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Craniectomy and Craniotomy in Traumatic Brain Injury: A Propensity-Matched Analysis of Long-Term Functional and Quality of Life Outcomes
Original Article
Craniectomy and Craniotomy in Traumatic Brain Injury: A Propensity-Matched Analysis of Long-Term Functional and Quality of Life Outcomes Michael L. Kelly1, Berje Shammassian3, Mary Jo Roach2, Charles Thomas2, Amy K. Wagner4
OBJECTIVE: To report the comprehensive long-term functional and quality of life outcomes after craniectomy (CE) and craniotomy (CO) in individuals with traumatic brain injury (TBI).
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METHODS: Information on all individuals with TBI who had undergone CE or CO were extracted from the TBI Model Systems database from 2002 to 2012. A 1:1 propensity matching with replacement technique was used to balance the baseline characteristics across groups. The matched sample was analyzed for outcomes during hospitalization, acute rehabilitation, and £2 years of follow-up.
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RESULTS: We identified 1470 individuals who had undergone CE or CO. Individuals undergoing CE compared with CO demonstrated a longer length of stay in the hospital (median, 22 vs. 18 days; P < 0.0001) and acute rehabilitation (median 26 vs. 21 days; P < 0.0001). Individuals with CE had required rehospitalization more often by the 1-year follow-up point (39% vs. 25%; P < 0.0001) for reasons other than cranioplasty, including seizures (12% vs. 8%; P < 0.0001), neurologic events (i.e., hydrocephalus; 9% vs. 4%; P < 0.0001), and infections (10% vs 6%; P < 0.0001). Individuals with CE had significantly greater impairment using the Glasgow Outcome Scale-Extended, required more supervision, and were less likely to be employed at 1 and 2 years after TBI. No difference was observed in the satisfaction with life scale scores at 2 years. The
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Keywords Outcome measures - Rehabilitation - Surgery - TBI model systems - Traumatic brain injury -
Abbreviations and Acronyms CE: Craniectomy CO: Craniotomy CT: Computed tomography FIM: functional independence measure GCS: Glasgow Coma Scale GOSE: Glasgow Outcome Scale-Extended ICP: Intracranial pressure LSO: length of stay
Kaplan-Meier mortality estimates at 1 and 2 years showed no differences between the 2 groups (hazard ratio, 0.57; P [ 0.4). CONCLUSION: In a matched cohort, individuals undergoing CE compared with CO after TBI had a longer length of stay, decreased functional status, and more rehospitalizations. The survival at 2 years and the satisfaction with life scale scores were similar.
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INTRODUCTION
S
urgery for individuals with traumatic brain injury (TBI) remains controversial.1 Studies have documented variability in surgical procedural rates, timing, and the type of surgery performed.1-3 Debate continues regarding whether decompressive craniectomy (CE) (i.e., bone removal with later reimplantation) is superior to craniotomy (CO) (i.e., bone removal and replacement in the same surgery) in those with acute TBI.1,4 Some studies have suggested that CE might be superior because it reduces intracranial pressure (ICP) and more effectively limits brain swelling, leading to improved survival and better functional outcomes.5,6 Other studies have emphasized the risks and complications of CE, including subdural hygromas, seizures, hydrocephalus, and sinking flap syndrome.7-10 The studies that compared CE and CO often lacked comprehensive outcome measures, including quality of life scores,
TBI: Traumatic brain injury TBIMS: Traumatic brain injury model systems From the 1Department of Neurosurgery and 2Center for Healthcare Research and Policy, Case Western Reserve University School of Medicine, MetroHealth Medical Center, Cleveland, Ohio, USA; 3Department of Neurosurgery, University Hospitals Cleveland Medical Center, Cleveland, Ohio, USA; and 4Department of Physical Medicine and Rehabilitation, Neuroscience, Safar Center for Resuscitation Research, Center for Neurobiology, University of Pittsburgh School of Medicine, Pittsburgh, Pennsylvania, USA To whom correspondence should be addressed: Michael L. Kelly, M.D. [E-mail: [email protected]] Citation: World Neurosurg. (2018). https://doi.org/10.1016/j.wneu.2018.07.124 Journal homepage: www.WORLDNEUROSURGERY.org Available online: www.sciencedirect.com 1878-8750/$ - see front matter ª 2018 Elsevier Inc. All rights reserved.
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detailed functional assessments, and longer term follow-up data. Data beyond a 3- to 6-month post-TBI period is especially important in the CE population because cranial bone reimplantation often occurs several months after the initial surgery and carries additional risks related to a second cranial operation, including infection, bleeding, and cerebrospinal fluid leakage.10 The traditional outcome measures such as the Glasgow Outcome Scale-Extended (GOSE) lack specificity and sensitivity to treatment effects in this population.11 Given the conflicting study results and limitations in the design of existing studies, the 2006 Brain Trauma Foundation guidelines for the surgical management of TBI identified the issues of CE versus CO as a top priority for future research.12,13 In the present study, we analyzed the National Institute on Disability, Independent Living, and Rehabilitation Research TBI model systems (TBIMS) database to compare the long-term survival and functional outcomes between individuals with TBI who had undergone CE compared with CO in medical centers across the United States. We hypothesized that higher survival rates, but lower functional outcomes scores, would be found for individuals who had undergone CE compared with CO. METHODS Data Source The TBIMS national database was queried to identify all TBI admissions to rehabilitation facilities in the United States participating in the TBIMS program from 2002 through 2012. The TBIMS is a national project funded by the National Institute on Disability, Independent Living, and Rehabilitation Research. The project is the first prospective, multicenter study of the recovery and outcomes of individuals with TBI after participation in a coordinated system of acute neurotrauma care and inpatient rehabilitation. Institutions that are designated as TBIMS centers must have access to level 1 trauma center care, acute neurosurgical care, comprehensive inpatient rehabilitation services, and long-term interdisciplinary follow-up and rehabilitation services. Currently, 16 TBIMS centers and 3 previously funded facilities that continue to provide follow-up data have been designated across the United States. The TBIMS database inclusion criteria are (1) complicated mild, moderate, or severe TBI; (2) emergency department evaluation within 72 hours of injury; (3) age 16 years; (4) hospital care and inpatient rehabilitation received within a participating TBIMS facility; and (5) written informed consent provided by the patient and/or guardian. More information is available from the National Data and Statistical Center (available at: https://www.tbindsc.org/). Patient Selection and Characteristics We identified all TBIMS participants who had undergone either CO or CE during their acute hospital admission. Individuals who had initially undergone CO but then underwent a subsequent CE during the same hospitalization were included in the CE group. All available hospitalization-related factors known to influence postdischarge outcomes in postoperative patients with TBI were analyzed, including clinical information, demographic data, and
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socioeconomic factors.14,15 Race was dichotomized into African-American and noneAfrican-American. The TBI subtype was defined using the TBIMS intracranial computed tomography (CT) diagnosis variable and included subarachnoid hemorrhage, subdural hemorrhage, intraventricular hemorrhage, and intracranial hemorrhage and/or contusions. Each individual with TBI could have had multiple TBI subtypes recorded. The TBIMS variable for the Marshall CT score was used to identify the extent of intracranial compression on the CT scan. Elevated ICP was identified using the variable “CC_Hypertension” and is defined in the TBIMS database as 1 documented ICP peaks of 20 mm Hg during the acute hospitalization period. The ICP data were typically obtained from the nursing flowsheets from the intensive care unit in the hospital records. The insurance type was coded as none, private, Medicaid, and Medicare using the TBIMS variable for insurance status (“AcutePay1”). The education level was recoded as high school graduate or less, college degree or some college, and graduate degree using the TBIMS education variable. Outcomes The length of stay (LOS) was defined as total number of days the individual was admitted to the acute hospital or TBI rehabilitation. Functional outcomes were measured at admission to the TBIMS rehabiliation unit, discharge from the rehabilitation unit, and at the 1- and 2-year follow-up points. The functional independence measure (FIM) score was