Abstract
Introduction:
Cerebral autoregulation is an essential mechanism for maintaining cerebral blood flow stability. The phenomenon of transtentorial intracranial pressure (ICP) gradient after neurosurgical operations, complicated by edema and intracranial hypertension in the posterior fossa, has been described in clinical practice but is still underinvestigated. The aim of the study was to compare autoregulation coefficients (PRx) in two compartments (infra- and supratentorial) during the ICP gradient phenomenon.
Materials and Methods:
Three male patients, aged 24, 32, and 59, were involved in the study after posterior fossa surgery. Arterial blood pressure and ICP were invasively monitored. Infratentorial ICP was measured in the cerebellar parenchyma. Supratentorial ICP was measured either in the parenchyma of the cerebral hemispheres or through the EVD. Cerebral autoregulation was evaluated by the PRx coefficient (ICM +, Cambridge, UK).
Results:
In all patients, ICP was higher in the posterior fossa, and the transtentorial ICP gradient was 5 +/− 1.6; 8.5 +/− 4.4 and 7.7 +/− 2.2 mm Hg, respectively. ICP in the infratentorial space was 17 +/− 4; 18 +/− 4.4 and 20 +/− 4 mm Hg, respectively. PRx values in the supratentorial and infratentorial spaces had the smallest difference −0.01, 0,02, 0,01 and the limits of precision were 0,1, 0,2, and 0,1 in the first, second, and third patients, respectively. The correlation coefficient between the PRx values in the supratentorial and infratentorial spaces was 0.98, 0.95, and 0.97, respectively.
Conclusion:
A high degree of correlation was established between the autoregulation coefficient PRx in two compartments in the presence of transtentorial ICP gradient and persistent intracranial hypertension in the posterior fossa. Cerebral autoregulation, according to the PRx coefficient in both spaces, was similar.
Keywords: cerebral autoregulation1, pressure reactivity2, fossa posterior3, transtentorial gradient4, intracranial hypertension5, gradient intracranial pressure6
Introduction
Cerebral autoregulation (CA) is a crucial mechanism for maintaining stable cerebral blood flow (CBF) [1,2]. Impaired cerebral autoregulation in patients with brain injuries and cerebrovascular accidents is often complicated by cerebral ischemia and unfavorable outcome [3,4]. Compromised cerebral autoregulation is a key element in secondary brain damage and is often associated with intracranial hypertension. [3–5].
Currently, clinicians have access to various methods for assessing the status of autoregulation [6;7]. According to Consensus (expert opinion), none of the existing techniques can be considered a standard for autoregulation assessment [8]. Nevertheless, the most straightforward and most accessible method of surrogate evaluation of cerebral autoregulation in patients with acute cerebral injury remains the pressure reactivity index (PRx) [3;6–8]. PRx calculates as a moving correlation coefficient between intracranial pressure (ICP) and arterial blood pressure (ABP) signals [9].
Treatment of intracranial hypertension in acute cerebral pathology, including brain injuries and cerebrovascular accidents, remains the cornerstone of neurointensive care [4,10,11]. The development of intracranial hypertension is also possible in neurosurgical patients with complicated courses of disease [4,10,11]. Interestingly, neurosurgical intervention on the posterior cranial fossa (PCF) often leads to the development of a very unusual phenomenon – transtentorial ICP gradient. Edema in the area of surgical intervention, mass effect (hematoma, bleeding), venous stasis and compression of the CSF pathways in the PCF area lead to the formation of compartment syndrome and transtentorial ICP gradient with a predominance of ICP values in the infratentorial space [12;13]. The phenomenon of transtentorial ICP gradient is described both in experiments on animal models and in clinical practice [12–17].
The aim of our study was to evaluate the state of autoregulation above and below the cerebellar tentorium in patients with complicated courses after neurosurgical interventions on the PCF and developed transtentorial ICP gradient.
Materials and methods
In this work, we present retrospective data from 3 patients after neurosurgical intervention on PCF (Table 1). Before surgery, all patients had moderate bulbar palsy, cerebellar symptoms, headache, and dizziness. These patients had a high degree of vascularization at the surgical site, revealed by angiography, suggesting the likelihood of venous congestion in the trunk region, risk of increased bulbar dysfunction, and prolonged intensive care. Monitoring of ICP in the supra- and infratentorial space in two patients was performed immediately after the operation (the first and third patients). In one patient (the second patient), supratentorial ICP monitoring was done through the external ventricular drainage (EVD) that was installed three days after the surgery, followed by PCF decompression to attenuate the edema in PCF, hydrocephalus, and neurological impairment.
