Abstract
Background:
Considering that the measurement of optic nerve sheath diameter (ONSD) can be easily performed by ultrasound, and previous studies have addressed its possible association with brain damage, the very aim of the present study was to compare the diagnostic value of ultrasound and Rotterdam CT scoring (RCTS) criterion used for measuring ONSD in the prognosis of the mortality and disability level of patients with head trauma.
Materials and Methods:
The prospective cohort study was performed on 142 patients with traumatic brain injury (TBI). CT scan was performed for all patients, and the results were recorded. However, the average ONSD values for both eyes were measured using ultrasound and recorded. Moreover, the patient’s level of disability and outcome were evaluated and recorded based on the RCTS classification and the Glasgow coma scale.
Results:
The diagnostic value of RCTS had the cut-off value of greater than 2 in the prognosis of patients’ mortality (sensitivity: 76.92% and specificity: 73.28%) and the cut-off value of greater than 2 in the prognosis of patients’ disability level (sensitivity: 80.39% and specificity: 89.01%)(P value < 0.001). The ONSD value had a cut-off value > 6.9 mm in the prognosis of disability level (sensitivity: 68.63% and specificity: 82.42%) and had a cut-off value >6.8 mm in the prognosis of mortality (sensitivity: 88.46% and specificity: 40.52%) (P value < 0.001).
Conclusion:
According to the results of the present study, both RCTS and ONSD had an acceptable diagnostic value in the prognosis of the mortality and disability level of patients with TBI.
Keywords: Glasgow coma scale, Optic nerve sheath, Rotterdam CT score, Trauma
INTRODUCTION
At present, trauma is the most common cause of mortality in the first three decades of life.[1] In this regard, brain trauma is the leading cause of death, disability, and economic and social problems in developing countries. It is estimated that approximately 1.5–2 million people are injured each year, and one million of the mentioned people pass away. Moreover, 20% –25% and 10% of brain traumas are caused by road accidents and conflict and violence, respectively.[1,2,3]
Rapid, accurate, and appropriate control of patients’ brain function is of great significance because of the increasing prevalence of traumatic brain injuries and their various complications, especially severe physical and psychological complications, high financial costs, and high mortality rates.[2] In case of any change and increase in any of the components of the skull, a change in the volume of the other components inside the skull and consequently an increase in the intracranial pressure (ICP) owing to the limited space inside the skull will be caused.[3,4]
At present, the use of alternative and non-invasive methods that do not have complications has received due attention given that patients with traumatic brain injury (TBI) [Glasgow coma scale (GCS≤8)] are at risk of poor hemodynamic conditions, it is less likely of being able to move these patients between different therapeutic and diagnostic departments, and there are shortcomings in standard ICP monitoring methods such as the rigid method, the increased risk of bleeding and infection, the need for transferring patients to the operating room to insert an intraventricular catheter, and therefore the need for a special team for performing ventricular catheterization.[5]
In recent decades, neuroimaging techniques have sought radiological criteria to assess the severity of brain trauma and have defined two main classification systems: Marshall CT classification and Rotterdam CT score (RCTS) classification. The prognosis of the Marshall classification does not examine epidural and subdural hematomas separately and does not predict injuries resulting from subarachnoid hemorrhage (SAH). In contrast, the RCTS classification does not have the limitations of the Marshall classification, has been evaluated and validated by many studies, and has been indicated to be an independent predictor of TBI outcome.[5,6,7]
Among non-invasive methods, the measurement of optic nerve sheath diameter (ONSD) with optic nerve ultrasound has been introduced as a valuable alternative to invasive methods for monitoring ICP in patients with severe TBI (GCS ≤ 8). The advantage of this method is that it is easy to perform, which is also convenient for the patient, and does not need to transfer the patient to other equipped wards. In addition, the mentioned method does not have the side effects of invasive methods such as bleeding and infection and is less expensive.[8,9]
In this regard, various studies have indicated that there is a significant direct association between ONSD and ICP levels in individuals.[3,4,10,11,12] However, few studies have addressed the diagnostic value of RCTS or ONSD in the prognosis of mortality and disability levels in patients with pulmonary edema,[13] patients requiring craniotomy,[14] and patients with brain trauma.[15,16] Therefore, the present study aimed at evaluating the diagnostic value of ONSD measured by ultrasound and RCTS criterion in the prognosis of the mortality and disability level in patients with head trauma.
