- Department of Neurosurgery, SMS Medical College and Hospital, Jaipur, Rajasthan, India.
Correspondence Address:
Keshav Mishra, Department of Neurosurgery, SMS Medical College and Hospital, Jaipur, Rajasthan, India.
DOI:10.25259/SNI_1003_2023
Copyright: © 2024 Surgical Neurology International This is an open-access article distributed under the terms of the Creative Commons Attribution-Non Commercial-Share Alike 4.0 License, which allows others to remix, transform, and build upon the work non-commercially, as long as the author is credited and the new creations are licensed under the identical terms.How to cite this article: Manish Agrawal1, Keshav Mishra1. Neurocognitive outcome post cranioplasty: The role of cerebral hemodynamics and cerebrospinal fluid dynamics. 21-Jun-2024;15:204
How to cite this URL: Manish Agrawal1, Keshav Mishra1. Neurocognitive outcome post cranioplasty: The role of cerebral hemodynamics and cerebrospinal fluid dynamics. 21-Jun-2024;15:204. Available from: https://surgicalneurologyint.com/surgicalint-articles/12958/
Abstract
Background: Cranioplasty has been useful in treating the symptoms associated with the “Sunken skin flap syndrome” post decompressive craniectomy, for which various mechanisms have been proposed. In this study, we aim to assess the changes in the cerebral blood flow and intracranial cerebrospinal fluid (CSF) dynamics post cranioplasty and correlate with the improvement in the neurocognitive status.
Methods: Computed tomography perfusion and cine magnetic resonance imaging studies were done to study the changes in cerebral perfusion and CSF flow dynamics postcranioplasty. The cognitive status was assessed using Montreal cognitive assessment, mini-mental state examination, and frontal assessment battery scores in the preoperative period and at 1 and 6 months follow-up.
Results: There was a significant change in cognitive status postcranioplasty, both at 1 and 6 months follow-up, which was associated with a significant improvement in cerebral blood flow, decreased mean transit time, and improvement in the mean and peak CSF flow velocities at the foramen of Magendie and aqueduct of Sylvius.
Conclusion: Cranioplasty leads to a marked improvement in cerebral hemodynamics, which is more significant on the ipsilateral side. It also leads to increased CSF turnover and improved CSF circulation. Improved cerebral perfusion and, more importantly, CSF dynamics may be responsible for the demonstrable improvement in the neurocognition in the postcranioplasty period.
Keywords: Cerebral hemodynamics, Cerebrospinal fluid flow, Computed tomography perfusion, Cranioplasty, Neurocognition
INTRODUCTION
Decompressive craniectomy (DC) is a lifesaving procedure to treat medically refractory intracranial hypertension in patients with severe head injury.[
The “sinking” of the skin flap due to atmospheric pressure onto the dura with irritation of the cortical tissue and gliosis[
The neurological recovery after cranioplasty is multifactorial, and this study aims to investigate the impact of changes in CSF dynamics along with cerebral blood flow on improvement in neurocognitive outcomes in post-cranioplasty patients.
MATERIALS AND METHODS
We performed a prospective observational single-center study on 26 consecutive patients who were operated on in the Department of Neurosurgery, SMS Medical College and Hospital for cranioplasty post-head injury between September 2017 and August 2019 after clearance from the Institutional Ethical Committee. Patients with previous CSF diversion surgery, repeated head injury, previous history of cognitive impairment or mental retardation, and allergy to iodine contrast were excluded from the study. Written and informed consent was obtained from the patient and/or nearest relative.
Cine phase retrospective cardiac gated MRI to assess CSF flow at the aqueduct of Sylvius and foramen of Magendie was done. Computed tomography perfusion (CTP) study brain was obtained to assess the baseline cerebrovascular hemodynamic parameters. Both the CTP and Cine MRI studies were repeated on the 7th postoperative day and the results were compared with the preoperative study.
