http://informahealthcare.com/bij ISSN: 0269-9052 (print), 1362-301X (electronic) Brain Inj, 2014; 28(13–14): 1744–1747 ! 2014 Informa UK Ltd. DOI: 10.3109/02699052.2014.947621
ORIGINAL ARTICLE
A Spanish validation of the Coma Recovery Scale-Revised (CRS-R) Mercedes Tamashiro1, Maria Elisa Rivas1, Melania Ron2, Fernando Salierno1, Marisol Dalera2, & Lisandro Olmos3 Department of Physical Therapy and 2Department of Occupational Therapy, and 3Department of Rehabilitation Medicine, FLENI Rehabilitation Institute, Escobar, Argentina
Brain Inj Downloaded from informahealthcare.com by Nyu Medical Center on 06/19/15 For personal use only.
1
Abstract
Keywords
Research design: Analysis of inter-rater reliability and concurrent validity. Objective: To determine measurement properties of a Spanish version of The Coma Recovery Scale-Revised (CRS-R). Methods and procedures: A sample of 35 in-patients with severe acquired brain injury. To test concurrent validity of the translated scale, the Glasgow Coma Scale (GSC) and Disability Rating Scale (DRS) were also administered. Two experts in the field were recruited to assess inter-rater agreement. Results: Inter-rater reliability was good for total CRS-R scores (Cronbach ¼ 0.973, p ¼ 0.001). Sub-scale analysis showed moderate-to-high inter-rater agreement. Total CRS-R scores correlated significantly (p50.05) with total GCS (r ¼ 0.74) and DRS (r ¼ 0.54) scores, indicating acceptable concurrent validity. Conclusions: The Spanish version of CRS-R can be administered reliably by trained and experienced examiners. CRS-R appears capable of differentiating patients in Emergence from Minimally Conscious State (EMCS) or in Minimally Conscious State (MCS) from those in a Vegetative State (VS).
Assessment scale, coma, Coma-Recovery Scale revised, disorders of consciousness, minimally conscious state, vegetative state
Introduction In recent years, improvements in intensive care patient management have increased the number of individuals surviving severe acute brain injuries. Although most patients recover from coma within the first days of head trauma, others remain in ‘wakeful unawareness’ or in a vegetative state (VS). Clinically, recognizing unambiguous signs of conscious perception of the environment or of the self in such patients can be extremely challenging. This difficulty is reflected in frequent misdiagnosis of the condition and in confusion between vegetative state and other related conditions such as minimally conscious state (MCS) and locked-in syndrome [1–4]. Several scales have been developed to assess the degree of consciousness. Among the most widely used are: the Glasgow Coma Scale, the Disability Rating Scale and the Wessex Head Injury Matrix (WHIM). The Glasgow Coma Scale was developed to evaluate patients during acute stages following severe head trauma, to determine the extent of brain injury. The WHIM monitors patient recovery from coma until consciousness and the Disability Rating Scale measures progress over time during recovery from coma up until community integration [5]. Correspondence: Mercedes Tamashiro, FLENI Institute, Ruta 9 Km 52,5 (B1625XAF) Escobar, Pcia de Buenos Aires, Argentina. Tel/Fax: +5411 3488 410000. E-mail: [email protected]
History Received 24 October 2013 Revised 9 May 2014 Accepted 20 July 2014 Published online 29 September 2014
In 1991 Giacino et al. [6] published the Coma Recovery Scale. An updated version of the scale was later published by Giacino and Kalmar [7] in 2004 as the Coma Recovery ScaleRevised. CRS-R is based on Aspen Work Group criteria. It is a reliable tool, able to distinguish between patients in MCS and VS. Psychometric properties of the scale have also been studied. Inter-rater reliability is good, indicating reproducibility between examiners. Test–re-test reliability is also good, indicating stability after a 36-hour interval between evaluations. Concurrent validity was established in relation to the Disability Recovery Scale [8]. Use of the Coma Recovery Scale-Revised is recommended when diagnosing disorders of consciousness after coma, rather than performing an unstructured clinical assessment. The scale has been shown to be more sensitive than other previously developed scales for assessing patients with disorders of consciousness [5]. This study considers a reliable and valid Spanish version of CRS-R is needed for use in clinical practice and research. The scale is currently available in English, French and Italian [7, 9, 10] but not in Spanish. A version for Spanish-speaking countries following the same criteria used in the original would be beneficial to clinicians. The present study, therefore, explored concurrent validity, inter-rater agreement and diagnostic sensitivity of a Spanish version of CRS-R and compared it to other coma scales, namely GCS and DRS.
