Cerebral Critical Closing Pressure in Concomitant Traumatic Brain Injury and Intracranial Hematomas

Abstract

The critical closing pressure (CrCP) is the pressure below which the local pial blood pressure is inadequate to prevent blood flow cessation. The cerebral CrCP in concomitant traumatic brain injury (TBI) and intracranial hematomas (TBI + ICH) remains understudied. The aim was to determine the status of the CrCP at cTBI with and without the ICH development. Material and methods. The results of the treatment of 90 patients with severe to moderate cTBI were studied (male/female – 49:41). The average age was 34.2 ± 14.4 years. Depending on the presence of ICH, patients were divided into two groups. All patients were subjected to transcranial Doppler of the both middle cerebral arteries, and evaluation of mean arterial pressure (MAP). Based on data obtained, the CrCPs were calculated. Significance was preset to p < 0.05. Results. The mean CrCP values in each group appeared to be significantly higher than a referral value (p < 0.05). The mean CrCP values in the peri-focal zone of removed hematoma were significantly higher than in TBI patients without ICH (p = 0.015 and p = 0.048, respectively). Analysis of CrCP values in various types of ICH showed no statistically significant differences (p > 0.05). Discussion. The CrCP significantly differs in the groups of TBI patients with and without ICH. The comparability of the groups in respect to the concomitant injury structure proves that the revealed CrCP changes result from the traumatic compression of the brain.

1. Introduction

Maintaining adequate brain perfusion is the most important goal of the treatment of traumatic brain injury (TBI) [7]. According to current views, cerebral perfusion pressure (CPP) is calculated as the difference between the mean arterial pressure (MAP) and the effective lower cerebral circulation pressure, which is usually represented by intracranial pressure (ICP) [22]. However, as previously described, ICP gradients that develop in a damaged brain seriously complicate the calculation of regional CPP [15]. Previous studies have shown that cerebral microcirculation is more accurately described by the “effective” perfusion pressure or closure margin, which defined as the difference between MAP and the pressure, below which pial blood flow ceases. Previous researchers called this parameter critical closing pressure (CrCP) [5, 20, 21]. They showed that CrCP is a sum of cerebral intraparenchymal pressure, venous pressure in the superior sagittal sinus, and vascular tone tension [30]. Considering that the first two parameters determine ICP, CrCP can be calculated by the following formula [29]: CrCP = ICP + WT – CrCP, critical closing pressure; ICP, intracranial pressure; and WT, vascular tone tension or vascular tone.

The CrCP value is considered a result of smoothing the pulse fluctuations in blood pressure to a level below which an avalanche-like collapse of the microvasculature occurs [25]. It was previously shown that CrCP is significantly correlated with invasive CPP and ICP value measurement [21]. Thus, the determination of CrCP becomes practically essential since it allows noninvasive assessment of cerebral perfusion when invasive ICP monitoring is impossible [4]. CrCP dynamics have been studied in preterm infants [8], hydrocephalus [27], TBI [28], subarachnoid hemorrhage, and cerebral vasospasm [25].

However, the cerebral CrCP in patients with concomitant TBI (cTBI) and intracranial hematomas (ICH) remains understudied. The aim was to determine the status of the cerebral CrCP in cTBI with ICH comparing to TBI without ICH.

2. Methods

This non-randomized single-center retrospective study complies with the Declaration of Helsinki. The protocol was approved by the local Ethics Committee of Regional Hospital named after N.A. Semashko. All the patients gave informed consent to participate in the study.

The inclusion criteria were as follows:

1. Moderate to severe TBI within 21 days after a head injury

2. GCS more than 4 and less than 12

3. The absence of any intracranial volume lesion (Marshall grades I, II, and V)

How about hematoma?

The exclusion criteria were as follows:

1. Younger than 16 years or older 70 years

2. Injury Severity Score (ISS) less than 18

3. Any non-evacuated intracranial volume (Marshall grades III and VI) (ICH, parenchymal lesions, etc.)

4. Cardiovascular injury. Declaration.

2.1. Population

We studied 90 patients with moderate to severe TBI who were treated at the Nizhny Novgorod Regional Clinical Hospital named after N.A. Semashko in 2013–2019. The study involved 49 men and 41 women, with mean age of 34.2 ± 14.4 years. All patients received the therapy according to the Advanced Trauma Life Support protocol and the current TBI guideline [6]. The patients were divided into two groups: the first included 47 TBI patients without ICH, and the second comprised 43 patients with TBI after surgical removal of ICH. According to the Glasgow Coma Scale (GCS), severity was 10.5 ± 2.5 in the first group and 10.7 ± 2.7 in the second group. According to the ISS, severity was 31 ± 9 in the first group and 32 ± 8 in the second group. Among 43 patients of the second group, epidural hematomas were removed in seven patients. Subdural hematomas were removed in 32 patients, and multiple hematomas were removed in four patients. All patients underwent decompressive craniectomy within the first 3 days of the injury. The treatment outcomes were assessed according to Glasgow Outcome Scale Extended (GOS-E) on discharge from the hospital (Table 1).

Table 1.

Clinical outcome (Glasgow Outcome Score Extended)

		Group 1	Group 2
1	Death	4	5
2	Vegetative state	7	5
3	Lower severe disability	6	8
4	Upper severe disability	3	3
5	Lower moderate disability	11	8
6	Upper moderate disability	10	9
7	Lower good recovery	3	3
8	Upper good recovery	3	2
	Total	47 (100%)	43 (100%)

2.2. Critical Closing Pressure

The arterial blood pressure was noninvasively monitored using IntelliVue MP5 (Philips Medizin Systeme, Germany). Cerebral blood flow velocity (CBFV) in both middle cerebral arteries (MCA) was bilaterally measured using ultra-sound Doppler with a 2-MHz probe within 10 min (Sonomed 300 M, Spectromed, Russia) according to Aaslid [1]. We used the neuromonitoring complex “Centaurus” (Ver. 3.0, Privolzhsky Research Medical University, Russia).

