Is Preoperative Brain Midline Shift a Determinant Factor for Neurological Improvement After Cranioplasty?

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Provided by Elsevier - Publisher Connector Journal of the Formosan Medical Association (2015) 114, 577e582

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ORIGINAL ARTICLE Is preoperative brain midline shift a determinant factor for neurological improvement after cranioplasty?

Chun-Hsien Lin a,b, Jen-Tsung Yang a,b, Ting-Chung Wang a,b, Martin Hsiu-Chu Lin a,b, Wan-Chun Cheng a,b, Ming-Hsueh Lee a,c,*

a Department of Neurosurgery, Chang Gung Memorial Hospital, Chia-Yi 613, Taiwan b College of Medicine, Chang Gung University, Tao-Yuan, Taiwan c Chang Gung Institute of Technology, Chia-Yi, Taiwan

Received 15 March 2013; received in revised form 3 September 2013; accepted 10 September 2013

KEYWORDS Background/Purpose: In patients with traumatic brain injury, the degree of brain midline shift brain midline shift; is related to prognosis. In this study, we evaluated the impact of the presence of a preopera- craniectomy; tive brain midline shift on the Glasgow Coma Scale (GCS) scores and muscle power (MP) cranioplasty; improvement after cranioplasty. neurological Methods: In this 6-year retrospective cohort study, we compared cranioplasty patients from improvement Taiwan with and without a preoperative brain midline shift. We assigned the patients to the following two groups: the midline shift group and the nonmidline shift group. The GCS score and MP contralateral to the lesion site were recorded and analyzed both prior to and 1 year after the operation. Results: We enrolled 56 cranioplasty patients (35 patients with a midline shift and 21 without a midline shift) and analyzed their complete clinical characteristics. There were signiﬁcant improvements in the GCS (p Z 0.0078), arm MP (p Z 0.0056), and leg MP (p Z 0.0006) scores after cranioplasty. There was also a signiﬁcant improvement in the GCS score in the brain midline shift group (0.4 Æ 0.149 in the brain midline shift group vs. 0.05 Æ 0.48 in the nonmidline shift group, p Z 0.03). Conclusion: For patients who underwent craniectomy, an improvement in neurological function 1 year after cranioplasty was observed. The patients with brain midline shift showed more

* Corresponding author. Department of Neurosurgery, Chang Gung Memorial Hospital, Number 6, West Section, Chia-Pu Road, Pu Tz City, Chia-Yi 613, Taiwan. E-mail address: [email protected] (M.-H. Lee).

improvement in consciousness after cranioplasty than those without a brain midline shift. The presence of a preoperative brain midline shift may be an isolated determinant for the prediction of the outcome after cranioplasty. Copyright ª 2013, Elsevier Taiwan LLC & Formosan Medical Association. All rights reserved.

Introduction We assigned the patients based on the preoperative brain CT findings into the following groups: the midline shift À Cranioplasty is performed mainly to protect the brain and group (midline shift: 1 12 mm; 35 patients) and the non- to restore preinjury appearance.1 It has been reported that midline shift group (midline shift: 0 mm; 21 patients). The some patients with large skull defects showed improve- GCS scores and MP of the upper and lower limbs contra- 2,3 lateral to the lesion site were recorded prior to and 1 year ments in neurological status after cranioplasty. The 2 reversal in neurological deterioration is generally thought after cranioplasty. The midline shift distances were to be related to a reduction in the effects of local cerebral calculated using brain CT prior to cranioplasty by the same compression by atmospheric pressure. Over time, many neurosurgeon. The GCS scores and MP of patients with sunken brain were also recorded and defined as non- craniectomy patients present with a persistent contralat- 6 eral brain midline shift.4 In this study, we aimed to deter- pulsatile concave and unpinchable scalp. A plain CT image mine whether such a brain midline shift is a significant of the brain is shown in Fig. 1. factor in functional improvement after cranioplasty. Statistical analyses

