Abstract
Introduction.
The knowledge of the conservative treatment modalities for chronic subdural hematoma (CSDH) is still based on low-grade evidence The purpose was to study the condition of the microcirculation and autoregulation in the perifocal CSDH zone for understanding the mechanism of CSDH development.
Methods.
Cerebral microcirculation was evaluated in patients with the aid of brain perfusion computed tomography (PCT) within the first day. Perfusion parameters were assessed quantitatively in the cortex zone adjacent to the CSDH and in a similar zone of the contralateral hemisphere. The same PCT data were assessed quantitatively without and with the use of the perfusion calculation mode excluding large vessels voxels ‘Remote Vessels’ (RV), 1st and 2nd method, respectively.
Results.
The 1st method of analysis of a similar zone in the contralateral hemisphere revealed a significant increase in CBV and CBF (p <0.01) compared to normal values. The use of the 2nd method with RV showed no significant changes in the perfusion parameters in the microcirculatory blood flow of the cortex on the contralateral to the hematoma side.
Conclusion
The persistence of the microcirculatory blood flow perfusion reflects the preservation of the cerebral blood flow autoregulation in patients with chronic subdural hematomas.
Keywords: chronic subdural hematoma, perfusion computed tomography, cerebral autoregulation
Introduction
A chronic subdural hematoma (CSDH) is a common neurosurgical disease characterized by the formation of a capsule around subdural hemorrhage, causing local compression of cerebral tissue [1]. CSDHs are usually formed in elderly patients after non-severe traumatic brain injury [2]. Risk factors for its development are age, alcoholism, use of anticoagulants and coagulopathy. Key factors determining the course and clinical outcome of CSDH are reactions of microcirculation bed in the underlying region of the cerebral cortex, so-called perifocal zone [3]. The results of a few investigations about the state of global and local cortical perfusion, as well as about the state of autoregulation in this zone are contradictory. Commonly, the study of cerebral blood flow is done by xenon-enhanced and perfusion computed tomography (PCT). However, the imperfections in existing software for cerebral perfusion quantification during computed tomography [4] lead to contradictory results. At the same time, the introduction of CT algorithms that exclude voxels with blood flow in the cortical vessels makes it possible to assess the state of pial blood flow in the “region of interest” without an admixture of large vessels flow data [5]. Thus, it becomes possible to assess the cerebral blood flow and the autoregulation status in the perifocal zone of CSDH, because the knowledge of the conservative treatment modalities for CSDH is sparse and based on small case series and low-grade evidence [12].
The purpose of this work was to study cerebral microcirculation and autoregulation in the perifocal CSDH zone based on the analysis of perfusion computed tomography (PCT) for understanding the mechanisms of CSDH development.
Materials and Methods
This retrospective observational non-randomized single-center study was conducted as an analysis of a prospectively maintained database cohort (2016-2018) and included patients in the subacute stage of severe polytrauma and head injury. The protocol of the study was reviewed and approved by the Institutional Ethical Committee and conformed to the standards of the Declaration of Helsinki. All the patients gave informed consent to participate in the study. Twenty patients with CSDH after polytrauma (January 2016 – July 2018) were included in the study. The inclusion criteria were: 1) CSDH on CT or magnetic resonance scans, 2) indication for surgery; 3) signed informed consent to participate in the study and 4) baseline PCT. We excluded patients who had the following: 1) age younger than 16 years; 2) bilateral CSDH; 3) serum blood creatinine level >120 mmol/L and 4) acute deterioration necessitating decompressive craniotomy. The study was performed under an approved institutional review board guideline as part of a multicenter study of the results of conservative and surgical CSDH treatment in the chronic stage of concomitant TBI.