Spanish version of the CRS-R
DOI: 10.3109/02699052.2014.947621
Methods Translation The original CRS-R was translated into Spanish by experienced and trained clinicians, with back translation completed by a registered medical English translator based on the final Spanish version (See Spanish version of CRS-R in Appendix 1).
Brain Inj Downloaded from informahealthcare.com by Nyu Medical Center on 06/19/15 For personal use only.
Subjects A convenience sample of 35 inpatients was included. Participants were actively involved in a Sensory–Motor Stimulation Programme (SSMP). Inclusion criteria required were the absence of centrally acting drugs, neuromuscular blockers or sedation within 24 hours prior to evaluation and diagnosis established according to international criteria consistent with: (a) vegetative state or (b) minimally conscious state. Table I describes patient characteristics. Diagnoses included 24 patients with sustained TBI, six with hypoxicischaemic brain injury, four with stroke and one tumour. Median age was 30 (range ¼ 18–62 years) and 23 were men. Median time elapsed since occurrence of trauma was 146 days (range ¼ 28–1154). Mean CRS-R score was 9.31 (SD ¼ 4.4) and mean DRS ¼ 23.20 (SD ¼ 1.9). The Institutional Ethics Committee approved the research protocol and informed consent was obtained from each subject and/or legal guardian. Procedure Two professionals, a physiotherapist (PT) and an occupational therapist (OT), from FLENI Escobar Rehabilitation Center were recruited to assess inter-rater agreement. Both had extensive experience working with post-coma patients as well as applying the CRS-R. Nevertheless, prior to participation in this reliability study, raters were re-trained in CRS-R scale use. Videotapes on administration procedure for each item, as well as observations with real patients, were used for re-training, after which a scoring exercise conducted from videos, showing three patients being administered each item successively. Participants were asked to score each item administered. Table I. Demographic characteristics of patients. Characteristic
Median
Age (y) Days postinjury
30 146 n
Gender Males Females Etiology TBI Anoxia Tumor Stroke CRS-R total score DRS total score SD, standard deviation.
Range 18–62 28–1154
23 12 24 6 1 4 Mean (SD) 9.31 (4.39) 23.20 (1.89)
1745
Videotape assessment scoring was used in the present study. Inter-rater agreement: CRS-R was administered to all patients by the same two raters. Both the PT and OT were senior staff members, with over 7 years experience in coma rehabilitation [11]. Each rater recorded patient responses independently during the examination and scored CRS-R sub-scales immediately on completion. Raters also entered diagnoses of VS, MCS or EMCS based on the CRS-R Response Profile. Concurrent validity: To investigate validity, total CRS-R scores were compared to total DRS and GCS scores. GCS scores represent the sum of three sub-scores (eye opening subscale, motor sub-scale and verbal response scale) and results range from 3 for worst to 15 for best clinical outcome [12]. The DRS scale was originally developed to accurately measure general functional changes over the course of recovery, in individuals with moderate-to-severe traumatic brain injury (TBI). One advantage of the DRS is its ability to track individual patient course from coma right up until re-insertion into the community. The maximum score a patient can obtain on the DRS is 29 (extreme vegetative state). A person with no disability would score zero. DRS is a widely used scale in rehabilitation settings and its psychometric characteristics have been well-described [13]. CRS-R consists of 29 hierarchically organized items divided into six sub-scales addressing auditory, visual, motor, oromotor, communication and arousal processes. The lowest item on each sub-scale represents reflexive activity and the highest item cognitively mediated behaviour. Scoring is based on presence or absence of specific responses to standardized stimuli. Total scores range from 0 as the worst and 23 points as the best result. Statistical analyses Concurrent validity was determined by comparing total CRS-R scores to total GCS and DRS scores. Inter-correlation between scores of the three scales was calculated by applying the Spearman rank correlation method. To investigate interrater reliability, a Cronbach -test was used to determine reproducibility of total CRS-R and a Cohen for sub-scale scores. Kappa scores significance is established at values of 0.4 or less for poor results, 0.4–0.6 for fair-to-moderate, 0.6–0.8 for good and 40.8 for excellent inter-rater agreement. Total Cohen scores could not be calculated in this sample because of the low frequency or absence of some scores, as evidenced in the data distribution histogram. Additionally, the Paired Samples t-test was calculated to compare total scores obtained by different raters. Diagnostic agreement was also calculated using Kappa analysis to establish the degree to which raters agreed patient responses were indicative of VS or MCS. Chi-square analysis was performed to compare divergent diagnosis frequency between raters.
