Letter: Early Cranioplasty is Associated With Greater Neurological Improvement: A Systematic Review and Meta-Analysis

Letter: Early Cranioplasty is Associated With Greater Neurological Improvement: A Systematic... ABBREVIATIONS ABBREVIATIONS BI Barthel index CP cranioplasty DC decompressive craniectomy RCT randomized controlled trials SMD standardized mean differences To the Editor: The systematic review and meta-analysis on timing of cranioplasty (CP) and differences on neurological outcome by Malcolm et al1 update their previous study from 2016,2 and follow another relatively recent one written by Xu et al in 20153 on the complications and recovery of neurological function in patients treated with early or late CP following decompressive craniectomy (DC). When comparing those studies, we have noticed that not much has changed in the last 3 yr. This also reflects our still limited understanding of the biological impact of DC and CP in terms of cerebral blood flow alterations, cerebrospinal fluid hydrodynamics, and brain metabolism; hence the open questions related to their functional and behavioral drawbacks.4-10 Hopefully, the attention of the scientific community is vivid as demonstrated by the average 80 + articles indexed on PubMed each year on these topics: this outlines the increased awareness that the interval between DC and CP, the shape and materials used for CP could all act as modifiable factors potentially influencing the clinical outcome.11-13 Of note, the 2 groups propose a different definition of early and late CP (<3 mo vs <6 mo; and 3-6 mo vs >6 mo, respectively); it is therefore not surprising that, despite roughly covering the same decade, only 2 surgical series were considered by both.14,15 As a result of these initial differences, the authors focused on slightly different aspects revolving around CP and somehow reached different conclusions. Both groups agree that early and late CP carry similar risks of overall surgical complications (namely: infection rate, intracranial hematoma, subdural collections); although Xu et al3 suggest that early CP might bear an increased risk of hydrocephalus. As for Malcolm et al,1 it would have been interesting to enrich their meta-analysis with more insights on this issue, but on this occasion unveiling how shunting influences outcome in early and late CP was beyond the scope of their study.16 On the other hand, both groups pinpointed that CP at any time is associated with significant neurological improvement; whereas the superiority of early CP is mostly strengthened by the 2 surgical series they have in common, which represent also those with longer follow ups (5-6 mo), thus raising concerns that shorter outcome could have biased the results in other series.14,15 Malcolm et al1 certainly deserve praise for attempting a more in-depth analysis on functional outcome following CP, and suggesting Barthel index (BI) as the most sensitive tool for discriminating the optimal time for this procedure. Their task was difficult, as they claim, due to the heterogeneity of the literature in terms of reason for DC, type of CP, cohort subgroups, and outcome measures reported. As shown by the funnel plot that we have reconstructed (MedCalc Version 18.2.1, MedCalc Software, Ostend, Belgium) with data from the 5 studies reporting BI as outcome measure (see Figure), Malcolm et al1 based their conclusion on very diverse (Cochran's Q test for heterogeneity: 33.07) and inconsistent raw data (I2 inconsistency index: 87.91%).7,14,15,17,18 A funnel test is less accurate whenever based on a limited number of studies, as in this case, nonetheless we herein propose this additional analysis because it provides the readers with a strong visual impact, and a fairly accurate estimate of the external validity of the results discussed. FIGURE. View largeDownload slide Tests for heterogeneity, Forest plot and funnel plot (software used: MedCalc Version 18.2.1) realized by considering the standardized mean differences (SMD) in Barthel Index (BI) from some of the studies included by Malcolm et al1 in their systematic review. BI was the performance scale used in 5 out of 8 of the studies reviewed.7,14,15,17,18 The