Background and Purpose: Optic nerve sheath diameter (ONSD) enlargement occurs in patients with intracerebral hemorrhage (ICH). However, the relationship between ONSD and prognosis of ICH is uncertain. This study aimed to investigate the predictive value of ONSD on poor outcome of patients with acute spontaneous ICH. Methods: We studied 529 consecutive patients with acute spontaneous ICH who underwent initial CT within 6 h of symptom onset between October 2016 and February 2019. The ONSDs were measured 3 mm behind the eyeball on initial CT images. Poor outcome was defined as having a Glasgow Outcome Scale (GOS) score of 1–3, and favorable outcome was defined as having a GOS score of 4–5 at discharge. Results: The ONSD of the poor outcome group was significantly greater than that of the favorable outcome group (5.87 ± 0.86 vs. 5.21 ± 0.69 mm, p < 0.001). ONSD was related to hematoma volume (r = 0.475, p < 0.001). Adjusting other meaningful predictors, ONSD (OR: 2.83; 95% CI: 1.94–4.15) was associated with poor functional outcome by multivariable logistic regression analysis. Receiver operating characteristic curve showed that the ONSD improved the accuracy of ultraearly hematoma growth in the prediction of poor outcome (AUC: 0.790 vs. 0.755, p = 0.016). The multivariable logistic regression model with all the meaningful predictors showed a better predictive performance than the model without ONSD (AUC: 0.862 vs. 0.831, p = 0.001). Conclusions: The dilated ONSD measured on initial CT indicated elevated intracranial pressure and poor outcome, so appropriate intervention should be taken in time.

Intracerebral hemorrhage (ICH) accounts for 10%–15% of all strokes and is the most life-threatening subtype [1]. Increased intracranial pressure (ICP) is a common complication of ICH [2] and is associated with high short-term mortality [3] and poor clinical outcome [4]. Optic nerve sheath diameter (ONSD), a noninvasive estimator of ICP, has been proved to be useful in ICP assessment [5‒7]. ONSD almost concurrently reacted to the variations of ICP in intracranial hemorrhage patients [5]. Several studies have detected that the optic nerve sheath was dilated in the early phase of ICH [5, 8, 9]. The enlarged ONSD has been proved to be a valuable predictor of poor outcome of patients with brain trauma [10], subarachnoid hemorrhage [11], and cardiac arrest [12]. However, it has not been confirmed whether there is a relationship between ONSD and prognosis of ICH. Accurate and early prediction of poor neurological outcome is critically important in the clinical treatment and stratification of patients in clinical trials. Thus, the aim of the present study was to investigate the value of the ONSD measured on initial CT for predicting early outcome and indicating surgical interventions in acute spontaneous ICH patients.

Study Participants

We enrolled patients diagnosed as acute ICH who underwent initial CT scan within 6 h of symptom onset between October 2016 and February 2019. A total of 861 consecutive patients were initially evaluated. Patients who met the following situations were excluded from this study: (1) traumatic ICH (n = 202); (2) anticoagulant or antiplatelet treatment before onset (n = 46); (3) hemorrhagic transformation of cerebral infarction (n = 42); (4) aneurysm or arteriovenous malformation (n = 27); (5) tumor (n = 5); (6) orbital mass lesions, orbital surgery, and ocular or retro-orbital injury (n = 6); and (7) motion artifacts making ONSD measurement unavailable (n = 4). Finally, 529 patients were included in this study, and the selection process of patients is shown in Figure 1.

Fig. 1.

Flowchart of patient selection process. ICH, intracerebral hemorrhage; ONSD, optic nerve sheath diameter.

Fig. 1.

Flowchart of patient selection process. ICH, intracerebral hemorrhage; ONSD, optic nerve sheath diameter.

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Clinical Assessment

We recorded age, sex, systolic and diastolic blood pressure, Glasgow Coma Scale (GCS) score, medical history, and laboratory tests on admission. We obtained the Glasgow Outcome Scale (GOS) score to assess neurological outcome at discharge. Poor outcome was defined as having a GOS score of 1–3, and favorable outcome was defined as having a GOS score of 4–5 [13].

