Neurobehavioural deficits after severe traumatic brain injury (TBI)

Brain Injury, June 2006, 20(6): 569 574 Neurobehavioural deficits after severe traumatic brain injury (TBI) MARCELLA LIPPERT-GRÜNER 1, JOHANNES KUCHTA 1, MARTIN HELLMICH 2,& NORFRID KLUG 1 1 Department of Neurosurgery and 2 Institute of Medical Statistics, Informatics and Epidemiology Cologne University Hospital, Germany (Received 11 May 2005; accepted 11 January 2006) Abstract Objectives: Debilitating neurobehavioural sequalae often complicate traumatic brain injury (TBI). Cognitive deficits, particularly of attention, memory, information-processing speed and problems in self-perception, are very common following severe TBI. Method: The Neurobehavioural Rating Scale (NRS) is a multi-dimensional clinical-based assessment instrument designed and validated to measure neurobehavioural disturbances following TBI. This study examined 41 patients who were admitted to the intensive care unit of the Department of General Neurosurgery at Cologne University Hospital after severe TBI between January 1995 and July 2003. All 27 items of the NRS were assessed 6 and 12 months post-injury. Results: Subjects after severe TBI (GCS<9) showed relatively high overall scores on the NRS, reflecting a high degree of overall neurobehavioural dysfunction. NRS items did not change significantly between 6 and 12 months post-trauma for anxiety, expressive deficit, emotional withdrawal, depressive mood, hostility, suspiciousness, fatigability, hallucinatory behaviour, motor retardation, unusual thought content, liability of mood and comprehension deficit. There was a tendency of improvement for inattention, somatic concern, disorientation, guilt feelings, excitement, poor planning and articulation deficits. For conceptual disorganization, disinhibition, memory deficit, agitation, inaccurate self-appraisal, decreased initiative, blunted affect and tension even a tendency for further deterioration in the post-traumatic follow-up was detected. Changes between 6 and 12 months post-tbi were statistically significant for disorientation (improvement), inattention/ reduced alertness (improvement) and excitement (deterioration). Conclusion: The data shows that neurobehavioural deficits after TBI do not show a general tendency to disappear over time. Some aspects related to self-appraisal, conceptual disorganization and affect may even deteriorate, thereby presenting a challenging problem for both the patients and relatives. This is in contrast to the parallel improvement of post-traumatic sensomotoric deficits. Keywords: Neurobehavioural rating scale (NRS), traumatic brain injury Objectives Rehabilitative treatment in the last decades has focused mainly on the treatment of sensomotoric deficits and only recently on neuropsychological and behavioural deficits. Whereas in the case of sensomotoric deficits the use of compensation strategies and the provision of individually adapted mechanical aids may often offer the patients a good quality of life, it is the amount of neuropsychological and behavioural deficits that determine successful social and occupational reintegration [1]. Behavioural disturbances typically become obvious some time after the acute phase of the disease. To cope with these changes in the personality of the patient is sometimes very difficult not only for the patient itself, but also for its relatives and his or her social environment. These deficits are generally not as easily tolerated and understood by the family when compared to sensomotoric deficits. For the outcome of patients after severe TBI it is important that after the acute medical treatment or whenever possible already during this treatment is Correspondence: Johannes Kuchta, Department of Neurosurgery, Cologne University, Joseph-Stelzmann-Str 9, 50924 Cologne, Germany. Tel: +49 221 4785206. Fax: +49 221 4785921. E-mail: johannes.kuchta@uk-koeln.de ISSN 0269 9052 print/issn 1362 301X online ß 2006 Taylor & Francis DOI: 10.1080/02699050600664467

