British Journal of Neurosurgery, February 2015; 29(1): 64–69 © 2014 The Neurosurgical Foundation ISSN: 0268-8697 print / ISSN 1360-046X online DOI: 10.3109/02688697.2014.957157
ORIGINAL ARTICLE
Autologous cranioplasty following decompressive craniectomy in the trauma setting Wessam El Ghoul1, Stuart Harrisson2 & Antonio Belli3 1Department of Neurosurgery, Skane University Hospital, Lund, Sweden, 2Department of Neurosurgery, Wessex Neurological
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Centre, Southampton Hospital University Trust, Southampton, UK, and 3NIHR Surgical Reconstruction and Microbiology Research Centre, University Hospitals Birmingham, Birmingham, UK
Abstract Background. Decompressive craniectomy (DC) is an option for the treatment of increased intracranial pressure resulting from an acute neurological insult, including insults caused by trauma. When the brain swelling has receded, the skull is reconstructed with a wide choice of materials, each with its own advantages and disadvantages in terms of cost, cosmetic appearance, biocompatibility, implant strength and complication rate. Autologous cranioplasty (AC), where the patient’s own bone flap is stored and reutilised, is common in many countries. No outcome studies have, however, been published on this technique for traumatic injuries. Methods. A retrospective study was conducted including all AC operations performed following DC due to traumatic brain injury. All operations were performed in one institution during a 4-year time period. Results were analysed for complication rates. Results. 44 cases were included. The mean time from craniotomy to cranioplasty was 86 (95% CI: 63–109) days. Complications severe enough to warrant readmission or further surgery were found in 13 cases (30%). No statistically significant predictor of complication from cranioplasty was detected. The complication rate was similar to published data on cranioplasty using artificial prosthetic materials. Conclusions. AC in the trauma setting is a valid treatment option with a complication rate that seems no worse than other alternatives.
This leaves the patient with a large bone defect, which in the vast majority of cases will need eventual repair.3 The indications for repair are protection of the vulnerable brain, cosmesis and facilitation of physiotherapy and mobilisation.4 Additionally, patients who have a large DC can report delayed neurological deterioration or poor recovery, known as syndrome of the trephined, as well as headaches, hygromas, hydrocephalus and discomfort. Improvement of neurological function following skull reconstruction has frequently been reported in the literature.5,6 Reconstruction cannot take place until the cerebral swelling has settled and it is common for patients to have their cranioplasty weeks or months after the decompression. Options for reconstruction are numerous and include autologous cranioplasty or construction of a replacement flap from synthetic material.3,4 If autologous cranioplasty is used, this presents the challenge of where to store the bone flap before reinsertion. The options are external cryopreservation and internal storage in the patient, often in the abdominal subcutaneous tissue. In our institution, we routinely perform autologous cranioplasty (AC) after storage of the bone flap in the abdominal wall, as our treatment of choice after post-traumatic DC. While AC is undoubtedly cheaper than custom-made synthetic materials, there are questions over its viability in traumatic cases since the risk of contamination at time of injury could be high. Cranioplasty, whatever material is used, has a high complication rate, including catastrophic intracranial haemorrhage, neurological deterioration, wound dehiscence, subgaleal collection, cerebrospinal fluid (CSF) leak, poor cosmetic result, implant failure and subacute or chronic infection. As there is no previously published literature on the outcome and complication rate of AC in trauma using a bone flap stored in a subcutaneous pouch in the patient’s abdomen, it will be useful to present our experience in using this technique at a single centre. This complements a recently
Keywords: complications; cranioplasty; decompressive craniectomy; traumatic brain injury; treatment
Introduction Decompressive craniectomy (DC) is performed as a lifesaving measure in patients with raised intra-cranial pressure as both primary (removing a space-occupying lesion) and secondary (removing a bone flap to treat diffuse swelling) procedures. The cause can be trauma, intracerebral haemorrhage, ischaemic stroke or other acute neurological insults.1,2
Correspondence: Wessam El Ghoul, Department of Neurosurgery, Skane University Hospital, 221 85 Lund, Sweden. E-mail: [email protected] Received for publication 1 April 2014; accepted 14 August 2014
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Autologous cranioplasty following decompressive craniectomy published study, which investigated the use of AC with flap stored frozen externally.7
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Materials and methods Data were collected from Wessex Neurological Centre in Southampton, UK, a regional major trauma centre. Using the head injury database of patients admitted, we identified all cases who underwent a DC for traumatic brain injury between 2007 and 2010. The relevant case notes were reviewed and the presence of skull fractures and extent of DC were recorded together with patient age, gender, pre-existing medical conditions, seniority of primary operator and mechanisms of injury. Records were then followed to establish the type of cranioplasty used and the presence of complications including infections, follow-up period and overall outcome. Cases were excluded if no AC was performed or if a synthetic implant was used to reconstruct the skull. Statistical analysis was conducted using SPSS for windows version 19 (IBM). Data were analysed using bivariate correlation and linear regression models to attempt and establish any risk factors of poor outcomes. Statistical significance was established at p ⬍ 0.05.
Subcutaneous abdominal storage of the autologous bone flap At the time of decompressive craniectomy, the excised bone flap is placed into the subcutaneous space in the patient’s abdominal wall. This space is accessed by an appropriately sized transverse incision in the right abdominal wall (up to 10 cm in length) midway between the costal margin and the anterior superior iliac spine. The bone flap has to be sited high enough for it to not impact on the iliac crest in the sitting position, as this may be uncomfortable and may hinder the early stage of rehabilitation. A space is created just superficial to the abdominal wall muscles into which the bone flap can be placed. If necessary, the bone flap may be divided into two pieces to allow it to fit into the subcutaneous pouch. It is recommended, if the bone flap is in multiple fragments, that these are reconstructed into one or two pieces prior to storage in the abdominal wall, as this will later aid reconstruction. Any sharp edges will have to be trimmed back, whilst avoiding excessive bone removal. After haemostasis the skin is closed over the bone flap.
