Predictive Factors for Shunt Dependency in Patients with Spontaneous Intraventricular Hemorrhage

doi:10.21203/rs.3.rs-2948583/v1

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Predictive Factors for Shunt Dependency in Patients with Spontaneous Intraventricular Hemorrhage

https://doi.org/10.21203/rs.3.rs-2948583/v1

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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.

Health sciences/Neurology

Health sciences/Diseases

Health sciences/Diseases/Neurological disorders

Spontaneous intracerebral hemorrhage (ICH) is a cerebrovascular accident (CVA) with high morbidity and mortality, accounting for approximately 10–15% of all CVAs [1], 7–20% of all CVAs in Western countries [2, 3], and 23–30% of all CVAs in Asia [4, 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 outcomes [8]. Furthermore, IVH-related acute hydrocephalus accounts for 45% of all hydrocephalus cases [9].

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 diversion [10, 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 surgery [12–14]. 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. 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. 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). The use of urokinase for blood clot thrombolysis for patients who underwent EVD insertion was recorded, including dosage.

Table 1

Baseline demographics, comorbidities, and clinical severity factors in patients with spontaneous IVH
Demographic factors	Shunt not required n = 133 (73.3%)	Shunt required n = 49 (26.7%)	p-value
Sex			0.968
Female	38 (28.6%)	13 (28.3%)
Male	95 (71.4%)	33 (71.7%)
Mean age, year (SD)	64.8 (15.1)	68.7 (13.5)	0.123
Hypertension	111 (83.5%)	41 (89.1%)	0.354
Diabetes mellitus	28 (21.1%)	11 (23.9%)	0.685
GCS at arrival**	14.0 (10.0–15.0)	11.5 (8.0–15.0)	0.027*
ICH location			0.039*
Primary IVH	28 (21.1%)	4 (8.7%)
Lobar ICH	15 (11.3%)	4 (8.7%)
Caudate/putamen	22 (16.5%)	2 (4.3%)
Cerebellar	8 (6.0%)	5 (10.9%)
Pons	4 (3.0%)	3 (6.5%)
Thalamus	56 (42.1%)	28 (60.9%)
ICH volume**	9.1 (4.5–29.5)	12.4 (5.8–20.9)	0.625
mGraeb score**	7.0 (4.0–12.0)	12.0 (6.5–15.0)	0.001*
Bicaudate index**	0.16 (0.13–0.18)	0.20 (0.17–0.23)	< 0.001*
Shunt placement days after ICH	–	17.0 (13.0–29.0)	–
GCS, Glasgow Coma Scale; ICH, intracerebral hemorrhage; IVH, intraventricular hemorrhage; mGraeb score, modified Graeb score; SD, standard deviation. P < 0.05. *Median (interquartile range (IQR)).

The ICH location was divided into two categories: basal ganglia ICH or lobar ICH located in subcortical or cortical areas. The ICH volume was calculated using the following formula mentioned in Eq. (1).

ICH volume = A * B * C / 2 (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.

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.

Statistical analysis

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 = 42) and “shunt not required” (n = 93) 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 0.7 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.

Factors related to permanent shunt requirements

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).

Table 2

Receiver operating characteristic curve (ROC curve) analysis for permanent cerebral spinal fluid (CSF) shunting prediction
Variables	AUC	95%CI	p-value	Optimal cut-off	Sensitivity	Specificity
mGraeb score	0.660	0.586–0.729	< 0.001	> 8	71.74%	57.14%
Bicaudate index	0.804	0.739–0.860	< 0.001	> 0.16	86.96%	59.40%
AUC, area under the ROC curve; CI, confidence interval; mGraeb score, modified Graeb score.

Hematoma related factors analysis

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%).

Subgroups analysis

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.

Table 3

Analysis of the association between intraventricular urokinase use and permanent CSF shunting
	Total	Shunt not required	Shunt required	p-value
Patient with EVD	n = 135	n = 93	n = 42
Urokinase use				0.533
No	60 (44.4%)	43 (46.2%)	17 (40.5%)
Yes	75 (55.6%)	50 (53.8%)	25 (59.5%)
EVD, external

It is generally accepted that patients with non-subarachnoid hemorrhagic ICH have a lower incidence of developing chronic hydrocephalus than patients with aneurysmal subarachnoid hemorrhage [16, 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 admission [18], thalamic ICH location [10], elevated ICP level [10, 12, 19–21], hypertension, and slow CSF circulation [22]. Furthermore, huge variability concerning the incidence of shunt-dependent hydrocephalus in patients with spontaneous IVH has been reported [23]. 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 needed [26, 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 ventricles [14]. 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.

The bicaudate index is one of the commonly used tools to define hydrocephalus in clinical practice. Previous studies have reported a positive correlation between age and the bicaudate index [28–31]. Dhok et al showed that the difference in the mean values of both sexes was statistically significant. In this study, a threshold of 0.16 was found via the ROC analysis to evaluate the association between the bicaudate index and shunt dependency. A multivariable logistic regression model was adjusted for age and sex. The results showed that a value of the bicaudate index higher than 0.16 was a significant predictor of 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 optimistic [32–34], with a lower risk of mortality and ventriculitis. Similar positive findings with lower mortality were proposed by van Solinge et al. [35]. 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. [36] 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.

Our research adhered to the ethical standards set forth by the IRB (No. CE22334A) and conformed to the guidelines for human research ethics. Written informed consent was obtained from all the participants.

Data Availability Statement

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.

Competing Interests

The authors declare no competing interests.

Author Contributions

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.

Acknowledgements

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

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No competing interests reported.

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Predictive Factors for Shunt Dependency in Patients with Spontaneous Intraventricular Hemorrhage

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Abstract

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Introduction

Methods

Statistical analysis

Results

Factors related to permanent shunt requirements

Hematoma related factors analysis

Subgroups analysis

Discussion

Conclusions

Declarations

References

Additional Declarations

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Version 1