Correlation of Positive End-Expiratory and Intracranial Pressure Using the Ultrasonographic-Guided Measurement of Optic Nerve Sheath Diameter in Traumatic Brain Injury Patients
Keywords: Cerebral perfusion pressure, intracranial pressure, optic nerve sheath diameter, positive end-expiratory pressure, supine position
Traumatic brain injury (TBI) is a major cause of disablement, decease, and economic burden to our society. The peak incidence of which has been consistently reported in younger age groups. However, in recent times, there has been a declining trend in mortality from 50–25% due to the systematic use of evidence-based protocols that emphasize monitoring and maintaining adequate cerebral perfusion., Protocols that emphasize intracranial pressure (ICP) monitoring have further demonstrated improved outcomes, particularly in TBI patients.,
All body systems need to be addressed as one moves from the initial to the long-term management of the TBI. The initial injury to the brain is truly irreversible by any medical modalities available today. Hence, after the initial resuscitation, medical maneuvers are directed at limiting secondary damage to the brain that occurs in response to inflammatory changes, expanding hematomas, cellular swelling, seizures, and systemic complications (i.e., hemodynamic or pulmonary changes, fever, pain); vulnerable surrounding brain tissue can be damaged through alterations in cerebral perfusion and metabolism. Treatments to address these issues include, though are not limited to, analgesics, sedatives, anticonvulsants, hyperosmotic agents, and hypothermia.,,
Several factors such as traumatically induced masses, cerebral edema, hyperemia, hypoventilation, hydrocephalus, increased intrathoracic, or intra-abdominal pressure often contribute towards increasing the ICP in TBI patients. After the evacuation of traumatic mass lesions, the most important cause of increased ICP was thought to be vascular engorgement leading to cerebral edema. A secondary increase in the ICP often is observed 3–10 days after the trauma, principally as a result of a delayed hematoma formation such as epidural hematomas, acute subdural hematoma, and traumatic hemorrhagic contusions with surrounding edema, sometimes requiring evacuation. Other potential causes of delayed increases in ICP are cerebral vasospasm, hypoventilation, and hyponatremia. In comatose patients, clinical symptoms of increased ICP are impossible to elicit. Papilledema is a reliable sign of intracranial hypertension but is rarely found in head injury having documented elevated ICP.
The anatomy of the optic nerve sheath (ONS) in the optic canal is especially important as it functions effectively as the “access portal” for cerebrospinal fluid (CSF) entering the ONS from the intracranial subarachnoid space (SAS). The thick fibrous bands connecting the dura and pia in the optic canal not only holds the optic nerve firmly in position but also maintains the dura and optic nerve in close proximity. Dilatation of ONS has been shown to be a much earlier manifestation of ICP rise.,,, There has been a good positive correlation of ultrasound-measured optic nerve sheath diameter (ONSD) with ICP, as measured by CSF manometry. It has also shown that an ONSD of >0.63 cm suggests a CSF pressure of >20 cm of water with 77.3% sensitivity and 92.3% specificity.
Mechanical ventilation is often required while managing brain-injured patients. Common indications include pulmonary contusions, airway compromise from depressed mental status, acute respiratory distress syndrome, neurogenic pulmonary edema, pneumonia, and need for sedatives to facilitate procedures and control ICP. One of the established ventilation strategies to improve oxygenation index in lung injury is by recruiting collapsed alveoli through the application of high positive end-expiratory pressure (PEEP). Patients with concurrent TBI and severe acute respiratory distress syndrome present a significant therapeutic challenge, as it may be difficult to maintain adequate oxygenation and an appropriate carbon dioxide level without deleterious ventilator settings. Various strategies have been successfully applied in this patient population like airway pressure release ventilation, prone positioning, and extracorporeal lung support techniques. Optimizing ICP and cerebral perfusion pressure (CPP) is crucial in the management of severe TBI. In trauma patients with TBI and respiratory dysfunction, PEEP is often required to improve oxygenation. At the same time, PEEP may lead to reduced CPP. Therefore, we hypothesized that the increase in PEEP is associated with compromised hemodynamics and altered cerebral perfusion.
In this study, we aim to evaluate the association of PEEP and ICP via measuring ONSD in TBI patients.
After getting approval from the Institutional Ethics Committee, the study was performed on patients admitted to trauma ventilator unit (TVU) trauma center KGMU for traumatic brain injury. Informed consent was taken from the patient's attendant. Patients with age ≥18 years, severe brain injury (GCS 8 or less), receiving mechanical ventilation, initial PEEP ≤4 mmHg and no history of severe cardiopulmonary disease were included in this study. Patients with intracranial hypertension (defined as ICP >20 mmHg) and already receiving PEEP >15 cm H2O at enrollment were excluded from the study.