reported as an overall score and as separate subscores for motor and cognitive function. The Glasgow Outcome Scale-Extended (GOSE) score was dichotomized into unfavorable (GOSE 4) and favorable (GOSE >4) outcomes at the 1- and 2-year follow-up points. The Supervision Rating Scale was completed at the 1- and 2-year follow-up points and was dichotomized as full-time supervision or partial supervision/independent living. The Satisfaction with Life Scale score is a standardized, self-reported outcome measure that was reported as the median value at the 1- and 2-year follow-up points. The Disability Rating Scale measures objective signs of physical impairment and was reported as the median value at the 1- and 2-year follow-up points. The employment variable (EMPLOY) was measured at the 1- and 2-year follow-up points and dichotomized into unemployed and any type of employment. The discharge disposition from TBI rehabilitation was dichotomized into home or any assisted living facility or nursing facility using the TBIMS variable RESIDENCE. The total number of rehospitalizations (REHOSP) in the preceding year are recorded in the TBIMS at each annual follow-up examination. Rehospitalization was defined in the present study as 1 rehospitalization events annually. For each rehospitalization event, the rehospitalization diagnosis was also recorded from the individual and family self-report, including seizures, neurologic disorders (i.e., head injury, hydrocephalus, headaches), psychiatric issues, infections (i.e., wound infection, meningitis), orthopedic procedures (i.e., cranioplasty or any reconstructive surgeries), general health-related problems, and other miscellaneous medical problems. The rehospitalization diagnosis was only reported at the 1-year follow-up point because >30% of these data were missing at the 2-year follow-up examination. Multiple diagnoses could be reported by the participant and/or family for each rehospitalization
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event. The survival time was calculated using the TBIMS “Death Date” variable, with the data extracted from the Social Security Death Index. Statistical Analysis Propensity scores were generated to reduce any potential bias between individuals in the CO and CE groups using the following variables: age, sex, race, insurance status, marital status, education level, employment status, TBI subtypes, GCS score, penetrating injury, elevated ICP, and Marshall CT score.16 We imputed for any baseline patient variables that were missing at random using a multivariate regression method of imputation before implementing the propensity score-matching routine. Propensity scores have been used to reduce biased estimates of treatment effects in observational studies.17 A 1:1 propensity-matching technique with replacement was used to balance patients across the CO and CE groups. The criterion for successful matching was established as an absolute standardized difference of <10. Individual baseline characteristics and outcomes were compared across the CO and CE groups using the Pearson c2 test for categorical variables and the Mann-Whitney U test for all nonparametric continuous variables.18 Covariates were compared between the CO and CE groups in the matched sample across all outcome measures. Cox proportional hazard modeling was performed after matching to determine the survival estimates for both groups. Analyses were performed using SPSS software, version 23.0 (IBM Corp., Armonk, New York, USA) and R software (R Foundation for Statistical Computing, Vienna, Austria). Statistical significance was set at P 0.05. RESULTS A total of 2567 admissions were identified in the TBIMS database before propensity matching, including 1470 CO participants and 1097 CE participants. The rates of CE and CO varied across the TBIM institutions. The CE rates ranged from 30% to 70% of all surgical admissions to TBIMS institutions. After propensity matching with replacement, we identified a cohort of 1470 individuals in each group who were matched across all baseline admission characteristics (Figure 1). The individuals in the CO and CE groups were successfully matched across age, sex, race, insurance type, educational level, marital status, GCS score, TBI subtype, Marshall CT score, elevated ICP, and penetrating injury mechanism (Table 1). The median GCS score was 11 (interquartile range, 7e14) for both groups, and most individuals in the CE (72%) and CO (74%) groups presented with a subdural hemorrhage. The CE participants had a longer LOS in the hospital (median, 22 vs. 18 days; P < 0.0001) and in acute rehabilitation (median, 26 vs. 21 days; P < 0.0001; Table 2). Fewer individuals with CE were discharged to home after inpatient rehabilitation (72% vs. 80%; P < 0.0001), and fewer were employed at the 1-year follow-up examination (22% vs. 26%; P ¼ 0.007). More CE participants were readmitted to the hospital at some point during the 1-year (39% vs. 25%; P < 0.0001) and 2-year (48% vs. 35%; P < 0.0001) follow-up periods. More individuals with CE had been hospitalized at 1 year with seizures (12% vs. 8%; P <0.0001), neurologic disorders (9% vs. 4%; P <0.0001), infections (10% vs. 6%; P <0.0001),
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Figure 1. Absolute standardized difference plot for propensity matching showing the standardized difference between the craniotomy and craniectomy groups for all baseline variables before and after propensity matching. After matching, all baseline variables in the craniotomy and craniectomy groups had an absolute standardized difference of <10, which fulfilled the criteria for a successful match. AA, African American; CT, computed tomography; GCS, Glasgow Coma Scale; ICH, intracranial hemorrhage; ICP, intracranial pressure; IVH, intraventricular hemorrhage; SAH, subarachnoid hemorrhage; SDH, subdural hemorrhage.
orthopedic procedures (11% vs. 8%; P ¼ 0.001), and general health problems (11% vs. 8%; P ¼ 0.001). The functional outcomes for CE participants showed lower median total FIM scores on admission to inpatient rehabilitation (38 vs. 47; P < 0.0001) and on discharge from rehabilitation (86 vs. 92; P < 0.0001; Table 3). The FIM motor subscores were also lower in the CE group at rehabilitation admission (25 vs. 32; P < 0.0001) and discharge (63 vs. 67; P < 0.0001). The FIM cognitive subscores were also lower for CE patients at rehabilitation admission (11 vs. 14; P < 0.0001) and discharge (22 vs. 24; P < 0.0001). The total FIM scores, FIM motor subscores, and FIM cognitive subscores at the 1-year and 2-year follow-up examinations were clinically similar between the 2 groups, although a statistically significant difference was observed. The CE and CO groups both showed clinically significant within-group gains in total FIM scores from rehabilitation admission to the 1-year follow-up examination, although no differences in the median score gains were observed between the 2 groups (66 vs. 64; P ¼ 0.3). More individuals with CE demonstrated an unfavorable GOSE score (i.e., GOSE 4) at the 1-year (50% vs 42%; P ¼ 0.0001) and 2-year (45% vs. 38%; P ¼ 0.0002) follow-up examination (Table 3). The percentage of individuals requiring full-time supervision on the Supervision Rating Scale was greater in the CE group at the 1-year (25% vs. 18%; P < 0.0001) and 2-year (20% vs. 17%; P ¼ 0.03) follow-up visits. The disability rating scale scores at 1 and 2 years were not significantly different between the CO and CE groups. Despite lower functional scores, the median scores for the Satisfaction with Life Scale were similar between the 2 groups at 1 (31 vs. 29; P ¼ 0.5) and 2 (32 vs. 29; P ¼ 0.7) years. The mortality rates were similar between the CO and CE groups at 1 (4%) and
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Table 1. Baseline Admission Characteristics for All PropensityMatched TBI Patients Characteristic
Craniotomy (n [ 1470)
Craniectomy (n [ 1470)
Age (years) Median
Mean Standardized Difference 6.4
43
42
IQR
26e60
27e56
Male sex
1102 (75)
1097 (75)
0.15
AA race
305 (21)
321 (22)
2.9
Total GCS score Median IQR
3.7 11
11
7e14
7e14
Insurance type None
67 (5)
70 (5)
Referent
Private
706 (48)
707 (48)
3.0
Medicaid
414 (28)
414 (28)
4.7
Medicare
283 (19)
279 (19)
2.2
Education level
5.7
High school or less
878 (60)
899 (61)
College
486 (33)
462 (31)
Graduate
88 (6)
71 (5)
528 (36)
527 (36)
0.9
SAH
988 (67)
957 (65)
6.8
SDH
1085 (74)
1057 (72)
8.0
Married TBI subtype
IVH
407 (28)
416 (28)
0.5
ICH
1084 (74)
1090 (74)
0.15
I
342 (23)
385 (26)
Referent
II
278 (19)
265 (18)
4.2
III
244 (16)
237 (16)
0.9
IV
606 (41)
583 (40)
3.0
Elevated ICP
700 (48)
647 (44)
5.6
Penetrating injury
131 (9)
128 (9)
1.9
Marshall CT score
Data presented as n (%). IQR, interquartile range; AA, African American; GCS, Glasgow Coma Scale; TBI, traumatic brain injury; SAH, subarachnoid hemorrhage; SDH, subdural hemorrhage; IVH, intraventricular hemorrhage; ICH, intracerebral hemorrhage and/or contusions; CT, computed tomography; ICP, intracranial pressure.
2 (7%) years. The Kaplan-Meier estimates for mortality at the 1- and 2-year follow-up examinations were not different between the CE and CO groups (hazard ratio, 0.57; P ¼ 0.4; Figure 2).
