The Effect of Cranioplasty Following Decompressive Craniectomy on Cerebral Blood Perfusion, Neurological, and Cognitive Outcome

CLINICAL ARTICLE J Neurosurg 128:229–235, 2018

The effect of cranioplasty following decompressive craniectomy on cerebral blood perfusion, neurological, and cognitive outcome

Adnan Hussain Shahid, MS,1 Manju Mohanty, PhD,1 Navneet Singla, MCh,1 Bhagwant Rai Mittal, MD,2 and Sunil Kumar Gupta, MCh1

Departments of 1Neurosurgery and 2Nuclear Medicine, Postgraduate Institute of Medical Education and Research, Chandigarh, India

OBJECTIVE Decompressive craniectomy is an established therapy for refractory intracranial hypertension. Cranio- plasty following decompressive craniectomy not only provides protection to the brain along with cosmetic benefits, but also enhances rehabilitation with meaningful functional recovery of potentially reversible cortical and subcortical dam- aged areas of the affected as well as the contralateral hemisphere. The aim of the study was to assess neurological and cognitive outcome as well as cerebral blood flow after cranioplasty. METHODS Thirty-four patients admitted for replacement cranioplasty after decompressive craniectomy for head injury were studied prospectively. Clinical, neurological, and cognitive outcomes were assessed by the Glasgow Outcome Scale (GOS), the Glasgow Coma Scale, and a battery of cognitive tests, respectively. Simultaneously, cerebral blood perfusion was assessed by technetium-99m ethyl cysteinate dimer (99mTc-ECD) brain SPECT imaging 7 days prior to and 3 months after cranioplasty. RESULTS Prior to cranioplasty 9 patients (26.5%) had GOS scores of 5 and 25 patients (73.5%) had GOS scores of 4, whereas postcranioplasty all 34 patients (100%) improved to GOS scores of 5. Approximately 35.3%–90.9% patients showed cognitive improvement postcranioplasty in various tests. Also, on comparison with brain SPECT, 94% of patients showed improvement in cerebral perfusion in different lobes. CONCLUSIONS Cranioplasty remarkably improves neurological and cognitive outcomes supported by improvement in cerebral blood perfusion. https://thejns.org/doi/abs/10.3171/2016.10.JNS16678 KEY WORDS cranioplasty; GOS; GCS; decompressive craniectomy; SPECT; cognitive outcome; trauma

he management of refractory intracranial hyperten- following decompressive craniectomy was previously sion remains a therapeutic challenge for the neuro- thought to be beneficial simply for protective and cosmetic surgeon. In modern-day neurosurgical practice, de- purposes. However, in recent years its role in improving Tcompressive craniectomy is often required in patients with cortical and subcortical functions as well as restoring CSF severe head injuries, middle cerebral artery infarctions, dynamics is increasingly being recognized.7,8,10,13–17,23,27,37 and severe brain edema secondary to infective or neo- In addition, subcutaneously preserved autologous bone plastic processes.1,3,22 It has been proven that therapeutic flaps have been found to be more effective for cranioplasty decompressive craniectomy reduces mortality and mor- following decompressive craniectomy.30 Although clinical bidity rates in a significant proportion of patients if used improvement has been documented in several studies, pre- in appropriate settings, but it also can result in different and postcranioplasty neuropsychological assessment has symptomatologies like “syndrome of trephined,” altered been documented only in few studies, and most of them CSF hydrodynamics, and impairment in underlying cere- are case reports.2,11,12 A few studies have also documented bral perfusion.4,18,19, 22, 25,29,31,32, 38,39 Restorative cranioplasty the role of increased cerebral blood perfusion (CBP) fol-

ABBREVIATIONS CBF = cerebral blood flow; CBP = cerebral blood perfusion; COWAT = Controlled Oral Word Association Test; DSST = Digit Symbol Substitution Test; DST = Digit Span Test; GCS = Glasgow Coma Scale; GOS = Glasgow Outcome Scale; RAVLT-DR, RAVLT-IR = Rey Auditory Verbal Learning Test–delayed recall, RAVLT– immediate recall; TMT-A, TMT-B = Trail-Making Test, Parts A and B; 99mTc-ECD = technetium-99m ethyl cysteinate dimer. SUBMITTED March 18, 2016. ACCEPTED October 14, 2016. INCLUDE WHEN CITING Published online March 3, 2017; DOI: 10.3171/2016.10.JNS16678.