Reconstruction This is technically straightforward. Prophylactic antibiotics were used in all cases (single dose on induction and no postoperative antibiotics). Chlorhexidine alone was used for skin preparation. The bone flap was retrieved from the abdomen and washed in an antiseptic solution, which was thoroughly rinsed with saline before re-implantation. We inspected the bone flap for signs of infection before the scalp incision. It is important to note that a serous or serosanguinous collection in the abdominal pouch is common and this is not a sign of infection. In most cases, we laid a protective silastic sheet to cover the dura and dural defect (trimmed using the bone flap as template to fit the bony defect precisely) at craniectomy to prevent adhesions between the temporalis muscle or the
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subcutaneous tissue and the brain or dura. This facilitates and expedites tissue dissection at cranioplasty, thereby reducing operating time. The bone flap was then fixed to the craniectomy edge using mini-plates. A wound drain was used at the surgeon’s discretion, but in this series this was avoided in the majority of cases. Wound was closed using vicryl for galea and staples for the skin.
Results Between October 2007 and October 2010, a total of 53 decompressive craniotomies were performed for traumatic brain injury. Of those, 40 were male and 13 female with a mean age of 37 (32–41) years. Forty-four of these cases underwent autologous cranioplasty and where included in the analysis. The excluded cases consisted of five who had titanium mesh cranioplasty, one who had a combination of both materials, two who did not survive to have cranioplasty and one case who refused cranioplasty. Two patients in the series were intravenous drug abusers (IVDA) and 2 had pre-existing heart conditions. As for mechanism, 23 (52%) were due to falls, 13 (30%) due to road traffic accidents (RTA) and 8 (18%) due to assaults. Twenty-one (47%) of cases suffered some form of a skull fracture. Twenty-eight (64%) of the DC performed were for primary evacuation of an intracranial haematoma, while the rest were secondary procedures for cerebral swelling (Table I). Twenty-eight (64%) of the operations were unilateral and 16 (36%) were bifrontal. All data are presented in Table I. Twenty-nine (66%) of the operations were performed by a specialist trainee with at least 2 years of neurosurgical training. Six (14%) operations were performed at consultant level. Seniority of the primary operator was not recorded in the remaining cases. Mean interval from DC to cranioplasty was 86 (95% CI: 63–109) days. Mean time for duration of hospital stay after cranioplasty was 8 days.4–12 Mean follow-up was 8 (95% CI: 6–11) months with 6 deaths noted in patients who underwent AC (Table II), of which only 1 was in the immediate post-operative period. Mild complications were found in 21 cases (46%) (Table III). Major complications, however (Tables IV and V), severe enough to warrant readmission and/or reoperation were found in a total of 13 cases (30%). One of those cases developed a hydrocephalus after AC, which required insertion of a ventriculoperitoneal (VP) shunt, and died 6 months later due to sepsis. Mean duration of stay during readmission was 9 days6–23 with mode of 1 day and median of 2 days. In terms of post-operative infection, only 2 cases were identified: 1 of them needed revision using titanium mesh, while the other was managed using antibiotics only. The responsible organism was Staphylococcus aureus in both cases. No statistically significant predictor of poor outcome from cranioplasty was detected (age, gender, presence of skull fracture, delay to cranioplasty, seniority of operator or co-morbidities) using bivariate correlations and regression analysis.
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Table I. Summary of findings. Case Age Gender 1 2 3 4 5 6 7
4 63 18 39 40 20 78
M F M M M M F
8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44
35 37 77 25 21 57 42 34 40 33 55 20 26 43 57 26 36 38 18 19 41 34 39 35 35 20 36 67 30 19 71 36 34 33 46 17 28
F M F M M M F F M M M M M M M M M M M M F M M M M M M M M M M M F M M F M
Co-Morbidities – – –
IVDA – – Hypertension, ischaemic heart disease – – – – – – – – Hepatitis B carrier – – – – – – – – – – – – IVDA Epilepsy – – – Alcoholic liver disease Chronic lymphocytic leukaemia – – Atrial fibrillation – – – – Juvenile arthritis –
Discussion As the evidence base for DC in trauma is still being assessed with published results from the DECRA trial and the final results of RescueICP trial are awaited, cranioplasty also needs to be thoroughly evaluated and best practice established.8,9 Evidence for which type of cranioplasty and in what setting it is to be used is lacking. In this study we have shown a single unit’s experience of AC in the setting of trauma. We cannot offer any firm conclusions as to what might be a risk factor Table II. Mortality. Age (years) Survival after AC 19
6 months
26 28 37 77
1 year 1 year 22 months 5 days (9 days after sustaining primary injury)
78
26 months
Mechanisms Skull fracture
DC type
Extent of DC
Fall Fall RTA RTA Assault RTA RTA
Yes No No Yes No Yes No
Primary Primary Primary Secondary Primary Primary Primary
Bifrontal Unilateral Unilateral Unilateral Bifrontal Unilateral Unilateral
Fall Fall Fall RTA Fall RTA Assault Fall Fall RTA Fall RTA RTA Assault Fall RTA Assault Fall RTA RTA Fall Assault Fall Assault Fall Assault Fall Fall Fall Assault Fall Fall Fall Fall Fall RTA Fall
No Yes No No Yes Yes No Yes Yes No No Yes Yes Yes Yes No Yes No Yes No No Yes Yes No No No No Yes Yes Yes No No Yes Yes No Yes No
Secondary Secondary Primary Primary Primary Secondary Secondary Secondary Secondary Primary Secondary Primary Primary Primary Secondary Secondary Secondary Primary Secondary Secondary Primary Primary Secondary Secondary Primary Primary Primary Primary Primary Primary Primary Primary Primary Secondary Primary Primary Primary
Unilateral Bifrontal Unilateral Bifrontal Unilateral Bifrontal Bifrontal Bifrontal Unilateral Bifrontal Bifrontal Unilateral Unilateral Unilateral Unilateral Bifrontal Unilateral Unilateral Bifrontal Unilateral Unilateral Bifrontal Unilateral Unilateral Unilateral Unilateral Unilateral Unilateral Bifrontal Unilateral Unilateral Unilateral Bifrontal Bifrontal Unilateral Bifrontal Unilateral
