Skip to main content

Advertisement

SpringerLink
Log in

Improvement in neurological outcome and brain hemodynamics after late cranioplasty

  • Original Article - Brain trauma
  • Published:
Acta Neurochirurgica Aims and scope Submit manuscript

Abstract

Background

Early cranioplasty has been encouraged after decompressive craniectomy (DC), aiming to reduce consequences of atmospheric pressure over the opened skull. However, this practice may not be often available in low-middle-income countries (LMICs). We evaluated clinical improvement, hemodynamic changes in each hemisphere, and the hemodynamic balance between hemispheres after late cranioplasty in a LMIC, as the institution’s routine resources allowed.

Methods

Prospective cohort study included patients with bone defects after DC evaluated with perfusion tomography (PCT) and transcranial Doppler (TCD) and performed neurological examinations with prognostic scales (mRS, MMSE, and Barthel Index) before and 6 months after surgery.

Results

A final sample of 26 patients was analyzed. Satisfactory improvement of neurological outcome was observed, as well as significant improvement in the mRS (p = 0.005), MMSE (p < 0.001), and Barthel Index (p = 0.002). Outpatient waiting time for cranioplasty was 15.23 (SD 17.66) months. PCT showed a significant decrease in the mean transit time (MTT) and cerebral blood volume (CBV) only on the operated side. Although most previous studies have shown an increase in cerebral blood flow (CBF), we noticed a slight and nonsignificant decrease, despite a significant increase in the middle cerebral artery flow velocity in both hemispheres on TCD. There was a moderate correlation between the MTT and contralateral muscle strength (r =  − 0.4; p = 0.034), as well as between TCD and neurological outcomes ipsilateral (MMSE; r = 0.54, p = 0.03) and contralateral (MRS; p = 0.031, r =  − 0.48) to the operated side.

Conclusion

Even 1 year after DC, cranioplasty may improve cerebral perfusion and neurological outcomes and should be encouraged.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

Data availability

Datasets are available on request. The raw data supporting the conclusions of this article will be made available by the authors, without undue reservation.

References

  1. Akins PT, Guppy KH (2008) Sinking skin flaps, paradoxical herniation, and external brain tamponade: a review of decompressive craniectomy management. Neurocrit Care 9:269–276. https://doi.org/10.1007/s12028-007-9033-z

    Article  PubMed  Google Scholar 

  2. Amorim RL, Bor-Seng-Shu E, G SG, Paiva W, de Andrade AF, Teixeira MJ (2012) Decompressive craniectomy and cerebral blood flow regulation in head injured patients: a case studied by perfusion CT. J Neuroradiol 39:346-349. https://doi.org/10.1016/j.neurad.2012.02.006

  3. Amorim RL, de Andrade AF, Gattas GS, Paiva WS, Menezes M, Teixeira MJ, Bor-Seng-Shu E (2014) Improved hemodynamic parameters in middle cerebral artery infarction after decompressive craniectomy. Stroke 45:1375–1380. https://doi.org/10.1161/STROKEAHA.113.003670

    Article  PubMed  Google Scholar 

  4. Carota A, Pintucci M, Zanchi F, D’Ambrosio E, Calabrese P (2011) ‘Cognitive’ sinking skin flap syndrome. Eur Neurol 66:227–228. https://doi.org/10.1159/000331939

    Article  CAS  PubMed  Google Scholar 

  5. Chibbaro S, Vallee F, Beccaria K, Poczos P, Makiese O, Fricia M, Mateo J, Gobron C, Guichard JP, Romano A, Levy B, George B, Vicaut E (2013) 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) 169:240–248. https://doi.org/10.1016/j.neurol.2012.06.016

    Article  CAS  Google Scholar 

  6. Coelho F, Oliveira AM, Paiva WS, Freire FR, Calado VT, Amorim RL, Neville IS, de Andrade AF, Bor-Seng-Shu E, Anghinah R, Teixeira MJ (2014) Comprehensive cognitive and cerebral hemodynamic evaluation after cranioplasty. Neuropsychiatr Dis Treat 10:695–701. https://doi.org/10.2147/ndt.S52875

    Article  PubMed  PubMed Central  Google Scholar 

  7. de Quintana-Schmidt C, Clavel-Laria P, Asencio-Cortes C, Vendrell-Brucet JM, Molet-Teixido J (2011) Sinking skin flap syndrome. Rev Neurol 52:661–664