MATERIALS AND METHODS
This study was a prospective cohort study with the aim of diagnostic value. The population of the present study included all patients with brain trauma, which referred to the emergency departments of Al-Zahra and Kashani hospitals in Isfahan in 2019–2020. However, 142 patients were selected as the sample of the study from the mentioned population according to the sample size formula in diagnostic studies and considering a 95% confidence interval, 80% test power, and the diagnostic sensitivity of ONSD in detecting ICP in comparison with RCTS in previous studies equal to 82%, the adaptation ratio equal to 0.90,[16] and the error level of 0.2.
Inclusion criteria were patients with head trauma (moderate to severe), over 18 years old, no eye injuries, and the consent provided by the patient or their companions to participate in the study. If ICP was suspected for other reasons such as a brain tumor, the patient was excluded from the study and replaced with another case.
After obtaining the consent of the companions or patients eligible to enter the study, first patients’ demographic and clinical characteristics were recorded. They were classified in terms of the severity of TBI according to the GCS. GCS scores of 13–15, 9–12, and 8 or less were regarded as mild, moderate, and severe brain damage, respectively.[17,18]
Furthermore, during the initial examination, the ONSD was measured by a trained and experienced physician, and the average ONSD values measured for both eyes were recorded. ONSD was measured using an ultrasound device (GE Voluson E6) in such a way that first, the patients were in the supine position with their head elevated up to 20 degrees, and if necessary, the patients were sedated using 0.5–10 mg midazolam intravenously before performing the ultrasound.
It should be noted that the prescribed dose of midazolam was determined by an emergency medicine specialist based on the age and weight of the patient and the desired level of sedation.
To prevent any pressure on the eye, a thick layer of gel was rubbed on the closed upper eyelid, then a linear prop of 6.5–7.5 MHz was placed on the temporal surface of the eye and the gel, and ultrasound was performed. It should be noted that if the patient had a life-threatening condition, an ultrasound was performed after a CT scan.
In the next stage, brain CT scans were performed for patients according to the treatment protocol, and CT scan findings such as midline shift, intraventricular hemorrhage (IVH), traumatic SAH, subdural hematoma (SDH), epidural hematoma, intracerebral hemorrhage, and cerebral hemorrhagic contusion were recorded. Then, the patients’ RCTS score was determined [Table 1].
Table 1.
Determination and classification of RCTS score
| 1. Basal cistern effacement |
| 0=none |
| 1=partially effaced (compressed) |
| 2=completely effaced (compressed) |
| 2. Midline shift |
| 0=no shift or <=5 mm |
| 1=>5 mm |
| 3. EDH (epidural hematoma) |
| 0=EDH present |
| 1=no EDH |
| 4. IVH (intra-ventricular hemorrhage) or SAH (subarachnoid hemorrhage) |
| 0=neither present |
| 1=either present |
| 2=add 1 to score |
| Total score=1-6 point |
Moreover, the total disability level of the patient during discharge from the hospital was measured and recorded using the Glasgow outcome scale (GOS) [Table 2], in which scores 1, 2, and 3 were considered as the undesirable level of the patient condition and scores 4 and 5 were regarded as the desirable level of the patient condition.[19]
Table 2.
Glasgow Outcome Scale (GOS)
| GOS Category | Description |
|---|---|
| 1. Death | Severe injury or death without recovery of consciousness |
| 2. Persistent vegetative state | Severe damage with prolonged state of unresponsiveness and a lack of higher mental functions |
| 3. Severe disability | Severe injury with permanent need for help with daily living |
| 4. Moderate disability | No need for assistance in everyday life, employment is possible but may require special equipment. |
| 5. Low disability (good recovery) | Light damage with minor neurological and psychological deficits. |
Finally, the patient outcome, i.e., death or survival, was followed up and recorded six months later.