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Unauthenticated | Downloaded 10/07/21 05:12 AM UTC A. H. Shahid et al. lowing cranioplasty in improvement of patients’ function- Rey Auditory Verbal Learning Test ing.8,15,37,40 In this investigation an attempt has been made The Rey Auditory Verbal Learning Test (RAVLT) is to study the effect of cranioplasty following decompres- a measure of verbal learning and memory. There are 2 sive craniectomy on CBP, and on neurological and cogni- lists, A and B, consisting of 15 words each. The number of tive outcome. words recalled correctly in the immediate recall (RAVLT- IR) trial, delayed recall (RAVLT-DR) trial, and the recog- Methods nition trial will form the memory score.28 This prospective observational study was conducted Digit Span Test in the Department of Neurosurgery, Postgraduate Insti- The Digit Span Test (DST) is a subtest of the PGI Mem- tute of Medical Education and Research, in Chandigarh, ory Scale, which is an Indian adaptation of the Wechsler India. After receiving approval from the Institute’s eth- Memory Scale, and it measures auditory attention and ics committee, 37 patients who had previously undergone working memory. The score will be the maximum number decompressive craniectomy following head injury were of digits recalled correctly.24 admitted for replacement cranioplasty between Janu- ary 2014 and September 2014. They were enrolled after Digit Symbol Substitution Test giving informed consent. Of the 37 patients recruited, 3 were lost to follow-up and were excluded from the study. The Digit Symbol Substitution Test (DSST) is a test of The demographic and clinical details at the time of in- mental speed, which requires motor persistence, sustained jury and after decompressive craniectomy (at time of dis- attention, and response speed. Rapid information processing is required to substitute the symbols accurately and charge) were recorded. There were 30 (88.2%) male and 4 36 (11.8%) female patients. The mean age was 31.53 ± 10.08 quickly. years, and mean educational level was 10.76 ± 2.93 years. For each test the raw scores obtained were compared Eleven (32.4%) patients had severe, 13 (38.2%) had mod- with normative data for the respective tests and then were erate, and 10 (29.4%) had mild head injury. The patients converted into either percentiles or Z scores. The patients with mild and moderate head injuries were initially man- scoring below the 15th percentile or below 1.5 SD were aged conservatively, and decompressive craniectomy was considered to have significant impairment in that specific done when they deteriorated after clinical and imaging domain. evidence of significant mass effect or herniation. At the 99m time of admission for cranioplasty, 16 patients (47.1%) Tc-ECD Brain SPECT Imaging had left, 17 (50.0%) had right, and 1 (2.9%) had bifrontal All the patients underwent technetium-99m ethyl cys- craniectomy defects. The median interval between crani- teinate dimer (99mTc-ECD) brain SPECT imaging. After ectomy and cranioplasty was 5 months, with a range of intravenous administration of the radiotracer (mean 700 3–29 months. Thirty-two patients underwent autologous MBq), brain SPECT acquisition started at 0.5–1 hour by bone graft placement and 2 underwent titanium plate cra- using a dual-head SPECT gamma camera (Symbia T16, nioplasty (due to autologous bone infection). All patients Siemens). The SPECT data were acquired over a 360° underwent neurological assessment, cognitive assessment, rotation (circular orbit) in 128 projections (20 seconds/ and SPECT imaging 1 week prior to and 3 months after projection) in a 128 × 128 matrix with a zoom factor of cranioplasty. 1.5. The acquired SPECT data were then reconstructed using an iterative reconstruction algorithm and Butterworth Neurological Assessment smoothing filter. Subsequently, the reconstructed data Glasgow Coma Scale (GCS)35 and Glasgow Outcome were displayed in 3 planes (axial, sagittal, and coronal) for Scale (GOS) scores20 were used to assess the neurological visual localization and interpretation of the lesions dem- outcome. onstrating focal and abnormal uptake of the radiotracer. The SPECT data were analyzed using SCENIUM dedicated software for regional analyses of brain projections. Cognitive Assessment The minimum cerebral perfusion was calculated by the A battery comprising the following tests was used for SCENIUM dedicated application in the syngo (Molecular cognitive assessment. Imaging) application for regional analyses of brain projections. This application measures minimum, maximum, Trail-Making A and B Test and mean perfusion within each lobe or region. The ra- The Trail-Making Test (TMT) is a measure of visuo- tio of minimum perfusion of all lobes was calculated and conceptual and visuomotor functions. It consists of 2 compared with postcranioplasty results. A change in ratio parts: part A measures visual attention and psychomotor by even 1% was considered an improvement.34 speed, and part B measures cognitive flexibility and task All the assessments were performed at 2 time points, switching.26 first at 1 week prior to cranioplasty and then at 3 months after cranioplasty. The cohort of patients was also divid- Controlled Oral Word Association Test ed into 2 groups according to the time interval between The Controlled Oral Word Association Test (COWAT) craniotomy and cranioplasty: Group 1 (early—patients is a measure of phonemic fluency. In this test the subject subjected to cranioplasty within 6 months); and Group 2 generates words based on their phonetic similarity.6 (late—patients subjected to cranioplasty after 6 months).

