The pathophysiology of traumatic brain swelling remains little understood to date; as a consequence, there are few therapeutic options to control this condition and a number of patients develop increased intracranial pressure (ICP), brain ischemia, and herniation [
To our knowledge, there are no studies concerning disturbances of intracranial circulation associated with the process of brain herniation and refractory intracranial hypertension due to severe traumatic brain swelling. An improved understanding of intracranial circulatory process related to this condition may have treatment implications.
The objective of this study was to investigate the cerebral hemodynamic changes associated with refractory elevated ICP and brain herniation syndrome due to traumatic brain swelling. The relationships between such cerebral hemodynamic patterns and the patients’ outcome, as well as between cerebral hemodynamic patterns and computerized tomography (CT) scan findings, were also verified.
Traumatic brain injury (TBI) patients with clinical and tomographic signs of intracranial hypertension and brain herniation due to uncontrollable brain swelling for whom decompressive craniectomy was indicated and in whom transcranial Doppler (TCD) ultrasonography had been performed were prospectively enrolled. Exclusion criteria were penetrating head injuries, Glasgow Coma Scale (GCS) score of 3 associated with bilaterally fixed and dilated pupils, and impossibility to assess cerebral circulation by TCD ultrasonography. Patients with multisystem trauma were not excluded. Demographic, clinical, and radiological data were collected for every patient. This study was approved by our research ethics committee and conducted according to the Declaration of Helsinki principles.
All patients were managed by a standard regimen based on the guidelines of the American College of Surgeons (Advanced Trauma Life Support) and of the American Association of Neurological Surgeons as described in our previous report [
Clinical evidence of cerebral herniation syndrome consisted of neurological deterioration characterized by decrease in GCS score and/or dilation of pupils that were unresponsive to light, unilaterally or bilaterally, in conjunction with CT evidence of brain herniation characterized by severe diffuse brain swelling or predominantly unilateral diffuse brain swelling associated with mass effect, a shift of midline cerebral structures >5 mm, and/or obliteration of perimesencephalic cisterns. Patients with persisting GCS score of 3 and/or bilaterally fixed and dilated pupils did not undergo decompressive craniectomy and were excluded.
The neurosurgical team was oriented to maintain their routine practice, without waiting for the arrival of TCD physician to avoid any delay in the patients’ treatment. In most instances, TCD measurements were obtained, while the patient waited to go into the operating theater (one case) or while the anesthesiologist prepared the patient in the operating room.
The middle cerebral artery (MCA) and the distal segment of the extracranial internal carotid artery (ICA) were insonated using a portable 2 MHz pulsed TCD device (Pioneer TC 2020 EME; Nicolet Biomedical, Madison, WI) via temporal and submandibular ultrasound windows, respectively. The MCA and extracranial ICA blood flow variables that were recorded and analyzed included the mean velocity (the time mean of the peak velocities over the course of four cardiac cycles) and the pulsatility index (PI = [systolic velocity – diastolic velocity]/mean velocity).
Physiological data, including hematocrit, arterial blood carbon dioxide and oxygen pressures, body temperature, and systemic arterial blood pressure, were documented in each TCD study.
Elevated TCD flow velocities have been found in both cerebral vasospasm and hyperemia. Given that the extracranial ICA is not involved in the spasm process, flow velocity changes within this artery are associated with changes in CBF rather than with changes in arterial diameter [
Patients with hyperemia in both cerebral hemispheres or hyperemia in one cerebral hemisphere and nonspecific circulatory pattern in another hemisphere were considered as presenting cerebral hyperemia. On the other hand, patients with oligoemia in both cerebral hemispheres or oligoemia in one cerebral hemisphere and nonspecific hemodynamic pattern in the opposite hemisphere were defined as having cerebral oligoemia. Patients with hyperemia in one cerebral hemisphere and oligoemia in the contralateral hemisphere were grouped separately.
Information on age, gender, date of accident, time intervals between the accident and hospital admission and between admission and surgical treatment, mechanism of injury, neurological status (GCS score and pupil response) at admission, before, and after decompressive craniectomy, shift degree of midline cerebral structures, associated intracranial lesions, length of hospital stay, and outcome were registered. Outcome was evaluated at 6 months after injury by Glasgow Outcome Scale (GOS) score. Patients with good recovery (GOS score of 5) or with moderate disability (GOS score of 4) were considered as presenting favorable outcome, while patients with severe disability (GOS score of 3) or in a vegetative state (GOS score of 2) or those who died (GOS score of 1) were defined as having unfavorable outcome.