Methods The GCS scores and MP of the upper and lower limbs contralateral to the lesion site prior to and after cranio- Between May 2003 and November 2009, we conducted a plasty were compared between the midline shift and the retrospective cohort study and included 82 cranioplasty nonmidline shift groups. Categorical data were compared patients undergoing regular follow-up for 1 year at Chang using the Chi-square test, and continuous data were Gung Memorial Hospital, a tertiary care center in Chia-Yi compared using an unpaired t test. Pearson correlation (Taiwan). The indications of decompressive craniectomy coefficient was used to evaluate associations between were cerebral edema due to post-traumatic or post- variables. For all relevant results, 95% confidence interval ischemic brain swelling, or epidural abscess. During the (CI) was used. In the midline shift group, the midline shift study period, the Glasgow Coma Scale (GCS) score and distance was analyzed using linear regression analysis to muscle power (MP) in the upper and lower limbs contra- evaluate whether neurological improvement was related to lateral to the cranioplasty site were recorded in the reha- the midline shift grading. A result was considered statisti- bilitation ward or in the neurosurgery clinic. Inclusion cally significant if two-tailed p < 0.05. criteria were (1) unilateral craniectomy, (2) diameter of craniectomy defect >10 cm, (3) the duration between craniectomy and cranioplasty was 2 months, (4) brain Results computed tomography (CT) scan images or magnetic reso- nance images were obtained 1 week prior to cranioplasty, Table 1 shows the characteristics of the 56 patients. The (5) regular follow-up in the rehabilitation ward or in the mean age in the midline shift group and the nonmidline neurosurgery clinic of our hospital for >1 year. Exclusion shift group was 41.5 Æ 17.4 years and 37.4 Æ 17.7 years, criteria were (1) accept further brain surgery after cra- respectively (p Z 0.40). There were 21 men (out of 35 nioplasty during our follow-up and (2) lost to follow-up. patients) in the midline shift group and 16 men (out of 21 Sixteen patients were excluded from the study because patients) in the nonmidline shift group (p Z 0.21). The they required further brain surgery after cranioplasty [a number of patients with previous VP shunt was five (14%) in ventriculoperitoneal (VP) shunt or a craniectomy because the midline shift group and two (10%) in the nonmidline of an epidural abscess]. Ten patients were excluded shift group. The number of patients with sunken brain prior because they were admitted for other severe medical dis- to cranioplasty was eight (23%) in the midline shift group eases. Finally, 56 patients were enrolled in the study. and two (10%) in the nonmidline shift group. The GCS score The patients in this trial had undergone a CT scan more Æ standard deviation (SD) prior to cranioplasty was than 2 months after a craniectomy and had a stationary 13.6 Æ 2.1 in the midline shift group and 14.2 Æ 1.4 in the neurological condition prior to cranioplasty. Craniectomy nonmidline shift group (p Z 0.23). The GCS score Æ SD after was performed to treat severe head injury, intracerebral cranioplasty was 14.2 Æ 0.3 in the midline shift group and hemorrhage, malignant large infarction, and intracranial 14.0 Æ 0.3 in the non-midline shift group (p Z 0.63). The infection. In the subgroup of patients with traumatic brain worst GCS score in our patients was 8. The arm MP Æ SD injury, their precraniectomy CT scans were categorized value before cranioplasty was 3.74 Æ 0.26 in the midline according to the Marshall CT classification5 and are pre- shift group and 3.52 Æ 0.46 in the non-midline shift group (p sented in Table 2. The Marshall CT classification was a CT Z 0.81). The leg MP Æ SD value before cranioplasty was classification for grouping patients with traumatic brain 3.74 Æ 0.26 in the midline shift group and 3.52 Æ 0.46 in the injury according to multiple CT characteristics.5 non-midline shift group, (p Z 0.66). The arm MP Æ SD value Preoperative brain midline shift and cranioplasty 579

Figure 1 A 76-year-old female had right malignant middle cerebral artery infarction. (A) Plain CT scan 3 days after right craniectomy revealing right hemisphere with mass effect. (B) Plain CT scan 6 weeks after right craniectomy revealing non-pulsatile sunken brain. after cranioplasty was 3.68 Æ 0.31 in the midline shift group hemorrhage (midline shift group, 28 cases; nonmidline shift and 3.66 Æ 0.43 in the non-midline shift group (p Z 0.91). group, 18 cases) and large infraction or intracranial infec- The leg MP Æ SD value after cranioplasty was 4.11 Æ 0.23 in tion (midline shift group, 7 cases; nonmidline shift group, 3 the midline shift group and 3.76 Æ 0.43 in the non-midline cases; p Z 0.59). The number of patients with dominant shift group (p Z 0.43). hemisphere injury was 13 (out of 35 patients) in the midline The time between craniectomy and cranioplasty was shift group and 13 (out of 21 patients) in the nonmidline 143 Æ 108 days in the midline shift group and 103 Æ 39 days shift group (p < 0.05). in the nonmidline shift group. The time between craniec- In patients with traumatic brain injury, precraniectomy tomy and cranioplasty was significantly longer in the CT scans of the patients were categorized according to the midline shift group (p < 0.05). The cause of craniectomy Marshall CT classification5 and are presented in Table 2. performed previously was classified into two groups, There were 35 traumatic brain injury patients in the study. namely, head injury or spontaneous intracranial The definition of diffuse injury IV5 was that brain CT scan