570 M. Lippert-Grüner et al. started, a targeted, individually adapted, intensive rehabilitative treatment should be started. Early rehabilitation should help the patient to re-integrate into his family and his social and occupational environment [2, 3]. It is well-known that, unlike other chronic disease during which there is often a stabilization or even an improvement of psychic functions, behavioural deficits caused by TBI may persist for years without the motivating tendency to improve. In the literature the patient s outcome after severe TBI is described in terms of function scores which mostly state the amount of recovery semiquantitatively, thus allowing only an estimation of the patient s state [4]. Also the function-oriented scores (e.g. for example the Functions Independence Measure ( FIM ) or the Barthel Index ), which are essentially intended to test the ability for activities of daily life, are not suitable to describe the amount of neuropsychological deficits or behavioural disturbances. In the current literature only few studies, which assess the amount of behavioural deficits after severe TBI patients, can be found [1 3, 5 8]. The problematic is also that during the first 3 months after severe TBI a targeted analysis of behavioural deficits is complicated by persistent acute psychosyndromes. These may cause disturbances of orientation and concentration, thereby making the patient unable to complete the neurobehavioural test. The Brief Psychiatric Rating Scale (BPRS) as revised by Levin et al. [5] is an important score for the assessment of behavioural disturbances at the neurobehavioural level. Nevertheless, this scale was designed mainly for psychiatric patients and does not take into account important neurobehavioural deficits typically observed after TBI (attention, memory, etc.). For this purpose the,neurobehavioural Rating Scale (NRS) as initially described by Levin et al. in 1978 was developed. The NRS has been validated by various authors and has been used in this study for the assessment of behavioural deficits after severe TBI [7, 9]. Methods Subjects and procedures A prospective study assessed behavioural deficits in 59 patients who were admitted to the neurosurgical intensive care unit of Cologne University Hospital after severe TBI. Sixteen patients died during the acute phase of the treatment, two patients died during the test period (within the first year after severe TBI). Glasgow Coma Scale scores of all patients were 8 for more than 24 hours post-trauma. Severity of the trauma was assessed using the Injury-Severity-score (ISS). The mean ISS score of the patients was 32.5 (9 50). Thirty-eight (79%) of the patients included suffered from a closed head injury and 10 (21%) patients suffered from an open head injury. Patients with a documented history of psychiatric disorders or prior brain injury were excluded from the study. Patients were investigated with the help of the Neurobehavioural Rating Scale, 6 (n ¼ 46) and 12 (n ¼ 41) months after the trauma. The Neurobehavioural Rating Scale [6] is a 27 item, multi-dimensional clinically based assessment instrument designed to measure neurobehavioural disturbances. Based on the brief psychiatric rating scale (BPRS), the NRS includes items for the assessment of neuropsychiatric symptoms resulting from closed head injury [8, 9]. The neurobehavioural rating scale has been shown to be a reliable and valid instrument for quantifying behavioural disturbances and gross cognitive impairments in those with neuropsychiatric syndromes including TBI [10]. All patients underwent early rehabilitation directly after the acute treatment on the intensive care unit after weaning from artificial ventilation and cardio-pulmonal stabilization. The duration of early rehablitative treatment was between 4 78 days (mean ¼ 18 days). Rehablitative treatment was adapted to the need of each patient and was performed between 4 5 hours per day. Multi-modal rehabilitation included: physiotherapy, ergotherapy, speech therapy and neuropsychological training. After early rehabilitation on the intensive care unit the patiens were transfered to a specialized neurorehabilitation centre where the patients were hospitalized for 8 21 weeks (mean ¼ 12 weeks). The NRS after 6 and 12 months was assessed by the same person (ML). Statistical analysis NRS ratings were summarized for each time point (6 and 12 months) giving the mean and the standard deviation. Changes of NRS ratings over time were assessed by means of the paired t-test with corresponding 95% confidence interval. Changes over time of the factors proposed by Levin et al. [6] were assessed using the paired t-test (for factor scores; high power if all items change in the same direction) as well as the multi-variate Hotelling s trace (MANOVA). P-values equal or below 0.05 were considered statistically significant, though no adjustment for multiple testing was made. All statistical analyses were performed using SPSS 12.0.2 for Windows.