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DISCUSSION For individuals treated within the TBIMS, CE was associated with an increased LOS, lower functional outcome scores, and more rehospitalizations. The CE participants also demonstrated lower FIM scores at both admission and discharge from acute TBI rehabilitation across the motor, cognitive, and total score domains compared with the CO patients. More CE participants had unfavorable GOSE scores and worse Supervision Rating Scale scores at the 1- and 2-year follow-up examinations. Fewer participants with CE were discharged to home or were employed at the 1-year follow-up examination, and more patients in the CE group were hospitalized for seizures, infections, and other neurologic disorders at the 1-year follow-up visit. Despite worse functional outcomes for those in the CE group over several domains, the Satisfaction with Life Scale scores and mortality remained similar between the 2 groups. Our results suggest that CE for individuals with moderately severe TBI is associated with significant functional burdens during a long-term follow-up period. Traditionally, CE has been reserved for the most severely injured TBI patients as a last resort, lifesaving measure. Recent studies have suggested that primary CE for patients with TBI, including subdural hemorrhage and/or intracranial hemorrhage, might improve survival and functional outcomes for patients with moderate to severe TBI.5,19-21 Most studies that have reported favorable CE outcomes have emphasized the noninferiority of CE compared with CO were limited by selection bias, the length of follow-up, and the use of the GOSE as the primary outcome measure.5,19-21 Other studies have suggested that CE confers no long-term benefits compared with CO,22 can lead to worse outcomes in severely injured patients with TBI with a GCS score of <5,23 and can be associated with greater in-hospital mortality.3 Our data examined a moderate to severely injured patient population with TBI with a median admission GCS score of 11 who required surgical intervention and who had survived their initial injuries well enough to participate in an inpatient rehabilitation program. In this particular patient population, CE for TBI did not alter the longer term survival rates and was associated with worse functional outcomes. Several studies have described the complications and burdens associated with CE for TBI, including seizures, hydrocephalus, infection, and complications associated with cranioplasty.1,10,24-26 In addition to procedural complications, the effect of a CE defect on long-term neurologic recovery remains poorly understood, with some recent studies suggesting reduced cerebral perfusion in patients with CE that improves after cranioplasty.27 How these complications and burdens affect patient outcomes during a long-term follow-up period across multiple functional domains has been less adequately described. Our results suggest that these complications and burdens are associated with significant functional limitations during long-term follow-up. Moreover, recently reported work from the TBIMS has suggested that the odds of late seizures after CE is almost double that observed with CO.28 However, another epidemiological study from the TBIMS has suggested that surgical evacuation of any type carries an increased risk of both early and late post-traumatic seizures (post-traumatic epilepsy).29 The elevated seizure risk in
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Table 2. Outcomes for Propensity-Matched Surgery Groups Variable
Craniotomy (n [ 1470)
Craniectomy (n [ 1470)
Median IQR
18
22
10-26
15e33
IQR Acute rehabilitation discharge to home
21
26
13e32
16e44
1172 (80)
1061 (72)
Variable
Craniotomy (n [ 1470)
Craniectomy (n [ 1470)
P Value
47 (27e66)
38 (21e60)
<0.0001*
FIM total score Rehab admission <0.0001*
LOS acute rehabilitation (days) Median
P Value <0.0001*
LOS hospital (days)
Table 3. Outcome Scales for Propensity-Matched Surgery Groups
<0.0001*
Employed 1 year
385 (26)
324 (22)
0.007*
2 years
351 (24)
302 (21)
0.3
Rehospitalization
92 (76e105)
86 (69e201)
<0.0001*
1 year
122 (113e126)
119 (106e125)
<0.0001*
2 years
123 (125e126)
122 (110e126)
0.0002*
Rehab admission
32 (17e47)
25 (14e41)
<0.0001*
Rehab discharge
67 (55e79)
63 (50e77)
<0.0001*
1 year
90 (84e91)
89 (78e91)
<0.0001*
2 years
91 (85e91)
90 (81e91)
0.0004*
Rehab discharge
FIM motor score
FIM cognitive score
1 year
371 (25)
569 (39)
<0.0001*
Rehab admission
14 (8e20)
11 (6e18)
<0.0001*
2 years
511 (35)
700 (48)
<0.0001*
Rehab discharge
24 (19e28)
22 (16e27)
<0.0001*
1 year
33 (29e35)
32 (27e35)
<0.0001*
2 years
33 (30e35)
33 (28e35)
0.0009*
Rehospitalization diagnosisy Seizures
115 (8)
183 (12)
<0.0001*
Neurologic disorder
61 (4)
138 (9)
<0.0001*
Disability rating scaley
Psychiatric
44 (3)
54 (4)
0.3
Rehab admission
12 (8e17)
14 (10e18)
<0.0001*
Infectious
90 (6)
150 (10)
<0.0001*
Rehab discharge
6 (5e8)
6 (5e9)
<0.0001*
Orthopedic
114 (8)
166 (11)
0.001*
1 year
3 (1e6)
3 (1e7)
0.006*
General health
113 (8)
163 (11)
0.001*
2 years
2 (0e5)
3 (1e7)
0.05
Other
114 (8)
117 (8)
0.8
1 year
624 (42)
727 (50)
0.0001*
2 years
558 (38)
657 (45)
0.0002*
1 year
260 (18)
363 (25)
<0.0001*
2 years
247 (17)
293 (20)
0.03*
1 year
29 (20e77)
31 (19e77)
0.5
2 years
29 (19e77)
32 (20e77)
0.7
Mortality 6 months
23 (2)
36 (2)
0.09
1 year
57 (4)
56 (4)
0.9
2 years
96 (7)
99 (7)
0.8
Data presented as n (%). LOS, length of stay; IQR, interquartile range. *Statistically significant. yOne-year follow-up point.
the TBI population has been linked to worse functional outcomes, including mental health conditions such as depression and anxiety,30,31 reduced cognitive performance,32 and a decreased return to work.33 Recurrent seizures can also contribute to injury beyond the initial TBI event via increased glial scar formation,34 inflammation,35 and excitotoxicity.36 The effect of rehospitalization for individuals with TBI is also understudied, especially in studies comparing CE and CO. Rehospitalization is a known predictor of poor outcomes for patients with TBI37 and results in substantial costs to the patients, families, and healthcare system.38 The rehospitalization rates for individuals with TBI have been
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GOSE score 4
Full-time supervision
Satisfaction with Life Scale
Data presented median (interquartile range) or as n (%). FIM, functional independence measure; Rehab ¼ acute rehabilitation; GOSE ¼ Glasgow Outcome Score-Extended. *Statistically significant. yHigher scores reflect more disability.
reported to be as great as 36%, with rehospitalization events occurring for many years after the initial injury.39,40 Our data suggest that after CE individuals experience more rehospitalization events related to post-TBI seizures, infections, and other neurologic sequelae such as headaches and hydrocephalus compared with those undergoing CO.
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Figure 2. Kaplan-Meier estimate of 2-year survival. The x-axis shows the time in days and the y-axis shows the
Most studies comparing the outcomes in the CE and CO patient populations have also lacked standardized follow-up protocols after hospital discharge, limiting the generalizability of the longterm outcome results.5,19-21 These studies also did not control for post-acute hospital discharge factors such as admission to a TBI rehabilitation unit, which has been associated with improved outcomes for TBI patients.41-44 The variability in post-acute hospital discharge care settings can affect the long-term outcomes of TBI patients.45 Our study has provided a standardized setting for assessing long-term outcomes, because all the individuals were treated in a TBI rehabilitation unit and had undergone a standardized follow-up protocol. Future prospective trials comparing CE and CO for patients with TBI should control for factors related to the posthospitalization care environment. Study Limitations The present study was a retrospective analysis of prospectively collected data and had several biases related to retrospective analyses, including surgical selection bias. In our nonrandomized sample, the baseline differences between study groups could have affected the outcomes. However, our study sample was wellmatched across groups and used propensity matching to control for selection bias according to the known predictors of outcomes of patients with TBI.14-17 The CE and CO groups both had similar TBI injury patterns, with similar Marshall CT scores and TBI subtypes observed in both populations. Propensity scores have been used for years to reduce the biased estimates of treatment effects in observational studies.17 Although a randomized controlled trial would better address some of these biases, the effect of surgeon selection and patient and family preferences in randomized controlled trials, especially in TBI, remains a
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probability of survival for the craniotomy and craniectomy groups.