The collected data was entered into SPSS software (Ver. 25). Data was presented as means ± standard deviation (SD) or n (%). The independent samples t-test and Chi-square test were used at the level of inferential statistics. In addition, ROC analysis was used to evaluate the diagnostic value. A significance level of less than 0.05 was considered in all analyses.
RESULTS
In the present study, out of 142 patients with brain trauma with a mean age of 41.96 ± 11.42 years, 95 (66.9%) and 47 (33.1%) were male and female, respectively. 18.3% of the mentioned patients died after six months. Demographic and clinical factors such as gender, age, midline shift, IVH, and SAH were significantly associated with patient mortality (P value < 0.05). In addition, the median RCTS score in deceased patients was higher than that of the survived patients (median (IQR): 3 (1–4) vs. 2 (1–3); P value < 0.001). The median GOS was lower in deceased patients as compared with survived patients (median (IQR): 3 (1–3) vs. 4 (3–4); P value < 0.001) [Table 3].
Table 3.
Baseline and clinical characteristics of patients based on their outcome
| Characteristics | Total | Deceased (n=26) | Survived (n=116) | P |
|---|---|---|---|---|
| Sex | ||||
| Male | 95 (66.9%) | 10 (38.5%) | 85 (73.3%) | 0.001 |
| Female | 47 (33.1%) | 16 (61.5%) | 31 (26.7%) | |
| Age; year | 41.96±11.42 | 46.46±10.85 | 40.96±11.35 | 0.026 |
| CT findings | ||||
| Midline shift | 41 (28.9%) | 12 (46.2%) | 29 (25.0%) | 0.031 |
| IVH | 31 (21.8%) | 14 (53.8%) | 17 (14.7%) | <0.001 |
| SAH | 25 (17.6%) | 12 (46.2%) | 13 (11.2%) | <0.001 |
| SDH | 47 (33.1%) | 8 (30.8%) | 39 (33.6%) | 0.780 |
| EDH | 50 (35.2%) | 9 (34.6%) | 41 (35.3%) | 0.944 |
| CHC | 76 (53.5%) | 14 (53.8%) | 62 (53.4%) | 0.971 |
| Need surgery | 82 (57.7%) | 16 (61.5%) | 66 (56.9%) | 0.665 |
| RCTS | ||||
| Median (IQR) | 2 (1-3) | 3 (1-4) | 2 (1-3) | <0.001 |
| 1 | 56 (39.4%) | 4 (15.4%) | 52 (44.8%) | |
| 2 | 35 (24.6%) | 2 (7.7%) | 33 (28.4%) | |
| 3 | 31 (21.8%) | 8 (30.8%) | 23 (19.8%) | |
| 4 | 20 (14.1%) | 12 (46.2%) | 8 (6.9%) | |
| GOS | ||||
| Median (IQR) | 4 (3-4) | 3 (1-3) | 4 (3-4) | <0.001 |
| 1 | 15 (10.6%) | 11 (42.3%) | 4 (3.4%) | |
| 2 | 0 (0%) | 0 (0%) | 0 (0%) | |
| 3 | 36 (25.4%) | 9 (34.6%) | 27 (23.3%) | |
| 4 | 61 (43%) | 3 (11.5%) | 58 (50.0%) | |
| 5 | 30 (21.1%) | 3 (11.5%) | 27 (23.3%) | |
| GCS | ||||
| <13 | 102 (71.8%) | 93 (80.2%) | 9 (34.6%) | <0.001 |
| ≥13 | 40 (28.2%) | 23 (19.8%) | 17 (65.4%) | |
| ONSD | ||||
| Right | 6.76±0.32 | 6.87±0.27 | 6.74±0.33 | 0.034 |
| Left | 6.75±0.28 | 6.89±0.25 | 6.72±0.27 | 0.005 |
| Average (Both eyes) | 6.76±0.29 | 6.88±0.25 | 6.73±0.29 | 0.017 |
IVH: Intraventricular hemorrhage, SAH: Subarachnoid hemorrhage, SDH: Subdural hematoma, EDH: Epidural hematoma, CHC: Cerebral hemorrhagic contusion were recorded; ONSD: optic nerve sheath diameter; RCTS: Rotterdam CT scoring; GCS: Glasgow coma scale; GOS: Glasgow outcome scale
In addition, the right and left ONSD values in deceased patients with the means of 6.87 ± 0.27 mm and 6.89 ± 0.25 mm were higher than those of the survived patients with the means of 6.74 ± 0.33 mm and 6.72 ± 0.27 mm, respectively (P value < 0.05). It is significant to note that considering the results of the independent samples t-test revealing no significant difference between the ONSD values of the patient’s right and left eyes (P value > 0.05) [Figure 1], the mean ONSD of two eyes was considered as the addressed ONSD value in this study. The ONSD value of the deceased patients with a mean of 6.88 ± 0.25 mm was significantly higher than that of the survived patients with a mean of 6.73 ± 0.29 mm [Table 3].