All patients underwent craniotomy with a burr hole under the navigation by Sina App (Sina Intraoperative Neurosurgical Assist). The cavity of CSDH was washed out with a warm isotonic saline solution. The drainage catheter (Pleurofix® B. Braun Melsungen AG, Germany) was placed in the cavity of CSDH for 48 days. All patients underwent PCT within the first day before surgery. CTP was performed on CT scanner Philips Ingenuity CT® (Philips Medical Systems, Cleveland, USA). We used the following scan parameters: 160-mm coverage in the z-axis, 80 kV, 150 mA, effective dose = 3.3 mSv, slice thickness = 5 mm, collimation = 64 × 0.625 mm. Total acquisition time was 60 seconds (30 consecutive spiral acquisitions of 2 seconds each). 50 mL of Ultravist 370 (Schering AG, Germany) was injected intravenously through a 20 G catheter by an automatic syringe-injector (Stellant, One Medrad, USA). CTP data were processed using Philips Ingenuity Core workstation (Philips Healthcare Nederland B.V., the Netherlands, 2013, v.3.5.5.25007). First, the arterial input function was detected automatically using a cluster-analysis algorithm. This arterial input function was subsequently used by the Bayesian probabilistic method to generate the perfusion parametric maps. Color-coded perfusion maps were produced to describe cerebral perfusion: cerebral blood volume (CBV), cerebral blood flow (CBF), mean transit time (MTT), and time to peak concentration of the contrast (TTP). The same PCT data were assessed quantitatively in cortical brain region beneath the CSDH (zone 1), and in the corresponding contralateral brain hemisphere (zone 2) without and with use of the perfusion calculation mode excluding vascular voxel ‘Remote Vessels’ (RV), 1st and 2nd analysis method, respectively. Quantitative perfusion indices, including CBF, were calculated on a voxelwise basis and were used to generate color-coded maps. The voxels with CBF >100 mL/100 g/min or CBV >8 mL/100g were assumed to contain vessels and removed from the perfusion map [6]. Statistical analysis was performed using the paired Student’s t-test. Data are shown as a mean ± standard deviation. P<0.05 was considered statistically significant.
Results.
Sex distribution had a male predominance (8 women, 12 men). The mean age was 54.7±15.6 (range 17-87) years. The CSDH mainly located in the left hemisphere (11 patients). The average volume of the CSDH was 84.2±12.4 (range 55-113) cm3. The mean midline shift was 9.1±1.2 (range 7-12) mm. The level of wakefulness according to the Glasgow Coma Score was 13.1±0.5 (range 10-15) and Markwalder level was 1.8±0.5 (range 0-3). The acquired and analyzed data are summarized in Table 1. Comparison with normal values for perfusion indices [7] in the zone 1 in the calculation algorithm with the flow in cortical vessels (1st analysis method) showed a significant (p <0.01) increase in CBV and CBF, and no significant increase in MTT and TTP (p >0.01). However, when vascular voxels were excluded by RV mode (2nd analysis method), the comparison of perfusion parameters in zone 1 with normal values showed nonsignificant changes (p >0.01). In the zone 2 (contralateral side), the comparison with normal values for perfusion indices revealed in the 1st analysis method a statistically reliable increase in CBV and CBF (p <0.01), but the changes of MTT and TTP also were nonsignificant. At the same time, the use of the 2nd analysis method showed no statistically reliable change of perfusion parameters (p >0.01) on zone 2.
Table 1.
Data of the analyzed parameters.
| CBF (ml/100 g x min) | CBV (ml/100 g) | TTP (sec) | MTT (sec) | ||
|---|---|---|---|---|---|
| 1 | 1st analysis method (zone 1 without RV) | 148.97±32.98 | 10.98±2.79 | 28.58±0.79 | 4.23±0.63 |
| 2 | 1st analysis method (zone 2 without RV) | 123.15±29.51 | 9.28±2.25 | 27.72±1.17 | 4.61±0.77 |
| 3 | 2nd analysis method (zone 1 with RV) | 87.97±15.95 | 5.57±0.91 | 26.45±0.81 | 3.14±0.59 |
| 4 | 2nd analysis method (zone 2 with RV) | 74.88±21.02 | 5.14±0.76 | 28.06±1.28 | 4.11±0.85 |
| 5 | Normal value [10] | 64.02±0.6 | 4.6±0.8 | - | 4.3±0.8 |
| P (1-2) | 0.011 | 0.041 | 0.521 | 0.532 | |
| P (1-3) | <0.001* | <0.001* | 0.702 | 0.004* | |
| P (2-4) | 0.002* | <0.001* | 0.704 | 0.049 | |
| P (3-4) | 0.047 | 0.091 | 0.192 | 0.321 |
Significant difference (p<0.01).