    PubMed  Google Scholar 

  8. Dujovny M, Aviles A, Agner C, Fernandez P, Charbel FT (1997) Cranioplasty: cosmetic or therapeutic? Surg Neurol 47:238–241. https://doi.org/10.1016/s0090-3019(96)00013-4

    Article  CAS  PubMed  Google Scholar 

  9. Erdogan E, Duz B, Kocaoglu M, Izci Y, Sirin S, Timurkaynak E (2003) The effect of cranioplasty on cerebral hemodynamics: evaluation with transcranial Doppler sonography. Neurol India 51:479–481

    CAS  PubMed  Google Scholar 

  10. Gadde J, Dross P, Spina M (2012) Syndrome of the trephined (sinking skin flap syndrome) with and without paradoxical herniation: a series of case reports and review. Del Med J 84:213–218

    PubMed  Google Scholar 

  11. Grant FC, Norcross NC (1939) Repair of cranial defects by cranioplasty. Ann Surg 110:488–512. https://doi.org/10.1097/00000658-193910000-00002

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Halani SH, Chu JK, Malcolm JG, Rindler RS, Allen JW, Grossberg JA, Pradilla G, Ahmad FU (2017) Effects of Cranioplasty on cerebral blood flow following decompressive craniectomy: a systematic review of the literature. Neurosurgery 81:204–216. https://doi.org/10.1093/neuros/nyx054

    Article  PubMed  Google Scholar 

  13. Iaccarino C, Carretta A, Nicolosi F, Morselli C (2018) Epidemiology of severe traumatic brain injury. J Neurosurg Sci 62:535–541. https://doi.org/10.23736/S0390-5616.18.04532-0

    Article  PubMed  Google Scholar 

  14. Iaccarino C, Kolias A, Adelson PD, Rubiano AM, Viaroli E, Buki A, Cinalli G, Fountas K, Khan T, Signoretti S, Waran V, Adeleye AO, Amorim R, Bertuccio A, Cama A, Chesnut RM, De Bonis P, Estraneo A, Figaji A, Florian SI, Formisano R, Frassanito P, Gatos C, Germanò A, Giussani C, Hossain I, Kasprzak P, La Porta F, Lindner D, Maas AIR, Paiva W, Palma P, Park KB, Peretta P, Pompucci A, Posti J, Sengupta SK, Sinha A, Sinha V, Stefini R, Talamonti G, Tasiou A, Zona G, Zucchelli M, Hutchinson PJ, Servadei F (2020) Consensus statement from the international consensus meeting on post-traumatic cranioplasty. Acta Neurochir (Wien). https://doi.org/10.1007/s00701-020-04663-5

    Article  Google Scholar 

  15. Isago T, Nozaki M, Kikuchi Y, Honda T, Nakazawa H (2004) Sinking skin flap syndrome: a case of improved cerebral blood flow after cranioplasty. Ann Plast Surg 53:288–292. https://doi.org/10.1097/01.sap.0000106433.89983.72

    Article  PubMed  Google Scholar 

  16. Jeyaraj P (2015) Importance of early cranioplasty in reversing the “syndrome of the trephine/motor trephine syndrome/sinking skin flap syndrome”. J Maxillofac Oral Surg 14:666–673. https://doi.org/10.1007/s12663-014-0673-1

    Article  PubMed  Google Scholar 

  17. Kamalian S, Kamalian S, Konstas AA, Maas MB, Payabvash S, Pomerantz SR, Schaefer PW, Furie KL, Gonzalez RG, Lev MH (2012) CT perfusion mean transit time maps optimally distinguish benign oligemia from true “at-risk” ischemic penumbra, but thresholds vary by postprocessing technique. AJNR Am J Neuroradiol 33:545–549. https://doi.org/10.3174/ajnr.A2809

    Article  PubMed  PubMed Central  Google Scholar 

  18. Kolias AG, Viaroli E, Rubiano AM, Adams H, Khan T, Gupta D, Adeleye A, Iaccarino C, Servadei F, Devi BI, Hutchinson PJ (2018) The current status of decompressive craniectomy in traumatic brain injury. Curr Trauma Rep 4:326–332. https://doi.org/10.1007/s40719-018-0147-x