Figure 1.
Comparison of the average ONSD of right and left eyes in general and by patient outcome. ONSD: optic nerve sheath diameter
The diagnostic value of the RCTS score in the prognosis of mortality had a cut-off value of greater than 2, a sensitivity of 76.92%, and a specificity of 73.28%. Moreover, the diagnostic value of the RCTS score in the prognosis of the undesirable level of the patient condition had a cut-off value of greater than 2, a sensitivity of 80.39%, and a specificity of 89.01% (P value < 0.001) [Table 4].
Table 4.
Diagnostic value of RCTS score and ONSD value in the prognosis of mortality and disability level of studied patients
| Variables | Parameters of ROC | Mortality | Disability level* |
|---|---|---|---|
| Rotterdam CT Scoring System | AUC [95% CI] | 0.78 [0.67-0.89] | 0.88 [0.82-0.94] |
| P | <0.001 | <0.001 | |
| Cut off point | >2 | >2 | |
| Sensitivity, [95% CI] | 76.92[56.4 - 91.0] | 80.39[66.9 - 90.2] | |
| Specificity, [95% CI] | 73.28[64.3 - 81.1] | 89.01[80.7 - 94.6] | |
| PPV, [95% CI] | 39.2[25.8 - 53.9] | 80.4[66.9 - 90.2] | |
| NPV, [95% CI] | 93.4[86.2 - 97.5] | 89.0[80.7 - 94.6] | |
| ONSD | AUC [95% CI] | 0.68[0.57-0.79] | 0.80[0.73-0.87] |
| P | 0.0017 | <0.001 | |
| Cut off point | >6.8 | >6.9 | |
| Sensitivity, [95% CI] | 88.46[69.8 - 97.6] | 68.63[54.1 - 80.9] | |
| Specificity, [95% CI] | 40.52[31.5 - 50.0] | 82.42[73.0 - 89.6] | |
| PPV, [95% CI] | 25.0[16.6 - 35.1] | 68.6[54.1 - 80.9] | |
| NPV, [95% CI] | 94.0[83.5 - 98.7] | 82.4[73.0 - 89.6] |
*: The disability level was determined according to the GOS criteria such that the values of 1, 2, and 3 indicate the undesirable levels, and values 4 and 5 show desirable levels of the patient. ONSD: optic nerve sheath diameter; RCTS: Rotterdam CT scoring; PPV: positive predictive value, NPV: negative predictive value, AUC: area under the ROC curve
In addition, the ONSD value in the prognosis of the undesirable level of the patient condition had a cut-off value of greater than 6.9 mm, a sensitivity of 68.63%, and a specificity of 82.42%. Moreover, its cut-off value in the prognosis of patient mortality was > 6.8 mm with the sensitivity and specificity of 88.46% and 40.52%, respectively. Statistically, this criterion can be acceptable and significant in the prognosis of the undesirable condition and mortality of patients (AUC: mortality = 0.68, disability = 0.80; P value < 0.001) [Table 4]. The comparison of the diagnostic value of the RCTS criterion and the ONSD value indicated that generally, the RCTS criterion had a better diagnostic value than ONSD in the prognosis of the disability level and mortality of the patients (P value < 0.05) [Figure 2].
Figure 2.