for complication. It is unlikely for single-centre cohort studies or case series to elucidate whether the complications are directly associated with the choice of implant, given the significant variability in risk factors, such as co-morbidity, recovery status, mechanism of injury, timing of surgery, size and location of the DC. A national cranial reconstruction register has been proposed, which will hopefully provide sufficient cases for a multivariate analysis.10 The cosmetic results of AC are good and there is no risk of foreign body reaction.11 However, there is the challenge of preserving the bone flap in such condition as to allow
Cause Sepsis and multi-organ failure Pneumonia Unknown Aspiration pneumonia Primary injury: treatment withdrawn in view of poor prognosis Unknown
Table III. Summary of the mild complications reported. Mild Complication Headaches Ridging at edge of cranioplasty Mild facial drop Minor pulmonary embolism Pneumonia Fluctuating wound swelling Subjective sensation of instability in bone flap
Autologous cranioplasty following decompressive craniectomy Table IV. Major complications during index admission. Complication Management
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Extradural haematoma Wound drain stuck Extradural haematoma Worsening contusions
Burr hole evacuation Removal of drain in operating theatre Craniotomy evacuation Death
maintenance of bony structure and shape, and prevention of contamination. Two solutions are frequently used that solve this issue. Cryopreservation, i.e. sterilising and storing the bone flap in a freezer, is one option.12 This is most commonly used, although no universally agreed guidelines exist with regard to temperature for storage and choice of storage medium.1 Routine practice is to sterilise the bone flap prior to cryopreservation at temperatures of up to ⫺ 80°C, although a recent paper reported good results when using higher temperatures.13 Several problems exist with this approach though. Primarily, this runs the risk of denaturation and inactivation of pro-osteoblastic proteins in the bone flap.14 This can lead to excessive bone reabsorption and impaired healing. Storage of the bone flap can also be costly due to logistic, legislative and regulatory requirements, such as freezer maintenance, temperature monitoring, correct labelling of the bone flap and prevention of infection. The second available option for storage is inside the patient’s own subcutaneous tissue, normally in the abdomen as described here.15 The bone flap can also be stored in the subgaleal space, thereby avoiding the need for a further incision in the abdomen. This storage solution avoids the risk of devitalising the bone flap and the problems associated with external storage. The subcutaneous tissue is naturally sterile, accessible and physiologically suitable for granulation thereby maintaining bone flap integrity.1,4 We encountered no problems with bone resorption by storing the flap internally, a problem which is often reported in other case series using cryopreservation of bone flap.7 There are instances where AC may not be possible. The bone flap might be shattered into small fragments that would be impractical to piece together, or it may be contaminated. Various synthetic materials have, therefore, been developed for repair of the cranial defect after craniectomy.5,16,17 These include titanium plates, polymethylmethacrylate (PMMA), polyether ether ketone and hydroxyapatite. Some materials Table V. Cases readmitted. Readmission cause Wound infection CSF collection Hydrocephalus CSF collection Extra-axial wound haematoma Poor cosmesis Stroke with dysphasia Wound infection Bony step and temporal hollowing
Duration of stay (days) 8 1 66 2 1 1 2 3 1
Management Treated with antibiotics Needle aspiration VP shunt insertion Lumbar shunt insertion Conservative Revision with titanium mesh Conservative Bone flap removal and titanium mesh cranioplasty at a later admission Titanium mesh cranioplasty
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can either be shaped directly by the surgeon in theatre or be custom-made in advance.4 The advantage is that these various materials can be used in the absence of the original bone flap. One study also found synthetic cranioplasty to last significantly longer than autologous bone flaps.18 Disadvantages include manufacturing and planning costs (custom-made implants usually require a planning stereology scan), biocompatibility issues and the potential technical challenge in shaping and securing the implant.19
Timing Following removal of bone flap the brain will need several days to weeks to recover from the acute swelling.20,21 Once the acute phase is over and the patient starts to recover, the question of when to perform the cranioplasty arises. Previously accepted practice was for patients to wait for up to 6 months before having their skull reconstruction.18,22 The logic behind this delay was dictated by concerns regarding missing a diagnosis of late-presentation hydrocephalus and a hypothetical heightened risk of infection with early surgery.3 Delaying the cranioplasty, however, carries its own risks. Communicating hydrocephalus can occur and prolonged exposure to atmospheric pressure may cause mass effect leading to paradoxical herniation of brain.23,24 Additionally, there is a suggestion that skull reconstruction may have some direct benefit on neurological recovery.25 A recently published case series further supports this theory.26 Early reconstruction facilitates rehabilitation and offers structural integrity when the patient starts to mobilise, avoiding the need for protective helmets to be worn.27 Several studies have, therefore, been completed to assess whether earlier cranioplasty after DC is safe. One study found that cranioplasty at 2–6 weeks post craniectomy showed no increase in risks of infection or hydrocephalus but it did expedite patient transfer to rehabilitation and improve outcome.3 A further study assessing neurological function after early cranioplasty revealed marked improvement with no significant increase in complication rates.22 Improvements have also been observed radiologically. CT perfusion scans have shown enhanced cerebral perfusion, while improved CSF flow has been confirmed using contrast MRI and lumbar puncture pressure measurements.28,29 Despite some variability in practice, there is consensus that cranioplasty should be performed as soon as brain oedema has settled. However, given the benefit of early rehabilitation, it is common practice to defer the reconstruction until the initial rehabilitative intervention has been delivered. Patients at our centre had a mean waiting time to AC of 86 days.