Table 1.
General characteristics of patients.
| Pts № | Gender | Age (years) | DS | DC of fossa posterior | EVD | Duration of stay in NICU (day) | Duration of stay in hospital (day) | Outcome/Karnofsky performance scale (1949)* |
|---|---|---|---|---|---|---|---|---|
| 1 | Male | 32 | Hemangioma of the caudal parts of the IV ventricle. | no | no | 6 | 64 | Survived / 60 |
| 2 | Male | 24 | Malformation of the right cerebellar hemisphere. Chronic hematoma of the right cerebellar hemisphere. | yes | yes | 16 | 20 | Died / 0 |
| 3 | Male | 59 | Hemangioblastoma of brainstem. | no | no | 51 | 97 | Survived / 80 |
DS – diagnosis; DC – decompression; EVD – external ventricular drainage; NICU – neurosurgical intensive care unit;
– Karnofsky DA, Burchenal JH (1949) Evaluation of chemotherapeutic agents in cancer. In: Macleod CM (ed) Evaluation chemotherapy agents. Columbia University Press, New York, pp 191–205.
The ICP monitoring indicated a high probability of edema and intracranial hypertension in the PCF. The Codman probes were installed at the end of the surgery after preliminary calibrations. In all three patients, the infratentorial transducers were implanted in a sitting position into the cerebellar hemisphere to a depth of 1.5 cm. The dura mater was sealed by suture, the bone flap was placed in place and fixed, and soft tissues were sewn in layers. After that, the patient was transferred to a horizontal position. The second transducer was installed supratentorial (in two patients) through the trephined hole at the Kocher point to a depth of 2 cm. Each transducer was connected to an “ICP Express Codman” monitor (Codman & Shurtleff Inc., Raynham, MA), connected to the bedside Philips IntelliVue MP60 (Philips Medical Systems, Best, The Netherlands). In one patient (the second), ICP measurement in supratentorial space was performed through the EVD that was installed due to hydrocephalus.
Data acquisition
Arterial blood pressure (ABP) was recorded through arterial lines connected to pressure transducers. ICP was acquired from an intraparenchymal strain gauge probe (Codman ICP MicroSensor; Codman & Shurtleff Inc., Raynham, MA). All data were recorded using digital data transfer and sampled at a frequency of 100 Hz using the ICM+ software (Cambridge, UK). Signal artifacts were removed using both manual methods before further processing or analysis. Duration of intracranial hypertension was measured to summarize the time when ICP was above 20 mmHg from all times of monitoring and presented in percent (%). The length of impaired autoregulation was calculated as the time when PRx was above 0,2 and presented in percent (%).
Signal processing
Ten-second moving averages (updated every 10 seconds to avoid data overlap) were calculated for signals: ICP and ABP. PRx was calculated as the moving correlation coefficient between 30 consecutive 10-second mean windows of ICP and ABP, updated every minute using the ICM+ software (Cambridge Enterprise Ltd, Cambridge, UK, http://icmplus.neurosurg.cam.ac.uk) [9]. The threshold of the PRx was set to 0,2. Mean values over the recording period were calculated.
Autoregulation status was considered as preserved if PRx ≤ 0.2. Autoregulation status was deemed to be non-preserved or impaired if PRx > 0.2.
Statistical analysis
Statistical analyses were performed using Statistica10.0 (StatSoft, USA). The Bland-Altman method was used to compare the autoregulation coefficient (PRx) in supratentorial and infratentorial spaces. The correlation between ICP and PRx values in the supra- and infratentorial spaces were done using Pearson’s correlation coefficient. All data are presented as mean ± standard deviation.