Table 1 Baseline characteristics of the patients. Characteristic With midline shift (N Z 35) Without midline shift (N Z 21) p* Age (y) Mean 41.5 Æ 17.4 37.4 Æ 17.7 0.40 Male sex 21 16 0.21 Patients with previous VP shunt 5 (14) 2 (10) d Patients with sunken brain prior to cranioplasty 8 (23) 2 (10) d GCS prior to cranioplasty 13.6 Æ 2.1 14.2 Æ 1.4 0.23 GCS after cranioplasty 14.2 Æ 0.3 14.0 Æ 0.3 0.63 Arm MP prior to cranioplasty 3.40 Æ 0.31 3.52 Æ 0.44 0.81 Leg MP prior to cranioplasty 3.74 Æ 0.26 3.52 Æ 0.46 0.66 Arm MP after cranioplasty 3.68 Æ 0.31 3.66 Æ 0.43 0.97 Leg MP after cranioplasty 4.11 Æ 0.23 3.76 Æ 0.43 0.43 Interval between craniectomy and cranioplasty, d 143 Æ 108 103 Æ 39 <0.05 Cause of previous craniectomydcase number Head injury or spontaneous ICH 28 18 0.59 Large infarction or intracranial infection 7 3 Injury on dominant hemisphere 13 13 <0.05

Data are presented as n, n (%), or mean Æ standard deviation. *The t and Pearson Chi-square tests were signiﬁcant at p < 0.05. GCS Z Glasgow Coma Scale; MP Z muscle power; ICH Z intracranial hemorrhage. 580 C.-H. Lin et al.

Table 2 Patients with traumatic brain injury between midline shift and nonmidline shift groups (N Z 35). Marshall computed tomographic classiﬁcationa Midline shift group (N Z 22) Nonmidline shift (N Z 13) p* No. of patients with diffuse injury IV (shift) 2 4 <0.05 No. of patients with evacuated mass lesion 20 9 <0.05