classical measure of heterogeneity is Cochran's Q, which is calculated as the weighted sum of squared differences between individual study effects and the pooled effect across studies; whereas the I² statistic describes the percentage of variation across studies that is due to heterogeneity rather than chance. Theoretically, it can be assumed that studies with high precision included in any given systematic review when plotted in a funnel triangle will tend to the height of the triangle (average value), whereas studies with low precision will be spread evenly on both sides of the average, creating a roughly funnel-shaped distribution. Whereas the Forest plot indicates that patients undergoing early CP showed significant improvement in BI (a measure advocated as the most sensitive tool for discriminating the optimal time for CP), the additional statistics reveals that most of the studies included fall outside the funnel triangle highlighting the limited inferences that can be obtained from their comparison. FIGURE. View largeDownload slide Tests for heterogeneity, Forest plot and funnel plot (software used: MedCalc Version 18.2.1) realized by considering the standardized mean differences (SMD) in Barthel Index (BI) from some of the studies included by Malcolm et al1 in their systematic review. BI was the performance scale used in 5 out of 8 of the studies reviewed.7,14,15,17,18 The classical measure of heterogeneity is Cochran's Q, which is calculated as the weighted sum of squared differences between individual study effects and the pooled effect across studies; whereas the I² statistic describes the percentage of variation across studies that is due to heterogeneity rather than chance. Theoretically, it can be assumed that studies with high precision included in any given systematic review when plotted in a funnel triangle will tend to the height of the triangle (average value), whereas studies with low precision will be spread evenly on both sides of the average, creating a roughly funnel-shaped distribution. Whereas the Forest plot indicates that patients undergoing early CP showed significant improvement in BI (a measure advocated as the most sensitive tool for discriminating the optimal time for CP), the additional statistics reveals that most of the studies included fall outside the funnel triangle highlighting the limited inferences that can be obtained from their comparison. The point here is that we are still far away from addressing the initial research question regarding the optimal timing for CP. To have greater chances to do so in the future, we should perhaps ask ourselves which management protocols should be homogenized, as well as which areas of research would deserve investments the most.19 An awareness that many different factors, not only clinical but also organizational, come into play in the decision-making process regarding the timing for CP, would optimize the inclusion criteria and protocols for future trials. In the last 15 yr, for instance, the number of certified tissue banks has steadily increased; this trend was paralleled by a reduced use of cryopreservation or subcutaneous abdominal implantation of autologous bone flap after DC.20 Differences in healthcare systems, along with the abovementioned changes in clinical practice, simply reflect that management strategies are evolving over time and so is our approach to CP: bone flaps are more and more discarded after initial DC with a tendency to offer custom made bone flaps to our patients, should they survive the acute phase of the underlying pathology.21 At times, these aspects could all result in a procrastination of the intervention date. What is needed then is a collegiate effort to foster both large randomized controlled trials (RCT) and mechanistic studies. RCT could actually overcome the low evidence of a superiority of early CP (Class IIb, Level C) deriving from non-randomized retrospective cohort studies; it is therefore disappointing to interrogate international clinical trials databases (clinicaltrial.gov; eudract.ema.europa.eu; ukctg.nihr.ac.uk) and find only 2 prospective RCT on timing of CP, currently ongoing in Germany (DRKS-ID: DRKS00007931) and