Discussion
The main property of the brain circulation – cerebral autoregulation, is the ability to maintain constant cerebral perfusion under fluctuating mean arterial and intracranial pressure [8]. It was noted that indicators of cerebral perfusion and the state of autoregulation are in close interdependence and microvasculature perfusion disorders result from damage to the autoregulation mechanisms [9,10]. It has been proposed that CSDH disrupts the mechanisms of cerebral blood flow autoregulation, as evident through cerebral microcirculation disorders with the development of congestion and hyperperfusion syndromes. Thus, there was a fair increase in CBV as compared to the symmetrical zones of the opposite hemisphere, while time characteristics have not significantly changed corresponding to congestion and hyperperfusion patterns, indicating cerebral autoregulation disorder [3,1]. Nevertheless, these findings, as well as the fact that the studies were carried out without using algorithms, appeared to be the basis for critical comments on the work. In our study, we used a CT analysis algorithm that excludes pixels from large vessels thus enabling to adequately assess perfusion in the pial bed of the perifocal zone of the CSDH. We think that we can use the 2nd algorithm in the «intact» hemisphere because microcirculation in this area is also abnormal in patients with CSDH. Microcirculatory disturbances in the «intact» hemisphere probably caused by venous drainage failure and intracranial hypertension. This belief is based on the results reported by other investigators [1,3]. Our data prove the stability of microvasculature perfusion in the CSDH perifocal zone and, consequently, preserved cerebral blood flow autoregulation in patients with such pathology. Hyperemia and hyperperfusion in the perifocal zone of CSDH, described in previous studies [3], do not affect the microcirculation, as no pial perfusion disorders were revealed. A possible reason for the development of such syndromes in the perifocal zone could be the formation of de novo blood vessels in the capsule, with the development of over-capillary shunting phenomena causing an increasing volume of blood flow rate. In practice, our results show that the onset of foci of local cerebral hyperperfusion non-affecting the pial bed direction is probably an early marker of de novo angiogenesis in the capsule formation with the development of brain compression [11]. Clarification of this statement might be the basis for early diagnosis of compression formation based on the detection of the characteristic features of cerebral perfusion. It should be noted that our study has some methodological limitations, the main one being the impossibility of dynamic non-invasive assessment of the state of perfusion in the perihematomal area without PCT rescanning. Moreover, considering the characteristics of our study design, we were unable to assess the perfusion characteristics of the perifocal zone in patients with a bilateral CSDH or in patients with a CSDH at a decompensated state. Both of these issues require further study.
Limitation of the Study
We suppose that it is impossible to carry out the dynamic assessment of cerebral perfusion parameters without a repeated PCT. We have to admit that we have failed to completely eliminate a mathematical error associated with the measurement of the “area of interest” space.
Conclusion
The detection of hyperemia and hyperperfusion in the perifocal zone of the CSDH in the 1st analysis method is associated with the change in blood flow and blood supply at the level of resistive and capacitive vessels and does not affect the capillary bed. The perfusion indices of blood flow in the perifocal zone of the CSDH show no significant differences from the symmetrical zone of the contralateral hemisphere. The maintenance of microcirculatory blood flow perfusion reflects the preservation of cerebral blood flow autoregulation in patients with chronic subdural hematomas. The exclusion of large vessels from the analysis of microcirculation (2nd method) is more suitable for the evaluation of cerebral blood flow status in patients with CSDH.
Acknowledgments:
DB was supported by NIH R01NS112808-01. AT was supported by a Grant-in-Aid for Exploratory Research from the Privolzhsky Research Medical University.
Footnotes
Conflict of interest. We declare that we have no conflict of interest.
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