CT Scans and Measurements

Noncontrast CT images were acquired using a 64-section multidetector CT scanner (LightSpeed VCT; GE Healthcare, Milwaukee, WI, USA) with a slice thickness of 5 mm, an interval of 5 mm, a tube current of 80 mA, and a tube voltage of 120 kV(p). The image matrix size was 512 × 512. Two experienced radiologists blinded to clinical status and data of the patients evaluated all CT images. The images were adjusted to the “chest/abdomen” window (window width 300 and window level 10) and magnified 4-fold on the slice where the largest diameter of the optic nerve sheath was shown. From one side to the other, ONSD was measured 3 mm behind the eyeball in a perpendicular vector with reference to the linear axis of the nerve [11] (Fig. 2), and the mean ONSD of both eyes was obtained. Each measurement was performed 3 times, and the mean value was calculated. Hematoma borders were manually segmented on each CT image at Advantage Workstation 4.6 (GE Healthcare), and the corresponding hematoma volume was automatically acquired [14]. Ultraearly hematoma growth (uHG) was defined as baseline hematoma volume (mL) divided by the time from ICH onset to initial CT (hours) [15]. The presence of intraventricular and subarachnoid hemorrhage was recognized. The midline shift was measured on the CT image with the maximum hematoma area [16].

Fig. 2.

Measurement of optic nerve sheath diameter on a brain CT image.

Fig. 2.

Measurement of optic nerve sheath diameter on a brain CT image.

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Statistical Analysis

The categorical variables are presented as absolute values (%), and the continuous variables are presented as means ± SD or medians and interquartile ranges. The Shapiro-Wilk test was used to assess the normality of continuous variables. Statistical significance for intergroup differences was assessed by Pearson χ2 or Fisher’s exact test for categorical variables and by Student’s t test or Mann-Whitney U test for continuous variables. The intraclass correlation coefficient was used to assess the intraobserver and interobserver repeatability for ONSD measurements. Pearson’s correlation was employed to evaluate the correlation between ONSD and hematoma volume. Logistic regression was used to determine the independent predictors for poor outcome at discharge, and the included variables were those associated with poor outcome on univariate analysis (p ≤ 0.1) or risk factors reported by previous research studies. A backward stepwise method was used in multivariable analysis to eliminate nonsignificant variables, and corresponding prediction models with different meaningful predictors were established. Reliability of the model for predicting poor outcome was evaluated with the Hosmer-Lemeshow goodness-of-fit test. Receiver operating characteristic (ROC) curves were depicted to assess the predictive performance of outcome for ONSD and other meaningful predictors, and areas under the curve (AUCs) were compared using MedCalc version 19.0 software (MedCalc Software, Ostend, Belgium) in a method published by DeLong et al. [17]. We obtained optimal cutoffs of ONSD and other predictors for poor neurological outcomes by ROC curve and Youden index. A p value of <0.05 was considered statistically significant for all tests. All statistical analyses other than ROC curve comparison were performed using SPSS 22.0 software (IBM SPSS, Armonk, NY, USA).

The main baseline demographic, clinical, and radiologic characteristics of the patients are summarized in Table 1. In total, 370 of 529 patients (69.9%) experienced poor early outcome at discharge.

Table 1.

Baseline characteristics and potential factors associated with neurologic poor outcome at discharge in patients with ICH

 Baseline characteristics and potential factors associated with neurologic poor outcome at discharge in patients with ICH
 Baseline characteristics and potential factors associated with neurologic poor outcome at discharge in patients with ICH