China (CTG-ID: NCT03222297).22,23 Reaching a consensus on the definition of early and late CP would certainly help in reducing the existing confusion; furthermore consistency in terms of outcome measures reported would enhance the inferences of clinical research on national and international guidelines.24 Going forward, our specialty will benefit from an international validation of objective measures able to guide clinicians in choosing the best timing for CP. The Brain Sunken Ratio is a valid attempt to propose an objective measure other than the time interval between the DC and CP to enhance neurological outcome; in a preliminary study, this radiological ratio resulted statistically significant in predicting complications rate and overall outcome.25 Noteworthy, the investigators of a recently concluded French RCT (CTG-ID: NCT01113645) studying the impact of cranioplasty on cerebral hemodynamic and blood flow suggested that CT perfusion could be a viable tool in the decision-making process for CP.26 A systematic review is successful whenever it identifies knowledge gaps; hence, we believe that the best path toward optimization of timing for CP surgery and consequent quality care improvement should pass through adoption of unified definitions, consistent outcome measures, and validation of predicting biomarkers/biosignatures.19,21-24,27 Disclosure The authors have no personal, financial, or institutional interest in any of the drugs, materials, or devices described in this article. REFERENCES 1. Malcolm JG , Rindler RS , Chu JK et al. Early cranioplasty is associated with greater neurological improvement: a systematic review and meta-analysis . Neurosurgery . 2018 ; 82 ( 3 ): 278 - 288 . Google Scholar CrossRef Search ADS PubMed 2. Malcolm JG , Rindler RS , Chu JK et al. Complications following cranioplasty and relationship to timing: a systematic review and meta-analysis . J Clin Neurosci . 2016 ; 33 : 39 - 51 . Google Scholar CrossRef Search ADS PubMed 3. Xu H , Niu C , Fu X et al. Early cranioplasty vs. late cranioplasty for the treatment of cranial defect: a systematic review . Clin Neurol Neurosurg . 2015 ; 136 : 33 - 40 . Google Scholar CrossRef Search ADS PubMed 4. Gang W , Lan Y , Xiao Ming Z et al. Evaluation of cerebral hemodynamics by computed tomography perfusion imaging before and after cranioplasty in patients with brain injury . Brain Inj . 2017 ; 31 ( 12 ): 1656 - 1659 . Google Scholar CrossRef Search ADS PubMed 5. Halani SH , Chu JK , Malcolm JG et al. Effects of cranioplasty on cerebral blood flow following decompressive craniectomy: A systematic review of the literature . Neurosurgery . 2017 ; 81 ( 2 ): 204 - 216 . Google Scholar CrossRef Search ADS PubMed 6. Voss HU , Heier LA , Schiff ND . Multimodal imaging of recovery of functional networks associated with reversal of paradoxical herniation after cranioplasty . Clin Imaging . 2011 ; 35 ( 4 ): 253 - 258 . Google Scholar CrossRef Search ADS PubMed 7. Kuo JR , Wang CC , Chio CC , Cheng TJ . Neurological improvement after cranioplasty - analysis by transcranial doppler ultrasonography . J Clin Neurosci . 2004 ; 11 ( 5 ): 486 - 489 . Google Scholar CrossRef Search ADS PubMed 8. Láng J , Ganau M , Prisco L , Bozsik K , Banczerowski P . Syndrome of trephined-underestimated and poorly understood complication after decompressive craniectomy . Ideggyogy Sz . 2016 ; 69 ( 7-8 ): 227 - 232 . Google Scholar CrossRef Search ADS PubMed 9. Ashayeri K , Jackson M E , Huang J , Brem H , Gordon R C . Syndrome of the Trephined: A systematic review . Neurosurgery . 2016 ; 79 ( 4 ): 525 - 534 . Google Scholar CrossRef Search ADS PubMed 10. Shahid AH , Mohanty M , Singla N , Mittal BR , Gupta SK . The effect of cranioplasty following decompressive craniectomy on cerebral blood perfusion, neurological, and cognitive outcome . J Neurosurg . 2018 ; 128 ( 1 ): 229 - 235 Google Scholar CrossRef Search ADS PubMed 11. Yang NR , Song J , Yoon KW , Seo EK . How early can we perform cranioplasty for traumatic brain injury after decompressive craniectomy? A retrospective multicenter study . World Neurosurg . 