considerable challenge.46 This challenge is perhaps even more pronounced for investigations of CO and CE in patients with TBI, because variations in the surgical rates exist across geographic regions and institutions.3 Clinical studies of TBI have been criticized for population heterogeneity and a lack of more specific outcome measures beyond the use of GOSE.11 Our study sample was a more homogenous population of individuals with moderately severe TBI who had undergone surgery and were able to participate in acute rehabilitation after hospitalization. The results of the present study do not apply to nonoperative TBI patients and might not apply to more severely injured TBI patients who are not admitted to acute inpatient TBI rehabilitation at acute care hospital discharge or who are not treated at a TBIMS institution. The distribution of GCS scores and Marshall CT scores in the present study population might limit the generalizability of our results because the CO and CE rates might not reflect the surgical practice patterns across the United States. However, the TBIMS population is considered representative of inpatient TBI rehabilitation programs and services in the United States,47 and previous TBIMS studies have described a moderately severe TBI population when more comprehensive injury severity criteria were applied such as Department of Defense TBI severity criteria.28,29 Furthermore, significant variations in CO and CE rates for TBI have been demonstrated across geographic regions and institutions, suggesting that the surgical rates could be driven by factors external to patient injury characteristics alone. The limitations of the TBIMS database include a lack of preinjury antithrombotic use, concomitant medical comorbidities, and additional radiographic information such as the presence of chronic subdural hematoma. These limitations in trauma databases are well-known and have
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prompted collaborative improvement efforts in forums such as the American College of Surgeons Trauma Quality Improvement Program.48 The TBIMS variable for elevated ICP does not provide detailed information about when the ICP elevations occurred or how long the ICP elevations were sustained. However, in the present study, ICP was used only for matching between the CE and CO participant groups and was not directly analyzed for its effects on outcome. In addition, the TBIMS variable for CO versus CE does not provide additional surgical details, including the size and type of CE performed. The rehospitalization data did not provide granularity for the rehospitalization diagnosis beyond the categories listed in Table 2. For example, increased infections in the CE group might or might not have been related to the cranioplasty procedure. However, infections unrelated to cranioplasty have also been associated with worse outcomes in patients with TBI.26,49,50 We used several functional outcome measures in the present study to overcome the limitations of the GOSE. However, standardized scales such as the FIM score have known ceiling effects among individuals with TBI, especially at long-term follow-up and might not be sufficiently sensitive to changes at the upper end of the scale over time.51 We were able to describe TBI subtypes; however,
2. Kolias AG, Hutchinson PJ, Menon DK, Manley GT, Gallagher CN, Servadei F. Decompressive craniectomy for acute subdural hematomas. J Neurosurg. 2014;120:1247-1249 [author reply: 1249]. 3. Rush B, Rousseau J, Sekhon MS, Griesdale DE. Craniotomy versus craniectomy for acute traumatic subdural hematoma in the united states: a national retrospective cohort analysis. World Neurosurg. 2016;88:25-31. 4. Kolias AG, Li LM, Guilfoyle MR, Timofeey I, Corteen EA, Pickard JD, et al. Decompressive craniectomy for acute subdural hematomas: time for a randomized trial. Acta Neurochir (Wien). 2013; 155:187-188. 5. Hartings JA, Vidgeon S, Strong AJ, Zacko C, Vagal A, Andaluz N, et al. Surgical management of traumatic brain injury: a comparativeeffectiveness study of 2 centers. J Neurosurg. 2014; 120:434-446. 6. Aarabi B, Hesdorffer DC, Ahn ES, Aresco C, Scalea TM, Eisenberg HM. Outcome following decompressive craniectomy for malignant swelling due to severe head injury. J Neurosurg. 2006;104:469-479. 7. Aarabi B, Chesler D, Maulucci C, Blacklock T, Alexander M. Dynamics of subdural hygroma following decompressive craniectomy: a comparative study. Neurosurg Focus. 2009;26:E8. 8. De Bonis P, Pompucci A, Mangiola A, Rigante L, Anile C. Post-traumatic hydrocephalus after
CONCLUSION The individuals who underwent CE compared with CO after TBI required a longer LOS in the hospital and acute rehabilitation and experienced decreased functional status and more rehospitalizations. Survival at 2 years and the Satisfaction with Life scores remained similar. In our study, CE for moderate to severe TBI was associated with worse functional outcomes. ACKNOWLEDGMENTS The TBIMS national database is a multicenter study of the TBIMS Centers Program and is supported by the National Institute on Disability, Independent Living, and Rehabilitation Research, a center within the Administration for Community Living, Department of Health and Human Services. However, the contents do not necessarily reflect the opinions or views of the TBIMS Centers, National Institute on Disability, Independent Living, and Rehabilitation Research, Administration for Community Living, or Department of Health and Human Services.
decompressive craniectomy: an underestimated risk factor. J Neurotrauma. 2010;27:1965-1970.
18. Stuart EA. Matching methods for causal inference: a review and a look forward. Stat Sci. 2010;25:1-21.
9. Joseph V, Reilly P. Syndrome of the trephined. J Neurosurg. 2009;111:650-652.
19. Li LM, Kolias AG, Guilfoyle MR, Timofeev I, Corteen EA, Pickard JD, et al. Outcome following evacuation of acute subdural haematomas: a comparison of craniotomy with decompressive craniectomy. Acta Neurochir (Wien). 2012;154: 1555-1561.
REFERENCES 1. Kolias AG, Kirkpatrick PJ, Hutchinson PJ. Decompressive craniectomy: past, present and future. Nat Rev Neurol. 2013;9:405-415.
we were not able to isolate these subtypes for further analysis because most individuals in our sample had had >1 TBI injury subtype.
10. Honeybul S, Ho KM. Cranioplasty: morbidity and failure. Br J Neurosurg. 2016;30:1-6. 11. Manley GT, Maas AI. Traumatic brain injury: an international knowledge-based approach. JAMA. 2013;310:473-474. 12. Bullock MR, Chesnut R, Ghajar J, Gordon D, Hartl R, Newell DW, et al. Surgical management of acute subdural hematomas. Neurosurgery. 2006; 58(suppl):S16-S24 [discussion: Si-Siv]. 13. Bullock MR, Chesnut R, Ghajar J, Gordon D, Hartl R, Newell DW, et al. Surgical management of traumatic parenchymal lesions. Neurosurgery. 2006;58(suppl):S25-S46 [discussion: Si-Siv]. 14. Baum J, Entezami P, Shah K, Medhkour A. Predictors of outcomes in traumatic brain injury. World Neurosurg. 2015;90:525-529. 15. Yue JK, Vassar MJ, Lingsma HF, Cooper SR, Okonwo DO, Valadka AB, et al. Transforming research and clinical knowledge in traumatic brain injury pilot: multicenter implementation of the common data elements for traumatic brain injury. J Neurotrauma. 2013;30:1831-1844. 16. Rosenbaum PR, Rubin D. The central role of the propensity score in observational studies for causal effects. Biometrika. 1983;70:41-55. 17. D’Agostino RB Jr. Propensity score methods for bias reduction in the comparison of a treatment to a non-randomized control group. Stat Med. 1998; 17:2265-2281.
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20. Huang AP, Tu YK, Tsai YH, Chen YS, Hong WC, Yang CC, et al. Decompressive craniectomy as the primary surgical intervention for hemorrhagic contusion. J Neurotrauma. 2008;25:1347-1354. 21. Chen SH, Chen Y, Fang WK, Huang DW, Huang KC, Tseng SH. Comparison of craniotomy and decompressive craniectomy in severely headinjured patients with acute subdural hematoma. J Trauma. 2011;71:1632-1636. 22. Woertgen C, Rothoerl RD, Schebesch KM, Albert R. Comparison of craniotomy and craniectomy in patients with acute subdural haematoma. J Clin Neurosci. 2006;13:718-721. 23. Pompucci A, De Bonis P, Pettorini B, Petrella G, Di Chirico A, Anile C. Decompressive craniectomy for traumatic brain injury: patient age and outcome. J Neurotrauma. 2007;24:1182-1188. 24. Zanaty M, Chalouhi N, Starke RM, Clark SW, Bovenzi CD, Saigh M, et al. Complications following cranioplasty: incidence and predictors in 348 cases. J Neurosurg. 2015;123:182-188. 25. Honeybul S, Ho KM. Decompressive craniectomy for severe traumatic brain injury: the relationship between surgical complications and the prediction of an unfavourable outcome. Injury. 2014;45: 1332-1339.
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26. Stiver SI. Complications of decompressive craniectomy for traumatic brain injury. Neurosurg Focus. 2009;26:E7.
reactions in human medial temporal lobe epilepsy with hippocampal sclerosis. Brain Res. 2002;952: 159-169.
46. Honeybul S, Ho KM, Lind CR. What can be learned from the DECRA study. World Neurosurg. 2013;79:159-161.
27. Paredes I, Castano-Leon AM, Cepeda S, Fernández Alén JA, Salvador E, Millán JM, et al. The effect of cranioplasty on cerebral hemodynamics as measured by perfusion CT and Doppler ultrasonography. J Neurotrauma. 2016;33:1586-1597.
36. Coulter DA, Eid T. Astrocytic regulation of glutamate homeostasis in epilepsy. Glia. 2012;60:1215-1226.
47. Corrigan JD, Cuthbert JP, Whiteneck GG, Dijkers MP, Coronado V, Heinemann AW, et al. Representativeness of the Traumatic Brain Injury Model Systems national database. J Head Trauma Rehabil. 2012;27:391-403.
