Clinical Neurology and Neurosurgery 115 (2013) 2482–2488
Contents lists available at ScienceDirect
Clinical Neurology and Neurosurgery journal homepage: www.elsevier.com/locate/clineuro
Long-term neurological and neuropsychological outcome in patients with severe traumatic brain injury Oliver P. Gautschi a,b,∗,1 , Mélanie C. Huser a,1 , Nicolas R. Smoll b , Sven Maedler c , Stephan Bednarz c , Alexander von Hessling d , Roger Lussmann c , Gerhard Hildebrandt a , Martin A. Seule a a
Department of Neurosurgery, Kantonsspital, St.Gallen, Switzerland Department of Neurosurgery and Faculty of Medicine, University Hospital, Geneva, Switzerland c Surgical Intensive Care Unit, Kantonsspital, St.Gallen, Switzerland d Department of Neuroradiology, Kantonsspital, St.Gallen, Switzerland b
a r t i c l e
i n f o
Article history: Received 21 May 2013 Received in revised form 8 September 2013 Accepted 29 September 2013 Available online 12 October 2013 Keywords: Traumatic brain injury ICP-targeted therapy Neuropsychological outcome Glasgow Outcome Scale Long-term outcome
a b s t r a c t Background: Severe traumatic brain injury (TBI) remains a major cause of death and disability worldwide. The aim of the study was to evaluate predictors for neurological and neuropsychological long-term outcome in patients with severe TBI treated according to an intracranial pressure (ICP-) targeted therapy. Methods: From 08/2005 to 12/2008, 46 patients with severe TBI and more than 12 h of intensive care treatment were included in this study. Neurological outcome was assessed with the Glasgow Outcome Scale (GOS). Neuropsychological performance assessing 9 different domains was evaluated at longterm follow-up (median 20.5 months; range 10–46). Logistic regression was used to identify favourable outcomes according to the GOS and Fisher’s exact tests were used to identify predictors of severe neuropsychological impairments at follow-up. Results: Twenty-nine patients were available for neuropsychological assessment at long-term followup. Only 2 out of 29 patients presented normal or average neuropsychological findings throughout all 9 neuropsychological domains at long-term follow-up. The percentage of a favourable outcome (GOS 4-5) increased from 13.8% at hospital discharge to 75.8% at rehabilitation discharge to 79.3% at longterm follow-up, respectively. Age ≤40 was found to be a strong predictor of favourable outcome at follow-up (OR 5.95, 95% CI 1.41 25.00, p = 0.015). The GOS at hospital discharge was not a predictor for severe impairments in any of the 9 different neuropsychological domains (all p-values were p > 0.268). In contrast, the GOS at rehabilitation discharge was found to be a predictor of severe impairments at follow-up in all but one domain assessed (all p-values less than p < 0.038). Conclusions: The GOS at rehabilitation discharge should be regarded as a better predictor for neuropsychological impairments at long-term follow-up than the GOS at hospital discharge. Even in patients with favourable GOS after finishing a course of rehabilitation, three quarters of these patients may have at least one severe neuropsychological deficit. Therefore, it remains of paramount importance to provide long-term neuropsychological support to further improve outcome after TBI. © 2013 Elsevier B.V. All rights reserved.
1. Introduction Traumatic brain injuries (TBI) remain a major cause of death and disability worldwide, particularly among young people,
∗ Corresponding author at: Département de Neurosciences cliniques, Service de Neurochirurgie, Hôpitaux Universitaires de Genève, Rue Gabrielle-Perret-Gentil 4, 1211 Genève 14, Switzerland. Tel.: +41 79 55 33 777; fax: +41 22 372 82 25. E-mail addresses: [email protected], [email protected] (O.P. Gautschi). 1 These authors have both equally contributed to the study and should both be regarded as first authors. 0303-8467/$ – see front matter © 2013 Elsevier B.V. All rights reserved. http://dx.doi.org/10.1016/j.clineuro.2013.09.038
therefore generating a dramatic impact on the general population [1,2]. Severe TBI, defined as Glasgow Coma Scale (GCS) ≤ 8, is associated with mortality rates between 35% and 40% and severe disability in nearly one third of the survivors [3,4]. Two different main concepts for the treatment of severe TBI have been established in the past. The conventional cerebral perfusion pressure (CPP)-targeted therapy is recommended in well-established United States (US) and European guidelines, and may be characterized by the maintenance of relatively high CPP using vasopressors and volume expansion [5,6]. On the other hand, the intracranial pressure (ICP)-targeted therapy based on the Lund concept aims to control ICP by reducing transcapillary fluid filtration through a disrupted
O.P. Gautschi et al. / Clinical Neurology and Neurosurgery 115 (2013) 2482–2488
blood brain barrier and avoiding passive increases in blood vessel diameter with the loss of vascular autoregulation [7]. Outcome studies using the ICP-targeted therapy based on the Lund concept have shown mortality rates around 10–15% and favourable outcomes (Glasgow Outcome Scale (GOS) score 4–5) in the range of 60–70% after severe TBI [8–11]. Nevertheless, recent evidence suggests that many patients with TBI have long-term cognitive and psychosocial adjustment difficulties [12–18]. Additionally, neurological outcome assessed by the GOS may not account for subjective domains such as effects on work roles and responsibilities. Different prognostic models have been suggested in the past in order to predict the outcome after moderate or severe TBI. Two models, which were externally validated, have been developed with data from the Corticoid Randomisation After Significant Head Injury (CRASH) and the International Mission on Prognosis and Analysis of Clinical Trials (IMPACT) [19–21]. The key predictors in all models comprise mostly age, GCS motor score, and pupillary reactivity. These models were developed to predict early mortality as well as death and severe disability 6 months after TBI. However, they were not developed to predict long-term functional or neuropsychological outcome. The specific aim of this study was to evaluate predictors of neurological and neuropsychological long-term outcome for patients treated according to the ICP-targeted therapy. 2. Patients and methods The Department of Neurosurgery at the Kantonsspital St.Gallen is responsible for all patients older than 12 years of age with severe TBI in the eastern part of Switzerland, and serves a population of about 680,000 inhabitants. From August 2005 to December 2008, a total of 59 consecutive patients with moderate and severe TBI were treated based on an ICP-targeted therapy according to the Lund concept [7]. Of these, 46 patients with severe TBI, defined as GCS ≤ 8 at time of intubation and sedation, requiring >24 h of intensive care treatment, were included in this study. Ten patients with an initial GCS ≥ 9 before intubation and sedation and 3 patients with a manifest brain stem herniation dying within 12 h after hospital admission were not included. An inclusion criterion was the ability to speak and understand sufficiently the German language. 2.1. Outcome measurements Neurological outcome was assessed in all patients at three different time-points using the GOS (Score 1–5): (1) at hospital discharge, (2) at rehabilitation discharge, and (3) at long-term follow-up. Thereby, GOS 1 was denominated death, GOS 2 vegetative state, GOS 3 severe disability, GOS 4 moderate disability, and GOS 5 mild or no disability [22]. Per protocol, an unfavourable outcome was defined as GOS 1–3 (except for the evaluation of neuropsychological predictors of outcome where the GOS 1 category was dropped) and a favourable outcome as GOS 4–5. Based on recommendations of the American Brain Injury Consortium [23], neuropsychological evaluation was performed by a single investigator (M.C.H.) at long-term follow-up, which was performed in 36 of 37 survivors (97.3%) with one patient lost of followup. Of these, 29 patients were evaluated in our outpatient clinic and seven patients by a structured telephone interview using a validated questionnaire [24]. These seven patients were not available for an outpatient appointment, but did agree to undergo a structured telephone interview. The test battery addressed executive functions [25,26], attention and concentration [26], memory function [27], as well as visuoconstruction and visuomotor coordination (Table 1) [28]. More specifically, the Regensburger word fluency test (animals) was used to assess semantical word-fluency,
2483
Table 1 Neuropsychological tests. Domain assessed
Neuropsychological test
Semantical word-fluency Lexical word-fluency Cognitive flexibility Focused attention Sustained attention and concentration Verbal episodic memory
Regensburger word fluency test (animals) Regensburger word fluency test (s-words) Trail-Making Test Part B Trail-Making Test Part A Digit-Symbol-Test (Wechsler Adult Intelligence Scale) Logical Memory I – Text reproduction (Wechsler Memory Scales-R) Rey–Osterrieth complex figure test delayed recall (ROCF) Rey figure Grooved Pegboard
Visual episodic memory Visuoconstructive ability Visuomotoric coordination
the Regensburger word fluency test (s-words) to assess lexical word-fluency [26], the Trail-Making Test Part B to assess cognitive flexibility, the Trail-Making Test Part A to assess focused attention [29–31], the Digit-Symbol-Test (Wechsler Adult Intelligence Scale) to assess sustained attention and concentration [32,33], the Logical Memory I – test reproduction (Wechsler Memory ScalesR) to assess verbal episodic memory [34,35], the Rey–Osterrieth complex figure test delayed recall (ROCF) to assess visual episodic memory, the Rey Figure test to assess visuoconstructive ability, and the Grooved Pegboard test to assess visuomotor coordination, respectively. The performances on the neuropsychological tests were analysed by z-scores and thereafter classified into category 1: Average or superior (score > −1.0 standard deviation (SD) and accordingly z-values > −1 and T-values > 40); category 2: Mild to mid-severe impairment (−2.0 SD ≤ score ≥ −1.0 SD and accordingly z-values between −2.0 and −1.0 and T-values between 30 and 40); and category 3: Severe impairment (score < −2.0 SD and accordingly z-values < −2.0 and T-values ≤ 29) (Table 2). For further analysis, the neuropsychological test results from each domain were dichotomized into severe impairments (z < −2.0) and nonsevere impairments (z ≥ −2.0). Additionally, the work status was evaluated through an interview at long-term follow-up. 2.2. Statistical methods Data are presented as medians and range, respectively means and SD, where appropriate. Comparison of categorical variables was done using Fisher’s exact tests. Univariate and multivariate logistic regression models were used to assess relationships between baseline characteristics and GOS at follow-up. At this stage of the analysis, a p-value of 0.268) (Table 5). In contrast, the GOS at rehabilitation discharge was found to be a predictor of severe impairments at follow-up in all but one domain assessed (all p-values less than p < 0.038). A thorough analysis of the neuropsychological assessment at long-term follow-up categorized into average or superior, mild to moderate, or severe neuropsychological impairment is depicted in Table 2. The only neuropsychological domain where the GOS at rehabilitation discharge was not a predictor of severe impairments at follow-up was the semantical word-fluency assessed by the Regensburger word fluency test (animals). Respecting a level of significance of p < 0.005 in order to minimize type I error still revealed that the lexical word-fluency, cognitive flexibility, focused attention, sustained attention and concentration, verbal episodic memory, and visuomotor coordination, including tests from all four different domains executive function, attention and concentration, memory function, and visuoconstruction and motoric function, were predictors of severe neuropsychological impairments at longterm follow-up (p < 0.008). The following characteristics were not predictors of severe neuropsychological impairments at long-term follow-up (p > 0.114): age, gender, GCS, AIS head score, ISS score, presence of polytrauma, performed neurosurgical intervention, secondary DC, craniotomy with evacuation of a mass lesion, primary DCHC with evacuation of a mass lesion, and insertion of a VP-shunt. However, the presence of a primary DC trended to be significant to predict severe impairments in the cognitive flexibility and focused attention (p = 0.017). 3.4. Long-term outcome: functional and work status Work status at time of long-term follow-up was available in 32 of 36 patients (88.9%). Of these, 28 patients (87.5%) lived in private households and 22 patients (68.8%) received financial aid to some degree. Eighteen patients (56.3%) were able to resume work, of which 9 returned to their pre-traumatic employment and 9 had a voluntary or involuntary job change. Ten patients were able to work full time, whereby 8 had a reduced work quota. None of the 5 patients who had severe impairments throughout all neuropsychological domains assessed at follow-up were able to resume work, whereas both patients with good or average performance throughout all 9 neuropsychological domains resumed work. One patient returned to his pretraumatic employment and the other resumed another work with a reduced work quota of 20%. The median GOS (range) from all 18 patients who were able to resume work was 3 (2–4) at hospital discharge, 4 (4–5) at rehabilitation discharge, and 5 (4–5) at follow-up. Three patients with a hospital
discharge GOS of 2 were able to resume work, whereby one patient could resume in a reduced work quota of 80% his pretraumatic employment, and the other 2 patients a new employment with a work quota of 100% and 80%, respectively. All these 3 patients improved to a GOS of 4 at rehabilitation discharge.