    Article  PubMed  PubMed Central  Google Scholar 

  19. Kuo JR, Wang CC, Chio CC, Cheng TJ (2004) Neurological improvement after cranioplasty - analysis by transcranial doppler ultrasonography. J Clin Neurosci 11:486–489. https://doi.org/10.1016/j.jocn.2003.06.005

    Article  PubMed  Google Scholar 

  20. Las DE, Verwilghen D, Mommaerts MY (2020) A systematic review of cranioplasty material toxicity in human subjects. J Craniomaxillofac Surg. https://doi.org/10.1016/j.jcms.2020.10.002

    Article  PubMed  Google Scholar 

  21. Maeshima S, Kagawa M, Kishida Y, Kobayashi K, Makabe T, Morita Y, Kunishio K, Matsumoto A, Tsubahara A (2005) Unilateral spatial neglect related to a depressed skin flap following decompressive craniectomy. Eur Neurol 53:164–168. https://doi.org/10.1159/000086129

    Article  CAS  PubMed  Google Scholar 

  22. Martin NA, Patwardhan RV, Alexander MJ, Africk CZ, Lee JH, Shalmon E, Hovda DA, Becker DP (1997) Characterization of cerebral hemodynamic phases following severe head trauma: hypoperfusion, hyperemia, and vasospasm. J Neurosurg 87:9–19. https://doi.org/10.3171/jns.1997.87.1.0009

    Article  CAS  PubMed  Google Scholar 

  23. Narapareddy BR, Narapareddy L, Lin A, Wigh S, Nanavati J, Dougherty J 3rd, Nowrangi M, Roy D (2020) Treatment of Depression After Traumatic Brain Injury: A Systematic Review Focused on Pharmacological and Neuromodulatory Interventions. Psychosomatics 61:481–497. https://doi.org/10.1016/j.psym.2020.04.012

    Article  PubMed  Google Scholar 

  24. Pan J, Zhang J, Huang W, Cheng X, Ling Y, Dong Q, Geng D (2013) Value of perfusion computed tomography in acute ischemic stroke: diagnosis of infarct core and penumbra. J Comput Assist Tomogr 37:645–649. https://doi.org/10.1097/RCT.0b013e31829866fc

    Article  PubMed  Google Scholar 

  25. Paredes I, Castano AM, Cepeda S, Alen JA, Salvador E, Millan JM, Lagares A (2016) The effect of cranioplasty on cerebral hemodynamics as measured by perfusion computed tomography and Doppler ultrasonography. J Neurotrauma 33:1586–1597. https://doi.org/10.1089/neu.2015.4261

    Article  PubMed  PubMed Central  Google Scholar 

  26. Piazza M, Grady MS (2017) Cranioplasty. Neurosurg Clin N Am 28:257–265. https://doi.org/10.1016/j.nec.2016.11.008

    Article  PubMed  Google Scholar 

  27. Richaud J, Boetto S, Guell A, Lazorthes Y (1985) Effects of cranioplasty on neurological function and cerebral blood flow. Neurochirurgie 31:183–188

    CAS  PubMed  Google Scholar 

  28. Sakamoto S, Eguchi K, Kiura Y, Arita K, Kurisu K (2006) CT perfusion imaging in the syndrome of the sinking skin flap before and after cranioplasty. Clin Neurol Neurosurg 108:583–585. https://doi.org/10.1016/j.clineuro.2005.03.012

    Article  PubMed  Google Scholar 

  29. Sarubbo S, Latini F, Ceruti S, Chieregato A, d’Esterre C, Lee TY, Cavallo M, Fainardi E (2014) Temporal changes in CT perfusion values before and after cranioplasty in patients without symptoms related to external decompression: a pilot study. Neuroradiology 56:237–243. https://doi.org/10.1007/s00234-014-1318-2

    Article  PubMed  Google Scholar 

  30. Schiffer J, Gur R, Nisim U, Pollak L (1997) Symptomatic patients after craniectomy. Surg Neurol 47:231–237. https://doi.org/10.1016/s0090-3019(96)00376-x