28. Ritter AC, Wagner AK, Szaflarski JP, Brooks MM, Zafonte RD, Pugh MJ, et al. Prognostic models for predicting posttraumatic seizures during acute hospitalization, and at 1 and 2 years following traumatic brain injury. Epilepsia. 2016;57:1503-1514. 29. Ritter AC, Wagner AK, Fabio A, Pugh MJ, Walker WC, Szaflarski JP, et al. Incidence and risk factors of posttraumatic seizures following traumatic brain injury: a Traumatic Brain Injury Model Systems study. Epilepsia. 2016;57:1968-1977. 30. Hesdorffer DC, Ishihara L, Mynepalli L, Webb DJ, Weil J, Hauser WA. Epilepsy, suicidality, and psychiatric disorders: a bidirectional association. Ann Neurol. 2012;72:184-191. 31. Juengst SB, Wagner AK, Ritter AC, Szaflarski JP, Walker WC, Zafonte RD, et al. Post-traumatic epilepsy associations with mental health outcomes in the first two years after moderate to severe TBI: a TBI Model Systems analysis. Epilepsy Behav. 2017; 73:240-246. 32. Dikmen SS, Machamer JE, Winn HR, Anderson GD, Temkin NR. Neuropsychological effects of valproate in traumatic brain injury: a randomized trial. Neurology. 2000;54:895-902. 33. Bushnik T, Englander J, Wright J, KolakowskyHayner SA. Traumatic brain injury with and without late posttraumatic seizures: what are the impacts in the post-acute phase: a NIDRR Traumatic Brain Injury Model Systems study. J Head Trauma Rehabil. 2012;27:E36-E44. 34. Robel S. Astroglial scarring and seizures: a cell biological perspective on epilepsy [e-pub ahead of print]. Neuroscientist. accessed January 26, 2018. 35. Crespel A, Coubes P, Rousset MC, Brana C, Rougier A, Rondouin G, et al. Inflammatory
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37. Cameron CM, Purdie DM, Kliewer EV, McClure RJ. Ten-year outcomes following traumatic brain injury: a population-based cohort. Brain injury. 2008;22:437-449. 38. Jencks SF, Williams MV, Coleman EA. Rehospitalizations among patients in the Medicare fee-forservice program. N Engl J Med. 2009;360:1418-1428. 39. Marwitz JH, Cifu DX, Englander J, High WM Jr. A multi-center analysis of rehospitalizations five years after brain injury. J Head Trauma Rehabil. 2001;16:307-317. 40. Saverino C, Swaine B, Jaglal S, Lewko J, Vernich L, Voth J, et al. Rehospitalization after traumatic brain injury: a population-based study. Arch Phys Med Rehabil. 2016;97(suppl):S19-S25. 41. Griesbach GS, Kreber LA, Harrington D, Ashley MJ. Post-acute traumatic brain injury rehabilitation: effects on outcome measures and life care costs. J Neurotrauma. 2015;32:704-711. 42. Kelly ML, Roach MJ, Banerjee A, Steinmetz MP, Claridge JA. Functional and long-term outcomes in severe traumatic brain injury following regionalization of a trauma system. J Trauma Acute Care Surg. 2015;79:372-377. 43. Pickelsimer EE, Selassie AW, Sample PL, W Heinemann A, Gu JK, Veldheer LC. Unmet service needs of persons with traumatic brain injury. J Head Trauma Rehabil. 2007;22:1-13. 44. Turner-Stokes L, Disler PB, Nair A, Wade DT. Multi-disciplinary rehabilitation for acquired brain injury in adults of working age. Cochrane Database Syst Rev. 2005:CD004170.
48. American College of Surgeons. Trauma Quality Improvement Program (TQIP) Collaboratives 2018. Available at: https://www.facs.org/qualityprograms/trauma/tqip/collaboratives. Accessed July 12, 2018. 49. Harrison-Felix C, Pretz C, Hammond FM, Cuthbert JP, Bell J, Corrigan J, et al. Life expectancy after inpatient rehabilitation for traumatic brain injury in the United States. J Neurotrauma. 2015;32:1893-1901. 50. Kumar RG, Boles JA, Wagner AK. Chronic inflammation after severe traumatic brain injury: characterization and associations with outcome at 6 and 12 months postinjury. J Head Trauma Rehabil. 2015;30:369-381. 51. Hall KM, Mann N, High WM, Wright J, Kreutzer J, Wood D. Functional measures after traumatic brain injury: ceiling effects of FIM, FIMþFAM, DRS, and CIQ. J Head Trauma Rehabil. 1996;11: 27-39.
Conflict of interest statement: This work was supported in part by the National Institute on Disability, Independent Living, and Rehabilitation Research (grant 90DP0041 to A.K.W.). A portion of this work was presented at the 2016 Congress of Neurological Surgeons Annual Meeting. Received 31 May 2018; accepted 13 July 2018 Citation: World Neurosurg. (2018). https://doi.org/10.1016/j.wneu.2018.07.124 Journal homepage: www.WORLDNEUROSURGERY.org
45. Kelly ML. Intensive care unit guideline adherence and severe traumatic brain injury: the challenge of comprehensive neurotrauma care worldwide. World Neurosurg. 2016;90:659-660.
Available online: www.sciencedirect.com 1878-8750/$ - see front matter ª 2018 Elsevier Inc. All rights reserved.
WORLD NEUROSURGERY, https://doi.org/10.1016/j.wneu.2018.07.124
Craniectomy and Craniotomy in Traumatic Brain Injury: A Propensity-Matched Analysis of Long-Term Functional and Quality of Life Outcomes Michael L. Kelly1, Berje Shammassian3, Mary Jo Roach2, Charles Thomas2, Amy K. Wagner4
OBJECTIVE: To report the comprehensive long-term functional and quality of life outcomes after craniectomy (CE) and craniotomy (CO) in individuals with traumatic brain injury (TBI).
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METHODS: Information on all individuals with TBI who had undergone CE or CO were extracted from the TBI Model Systems database from 2002 to 2012. A 1:1 propensity matching with replacement technique was used to balance the baseline characteristics across groups. The matched sample was analyzed for outcomes during hospitalization, acute rehabilitation, and £2 years of follow-up.
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RESULTS: We identified 1470 individuals who had undergone CE or CO. Individuals undergoing CE compared with CO demonstrated a longer length of stay in the hospital (median, 22 vs. 18 days; P < 0.0001) and acute rehabilitation (median 26 vs. 21 days; P < 0.0001). Individuals with CE had required rehospitalization more often by the 1-year follow-up point (39% vs. 25%; P < 0.0001) for reasons other than cranioplasty, including seizures (12% vs. 8%; P < 0.0001), neurologic events (i.e., hydrocephalus; 9% vs. 4%; P < 0.0001), and infections (10% vs 6%; P < 0.0001). Individuals with CE had significantly greater impairment using the Glasgow Outcome Scale-Extended, required more supervision, and were less likely to be employed at 1 and 2 years after TBI. No difference was observed in the satisfaction with life scale scores at 2 years. The
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Keywords Outcome measures - Rehabilitation - Surgery - TBI model systems - Traumatic brain injury -
Abbreviations and Acronyms CE: Craniectomy CO: Craniotomy CT: Computed tomography FIM: functional independence measure GCS: Glasgow Coma Scale GOSE: Glasgow Outcome Scale-Extended ICP: Intracranial pressure LSO: length of stay
Kaplan-Meier mortality estimates at 1 and 2 years showed no differences between the 2 groups (hazard ratio, 0.57; P [ 0.4). CONCLUSION: In a matched cohort, individuals undergoing CE compared with CO after TBI had a longer length of stay, decreased functional status, and more rehospitalizations. The survival at 2 years and the satisfaction with life scale scores were similar.
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INTRODUCTION
S
urgery for individuals with traumatic brain injury (TBI) remains controversial.1 Studies have documented variability in surgical procedural rates, timing, and the type of surgery performed.1-3 Debate continues regarding whether decompressive craniectomy (CE) (i.e., bone removal with later reimplantation) is superior to craniotomy (CO) (i.e., bone removal and replacement in the same surgery) in those with acute TBI.1,4 Some studies have suggested that CE might be superior because it reduces intracranial pressure (ICP) and more effectively limits brain swelling, leading to improved survival and better functional outcomes.5,6 Other studies have emphasized the risks and complications of CE, including subdural hygromas, seizures, hydrocephalus, and sinking flap syndrome.7-10 The studies that compared CE and CO often lacked comprehensive outcome measures, including quality of life scores,
TBI: Traumatic brain injury TBIMS: Traumatic brain injury model systems From the 1Department of Neurosurgery and 2Center for Healthcare Research and Policy, Case Western Reserve University School of Medicine, MetroHealth Medical Center, Cleveland, Ohio, USA; 3Department of Neurosurgery, University Hospitals Cleveland Medical Center, Cleveland, Ohio, USA; and 4Department of Physical Medicine and Rehabilitation, Neuroscience, Safar Center for Resuscitation Research, Center for Neurobiology, University of Pittsburgh School of Medicine, Pittsburgh, Pennsylvania, USA To whom correspondence should be addressed: Michael L. Kelly, M.D. [E-mail: [email protected]] Citation: World Neurosurg. (2018). https://doi.org/10.1016/j.wneu.2018.07.124 Journal homepage: www.WORLDNEUROSURGERY.org Available online: www.sciencedirect.com 1878-8750/$ - see front matter ª 2018 Elsevier Inc. All rights reserved.