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FIG. 1. A: Transaxial CT image showing right craniotomy defect. B and C: Transaxial and sagittal brain SPECT images of a patient with right craniotomy showing perfusion defect in frontal, parietal, and occipital lobes. D and E: Postcranioplasty SPECT images of the same patient showing improvement in perfusion in the respective lobes. Arrows designate the site of craniotomy and the perfusion defects. Figure is available in color online only.

The data were analyzed using SPSS 21 (IBM). The data patients falling in the impaired range decreased to 42.4% for categorical and continuous variables have been present- in the DSST, 57.6% in the TMT-A, 60% in the TMT-B, ed as frequency (percentage) and mean (SD), respectively. 14.7% in the DST, 44.1% in the COWAT, 55.9% in the The quantitative data were analyzed using either the paired RAVLT-IR, and 55.9% in the RAVLT-DR. t-test or Wilcoxon signed-rank test (data not normally dis- The comparison between pre- and postassessment tributed) to compare the changes in pre- and postperfu- values revealed significant improvement in global func- sion (SPECT scans) and cognitive tests. All analysis was tioning (GOS). The patients having impairment in visual 2-tailed and the level of significance was taken as p ≤ 0.05. acuity and motor weakness also showed complete improvement. With regard to CBP, only 2 (6%) patients did not show improvement in any of the lobes, whereas the Results remaining 32 (94%) showed improvement in 1 or more Assessments performed prior to cranioplasty showed lobes (Figs. 1–4). The maximum number of patients had that all patients had recovered from their head injury improvement in frontal lobe (21) and occipital lobe (20). and had a GCS score of 15. Regarding global outcome, Fourteen patients showed improvement in the parietal 9 (26.5%) patients had a GOS score of 5, and 25 (73.5%) lobe and 11 each in the temporal lobe and basal ganglia. patients had a GOS score of 4. Three patients had visual The comparison between pre- and postassessment values acuity impairment and 10 had motor weakness (MRC revealed statistically significant differences only in the Grade 4/4+). The mean perfusion ratios precranioplasty occipital lobe and basal ganglia. There was an increase were 0.673 ± 0.448 in frontal lobes, 1.09 ± 0.535 in pari- in the brain perfusion scores in the occipital lobe and a etal lobes, 0.79 ± 0.597 in occipital lobes, 0.766 ± 0.369 decrease in the basal ganglia. Although there was an in- in temporal lobes, and 0.949 ± 0.338 in basal ganglia. On crease in the brain perfusion ratio following cranioplasty preoperative cognitive assessment, the patients whose in the frontal lobe and a decrease in the temporal and scores were in the impaired range were 78.8% in the parietal lobes, the differences were not statistically sig- DSST, 84.8% in the TMT-A, 86.2% in the TMT-B, 70.6% nificant. A trend of improvement (change of scores ± 1 in the DST, 61.8% in the COWAT, 94.1% in the RAVLT- SD) from pre- to postcognitive assessments was observed IR, and 88.2% in the RAVLT-DR. in 35.3%–90.9% of patients, including those who were At postcranioplasty assessment all 34 patients had a still in the impaired range. The maximum improvement GOS score of 5. The mean perfusion ratios postcranio- (90.9%) was observed in DSST, a measure of information plasty were 0.798 ± 0.374 in frontal lobes, 0.999 ± 0.174 processing speed, and minimum improvement (35.3%) in parietal lobes, 0.869 ± 0.340 in occipital lobes, 0.673 ± was seen in the COWAT, a measure of phonemic fluency. 0.214 in temporal lobes, and 0.826 ± 0.179 in basal gan- Only 1 patient showed deterioration in performance on glia. With regard to cognitive functioning, the number of the DST, a measure of attention (Table 1). The results of