Neurobehavioural deficits after severe traumatic brain injury (TBI) 571 Figure 1. (a) Factor I: cognition, energy: paired t-test for factor scores, p ¼ 0.704, Hotelling s trace, p < 0.0001; (b) Factor II: metacognition: paired t-test for factor scores, p ¼ 0.036; Hotelling s trace, p < 0.357. Results The patients investigated were unconscious for 9.8 days on average (range 2 55 days). Early rehabilitative treatment was initiated in all patients at the neurosurgical intensive care unit already during the acute post-traumatic phase. This therapy was performed 3 4 hours per day and included physiotherapy, ergotherapy, speech therapy and neuropsychology. In more than 90% of the patients rehabilitation therapy was continued after transfer to a specialized rehabilitation centre or on an ambulatory basis. Rehabilitative treatment was performed for 12 weeks post-trauma on average. All patients included in this study were able to complete the mini-mental state test [10] and were able to concentrate and communicate clear enough to answer the questions posed within the NRS. The age distribution was between 16 64 years (mean ¼ 33.6 years) with a male : female ratio of 4 : 1. The cranial injury pattern of the patients (Figure 2) included acute epidural haematoma (22%), acute subdural haematoma (42%), traumatic subarachnoid haemorrhage (29%), contusion (80%), skull fractures (22%), skull-base fracture (34%) and contusion of the brain stem (18%). Attendant injuries (Figure 3) included mid-face injuries (33%), lung contusion (10%), rib fracture (10%), pneumothorax (16%), clavicle fracture (12%), spleen rupture (45%), fracture of the pelvis (10%), upper extremity fracture (8%), lower extremity fracture (17%) and spine injury (18%). The Neurobehavioural-Rating-Scale (NRS) distinguishes between seven values with 1 ¼ not present, 2 ¼ very slight, 3 ¼ slight, 4 ¼ moderate, 5 ¼ rather severe, 6 ¼ severe and 7 ¼ extremely severe. Only two of the 27 items covered by the Neurobehavioural rating scale improved significantly ( p < 0.001) between 6 and 12 months after severe TBI in the 41 patients tested. These items included Inattention, reduced alertness (3.71 2.76, paired differences: 0.95 (1.40)) and Disorientation (2 39 to 1.27, paired differences: 1.12 (1.38)). Surprisingly, 12 out of 27 items showed a tendency (paired differences >0.3) to deteriorate in the followup period. These items included (Figure 1): conceptual disorganization, agitation, inaccurate insight,

572 M. Lippert-Grüner et al. Figure 2. Cranial injury patterns (n ¼ 41). sedh ¼ acute epidural haematoma, asdh ¼ acute subdural haematoma, tsab ¼ traumatic subarachnoid haemorrhage, CONT ¼ brain contusions, cfract ¼ convexity skull fractures, sbfract ¼ skull base fractures, BSC ¼ brainstem contusions. Figure 3. Additional injury patterns (n ¼ 41). ffract ¼ Le Fort fractures, lungk ¼ pulmonary contusion, ribfr ¼ rib fractures, lefract ¼ fractures of the lower extremities, uefract ¼ fractures of the upper extremities. emotional withdrawal, disinhibition, memory deficit, decreased initiative, unusual thought content, blunted affect, excitement, tension and poor planning. All other items tested showed no clear changes over time (for complete data see Appendix). Discussion Behavioural deficits after severe TBI can be assessed objectively using the neurobehavioural rating scale [8]. The amount of neurobehavioural deficits is crucially important for the rate at which TBI patients can re-integrate into their families, their social and occupational groups. The NRS can assess these deficits after a semi-structured interview and based on a relatively brief interaction with the patient. In a clinical setting, the NRS can be an important source of information about a patient s pattern of improvement and residual behavioural deficits. This provides the clinician with a basis from which to determine the patient and family

Neurobehavioural deficits after severe traumatic brain injury (TBI) 573 perspective, which can be important for rehabilitation planning. Even today a targeted therapeutic behavioural treatment of rehabilitation in-patients is offered by a small number of centres only. At least during the acute post-trauma phase the problem of behavioural deficits is initially overshadowed by the clinically prominent sensomotoric deficits. Because the patients are seriously ill, behavioural problems are often neglected in the first weeks by the patient, its relatives, but also by medical staff. These deficits become apparent during the post-acute post-traumatic phase, when the patient and his or her relatives become more sensible for behavioural dysfunctions. With the help of the NRS, Levin et al. [6] were able to