Neurocognitive assessment of all the enrolled patients was done using the Montreal cognitive assessment (MoCA) score, mini-mental state examination (MMSE) score, and frontal assessment battery (FAB) preoperatively.[
CTP analysis was performed using a 40-slice computed tomography (CT) scanner (Philips) using a 40-slice long continuous (cine) scan. One hundred and twenty axial images were constructed with eight 5 mm thick sections which covered a total of 40 mm thickness (as per available CT scanner). The CT scanner protocols are 80 kV, 209 mA, 1 s per rotation at 0° gantry. The CTP scan was started with a 4 s delay after the injection of 50 mL non-ionic contrast agent Iopamidol at a rate of 4 mL/s with an infuser pump. Perfusion maps were generated for each patient, and CBF and mean transit time (MTT) were measured in five regions of interest (ROI), that is, orbitofrontal cortex (OFC), internal capsule (IC), thalamus, caudate nucleus, and white fiber tract from Motor-Sensory Cortex (MSC). The ROI was manually drawn in the CTP images both on the same and contralateral side as the craniectomy defect and the values were generated and compared with the help of the manufacturer’s software package of CTP.[
CBF is defined as the volume of blood that flows per unit mass per unit of time in brain tissue and is typically expressed in milliliters of blood per minute per 100 g of brain tissue.[
Cine MRI study was performed on a 3-T magnetic resonance scanner (Philips) with a 30 mT/m maximum gradient strength and a 150 mT/m per millisecond slow rate using a head coil. The PC velocity encoded cine MRI (TR/TE:15.0/2.1, FOV: 230, matrix: 512 × 512, Voxel size: 0.575 × 0.575 × 1 mm) was obtained using Retrospective Cardiac Gating and 13 phases were evaluated for each cardiac cycle. Subsequent analysis and measurements were carried out using the manufacturer’s software package. Peak CSF flow rate and mean CSF velocity were evaluated for each patient at the aqueduct of Sylvius and foramen of Magendie.[
Statistical analysis was done using computer software (Statistical Package for the Social Sciences trial version 24). The qualitative data were expressed in proportion and percentages, and the quantitative data were expressed as mean ± standard deviations. The difference in proportion was analyzed using the Chi-square test, and the difference in means was analyzed using either two-tailed paired t-tests or the Wilcoxon sign-ranked test, depending on the type of distribution of data determined by the Shapiro–Wilk test. An error probability of <0.05 was considered to be statistically significant.
RESULTS
Twenty-six patients were recruited for the study, and CTP and Cine MRI studies were done for all the patients according to the specified protocol except for one patient who could not undergo Cine MRI due to significant motion artifacts. The change in neurocognitive status post-cranioplasty was evaluated at 1-month and 6-month intervals post-cranioplasty, which could not be attained for three patients who were lost to follow-up.
The study population comprised 21 males (80.76%) and five females aged 18–63 years, with a mean age of 32.2 years. All the participants had undergone DC 3–44 months before cranioplasty, with two outliers at 65 and 84 months. The mean time difference between the two surgeries was 16.46 months. At the time of undergoing surgery, 21 out of 26 patients were conscious and cooperative, but five had impaired consciousness, with GCS scores ranging from 4 to 11. The participants had, on average, 9.3 years of formal education, and only 11 subjects had received 12 or more years of education.
The change in neurocognitive status assessed with MoCA, MMSE, and FAB scores all showed significant improvements measured at 1- and 6-month duration postsurgery [
Figure 1:
(a) Box and whisker plot showing improvement in cognitive function using Montreal cognitive assessment scores. (b) Box and whisker plot showing improvement in cognitive function using mini-mental state examination scores. (c) Box and whisker plot showing improvement in cognitive function using frontal assessment battery scores. MoCA: Montreal cognitive assesment score, MMSE: Mini-mental state examination, FAB: Frontal assesment battery.