Complications Cranioplasty can lead to the same complications as any other surgical procedure such as risks associated with anaesthesia, haemorrhage and wound infection. Complications more specific to the procedure are hydrocephalus, extra-axial collection, seizures and bone flap infection.5 Overall complication rates reported vary greatly ranging from 0 to 34%.5,12,30–32 This wide range is not surprising given that these case series have evaluated different methods of cranioplasty in different
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patient populations. Use of synthetic materials does seem to account for a rise in infection rate compared to autologous bone flaps.3,18 The difference is significant with the infection risk nearly doubled. An explanation for this dramatic difference is potentially due to the fact that synthetic implants are often resorted to after failure of AC.3 Direct comparison between PMMA and titanium plates found no significant difference in overall complication rates.5 One study, on the other hand, reported titanium plates as the superior material in regard to risk of infection.19 It is also worth pointing out that cosmesis is one of the indications for cranioplasty but cosmetic complications are common, although rarely significant. They include uneven surfaces due to muscle atrophy, fluid collection and discontinuity between flap and skull bone.18 Mild, self-limiting complications not requiring rehospitalisation or further intervention are common. The total complication rate was 46% in our series; severe complications leading to readmission, reoperation or death occurred in 30% of cases. This figure is high but in line with other series.5,12,30–33 The fact that our study population consisted of traumatic cases only may also have contributed to the high complication rates. Of note is that only 2 cases developed an infection, one of which severe enough to warrant a surgical revision. We have no firm conclusions to offer as to why we had such a comparatively low infection rate. Dissection of the skin flap free from brain could be easier due to shorter waiting time for AC and the use of a silastic sheet over the dural plane at craniectomy to prevent adhesions. This could lead to less CSF leakage and shorter operation times. Of note is also that none of the deaths in the study can be linked directly to the cranioplasty.
Study limitations This study is retrospective and has, therefore, the limitation of a possible underreporting of adverse events. However, all AC cases were followed up and it is very unlikely that any significant surgical complications leading to readmission, reoperation or death were missed. Given the heterogeneity of the cohort and the low numbers of infections and reoperations recorded, the sample size does not allow a proper statistical analysis of the risk factors for significant complications.
Conclusions Autologous cranioplasty in trauma is a practical, straightforward technique that has a complication rate similar to that when used in non-trauma cases.
Acknowledgements We wish to thank Andrew Dunford for assisting in data collection. Declaration of interest: The authors report no declarations of interest. The authors alone are responsible for the content and writing of the paper.
References 1. Kakar V, Nagaria J, John Kirkpatrick P. The current status of decompressive craniectomy. Br J Neurosurg 2009;23:147–57. 2. Ahmed AI, Eynon CA , Kinton L, Nicoll JA , Belli A . Decompressive craniectomy for acute disseminated encephalomyelitis. Neurocrit Care 2010;13:393–5. 3. Beauchamp KM, Kashuk J, Moore EE, et al. Cranioplasty after postinjury decompressive craniectomy: is timing of the essence? J Trauma 2010;69:270–4. 4. Baldo S, Tacconi L. Effectiveness and safety of subcutaneous abdominal preservation of autologous bone flap after decompressive craniectomy: a prospective pilot study. World Neurosurg 2010;73:552–6. 5. Stephens FL, Mossop CM, Bell RS, et al. Cranioplasty complications following wartime decompressive craniectomy. Neurosurg Focus 2010;28: E3. 6. Stiver SI, Wintermark M, Manley GT. Reversible monoparesis following decompressive hemicraniectomy for traumatic brain injury. J Neurosurg 2008;109:245–54. 7. Honeybul S, Ho KM. How “successful” is calvarial reconstruction using frozen autologous bone? Plast Reconstr Surg 2012;130: 1110–7. 8. Cooper DJ, Rosenfeld JV, Murray L, et al. Decompressive craniectomy in diffuse traumatic brain injury. N Engl J Med 2011;364:1493–502. 9. Hutchinson PJ, Corteen E, Czosnyka M, et al. Decompressive craniectomy in traumatic brain injury: the randomized multicenter RESCUEicp study (www.RESCUEicp.com). Acta Neurochir Suppl 2006;96:17–20. 10. Kolias AG, Bulters DO, Cowie CJ, et al. Proposal for establishment of the UK Cranial Reconstruction Registry (UKCRR). Br J Neurosurg 2014;28:310–4. 11. Goldberg VM, Lance EM. Revascularization and accretion in transplantation. Quantitative studies of the role of the allograft barrier. J Bone Joint Surg Am 1972;54:807–16. 12. Bhaskar IP, Zaw NN, Zheng M, Lee GY. Bone flap storage following craniectomy: a survey of practices in major Australian Neurosurgical centres. ANZ J Surg 2011;81:137–41. 13. Tahir MZ, Shamim MS, Sobani ZA , et al. Safety of untreated autologous cranioplasty after extracorporeal storage at - 26 degree celsius. Br J Neurosurg 2013;27:479–82. 