Results
ICP in the supra- and infratentorial space was monitored for 103 ± 9.5 hours. In all patients, ICP was higher in the posterior cranial fossa. The transtentorial ICP gradient was 5 ± 1.6 mmHg in the first patient, 8.5 ± 4.4 mmHg in the second, and 7.7 ± 2.2 mmHg in the third. ICP in the infratentorial space was 17 ± 4 mmHg in the first patient, 18 ± 4.4 mmHg in the second, and 20 ± 4 mmHg in the third. The total duration of intracranial hypertension (ICH) in supratentorial space in all patients was minimal 0.6%, 2.3% and 0.7%, respectively. The entire period of ICH in the infratentorial space was 25%, 34% and 45%, respectively of the monitoring time (Table 2). All patients showed a high degree of similarity between the ICP and Prx trends in the supra and infratentorial spaces (Supplement Figures 1,4,7, 10,11,12). The correlation coefficient between ICP values in the supratentorial and infratentorial spaces was 0.91 in the first patient, 0.64 in the second, and 0.86 in the third (Table 2).
Table 2.
Comparison of mean ICP in supra- and infratentorial spaces.
| Pts № | ICP monitoring time (hours) | ICPsupra (mmHg) | ICPinfra (mmHg) | Duration of ICPsupra >20mmHg (%) | Duration of ICPinfra >20mmHg (%) | Correlation ICPsupra and ICPinfra |
|---|---|---|---|---|---|---|
| 1 | 114 | 13±3,4 | 17±4 | 0,6 | 25 | 0,91 |
| 2 | 96 | 11±4,5 | 18±4,4 | 2,3 | 34 | 0,64 |
| 3 | 100 | 11±2,8 | 20±4 | 0,7 | 45 | 0,86 |
Pts – patient; ICPsupra – intracranial pressure in supratentorial spaces; ICPinfra - intracranial pressure in infratentorial spaces.
Most, of the time, autoregulatory status was preserved in all patients (PRx < 0.2), despite the ICP gradient and the development of episodes of persistent hypertension in the PCF (Table 3). The PRx in the supratentorial space in each patient was 0,02 ± 0,2, 0,07 ± 0,2 and 0,002 ± 0,2 and in the infratentorial space was 0,04 ± 0,2, 0,06 ± 0,2 and 0,02 ± 0,2 in the first, second and third patients, respectively (Table 3). The duration of the impaired autoregulation (PRx ≥ 0.2) in the supra- and infratentorial spaces was similar in all patients (Table 3), (Supplement Figures 3,6,9). The correlation coefficient between PRx values in the supratentorial and infratentorial spaces was 0.98, 0.95, and 0.97 in the first, second and third patient, respectively (Table 3), (Supplement Figures 2,5,8). PRx values in the supratentorial and infratentorial spaces had the smallest difference −0.01, 0,02, 0,01 and the limits of precision were 0,1, 0,2 and 0,1 in the first, second and third patient, respectively (Figure 1).
Table 3.
Comparison of PRx in supra- and infratentorial spaces.
| Pts № | ICP monitoring time (hours) | PRxsupra | PRxinfra | Duration (%) of PRxsupra | Duration (%) of PRxinfra | Correlation PRxsupra and PRxinfra | ||
|---|---|---|---|---|---|---|---|---|
| ≤0,2 | >0,2 | ≤0,2 | >0,2 | |||||
| 1 | 114 | 0,02±0,2 | 0,04±0,2 | 67 | 33 | 66 | 31 | 0,98 |
| 2 | 96 | 0,07±0,2 | 0,06±0,2 | 62 | 38 | 64 | 36 | 0,95 |
| 3 | 100 | 0,002± 0,2 | 0,002±0,2 | 61 | 39 | 61 | 39 | 0,97 |
Pts – patient; PRxsupra – coefficient autoregulation in supratentorial spaces; ICPinfra - coefficient autoregulation in infratentorial spaces.
Figure 1.
Bland-Altman plot for comparison of average paired PRx supratentorial and PRx infratentorial space plotted against their mean difference in first (A), second (B) and third (C) patient. A Bias was − 0,01, limit of precision 0,1. B Bias was 0,02, limit of precision 0,2.C Bias was 0,01, limit of precision 0,1.
Discussion
In this study, we evaluated cerebral autoregulation above and below the tentorium cerebelli in neurosurgical patients with a complicated postoperative period, accompanied by edema in PCF and ICH development. We observed that all patients had an ICP gradient with a predominance of ICP values in PCF. This phenomenon occurs during the formation of a compartment syndrome in the PCF in various cerebral pathologies, as described in the literature [12–17].