Data were reported as means ± standard deviations. The Mann-Whitney
Nineteen patients with severe traumatic brain swelling and evidence of elevated ICP and transtentorial herniation were included. The mean age of the patients was
Summary of patients’ demographic, clinical, and radiological data*.
Case no. | Age (yrs), Sex | Lesions operated at hospital admission | Interval from admission to TCD | GCS score | Pupils | Midbrain cisterns | Midline shift on CT (mm) | Side of maximal cerebral swelling | CHP | 6-Mo GOS score |
---|---|---|---|---|---|---|---|---|---|---|
1 | 63, F | 6 hours | 6 | Unequal | Absent | 12 | Right | Oligoemia | 1 | |
2 | 18, M | 4 hours | 6 | Unequal | Absent | 16 | Right | Nonspecific | 1 | |
3 | 28, M | 6 days | 6 | Unequal | Absent | 9 | Left | Oligoemia | 5 | |
4 | 39, F | 7 hours | 6 | Unequal | Absent | 11 | Right | Hyperemia | 3 | |
5 | 28, M | 3 hours | 7 | Unequal | Absent | 15 | Right | Oligoemia | 4 | |
6 | 25, M | 4 days | 6 | Unequal | Absent | 12 | Right | Oligoemia | 3 | |
7 | 19, F | ICH | 24 hours | 6 | Unequal | Right | Nonspecific | 4 | ||
8 | 28, F | 2 hours | 6 | Unreactive | Absent | 9 | Left | Oligoemia | 4 | |
9 | 22, M | 2 hours | 6 | Unequal | Absent | 14 | Right | Hyperemia | 2 | |
10 | 25, F | 6 days | 5 | Unequal | Absent | 8 | Right | Oligoemia | 1 | |
11 | 30, M | ICH | 2 days | 6 | Unequal | Absent | 17 | Right | Oligoemia | 1 |
12 | 27, M | SDH | 8 days | 6 | Unequal | Absent | 12 | Right | Nonspecific | 5 |
13 | 17, M | SDH | 3 days | 10 | Unequal | Absent | 5 | Left | Hyperemia | 4 |
14 | 39, M | EDH | 3 days | 12 | Unequal | Right | Oligoemia | 4 | ||
15 | 61, F | ICH SDH | 3 days | 9 | Unequal | Absent | 11 | Left | Oligoemia | 2 |
16 | 51, M | ICH | 4 days | 9 | Unequal | Absent | 19 | Left | Nonspecific | 3 |
17 | 43, M | SDH | 3 days | 6 | Unequal | Absent | 20 | Left | Nonspecific | 1 |
18 | 46, M | SDH | 9 days | 4 | Unequal | Absent | 10 | Right | Oligoemia | 2 |
19 | 23, M | ICH | 1 day | 6 | Unreactive | Absent | 15 | Left | Nonspecific | 3 |
Mean flow velocities in the MCA ranged widely from 8 to 143 cm/s. The average MCA mean flow velocities were
Ten patients (52.7%) were considered as having cerebral oligoemia, 3 patients (15.8%) met the criteria for cerebral hyperemia, and 6 patients (31.5%) were found to present nonspecific circulatory pattern. No patients were found to have hyperemia in one cerebral hemisphere and oligoemia in the opposite hemisphere (Table
Number of patients according to cerebral hemodynamic patterns.
Hemodynamic patterns | No. of patients |
---|---|
Hyperemia | 3 (15.8%) |
Oligoemia | 10 (52.7%) |
Nonspecific | 6 (31.5%) |
In the most swollen cerebral hemisphere, 52.6% of the patients presented MCA mean flow velocities <40 cm/s (cerebral oligoemia), 36.9% between 40 and 100 cm/s (nonspecific hemodynamic pattern), and 10.5% >100 cm/s (cerebral hyperemia). In the opposite side, 17.6% of the patients had MCA mean flow velocities <40 cm/s (cerebral oligoemia), 76.5% between 40 and 100 cm/s (nonspecific hemodynamic pattern), and 5.9% >100 cm/s (cerebral hyperemia) (Table
No correlation was found between cerebral hemodynamic patterns and other variables such as preoperative GCS score, the degree of midline cerebral structures shift on preoperative CT scan, GOS scores at 6 months after injury, and neurological recovery according to favorable (good recovery and moderate disability) or unfavorable outcome (severe disability, vegetative state, or death) at 6 months followup.