2018 ; 110 : e160 - e167 . Google Scholar CrossRef Search ADS PubMed 12. Servadei F , Iaccarino C . The therapeutic cranioplasty still needs an ideal material and surgical timing . World Neurosurg . 2015 ; 83 ( 2 ): 133 - 135 . Google Scholar CrossRef Search ADS PubMed 13. Lindner D , Schlothofer-Schumann K , Kern BC et al. Cranioplasty using custom-made hydroxyapatite versus titanium: a randomized clinical trial . J Neurosurg . 2017 ; 126 ( 1 ): 175 - 183 . Google Scholar CrossRef Search ADS PubMed 14. Zhang GL , Yang WZ , Jiang YW , Zeng T . Extensive duraplasty with autologous graft in decompressive craniectomy and subsequent early cranioplasty for severe head trauma . Chin J Traumatol . 2010 ; 13 ( 5 ): 259 - 264 . Google Scholar PubMed 15. Bender A , Heulin S , Röhrer S et al. Early cranioplasty may improve outcome in neurological patients with decompressive craniectomy . Brain Inj . 2013 ; 27 ( 9 ): 1073 - 1079 . Google Scholar CrossRef Search ADS PubMed 16. Mustroph CM , Malcolm JG , Rindler RS et al. Cranioplasty infection and resorption are associated with the presence of a ventriculoperitoneal shunt: a systematic review and meta-analysis . World Neurosurg . 2017 ; 103 : 686 - 693 . Google Scholar CrossRef Search ADS PubMed 17. Cho KC , Park SC . Safety and efficacy of early cranioplasty after decompressive craniectomy in traumatic brain injury patients . J Korean Neurotraumatol Soc . 2011 ; 7 ( 2 ): 74 - 77 . Google Scholar CrossRef Search ADS 18. Paredes I , Castaño-León AM , Munarriz PM et al. Cranioplasty after decompressive craniectomy. A prospective series analyzing complications and clinical improvement . Neurocirugía . 2015 ; 26 ( 3 ): 115 - 125 . Google Scholar CrossRef Search ADS PubMed 19. Rubiano AM , Carney N , Chesnut R , Puyana JC . Global neurotrauma research challenges and opportunities . Nature . 2015 ; 527 ( 7578 ): S193 - S197 . Google Scholar CrossRef Search ADS PubMed 20. Corliss B , Gooldy T , Vaziri S , Kubilis P1 , Murad G1 , Fargen K . Complications after in vivo and ex vivo autologous bone flap storage for cranioplasty: a comparative analysis of the literature . World Neurosurg . 2016 ; 96 : 510 - 515 . Google Scholar CrossRef Search ADS PubMed 21. Iaccarino C , Viaroli E , Fricia M , Serchi E , Poli T , Servadei F . Preliminary results of a prospective study on methods of cranial reconstruction . J Oral Maxillofac Surg . 2015 ; 73 ( 12 ): 2375 - 2378 Google Scholar CrossRef Search ADS PubMed 22. Giese H , Sauvigny T , Sakowitz OW et al. German Cranial Reconstruction Registry (GCRR): protocol for a prospective, multicentre, open registry . BMJ Open . 2015 ; 5 ( 9 ): e009273 . Google Scholar CrossRef Search ADS PubMed 23. NIH US National Library of Medicine . ClinicalTrials.gov. Available at: https://clinicaltrials.gov/show/NCT03222297 [accessed March 2018 ] 24. Kolias AG , Bulters DO , Cowie CJ et al. Proposal for establishment of the UK Cranial Reconstruction Registry (UKCRR) . Br J Neurosurg . 2014 ; 28 ( 3 ): 310 - 314 . Google Scholar CrossRef Search ADS PubMed 25. Lee JM , Whang K , Cho SM et al. Factors affecting optimal time of cranioplasty: Brain sunken ratio . Korean J Neurotrauma . 2017 ; 13 ( 2 ): 113 - 118 . Google Scholar CrossRef Search ADS PubMed 26. Chibbaro S , Vallee F , Beccaria K et al. The impact of early cranioplasty on cerebral blood flow and its correlation with neurological and cognitive outcome. Prospective multi-centre study on 24 patients . Rev Neurol (Paris) . 2013 ; 169 ( 3 ): 240 - 248 . Google Scholar CrossRef Search ADS PubMed 27. Ganau M , Syrmos N , Paris M et al. Current and future applications of biomedical engineering for proteomic profiling: Predictive biomarkers in neuro-traumatology . Medicines . 2018 ; 5 ( 1 ): 19 . Google Scholar CrossRef Search ADS Copyright © 2018 by the Congress of Neurological Surgeons This article is published and distributed under the terms of the Oxford University Press, Standard Journals Publication Model (https://academic.oup.com/journals/pages/about_us/legal/notices) http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Neurosurgery Oxford University Press

Letter: Early Cranioplasty is Associated With Greater Neurological Improvement: A Systematic Review and Meta-Analysis

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Oxford University Press