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FIG. 2. A: Transaxial CT image obtained in a patient with a left craniotomy defect. B: Transaxial brain SPECT of the same patient showing a decrease in CBP in left frontal, parietal, and occipital lobes. C: Postcranioplasty SPECT suggestive of improvement in cerebral perfusion. Arrows designate the site of craniotomy and the perfusion defects. Figure is available in color online only. the paired t-test or Wilcoxon signed-rank test indicated prised more patients having impairment on the RAVLT- a significant difference in all the domains of cognitive IR, RAVLT-DR, and COWAT, but the differences were not functioning (Table 2). statistically significant except for TMT-A. Postcranioplas- Because the time lapse between craniectomy and cra- ty, significant improvement was observed in all cognitive nioplasty could contribute to the cognitive changes over domains for both the groups; however, the recovery was time, hence the performance in 2 groups, the early cra- better in the early cranioplasty group (Table 3). nioplasty group and the late cranioplasty group, was also compared. Both groups were comparable in terms of age, sex, education, severity of injury, and GOS score, but sig- Discussion nificantly different with regard to interval between cra- In the present study we have demonstrated that the re- niectomy and cranioplasty. Prior to cranioplasty, the late storative cranioplasty improves the neurological status, group comprised more patients having impairment on the cognitive functions, and CBP. This strengthens the hy- TMT-A, TMT-B, and DSST, whereas the early group com- pothesis that decompressive craniectomy can cause al-

FIG. 3. A: Transaxial CT image showing right craniotomy defect. B and C: Precranioplasty SPECT of patient with right craniotomy defect. D and E: Postcranioplasty SPECT showing marked improvement in CBP in occipital lobe in the same patient. Arrows designate the site of craniotomy and the perfusion defects. Figure is available in color online only.