The ONSD of the poor neurological outcome group was significantly greater than that of the favorable outcome group (5.87 ± 0.86 vs. 5.21 ± 0.69 mm, p < 0.001). The percentage of ICH patients with poor outcome was 47.7%, 60.7%, 80.5%, and 90.8% among groups with interquartile ranges of ONSDs (Fig. 3). ONSD was related to baseline hematoma volume (r = 0.475, p < 0.001) (online suppl. Fig. 1; for all online suppl. material, see www.karger.com/doi/10.1159/000518724). Compared with the conservative treatment group, patients who underwent surgical treatment did have larger hematoma volumes (43.6 [30.1–64.3] vs. 16.4 [8.8–30.7] mL, p < 0.001) and ONSDs (6.23 ± 0.86 vs. 5.41 ± 0.73 mm, p < 0.001). The ONSD of the patients with intraventricular hemorrhage (IVH) was significantly greater than that of the patients without IVH (5.90 ± 0.91 vs. 5.44 ± 0.74 mm, p < 0.001). The intraclass correlation coefficient of intraobserver and interobserver repeatability for ONSD measurements was 0.95 (95% CI: 0.91–0.97, p < 0.001) and 0.90 (95% CI: 0.84–0.94, p < 0.001).

Fig. 3.

Percentage of ICH patients with poor outcome among interquartile ranges of ONSDs. Percent of ICH patients encountering poor outcome with ONSD <5.03 mm: 47.7%, 5.03–5.60 mm: 60.7%, 5.60–6.20 mm: 80.5%, and >6.20 mm: 90.8%. ICH, intracerebral hemorrhage; ONSD, optic nerve sheath diameter.

Fig. 3.

Percentage of ICH patients with poor outcome among interquartile ranges of ONSDs. Percent of ICH patients encountering poor outcome with ONSD <5.03 mm: 47.7%, 5.03–5.60 mm: 60.7%, 5.60–6.20 mm: 80.5%, and >6.20 mm: 90.8%. ICH, intracerebral hemorrhage; ONSD, optic nerve sheath diameter.

Close modal

Age, GCS, ONSD, ICH volume, uHG, midline shift, IVH, and surgical treatment were selected as potential predictors of poor functional outcome at discharge by the univariate analysis or previous studies. Age, GCS, ONSD, uHG, midline shift, infratentorial location, IVH, and surgical treatment were identified as independent predictors for poor functional outcome by multivariable logistic regression analysis (Table 2).

Table 2.

Multivariable logistic regression analysis of poor outcome at discharge in patients with ICH

 Multivariable logistic regression analysis of poor outcome at discharge in patients with ICH
 Multivariable logistic regression analysis of poor outcome at discharge in patients with ICH

The ROC curve is presented in Figure 4. ONSD had moderate predictive value (AUC: 0.728, 95% CI: 0.688–0.765), and uHG showed the best predictive value (AUC: 0.755, 95% CI: 0.716–0.791) among those predictors. There were no significant differences in the predictive performance between ONSD and uHG (Z = 1.002, p = 0.316). The midline shift had an ordinary predictive value (AUC: 0.651, 95% CI: 0.608–0.691), and the ONSD showed a higher performance than the midline shift (Z = 2.504, p = 0.012). The combination of ONSD and uHG showed a higher performance (AUC: 0.790, 95% CI: 0.752–0.824) to predict poor neurological outcomes than either ONSD (Z = 3.953, p < 0.001) or uHG (Z = 2.417, p = 0.016). The multivariable logistic regression model with all the meaningful predictors was well calibrated by the Hosmer-Lemeshow test (p = 0.320) and showed a better predictive performance (AUC: 0.862, 95% CI: 0.830–0.891) than the model with all the meaningful predictors except for ONSD (AUC: 0.831, 95% CI: 0.797–0.862) (Z = 3.283, p = 0.001).

Fig. 4.

ROC curves of the predictive models and predictors to predict poor outcome. Model 1 represents the multivariable logistic regression model with age, GCS, ONSD, uHG, midline shift, infratentorial location, IVH, and surgical treatment. Model 2 represents the multivariable logistic regression model with age, GCS, uHG, midline shift, infratentorial location, IVH, and surgical treatment. ROC, receiver operator characteristic; GCS, Glasgow Coma Scale; ONSD, optic nerve sheath diameter; uHG, ultraearly hematoma growth; MLS, midline shift; IVH, intraventricular hemorrhage.