3.5. Long-term outcome: physical complaints The most common physical complaints were sense of balance problems (n = 13, 40.6%) and headaches (n = 8, 25.0%). Patients emphasized the mental distress due to neuropsychological restrictions such as diminished concentration (n = 14, 43.8%) as well as verbal expression and comprehension deficits. Seven patients (21.9%) were taking anti-seizure medication and five were receiving antidepressants (15.6%).
4. Discussion The GOS at hospital discharge was not a predictor for severe impairments in all 9 neuropsychological domains assessed at longterm follow-up. However, the GOS at rehabilitation discharge was predictive to show severe impairments at follow-up in a total of 6 out of 9 neuropsychological domains. Our data suggest that the GOS is best measured at rehabilitation discharge, as this will best predict long-term neuropsychological deficits. Despite a favourable long-term functional outcome at follow-up in two thirds of the patients after severe TBI, severe neuropsychological impairment was present in 20.7–44.8% of the patients (depending on the according domain assessed), and only half of all patients were able to return to work. These findings show that results from specific neuropsychological tests do not necessarily correlate with functional outcome. Clifton et al. studied the relationship of 19 neuropsychological tests with 110 severely brain injured patients to the GOS at 3 and 6 months [39]. They found a close relationship to the GOS for four tests, namely the Controlled Oral Word Association, Grooved Pegboard, Trailmaking Part B, and Rey–Osterrieth complex figure delayed recall. At long-term follow-up, we could reproduce this finding between the association of the GOS and neuropsychological test results. All 9 neuropsychological domains tested, including Grooved Pegboard, Trailmaking Part B, and Rey–Osterrieth complex figure delayed recall test, showed a significant association with the GOS at follow-up (p < 0.018). The exact relationship between GOS scores and neuropsychological deficit remains to be further described. Satz et al. used discriminate validity analysis of the GOS at 6 months post injury in 100 patients with moderate to severe TBI [40]. The authors could show a systematic decrease in neuropsychological test performance as a function of decreasing GOS score as well as an increased prevalence of symptoms of depression and lower ratings on measures assessing employability and capacity for self care. Although the exact relationship between the neurological status after head injury (using the GOS) and neuropsychological status remains unclear, our results demonstrate that the GOS is most accurate at
2486
Table 5 Predictors of Neuropsychological outcome at long-term follow-up. Predictor
Executive function
Attention and concentration
Semantical word-fluency (1)
Lexical word-fluency (2)
Cognitive flexibility (3)
Memory function
Focused attention (4)
Visual episodic memory (7)
Verbal episodic memory (6)
Visuoconstructive ability (8)
Visuomotoric coordination (9)
Severe impairment
Non-severe impairment
Severe impairment
Non-severe impairment
Severe impairment
Non-severe impairment
Severe impairment
Non-severe impairment
Severe impairment
Non-severe impairment
Severe impairment
Non-severe impairment
Severe impairment
Non-severe impairment
Severe impairment
Non-severe impairment
Severe impairment
Non-severe impairment
GOS-HD; 2–3 GOS-HD; 4–5
11 (100) 0 (0.0)
14 (77.8) 4 (22.2)
9 (90.0) 1 (10.0)
16 (84.2) 3 (15.8)
8 (80.0) 2 (20.0)
17 (89.5) 2 (10.5)
8 (80.0) 2 (20.0)
17 (89.5) 2 (10.5)
6 (85.7) 1 (14.3)
19 (86.4) 3 (13.6)
12 (92.3) 1 (7.7)
12 (80.0) 3 (20.0)
6 (100) 0 (0.0)
19 (82.6) 4 (17.4)
6 (85.7) 1 (14.3)
19 (86.4) 3 (13.6)
7 (87.5) 1 (12.5)
18 (85.7) 3 (14.3)
GOS-RD; 2–3
4 (36.4)
3 (16.7)
6 (60.0)
1 (5.3)
6 (60.0)
1 (5.3)
6 (60.0)
1 (5.3)
5 (71.4)
2 (9.1)
7 (53.8)
0 (0.0)
4 (66.7)
3 (13.0)
4 (57.1)
3 (13.6)
5 (62.5)
2 (9.5)
GOS-RD; 4–5
7 (63.6)
15 (83.3)
4 (40.0)
18 (94.7)**
4 (40.0)
18 (94.7)**
4 (40.0)
18 (94.7)**
2 (28.6)
20 (90.9)**
6 (46.2)
15 (100)**
3 (33.3)
20 (87.0)*
3 (42.9)
19 (86.4)*
3 (37.5)
19 (90.5)**
Age; >40 Age; ≤40
5 (45.5) 6 (54.5)
5 (27.8) 13 (72.2)
5 (50.0) 5 (50.0)
5 (26.3) 14 (73.7)
4 (40.0) 6 (60.0)
6 (31.6) 13 (68.4)
4 (40.0) 6 (60.0)
6 (31.6) 13 (68.4)
4 (57.1) 3 (42.9)
6 (27.3) 16 (72.7)
7 (53.8) 6 (46.2)
3 (20.0) 12 (80.0)
3 (50.0) 3 (50.0)
7 (30.4) 16 (69.6)
4 (57.1) 3 (42.9)
6 (27.3) 16 (72.7)
4 (50.0) 4 (50.0)
6 (28.6) 15 (71.4)
Gender, female Gender, male
2 (18.2) 9 (81.8)
6 (33.3) 12 (66.7)
2 (20.0) 8 (80.0)
6 (31.6) 13 (68.4)
1 (10.0) 9 (90.0)
7 (36.8) 12 (63.2)
1 (10.0) 9 (90.0)
7 (36.8) 12 (63.2)
0 (0.0) 7 (100)
8 (36.4) 14 (63.6)
2 (15.4) 11 (84.6)
5 (33.3) 10 (66.7)
0 (0.0) 6 (100)
8 (34.8) 15 (65.2)
0 (0.0) 7 (100)
8 (36.4) 14 (63.6)
1 (12.5) 7 (87.5)
7 (33.3) 14 (66.7)
GCS, 4 AIS head, ≤4
3 (27.3) 8 (72.7)
3 (16.7) 15 (83.3)
3 (30.0) 7 (70.0)
3 (15.8) 16 (84.2)
3 (30.0) 7 (70.0)
3 (15.8) 16 (84.2)
3 (30.0) 7 (70.0)
3 (15.8) 16 (84.2)
2 (28.6) 5 (71.4)
4 (18.2) 18 (81.8)
3 (23.1) 10 (76.9)
3 (20.0) 12 (80.0)
2 (33.3) 4 (66.7)
4 (17.4) 19 (82.6)
1 (14.3) 6 (85.7)
5 (22.7) 17 (77.3)
2 (25.0) 6 (75.0)
4 (19.0) 17 (81.0)
ISS, >25 ISS, ≤25
8 (72.7) 3 (27.3)
10 (55.6) 8 (44.4)
6 (60.0) 4 (40.0)
12 (63.2) 7 (36.8)
5 (50.0) 5 (50.0)
13 (68.4) 6 (31.6)
5 (50.0) 5 (50.0)
13 (68.4) 6 (31.6)
4 (57.1) 3 (42.9)
14 (63.6) 8 (36.4)
8 (61.5) 5 (38.5)
10 (66.7) 5 (33.3)
4 (66.7) 2 (33.3)
14 (60.9) 9 (39.1)
4 (57.1) 3 (42.9)
14 (63.6) 8 (36.4)
5 (62.5) 3 (37.5)
13 (61.9) 8 (38.1)
Polytrauma, yes Polytrauma, no
9 (81.8) 2 (18.2)
10 (55.6) 8 (44.4)
8 (80.0) 2 (20.0)
11 (57.9) 8 (42.1)
7 (70.0) 3 (30.0)
12 (63.2) 7 (36.8)
7 (70.0) 3 (30.0)
12 (63.2) 7 (36.8)
5 (71.4) 2 (28.6)
14 (63.6) 8 (36.4)
11 (84.6) 2 (15.4)
8 (53.3) 7 (46.7)
5 (83.3) 1 (16.7)
14 (60.9) 9 (39.1)
5 (71.4) 2 (28.6)
14 (63.6) 8 (36.4)
6 (75.0) 2 (25.0)
13 (61.9) 8 (38.1)
Surgery, yes Surgery, no
8 (72.7) 3/27.3)
10 (55.6) 8 (44.4)
7 (70.0) 3 (30.0)
11 (57.9) 8 (42.1)
8 (80.0) 2 (20.0)
10 (52.6) 9 (47.4)
8 (80.0) 2 (20.0)
10 (52.6) 9 (47.4)
5 (71.4) 2 (28.6)
13 (59.1) 9 (40.9)
9 (69.2) 4 (30.8)
8 (53.3) 7 (46.7)
5 (83.3) 1 (16.7)
13 (56.5) 10 (43.5)
4 (57.1) 3 (42.9)
14 (63.6) 8 (36.4)
6 (75.0) 2 (25.0)
12 (57.1) 9 (42.9)
Primary DC, yes
5 (45.5)
6 (33.3)
5 (50.0)
6 (31.6)
7 (70.0)
4 (21.1)
7 (70.0)
4 (21.1)
4 (57.1)
7 (31.8)
6 (46.2)
5 (33.3)
4 (66.7)
7 (30.4)
4 (57.1)
7 (31.8)
5 (62.5)
6 (28.6)
Primary DC, no
6 (54.5)
12 (66.7)
5 (50.0)
13 (68.4)
3 (30.0)
15 (78.9)*
3 (30.0)
15 (78.9)*
3 (42.9)
15 (68.2)
7 (53.8)
10 (66.7)
2 (33.3)
16 (69.6)
3 (42.9)
15 (68.2)
3 (37.5)
15 (71.4)
Second. DC, yes Second. DC, no
3 (27.3) 8 (72.7)
4 (22.2) 14 (77.8)
3 (30.0) 7 (70.0)
4 (21.1) 15 (78.9)
2 (20.0) 8 (80.0)
5 (26.3) 14 (73.7)
2 (20.0) 8 (80.0)
5 (26.3) 14 (73.7)
1 (14.3) 6 (85.7)
6 (27.3) 16 (72.7)
3 (23.1) 10 (76.9)
3 (20.0) 12 (80.0)
1 (16.7) 5 (83.3)
6 (26.1) 17 (73.9)
0 (0.0) 7 (100)
7 (31.8) 15 (68.2)
2 (25.0) 6 (75.0)
5 (23.8) 16 (76.2)
Craniot. evac. (y) Mass lesion (n)
3 (27.3) 8 (72.7)
4 (22.2) 14 (77.8)
2 (20.0) 8 (80.0)
5 (26.3) 14 (73.7)
1 (10.0) 9 (90.0)
6 (31.6) 13 (68.4)
1 (10.0) 9 (90.0)
6 (31.6) 13 (68.4)
1 (14.3) 6 (85.7)
6 (27.3) 16 (72.7)
3 (23.1) 10 (76.9)
3 (20.0) 12 (80.0)
1 (16.7) 5 (83.3)
6 (26.1) 17 (73.9)
0 (0.0) 7 (100)
7 (31.8) 15 (68.2)
1 (12.5) 7 (87.5)
6 (28.6) 15 (71.4)
PrimaryDCHC (y) w Mass lesion (n)
3 (27.3) 8 (72.7)
5 (27.8) 13 (72.2)
2 (20.0) 8 (80.0)
6 (31.6) 13 (68.4)
4 (40.0) 6 (60.0)
4 (21.1) 15 (78.9)
4 (40.0) 6 (60.0)
4 (21.1) 15 (78.9)
2 (28.6) 5 (71.4)
6 (27.3) 16 (72.7)
3 (23.1) 10 (76.9)
5 (33.3) 10 (66.7)
2 (33.3) 4 (66.7)
6 (26.1) 17 (73.9)
2 (28.6) 5 (71.4)
6 (27.3) 16 (72.7)
2 (25.0) 6 (75.0)
6 (28.6) 15 (71.4)
VP shunt, yes VP shunt, no
4 (36.4) 7 (63.6)
3 (16.7) 15 (83.3)
3 (30.0) 7 (70.0)
4 (21.1) 15 (78.9)
4 (40.0) 6 (60.0)
3 (15.8) 16 (84.2)
4 (40.0) 6 (60.0)
3 (15.8) 16 (84.2)
2 (28.6) 5 (71.4)
5 (22.7) 17 (77.3)
4 (30.8) 9 (69.2)
3 (20.0) 12 (80.0)
2 (33.3) 4 (66.7)
5 (21.7) 18 (78.3)
2 (28.6) 5 (71.4)
5 (22.7) 17 (77.3)
3 (37.5) 5 (62.5)
4 (19.0) 17 (81.0)
GOS, Glasgow Outcome Scale; HD, hospital discharge; RD, rehabilitation discharge; GCS, Glasgow coma scale; AIS, abbreviated injury score; ISS, injury severity score; (y), yes; (n), no; PrimaryDCHC(y)w mass lesion, primary decompressive hemicraniectomy with evacuation of a mass lesion; VP, ventriculo-peritoneal. * p < 0.05; Fisher’s exact test. ** p < 0.005; Fisher’s exact test.