14. Ellis E III, Sinn DP. Use of homologous bone in maxillofacial surgery. J Oral Maxillofac Surg 1993;51:1181–93. 15. Flannery T, McConnell RS. Cranioplasty: why throw the bone flap out? Br J Neurosurg 2001;15:518–20. 16. Gladstone HB, McDermott MW, Cooke DD. Implants for cranioplasty. Otolaryngol Clin North Am 1995;28:381–400. 17. Gosain AK. Hydroxyapatite cement paste cranioplasty for the treatment of temporal hollowing after cranial vault remodeling in a growing child. J Craniofac Surg 1997;8:506–11. 18. Aziz TZ, Mathew BG, Kirkpatrick PJ. Bone flap replacement vs acrylic cranioplasty: a clinical audit. Br J Neurosurg 1990;4: 417–9. 19. Matsuno A , Tanaka H, Iwamuro H, et al. Analyses of the factors influencing bone graft infection after delayed cranioplasty. Acta Neurochir (Wien) 2006;148:535–40; discussion 40. 20. Aarabi B, Hesdorffer DC, Ahn ES, et al. Outcome following decompressive craniectomy for malignant swelling due to severe head injury. J Neurosurg 2006;104:469–79. 21. Jiang JY, Xu W, Li WP, et al. Efficacy of standard trauma craniectomy for refractory intracranial hypertension with severe traumatic brain injury: a multicenter, prospective, randomized controlled study. J Neurotrauma 2005;22:623–8. 22. Liang W, Xiaofeng Y, Weiguo L, et al. Cranioplasty of large cranial defect at an early stage after decompressive craniectomy performed for severe head trauma. J Craniofac Surg 2007;18:526–32. 23. Mazzini L, Campini R, Angelino E, et al. Posttraumatic hydrocephalus: a clinical, neuroradiologic, and neuropsychologic assessment of long-term outcome. Arch Phys Med Rehabil 2003;84:1637–41. 24. Waziri A , Fusco D, Mayer SA , McKhann GM II, Connolly ES Jr. Postoperative hydrocephalus in patients undergoing decompressive hemicraniectomy for ischemic or hemorrhagic stroke. Neurosurgery 2007;61:489–93; discussion 93–4. 25. Schmidt JH III, Reyes BJ, Fischer R, Flaherty SK. Use of hinge craniotomy for cerebral decompression. Technical note. J Neurosurg 2007;107:678–82.
Autologous cranioplasty following decompressive craniectomy
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26. Di Stefano C, Sturiale C, Trentini P, et al. Unexpected neuropsychological improvement after cranioplasty: a case series study. Br J Neurosurg 2012;26:827–31. 27. Ziai WC, Port JD, Cowan JA , et al. Decompressive craniectomy for intractable cerebral edema: experience of a single center. J Neurosurg Anesthesiol 2003;15:25–32. 28. Dujovny M, Aviles A , Agner C, Fernandez P, Charbel FT. Cranioplasty: cosmetic or therapeutic? Surg Neurol 1997;47: 238–41. 29. Krishnan P, Bhattacharyya AK , Sil K , De R. Bone flap preservation after decompressive craniectomy–experience with 55 cases. Neurol India 2006;54:291–2.
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30. Prolo DJ, Burres KP, McLaughlin WT, Christensen AH. Autogenous skull cranioplasty: fresh and preserved (frozen), with consideration of the cellular response. Neurosurgery 1979;4:18–29. 31. Gooch MR, Gin GE, Kenning TJ, German JW. Complications of cranioplasty following decompressive craniectomy: analysis of 62 cases. Neurosurg Focus 2009;26: E9. 32. Movassaghi K, Ver Halen J, Ganchi P, et al. Cranioplasty with subcutaneously preserved autologous bone grafts. Plast Reconstr Surg 2006;117:202–6. 33. Walcott BP, Kwon CS, Sheth SA , et al. Predictors of cranioplasty complications in stroke and trauma patients. J Neurosurg 2013; 118:757–62.
ORIGINAL ARTICLE
Autologous cranioplasty following decompressive craniectomy in the trauma setting Wessam El Ghoul1, Stuart Harrisson2 & Antonio Belli3 1Department of Neurosurgery, Skane University Hospital, Lund, Sweden, 2Department of Neurosurgery, Wessex Neurological
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Centre, Southampton Hospital University Trust, Southampton, UK, and 3NIHR Surgical Reconstruction and Microbiology Research Centre, University Hospitals Birmingham, Birmingham, UK
Abstract Background. Decompressive craniectomy (DC) is an option for the treatment of increased intracranial pressure resulting from an acute neurological insult, including insults caused by trauma. When the brain swelling has receded, the skull is reconstructed with a wide choice of materials, each with its own advantages and disadvantages in terms of cost, cosmetic appearance, biocompatibility, implant strength and complication rate. Autologous cranioplasty (AC), where the patient’s own bone flap is stored and reutilised, is common in many countries. No outcome studies have, however, been published on this technique for traumatic injuries. Methods. A retrospective study was conducted including all AC operations performed following DC due to traumatic brain injury. All operations were performed in one institution during a 4-year time period. Results were analysed for complication rates. Results. 44 cases were included. The mean time from craniotomy to cranioplasty was 86 (95% CI: 63–109) days. Complications severe enough to warrant readmission or further surgery were found in 13 cases (30%). No statistically significant predictor of complication from cranioplasty was detected. The complication rate was similar to published data on cranioplasty using artificial prosthetic materials. Conclusions. AC in the trauma setting is a valid treatment option with a complication rate that seems no worse than other alternatives.