Results Concurrent validity (18–27)
Total CRS-R scores were correlated with total GCS and DRS scores to establish concurrent validity. Spearman coefficients were significant between CRS-R and GCS (r ¼ 0.74,
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Brain Inj, 2014; 28(13–14): 1744–1747
p50.001) as well as between CRS-R and DRS (r ¼ 0.54, p ¼ 0.001).
However, there were 14 cases in which CRS-R diagnosis was indicative of MCS, whereas DRS diagnosis was indicative of VS (see Table IV).
Brain Inj Downloaded from informahealthcare.com by Nyu Medical Center on 06/19/15 For personal use only.
Inter-rater agreement No significant difference in total scores obtained by different rates (p ¼ 0.81) was observed. Inter-rater reliability for total CRS-R score was high (Cronbach ¼ 0.973, p ¼ 0.001), indicating the scale yields reproducible findings across examiners. For inter-rater reliability analysis of each subscale, mean kappa values were obtained. Kappa values were good for auditory ( ¼ 0.78), visual ( ¼ 0.77) and communication ( ¼ 0.78) sub-scales; moderate for motor ( ¼ 0.56) and poor for oromotor ( ¼ 0.36) sub-scales. However, the Kappa coefficient could not be calculated due to infrequent scoring results available on the arousal sub-scale (Table II). Diagnoses established by raters A and B showed significant correlation ( ¼ 0.79, p50.001), indicating examiners clearly distinguished between VS, MCS and MCS+ using CRS-R. Raters agreed on diagnosis in 31 of 35 patients examined. Of the four cases in which raters disagreed on diagnosis, two involved a discrepancy between MCS and EMCS and two between VS and MCS. 2 ¼ 37.54; p50.001 (Table III). Frequency of diagnostic agreement between CRS-R and DRS is shown in Table IV. In six of 35 patients assessed, both scales indicated diagnosis of MCS. An additional 15 patients were diagnosed as VS by both scales. There were no cases in which DRS favoured MCS diagnosis, but CRS-R did not. Table II. Inter-rater reliability of CRS-R sub-scale scores. CRS-R subscale
Kappa Coef.
p Value
Auditive Visual Motor Oromotor/verbal Communication Arousal
0.78 0.77 0.57 0.37 0.78 *n/a
0.000 0.000 0.000 0.001 0.000 *n/a
*Not applicable.