O.P. Gautschi et al. / Clinical Neurology and Neurosurgery 115 (2013) 2482–2488
Sustained attention and concentration (5)
Visuoconstruction and -motoric function
O.P. Gautschi et al. / Clinical Neurology and Neurosurgery 115 (2013) 2482–2488
predicting neuropsychological deficits after the rehabilitation process has been completed. Although the majority of patients with severe TBI in long-term outcome studies are presenting good physical recovery with independence in locomotion and basic life skills, neuropsychological sequelae are thought to create difficulty in social reintegration [12,14,15,17,18]. It was found that 2–5 years post TBI, physical abilities recover better than cognitive functions [13]. However, the temporal profile of recovery after severe TBI has not been investigated in depth so far. Our data showed that an overwhelming majority of patients experience a dramatic improvement from hospital discharge to time of follow-up. At long-term follow-up, over two thirds of patients presented with higher functional independence. In concordance with previous studies, many of our patients lost their pre-trauma level of employment or were not able to work full-time [13,14]. Return to work has been defined as an important external measurement of outcome, since it does not depend on subjective judgement, unlike the GOS. While cognitive changes after TBI can lead to social isolation and unemployment [41], the resulting situation may also aggravate cognitive and behavioural problems. Our data, presenting a return to work ratio of more than 50%, agrees with findings of other studies, where the return to work quota ranged from 23% to 72% one year post-discharge [42–45]. However, only half of all patients of our study groups who returned to work, returned to their pre-traumatic employment. A closer analysis of the course of the GOS from hospital to rehabilitation discharge to follow-up of all 18 patients who were able to return to work revealed a median score of 3, 4, and 5, respectively, indicating a steady improvement. Moreover, even 3 patients with a hospital discharge GOS of 2 resumed work at follow-up. All these 3 patients experienced a decisive amelioration to a GOS of 4 after rehabilitation. This fact not only stresses the importance of an adequate neurosurgical and intensive care treatment at the best, but also underlines the significance of an adequate rehabilitation to the earliest possible moment. Although an increasing percentage of patients after severe TBI may achieve a favourable outcome (GOS 4 and 5), cognitive, emotional, vocational, and social disturbances will always play a major role in the final disability of these patients [46]. Therefore, recovery assessment scales of functional, neuropsychological, and psychosocial domains are indispensable not only to guide the post-acute care and to provide information concerning long-term outcome to the next of kin, but also to compare the outcome of TBI cohorts undergoing different acute phase management and post-acute phase rehabilitation protocols [47,48]. Further prospective studies are needed in order to validate our findings and especially to elucidate which patients with severe brain injuries might profit the most from a neurorehabilitation programme to achieve a favourable functional and cognitive outcome. 5. Conclusions The GOS at rehabilitation discharge should be regarded as a better predictor for neuropsychological impairments at long-term follow-up than the GOS at hospital discharge. Even in patients with favourable GOS after finishing a course of rehabilitation, three quarters of these patients may have at least one severe neuropsychological deficit. Therefore, it remains of paramount importance to provide long-term neuropsychological support to further improve outcome after TBI. Conflict of interest The authors do not report any conflict of interest concerning this study or the findings specified in this paper.
2487
Acknowledgements The authors would like to thank all the participating patients for their valuable cooperation. Special thanks to Dr. phil. Erika Foster and Andrea Näpflin for their neuropsychological expertise and the rehabilitation clinics Zihlschlacht, Valens, Affoltern, Wald and Bellikon not only for their hard work with patients but also for their contribution to this study.
References [1] Leibson CL, Brown AW, Hall Long K, Ransom JE, Mandrekar J, Osler TM, et al. Medical care costs associated with traumatic brain injury over the full spectrum of disease: a controlled population-based study. Journal of Neurotrauma 2012;29(July 20 (11)):2038–49 [PubMed PMID: 22414023. Epub 2012/03/15. eng]. [2] Tagliaferri F, Compagnone C, Korsic M, Servadei F, Kraus J. A systematic review of brain injury epidemiology in Europe. Acta Neurochirurgica 2006;148(March (3)):255–68 [discussion 68. PubMed PMID: 16311842. Epub 2005/11/29. eng]. [3] Marshall LF, Gautille T. The outcome of severe closed head-injury. Journal of Neurosurgery 1991;75:S28–36. [4] Murray GD, Teasdale GM, Braakman R, Cohadon F, Dearden M, Iannotti F, et al. The European Brain Injury Consortium survey of head injuries. Acta Neurochirurgica 1999;141(3):223–36 [PubMed PMID: 10214478. Epub 1999/04/24. eng]. [5] Bullock R, Chesnut RM, Clifton G, Ghajar J, Marion DW, Narayan RK, et al. Guidelines for the management of severe head injury. Brain Trauma Foundation. European Journal of Emergency Medicine: Official Journal of the European Society for Emergency Medicine 1996;3(June (2)):109–27 [PubMed PMID: 9028756. Epub 1996/06/01. eng]. [6] Maas AI, Dearden M, Teasdale GM, Braakman R, Cohadon F, Iannotti F, et al. EBIC-guidelines for management of severe head injury in adults, European Brain Injury Consortium. Acta Neurochirurgica 1997;139(4):286–94 [PubMed PMID: 9202767. Epub 1997/01/01. eng]. [7] Grande PO. The “Lund Concept” for the treatment of severe head trauma – physiological principles and clinical application. Intensive Care Medicine 2006;32(October (10)):1475–84 [PubMed PMID: 16896859. Epub 2006/08/10. eng]. [8] Eker C, Asgeirsson B, Grande PO, Schalen W, Nordstrom CH. Improved outcome after severe head injury with a new therapy based on principles for brain volume regulation and preserved microcirculation. Critical Care Medicine 1998;26(November (11)):1881–6 [PubMed PMID: 9824083. Epub 1998/11/21. eng]. [9] Naredi S, Eden E, Zall S, Stephensen H, Rydenhag B. A standardized neurosurgical neurointensive therapy directed toward vasogenic edema after severe traumatic brain injury: clinical results. Intensive Care Medicine 1998;24(May (5)):446–51 [PubMed PMID: 9660259. Epub 1998/07/11. eng]. [10] Naredi S, Olivecrona M, Lindgren C, Ostlund AL, Grande PO, Koskinen LO. An outcome study of severe traumatic head injury using the “Lund therapy” with low-dose prostacyclin. Acta Anaesthesiologica Scandinavica 2001;45(April (4)):402–6 [PubMed PMID: 11300376. Epub 2001/04/13. eng]. [11] Olivecrona M, Rodling-Wahlstrom M, Naredi S, Koskinen LO. Effective ICP reduction by decompressive craniectomy in patients with severe traumatic brain injury treated by an ICP-targeted therapy. Journal of Neurotrauma 2007;24(June (6)):927–35 [PubMed PMID: 17600510. Epub 2007/06/30. eng]. [12] Colantonio A, Ratcliff G, Chase S, Kelsey S, Escobar M, Vernich L. Long-term outcomes after moderate to severe traumatic brain injury. Disability and Rehabilitation 2004;26(March 4 (5)):253–61 [PubMed PMID: 15200240. Epub 2004/06/18. eng]. [13] deGuise E, leBlanc J, Feyz M, Meyer K, Duplantie J, Thomas H, et al. Long-term outcome after severe traumatic brain injury: the McGill interdisciplinary prospective study. Journal of Head Trauma Rehabilitation 2008;23(September–October (5)):294–303 [PubMed PMID: 18815506. Epub 2008/09/26. eng]. [14] Dikmen SS, Machamer JE, Powell JM, Temkin NR. Outcome 3 to 5 years after moderate to severe traumatic brain injury. Archives of Physical Medicine and Rehabilitation 2003;84(October (10)):1449–57 [PubMed PMID: 14586911. Epub 2003/10/31. eng]. [15] Hoofien D, Gilboa A, Vakil E, Donovick PJ. Traumatic brain injury (TBI) 10-20 years later: a comprehensive outcome study of psychiatric symptomatology, cognitive abilities and psychosocial functioning. Brain Injury: [BI] 2001;15(March (3)):189–209 [PubMed PMID: 11260769. Epub 2001/03/22. eng]. [16] Novack TA, Bush BA, Meythaler JM, Canupp K. Outcome after traumatic brain injury: pathway analysis of contributions from premorbid, injury severity, and recovery variables. Archives of Physical Medicine and Rehabilitation 2001;82(March (3)):300–5 [PubMed PMID: 11245749. Epub 2001/03/14. eng]. [17] Ratcliff G, Colantonio A, Escobar M, Chase S, Vernich L. Long-term survival following traumatic brain injury. Disability and Rehabilitation 2005;27(March 18 (6)):305–14 [PubMed PMID: 16040532. Epub 2005/07/26. eng]. [18] Wood RL, Rutterford NA. Psychosocial adjustment 17 years after severe brain injury. Journal of Neurology, Neurosurgery, and Psychiatry 2006;77(January