This leaves the patient with a large bone defect, which in the vast majority of cases will need eventual repair.3 The indications for repair are protection of the vulnerable brain, cosmesis and facilitation of physiotherapy and mobilisation.4 Additionally, patients who have a large DC can report delayed neurological deterioration or poor recovery, known as syndrome of the trephined, as well as headaches, hygromas, hydrocephalus and discomfort. Improvement of neurological function following skull reconstruction has frequently been reported in the literature.5,6 Reconstruction cannot take place until the cerebral swelling has settled and it is common for patients to have their cranioplasty weeks or months after the decompression. Options for reconstruction are numerous and include autologous cranioplasty or construction of a replacement flap from synthetic material.3,4 If autologous cranioplasty is used, this presents the challenge of where to store the bone flap before reinsertion. The options are external cryopreservation and internal storage in the patient, often in the abdominal subcutaneous tissue. In our institution, we routinely perform autologous cranioplasty (AC) after storage of the bone flap in the abdominal wall, as our treatment of choice after post-traumatic DC. While AC is undoubtedly cheaper than custom-made synthetic materials, there are questions over its viability in traumatic cases since the risk of contamination at time of injury could be high. Cranioplasty, whatever material is used, has a high complication rate, including catastrophic intracranial haemorrhage, neurological deterioration, wound dehiscence, subgaleal collection, cerebrospinal fluid (CSF) leak, poor cosmetic result, implant failure and subacute or chronic infection. As there is no previously published literature on the outcome and complication rate of AC in trauma using a bone flap stored in a subcutaneous pouch in the patient’s abdomen, it will be useful to present our experience in using this technique at a single centre. This complements a recently
Keywords: complications; cranioplasty; decompressive craniectomy; traumatic brain injury; treatment
Introduction Decompressive craniectomy (DC) is performed as a lifesaving measure in patients with raised intra-cranial pressure as both primary (removing a space-occupying lesion) and secondary (removing a bone flap to treat diffuse swelling) procedures. The cause can be trauma, intracerebral haemorrhage, ischaemic stroke or other acute neurological insults.1,2
Correspondence: Wessam El Ghoul, Department of Neurosurgery, Skane University Hospital, 221 85 Lund, Sweden. E-mail: [email protected] Received for publication 1 April 2014; accepted 14 August 2014
64
Autologous cranioplasty following decompressive craniectomy published study, which investigated the use of AC with flap stored frozen externally.7
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Materials and methods Data were collected from Wessex Neurological Centre in Southampton, UK, a regional major trauma centre. Using the head injury database of patients admitted, we identified all cases who underwent a DC for traumatic brain injury between 2007 and 2010. The relevant case notes were reviewed and the presence of skull fractures and extent of DC were recorded together with patient age, gender, pre-existing medical conditions, seniority of primary operator and mechanisms of injury. Records were then followed to establish the type of cranioplasty used and the presence of complications including infections, follow-up period and overall outcome. Cases were excluded if no AC was performed or if a synthetic implant was used to reconstruct the skull. Statistical analysis was conducted using SPSS for windows version 19 (IBM). Data were analysed using bivariate correlation and linear regression models to attempt and establish any risk factors of poor outcomes. Statistical significance was established at p ⬍ 0.05.
Subcutaneous abdominal storage of the autologous bone flap At the time of decompressive craniectomy, the excised bone flap is placed into the subcutaneous space in the patient’s abdominal wall. This space is accessed by an appropriately sized transverse incision in the right abdominal wall (up to 10 cm in length) midway between the costal margin and the anterior superior iliac spine. The bone flap has to be sited high enough for it to not impact on the iliac crest in the sitting position, as this may be uncomfortable and may hinder the early stage of rehabilitation. A space is created just superficial to the abdominal wall muscles into which the bone flap can be placed. If necessary, the bone flap may be divided into two pieces to allow it to fit into the subcutaneous pouch. It is recommended, if the bone flap is in multiple fragments, that these are reconstructed into one or two pieces prior to storage in the abdominal wall, as this will later aid reconstruction. Any sharp edges will have to be trimmed back, whilst avoiding excessive bone removal. After haemostasis the skin is closed over the bone flap.
Reconstruction This is technically straightforward. Prophylactic antibiotics were used in all cases (single dose on induction and no postoperative antibiotics). Chlorhexidine alone was used for skin preparation. The bone flap was retrieved from the abdomen and washed in an antiseptic solution, which was thoroughly rinsed with saline before re-implantation. We inspected the bone flap for signs of infection before the scalp incision. It is important to note that a serous or serosanguinous collection in the abdominal pouch is common and this is not a sign of infection. In most cases, we laid a protective silastic sheet to cover the dura and dural defect (trimmed using the bone flap as template to fit the bony defect precisely) at craniectomy to prevent adhesions between the temporalis muscle or the
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subcutaneous tissue and the brain or dura. This facilitates and expedites tissue dissection at cranioplasty, thereby reducing operating time. The bone flap was then fixed to the craniectomy edge using mini-plates. A wound drain was used at the surgeon’s discretion, but in this series this was avoided in the majority of cases. Wound was closed using vicryl for galea and staples for the skin.
Results Between October 2007 and October 2010, a total of 53 decompressive craniotomies were performed for traumatic brain injury. Of those, 40 were male and 13 female with a mean age of 37 (32–41) years. Forty-four of these cases underwent autologous cranioplasty and where included in the analysis. The excluded cases consisted of five who had titanium mesh cranioplasty, one who had a combination of both materials, two who did not survive to have cranioplasty and one case who refused cranioplasty. Two patients in the series were intravenous drug abusers (IVDA) and 2 had pre-existing heart conditions. As for mechanism, 23 (52%) were due to falls, 13 (30%) due to road traffic accidents (RTA) and 8 (18%) due to assaults. Twenty-one (47%) of cases suffered some form of a skull fracture. Twenty-eight (64%) of the DC performed were for primary evacuation of an intracranial haematoma, while the rest were secondary procedures for cerebral swelling (Table I). Twenty-eight (64%) of the operations were unilateral and 16 (36%) were bifrontal. All data are presented in Table I. Twenty-nine (66%) of the operations were performed by a specialist trainee with at least 2 years of neurosurgical training. Six (14%) operations were performed at consultant level. Seniority of the primary operator was not recorded in the remaining cases. Mean interval from DC to cranioplasty was 86 (95% CI: 63–109) days. Mean time for duration of hospital stay after cranioplasty was 8 days.4–12 Mean follow-up was 8 (95% CI: 6–11) months with 6 deaths noted in patients who underwent AC (Table II), of which only 1 was in the immediate post-operative period. Mild complications were found in 21 cases (46%) (Table III). Major complications, however (Tables IV and V), severe enough to warrant readmission and/or reoperation were found in a total of 13 cases (30%). One of those cases developed a hydrocephalus after AC, which required insertion of a ventriculoperitoneal (VP) shunt, and died 6 months later due to sepsis. Mean duration of stay during readmission was 9 days6–23 with mode of 1 day and median of 2 days. In terms of post-operative infection, only 2 cases were identified: 1 of them needed revision using titanium mesh, while the other was managed using antibiotics only. The responsible organism was Staphylococcus aureus in both cases. No statistically significant predictor of poor outcome from cranioplasty was detected (age, gender, presence of skull fracture, delay to cranioplasty, seniority of operator or co-morbidities) using bivariate correlations and regression analysis.