establish a profile of the neurobehavioural status during the sub-acute phase after TBI. They found that disturbances relating to concept building, planning and realistic self-assessment are very common in the long-term follow-up after severe head injury. The data presented here supports these findings. Improved mobility of the patients in the sub-acute stage may be a factor for the dynamic emergence of behavioural disturbances. While during the acute phase after TBI mainly elements such as disorientation and psychomotoric restlessness prevail, now after discharge of the patients from the hospital with a higher degree of social interaction, the behavioural spectrum widens so that many behavioural deficits may be detected for the first time. The data shows that, even after 12 months post- TBI, a wide spectrum of behavioural deficits can be observed. Comparing the degree neurobehavioural deficits at 6 and 12 months post-tbi, behavioural deficits not only persist, but may even become more severe. Also confirming the literature, this study shows that the highest degree of severity is reached by disturbances relating to attention, concept building, increased excitability as well as deficits in the thinking involved in planning, followed by deficits like reduced affective oscillation capacity, memory deficits as well as decrease in critical capacity. Deficits like symptom building, orientational disturbances, as well as deficits in communicative ability, which are regarded in the literature as characteristic of a neurobehavioural disturbance profile in the acute illness phase, play a less important role in the long-term follow-up of the group of patients that have been examined. Regarding behavioural deficits like breakingdown inhibitions, reduced affective oscillation capacity, weakened critical thinking, affective degeneration as well as disturbances in concept building and the thinking involved in planning, a non-significant tendency was found to increase in severity. This again may reflect the increasing interaction with the family and the social environment, going along with an increase in mobility and an improvement of sensomotoric deficits. Patients with severe head injury as discussed here are predominantly young male individuals. Many neurobehavioural deficits become clearly visible when these patients try to go back into their former occupation or when the patients have to integrate in a new working environment. A lack of communicative abilities or social competence may become evident more easily in these young patients than in older patients who have already fixed social relations and environmental positions. Providing early and individually adapted neuro-psychological and behavioural therapy, as well as therapeutic care for the family and the social environment, will substantially improve the quality of life in patients after severe TBI. References 1. Lippert-Gruener M, Wedekind Ch, Klug N. Functional and psychosocial outcome one year after brain injury and early onset rehabilitation therapy. Journal of Rehabilitation Medicine 2002;34:211 214. 2. Dombrovy ML, Olek AC. Recovery and rehabilitation following traumatic brain injury. Brain Injury 1997;11:305 318. 3. Brooks DN, McKinlay W. Personality and behavioural change after severe blunt head injury-a relative s view. Journal of Neurology, Neurosurgery & Psychiatry 1983;46:336 344. 4. Jennett M, Bond M. Assessment of outcome after brain damage. Lancet 1975;1:480 487. 5. Levin HS, Grossman RG. Behavioural sequelae of closed head injury. A quantitative study. Archives of Neurology 1978;35:720 727. 6. Levin HS, High WM, Goethe KE, Sisson RA, Overall JE, Rhoades HM, Eisenberg HM, Kalisky Z, Gary HE. The neurobehavioural rating scale: Assessment of the behavioural sequelae of head injury by the clinician. Journal of Neurology, Neurosurgery & Psychiatry 1987;50:183 193. 7. Livingstone MG, Brooks DN, Bond MR. Patient outcome in the year following severe head injury and relative s psychiatric and social functioning. Journal of Neurology, Neurosurgery & Psychiatry 1985;48:876 881. 8. McCauley SR, Levin HS, Vanier M, Mazaux JM, Boake C, Goldfader PR, Rockers D, Butters M, Kareken DA, Lambert J, Clifton GL. The neurobehavioral rating scalereviesed: Sensitivity and validity in closed head injury assessment. Journal of Neurology, Neurosurgery & Psychiatry 2001;71:643 651. 9. Corrigan JD, Dickerson J, Fisher E, Meyer P. The neurobehavioral rating scale: Replication in an acute, inpatient rehabilitation setting. Brain Injury 1990;4:215 222. 10. Crum RM, Anthony JC, Bassett SS, Folstein MF. Population-based norms for the mini-mental state examination by age and educational level. JAMA 1993;269(18):2386 2391.