2488
[19]
[20]
[21]
[22]
[23]
[24]
[25] [26] [27] [28]
[29]
[30] [31] [32] [33] [34]
[35]
O.P. Gautschi et al. / Clinical Neurology and Neurosurgery 115 (2013) 2482–2488
(1)):71–3 [PubMed PMID: 16361596. Pubmed Central PMCID: 2117407. Epub 2005/12/20. eng]. Perel P, Arango M, Clayton T, Edwards P, Komolafe E, Poccock S, et al. Predicting outcome after traumatic brain injury: practical prognostic models based on large cohort of international patients. British Medical Journal 2008;336(February 23 (7641)):425–9 [PubMed PMID: 18270239. Pubmed Central PMCID: 2249681. Epub 2008/02/14. eng]. Roozenbeek B, Lingsma HF, Lecky FE, Lu J, Weir J, Butcher I, et al. Prediction of outcome after moderate and severe traumatic brain injury: external validation of the International Mission on Prognosis and Analysis of Clinical Trials (IMPACT) and Corticoid Randomisation After Significant Head injury (CRASH) prognostic models. Critical Care Medicine 2012;40(May (5)):1609–17 [PubMed PMID: 22511138. Pubmed Central PMCID: 3335746. Epub 2012/04/19. eng]. Steyerberg EW, Mushkudiani N, Perel P, Butcher I, Lu J, McHugh GS, et al. Predicting outcome after traumatic brain injury: development and international validation of prognostic scores based on admission characteristics. PLoS Medicine 2008;5(August 5 (8)):e165 [discussion e. PubMed PMID: 18684008. Pubmed Central PMCID: 2494563. Epub 2008/08/08. eng]. Jennett B, Snoek J, Bond MR, Brooks N. Disability after severe head injury: observations on the use of the Glasgow Outcome Scale. Journal of Neurology, Neurosurgery, and Psychiatry 1981;44(April (4)):285–93 [PubMed PMID: 6453957. Pubmed Central PMCID: 490949. Epub 1981/04/01. eng]. Bullock MR, Merchant RE, Choi SC, Gilman CB, Kreutzer JS, Marmarou A, et al. Outcome measures for clinical trials in neurotrauma. Neurosurgical Focus 2002;13(July 15 (1)):ECP1 [PubMed PMID: 15916412. Epub 2005/05/27. eng]. Wilson JT, Pettigrew LE, Teasdale GM. Structured interviews for the Glasgow Outcome Scale and the extended Glasgow Outcome Scale: guidelines for their use. Journal of Neurotrauma 1998;15(August (8)):573–85 [PubMed PMID: 9726257. Epub 1998/09/03. eng]. Aschenbrenner ST, Lange KW. Regensburger Wortflüssigkeits-test (RWT). Hogrefe: Göttingen; 2000. Lezak M. Neuropsychological assessment. 3rd ed. Oxford University Press; 1995. Rey A. Léxamen psychologique dans le cas d’encéphalopathie traumatique. Archives of Psychology 1941;28:286–340. Ruff RM, Parker SB. Gender-age-specific changes in motor speed eye-hand coordination in adults: normative values for the Finger Tapping Grooved Pegboard Tests. Perceptual Motor Skills 1993;76(June (3 Pt 2)):1219–30 [PubMed PMID:, 8337069. Epub 1993/06/01. eng]. Merten T, Green P, Henry M, Blaskewitz N, Brockhaus R. Analog validation of German-language symptom validity tests and the influence of coaching. Archives of Clinical Neuropsychology: The Official Journal of the National Academy of Neuropsychologists 2005;20(August (6)):719–26 [PubMed PMID: 16005815]. Reitan RM. Validity of the trail making test as an indicator of organic brain damage. Perceptual and Motor Skills 1958;8:271–6. Reitan RM. Trail making test. Manual for administration and scoring. South Tucson, AZ: Reitan Neuropsychology Laboratory; 1992. Aster M, Neubauer A, Horn R. Wechsler-Intelligenztest für Erwachsene WIEmanual. Frankfurt: Harcourt Test Services; 2006. Petermann F, Lepach A. Wechsler memory scale – fourth edition, German edition. Manual. Frankfurt: Pearson Assessment; 2012. Härting C, Markowitsch HJ, Neufeld H, Calabrese P, Deisinger P, Kessler J. Wechsler Gedächtnistest-Revidierte Fassung Deutsche Adaptation der revidierten Fassung der Wechsler memory scale. Bern, Switzerland: Huber; 2000. Wechsler D. WMS-R: Wechsler memory scale-revised. San Antonio: The Psychological Corporation; 1987.
[36] Baker SP, O’Neill B, Haddon Jr W, Long WB. The injury severity score: a method for describing patients with multiple injuries and evaluating emergency care. Journal of Trauma 1974;14(March (3)):187–96 [PubMed PMID: 4814394. Epub 1974/03/01. eng]. [37] Civil ID, Schwab CW. The abbreviated injury scale, 1985 revision: a condensed chart for clinical use. Journal of Trauma 1988;28(January (1)):87–90 [PubMed PMID: 3339667. Epub 1988/01/01. eng]. [38] Marshall LF, Marshall SB, Klauber MR, Van Berkum Clark M, Eisenberg H, Jane JA, et al. The diagnosis of head injury requires a classification based on computed axial tomography. Journal of Neurotrauma 1992;1(March (9 Suppl)):S287–92 [PubMed PMID: 1588618. Epub 1992/03/01. eng]. [39] Clifton GL, Kreutzer JS, Choi SC, Devany CW, Eisenberg HM, Foulkes MA, et al. Relationship between Glasgow Outcome Scale and neuropsychological measures after brain injury. Neurosurgery 1993;33(July (1)):34–8 [discussion 8-9. PubMed PMID: 8355845. Epub 1993/07/01. eng]. [40] Satz P, Zaucha K, Forney DL, McCleary C, Asarnow RF, Light R, et al. Neuropsychological, psychosocial and vocational correlates of the Glasgow Outcome Scale at 6 months post-injury: a study of moderate to severe traumatic brain injury patients. Brain injury: [BI] 1998;12(July (7)):555–67 [PubMed PMID: 9653519. Epub 1998/07/08. eng]. [41] Draper K, Ponsford J, Schonberger M. Psychosocial and emotional outcomes 10 years following traumatic brain injury. Journal of Head Trauma Rehabilitation 2007;22(September–October (5)):278–87 [PubMed PMID: 17878769. Epub 2007/09/20. eng]. [42] Annoni JM, Beer S, Kesselring J. [Sequelae of severe craniocerebral injuries, An epidemiological study in the Canton of St. Gallen]. Schweizerische Medizinische Wochenschrift 1991;121(February 16 (7)):207–13 [PubMed PMID: 1901176. Epub 1991/02/16. Folgen des schweren Schadel-Hirn-Traumas. Eine epidemiologische Studie im Kanton St. Gallen. ger.]. [43] Benedictus MR, Spikman JM, van der Naalt J. Cognitive and behavioral impairment in traumatic brain injury related to outcome and return to work. Archives of Physical Medicine and Rehabilitation 2010;91(September (9)):1436–41 [PubMed PMID: 20801264. Epub 2010/08/31. eng]. [44] Green RE, Colella B, Hebert DA, Bayley M, Kang HS, Till C, et al. Prediction of return to productivity after severe traumatic brain injury: investigations of optimal neuropsychological tests and timing of assessment. Archives of Physical Medicine and Rehabilitation 2008;89(December (12 Suppl)):S51–60 [PubMed PMID: 19081442. Epub 2008/12/23. eng]. [45] Schonberger M, Ponsford J, Olver J, Ponsford M, Wirtz M. Prediction of functional and employment outcome 1 year after traumatic brain injury: a structural equation modelling approach. Journal of Neurology, Neurosurgery, and Psychiatry 2011;82(August (8)):936–41 [PubMed PMID: 21217165. Epub 2011/01/11. eng.]. [46] Formisano R, Carlesimo GA, Sabbadini M, Loasses A, Penta F, Vinicola V, et al. Clinical predictors and neuropsychological outcome in severe traumatic brain injury patients. Acta Neurochirurgica 2004;146(May (5)):457–62 [PubMed PMID: 15118882. Epub 2004/05/01. eng]. [47] Hudak AM, Caesar RR, Frol AB, Krueger K, Harper CR, Temkin NR, et al. Functional outcome scales in traumatic brain injury: a comparison of the Glasgow Outcome Scale (Extended) and the Functional Status Examination. Journal of Neurotrauma 2005;22(November (11)):1319–26 [PubMed PMID: 16305320. Epub 2005/11/25. eng]. [48] Nichol AD, Higgins AM, Gabbe BJ, Murray LJ, Cooper DJ, Cameron PA. Measuring functional and quality of life outcomes following major head injury: common scales and checklists. Injury 2011;42(March (3)):281–7 [PubMed PMID: 21145059. Epub 2010/12/15. eng].