All ultrasound image-acquisition was performed by a single investigator, experienced in the use of ultrasound. In all cases, patients were being mechanically ventilated. ONSD measurement was performed when hemodynamic parameters were most stable. All ONSD measurements were performed with patients in the supine position, with the head central and elevated to approximately 30°. A clear film protective dressing was placed over both eyes to protect the globe from any potential injury. A layer of coupling gel was applied over the closed upper eyelid. To identify and image the ONS the ultrasound probe with the smallest available footprint. Linear array probe having frequency 7–15 MHz was used in all cases. The positioning of the probe over the eye was always carefully performed. This process included the use of the middle finger and left hand to palpate the bony surface of the superior orbital rim, glabella and inferior orbital rim, to ensure that the application of the probe over the surface of the eyelid never exerted any pressure on the globe itself. This technique is especially important to prevent any pressure being applied on the globe. The probe is usually placed transversally. The depth should be adjusted to optimize the visualization of the intended structures, i.e. the optic nerve, the surrounding CSF space, and the ONS. The gain should be adjusted to create a hypoechoic posterior chamber. If the gain is too high, echoic artefacts could lead to image distortion, and if the gain is too low, image quality can be inadequate. The eye should be examined in at least two planes: the axial or transverse plane, with the probe oriented in the horizontal, left to the right direction; and the sagittal plane, which is imaged by rotating the probe and positioning it in a cranial to caudal orientation. The imaging should be performed in both eyes; area of the upper eyelid for optimal visualization of the ONS.
The depth was set to 4 cm as a default setting and the magnification was then adjusted to provide the best quality imaging for individual patients. ONSD measurement was performed at an angle perpendicular to the optic nerve, at a depth of 3 mm posterior to the lamina cribrosa of the sclera surface. Three measurements were acquired to ensure that the measurements could be appropriately analyzed for correlation and accuracy. The mean binocular ONSD measurement for each patient was then obtained and was used for comparing the ICP change. The digital calliper measuring tool on the ultrasound machine was used to measure the ONSD.
Similar reading was taken after increasing PEEP to 5, 10, 15 cm H2O in ventilator settings. Systolic, diastolic mean blood pressure, heart rate, saturation, and ventilator parameters were recorded before each reading. ONSD measurements were taken 5 min after changing PEEP in ventilator settings.
For the control group, 40 patients admitted in ICU were taken which were not the case of TBI patients but were mechanically ventilated with GCS less than 8. A similar procedure was done on increasing PEEP and measuring ONSD.
The demographic profile such as age and gender were comparable in between groups. The ONSD and ICP did not increase significantly when PEEP increased from 0–5 cm H2O and 5–10 cm H2O, though the increase was highly significant when PEEP increased from 10–15 cm H2O. Moreover, this increase is much greater in cases as compared to controls [Figure 1].
There was no significant difference noted while comparing measurements of ONS diameter in both eyes at all PEEP values in cases as well as control patients [Table 1].
There was a significant positive correlation between left and right ONSD values and PEEP. Karl Pearson's correlation coefficient was 0.856 and 0.868 for left and right ONSD, respectively [Table 2].
We observed an increase in heart rate values however, it was not a statistically significant difference. MAP decreased with an increase in PEEP value. The highly significant decrease occurred in MAP change from PEEP 10–15 in cases (P < 0.001) and control (P < 0.001) and these changes were pronounced in cases as compared to controls [Figure 2].
We observed a significant increase in CVP with an increase in PEEP values and these changes were greater in cases as compared to controls [Figure 3].
Various studies show that the effect of PEEP on the intracranial system has focused mainly on ICP, showing conflicting results.,,, It is still a global debate as to what should be the maximum level of PEEP that can correct hypoxemia without escalating ICP in patients with severe TBI. Although, there are few studies defining the optimal PEEP in adult patients. The PEEP value of 10 cm H2O slightly increased ICP and was clinically safe for adult patients with severe TBI. Moreover, the PEEP value up to 15 cm H2O did not significantly increase ICP or decrease CPP. Another study reported that there was no change in ICP even with PEEP as high as 40 cm H2O. On the contrary, the ICP increase of 10 mmHg or more after the administration of 4–8 cm H2O of PEEP along with a CPP decrease in 50% of the cases. PEEP was raised from 5 (basal) to 15 cm H2O in steps of 5 cm H2O, at 10 and 15 cm H2O produced a significant increase in ICP without a change in CPP.,
This is the first study to determine the effect of three sequentially increasing PEEP values (5, 10, and 15 cm H2O) primarily on ONSD in patients with severe TBI. Our results showed that both ONSD and ICP did not increase significantly when PEEP increased from 0–5 cm H2O and 5–10 cm H2O though the increase was highly significant when PEEP increased from 10–15 cm H2O. In addition, this increase is much greater in cases as compared to controls as patients of traumatic brain injury have impaired cerebral blood flow autoregulation.