Table III. Frequency of inter-rater agreement in diagnosis. Rater 1
Rater 2 VS MCS MCS+ Total
VS
MCS
MCS+
Total
13 1 0 14
1 17 2 20
0 0 1 1
14 18 3 35
Table IV. Frequency of diagnosis agreement between CRS-R and DRS. DRS CRS-R
MCS
VS
Total
MCS VS Total
6 0 6
14 15 29
20 15 35
Discussion The essential aim of this study was to determine diagnostic accuracy of a Spanish version of CRS-R. Results indicate that the translated version is reliable and generates valid measures of neurobehavioural responsiveness. Inter-rater reliability was high for total CRS-R scores. The findings showed low agreement between raters on the oromotor/verbal sub-scale, in agreement with the original version [7]. In this study cohort, no patients rated 3 (a result denoting MCS with intelligible verbalization) and low agreement (28%) was observed on reflex movements for scores of 1 and 2. Frequently, patients with disorders of consciousness may present different oromandibular movements including suction, chewing, bruxism or generating guttural vocal sounds [14]. All these responses represent forms of reflex movement and may give rise to score discrepancies, as raters may assign them 1 or 2 points on the oromotor scale. In the study on Coma Recovery Scale reliability by O’Dell et al. [15], the authors suggested that the relatively low agreement among raters on this sub-scale was due to lack of specialized training in oromotor function assessment. Investigation of individual sub-scale score reliability was limited by the restricted range of scores for some items. In the case of the arousal sub-scale, for example, it was uncommon to find high and low end scores. In the original version this sub-scale was eliminated from the analysis because arousal scores were not considered useful for differential diagnosis [7]. The present study used videotape assessments for scoring patients, eliminating any influence of arousal fluctuations as the same videotape was analysed by each rater. In this study, disagreement between VS and MCS was observed in two cases. In one case, one rater observed painful stimulus localization and the second interpreted flexion withdrawal. In the other case, one rater observed fixation and the second visual startle. In both cases patients were diagnosed as being in MCS because of their unique behavioural interaction with the external environment. Disagreement between raters on a single item of the scale, however, ultimately changed patient diagnosis. In these two cases, in which patients presented minimal level of interaction without following commands, MCS minus may be diagnosed. Recently, a proposal to sub-categorize MCS patients based on the complexity of their behaviour into two entities: ‘MCS minus’ (MCS) and ‘MCS plus’ (MCS+) [16] has been recommended. MCS+ corresponds to high level behavioural response such as command following, intelligible verbalizations or non-functional communication; and MCS shows only minimal levels of behavioural interaction characterized by non-reflex movements such as orientation of noxious stimuli, pursuit eye movements occurring in direct response to moving or salient stimuli and movements or affective behaviours occurring appropriately in relation to relevant environmental stimuli. Although the scale showed
DOI: 10.3109/02699052.2014.947621
high inter-rater reliability for diagnostic criteria, future research might consider incorporation of this MCS subcategorization, to better approximate clinical patient diagnosis. In one case, lack of agreement between raters was observed; one rater diagnosed MCS and the other EMCS. This was due to difficulty rating functional use of objects following the original scale protocol. The video shows the patient managing to make proper functional use of an object twice; however, correct use of a second object was doubtful, so that one rater scored 5 and the other 6 on the motor sub-scale. Diagnostic agreement levels between CRS-R and DRS show CRS-R is more sensitive to detect patients in MCS than DRS.
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Conclusion The steady rise in numbers of patients hospitalized in VS or MCS is a burden to health systems worldwide, requiring more specific programmes and therapeutic approaches to diagnose and treat them. The CRS-R published by Giacino et al. [7] is considered as the best tool to assess and treat different states of consciousness, because of its sensitivity in differentiating between patients in coma, VS, MCS and EMCS. Having this assessment tool available in Spanish will be useful both for future scientific research in Spanish speaking countries as well as for wider use of the scale in certain regions. This study suggests the Spanish version of the CRS-R is a valid scale for use during acute and chronic stages of patient recovery that can be administered reliably by all trained and experimented members of the rehabilitation staff.
Declaration of interest The authors report no conflicts of interest. The authors alone are responsible for the content and writing of the paper.
References 1. Andrews K, Murphy L, Munday R, Littlewood C. Misdiagnosis of the vegetative state: retrospective study in a rehabilitation unit. British Medical Journal 1996;313:13–16. 2. Childs NL, Mercer WN, Childs HW. Accuracy of diagnosis of persistent vegetative state. Neurology 1993;43:1465–1467.