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Copyright © 2018 by the Congress of Neurological Surgeons
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0148-396X
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10.1093/neuros/nyy205
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Abstract

ABBREVIATIONS ABBREVIATIONS BI Barthel index CP cranioplasty DC decompressive craniectomy RCT randomized controlled trials SMD standardized mean differences To the Editor: The systematic review and meta-analysis on timing of cranioplasty (CP) and differences on neurological outcome by Malcolm et al1 update their previous study from 2016,2 and follow another relatively recent one written by Xu et al in 20153 on the complications and recovery of neurological function in patients treated with early or late CP following decompressive craniectomy (DC). When comparing those studies, we have noticed that not much has changed in the last 3 yr. This also reflects our still limited understanding of the biological impact of DC and CP in terms of cerebral blood flow alterations, cerebrospinal fluid hydrodynamics, and brain metabolism; hence the open questions related to their functional and behavioral drawbacks.4-10 Hopefully, the attention of the scientific community is vivid as demonstrated by the average 80 + articles indexed on PubMed each year on these topics: this outlines the increased awareness that the interval between DC and CP, the shape and materials used for CP could all act as modifiable factors potentially influencing the clinical outcome.11-13 Of note, the 2 groups propose a different definition of early and late CP (<3 mo vs <6 mo; and 3-6 mo vs >6 mo, respectively); it is therefore not surprising that, despite roughly covering the same decade, only 2 surgical series were considered by both.14,15 As a result of these initial differences, the authors focused on slightly different aspects revolving around CP and somehow reached different conclusions. Both groups agree that early and late CP carry similar risks of overall surgical complications (namely: infection rate, intracranial hematoma, subdural collections); although Xu et al3 suggest that early CP might bear an increased risk of hydrocephalus. As for Malcolm et al,1 it would have been interesting to enrich their meta-analysis with more insights on this issue, but on this occasion unveiling how shunting influences outcome in early and late CP was beyond the scope of their study.16 On the other hand, both groups pinpointed that CP at any time is associated with significant neurological improvement; whereas the superiority of early CP is mostly strengthened by the 2 surgical series they have in common, which represent also those with longer follow ups (5-6 mo), thus raising concerns that shorter outcome could have biased the results in other series.14,15 Malcolm et al1 certainly deserve praise for attempting a more in-depth analysis on functional outcome following CP, and suggesting Barthel index (BI) as the most sensitive tool for discriminating the optimal time for this procedure. Their task was difficult, as they claim, due to the heterogeneity of the literature in terms of reason for DC, type of CP, cohort subgroups, and outcome measures reported. As shown by the funnel plot that we have reconstructed (MedCalc Version 18.2.1, MedCalc Software, Ostend, Belgium) with data from the 5 studies reporting BI as outcome measure (see Figure), Malcolm et al1 based their conclusion on very diverse (Cochran's Q test for heterogeneity: 33.07) and inconsistent raw data (I2 inconsistency index: 87.91%).7,14,15,17,18 A funnel test is less accurate whenever based on a limited number of studies, as in this case, nonetheless we herein propose this additional analysis because it provides the readers with a strong visual impact, and a fairly accurate estimate of the external validity of the results discussed. FIGURE. View largeDownload slide Tests for heterogeneity, Forest plot and funnel plot (software used: MedCalc Version 18.2.1) realized by considering the standardized mean differences (SMD) in Barthel Index (BI) from some of the studies included by