We assumed that the ICP gradient is associated with a more prominent impairment of cerebral autoregulation in the PCF. However, our study did not confirm the hypothesis because the autoregulation coefficient PRx was very similar in the supra and infratentorial spaces despite the existing ICP gradient. It should be noted that the relative duration of impaired autoregulation was the same above and below the tentorium in all patients (Table 3). For each individual patient, a minimal difference was found between PRx values (Figure 1) and a significant correlation of PRx (p < 0.05) above and below the tentorium of the cerebellum (Table 3, Supplement Figures 1,2,4,5,7,8, Supplement Tables 1–3).
Additionally, we compared PRx autoregulation coefficients in the supra and infratentorial spaces during periods of normal ICP in the PCF and during periods of increased ICP in the PCF above 20 mmHg. We purposefully analyzed and compared the state of autoregulation above and below the tentorium of the cerebellum depending on the presence or absence of intracranial hypertension only in the infratentorial space, so the duration of intracranial hypertension in the infratentorial space overlapped in time the duration of intracranial hypertension in the supratentorial space (Supplement Tables 1,2,3). However, we did not obtain a significant difference between the coefficients of autoregulation in each compartment during these periods (Supplement Figures 1.1;1.2;1.3).
Several authors studied the state of autoregulation in healthy volunteers using Doppler sonography in the anterior and posterior parts of the Circle of Willis [18,19]. They concluded that the damping effects of cerebral autoregulation in the PCA are lower than in the MCA territory and that in the posterior cerebral artery, absolute flow is more tightly regulated, but relative flow regulation is consistent across cerebrovascular territories [18,19]. They have used a transfer function analysis (TFA) with a Fourier decomposition of the two waveforms to quantify the effect of spontaneous ABP fluctuations in CBF. [20]. Our work has some similarities with those described above studies in terms of the assessment of autoregulation above and below the tentorium cerebelli. As opposed to them, we used the PRx coefficient to assess and compare autoregulation. This assessment is feasible with software and invasive blood pressure and ICP measurements above and below the cerebellar tentorium in clinical practice. We noted the similarity in wave characteristics of the ICP (the shape and amplitude of the waves above and below the cerebellum) but have not done a separate analysis.
Mouse et al. observed that supra- and infratentorial pulse amplitude, respiratory waves, and slow waves also have a high degree of correlation [21]. At the same time, all other ICP-derived parameters display symmetrical profiles [21].
In our opinion, cerebral autoregulation in patients with transtentorial ICP gradient is underinvestigated, and further study is essential. First, it complements the understanding of cerebral pathophysiology in the development of the transtentorial ICP gradient. Little is yet known about the ICP profiles in the supratentorial and infratentorial compartments in pathophysiology and clinical practice. Second, it will probably allow choosing the optimal blood pressure values during the development of ICH in the PCF to prevent cerebral ischemia both above and below the cerebellar tentorium. Third, it may help clarify the indications for decompression of the PCF during ICH development in the PCF.
Limitations
The presented work was done only on three patients, as the placement of ICP sensors in both compartments is a very rare case. In one patient (the second), supratentorial ICP measurement was performed through EVD and infratentorial ICP against the background of PCF decompression, which could affect the signal quality and wave characteristics of ICP. Patients were of different ages. The ICH profile in each examined patient had specifics, including dominated edema, impaired CSF circulation, and cerebral ischemia; some were likely to have a venous congestion. It is unclear which of the pathological processes predominated in each patient due to the retrospective character of the study. MRI and angiography were not routinely performed in patients after surgery. However, all three patients were diagnosed with postsurgical edema in the PCF by CT, and ICH was by invasive monitoring of ICP. All three required targeted intensive therapy (prolonged ventilation, hyperosmolar solutions, sedation, anesthesia, and in one patient, EVD and decompression of the PCF).
Conclusion:
In the presented series of reports, a high degree of correlation was established between the autoregulation coefficient PRx in two compartments in the presence of transtentorial ICP gradient and persistent intracranial hypertension in the posterior fossa. Cerebral autoregulation, according to the PRx coefficient in both spaces, was similar.
Supplementary Material
Acknowledgemets:
DB was supported by NIH RO1 NS112808
Footnotes
Ethics statement
The study conformed to the Declaration of Helsinki standards and was approved by the Burdenko Institute Ethics Committee.
Conflict of Interest: The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
Data availability statement
The raw data supporting the conclusions of this article will be made available by the authors without undue reservation.
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Associated Data
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Supplementary Materials
Data Availability Statement
The raw data supporting the conclusions of this article will be made available by the authors without undue reservation.