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detailed functional assessments, and longer term follow-up data. Data beyond a 3- to 6-month post-TBI period is especially important in the CE population because cranial bone reimplantation often occurs several months after the initial surgery and carries additional risks related to a second cranial operation, including infection, bleeding, and cerebrospinal fluid leakage.10 The traditional outcome measures such as the Glasgow Outcome Scale-Extended (GOSE) lack specificity and sensitivity to treatment effects in this population.11 Given the conflicting study results and limitations in the design of existing studies, the 2006 Brain Trauma Foundation guidelines for the surgical management of TBI identified the issues of CE versus CO as a top priority for future research.12,13 In the present study, we analyzed the National Institute on Disability, Independent Living, and Rehabilitation Research TBI model systems (TBIMS) database to compare the long-term survival and functional outcomes between individuals with TBI who had undergone CE compared with CO in medical centers across the United States. We hypothesized that higher survival rates, but lower functional outcomes scores, would be found for individuals who had undergone CE compared with CO. METHODS Data Source The TBIMS national database was queried to identify all TBI admissions to rehabilitation facilities in the United States participating in the TBIMS program from 2002 through 2012. The TBIMS is a national project funded by the National Institute on Disability, Independent Living, and Rehabilitation Research. The project is the first prospective, multicenter study of the recovery and outcomes of individuals with TBI after participation in a coordinated system of acute neurotrauma care and inpatient rehabilitation. Institutions that are designated as TBIMS centers must have access to level 1 trauma center care, acute neurosurgical care, comprehensive inpatient rehabilitation services, and long-term interdisciplinary follow-up and rehabilitation services. Currently, 16 TBIMS centers and 3 previously funded facilities that continue to provide follow-up data have been designated across the United States. The TBIMS database inclusion criteria are (1) complicated mild, moderate, or severe TBI; (2) emergency department evaluation within 72 hours of injury; (3) age 16 years; (4) hospital care and inpatient rehabilitation received within a participating TBIMS facility; and (5) written informed consent provided by the patient and/or guardian. More information is available from the National Data and Statistical Center (available at: https://www.tbindsc.org/). Patient Selection and Characteristics We identified all TBIMS participants who had undergone either CO or CE during their acute hospital admission. Individuals who had initially undergone CO but then underwent a subsequent CE during the same hospitalization were included in the CE group. All available hospitalization-related factors known to influence postdischarge outcomes in postoperative patients with TBI were analyzed, including clinical information, demographic data, and
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socioeconomic factors.14,15 Race was dichotomized into African-American and noneAfrican-American. The TBI subtype was defined using the TBIMS intracranial computed tomography (CT) diagnosis variable and included subarachnoid hemorrhage, subdural hemorrhage, intraventricular hemorrhage, and intracranial hemorrhage and/or contusions. Each individual with TBI could have had multiple TBI subtypes recorded. The TBIMS variable for the Marshall CT score was used to identify the extent of intracranial compression on the CT scan. Elevated ICP was identified using the variable “CC_Hypertension” and is defined in the TBIMS database as 1 documented ICP peaks of 20 mm Hg during the acute hospitalization period. The ICP data were typically obtained from the nursing flowsheets from the intensive care unit in the hospital records. The insurance type was coded as none, private, Medicaid, and Medicare using the TBIMS variable for insurance status (“AcutePay1”). The education level was recoded as high school graduate or less, college degree or some college, and graduate degree using the TBIMS education variable. Outcomes The length of stay (LOS) was defined as total number of days the individual was admitted to the acute hospital or TBI rehabilitation. Functional outcomes were measured at admission to the TBIMS rehabiliation unit, discharge from the rehabilitation unit, and at the 1- and 2-year follow-up points. The functional independence measure (FIM) score was reported as an overall score and as separate subscores for motor and cognitive function. The Glasgow Outcome Scale-Extended (GOSE) score was dichotomized into unfavorable (GOSE 4) and favorable (GOSE >4) outcomes at the 1- and 2-year follow-up points. The Supervision Rating Scale was completed at the 1- and 2-year follow-up points and was dichotomized as full-time supervision or partial supervision/independent living. The Satisfaction with Life Scale score is a standardized, self-reported outcome measure that was reported as the median value at the 1- and 2-year follow-up points. The Disability Rating Scale measures objective signs of physical impairment and was reported as the median value at the 1- and 2-year follow-up points. The employment variable (EMPLOY) was measured at the 1- and 2-year follow-up points and dichotomized into unemployed and any type of employment. The discharge disposition from TBI rehabilitation was dichotomized into home or any assisted living facility or nursing facility using the TBIMS variable RESIDENCE. The total number of rehospitalizations (REHOSP) in the preceding year are recorded in the TBIMS at each annual follow-up examination. Rehospitalization was defined in the present study as 1 rehospitalization events annually. For each rehospitalization event, the rehospitalization diagnosis was also recorded from the individual and family self-report, including seizures, neurologic disorders (i.e., head injury, hydrocephalus, headaches), psychiatric issues, infections (i.e., wound infection, meningitis), orthopedic procedures (i.e., cranioplasty or any reconstructive surgeries), general health-related problems, and other miscellaneous medical problems. The rehospitalization diagnosis was only reported at the 1-year follow-up point because >30% of these data were missing at the 2-year follow-up examination. Multiple diagnoses could be reported by the participant and/or family for each rehospitalization
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ORIGINAL ARTICLE MICHAEL L. KELLY ET AL.
CRANIECTOMY AND CRANIOTOMY IN TBI
event. The survival time was calculated using the TBIMS “Death Date” variable, with the data extracted from the Social Security Death Index. Statistical Analysis Propensity scores were generated to reduce any potential bias between individuals in the CO and CE groups using the following variables: age, sex, race, insurance status, marital status, education level, employment status, TBI subtypes, GCS score, penetrating injury, elevated ICP, and Marshall CT score.16 We imputed for any baseline patient variables that were missing at random using a multivariate regression method of imputation before implementing the propensity score-matching routine. Propensity scores have been used to reduce biased estimates of treatment effects in observational studies.17 A 1:1 propensity-matching technique with replacement was used to balance patients across the CO and CE groups. The criterion for successful matching was established as an absolute standardized difference of <10. Individual baseline characteristics and outcomes were compared across the CO and CE groups using the Pearson c2 test for categorical variables and the Mann-Whitney U test for all nonparametric continuous variables.18 Covariates were compared between the CO and CE groups in the matched sample across all outcome measures. Cox proportional hazard modeling was performed after matching to determine the survival estimates for both groups. Analyses were performed using SPSS software, version 23.0 (IBM Corp., Armonk, New York, USA) and R software (R Foundation for Statistical Computing, Vienna, Austria). Statistical significance was set at P 0.05. RESULTS A total of 2567 admissions were identified in the TBIMS database before propensity matching, including 1470 CO participants and 1097 CE participants. The rates of CE and CO varied across the TBIM institutions. The CE rates ranged from 30% to 70% of all surgical admissions to TBIMS institutions. After propensity matching with replacement, we identified a cohort of 1470 individuals in each group who were matched across all baseline admission characteristics (Figure 1). The individuals in the CO and CE groups were successfully matched across age, sex, race, insurance type, educational level, marital status, GCS score, TBI subtype, Marshall CT score, elevated ICP, and penetrating injury mechanism (Table 1). The median GCS score was 11 (interquartile range, 7e14) for both groups, and most individuals in the CE (72%) and CO (74%) groups presented with a subdural hemorrhage. The CE participants had a longer LOS in the hospital (median, 22 vs. 18 days; P < 0.0001) and in acute rehabilitation (median, 26 vs. 21 days; P < 0.0001; Table 2). Fewer individuals with CE were discharged to home after inpatient rehabilitation (72% vs. 80%; P < 0.0001), and fewer were employed at the 1-year follow-up examination (22% vs. 26%; P ¼ 0.007). More CE participants were readmitted to the hospital at some point during the 1-year (39% vs. 25%; P < 0.0001) and 2-year (48% vs. 35%; P < 0.0001) follow-up periods. More individuals with CE had been hospitalized at 1 year with seizures (12% vs. 8%; P <0.0001), neurologic disorders (9% vs. 4%; P <0.0001), infections (10% vs. 6%; P <0.0001),
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Figure 1. Absolute standardized difference plot for propensity matching showing the standardized difference between the craniotomy and craniectomy groups for all baseline variables before and after propensity matching. After matching, all baseline variables in the craniotomy and craniectomy groups had an absolute standardized difference of <10, which fulfilled the criteria for a successful match. AA, African American; CT, computed tomography; GCS, Glasgow Coma Scale; ICH, intracranial hemorrhage; ICP, intracranial pressure; IVH, intraventricular hemorrhage; SAH, subarachnoid hemorrhage; SDH, subdural hemorrhage.