Malcolm et al1 in their systematic review. BI was the performance scale used in 5 out of 8 of the studies reviewed.7,14,15,17,18 The classical measure of heterogeneity is Cochran's Q, which is calculated as the weighted sum of squared differences between individual study effects and the pooled effect across studies; whereas the I² statistic describes the percentage of variation across studies that is due to heterogeneity rather than chance. Theoretically, it can be assumed that studies with high precision included in any given systematic review when plotted in a funnel triangle will tend to the height of the triangle (average value), whereas studies with low precision will be spread evenly on both sides of the average, creating a roughly funnel-shaped distribution. Whereas the Forest plot indicates that patients undergoing early CP showed significant improvement in BI (a measure advocated as the most sensitive tool for discriminating the optimal time for CP), the additional statistics reveals that most of the studies included fall outside the funnel triangle highlighting the limited inferences that can be obtained from their comparison. FIGURE. View largeDownload slide Tests for heterogeneity, Forest plot and funnel plot (software used: MedCalc Version 18.2.1) realized by considering the standardized mean differences (SMD) in Barthel Index (BI) from some of the studies included by Malcolm et al1 in their systematic review. BI was the performance scale used in 5 out of 8 of the studies reviewed.7,14,15,17,18 The classical measure of heterogeneity is Cochran's Q, which is calculated as the weighted sum of squared differences between individual study effects and the pooled effect across studies; whereas the I² statistic describes the percentage of variation across studies that is due to heterogeneity rather than chance. Theoretically, it can be assumed that studies with high precision included in any given systematic review when plotted in a funnel triangle will tend to the height of the triangle (average value), whereas studies with low precision will be spread evenly on both sides of the average, creating a roughly funnel-shaped distribution. Whereas the Forest plot indicates that patients undergoing early CP showed significant improvement in BI (a measure advocated as the most sensitive tool for discriminating the optimal time for CP), the additional statistics reveals that most of the studies included fall outside the funnel triangle highlighting the limited inferences that can be obtained from their comparison. The point here is that we are still far away from addressing the initial research question regarding the optimal timing for CP. To have greater chances to do so in the future, we should perhaps ask ourselves which management protocols should be homogenized, as well as which areas of research would deserve investments the most.19 An awareness that many different factors, not only clinical but also organizational, come into play in the decision-making process regarding the timing for CP, would optimize the inclusion criteria and protocols for future trials. In the last 15 yr, for instance, the number of certified tissue banks has steadily increased; this trend was paralleled by a reduced use of cryopreservation or subcutaneous abdominal implantation of autologous bone flap after DC.20 Differences in healthcare systems, along with the abovementioned changes in clinical practice, simply reflect that management strategies are evolving over time and so is our approach to CP: bone flaps are more and more discarded after initial DC with a tendency to offer custom made bone flaps to our patients, should they survive the acute phase of the underlying pathology.21 At times, these aspects could all result in a procrastination of the intervention date. What is needed then is a collegiate effort to foster both large randomized controlled trials (RCT) and mechanistic studies. RCT could actually overcome the low evidence of a superiority of early CP (Class IIb, Level C) deriving from non-randomized retrospective cohort studies; it is therefore disappointing to interrogate international clinical trials databases (clinicaltrial.gov; eudract.ema.europa.eu; ukctg.nihr.ac.uk) and