Contents lists available at ScienceDirect
Clinical Neurology and Neurosurgery journal homepage: www.elsevier.com/locate/clineuro
Long-term neurological and neuropsychological outcome in patients with severe traumatic brain injury Oliver P. Gautschi a,b,∗,1 , Mélanie C. Huser a,1 , Nicolas R. Smoll b , Sven Maedler c , Stephan Bednarz c , Alexander von Hessling d , Roger Lussmann c , Gerhard Hildebrandt a , Martin A. Seule a a
Department of Neurosurgery, Kantonsspital, St.Gallen, Switzerland Department of Neurosurgery and Faculty of Medicine, University Hospital, Geneva, Switzerland c Surgical Intensive Care Unit, Kantonsspital, St.Gallen, Switzerland d Department of Neuroradiology, Kantonsspital, St.Gallen, Switzerland b
a r t i c l e
i n f o
Article history: Received 21 May 2013 Received in revised form 8 September 2013 Accepted 29 September 2013 Available online 12 October 2013 Keywords: Traumatic brain injury ICP-targeted therapy Neuropsychological outcome Glasgow Outcome Scale Long-term outcome
a b s t r a c t Background: Severe traumatic brain injury (TBI) remains a major cause of death and disability worldwide. The aim of the study was to evaluate predictors for neurological and neuropsychological long-term outcome in patients with severe TBI treated according to an intracranial pressure (ICP-) targeted therapy. Methods: From 08/2005 to 12/2008, 46 patients with severe TBI and more than 12 h of intensive care treatment were included in this study. Neurological outcome was assessed with the Glasgow Outcome Scale (GOS). Neuropsychological performance assessing 9 different domains was evaluated at longterm follow-up (median 20.5 months; range 10–46). Logistic regression was used to identify favourable outcomes according to the GOS and Fisher’s exact tests were used to identify predictors of severe neuropsychological impairments at follow-up. Results: Twenty-nine patients were available for neuropsychological assessment at long-term followup. Only 2 out of 29 patients presented normal or average neuropsychological findings throughout all 9 neuropsychological domains at long-term follow-up. The percentage of a favourable outcome (GOS 4-5) increased from 13.8% at hospital discharge to 75.8% at rehabilitation discharge to 79.3% at longterm follow-up, respectively. Age ≤40 was found to be a strong predictor of favourable outcome at follow-up (OR 5.95, 95% CI 1.41 25.00, p = 0.015). The GOS at hospital discharge was not a predictor for severe impairments in any of the 9 different neuropsychological domains (all p-values were p > 0.268). In contrast, the GOS at rehabilitation discharge was found to be a predictor of severe impairments at follow-up in all but one domain assessed (all p-values less than p < 0.038). Conclusions: The GOS at rehabilitation discharge should be regarded as a better predictor for neuropsychological impairments at long-term follow-up than the GOS at hospital discharge. Even in patients with favourable GOS after finishing a course of rehabilitation, three quarters of these patients may have at least one severe neuropsychological deficit. Therefore, it remains of paramount importance to provide long-term neuropsychological support to further improve outcome after TBI. © 2013 Elsevier B.V. All rights reserved.
1. Introduction Traumatic brain injuries (TBI) remain a major cause of death and disability worldwide, particularly among young people,
∗ Corresponding author at: Département de Neurosciences cliniques, Service de Neurochirurgie, Hôpitaux Universitaires de Genève, Rue Gabrielle-Perret-Gentil 4, 1211 Genève 14, Switzerland. Tel.: +41 79 55 33 777; fax: +41 22 372 82 25. E-mail addresses: [email protected], [email protected] (O.P. Gautschi). 1 These authors have both equally contributed to the study and should both be regarded as first authors. 0303-8467/$ – see front matter © 2013 Elsevier B.V. All rights reserved. http://dx.doi.org/10.1016/j.clineuro.2013.09.038
therefore generating a dramatic impact on the general population [1,2]. Severe TBI, defined as Glasgow Coma Scale (GCS) ≤ 8, is associated with mortality rates between 35% and 40% and severe disability in nearly one third of the survivors [3,4]. Two different main concepts for the treatment of severe TBI have been established in the past. The conventional cerebral perfusion pressure (CPP)-targeted therapy is recommended in well-established United States (US) and European guidelines, and may be characterized by the maintenance of relatively high CPP using vasopressors and volume expansion [5,6]. On the other hand, the intracranial pressure (ICP)-targeted therapy based on the Lund concept aims to control ICP by reducing transcapillary fluid filtration through a disrupted
O.P. Gautschi et al. / Clinical Neurology and Neurosurgery 115 (2013) 2482–2488
blood brain barrier and avoiding passive increases in blood vessel diameter with the loss of vascular autoregulation [7]. Outcome studies using the ICP-targeted therapy based on the Lund concept have shown mortality rates around 10–15% and favourable outcomes (Glasgow Outcome Scale (GOS) score 4–5) in the range of 60–70% after severe TBI [8–11]. Nevertheless, recent evidence suggests that many patients with TBI have long-term cognitive and psychosocial adjustment difficulties [12–18]. Additionally, neurological outcome assessed by the GOS may not account for subjective domains such as effects on work roles and responsibilities. Different prognostic models have been suggested in the past in order to predict the outcome after moderate or severe TBI. Two models, which were externally validated, have been developed with data from the Corticoid Randomisation After Significant Head Injury (CRASH) and the International Mission on Prognosis and Analysis of Clinical Trials (IMPACT) [19–21]. The key predictors in all models comprise mostly age, GCS motor score, and pupillary reactivity. These models were developed to predict early mortality as well as death and severe disability 6 months after TBI. However, they were not developed to predict long-term functional or neuropsychological outcome. The specific aim of this study was to evaluate predictors of neurological and neuropsychological long-term outcome for patients treated according to the ICP-targeted therapy. 2. Patients and methods The Department of Neurosurgery at the Kantonsspital St.Gallen is responsible for all patients older than 12 years of age with severe TBI in the eastern part of Switzerland, and serves a population of about 680,000 inhabitants. From August 2005 to December 2008, a total of 59 consecutive patients with moderate and severe TBI were treated based on an ICP-targeted therapy according to the Lund concept [7]. Of these, 46 patients with severe TBI, defined as GCS ≤ 8 at time of intubation and sedation, requiring >24 h of intensive care treatment, were included in this study. Ten patients with an initial GCS ≥ 9 before intubation and sedation and 3 patients with a manifest brain stem herniation dying within 12 h after hospital admission were not included. An inclusion criterion was the ability to speak and understand sufficiently the German language. 2.1. Outcome measurements Neurological outcome was assessed in all patients at three different time-points using the GOS (Score 1–5): (1) at hospital discharge, (2) at rehabilitation discharge, and (3) at long-term follow-up. Thereby, GOS 1 was denominated death, GOS 2 vegetative state, GOS 3 severe disability, GOS 4 moderate disability, and GOS 5 mild or no disability [22]. Per protocol, an unfavourable outcome was defined as GOS 1–3 (except for the evaluation of neuropsychological predictors of outcome where the GOS 1 category was dropped) and a favourable outcome as GOS 4–5. Based on recommendations of the American Brain Injury Consortium [23], neuropsychological evaluation was performed by a single investigator (M.C.H.) at long-term follow-up, which was performed in 36 of 37 survivors (97.3%) with one patient lost of followup. Of these, 29 patients were evaluated in our outpatient clinic and seven patients by a structured telephone interview using a validated questionnaire [24]. These seven patients were not available for an outpatient appointment, but did agree to undergo a structured telephone interview. The test battery addressed executive functions [25,26], attention and concentration [26], memory function [27], as well as visuoconstruction and visuomotor coordination (Table 1) [28]. More specifically, the Regensburger word fluency test (animals) was used to assess semantical word-fluency,
2483
Table 1 Neuropsychological tests. Domain assessed
Neuropsychological test
Semantical word-fluency Lexical word-fluency Cognitive flexibility Focused attention Sustained attention and concentration Verbal episodic memory
Regensburger word fluency test (animals) Regensburger word fluency test (s-words) Trail-Making Test Part B Trail-Making Test Part A Digit-Symbol-Test (Wechsler Adult Intelligence Scale) Logical Memory I – Text reproduction (Wechsler Memory Scales-R) Rey–Osterrieth complex figure test delayed recall (ROCF) Rey figure Grooved Pegboard
Visual episodic memory Visuoconstructive ability Visuomotoric coordination
the Regensburger word fluency test (s-words) to assess lexical word-fluency [26], the Trail-Making Test Part B to assess cognitive flexibility, the Trail-Making Test Part A to assess focused attention [29–31], the Digit-Symbol-Test (Wechsler Adult Intelligence Scale) to assess sustained attention and concentration [32,33], the Logical Memory I – test reproduction (Wechsler Memory ScalesR) to assess verbal episodic memory [34,35], the Rey–Osterrieth complex figure test delayed recall (ROCF) to assess visual episodic memory, the Rey Figure test to assess visuoconstructive ability, and the Grooved Pegboard test to assess visuomotor coordination, respectively. The performances on the neuropsychological tests were analysed by z-scores and thereafter classified into category 1: Average or superior (score > −1.0 standard deviation (SD) and accordingly z-values > −1 and T-values > 40); category 2: Mild to mid-severe impairment (−2.0 SD ≤ score ≥ −1.0 SD and accordingly z-values between −2.0 and −1.0 and T-values between 30 and 40); and category 3: Severe impairment (score < −2.0 SD and accordingly z-values < −2.0 and T-values ≤ 29) (Table 2). For further analysis, the neuropsychological test results from each domain were dichotomized into severe impairments (z < −2.0) and nonsevere impairments (z ≥ −2.0). Additionally, the work status was evaluated through an interview at long-term follow-up. 2.2. Statistical methods Data are presented as medians and range, respectively means and SD, where appropriate. Comparison of categorical variables was done using Fisher’s exact tests. Univariate and multivariate logistic regression models were used to assess relationships between baseline characteristics and GOS at follow-up. At this stage of the analysis, a p-value of 0.268) (Table 5). In contrast, the GOS at rehabilitation discharge was found to be a predictor of severe impairments at follow-up in all but one domain assessed (all p-values less than p < 0.038). A thorough analysis of the neuropsychological assessment at long-term follow-up categorized into average or superior, mild to moderate, or severe neuropsychological impairment is depicted in Table 2. The only neuropsychological domain where the GOS at rehabilitation discharge was not a predictor of severe impairments at follow-up was the semantical word-fluency assessed by the Regensburger word fluency test (animals). Respecting a level of significance of p < 0.005 in order to minimize type I error still revealed that the lexical word-fluency, cognitive flexibility, focused attention, sustained attention and concentration, verbal episodic memory, and visuomotor coordination, including tests from all four different domains executive function, attention and concentration, memory function, and visuoconstruction and motoric function, were predictors of severe neuropsychological impairments at longterm follow-up (p < 0.008). The following characteristics were not predictors of severe neuropsychological impairments at long-term follow-up (p > 0.114): age, gender, GCS, AIS head score, ISS score, presence of polytrauma, performed neurosurgical intervention, secondary DC, craniotomy with evacuation of a mass lesion, primary DCHC with evacuation of a mass lesion, and insertion of a VP-shunt. However, the presence of a primary DC trended to be significant to predict severe impairments in the cognitive flexibility and focused attention (p = 0.017). 3.4. Long-term outcome: functional and work status Work status at time of long-term follow-up was available in 32 of 36 patients (88.9%). Of these, 28 patients (87.5%) lived in private households and 22 patients (68.8%) received financial aid to some degree. Eighteen patients (56.3%) were able to resume work, of which 9 returned to their pre-traumatic employment and 9 had a voluntary or involuntary job change. Ten patients were able to work full time, whereby 8 had a reduced work quota. None of the 5 patients who had severe impairments throughout all neuropsychological domains assessed at follow-up were able to resume work, whereas both patients with good or average performance throughout all 9 neuropsychological domains resumed work. One patient returned to his pretraumatic employment and the other resumed another work with a reduced work quota of 20%. The median GOS (range) from all 18 patients who were able to resume work was 3 (2–4) at hospital discharge, 4 (4–5) at rehabilitation discharge, and 5 (4–5) at follow-up. Three patients with a hospital
discharge GOS of 2 were able to resume work, whereby one patient could resume in a reduced work quota of 80% his pretraumatic employment, and the other 2 patients a new employment with a work quota of 100% and 80%, respectively. All these 3 patients improved to a GOS of 4 at rehabilitation discharge.