574 M. Lippert-Grüner et al. Table I. Appendix: Neurobehavioural rating scale (NRS) data 6 and 12 months after severe brain injury. Variable 6 months (n ¼ 41) 12 months (n ¼ 41) Paired differences 95% CI p-value Inattention, reduced alertness 3.71 (1.08) 2.76 (1.02) 0.95 (1.40) 0.51 1.39 <0.001 Somatic concern 2.22 (1.74) 2.07 (1.63) 0.15 (2.23) 0.56 0.85 0.677 Disorientation 2.39 (1.24) 1.27 (0.67) 1.12 (1.38) 0.69 1.56 <0.001 Anxiety 2.10 (1.58) 2.32 (1.54) 0.22 (2.19) 0.91 0.47 0.524 Expressive deficit 1.85 (1.44) 1.68 (1.49) 0.17 (2.28) 0.55 0.89 0.634 Emotional withdrawal 2.54 (1.53) 2.90 (1.76) 0.37 (2.28) 1.08 0.35 0.310 Conceptual disorganization 2.90 (1.74) 3.49 (2.04) 0.59 (2.65) 1.42 0.25 0.166 Disinhibition 1.68 (1.31) 2.02 (1.71) 0.34 (2.07) 0.99 0.31 0.297 Guilt feelings 1.29 (0.87) 1.02 (0.16) 0.27 (0.90) 0.01 0.55 0.062 Memory deficit 2.73 (1.52) 3.07 (1.66) 0.34 (2.22) 1.04 0.36 0.331 Agitation 1.63 (1.30) 2.22 (1.75) 0.59 (2.10) 1.25 0.08 0.081 Inaccurate insight and self-appraisal 2.83 (1.72) 3.49 (2.06) 0.66 (2.60) 1.48 0.16 0.113 Depressive mood 2.20 (1.45) 2.27 (1.64) 0.07 (2.22) 0.77 0.63 0.834 Hostility, uncooperativeness 2.10 (1.67) 2.27 (1.78) 0.17 (1.97) 0.79 0.45 0.583 Decreased initiative, motivation 2.63 (1.48) 3.02 (1.68) 0.39 (2.15) 1.07 0.29 0.253 Suspiciousness 1.88 (1.47) 2.07 (1.56) 0.20 (2.18) 0.88 0.49 0.570 Fatiguability 3.24 (1.37) 3.34 (1.46) 0.10 (2.08) 0.76 0.56 0.766 Hallucinatory behaviour 1.15 (0.69) 1.12 (0.78) 0.02 (1.06) 0.31 0.36 0.884 Motor retardation 2.34 (1.44) 2.41 (1.66) 0.07 (2.09) 0.73 0.59 0.824 Unusual thought content 1.05 (0.31) 1.39 (1.22) 0.34 (1.28) 0.74 0.06 0.095 Blunted affect 1.90 (1.61) 2.51 (1.55) 0.61 (2.35) 1.35 0.13 0.105 Excitement 2.29 (1.74) 3.00 (2.01) 0.71 (2.24) 1.41 0.00 0.050 Poor planning 2.68 (1.78) 3.37 (1.93) 0.68 (2.57) 1.50 0.13 0.097 Lability of mood 2.34 (1.70) 2.44 (1.82) 0.10 (2.20) 0.79 0.60 0.778 Tension 2.07 (1.60) 2.56 (1.76) 0.49 (2.41) 1.25 0.27 0.202 Comprehension deficit 2.12 (1.81) 2.37 (1.71) 0.24 (2.79) 1.12 0.64 0.579 Speech articulation deficit 1.85 (1.35) 1.51 (1.27) 0.34 (1.77) 0.22 0.90 0.224