find only 2 prospective RCT on timing of CP, currently ongoing in Germany (DRKS-ID: DRKS00007931) and China (CTG-ID: NCT03222297).22,23 Reaching a consensus on the definition of early and late CP would certainly help in reducing the existing confusion; furthermore consistency in terms of outcome measures reported would enhance the inferences of clinical research on national and international guidelines.24 Going forward, our specialty will benefit from an international validation of objective measures able to guide clinicians in choosing the best timing for CP. The Brain Sunken Ratio is a valid attempt to propose an objective measure other than the time interval between the DC and CP to enhance neurological outcome; in a preliminary study, this radiological ratio resulted statistically significant in predicting complications rate and overall outcome.25 Noteworthy, the investigators of a recently concluded French RCT (CTG-ID: NCT01113645) studying the impact of cranioplasty on cerebral hemodynamic and blood flow suggested that CT perfusion could be a viable tool in the decision-making process for CP.26 A systematic review is successful whenever it identifies knowledge gaps; hence, we believe that the best path toward optimization of timing for CP surgery and consequent quality care improvement should pass through adoption of unified definitions, consistent outcome measures, and validation of predicting biomarkers/biosignatures.19,21-24,27 Disclosure The authors have no personal, financial, or institutional interest in any of the drugs, materials, or devices described in this article. REFERENCES 1. Malcolm JG , Rindler RS , Chu JK et al. Early cranioplasty is associated with greater neurological improvement: a systematic review and meta-analysis . Neurosurgery . 2018 ; 82 ( 3 ): 278 - 288 . Google Scholar CrossRef Search ADS PubMed 2. Malcolm JG , Rindler RS , Chu JK et al. Complications following cranioplasty and relationship to timing: a systematic review and meta-analysis . J Clin Neurosci . 2016 ; 33 : 39 - 51 . Google Scholar CrossRef Search ADS PubMed 3. Xu H , Niu C , Fu X et al. Early cranioplasty vs. late cranioplasty for the treatment of cranial defect: a systematic review . Clin Neurol Neurosurg . 2015 ; 136 : 33 - 40 . Google Scholar CrossRef Search ADS PubMed 4. Gang W , Lan Y , Xiao Ming Z et al. Evaluation of cerebral hemodynamics by computed tomography perfusion imaging before and after cranioplasty in patients with brain injury . Brain Inj . 2017 ; 31 ( 12 ): 1656 - 1659 . Google Scholar CrossRef Search ADS PubMed 5. Halani SH , Chu JK , Malcolm JG et al. Effects of cranioplasty on cerebral blood flow following decompressive craniectomy: A systematic review of the literature . Neurosurgery . 2017 ; 81 ( 2 ): 204 - 216 . Google Scholar CrossRef Search ADS PubMed 6. Voss HU , Heier LA , Schiff ND . Multimodal imaging of recovery of functional networks associated with reversal of paradoxical herniation after cranioplasty . Clin Imaging . 2011 ; 35 ( 4 ): 253 - 258 . Google Scholar CrossRef Search ADS PubMed 7. Kuo JR , Wang CC , Chio CC , Cheng TJ . Neurological improvement after cranioplasty - analysis by transcranial doppler ultrasonography . J Clin Neurosci . 2004 ; 11 ( 5 ): 486 - 489 . Google Scholar CrossRef Search ADS PubMed 8. Láng J , Ganau M , Prisco L , Bozsik K , Banczerowski P . Syndrome of trephined-underestimated and poorly understood complication after decompressive craniectomy . Ideggyogy Sz . 2016 ; 69 ( 7-8 ): 227 - 232 . Google Scholar CrossRef Search ADS PubMed 9. Ashayeri K , Jackson M E , Huang J , Brem H , Gordon R C . Syndrome of the Trephined: A systematic review . Neurosurgery . 2016 ; 79 ( 4 ): 525 - 534 . Google Scholar CrossRef Search ADS PubMed 10. Shahid AH , Mohanty M , Singla N , Mittal BR , Gupta SK . The effect of cranioplasty following decompressive craniectomy on cerebral blood perfusion, neurological, and cognitive outcome . J Neurosurg . 2018 ; 128 ( 1 ): 229 - 235 Google Scholar CrossRef Search ADS PubMed 11. Yang NR , Song J , Yoon KW , Seo EK . How early can we perform cranioplasty for traumatic brain injury after decompressive craniectomy? A retrospective multicenter study . World Neurosurg . 