CBFV, heart rate, and MAP were simultaneously recorded during at least 10 min at a sample rate of 50 Hz by an A/D converter (AX-21, Nizhny Novgorod, Russia) [26]. PaO2, PaCO2, and core temperature were within normal ranges, and patients were normotensive.

All patients during the study breathe spontaneously and did not require sedation or pharmacological support of the blood pressure. For calculation of the CrCP of cerebral microcirculatory bed, we used the equation proposed by Ogoh [19]:

$$\text{CrCp}=\text{ABPs}-\frac{\text{ABPs}-\text{ABPd}}{\text{Vs}-\text{Vd}}\times \text{Vs}$$

where CrCP – critical closing pressure (mmHg), ABPs – systolic arterial pressure (mmHg), ABPd – diastolic arterial pressure (mmHg), Vs – systolic CBFV (cm/s), Vd – diastolic CBFV (cm/s).

Reference range CrCP was chosen according Ogoh S. as 33 ± 2 mmHg.

2.3. Statistical Analysis

The obtained data had a normal distribution, so they were expressed as the mean ± standard deviation. Statistical analysis was performed using the paired Student’s t-test. Significant p-values were < 0.05. All analyses were performed using the software package Statistica 7.0 (Statsoft Inc., USA).

3. Results

Mean CrCP values in each TBI group (with and without ICH) were significantly higher compared to reference data (p < 0.01). No significant difference was found in CrCP values between the left and right sides in the first group (45.72 ± 12.07 mmHg vs. 44.32 ± 9.83 mmHg, respectively, p = 0.74) (Fig. 1). In the second group, the CrCP on the side of the former hematoma remained significantly higher than on the contralateral side (55.14 ± 18.52 mmHg vs. 45.28 ± 15.63 mmHg, respectively, p = 0.018) (Fig. 2). The intergroup comparison showed no statistically significant differences between the mean CrCP values in group 2 patients on the side opposite to the removed ICH compared to group 1 (p > 0.05). However, on the former ICH side, the mean CrCP values were significantly higher than in TBI patients without ICH (p = 0.015 and p = 0.048). Analysis of CrCP values after surgical removal of various ICH types showed no significant differences (p > 0.05). No significant effects of patient age on the CrCP value were found (p > 0.05).

Fig. 1.

The comparison of CrCP values between the left and right sides in the first group

Fig. 2.

The comparison of CrCP values in the formed hematoma and contralateral side

4. Discussion

A concept that cerebral blood flow ceases when the MAP falls below certain critical value was proposed by Burton [5].

Richards H. et al. noted that when half of the CrCP is reached, the blood flow stops proportionally in half of the total number of capillaries. This demonstrates the importance of CrCP determination as the parameter directly characterizing the state of cerebral microcirculation [11, 14, 23].

To date, several methods have been proposed for measuring CrCP. Most models define CrCP as the linear relationship between MAP and CBFV [11, 23]. However, this method’s main limitation is negative CrCP values obtained at cerebral vasospasm or high PaCO2 levels. Some researchers believe that negative values of CrCP cannot be physiologically interpreted [9, 25]. However, there are also opposite opinions [3, 10]. For example, Baker et al. showed that if diffuse correlation spectroscopy is used instead of ultrasonic Doppler, then negative values are not observed [2]. Moreover, Elizondo L. et al. showed a high correlation (r² = 0.93) between directly measured CrCP by linear regression method and impedance calculated CrCP [8].

This is the first study to validate the CrCP calculation in cTBI with surgically resected ICH. We have shown that the CrCP in CTBI patients significantly exceeds normal parameters. According to Burton, one of the possible causes may be the increasing concentration of catecholamines accompanying the acute stage of CTBI, which leads to the vasospasm and a drop in CrCP [5].

Another reason for the CrCP increase in CTBI might be the rise of the intrathoracic pressure due to lung injury, which was found in our study in all patients. This is consistent with previous research [16, 24, 29].

We have shown that the CrCP significantly differs in TBI patients with and without ICH.

The significant CrCP increase (p = 0.018) on the side of the removed ICH apparently has a complicated genesis. One possible cause is the microvascular vasospasm of pial vessels in the former ICH [25].

However, according to ter Laan M., the ultrasonic Doppler does not enable to assess the spasm on the microvascular vessels [13]. This is limitation of our work. The second possible limitation might be that presumable cerebral blood flow turbulence, caused by proximal vasospasm, impairs the linear relationship between blood pressure and CBFV, thus leading to an underestimation of CrCP [12, 18, 27].

In this study, ICP monitoring was not performed; however, the postoperative CT scans did not identify any intracranial volume lesion in all patients, which may indicate the absence of any interhemispheric ICP gradients [15, 17]. Therefore, the increase in CrCP in the area of the removed ICH (with constant ICP) is, probably, caused by an increase in vascular wall tones, which is consistent with other authors [17, 29].

Thus, we suggest that the changes in cerebral CrCP at cTBI exacerbate even after surgical ICH removal. Our study results provide conditions for a differentiated approach to solving the question on timing of surgical correction of extracranial injuries at polytrauma study.

5. Conclusion

Despite CrCP in patients with combined TBI is significantly increased compared to the normal value. After ICH evacuation, CrCP remains significantly elevated compared to the symmetrical zone in the contralateral hemisphere. Further research is required.