Fig. 4.

ROC curves of the predictive models and predictors to predict poor outcome. Model 1 represents the multivariable logistic regression model with age, GCS, ONSD, uHG, midline shift, infratentorial location, IVH, and surgical treatment. Model 2 represents the multivariable logistic regression model with age, GCS, uHG, midline shift, infratentorial location, IVH, and surgical treatment. ROC, receiver operator characteristic; GCS, Glasgow Coma Scale; ONSD, optic nerve sheath diameter; uHG, ultraearly hematoma growth; MLS, midline shift; IVH, intraventricular hemorrhage.

Close modal

The optimal cutoff for predicting poor outcome of ONSD and of uHG was 5.59 mm and 7.67 mL/h, respectively. A cutoff value of ONSD >5.59 mm had a sensitivity of 61.4% (95% CI: 56.2–66.3%) and a specificity of 76.1% (95% CI: 68.7–82.5%). A cutoff value of uHG >7.67 mL/h had a sensitivity of 64.6% (95% CI: 59.5–69.5%) and a specificity of 77.4% (95% CI: 70.1–83.6%).

When ONSD >5.59 mm and uHG >7.67 mL/h, the proportion of poor prognosis in ICH patients who underwent hemicraniectomy and hematoma evacuation was lower than that under conservative treatment (87.6% vs. 97.1%, p = 0.029). When ONSD >5.59 mm and GCS ≤12, the proportion of poor prognosis in IVH patients who underwent ventricular drainage was lower than that under conservative treatment (83.3% vs. 100.0%, p = 0.040).

This study investigated the predictive performance of ONSD on poor outcome of patients with acute spontaneous ICH. The finding demonstrated that the ONSD measured on CT images had moderate prognostic value, and it was helpful in improving the prediction of poor outcome at discharge in combination with other predictors.

In our study, ONSD of the poor neurological outcome group was significantly greater than that of the good outcome group. It was consistent with previous studies involving patients with brain trauma [10] and subarachnoid hemorrhage [11], which may reflect that intracranial hypertension leads to a poor prognosis. In previous studies, ONSD of >5.2–6.0 mm indicates an elevated ICP (>20 cm H2O) [5, 6, 18], and this variation may be due to different involved patients. A recent study of ICH patients shows that an ONSD of >5.6 mm indicates an elevated ICP [9]. We figured out that ONSD >5.59 mm is the best cutoff value to predict the poor prognosis of patients with ICH. This is precisely consistent with the cutoff value of the former study. Therefore, we believe that the dilated ONSD is a reflection of elevated ICP. The mechanism of the ONSD inflation in raised ICP is well clarified. An increase in the ICP will be transmitted to the space under the optic nerve sheath, the subarachnoid space surrounding the optic nerve, especially the retrobulbar segment [19]. Because of the limited intracranial space, the ICP raises precipitously while the hematoma expands or cerebral edema develops. Elevated ICP may cause secondary brain injuries such as cerebral ischemia because of the reduced cerebral perfusion pressure [20], which progressively evolves to herniation syndrome and poor prognosis.

In the ROC curve analysis, the ONSD showed moderate predictive value for predicting poor outcome, which was better than the midline shift. The possible explanation was that ONSD is a much better predictor of ICP than the CT features of brain tissue shift [6]. Our study showed a correlation between ONSD and baseline hematoma volume, which is in accordance with the result of a previous study [9]. This result reflected that the mass effect of intracerebral hematoma led to the increase of ICP and dilated ONSD. Among the determined meaningful continuous variables, uHG showed the best predictive ability. The uHG was first reported as a surrogate marker of the speed of hematoma expansion and a valuable parameter for poor outcome prediction [15]. Larger cohort studies subsequently verified that the uHG was associated with increased mortality [21, 22] and our former study also validated the value of uHG in predicting hematoma expansion [23]. However, hematoma growth is not the only factor associated with poor outcome, and uHG alone cannot be regarded as the optimal predictor of neurological prognosis of ICH patients. The composite of ONSD and uHG showed a higher ability to predict poor neurological outcome than either ONSD or uHG alone. Therefore, ONSD improved the predictive performance of uHG. More importantly, the multivariable logistic regression model with all the meaningful predictors showed a better predictive performance than the model without ONSD. In combination with other predictors, ONSD was helpful in improving the prediction of poor outcome.