*Pearson Chi-square test statistical significance: p < 0.05. a Classification category was according to Marshall computed tomographic classification. shows midline shift by more than 5 mm and had no high or improvement between the two groups (arm MP improve- mixed density lesion by more than 25 cm.3 The definition of ment was 0.29 Æ 0.12 in the brain midline shift group vs. evacuated mass lesion5 was that brain CT shows any lesion 0.14 Æ 0.078 in the nonmidline shift group, p Z 0.40; leg MP that was surgically removed. improvement was 0.37 Æ 0.12 in the brain midline shift Table 2 shows the number of patients with traumatic group vs. 0.23 Æ 0.11 in the nonmidline shift group, brain injury in the midline shift and in the nonmidline shift p Z 0.47). groups. The number of patients who had evacuated mass Table 6 shows the number of patients with neurological lesion was 20 (91%, 20 out of 22 patients) in the midline improvements in the midline shift and the nonmidline shift shift group and nine (70%, 9 out of 13 patients) in the groups. The number of patients who showed improvement nonmidline shift group (p < 0.05). in the GCS score was nine in the midline shift group and one Table 3 lists the neurological changes in both groups in the nonmidline shift group (p Z 0.047). The number of prior to and after cranioplasty. There were significant im- patients who showed improvement in arm MP was six in the provements in the GCS score after cranioplasty midline shift group and three in the nonmidline shift group (13.88 Æ 0.25 prior to cranioplasty vs. 14.14 Æ 0.23 after (p Z 0.778). The number of patients who showed cranioplasty, 95% CI Z À0.4624 to À0.07334, p Z 0.0078), improvement in leg MP was nine in the midline shift group arm MP (3.46 Æ 0.25 prior to cranioplasty vs. 3.67 Æ 0.23 and four in the nonmidline shift group (p Z 0.567). The after cranioplasty, 95% CI Z À0.3937 to À0.07063, midline shift distance was analyzed using linear regression p Z 0.0056), and leg MP (3.66 Æ 0.23 prior to cranioplasty analysis in the midline shift group (p Z 0.14). vs. 3.98 Æ 0.21 after cranioplasty, 95% CI Z À0.4992 to À0.1436, p Z 0.0006). Interestingly, two patients had verbal function improvement and one patient recovered Discussion from left-hand clumsiness on the day after cranioplasty. Table 4 lists the GCS score changes prior to and after Decompressive craniectomy was performed on patients cranioplasty between the left-side and right-side craniec- who had developed intracranial hypertension or infection. tomy groups. A total of 26 patients accepted left-side Neurological deficits attributable to brain damage are craniectomy and 30 patients accepted right-side craniec- usually detected in patients who have undergone craniectomy in the study. There were significant improvements in tomy. The main reasons for subsequent cranioplasty are for the GCS score after cranioplasty (13.31 Æ 0.41 prior to cosmesis or protection of the brain. In the past 40 years, cranioplasty vs. 13.81 Æ 0.39 after cranioplasty, several studies have shown that some patients exhibit a p Z 0.0016) in the left-side craniectomy group. reversal of neurological deterioration after There were no significant improvements in the GCS score cranioplasty.2e4,7 In 1975, Uemura et al7 reported the first after cranioplasty (14.37 Æ 0.29 prior to cranioplasty vs. clinical description of a patient with a progressive neuro- 14.43 Æ 0.27 after cranioplasty, p Z 0.16) in the right-side logical deficit and a large sunken skin flap who showed craniectomy group. improved neurological function following cranioplasty. Table 5 lists the neurological improvements in the brain Syndrome of the trephined and the general symptoms after midline shift and nonmidline shift groups. There were sig- craniectomy were also found in some of our patients, nificant improvements in the GCS score in the brain midline especially in patients with depressed scalp flap.3 This syn- shift group (0.4 Æ 0.149 in the brain midline shift group vs. drome includes dizziness, headache, or discomfort at the 0.05 Æ 0.048 in the nonmidline shift group, p Z 0.03). site of the defect, feeling of insecurity, mental depression, However, MP in the arms and legs showed no significant and intolerance to vibration.3 In our study, headache and dizziness improved after cranioplasty in our patients. Some studies implied that early cranioplasty may Table 3 Neurological status prior to and after cranio- contribute to better neurologic outcome.8e11 In this study, plasty (N Z 56). the interval between craniectomy and cranioplasty was Prior to cranioplasty After cranioplasty p* longer in the midline shift group than in the nonmidline GCS 13.88 Æ 0.25 14.14 Æ 0.23 0.0078 shift group (143 Æ 108 days vs. 103 Æ 39 days, Table 1). Arm MP 3.46 Æ 0.25 3.67 Æ 0.23 0.0056 Although the GCS score was lower in the midline shift group Leg MP 3.66 Æ 0.23 3.98 Æ 0.21 0.0006 than in the nonmidline shift group (13.6 Æ 2.1 vs. 14.2 Æ 1.4 0.23, Table 1), the difference was not significant in our Æ Data are presented as mean standard deviation. study (p Z 0.23). *The paired t test statistical significance: p < 0.05. The causes of neurological improvement following cra- GCS Z Glasgow Coma Scale; MP Z muscle power. nioplasty are still unclear. In 1984 and 1985, Stula12,13 Preoperative brain midline shift and cranioplasty 581

Table 4 The GCS score improvements prior to and after cranioplasty between the left-side (N Z 26) and right-side (N Z 30) craniectomy groups. Prior to cranioplasty After cranioplasty p* GCS score in the left-side craniectomy group 13.31 Æ 0.41 13.81 Æ 0.39 0.0016 GCS score in the right-side craniectomy group 14.37 Æ 0.29 14.43 Æ 0.27 0.16

Data are presented as mean Æ standard deviation. *The paired t test statistical signiﬁcance: p < 0.05. GCS Z Glasgow Coma Scale.