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FIG. 4. A: Transaxial CT image of patient with left craniotomy defect. B and C: Postcranioplasty SPECT (C) of the same patient showing ipsilateral and contralateral improvement in CBP, as compared with the precranioplasty SPECT (B). Arrows designate the craniotomy and perfusion defects. Figure is available in color online only. teration not only in CSF dynamics but that it also causes increase in the cerebral metabolism in both hemispheres, dysfunction of the cerebrum, leading to neurological and as measured by PET in 12 patients and CBF reactivity cognitive symptomatology. with transcranial Doppler and concluded that cranioplasty Regarding the results of brain SPECT, our study showed appears to affect postural blood flow regulation. Chibbaro that the majority of patients had improvement in CBP in et al. also demonstrated improvement in CBF and glucose both frontal and occipital lobes following cranioplasty, but uptake in both hemisphered by transcranial Doppler and the paired t-test revealed a significant difference only in 18FDG-PET in 100% of patients. the occipital lobe. A decrease in the mean perfusion of The results also revealed significant differences in all parietal and temporal lobes was observed that may be due the cognitive tests performed pre- and postcranioplasty, to redistribution of blood to frontal and occipital lobes, indicating significant improvement in the functions of which showed an increase in perfusion. frontal and temporal lobes. Regarding the frontal lobe The results revealed a significant improvement in global functions, significant improvement was observed in the functional outcome after cranioplasty. Prior to cranioplas- DSST, a measure of information processing speed, and ty, the majority of patients had a GOS score of 4, which also on the TMT-B, which requires executive control— improved to a GOS score of 5 after cranioplasty. These specifically flexibility of thinking and greater demand findings were supported by the study done by Chibbaro for working memory and attention (DST), respectively. et al.,8 who concluded that cranioplasty is helpful not only However, not much improvement was observed in results for cerebral protection but also for a patient’s functional of the COWAT, a measure of phonemic fluency. Chib- outcome. Suzuki et al.33 studied the cerebral blood flow baro et al.8 also reported positive outcome on measures (CBF) with dynamic CT scanning in patients undergoing of frontal lobe functions (Frontal Assessment Battery) in cranioplasty. They concluded that improvement in a pa- 91% of patients. With respect to memory, a function of tient’s neurological outcome might be due to an increase in bilateral CBF. Yoshida et al.40 were the first to study cognitive improvement in 7 patients with large cranial defects, TABLE 2. Comparison of neuropsychological test results and correlated their findings with CBF and metabolism by pre- and postcranioplasty using stable 133Xe CT and 31P MR spectroscopy. Winkler Precranioplasty Postcranioplasty p et al.37 showed that cranioplasty resulted in a significant Test No.* Mean SD Mean SD Value TMT-A 33 88.87 44.30 56.60 27.18 0.001 TABLE 1. Neuropsychological status of patients following TMT-B 29 255.93 154.79 133.58 74.41 0.001 cranioplasty DSST 33 508.39 211.92 346.45 149.51 0.001 No. w/ Status (%) DST 34 8.38 2.05 10.41 2.21 0.001 Test No.* Improvement No Change Deterioration RAVLT-IR 34 6.41 3.18 9.35 2.76 0.001 TMT-A 33 15 (45.5) 18 (54.5) 0 RAVLT-DR 34 6.05 3.21 9.55 2.83 0.001 TMT-B 30 23 (76.7) 7 (23.3) 0 COWAT 34 3.88 2.48 5.39 2.56 0.001 DSST 33 30 (90.9) 3 (9.1) 0 * Numbers vary because tests could not be administered in all patients. DST 34 22 (64.7) 11 (32.4) 1 (2.9) Regarding the discrepancy in number of patients for TMT-B in Tables 1 and 2; 1 of the 30 patients had a significant number of errors and could not complete COWAT 34 12 (35.3) 22 (64.7) 0 the test in the precranioplasty assessment. Hence he was considered to be im- RAVLT-IR 34 25 (73.5) 9 (26.5) 0 paired on preassessment. However, the score was not entered in the analysis RAVLT-DR 34 28 (82.4) 6 (17.6) 0 because the patient could not complete the test. He could complete the test without errors in the postcranioplasty assessment; therefore the paired t-test * Numbers vary because tests could not be administered in all patients. was computed for 29 patients.