In this study, the ONS diameter of both eyes was not significantly different at all PEEP values in between cases and controls. Similarly, the ONS diameter of both eyes was comparable in healthy volunteers in Bangladesh population. Previous studies also found similar results in a healthy population (infants and children and adults) in the right and left eye ONSD.,
In this study, we also studied the effects of increasing PEEP on heart rate, MAP, central venous pressure, peak airway pressures, and plateau pressures. Depending on the compliance of the lung parenchyma, high levels of PEEP increase intrathoracic pressure. This raises right atrial pressure and reduces the pressure gradient driving a venous return to the heart which, in turn, decreases systemic venous return and ventricular preload. If the reflex increase in heart rate is unable to compensate for this phenomenon, cardiac output falls and systemic hypotension may ensue.,
In our study, we observed an increase in heart rate values however, it was not a statistically significant difference. However, this increase in heart rate was consistent with previous findings., Previously, Viquerat et al. and Khandelwal et al., observed no significant change in heart rate with PEEP as compared to baseline values., Leech et al. found no significant effects on heart rate, PAP, ventricular size, or cardiac index assessed noninvasively with increasing positive intrathoracic pressures.
In our study, the MAP significantly decreased with increase in PEEP value from 10–15 cm in cases and controls. Angerpointner et al. (1977) observed in their study depression in stroke volume, cardiac output, peak aortic blood flow, arterial blood pressure, and peak left ventricular power even at 5 cm H2O PEEP and with higher PEEP levels and these effects were more pronounced. Algera et al. (2018) also mentioned the decreased cardiac output and hypotension seen with increasing peep in their article. However, Viquerat et al. (1983) and Khandelwal et al. (2018) observed that the hemodynamic parameters were comparable to baseline values during the sequential increase of PEEP., Similarly, Méndez et al. (2017) observed that different PEEP levels reduced cardiac output without changes in PaO2/FiO2 ratio, ScvO2, or hemodynamic values (heart rate or mean arterial pressure).
PEEP in patients under mechanical ventilation can affect CVP via increasing intrathoracic pressure. Various reports exist on the direct relationship between PEEP and CVP. Shojaee et al. (2017) revealed the direct relationship between PEEP and CVP stating that approximately, a 5 cm H2O increase in PEEP will be associated with about 2.5 cm H2O raise in CVP. In a study by Yang et al. (2011) observed that 1 cm H2O increase in PEEP led to 0.38 cm H2O increase in CVP. Cao et al. stated that CVP increased when PEEP is set > or = 10 cm H2O in mechanically ventilated patients, whose circulatory status is steady and who do not have a cardiopulmonary ailment or abdominal distention. Evaluating the effect of PEEP on CVP and stroke volume in 20 patients with cardiac diseases, Geerts et al. (2010) revealed that PEEP significantly affects CVP, while no significant relationship was detected between heart rate and MAP. Results of our study are consistent with the abovementioned studies and we observed a significant increase in CVP with an increase in PEEP values and these changes are greater in cases as compared to controls.
There are certain limitations of our study such as we acknowledge that lack of invasive ICP measurement limited the ability to interpret the accuracy of ONSD measurement. Moreover, we have not considered the clinical outcome, morbidity, and mortality of patients associated with raised ICP. In addition, longer and multicenter studies would be useful in confirming these findings.
We conclude that the PEEP up to 10 cm H2O can be safely applied in patients with TBI. Further increment of PEEP might improve oxygenation but at the cost of accentuation of ICP. At present, it is difficult to comment on whether such increment of ICP resulting from PEEP application has any bearing on clinical outcome. Large trials are required to further validate the effect of PEEP on ICP in patients with TBI.
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Conflicts of interest
There are no conflicts of interest.
[Figure 1], [Figure 2], [Figure 3]
[Table 1], [Table 2]