ICH over 7 years to compare the effect of urokinase versus alteplase (recombinant tissue plasminogen activator (rt-PA)). The results showed 12.2% shunt dependency in the urokinase group and 15.0% in the rt-PA group, with no statistically significant difference between both groups.

This study has some limitations. It was a retrospective analysis with a relatively small sample size due to the strict inclusion criteria. Additionally, no unified EVD challenge protocol or definition of shunt-dependent hydrocephalus was reported. Consequently, the need for a permanent CSF shunt was entirely decided by surgeons according to clinical symptoms, image findings, and personal experience. These subjective factors further influence the shunt placement interval and essentiality and make it difficult to generalize the results.

Shunt dependency after an IVH episode was associated with GCS at arrival, ICH location, mGraeb scores, and the bicaudate index. The logistic regression model revealed that thalamic ICH, mGraeb score > 8, and bicaudate index value > 0.16 are related to permanent shunt requirement. These findings may help identify patients at risk for a permanent shunt after IVH.

Data are available upon reasonable request. The datasets used during the current study are available from the Taichung Veterans General Hospital; however, restrictions apply regarding the availability of these data, as they are not publicly available. However, the data are available from the corresponding author upon reasonable request and with permission from the Taichung Veterans General Hospital.

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We would like to thank Enago (www.enago.com/karger) for English language editing.

Department of Neurosurgery, Neurological Institute, Taichung Veterans General Hospital, Taichung, Taiwan, ROC

Chi-Ruei Li, Chun-Ming Yen, Meng-Yin Yang, Wen-Yu Cheng, Chiung-Chyi Shen & Szu-Yuan Liu

Oncology Neurosurgery Division, Department of Neurosurgery, Neurological Institute, Taichung Veterans General Hospital, 1650 Taiwan Boulevard Section 4, Taichung, 40705, Taiwan, ROC

Meng-Yin Yang & Szu-Yuan Liu

College of Nursing, Central Taiwan University of Science and Technology, Taichung, Taiwan, ROC

Meng-Yin Yang

Institute of Biomedical Sciences, National Chung Hsing University, Taichung, Taiwan, ROC

Wen-Yu Cheng

Department of Physical Therapy, Hungkuang University, Taichung, Taiwan, ROC

Wen-Yu Cheng & Chiung-Chyi Shen

Basic Medical Education, Central Taiwan University of Science and Technology, Taichung, Taiwan, ROC

Chiung-Chyi Shen

Graduate Institute of Life Science, Department of Life Science, College of Life Science, National Chung Hsing University, Taichung, Taiwan, ROC

Szu-Yuan Liu

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Conceptualization, C.R.L. and S.Y.L.; formal analysis, C.R.L.; investigation, C.R.L.; writing—original draft preparation, C.R.L.; writing—review and editing, S.Y.L.; visualization, M.Y.Y., W.Y.C. and C.C.S.; supervision, C.C.S.; project administration, C.M.Y. All authors have read and agreed to the published version of the manuscript.

Correspondence to Szu-Yuan Liu.

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Li, CR., Yen, CM., Yang, MY. et al. Predictive factors for shunt dependency in patients with spontaneous intraventricular hemorrhage. Sci Rep 14, 26462 (2024). https://doi.org/10.1038/s41598-024-76752-9

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