orthopedic procedures (11% vs. 8%; P ¼ 0.001), and general health problems (11% vs. 8%; P ¼ 0.001). The functional outcomes for CE participants showed lower median total FIM scores on admission to inpatient rehabilitation (38 vs. 47; P < 0.0001) and on discharge from rehabilitation (86 vs. 92; P < 0.0001; Table 3). The FIM motor subscores were also lower in the CE group at rehabilitation admission (25 vs. 32; P < 0.0001) and discharge (63 vs. 67; P < 0.0001). The FIM cognitive subscores were also lower for CE patients at rehabilitation admission (11 vs. 14; P < 0.0001) and discharge (22 vs. 24; P < 0.0001). The total FIM scores, FIM motor subscores, and FIM cognitive subscores at the 1-year and 2-year follow-up examinations were clinically similar between the 2 groups, although a statistically significant difference was observed. The CE and CO groups both showed clinically significant within-group gains in total FIM scores from rehabilitation admission to the 1-year follow-up examination, although no differences in the median score gains were observed between the 2 groups (66 vs. 64; P ¼ 0.3). More individuals with CE demonstrated an unfavorable GOSE score (i.e., GOSE 4) at the 1-year (50% vs 42%; P ¼ 0.0001) and 2-year (45% vs. 38%; P ¼ 0.0002) follow-up examination (Table 3). The percentage of individuals requiring full-time supervision on the Supervision Rating Scale was greater in the CE group at the 1-year (25% vs. 18%; P < 0.0001) and 2-year (20% vs. 17%; P ¼ 0.03) follow-up visits. The disability rating scale scores at 1 and 2 years were not significantly different between the CO and CE groups. Despite lower functional scores, the median scores for the Satisfaction with Life Scale were similar between the 2 groups at 1 (31 vs. 29; P ¼ 0.5) and 2 (32 vs. 29; P ¼ 0.7) years. The mortality rates were similar between the CO and CE groups at 1 (4%) and
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CRANIECTOMY AND CRANIOTOMY IN TBI
Table 1. Baseline Admission Characteristics for All PropensityMatched TBI Patients Characteristic
Craniotomy (n [ 1470)
Craniectomy (n [ 1470)
Age (years) Median
Mean Standardized Difference 6.4
43
42
IQR
26e60
27e56
Male sex
1102 (75)
1097 (75)
0.15
AA race
305 (21)
321 (22)
2.9
Total GCS score Median IQR
3.7 11
11
7e14
7e14
Insurance type None
67 (5)
70 (5)
Referent
Private
706 (48)
707 (48)
3.0
Medicaid
414 (28)
414 (28)
4.7
Medicare
283 (19)
279 (19)
2.2
Education level
5.7
High school or less
878 (60)
899 (61)
College
486 (33)
462 (31)
Graduate
88 (6)
71 (5)
528 (36)
527 (36)
0.9
SAH
988 (67)
957 (65)
6.8
SDH
1085 (74)
1057 (72)
8.0
Married TBI subtype
IVH
407 (28)
416 (28)
0.5
ICH
1084 (74)
1090 (74)
0.15
I
342 (23)
385 (26)
Referent
II
278 (19)
265 (18)
4.2
III
244 (16)
237 (16)
0.9
IV
606 (41)
583 (40)
3.0
Elevated ICP
700 (48)
647 (44)
5.6
Penetrating injury
131 (9)
128 (9)
1.9
Marshall CT score
Data presented as n (%). IQR, interquartile range; AA, African American; GCS, Glasgow Coma Scale; TBI, traumatic brain injury; SAH, subarachnoid hemorrhage; SDH, subdural hemorrhage; IVH, intraventricular hemorrhage; ICH, intracerebral hemorrhage and/or contusions; CT, computed tomography; ICP, intracranial pressure.
2 (7%) years. The Kaplan-Meier estimates for mortality at the 1- and 2-year follow-up examinations were not different between the CE and CO groups (hazard ratio, 0.57; P ¼ 0.4; Figure 2).
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DISCUSSION For individuals treated within the TBIMS, CE was associated with an increased LOS, lower functional outcome scores, and more rehospitalizations. The CE participants also demonstrated lower FIM scores at both admission and discharge from acute TBI rehabilitation across the motor, cognitive, and total score domains compared with the CO patients. More CE participants had unfavorable GOSE scores and worse Supervision Rating Scale scores at the 1- and 2-year follow-up examinations. Fewer participants with CE were discharged to home or were employed at the 1-year follow-up examination, and more patients in the CE group were hospitalized for seizures, infections, and other neurologic disorders at the 1-year follow-up visit. Despite worse functional outcomes for those in the CE group over several domains, the Satisfaction with Life Scale scores and mortality remained similar between the 2 groups. Our results suggest that CE for individuals with moderately severe TBI is associated with significant functional burdens during a long-term follow-up period. Traditionally, CE has been reserved for the most severely injured TBI patients as a last resort, lifesaving measure. Recent studies have suggested that primary CE for patients with TBI, including subdural hemorrhage and/or intracranial hemorrhage, might improve survival and functional outcomes for patients with moderate to severe TBI.5,19-21 Most studies that have reported favorable CE outcomes have emphasized the noninferiority of CE compared with CO were limited by selection bias, the length of follow-up, and the use of the GOSE as the primary outcome measure.5,19-21 Other studies have suggested that CE confers no long-term benefits compared with CO,22 can lead to worse outcomes in severely injured patients with TBI with a GCS score of <5,23 and can be associated with greater in-hospital mortality.3 Our data examined a moderate to severely injured patient population with TBI with a median admission GCS score of 11 who required surgical intervention and who had survived their initial injuries well enough to participate in an inpatient rehabilitation program. In this particular patient population, CE for TBI did not alter the longer term survival rates and was associated with worse functional outcomes. Several studies have described the complications and burdens associated with CE for TBI, including seizures, hydrocephalus, infection, and complications associated with cranioplasty.1,10,24-26 In addition to procedural complications, the effect of a CE defect on long-term neurologic recovery remains poorly understood, with some recent studies suggesting reduced cerebral perfusion in patients with CE that improves after cranioplasty.27 How these complications and burdens affect patient outcomes during a long-term follow-up period across multiple functional domains has been less adequately described. Our results suggest that these complications and burdens are associated with significant functional limitations during long-term follow-up. Moreover, recently reported work from the TBIMS has suggested that the odds of late seizures after CE is almost double that observed with CO.28 However, another epidemiological study from the TBIMS has suggested that surgical evacuation of any type carries an increased risk of both early and late post-traumatic seizures (post-traumatic epilepsy).29 The elevated seizure risk in
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Table 2. Outcomes for Propensity-Matched Surgery Groups Variable
Craniotomy (n [ 1470)
Craniectomy (n [ 1470)
Median IQR
18
22
10-26
15e33
IQR Acute rehabilitation discharge to home
21
26
13e32
16e44
1172 (80)
1061 (72)
Variable
Craniotomy (n [ 1470)
Craniectomy (n [ 1470)
P Value
47 (27e66)
38 (21e60)
<0.0001*
FIM total score Rehab admission <0.0001*
LOS acute rehabilitation (days) Median
P Value <0.0001*
LOS hospital (days)
Table 3. Outcome Scales for Propensity-Matched Surgery Groups
<0.0001*
Employed 1 year
385 (26)
324 (22)
0.007*
2 years
351 (24)
302 (21)
0.3
Rehospitalization
92 (76e105)
86 (69e201)
<0.0001*
1 year
122 (113e126)
119 (106e125)
<0.0001*
2 years
123 (125e126)
122 (110e126)
0.0002*
Rehab admission
32 (17e47)
25 (14e41)
<0.0001*
Rehab discharge
67 (55e79)
63 (50e77)
<0.0001*
1 year
90 (84e91)
89 (78e91)
<0.0001*
2 years
91 (85e91)
90 (81e91)
0.0004*
Rehab discharge
FIM motor score
FIM cognitive score
1 year
371 (25)
569 (39)
<0.0001*
Rehab admission
14 (8e20)
11 (6e18)
<0.0001*
2 years
511 (35)
700 (48)
<0.0001*
Rehab discharge
24 (19e28)
22 (16e27)
<0.0001*
1 year
33 (29e35)
32 (27e35)
<0.0001*
2 years
33 (30e35)
33 (28e35)
0.0009*
Rehospitalization diagnosisy Seizures
115 (8)
183 (12)
<0.0001*
Neurologic disorder
61 (4)
138 (9)
<0.0001*
Disability rating scaley
Psychiatric
44 (3)
54 (4)
0.3
Rehab admission
12 (8e17)
14 (10e18)
<0.0001*
Infectious
90 (6)
150 (10)
<0.0001*
Rehab discharge
6 (5e8)
6 (5e9)
<0.0001*
Orthopedic
114 (8)
166 (11)
0.001*
1 year
3 (1e6)
3 (1e7)
0.006*
General health
113 (8)
163 (11)
0.001*
2 years
2 (0e5)
3 (1e7)
0.05
Other
114 (8)
117 (8)
0.8
1 year
624 (42)
727 (50)
0.0001*
2 years
558 (38)
657 (45)
0.0002*
1 year
260 (18)
363 (25)
<0.0001*
2 years
247 (17)
293 (20)
0.03*
1 year
29 (20e77)
31 (19e77)
0.5
2 years
29 (19e77)
32 (20e77)
0.7
Mortality 6 months
23 (2)
36 (2)
0.09
1 year
57 (4)
56 (4)
0.9
2 years
96 (7)
99 (7)
0.8
Data presented as n (%). LOS, length of stay; IQR, interquartile range. *Statistically significant. yOne-year follow-up point.