suggested that the atmospheric pressure acting on the un- demonstrated that there was a correlation between the protected brain produces brain compression that is return of the shifted structures to the midline and clinical normalized by cranioplasty. Some studies have shown that improvement following cranioplasty. The midline shift may cerebral blow may play a role in neurological improvement be caused by changes in intracranial pressure (i.e., atmo- after cranioplasty.2,3,14 After craniectomy, a high incidence spheric pressure acting on the unprotected brain), intra- of cerebrospinal fluid (CSF) flow abnormalities and hydro- cranial structure, or CSF dynamics.16 However, a CT scan cephalus was also reported.14,15 One study demonstrated did not show brain midline shifts in some precranioplasty that the cerebral blood flow was reduced in the hemisphere patients. In traumatic brain injury studies, a midline shift ipsilateral to the enlarged ventricle. Perfusion studies was observed to be associated with very poor showed improvement in the cerebral blood flow after cra- outcomes.17e20 nioplasty rather than after VP shunt insertion.14 Here, we To the best of our knowledge, no previous studies have have demonstrated that in patients with a large skull addressed the impact of a precranioplasty midline shift on defect, patients showed improved neurological status after neurological improvement. The results of our study (Tables cranioplasty (as assessed by the GCS score and the arm and 5 and 6) suggest that 1 year after cranioplasty, the leg MP). Although some improvements months after cra- improvement in the GCS score was more obvious in the niectomy are still possible without cranioplasty, for midline shift group than in the nonmidline shift group. cosmetic consideration, it is too hard to delay cranioplasty Sunken brain syndrome associated with neurological dete- in our country. We could not prove that our patients would rioration was one of the complications after decompressive not eventually gain neurological improvement without craniectomy.6,21 In our study, the percentage of sunken cranioplasty. However, in this study, three patients had brain associated with craniectomy was higher in the midline neurological improvement on the day after cranioplasty: shift group than in the nonmidline shift group (23% vs. 10%, two patients had verbal function improvement and one Table 1). The neurologic deficits associated with sunken patient recovered from left-hand clumsiness. Neurological brain may recover after cranioplasty, and also imply that recovery immediately after cranioplasty was found in some the midline shift group had more potential to recover than of our patients. We speculate that these improvements may the nonmidline shift group. be attributable to reversed atmospheric pressure or We speculate that the observed improvement may be increased cerebral blood flow. In this study, the patients attributable to the fact that cranioplasty reduces intra- with injury on dominant hemisphere gained more recovery cranial pressure and changes in CSF dynamics to a greater on GCS scores than on the right hemisphere (Table 4), and extent in the midline shift group than in the nonmidline hinted that the injury on the dominant hemisphere seemed shift group. Clearly, this matter deserves further attention to have more potential to recover on GCS scores after in future studies. From this study, we know that neurolog- cranioplasty than on the right side. ical improvement after cranioplasty is correlated with Brain midline shifts are usually detected in patients with precranioplasty midline shift, laterality, and probably CT large skull defects. In 1974, George et al4 published a case findings in the acute stage. Although not a must, multi- series of patients who underwent angiography after hemi- variate analysis can probably define the most important craniectomy. Over time, many patients presented with a factors for the prognosis. persistent contralateral midline shift that occurred simul- There are limitations to our study. First, our study is taneously with a concavity in the skin flap. Moreover, they retrospective in nature, and the data collection was by

Table 5 Neurological improvement between midline shift and nonmidline shift groups (N Z 56). Midline shift group (N Z 35) No midline shift (N Z 21) p* GCS improvement 0.4 Æ 0.149 0.05 Æ 0.048 0.03 Arm MP improvement 0.29 Æ 0.12 0.14 Æ 0.078 0.40 Leg MP improvement 0.37 Æ 0.12 0.24 Æ 0.11 0.47

Data are presented as mean Æ standard deviation. *The t test statistical signiﬁcance: p < 0.05. GCS Z Glasgow Coma Scale; MP Z muscle power. 582 C.-H. Lin et al.

3. Schiffer J, Gur R, Nisim U, Pollak L. Symptomatic patients after Table 6 Neurological improvement between midline shift craniectomy. Surg Neurol 1997;47:231e7. and nonmidline shift groups. 4. George AE, Morantz RA, Abad RM, Rovit RL, Chase N. Neuro- Midline shift No midline p* radiology of the posthemicraniectomy patient with special group shift group emphasis on the radiology of unilateral atrophy. Radiology e (N Z 35) (N Z 21) 1974;111:627 31. 5. Maas AI, Hukkelhoven CW, Marshall LF, Steyerberg EW. Predic- Number of patients 9 1 0.047 tion of outcome in traumatic brain injury with computed tomo- with GCS score graphic characteristics: a comparison between the computed improvement tomographic classification and combinations of computed Number of patients 6 3 0.778 tomographic predictors. Neurosurgery 2005;57:1173e82. with arm MP 6. Bhat AR, Kirmani AR, Nizami F, Kumar A, Wani MA. “Sunken improvement brain and scalp flap” syndrome following decompressive “extra-craniectomy”. 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