We report a series of 19 patients with traumatic brain swelling and evidence of increased ICP and brain herniation, refractory to clinical measures, in whom cerebral hemodynamic assessment by TCD ultrasonography was performed prior to decompressive craniectomy. Participants and their cerebral hemispheres (the side of maximal cerebral swelling and the opposite side) were categorized according to TCD hemodynamic patterns, and the findings correlated with preoperative GCS score, degree of midline cerebral structures shift on preoperative CT scan, GOS scores at 6 months after injury, and 6-month follow-up neurological outcome based on favorable or unfavorable recovery. To our knowledge, this is the first study that systematically evaluated the cerebral blood circulation of patients with traumatic brain swelling leading to uncontrollable raised ICP and brain herniation syndrome. Patients with severe brainstem injury (GCS score of 3 and/or bilaterally fixed and dilated pupils) were excluded from this study; therefore, this investigation refers to patients eligible for treatment. We showed a wide diversity of cerebral hemodynamic findings, ranging from severe oligoemia to hyperemia. Ten patients (52.7%) presented with cerebral oligoemia, 3 patients (15.8%) with cerebral hyperemia, and 6 patients (31.5%) with nonspecific circulatory pattern (Table
Hemodynamic patterns in the most swollen cerebral hemisphere and in the contralateral hemisphere (number of patients versus hemodynamic pattern in TCD). LR: Lindegaard ratio; MCA: middle cerebral artery; BFV: blood flow velocity; TCD: transcranial Doppler ultrasonography; All patients presented LR <3.
A potential criticism of our study is the absence of ICP measurements, quantitative estimations of CBF, cerebral arteriovenous oxygen difference, cerebral metabolic rate of oxygen consumption, and biochemical markers for cerebral ischemia. However, in our department, we have used clinical monitoring, measurements by noninvasive methods, and serial imaging. We have used ICP monitoring only in selected cases with findings suggestive of intracranial hypertension in the neurosonograhic assessment.
The management of severe TBI without ICP monitoring in all patients has been confirmed in the recent study by Chesnut et al. [
For interpreting the results of TCD ultrasonography, it is necessary to consider the possibility that both cerebral hyperemia (elevated CBF) and vasospasm usually occur more noticeably as of 2 days after injury [
Our results failed to demonstrate a correlation between cerebral hemodynamic patterns and GOS scores at 6 months after injury and between cerebral hemodynamic patterns and neurological recovery according to favorable or unfavorable outcomes at 6 months followup, although this fact does not mean that those correlations cannot exist because of the limitations of this investigation which include small patient sample, heterogeneous characteristics of the patient population, coexistence of several prognostic factors, and the complexity of the brain’s hemimetabolic phenomena.
In the Morgalla et al.’s series comprising 33 head-injured patients who underwent decompressive craniectomy, preoperative TCD ultrasonography disclosed high resistance CBF pattern in 24% of patients, systolic spikes in 12% of patients, systolic flow pattern with absent diastolic flow in 57% of patients, and normal TCD flow pattern in 12% of patients [
Interestingly, Morgalla et al. [
Current therapeutic strategy concerning CBF management in head-injured patients is to avoid states of critical cerebral hyperemia and oligoemia [
There is a considerable heterogeneity of cerebral hemodynamic findings among individuals with refractory intracranial hypertension and brain herniation syndrome due to traumatic brain swelling, and also between their cerebral hemispheres. These findings are in accordance with previous publications on TBI, which demonstrated cerebral heterogeneity in terms of circulation, pressure autoregulation, critical closing pressure, oxygenation, and metabolism. This supports the concept of heterogeneous nature of the pathophysiology of the TBI and of the patients’ outcomes, suggesting that therapeutic measures should be planned individually. The recognition of posttraumatic cerebral hemodynamic patterns and their significances is potentially useful for devising more specific therapeutic strategies.
There is no conflict of interests and no financial disclosure in this study.