When ONSD >5.59 mm and uHG >7.67 mL/h, the proportion of poor prognosis in ICH patients who underwent hemicraniectomy and hematoma evacuation was lower than that under conservative treatment, showing the potential value of ONSD in indicating surgery. As recommended in the guideline [24], hemicraniectomy with or without hematoma removal may reduce the mortality of patients with ICH, especially those with refractory intracranial hypertension or coma patients with significant midline shift caused by large hematoma. Logistic regression showed that hemicraniectomy and hematoma evacuation could improve the prognosis of ICH patients. This benefit is based on the idea that hematoma evacuation could reduce mass effect, decrease ICP, improve cerebral perfusion, and restrict secondary brain injury from toxic breakdown products released by the hematoma [25].

In this study, the proportion of patients with IVH in the poor prognosis group was significantly higher than that in the good prognosis group. Previous studies declared that IVH is an indicator of poor prognosis [26]. The mechanisms of IVH-related damage may involve the development of obstructive hydrocephalus, mass effect of hematoma, and secondary injury due to CSF contamination by blood. We found that the ONSD of the patients with IVH was significantly greater than that of the patients without IVH. This may attribute to that IVH often causes obstructive hydrocephalus and intracranial hypertension. When ONSD >5.59 mm and GCS ≤ 12, the proportion of poor prognosis in IVH patients who underwent ventricular drainage was lower than that under conservative treatment, indicating that the ventricular drainage may have the value in improving the prognosis. Patients with large intracerebral hematomas with mass effect or acute hydrocephalus due to IVH associated with decreased level of consciousness may require ventricular drainage as treatment [24].

This study has some limitations. First, we assessed the neurological outcome of ICH patients at discharge with the GOS, but the relationship between ONSD and long-term outcome is uncertain. Second, this study lacked ICP values; thus, the correlation between ICP and ONSD was not confirmed. Finally, selection bias could exist due to the single-center retrospective design, and the value of ONSD for indicating surgery remained to be verified.

The ONSD represents a widely available and easy-to-use parameter for predicting poor outcome at discharge in patients with acute spontaneous ICH. The dilated ONSD indicates elevated ICP and poor outcome, so appropriate surgical intervention should be taken in time. Multicenter prospective trials are needed to further verify the value of ONSD for predicting poor outcome and indicating surgical interventions in patients with acute spontaneous ICH.

This study was approved by the Ethical Review Board of the First Affiliated Hospital of Wenzhou Medical University (Reference No. 2018-128). All study procedures were conducted in accordance with the ethical standards of the 1964 Helsinki Declaration and its later amendments. The ethical review board waived the requirement for informed consent due to the retrospective design.

The authors have no conflicts of interest to declare.

This study was supported by the Scientific Research Incubation Project (FHY2019072), the Science and Technology Planning Projects of Wenzhou (Grant No. Y2020169), and the Zhenjiang Provincial Key Laboratory of Aging and Neurological Disorder Research (LH-001).

Haoli Xu designed and conceptualized the study, analyzed the data, and drafted the manuscript for intellectual content; Yuting Li analyzed the data and revised the manuscript; Jinjin Liu analyzed the data and revised the manuscript; Zhonggang Chen and Qian Chen hosted the data collection and revised the manuscript; Yilan Xiang collected the data and revised the manuscript; Mingyue Zhang collected and validated the data; Wenwen He collected the data; Yuandi Zhuang measured the optic nerve sheath diameters; Yunjun Yang supervised the project and revised the manuscript; Weijian Chen supervised the project and provided funding and resources; Yongchun Chen reviewed all images and protocol and conceptualized the study.

All data generated or analyzed during this study are available from the corresponding author upon reasonable request.

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