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Table I. Summary of findings. Case Age Gender 1 2 3 4 5 6 7
4 63 18 39 40 20 78
M F M M M M F
8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44
35 37 77 25 21 57 42 34 40 33 55 20 26 43 57 26 36 38 18 19 41 34 39 35 35 20 36 67 30 19 71 36 34 33 46 17 28
F M F M M M F F M M M M M M M M M M M M F M M M M M M M M M M M F M M F M
Co-Morbidities – – –
IVDA – – Hypertension, ischaemic heart disease – – – – – – – – Hepatitis B carrier – – – – – – – – – – – – IVDA Epilepsy – – – Alcoholic liver disease Chronic lymphocytic leukaemia – – Atrial fibrillation – – – – Juvenile arthritis –
Discussion As the evidence base for DC in trauma is still being assessed with published results from the DECRA trial and the final results of RescueICP trial are awaited, cranioplasty also needs to be thoroughly evaluated and best practice established.8,9 Evidence for which type of cranioplasty and in what setting it is to be used is lacking. In this study we have shown a single unit’s experience of AC in the setting of trauma. We cannot offer any firm conclusions as to what might be a risk factor Table II. Mortality. Age (years) Survival after AC 19
6 months
26 28 37 77
1 year 1 year 22 months 5 days (9 days after sustaining primary injury)
78
26 months
Mechanisms Skull fracture
DC type
Extent of DC
Fall Fall RTA RTA Assault RTA RTA
Yes No No Yes No Yes No
Primary Primary Primary Secondary Primary Primary Primary
Bifrontal Unilateral Unilateral Unilateral Bifrontal Unilateral Unilateral
Fall Fall Fall RTA Fall RTA Assault Fall Fall RTA Fall RTA RTA Assault Fall RTA Assault Fall RTA RTA Fall Assault Fall Assault Fall Assault Fall Fall Fall Assault Fall Fall Fall Fall Fall RTA Fall
No Yes No No Yes Yes No Yes Yes No No Yes Yes Yes Yes No Yes No Yes No No Yes Yes No No No No Yes Yes Yes No No Yes Yes No Yes No
Secondary Secondary Primary Primary Primary Secondary Secondary Secondary Secondary Primary Secondary Primary Primary Primary Secondary Secondary Secondary Primary Secondary Secondary Primary Primary Secondary Secondary Primary Primary Primary Primary Primary Primary Primary Primary Primary Secondary Primary Primary Primary
Unilateral Bifrontal Unilateral Bifrontal Unilateral Bifrontal Bifrontal Bifrontal Unilateral Bifrontal Bifrontal Unilateral Unilateral Unilateral Unilateral Bifrontal Unilateral Unilateral Bifrontal Unilateral Unilateral Bifrontal Unilateral Unilateral Unilateral Unilateral Unilateral Unilateral Bifrontal Unilateral Unilateral Unilateral Bifrontal Bifrontal Unilateral Bifrontal Unilateral
for complication. It is unlikely for single-centre cohort studies or case series to elucidate whether the complications are directly associated with the choice of implant, given the significant variability in risk factors, such as co-morbidity, recovery status, mechanism of injury, timing of surgery, size and location of the DC. A national cranial reconstruction register has been proposed, which will hopefully provide sufficient cases for a multivariate analysis.10 The cosmetic results of AC are good and there is no risk of foreign body reaction.11 However, there is the challenge of preserving the bone flap in such condition as to allow
Cause Sepsis and multi-organ failure Pneumonia Unknown Aspiration pneumonia Primary injury: treatment withdrawn in view of poor prognosis Unknown
Table III. Summary of the mild complications reported. Mild Complication Headaches Ridging at edge of cranioplasty Mild facial drop Minor pulmonary embolism Pneumonia Fluctuating wound swelling Subjective sensation of instability in bone flap
Autologous cranioplasty following decompressive craniectomy Table IV. Major complications during index admission. Complication Management
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Extradural haematoma Wound drain stuck Extradural haematoma Worsening contusions
Burr hole evacuation Removal of drain in operating theatre Craniotomy evacuation Death
maintenance of bony structure and shape, and prevention of contamination. Two solutions are frequently used that solve this issue. Cryopreservation, i.e. sterilising and storing the bone flap in a freezer, is one option.12 This is most commonly used, although no universally agreed guidelines exist with regard to temperature for storage and choice of storage medium.1 Routine practice is to sterilise the bone flap prior to cryopreservation at temperatures of up to ⫺ 80°C, although a recent paper reported good results when using higher temperatures.13 Several problems exist with this approach though. Primarily, this runs the risk of denaturation and inactivation of pro-osteoblastic proteins in the bone flap.14 This can lead to excessive bone reabsorption and impaired healing. Storage of the bone flap can also be costly due to logistic, legislative and regulatory requirements, such as freezer maintenance, temperature monitoring, correct labelling of the bone flap and prevention of infection. The second available option for storage is inside the patient’s own subcutaneous tissue, normally in the abdomen as described here.15 The bone flap can also be stored in the subgaleal space, thereby avoiding the need for a further incision in the abdomen. This storage solution avoids the risk of devitalising the bone flap and the problems associated with external storage. The subcutaneous tissue is naturally sterile, accessible and physiologically suitable for granulation thereby maintaining bone flap integrity.1,4 We encountered no problems with bone resorption by storing the flap internally, a problem which is often reported in other case series using cryopreservation of bone flap.7 There are instances where AC may not be possible. The bone flap might be shattered into small fragments that would be impractical to piece together, or it may be contaminated. Various synthetic materials have, therefore, been developed for repair of the cranial defect after craniectomy.5,16,17 These include titanium plates, polymethylmethacrylate (PMMA), polyether ether ketone and hydroxyapatite. Some materials Table V. Cases readmitted. Readmission cause Wound infection CSF collection Hydrocephalus CSF collection Extra-axial wound haematoma Poor cosmesis Stroke with dysphasia Wound infection Bony step and temporal hollowing
Duration of stay (days) 8 1 66 2 1 1 2 3 1