The ROC curve to compare the diagnostic value of RCTS score and ONSD value in the prognosis of mortality (a) and disability level (b) of patients. ONSD: optic nerve sheath diameter. RCTS: Rotterdam CT scoring
DISCUSSION
The results of the present study revealed that 18.3% of 142 patients with TBI passed away. More than 50% of the deceased patients were women and the mean age of these patients was more than that of the surviving patients. CT findings of these patients indicated that findings such as IVH, SAH, and midline shift were significantly higher in the deceased patients as compared with the surviving patients. It may be stated that these CT findings were significantly associated with the mortality of these patients. Moreover, the GOS criterion in determining the level of disability showed that the GOS score was significantly lower in deceased patients. It should be noted that the lower score of this criterion indicates the more undesirable patient’s condition.
Thus, although many factors can increase the chances of mortality and worsen patients’ condition, these factors are unavoidable.[20] From researchers’ perspective, achieving an appropriate and reliable criterion that can be a good predictor of patient outcome despite the existence of these factors is of higher significance to more consciously and properly manage these patients, perform the necessary activities, and prevent any unfavorable outcome for the patient.
In this regard, many researchers have paid due attention to the RCTS score. In this study, the mean RCTS score in the deceased patients was significantly higher than that of the surviving patients. The diagnostic value of this criterion in the prognosis of mortality had a cut-off value of greater than 2, a sensitivity of 76.92%, and a specificity of 73.28% and in the prognosis of the undesirable level of the patient’s condition had the cut-off value of greater than 2, the sensitivity of 80.39%, and the specificity of 89.01%.
In line with the findings of the present study, some other studies have evaluated the prognostic value of RCTS in the mortality of patients with severe head trauma after six months[15] and in 30-day mortality in patients requiring craniotomy[14] and have revealed that this criterion can be useful in predicting premature mortality.
Another study indicated that the increase in RCTS continued to be significantly associated with mortality in patients with TBI after adjusting for confounding variables.[20]
Moreover, the mean ONSD of the right and left eyes in deceased patients was significantly higher than that of the surviving patients in our study. It should be mentioned that there was no significant difference between the ONSD values of the two eyes so the average of these two values was considered as the ONSD value. The mentioned value was also higher in the deceased patients.
Consistent with the findings of the present study, many previous studies have not found a difference between the ONSD value of the right and left eyes and have found a strongly direct and significant association between the obtained values right and left of ONSD. Therefore, many studies have used the average ONSD of the two eyes as the ONSD value.[13,21]
In addition, the diagnostic value of ONSD in the prognosis of mortality of patients had a cut-off point >6.8 mm, a sensitivity of 88.46%, and a specificity of 40.52% and in the prognosis of the undesirable condition of patients had the cut-off value of greater than 6.9 mm, the sensitivity of 68.63%, and the specificity of 82.42%. It can be stated that measuring ONSD can be an acceptable factor in predicting the patient’s condition and outcome.
Various studies have been performed on the diagnostic value of ONSD in diagnosing ICP and the outcome of different types of patients. For instance, a study conducted by Dehnadi Moghadam et al.[10] revealed that ONSD above 7.25 mm is 100% sensitive and 95% specific in the diagnosis of the ICP above 15 mmHg.
Based on the results of some other studies, it was found that the average ONSD in patients without radiological signs of increased ICP was about 4.4 mm, and in patients with radiological signs of increased ICP was 6.3 mm with the specificity and the negative predictive value of 90% and 100%, respectively.[11,12] As mentioned, although some studies have evaluated the association or diagnostic value of ONSD with ICP, some other studies have evaluated the association or diagnosis of ONSD with patient outcomes. For example, Sekhon et al.[20] have shown that a 1 mm increase in ONSD increased the chance of mortality in TBI patients by 2.1 times. In other words, there was a direct and significant association between the ONSD value and the incidence of mortality in these patients.
Finally, the comparison made between the RCTS criterion and the ONSD value in our study showed that although both criteria had an acceptable diagnostic value in predicting the patient outcome and disability level, RCTS was preferable to ONSD as the area under the curve obtained from the Receiver operating characteristics (ROC) analysis in RCTS was higher than that of the ONSD.