3.5. Long-term outcome: physical complaints The most common physical complaints were sense of balance problems (n = 13, 40.6%) and headaches (n = 8, 25.0%). Patients emphasized the mental distress due to neuropsychological restrictions such as diminished concentration (n = 14, 43.8%) as well as verbal expression and comprehension deficits. Seven patients (21.9%) were taking anti-seizure medication and five were receiving antidepressants (15.6%).
4. Discussion The GOS at hospital discharge was not a predictor for severe impairments in all 9 neuropsychological domains assessed at longterm follow-up. However, the GOS at rehabilitation discharge was predictive to show severe impairments at follow-up in a total of 6 out of 9 neuropsychological domains. Our data suggest that the GOS is best measured at rehabilitation discharge, as this will best predict long-term neuropsychological deficits. Despite a favourable long-term functional outcome at follow-up in two thirds of the patients after severe TBI, severe neuropsychological impairment was present in 20.7–44.8% of the patients (depending on the according domain assessed), and only half of all patients were able to return to work. These findings show that results from specific neuropsychological tests do not necessarily correlate with functional outcome. Clifton et al. studied the relationship of 19 neuropsychological tests with 110 severely brain injured patients to the GOS at 3 and 6 months [39]. They found a close relationship to the GOS for four tests, namely the Controlled Oral Word Association, Grooved Pegboard, Trailmaking Part B, and Rey–Osterrieth complex figure delayed recall. At long-term follow-up, we could reproduce this finding between the association of the GOS and neuropsychological test results. All 9 neuropsychological domains tested, including Grooved Pegboard, Trailmaking Part B, and Rey–Osterrieth complex figure delayed recall test, showed a significant association with the GOS at follow-up (p < 0.018). The exact relationship between GOS scores and neuropsychological deficit remains to be further described. Satz et al. used discriminate validity analysis of the GOS at 6 months post injury in 100 patients with moderate to severe TBI [40]. The authors could show a systematic decrease in neuropsychological test performance as a function of decreasing GOS score as well as an increased prevalence of symptoms of depression and lower ratings on measures assessing employability and capacity for self care. Although the exact relationship between the neurological status after head injury (using the GOS) and neuropsychological status remains unclear, our results demonstrate that the GOS is most accurate at
2486
Table 5 Predictors of Neuropsychological outcome at long-term follow-up. Predictor
Executive function
Attention and concentration
Semantical word-fluency (1)
Lexical word-fluency (2)
Cognitive flexibility (3)
Memory function
Focused attention (4)
Visual episodic memory (7)
Verbal episodic memory (6)
Visuoconstructive ability (8)
Visuomotoric coordination (9)
Severe impairment
Non-severe impairment
Severe impairment
Non-severe impairment
Severe impairment
Non-severe impairment
Severe impairment
Non-severe impairment
Severe impairment
Non-severe impairment
Severe impairment
Non-severe impairment
Severe impairment
Non-severe impairment
Severe impairment
Non-severe impairment
Severe impairment
Non-severe impairment
GOS-HD; 2–3 GOS-HD; 4–5
11 (100) 0 (0.0)
14 (77.8) 4 (22.2)
9 (90.0) 1 (10.0)
16 (84.2) 3 (15.8)
8 (80.0) 2 (20.0)
17 (89.5) 2 (10.5)
8 (80.0) 2 (20.0)
17 (89.5) 2 (10.5)
6 (85.7) 1 (14.3)
19 (86.4) 3 (13.6)
12 (92.3) 1 (7.7)
12 (80.0) 3 (20.0)
6 (100) 0 (0.0)
19 (82.6) 4 (17.4)
6 (85.7) 1 (14.3)
19 (86.4) 3 (13.6)
7 (87.5) 1 (12.5)
18 (85.7) 3 (14.3)
GOS-RD; 2–3
4 (36.4)
3 (16.7)
6 (60.0)
1 (5.3)
6 (60.0)
1 (5.3)
6 (60.0)
1 (5.3)
5 (71.4)
2 (9.1)
7 (53.8)
0 (0.0)
4 (66.7)
3 (13.0)
4 (57.1)
3 (13.6)
5 (62.5)
2 (9.5)
GOS-RD; 4–5
7 (63.6)
15 (83.3)
4 (40.0)
18 (94.7)**
4 (40.0)
18 (94.7)**
4 (40.0)
18 (94.7)**
2 (28.6)
20 (90.9)**
6 (46.2)
15 (100)**
3 (33.3)
20 (87.0)*
3 (42.9)
19 (86.4)*
3 (37.5)
19 (90.5)**
Age; >40 Age; ≤40
5 (45.5) 6 (54.5)
5 (27.8) 13 (72.2)
5 (50.0) 5 (50.0)
5 (26.3) 14 (73.7)
4 (40.0) 6 (60.0)
6 (31.6) 13 (68.4)
4 (40.0) 6 (60.0)
6 (31.6) 13 (68.4)
4 (57.1) 3 (42.9)
6 (27.3) 16 (72.7)
7 (53.8) 6 (46.2)
3 (20.0) 12 (80.0)
3 (50.0) 3 (50.0)
7 (30.4) 16 (69.6)
4 (57.1) 3 (42.9)
6 (27.3) 16 (72.7)
4 (50.0) 4 (50.0)
6 (28.6) 15 (71.4)
Gender, female Gender, male
2 (18.2) 9 (81.8)
6 (33.3) 12 (66.7)
2 (20.0) 8 (80.0)
6 (31.6) 13 (68.4)
1 (10.0) 9 (90.0)
7 (36.8) 12 (63.2)
1 (10.0) 9 (90.0)
7 (36.8) 12 (63.2)
0 (0.0) 7 (100)
8 (36.4) 14 (63.6)
2 (15.4) 11 (84.6)
5 (33.3) 10 (66.7)
0 (0.0) 6 (100)
8 (34.8) 15 (65.2)
0 (0.0) 7 (100)
8 (36.4) 14 (63.6)
1 (12.5) 7 (87.5)
7 (33.3) 14 (66.7)
GCS, 4 AIS head, ≤4
3 (27.3) 8 (72.7)
3 (16.7) 15 (83.3)
3 (30.0) 7 (70.0)
3 (15.8) 16 (84.2)
3 (30.0) 7 (70.0)
3 (15.8) 16 (84.2)
3 (30.0) 7 (70.0)
3 (15.8) 16 (84.2)
2 (28.6) 5 (71.4)
4 (18.2) 18 (81.8)
3 (23.1) 10 (76.9)
3 (20.0) 12 (80.0)
2 (33.3) 4 (66.7)
4 (17.4) 19 (82.6)
1 (14.3) 6 (85.7)
5 (22.7) 17 (77.3)
2 (25.0) 6 (75.0)
4 (19.0) 17 (81.0)
ISS, >25 ISS, ≤25
8 (72.7) 3 (27.3)
10 (55.6) 8 (44.4)
6 (60.0) 4 (40.0)
12 (63.2) 7 (36.8)
5 (50.0) 5 (50.0)
13 (68.4) 6 (31.6)
5 (50.0) 5 (50.0)
13 (68.4) 6 (31.6)
4 (57.1) 3 (42.9)
14 (63.6) 8 (36.4)
8 (61.5) 5 (38.5)
10 (66.7) 5 (33.3)
4 (66.7) 2 (33.3)
14 (60.9) 9 (39.1)
4 (57.1) 3 (42.9)
14 (63.6) 8 (36.4)
5 (62.5) 3 (37.5)
13 (61.9) 8 (38.1)
Polytrauma, yes Polytrauma, no
9 (81.8) 2 (18.2)
10 (55.6) 8 (44.4)
8 (80.0) 2 (20.0)
11 (57.9) 8 (42.1)
7 (70.0) 3 (30.0)
12 (63.2) 7 (36.8)
7 (70.0) 3 (30.0)
12 (63.2) 7 (36.8)
5 (71.4) 2 (28.6)
14 (63.6) 8 (36.4)
11 (84.6) 2 (15.4)
8 (53.3) 7 (46.7)
5 (83.3) 1 (16.7)
14 (60.9) 9 (39.1)
5 (71.4) 2 (28.6)
14 (63.6) 8 (36.4)
6 (75.0) 2 (25.0)
13 (61.9) 8 (38.1)
Surgery, yes Surgery, no
8 (72.7) 3/27.3)
10 (55.6) 8 (44.4)
7 (70.0) 3 (30.0)
11 (57.9) 8 (42.1)
8 (80.0) 2 (20.0)
10 (52.6) 9 (47.4)
8 (80.0) 2 (20.0)
10 (52.6) 9 (47.4)
5 (71.4) 2 (28.6)
13 (59.1) 9 (40.9)
9 (69.2) 4 (30.8)
8 (53.3) 7 (46.7)
5 (83.3) 1 (16.7)
13 (56.5) 10 (43.5)
4 (57.1) 3 (42.9)
14 (63.6) 8 (36.4)
6 (75.0) 2 (25.0)
12 (57.1) 9 (42.9)
Primary DC, yes
5 (45.5)
6 (33.3)
5 (50.0)
6 (31.6)
7 (70.0)
4 (21.1)
7 (70.0)
4 (21.1)
4 (57.1)
7 (31.8)
6 (46.2)
5 (33.3)
4 (66.7)
7 (30.4)
4 (57.1)
7 (31.8)
5 (62.5)
6 (28.6)
Primary DC, no
6 (54.5)
12 (66.7)
5 (50.0)
13 (68.4)
3 (30.0)
15 (78.9)*
3 (30.0)
15 (78.9)*
3 (42.9)
15 (68.2)
7 (53.8)
10 (66.7)
2 (33.3)
16 (69.6)
3 (42.9)
15 (68.2)
3 (37.5)
15 (71.4)
Second. DC, yes Second. DC, no
3 (27.3) 8 (72.7)
4 (22.2) 14 (77.8)
3 (30.0) 7 (70.0)
4 (21.1) 15 (78.9)
2 (20.0) 8 (80.0)
5 (26.3) 14 (73.7)
2 (20.0) 8 (80.0)
5 (26.3) 14 (73.7)
1 (14.3) 6 (85.7)
6 (27.3) 16 (72.7)
3 (23.1) 10 (76.9)
3 (20.0) 12 (80.0)
1 (16.7) 5 (83.3)
6 (26.1) 17 (73.9)
0 (0.0) 7 (100)
7 (31.8) 15 (68.2)
2 (25.0) 6 (75.0)
5 (23.8) 16 (76.2)
Craniot. evac. (y) Mass lesion (n)
3 (27.3) 8 (72.7)
4 (22.2) 14 (77.8)
2 (20.0) 8 (80.0)
5 (26.3) 14 (73.7)
1 (10.0) 9 (90.0)
6 (31.6) 13 (68.4)
1 (10.0) 9 (90.0)
6 (31.6) 13 (68.4)
1 (14.3) 6 (85.7)
6 (27.3) 16 (72.7)
3 (23.1) 10 (76.9)
3 (20.0) 12 (80.0)
1 (16.7) 5 (83.3)
6 (26.1) 17 (73.9)
0 (0.0) 7 (100)
7 (31.8) 15 (68.2)
1 (12.5) 7 (87.5)
6 (28.6) 15 (71.4)
PrimaryDCHC (y) w Mass lesion (n)
3 (27.3) 8 (72.7)
5 (27.8) 13 (72.2)
2 (20.0) 8 (80.0)
6 (31.6) 13 (68.4)
4 (40.0) 6 (60.0)
4 (21.1) 15 (78.9)
4 (40.0) 6 (60.0)
4 (21.1) 15 (78.9)
2 (28.6) 5 (71.4)
6 (27.3) 16 (72.7)
3 (23.1) 10 (76.9)
5 (33.3) 10 (66.7)
2 (33.3) 4 (66.7)
6 (26.1) 17 (73.9)
2 (28.6) 5 (71.4)
6 (27.3) 16 (72.7)
2 (25.0) 6 (75.0)
6 (28.6) 15 (71.4)
VP shunt, yes VP shunt, no
4 (36.4) 7 (63.6)
3 (16.7) 15 (83.3)
3 (30.0) 7 (70.0)
4 (21.1) 15 (78.9)
4 (40.0) 6 (60.0)
3 (15.8) 16 (84.2)
4 (40.0) 6 (60.0)
3 (15.8) 16 (84.2)
2 (28.6) 5 (71.4)
5 (22.7) 17 (77.3)
4 (30.8) 9 (69.2)
3 (20.0) 12 (80.0)
2 (33.3) 4 (66.7)
5 (21.7) 18 (78.3)
2 (28.6) 5 (71.4)
5 (22.7) 17 (77.3)
3 (37.5) 5 (62.5)
4 (19.0) 17 (81.0)
GOS, Glasgow Outcome Scale; HD, hospital discharge; RD, rehabilitation discharge; GCS, Glasgow coma scale; AIS, abbreviated injury score; ISS, injury severity score; (y), yes; (n), no; PrimaryDCHC(y)w mass lesion, primary decompressive hemicraniectomy with evacuation of a mass lesion; VP, ventriculo-peritoneal. * p < 0.05; Fisher’s exact test. ** p < 0.005; Fisher’s exact test.