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TABLE 3. Frequency and percentages of patients falling into the with regard to optimal timing for cranioplasty, although impaired range: early versus late cranioplasty early intervention has been recommended. No. of Patients Impaired (%) The overall findings suggested a significant improve- Precranioplasty Postcranioplasty ment in neurological and cognitive functioning, which could be possible due to an improvement in the hemody- Test Early Late Early Late namic patterns in both cerebral hemispheres. It is suggest- TMT-A* 14 (73.7) 14 (100.0) 9 (47.4) 10 (71.4) ed that every cranial defect allows direct transmission of TMT-B* 13 (76.5) 12 (100.0) 7 (38.9) 11 (91.7) atmospheric pressure into the intracranial contents; i.e., af- DSST* 13 (68.6) 13 (92.9) 5 (26.3) 9 (64.3) fecting CBP. Before cranioplasty the entire cerebral perfusion in both hemispheres was affected in the same manner DST 14 (70.0) 10 (71.4) 2 (10.0) 3 (21.4) by intracranial pressure through the affected area. When COWAT 13 (65.0) 8 (57.1) 8 (40.0) 7 (50.0) the brain perfusions were compared after cranioplasty, RAVLT-IR 20 (100.0) 12 (85.7) 11 (55.0) 8 (57.1) they were found to be increasing. RAVLT-DR 18 (90.0) 12 (85.7) 11 (55.0) 8 (57.1) * Tests could not be administered in all patients (see also Tables 1 and 2): Conclusions the TMT-A and DSST could not be administered in 1 patient in the early The findings of the present study showed clear evidence precranioplasty and early postcranioplasty groups. The TMT–B could not be that cranioplasty triggers relevant neurological, functional, administered in 3 patients in the early precranioplasty group, in 2 patients in late precranioplasty group, and in 2 each in the early and late postcranioplasty and cognitive improvement in addition to cosmetic cor- groups. rections. The probable mechanism of this is improvement in perfusion of the underlying brain as depicted by brain SPECT. These possibilities should serve as a reminder to rehabilitation clinicians to give serious consideration to temporal lobe improvement was observed in both immedi- prompt performance of cranioplasty during the time allot- ate and delayed recall. The significant cognitive improve- ted for rehabilitation of the patients. ment in the present study has been supported by a number of investigators. The case series study of 4 patients by Di Stefano et al.12 showed remarkable improvement in cog- Acknowledgments nitive outcome after cranioplasty. Agner et al.2 presented I express my extreme pleasure in acknowledging the con- significant improvement in the regional CBF as measured tributions of all who have been instrumental in the successful by Xe-CT along with neuropsychological scores. Cogni- completion of this work. I would like to thank Ms. Sarika, Medical stat scores showed an improvement of 48.3% (assess dif- Physicist and Radiation Safety Officer, and Ms. Kusum Chopra, the ferent cognitive abilities), and Executive Interview showed statistician, for their help. an improvement of 32.95% (assesses executive functions) postcranioplasty. In a case report by Coelho et al.,9 signifi- References cant improvements in various cognitive tests were dem- 1. Aarabi B, Hesdorffer DC, Ahn ES, Aresco C, Scalea TM, onstrated in the task of verbal fluency, episodic memory, Eisenberg HM: Outcome following decompressive craniecto- audio-verbal learning, information processing speed, and my for malignant swelling due to severe head injury. J Neu- visual-constructive functions. There were comparable rosurg 104:469–479, 2006 results reported by Winkler et al.,37 who reported that of 2. Agner C, Dujovny M, Gaviria M: Neurocognitive assessment before and after cranioplasty. 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Liang W, Xiaofeng Y, Weiguo L, Gang S, Xuesheng Z, Fei als or methods used in this study or the findings specified in this C, et al: Cranioplasty of large cranial defect at an early stage paper. after decompressive craniectomy performed for severe head trauma. J Craniofac Surg 18:526–532, 2007 Author Contributions 24. Pershad D, Wig NN: Revised Manual for PGI Memory Scale (PGIMS). Agra, India: National Psychological Corpo- Conception and design: Gupta, Mohanty. Acquisition of data: ration, 1994 Shahid. Analysis and interpretation of data: Gupta, Mohanty, 25. Polin RS, Shaffrey ME, Bogaev CA, Tisdale N, Germanson Singla, Mittal. Drafting the article: Shahid. Critically revising the T, Bocchicchio B, et al: Decompressive bifrontal craniectomy article: Gupta, Mohanty, Singla. Reviewed submitted version of in the treatment of severe refractory posttraumatic cerebral manuscript: Gupta, Mohanty, Singla. Approved the final version edema. Neurosurgery 41:84–94, 1997 of the manuscript on behalf of all authors: Gupta. Statistical anal- 26. Reitan RM: Trail Making Test: Manual for Administra- ysis: Mohanty. Administrative/technical/material support: Gupta, tion and Scoring. Tuscon: Reitan Neuropsychology Labora- Mohanty. Study supervision: Gupta, Mohanty. tory, 1992 27. Schaller B, Graf R, Sanada Y, Rosner G, Wienhard K, Heiss Correspondence WD: Hemodynamic and metabolic effects of decompressive Sunil Kumar Gupta, Department of Neurosurgery, Post Graduate hemicraniectomy in normal brain. An experimental PET- Institute of Medical Education and Research, Secto 12, Chandi- study in cats. Brain Res 982:31–37, 2003 garh 160012, India. email: [email protected].

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