Management Treated with antibiotics Needle aspiration VP shunt insertion Lumbar shunt insertion Conservative Revision with titanium mesh Conservative Bone flap removal and titanium mesh cranioplasty at a later admission Titanium mesh cranioplasty
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can either be shaped directly by the surgeon in theatre or be custom-made in advance.4 The advantage is that these various materials can be used in the absence of the original bone flap. One study also found synthetic cranioplasty to last significantly longer than autologous bone flaps.18 Disadvantages include manufacturing and planning costs (custom-made implants usually require a planning stereology scan), biocompatibility issues and the potential technical challenge in shaping and securing the implant.19
Timing Following removal of bone flap the brain will need several days to weeks to recover from the acute swelling.20,21 Once the acute phase is over and the patient starts to recover, the question of when to perform the cranioplasty arises. Previously accepted practice was for patients to wait for up to 6 months before having their skull reconstruction.18,22 The logic behind this delay was dictated by concerns regarding missing a diagnosis of late-presentation hydrocephalus and a hypothetical heightened risk of infection with early surgery.3 Delaying the cranioplasty, however, carries its own risks. Communicating hydrocephalus can occur and prolonged exposure to atmospheric pressure may cause mass effect leading to paradoxical herniation of brain.23,24 Additionally, there is a suggestion that skull reconstruction may have some direct benefit on neurological recovery.25 A recently published case series further supports this theory.26 Early reconstruction facilitates rehabilitation and offers structural integrity when the patient starts to mobilise, avoiding the need for protective helmets to be worn.27 Several studies have, therefore, been completed to assess whether earlier cranioplasty after DC is safe. One study found that cranioplasty at 2–6 weeks post craniectomy showed no increase in risks of infection or hydrocephalus but it did expedite patient transfer to rehabilitation and improve outcome.3 A further study assessing neurological function after early cranioplasty revealed marked improvement with no significant increase in complication rates.22 Improvements have also been observed radiologically. CT perfusion scans have shown enhanced cerebral perfusion, while improved CSF flow has been confirmed using contrast MRI and lumbar puncture pressure measurements.28,29 Despite some variability in practice, there is consensus that cranioplasty should be performed as soon as brain oedema has settled. However, given the benefit of early rehabilitation, it is common practice to defer the reconstruction until the initial rehabilitative intervention has been delivered. Patients at our centre had a mean waiting time to AC of 86 days.
Complications Cranioplasty can lead to the same complications as any other surgical procedure such as risks associated with anaesthesia, haemorrhage and wound infection. Complications more specific to the procedure are hydrocephalus, extra-axial collection, seizures and bone flap infection.5 Overall complication rates reported vary greatly ranging from 0 to 34%.5,12,30–32 This wide range is not surprising given that these case series have evaluated different methods of cranioplasty in different
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patient populations. Use of synthetic materials does seem to account for a rise in infection rate compared to autologous bone flaps.3,18 The difference is significant with the infection risk nearly doubled. An explanation for this dramatic difference is potentially due to the fact that synthetic implants are often resorted to after failure of AC.3 Direct comparison between PMMA and titanium plates found no significant difference in overall complication rates.5 One study, on the other hand, reported titanium plates as the superior material in regard to risk of infection.19 It is also worth pointing out that cosmesis is one of the indications for cranioplasty but cosmetic complications are common, although rarely significant. They include uneven surfaces due to muscle atrophy, fluid collection and discontinuity between flap and skull bone.18 Mild, self-limiting complications not requiring rehospitalisation or further intervention are common. The total complication rate was 46% in our series; severe complications leading to readmission, reoperation or death occurred in 30% of cases. This figure is high but in line with other series.5,12,30–33 The fact that our study population consisted of traumatic cases only may also have contributed to the high complication rates. Of note is that only 2 cases developed an infection, one of which severe enough to warrant a surgical revision. We have no firm conclusions to offer as to why we had such a comparatively low infection rate. Dissection of the skin flap free from brain could be easier due to shorter waiting time for AC and the use of a silastic sheet over the dural plane at craniectomy to prevent adhesions. This could lead to less CSF leakage and shorter operation times. Of note is also that none of the deaths in the study can be linked directly to the cranioplasty.
Study limitations This study is retrospective and has, therefore, the limitation of a possible underreporting of adverse events. However, all AC cases were followed up and it is very unlikely that any significant surgical complications leading to readmission, reoperation or death were missed. Given the heterogeneity of the cohort and the low numbers of infections and reoperations recorded, the sample size does not allow a proper statistical analysis of the risk factors for significant complications.
Conclusions Autologous cranioplasty in trauma is a practical, straightforward technique that has a complication rate similar to that when used in non-trauma cases.
Acknowledgements We wish to thank Andrew Dunford for assisting in data collection. Declaration of interest: The authors report no declarations of interest. The authors alone are responsible for the content and writing of the paper.
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