O.P. Gautschi et al. / Clinical Neurology and Neurosurgery 115 (2013) 2482–2488
Sustained attention and concentration (5)
Visuoconstruction and -motoric function
O.P. Gautschi et al. / Clinical Neurology and Neurosurgery 115 (2013) 2482–2488
predicting neuropsychological deficits after the rehabilitation process has been completed. Although the majority of patients with severe TBI in long-term outcome studies are presenting good physical recovery with independence in locomotion and basic life skills, neuropsychological sequelae are thought to create difficulty in social reintegration [12,14,15,17,18]. It was found that 2–5 years post TBI, physical abilities recover better than cognitive functions [13]. However, the temporal profile of recovery after severe TBI has not been investigated in depth so far. Our data showed that an overwhelming majority of patients experience a dramatic improvement from hospital discharge to time of follow-up. At long-term follow-up, over two thirds of patients presented with higher functional independence. In concordance with previous studies, many of our patients lost their pre-trauma level of employment or were not able to work full-time [13,14]. Return to work has been defined as an important external measurement of outcome, since it does not depend on subjective judgement, unlike the GOS. While cognitive changes after TBI can lead to social isolation and unemployment [41], the resulting situation may also aggravate cognitive and behavioural problems. Our data, presenting a return to work ratio of more than 50%, agrees with findings of other studies, where the return to work quota ranged from 23% to 72% one year post-discharge [42–45]. However, only half of all patients of our study groups who returned to work, returned to their pre-traumatic employment. A closer analysis of the course of the GOS from hospital to rehabilitation discharge to follow-up of all 18 patients who were able to return to work revealed a median score of 3, 4, and 5, respectively, indicating a steady improvement. Moreover, even 3 patients with a hospital discharge GOS of 2 resumed work at follow-up. All these 3 patients experienced a decisive amelioration to a GOS of 4 after rehabilitation. This fact not only stresses the importance of an adequate neurosurgical and intensive care treatment at the best, but also underlines the significance of an adequate rehabilitation to the earliest possible moment. Although an increasing percentage of patients after severe TBI may achieve a favourable outcome (GOS 4 and 5), cognitive, emotional, vocational, and social disturbances will always play a major role in the final disability of these patients [46]. Therefore, recovery assessment scales of functional, neuropsychological, and psychosocial domains are indispensable not only to guide the post-acute care and to provide information concerning long-term outcome to the next of kin, but also to compare the outcome of TBI cohorts undergoing different acute phase management and post-acute phase rehabilitation protocols [47,48]. Further prospective studies are needed in order to validate our findings and especially to elucidate which patients with severe brain injuries might profit the most from a neurorehabilitation programme to achieve a favourable functional and cognitive outcome. 5. Conclusions The GOS at rehabilitation discharge should be regarded as a better predictor for neuropsychological impairments at long-term follow-up than the GOS at hospital discharge. Even in patients with favourable GOS after finishing a course of rehabilitation, three quarters of these patients may have at least one severe neuropsychological deficit. Therefore, it remains of paramount importance to provide long-term neuropsychological support to further improve outcome after TBI. Conflict of interest The authors do not report any conflict of interest concerning this study or the findings specified in this paper.
2487
Acknowledgements The authors would like to thank all the participating patients for their valuable cooperation. Special thanks to Dr. phil. Erika Foster and Andrea Näpflin for their neuropsychological expertise and the rehabilitation clinics Zihlschlacht, Valens, Affoltern, Wald and Bellikon not only for their hard work with patients but also for their contribution to this study.
References [1] Leibson CL, Brown AW, Hall Long K, Ransom JE, Mandrekar J, Osler TM, et al. Medical care costs associated with traumatic brain injury over the full spectrum of disease: a controlled population-based study. Journal of Neurotrauma 2012;29(July 20 (11)):2038–49 [PubMed PMID: 22414023. Epub 2012/03/15. eng]. [2] Tagliaferri F, Compagnone C, Korsic M, Servadei F, Kraus J. A systematic review of brain injury epidemiology in Europe. Acta Neurochirurgica 2006;148(March (3)):255–68 [discussion 68. PubMed PMID: 16311842. Epub 2005/11/29. eng]. [3] Marshall LF, Gautille T. The outcome of severe closed head-injury. Journal of Neurosurgery 1991;75:S28–36. [4] Murray GD, Teasdale GM, Braakman R, Cohadon F, Dearden M, Iannotti F, et al. The European Brain Injury Consortium survey of head injuries. Acta Neurochirurgica 1999;141(3):223–36 [PubMed PMID: 10214478. Epub 1999/04/24. eng]. [5] Bullock R, Chesnut RM, Clifton G, Ghajar J, Marion DW, Narayan RK, et al. Guidelines for the management of severe head injury. Brain Trauma Foundation. European Journal of Emergency Medicine: Official Journal of the European Society for Emergency Medicine 1996;3(June (2)):109–27 [PubMed PMID: 9028756. Epub 1996/06/01. eng]. [6] Maas AI, Dearden M, Teasdale GM, Braakman R, Cohadon F, Iannotti F, et al. EBIC-guidelines for management of severe head injury in adults, European Brain Injury Consortium. Acta Neurochirurgica 1997;139(4):286–94 [PubMed PMID: 9202767. Epub 1997/01/01. eng]. [7] Grande PO. The “Lund Concept” for the treatment of severe head trauma – physiological principles and clinical application. Intensive Care Medicine 2006;32(October (10)):1475–84 [PubMed PMID: 16896859. Epub 2006/08/10. eng]. [8] Eker C, Asgeirsson B, Grande PO, Schalen W, Nordstrom CH. Improved outcome after severe head injury with a new therapy based on principles for brain volume regulation and preserved microcirculation. Critical Care Medicine 1998;26(November (11)):1881–6 [PubMed PMID: 9824083. Epub 1998/11/21. eng]. [9] Naredi S, Eden E, Zall S, Stephensen H, Rydenhag B. A standardized neurosurgical neurointensive therapy directed toward vasogenic edema after severe traumatic brain injury: clinical results. Intensive Care Medicine 1998;24(May (5)):446–51 [PubMed PMID: 9660259. Epub 1998/07/11. eng]. [10] Naredi S, Olivecrona M, Lindgren C, Ostlund AL, Grande PO, Koskinen LO. An outcome study of severe traumatic head injury using the “Lund therapy” with low-dose prostacyclin. Acta Anaesthesiologica Scandinavica 2001;45(April (4)):402–6 [PubMed PMID: 11300376. Epub 2001/04/13. eng]. [11] Olivecrona M, Rodling-Wahlstrom M, Naredi S, Koskinen LO. Effective ICP reduction by decompressive craniectomy in patients with severe traumatic brain injury treated by an ICP-targeted therapy. Journal of Neurotrauma 2007;24(June (6)):927–35 [PubMed PMID: 17600510. Epub 2007/06/30. eng]. [12] Colantonio A, Ratcliff G, Chase S, Kelsey S, Escobar M, Vernich L. Long-term outcomes after moderate to severe traumatic brain injury. Disability and Rehabilitation 2004;26(March 4 (5)):253–61 [PubMed PMID: 15200240. Epub 2004/06/18. eng]. [13] deGuise E, leBlanc J, Feyz M, Meyer K, Duplantie J, Thomas H, et al. Long-term outcome after severe traumatic brain injury: the McGill interdisciplinary prospective study. Journal of Head Trauma Rehabilitation 2008;23(September–October (5)):294–303 [PubMed PMID: 18815506. Epub 2008/09/26. eng]. [14] Dikmen SS, Machamer JE, Powell JM, Temkin NR. Outcome 3 to 5 years after moderate to severe traumatic brain injury. Archives of Physical Medicine and Rehabilitation 2003;84(October (10)):1449–57 [PubMed PMID: 14586911. Epub 2003/10/31. eng]. [15] Hoofien D, Gilboa A, Vakil E, Donovick PJ. Traumatic brain injury (TBI) 10-20 years later: a comprehensive outcome study of psychiatric symptomatology, cognitive abilities and psychosocial functioning. Brain Injury: [BI] 2001;15(March (3)):189–209 [PubMed PMID: 11260769. Epub 2001/03/22. eng]. [16] Novack TA, Bush BA, Meythaler JM, Canupp K. Outcome after traumatic brain injury: pathway analysis of contributions from premorbid, injury severity, and recovery variables. Archives of Physical Medicine and Rehabilitation 2001;82(March (3)):300–5 [PubMed PMID: 11245749. Epub 2001/03/14. eng]. [17] Ratcliff G, Colantonio A, Escobar M, Chase S, Vernich L. Long-term survival following traumatic brain injury. Disability and Rehabilitation 2005;27(March 18 (6)):305–14 [PubMed PMID: 16040532. Epub 2005/07/26. eng]. [18] Wood RL, Rutterford NA. Psychosocial adjustment 17 years after severe brain injury. Journal of Neurology, Neurosurgery, and Psychiatry 2006;77(January