On the side of the cranioplasty, the improvement in CBF in IC, MSC, and the total ipsilateral hemispheric mean [
The CSF velocities (mean-V and peak-V), both at the aqueduct of Sylvius [
DISCUSSION
The use of DC has resulted in increasing complications such as hydrocephalus, infections, CSF leakage, and syndrome of trephined.[
Although numerous studies have proposed various hypotheses explaining the functional improvement post cranioplasty, no concrete conclusion has been reached. The literature is mainly concentrated on the mechanical effect of the environmental pressure gradient on the unprotected brain parenchyma, along with impaired venous return and changes in CBF.[
A recent review by Halani et al.[
The CSF contained in the craniospinal cavity shows a pulsatile flow in sync with the cardiac cycle, with only a negligible amount of CSF being absorbed during each cycle. As compliance of the craniospinal cavity is the most important driving factor for this pulsatile CSF flow; therefore, any change in compliance will be reflected in the changing characteristics of the CSF flow.[
Our study shows significant improvement in cognitive outcomes observed over 24 weeks after cranioplasty. The mean MoCA, MMSE, and FAB scores showed significant improvement in the mean scores compared to the baseline scores at 6 months. The mean time elapsed between craniectomy and cranioplasty was 16.46 months. As most of the neurological recovery after traumatic brain injury happens within the 1st year, therefore, the neurocognitive improvement is more likely an effect of cranioplasty. We had two outlier patients who underwent cranioplasty at 65 and 84 months after initial surgery and still showed significant improvement in the test scores [
Figure 4:
Graph showing improvement in cognition in two patients who underwent cranioplasty 65 and 84 months after initial trauma, which underlines the role of cranioplasty for improvement in cognition. MoCA: Montreal cognitive assesment score, MMSE: Mini-mental state examination, FAB: Frontal assesment battery.
Although we are reporting, to the best of our knowledge, the largest series of cranioplasty patients being evaluated by both CTP and Cine MRI studies along with neurocognition, a few limitations are obvious. The study population consists of head injury patients undergoing craniectomy due to a variety of pathologies ranging from subdural hematoma to parenchymal brain contusions. Moreover, the size of the craniectomy defect varied among individual patients. The CTP and Cine MRI studies were done at a single point of time (7 days before and after surgery), which could provide a potential source of bias due to inherent errors associated with point observations. The study population size limits the statistical power of the results.
CONCLUSION
Cranioplasty leads to marked and consistent improvement in CSF circulation and flow along with improved cerebral hemodynamics, specially on the ipsilateral side. Improved cerebral perfusion and, more importantly, CSF dynamics may be responsible for the demonstrable improvement in the neurocognition in the post-cranioplasty period.
Ethical approval
The Institutional Review Board approved the research/study at the Office of the Ethics Committee, SMS Medical College and attached hospitals, Jaipur, number 161 MC/EC/2018, dated May 15, 2020.
Declaration of patient consent
The authors certify that they have obtained all appropriate patient consent.
Financial support and sponsorship
Publication of this article was made possible by the James I. and Carolyn R Usman Educational Foundation.
Conflicts of interest
There are no conflicts of interest.
Use of artificial intelligence (AI)-assisted technology for manuscript preparation
The authors confirm that there was no use of artificial intelligence (AI)-assisted technology for assisting in the writing or editing of the manuscript and no images were manipulated using AI.
Disclaimer
The views and opinions expressed in this article are those of the authors and do not necessarily reflect the official policy or position of the Journal or its management. The information contained in this article should not be considered to be medical advice; patients should consult their own physicians for advice as to their specific medical needs.
Acknowledgments
Dr Rajeev Yadav, Professor, Department of Preventive and Social Medicine, SMS Medical College and Hospital, Jaipur, Rajasthan. Email: drrajeevyadav@gmail.com
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Oleg Malyshev
Posted July 2, 2024, 1:03 pm
Absolutely right!! Thank you!! It’s a great job.