    Article  CAS  PubMed  Google Scholar 

  31. Song J, Liu M, Mo X, Du H, Huang H, Xu GZ (2014) Beneficial impact of early cranioplasty in patients with decompressive craniectomy: evidence from transcranial Doppler ultrasonography. Acta Neurochir (Wien) 156:193–198. https://doi.org/10.1007/s00701-013-1908-5

    Article  Google Scholar 

  32. Stiver SI, Wintermark M, Manley GT (2008) Reversible monoparesis following decompressive hemicraniectomy for traumatic brain injury. J Neurosurg 109:245–254. https://doi.org/10.3171/JNS/2008/109/8/0245

    Article  PubMed  Google Scholar 

  33. Stocchetti N, Picetti E, Berardino M, Buki A, Chesnut RM, Fountas KN, Horn P, Hutchinson PJ, Iaccarino C, Kolias AG, Koskinen LO, Latronico N, Maas AI, Payen JF, Rosenthal G, Sahuquillo J, Signoretti S, Soustiel JF, Servadei F (2014) Clinical applications of intracranial pressure monitoring in traumatic brain injury : report of the Milan consensus conference. Acta Neurochir (Wien) 156:1615–1622. https://doi.org/10.1007/s00701-014-2127-4

    Article  Google Scholar 

  34. Teasdale TW, Engberg AW (2001) Suicide after traumatic brain injury: a population study. J Neurol Neurosurg Psychiatry 71:436–440. https://doi.org/10.1136/jnnp.71.4.436

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Tsianaka E, Drosos E, Singh A, Tasiou A, Gatos C, Fountas K (2020) Post-cranioplasty complications: lessons from a prospective study assessing risk factors. J Craniofac Surg Publish Ahead of Print. https://doi.org/10.1097/scs.0000000000007344

  36. Wen L, Lou HY, Xu J, Wang H, Huang X, Gong JB, Xiong B, Yang XF (2015) The impact of cranioplasty on cerebral blood perfusion in patients treated with decompressive craniectomy for severe traumatic brain injury. Brain Inj 29:1654–1660. https://doi.org/10.3109/02699052.2015.1075248

    Article  PubMed  Google Scholar 

  37. Winkler PA, Stummer W, Linke R, Krishnan KG, Tatsch K (2000) The influence of cranioplasty on postural blood flow regulation, cerebrovascular reserve capacity, and cerebral glucose metabolism. Neurosurg Focus 8:e9. https://doi.org/10.3171/foc.2000.8.1.1920

    Article  CAS  PubMed  Google Scholar 

  38. Yamaura A, Makino H (1977) Neurological deficits in the presence of the sinking skin flap following decompressive craniectomy. Neurol Med Chir (Tokyo) 17:43–53. https://doi.org/10.2176/nmc.17pt1.43

    Article  CAS  Google Scholar 

  39. Zhao YH, Gao H, Ma C, Huang WH, Pan ZY, Wang ZF, Li ZQ (2020) Earlier cranioplasty following posttraumatic craniectomy is associated with better neurological outcomes at one-year follow-up: a two-centre retrospective cohort study. Br J Neurosurg:1–11. https://doi.org/10.1080/02688697.2020.1853042

  40. Zheng F, Xu H, von Spreckelsen N, Stavrinou P, Timmer M, Goldbrunner R, Cao F, Ran Q, Li G, Fan R, Zhang Q, Chen W, Yao S, Krischek B (2018) Early or late cranioplasty following decompressive craniotomy for traumatic brain injury: a systematic review and meta-analysis. J Int Med Res 46:2503–2512. https://doi.org/10.1177/0300060518755148

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

We dedicate this study to all patients of São Paulo University.

Author information

Authors and Affiliations

  1. Division of Neurosurgery, University of São Paulo, 255 Enéas de Carvalho Aguiar, São Paulo, 05403-010, Brazil

    Arthur Maynart Pereira Oliveira, Robson Luis Oliveira Amorim, Sérgio Brasil, Almir Ferreira de Andrade, Fernando Mendes Paschoal Junior, Edson Bor-Seng-Shu, Manoel Jacobsen Teixeira & Wellingson Silva Paiva