In this regard, Waqas et al.[14] evaluated the RCTS criterion and ONSD value as predictors of patient outcome in need of craniotomy and found that the area under the ROC curve for the average ONSD as a predictor of mortality was significantly different between survivors and non-survivors. In addition, RCTS was able to significantly predict the 30-day mortality. Thus, they concluded that, unlike RCTS, the high ONSD value as a predictor could not accurately report mortality outcomes.
Das et al.[16] revealed that the average ONSD in mild brain trauma and RCTS of 2 and 3 were 3.3 and 4.1 mm, respectively. In addition, the mean ONSD in moderate to severe brain trauma (RCTS ≥ 4) was equal to or greater than 4.83 mm. Therefore, the average ONSD was directly and significantly associated with the RCTS criterion such that the RCTS score increased with the increase of ONSD. In line with the present study, the mentioned study also found the accuracy of RCTS to be more than that of ONSD.
Therefore, considering that there is a positive relationship between the increase in ICP and the amount of ONSD, it can be said that the increase in ONSD can be a warning for the increase in ICP. Therefore, its timely control can reduce complications and improve cerebral blood pressure and cerebral blood flow.
So far, both RCTS and ONSD criteria have been evaluated as independent predictors among patients with traumatic brain injury. The deterioration of RCT scores or the increase of ONSD can be independent predictors of poor outcomes. According to previous studies, the non-critical RCT score corresponded with normal ONSD and the deterioration of RCT scores was compatible with the gradual increase of ONSD. The higher the ONSD, the greater the severity of the traumatic brain injury and the more critical the TBI.[16]
Disadvantages of using CT imaging include the lack of real-time measurements and the difficulty in obtaining repeated measurements, radiation exposure, and cost. In this study, we suggested that it is better to record ONSD in the admission CT report so that it is possible to monitor ONSD sequentially using ultrasound to evaluate ICP changes from the beginning. This suggests that a sequential increase in ONSD, indicative of ICP, also implies an increase in RCT score. Therefore, this method can be used in developing countries and hospitals, where ICP monitors are unavailable or expensive.
It should be noted that lack of examination of the relation of neurological outcomes, lack of ICP assessment, GOS, and RCTS scoring by only one assessor (no possibility of inter-rater variability), and a lack of comparison with the control group to estimate normal ONSD are among the limitations of this study. In addition, although not assessing ICP may be a limitation of the present study, its measurement could not lead to new results owing to the large number of studies in this regard. However, it should be noted that considering the direct association between ONSD and RCTS, it may be possible to identify the deterioration of the patient’s condition as soon as possible and perform effective activities to prevent patient mortality by measuring ONSD by ultrasound on the patient’s bedside in cases where RCTS assessment is difficult or impossible. Another noteworthy point is that it may not be possible to determine the exact value of ICP in some medical centers owing to insufficient facilities, so the use of alternative criteria such as RCTS or ONSD can be a good choice in the prognosis of the disability level and the prevention of patient mortality. Therefore, the mentioned point indicates the strength of the present study as few studies have focused on the diagnostic value of ONSD in the patient outcome. However, it is suggested that future studies employ larger sample sizes and address other types of diseases so that the diagnostic value of ONSD can be more conclusively commented on in the prognosis of the patient’s condition and outcome.
CONCLUSION
According to the results of the present study, the mean values of RCTS and ONSD in deceased TBI patients were significantly higher than those of survived patients. In addition, although the RCTS criterion and the ONSD value both had an acceptable diagnostic value in predicting mortality and disability levels in patients with TBI, the RCTS criterion was more accurate than the ONSD. Considering the acceptable value of ONSD in the diagnosis of ICP, the importance of its early diagnosis and to reach more definitive results in all types of diseases with TBI and possible ICP, it is suggested to conduct more prospective studies to confirm the findings or to use a combination of RCTS and ONSD to improve predictions.
Ethics approval and consent to participate
This study approved by Ethics Committee of Isfahan University of Medical Sciences (Code: IR.MUI.MED. REC.1398.115).
Conflicts of interest
There are no conflicts of interest.
Funding Statement
Nil.
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