the TBI population has been linked to worse functional outcomes, including mental health conditions such as depression and anxiety,30,31 reduced cognitive performance,32 and a decreased return to work.33 Recurrent seizures can also contribute to injury beyond the initial TBI event via increased glial scar formation,34 inflammation,35 and excitotoxicity.36 The effect of rehospitalization for individuals with TBI is also understudied, especially in studies comparing CE and CO. Rehospitalization is a known predictor of poor outcomes for patients with TBI37 and results in substantial costs to the patients, families, and healthcare system.38 The rehospitalization rates for individuals with TBI have been
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GOSE score 4
Full-time supervision
Satisfaction with Life Scale
Data presented median (interquartile range) or as n (%). FIM, functional independence measure; Rehab ¼ acute rehabilitation; GOSE ¼ Glasgow Outcome Score-Extended. *Statistically significant. yHigher scores reflect more disability.
reported to be as great as 36%, with rehospitalization events occurring for many years after the initial injury.39,40 Our data suggest that after CE individuals experience more rehospitalization events related to post-TBI seizures, infections, and other neurologic sequelae such as headaches and hydrocephalus compared with those undergoing CO.
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CRANIECTOMY AND CRANIOTOMY IN TBI
Figure 2. Kaplan-Meier estimate of 2-year survival. The x-axis shows the time in days and the y-axis shows the
Most studies comparing the outcomes in the CE and CO patient populations have also lacked standardized follow-up protocols after hospital discharge, limiting the generalizability of the longterm outcome results.5,19-21 These studies also did not control for post-acute hospital discharge factors such as admission to a TBI rehabilitation unit, which has been associated with improved outcomes for TBI patients.41-44 The variability in post-acute hospital discharge care settings can affect the long-term outcomes of TBI patients.45 Our study has provided a standardized setting for assessing long-term outcomes, because all the individuals were treated in a TBI rehabilitation unit and had undergone a standardized follow-up protocol. Future prospective trials comparing CE and CO for patients with TBI should control for factors related to the posthospitalization care environment. Study Limitations The present study was a retrospective analysis of prospectively collected data and had several biases related to retrospective analyses, including surgical selection bias. In our nonrandomized sample, the baseline differences between study groups could have affected the outcomes. However, our study sample was wellmatched across groups and used propensity matching to control for selection bias according to the known predictors of outcomes of patients with TBI.14-17 The CE and CO groups both had similar TBI injury patterns, with similar Marshall CT scores and TBI subtypes observed in both populations. Propensity scores have been used for years to reduce the biased estimates of treatment effects in observational studies.17 Although a randomized controlled trial would better address some of these biases, the effect of surgeon selection and patient and family preferences in randomized controlled trials, especially in TBI, remains a
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probability of survival for the craniotomy and craniectomy groups.
considerable challenge.46 This challenge is perhaps even more pronounced for investigations of CO and CE in patients with TBI, because variations in the surgical rates exist across geographic regions and institutions.3 Clinical studies of TBI have been criticized for population heterogeneity and a lack of more specific outcome measures beyond the use of GOSE.11 Our study sample was a more homogenous population of individuals with moderately severe TBI who had undergone surgery and were able to participate in acute rehabilitation after hospitalization. The results of the present study do not apply to nonoperative TBI patients and might not apply to more severely injured TBI patients who are not admitted to acute inpatient TBI rehabilitation at acute care hospital discharge or who are not treated at a TBIMS institution. The distribution of GCS scores and Marshall CT scores in the present study population might limit the generalizability of our results because the CO and CE rates might not reflect the surgical practice patterns across the United States. However, the TBIMS population is considered representative of inpatient TBI rehabilitation programs and services in the United States,47 and previous TBIMS studies have described a moderately severe TBI population when more comprehensive injury severity criteria were applied such as Department of Defense TBI severity criteria.28,29 Furthermore, significant variations in CO and CE rates for TBI have been demonstrated across geographic regions and institutions, suggesting that the surgical rates could be driven by factors external to patient injury characteristics alone. The limitations of the TBIMS database include a lack of preinjury antithrombotic use, concomitant medical comorbidities, and additional radiographic information such as the presence of chronic subdural hematoma. These limitations in trauma databases are well-known and have
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CRANIECTOMY AND CRANIOTOMY IN TBI
prompted collaborative improvement efforts in forums such as the American College of Surgeons Trauma Quality Improvement Program.48 The TBIMS variable for elevated ICP does not provide detailed information about when the ICP elevations occurred or how long the ICP elevations were sustained. However, in the present study, ICP was used only for matching between the CE and CO participant groups and was not directly analyzed for its effects on outcome. In addition, the TBIMS variable for CO versus CE does not provide additional surgical details, including the size and type of CE performed. The rehospitalization data did not provide granularity for the rehospitalization diagnosis beyond the categories listed in Table 2. For example, increased infections in the CE group might or might not have been related to the cranioplasty procedure. However, infections unrelated to cranioplasty have also been associated with worse outcomes in patients with TBI.26,49,50 We used several functional outcome measures in the present study to overcome the limitations of the GOSE. However, standardized scales such as the FIM score have known ceiling effects among individuals with TBI, especially at long-term follow-up and might not be sufficiently sensitive to changes at the upper end of the scale over time.51 We were able to describe TBI subtypes; however,
2. Kolias AG, Hutchinson PJ, Menon DK, Manley GT, Gallagher CN, Servadei F. Decompressive craniectomy for acute subdural hematomas. J Neurosurg. 2014;120:1247-1249 [author reply: 1249]. 3. Rush B, Rousseau J, Sekhon MS, Griesdale DE. Craniotomy versus craniectomy for acute traumatic subdural hematoma in the united states: a national retrospective cohort analysis. World Neurosurg. 2016;88:25-31. 4. Kolias AG, Li LM, Guilfoyle MR, Timofeey I, Corteen EA, Pickard JD, et al. Decompressive craniectomy for acute subdural hematomas: time for a randomized trial. Acta Neurochir (Wien). 2013; 155:187-188. 5. Hartings JA, Vidgeon S, Strong AJ, Zacko C, Vagal A, Andaluz N, et al. Surgical management of traumatic brain injury: a comparativeeffectiveness study of 2 centers. J Neurosurg. 2014; 120:434-446. 6. Aarabi B, Hesdorffer DC, Ahn ES, Aresco C, Scalea TM, Eisenberg HM. Outcome following decompressive craniectomy for malignant swelling due to severe head injury. J Neurosurg. 2006;104:469-479. 7. Aarabi B, Chesler D, Maulucci C, Blacklock T, Alexander M. Dynamics of subdural hygroma following decompressive craniectomy: a comparative study. Neurosurg Focus. 2009;26:E8. 8. De Bonis P, Pompucci A, Mangiola A, Rigante L, Anile C. Post-traumatic hydrocephalus after
CONCLUSION The individuals who underwent CE compared with CO after TBI required a longer LOS in the hospital and acute rehabilitation and experienced decreased functional status and more rehospitalizations. Survival at 2 years and the Satisfaction with Life scores remained similar. In our study, CE for moderate to severe TBI was associated with worse functional outcomes. ACKNOWLEDGMENTS The TBIMS national database is a multicenter study of the TBIMS Centers Program and is supported by the National Institute on Disability, Independent Living, and Rehabilitation Research, a center within the Administration for Community Living, Department of Health and Human Services. However, the contents do not necessarily reflect the opinions or views of the TBIMS Centers, National Institute on Disability, Independent Living, and Rehabilitation Research, Administration for Community Living, or Department of Health and Human Services.
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19. Li LM, Kolias AG, Guilfoyle MR, Timofeev I, Corteen EA, Pickard JD, et al. Outcome following evacuation of acute subdural haematomas: a comparison of craniotomy with decompressive craniectomy. Acta Neurochir (Wien). 2012;154: 1555-1561.
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Conflict of interest statement: This work was supported in part by the National Institute on Disability, Independent Living, and Rehabilitation Research (grant 90DP0041 to A.K.W.). A portion of this work was presented at the 2016 Congress of Neurological Surgeons Annual Meeting. Received 31 May 2018; accepted 13 July 2018 Citation: World Neurosurg. (2018). https://doi.org/10.1016/j.wneu.2018.07.124 Journal homepage: www.WORLDNEUROSURGERY.org
45. Kelly ML. Intensive care unit guideline adherence and severe traumatic brain injury: the challenge of comprehensive neurotrauma care worldwide. World Neurosurg. 2016;90:659-660.
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