  2. Department of Medicine, Federal University of Sergipe, Aracaju, Brazil

    Arthur Maynart Pereira Oliveira

  3. Division of Neurosurgery, Surgery Hospital - FBHC, Aracaju, Brazil

    Arthur Maynart Pereira Oliveira

  4. Department of Surgery, Federal University of Amazonas, Manaus, Brazil

    Robson Luis Oliveira Amorim

  5. Division of Radiology, University of São Paulo, São Paulo, Brazil

    Gabriel Scarabotolo Gattás

  6. Department of Biomedical, Metabolic and Neural Sciences, University of Modena and Reggio Emilia, Modena, Italy

    Corrado Iaccarino

Authors
  1. Arthur Maynart Pereira Oliveira
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Robson Luis Oliveira Amorim
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Sérgio Brasil
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Gabriel Scarabotolo Gattás
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Almir Ferreira de Andrade
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Fernando Mendes Paschoal Junior
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Edson Bor-Seng-Shu
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Corrado Iaccarino
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Manoel Jacobsen Teixeira
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Wellingson Silva Paiva
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

AM and RL conception of the work, overall data collection, data analysis and interpretation, drafting the article, and final approval of the version to be published; WP conception of the work, data analysis, and interpretation and critical revision of the article; GS radiological data collection and interpretation; AF conception of the work and critical revision of the article; FM, EB transcranial Doppler data collection and interpretation; CI, MJ, and SB critical revision of the article. All authors contributed to manuscript revision, read and approved the submitted version.

Corresponding author

Correspondence to Sérgio Brasil.

Ethics declarations

Ethical approval

All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.

Informed consent

Informed consent was obtained from all individual participants included in the study.

Conflict of interest

The authors declare no competing interests.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Comments

Decompressive craniectomy effectively lowers ICP in patients with intracranial hypertension (e.g., following traumatic brain injury) and decreases the risk of intracranial herniation (e.g., following major ischaemic strokes). However, the treatment creates an abnormal intracranial physiology due to the post-operative incomplete rigid covering of the brain. The large skull defect probably affects cerebral autoregulation and, local blood flow, as well as CSF circulation and other fluid movements inside the brain. For some years, it is well recognized that cranioplasty improves neurological status in many patients and some studies have shown improved blood flow and normalized intracranial pressure physiology following the procedure, which might explain the positive clinical effect. The optimal timing of cranioplasty is, however, unknown and often depends of the individual patient. Most clinicians will probably consider the procedure at around 3 months after decompression. In this prospective study, the authors demonstrate that even delayed cranioplasty beyond 1 year after decompression seems to improve neurological status and reduce disabling symptoms such as posture- related headache. As traumatic brain injury occurs more frequently in low-middle income countries in which early cranioplasty is now always possible, the findings of this study are important and encourage cranioplasty even late after the primary procedure.

Alexander Lilja-Cyron, MD PhD

Rigshospitalet, Copenhagen, Denmark

Apart from concomitant medical treatment and intensive rehabilitative work, neurosurgical therapy can contribute significantly to the recovery of patients after decompressive craniectomy and its underlying cause. In this respect, the authors have added a valuable article to the literature on management of skull defects and cranioplasty. The results of their prospective study suggest that also late closure of the calotte can improve cerebral perfusion and clinical outcome. Although the benefits of early over late cranioplasty regarding both brain protection and hemodynamics, and patient recovery and esthetic aspect are obvious, this is not always feasible in a timely manner. The reasons for delayed cranioplasty can include the respective patient’'s clinical status, the institution’'s own resources, the conditions of the country the patients are living in, or the health care system the hospitals are embedded in. In addition, very early cranioplasty may be associated with potential problems such as increased intracranial pressure and risk of cerebrospinal fluid fistulas, depending on an accompanying brain swelling or the corresponding decompression technique applied. The main drawbacks of the present study are a small patient sample and lack of a control group. Despite these limitations, the authors could demonstrate that late cranioplasty seems to be reasonable and can be done effectively even one year after decompressive surgery with improvement of brain hemodynamics and neurological status.

Markus Florian Oertel

Zurich, Switzerland

This article is part of the Topical Collection on Brain trauma

University of São Paulo, School of Medicine Ethics Committee registration number: 0748/10

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Oliveira, A.M.P., Amorim, R.L.O., Brasil, S. et al. Improvement in neurological outcome and brain hemodynamics after late cranioplasty. Acta Neurochir 163, 2931–2939 (2021). https://doi.org/10.1007/s00701-021-04963-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00701-021-04963-4

Keywords

Search

Navigation