2488
[19]
[20]
[21]
[22]
[23]
[24]
[25] [26] [27] [28]
[29]
[30] [31] [32] [33] [34]
[35]
O.P. Gautschi et al. / Clinical Neurology and Neurosurgery 115 (2013) 2482–2488
(1)):71–3 [PubMed PMID: 16361596. Pubmed Central PMCID: 2117407. Epub 2005/12/20. eng]. Perel P, Arango M, Clayton T, Edwards P, Komolafe E, Poccock S, et al. Predicting outcome after traumatic brain injury: practical prognostic models based on large cohort of international patients. British Medical Journal 2008;336(February 23 (7641)):425–9 [PubMed PMID: 18270239. Pubmed Central PMCID: 2249681. Epub 2008/02/14. eng]. Roozenbeek B, Lingsma HF, Lecky FE, Lu J, Weir J, Butcher I, et al. Prediction of outcome after moderate and severe traumatic brain injury: external validation of the International Mission on Prognosis and Analysis of Clinical Trials (IMPACT) and Corticoid Randomisation After Significant Head injury (CRASH) prognostic models. Critical Care Medicine 2012;40(May (5)):1609–17 [PubMed PMID: 22511138. Pubmed Central PMCID: 3335746. Epub 2012/04/19. eng]. Steyerberg EW, Mushkudiani N, Perel P, Butcher I, Lu J, McHugh GS, et al. Predicting outcome after traumatic brain injury: development and international validation of prognostic scores based on admission characteristics. PLoS Medicine 2008;5(August 5 (8)):e165 [discussion e. PubMed PMID: 18684008. Pubmed Central PMCID: 2494563. Epub 2008/08/08. eng]. Jennett B, Snoek J, Bond MR, Brooks N. Disability after severe head injury: observations on the use of the Glasgow Outcome Scale. Journal of Neurology, Neurosurgery, and Psychiatry 1981;44(April (4)):285–93 [PubMed PMID: 6453957. Pubmed Central PMCID: 490949. Epub 1981/04/01. eng]. Bullock MR, Merchant RE, Choi SC, Gilman CB, Kreutzer JS, Marmarou A, et al. Outcome measures for clinical trials in neurotrauma. Neurosurgical Focus 2002;13(July 15 (1)):ECP1 [PubMed PMID: 15916412. Epub 2005/05/27. eng]. Wilson JT, Pettigrew LE, Teasdale GM. Structured interviews for the Glasgow Outcome Scale and the extended Glasgow Outcome Scale: guidelines for their use. Journal of Neurotrauma 1998;15(August (8)):573–85 [PubMed PMID: 9726257. Epub 1998/09/03. eng]. Aschenbrenner ST, Lange KW. Regensburger Wortflüssigkeits-test (RWT). Hogrefe: Göttingen; 2000. Lezak M. Neuropsychological assessment. 3rd ed. Oxford University Press; 1995. Rey A. Léxamen psychologique dans le cas d’encéphalopathie traumatique. Archives of Psychology 1941;28:286–340. Ruff RM, Parker SB. Gender-age-specific changes in motor speed eye-hand coordination in adults: normative values for the Finger Tapping Grooved Pegboard Tests. Perceptual Motor Skills 1993;76(June (3 Pt 2)):1219–30 [PubMed PMID:, 8337069. Epub 1993/06/01. eng]. Merten T, Green P, Henry M, Blaskewitz N, Brockhaus R. Analog validation of German-language symptom validity tests and the influence of coaching. Archives of Clinical Neuropsychology: The Official Journal of the National Academy of Neuropsychologists 2005;20(August (6)):719–26 [PubMed PMID: 16005815]. Reitan RM. Validity of the trail making test as an indicator of organic brain damage. Perceptual and Motor Skills 1958;8:271–6. Reitan RM. Trail making test. Manual for administration and scoring. South Tucson, AZ: Reitan Neuropsychology Laboratory; 1992. Aster M, Neubauer A, Horn R. Wechsler-Intelligenztest für Erwachsene WIEmanual. Frankfurt: Harcourt Test Services; 2006. Petermann F, Lepach A. Wechsler memory scale – fourth edition, German edition. Manual. Frankfurt: Pearson Assessment; 2012. Härting C, Markowitsch HJ, Neufeld H, Calabrese P, Deisinger P, Kessler J. Wechsler Gedächtnistest-Revidierte Fassung Deutsche Adaptation der revidierten Fassung der Wechsler memory scale. Bern, Switzerland: Huber; 2000. Wechsler D. WMS-R: Wechsler memory scale-revised. San Antonio: The Psychological Corporation; 1987.
[36] Baker SP, O’Neill B, Haddon Jr W, Long WB. The injury severity score: a method for describing patients with multiple injuries and evaluating emergency care. Journal of Trauma 1974;14(March (3)):187–96 [PubMed PMID: 4814394. Epub 1974/03/01. eng]. [37] Civil ID, Schwab CW. The abbreviated injury scale, 1985 revision: a condensed chart for clinical use. Journal of Trauma 1988;28(January (1)):87–90 [PubMed PMID: 3339667. Epub 1988/01/01. eng]. [38] Marshall LF, Marshall SB, Klauber MR, Van Berkum Clark M, Eisenberg H, Jane JA, et al. The diagnosis of head injury requires a classification based on computed axial tomography. Journal of Neurotrauma 1992;1(March (9 Suppl)):S287–92 [PubMed PMID: 1588618. Epub 1992/03/01. eng]. [39] Clifton GL, Kreutzer JS, Choi SC, Devany CW, Eisenberg HM, Foulkes MA, et al. Relationship between Glasgow Outcome Scale and neuropsychological measures after brain injury. Neurosurgery 1993;33(July (1)):34–8 [discussion 8-9. PubMed PMID: 8355845. Epub 1993/07/01. eng]. [40] Satz P, Zaucha K, Forney DL, McCleary C, Asarnow RF, Light R, et al. Neuropsychological, psychosocial and vocational correlates of the Glasgow Outcome Scale at 6 months post-injury: a study of moderate to severe traumatic brain injury patients. Brain injury: [BI] 1998;12(July (7)):555–67 [PubMed PMID: 9653519. Epub 1998/07/08. eng]. [41] Draper K, Ponsford J, Schonberger M. Psychosocial and emotional outcomes 10 years following traumatic brain injury. Journal of Head Trauma Rehabilitation 2007;22(September–October (5)):278–87 [PubMed PMID: 17878769. Epub 2007/09/20. eng]. [42] Annoni JM, Beer S, Kesselring J. [Sequelae of severe craniocerebral injuries, An epidemiological study in the Canton of St. Gallen]. Schweizerische Medizinische Wochenschrift 1991;121(February 16 (7)):207–13 [PubMed PMID: 1901176. Epub 1991/02/16. Folgen des schweren Schadel-Hirn-Traumas. Eine epidemiologische Studie im Kanton St. Gallen. ger.]. [43] Benedictus MR, Spikman JM, van der Naalt J. Cognitive and behavioral impairment in traumatic brain injury related to outcome and return to work. Archives of Physical Medicine and Rehabilitation 2010;91(September (9)):1436–41 [PubMed PMID: 20801264. Epub 2010/08/31. eng]. [44] Green RE, Colella B, Hebert DA, Bayley M, Kang HS, Till C, et al. Prediction of return to productivity after severe traumatic brain injury: investigations of optimal neuropsychological tests and timing of assessment. Archives of Physical Medicine and Rehabilitation 2008;89(December (12 Suppl)):S51–60 [PubMed PMID: 19081442. Epub 2008/12/23. eng]. [45] Schonberger M, Ponsford J, Olver J, Ponsford M, Wirtz M. Prediction of functional and employment outcome 1 year after traumatic brain injury: a structural equation modelling approach. Journal of Neurology, Neurosurgery, and Psychiatry 2011;82(August (8)):936–41 [PubMed PMID: 21217165. Epub 2011/01/11. eng.]. [46] Formisano R, Carlesimo GA, Sabbadini M, Loasses A, Penta F, Vinicola V, et al. Clinical predictors and neuropsychological outcome in severe traumatic brain injury patients. Acta Neurochirurgica 2004;146(May (5)):457–62 [PubMed PMID: 15118882. Epub 2004/05/01. eng]. [47] Hudak AM, Caesar RR, Frol AB, Krueger K, Harper CR, Temkin NR, et al. Functional outcome scales in traumatic brain injury: a comparison of the Glasgow Outcome Scale (Extended) and the Functional Status Examination. Journal of Neurotrauma 2005;22(November (11)):1319–26 [PubMed PMID: 16305320. Epub 2005/11/25. eng]. [48] Nichol AD, Higgins AM, Gabbe BJ, Murray LJ, Cooper DJ, Cameron PA. Measuring functional and quality of life outcomes following major head injury: common scales and checklists. Injury 2011;42(March (3)):281–7 [PubMed PMID: 21145059. Epub 2010/12/15. eng].