2018 ; 110 : e160 - e167 . Google Scholar CrossRef Search ADS PubMed 12. Servadei F , Iaccarino C . The therapeutic cranioplasty still needs an ideal material and surgical timing . World Neurosurg . 2015 ; 83 ( 2 ): 133 - 135 . Google Scholar CrossRef Search ADS PubMed 13. Lindner D , Schlothofer-Schumann K , Kern BC et al. Cranioplasty using custom-made hydroxyapatite versus titanium: a randomized clinical trial . J Neurosurg . 2017 ; 126 ( 1 ): 175 - 183 . Google Scholar CrossRef Search ADS PubMed 14. Zhang GL , Yang WZ , Jiang YW , Zeng T . Extensive duraplasty with autologous graft in decompressive craniectomy and subsequent early cranioplasty for severe head trauma . Chin J Traumatol . 2010 ; 13 ( 5 ): 259 - 264 . Google Scholar PubMed 15. Bender A , Heulin S , Röhrer S et al. Early cranioplasty may improve outcome in neurological patients with decompressive craniectomy . Brain Inj . 2013 ; 27 ( 9 ): 1073 - 1079 . Google Scholar CrossRef Search ADS PubMed 16. Mustroph CM , Malcolm JG , Rindler RS et al. Cranioplasty infection and resorption are associated with the presence of a ventriculoperitoneal shunt: a systematic review and meta-analysis . World Neurosurg . 2017 ; 103 : 686 - 693 . Google Scholar CrossRef Search ADS PubMed 17. Cho KC , Park SC . Safety and efficacy of early cranioplasty after decompressive craniectomy in traumatic brain injury patients . J Korean Neurotraumatol Soc . 2011 ; 7 ( 2 ): 74 - 77 . Google Scholar CrossRef Search ADS 18. Paredes I , Castaño-León AM , Munarriz PM et al. Cranioplasty after decompressive craniectomy. A prospective series analyzing complications and clinical improvement . Neurocirugía . 2015 ; 26 ( 3 ): 115 - 125 . Google Scholar CrossRef Search ADS PubMed 19. Rubiano AM , Carney N , Chesnut R , Puyana JC . Global neurotrauma research challenges and opportunities . Nature . 2015 ; 527 ( 7578 ): S193 - S197 . Google Scholar CrossRef Search ADS PubMed 20. Corliss B , Gooldy T , Vaziri S , Kubilis P1 , Murad G1 , Fargen K . Complications after in vivo and ex vivo autologous bone flap storage for cranioplasty: a comparative analysis of the literature . World Neurosurg . 2016 ; 96 : 510 - 515 . Google Scholar CrossRef Search ADS PubMed 21. Iaccarino C , Viaroli E , Fricia M , Serchi E , Poli T , Servadei F . Preliminary results of a prospective study on methods of cranial reconstruction . J Oral Maxillofac Surg . 2015 ; 73 ( 12 ): 2375 - 2378 Google Scholar CrossRef Search ADS PubMed 22. Giese H , Sauvigny T , Sakowitz OW et al. German Cranial Reconstruction Registry (GCRR): protocol for a prospective, multicentre, open registry . BMJ Open . 2015 ; 5 ( 9 ): e009273 . Google Scholar CrossRef Search ADS PubMed 23. NIH US National Library of Medicine . ClinicalTrials.gov. Available at: https://clinicaltrials.gov/show/NCT03222297 [accessed March 2018 ] 24. Kolias AG , Bulters DO , Cowie CJ et al. Proposal for establishment of the UK Cranial Reconstruction Registry (UKCRR) . Br J Neurosurg . 2014 ; 28 ( 3 ): 310 - 314 . Google Scholar CrossRef Search ADS PubMed 25. Lee JM , Whang K , Cho SM et al. Factors affecting optimal time of cranioplasty: Brain sunken ratio . Korean J Neurotrauma . 2017 ; 13 ( 2 ): 113 - 118 . Google Scholar CrossRef Search ADS PubMed 26. Chibbaro S , Vallee F , Beccaria K et al. The impact of early cranioplasty on cerebral blood flow and its correlation with neurological and cognitive outcome. Prospective multi-centre study on 24 patients . Rev Neurol (Paris) . 2013 ; 169 ( 3 ): 240 - 248 . Google Scholar CrossRef Search ADS PubMed 27. Ganau M , Syrmos N , Paris M et al. Current and future applications of biomedical engineering for proteomic profiling: Predictive biomarkers in neuro-traumatology . Medicines . 2018 ; 5 ( 1 ): 19 . Google Scholar CrossRef Search ADS Copyright © 2018 by the Congress of Neurological Surgeons This article is published and distributed under the terms of the Oxford University Press, Standard Journals Publication Model (https://academic.oup.com/journals/pages/about_us/legal/notices)

Journal

NeurosurgeryOxford University Press

Published: May 26, 2018

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