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3. Giacino J, Zasler ND. Outcome after severe brain injury: coma, vegetative state and the minimally responsive state. Journal of Head Trauma & Rehabilitation 1995;10:44–61. 4. Giacino JT, Ashwal S, Child SN, Cranford R, Jennett B, Katz DI, Kelly JP, Rosenberg JH, Whyte J, Zafonte RD, et al. The minimally conscious state: definition and diagnostic criteria. Neurology 2002; 58:349–353. 5. American Congress of Rehabilitation Medicine, Brain InjuryInterdisciplinary Special Interest Group, Disorders of Consciousness Task Force, Seel RT, Sherer M, Whyte J, Katz DI, Giacino JT, Rosenbaum AM, Hammond FM, Kalmar K, Pape TL, Zafonte R, et al. Assessment scales for disorders of consciousness: evidence-based recommendations for clinical practice and research. Archives of Physical Medicine & Rehabilitation 2010;91: 1795–1813. 6. Giacino JT, Kezmarsky MA, DeLuca J, Cicerone KD. Monitoring rate of recovery to predict outcome in minimally responsive patients. Archives of Physical Medicine & Rehabilitation 1991;72: 897–901. 7. Giacino JT, Kalmar K, Whyte J. The JFK Coma Recovery ScaleRevised: measurement characteristics and diagnostic utility. Archives of Physical Medicine & Rehabilitation 2004;85: 2020–2029. 8. Kalmar K, Giacino JT. The JFK Coma Recovery Scale–Revised. Neuropsychological Rehabilitation 2005;15:454–460. 9. Sacco S, Altobelli E, Pistarini C, Cerone D, Cazzulani B, Carolei A. Validation of the Italian version of the Coma Recovery Scale-Revised (CRS-R). Brain Injury 2011;25:488–495. 10. Schnakers C, Majerus S, Giacino J, Vanhaudenhuyse A, Bruno MA, Boly M, Moonen G, Damas P, Lambermont B, Lamy M, et al. A French validation study of the Coma Recovery Scale-Revised (CRS-R). Brain Injury 2008;22:786–792. 11. Løvstad M, Frøslie K, Giacino JT, Skandsen T, Anke A, Schanke A. Reliability and Diagnostic Characteristics of the JFK Coma Recovery Scale-Revised: exploring the influence of Rater’s Level of Experience. Journal of Head Trauma Rehabilitation 2010;25: 349–356. 12. Teasdale G, Jennett B. Assessment of coma and impaired consciousness. A practical scale. Lancet 1974;2:81–84. 13. Rappaport M, Hall KM, Hopkins K, Belleza T, Cope DN. Disability Rating Scale for severe head trauma coma to community. Archives of Physical Medicine & Rehabilitation 1982;63:118–123. 14. Tamashiro M, Cozzo D, Mattei M, Salierno F, Rivas ME, Alzu´a O, Olmos L, Bonamico L, Leiguarda R. Early motor predictors of recovery in patients with severe traumatic brain injury. Brain Injury 2012;26:921–926. 15. O’Dell MW, Jasin P, Stivers M, Lyons N, Schmidt S, Moore DE. Interrater Reliability of the Coma Recovery Scale. Journal of Head Trauma & Rehabilitation 1996;11:61–66. 16. Bruno MA, Vanhaudenhuyse A, Thibaut A, Moonen G, Laureys S. From unresponsive wakefulness to minimally conscious PLUS and functional locked-in syndromes: recent advances in our understanding of disorders of consciousness. Journal of Neurology 2011; 258:1373–1384.
ORIGINAL ARTICLE
A Spanish validation of the Coma Recovery Scale-Revised (CRS-R) Mercedes Tamashiro1, Maria Elisa Rivas1, Melania Ron2, Fernando Salierno1, Marisol Dalera2, & Lisandro Olmos3 Department of Physical Therapy and 2Department of Occupational Therapy, and 3Department of Rehabilitation Medicine, FLENI Rehabilitation Institute, Escobar, Argentina
Brain Inj Downloaded from informahealthcare.com by Nyu Medical Center on 06/19/15 For personal use only.
1
Abstract
Keywords
Research design: Analysis of inter-rater reliability and concurrent validity. Objective: To determine measurement properties of a Spanish version of The Coma Recovery Scale-Revised (CRS-R). Methods and procedures: A sample of 35 in-patients with severe acquired brain injury. To test concurrent validity of the translated scale, the Glasgow Coma Scale (GSC) and Disability Rating Scale (DRS) were also administered. Two experts in the field were recruited to assess inter-rater agreement. Results: Inter-rater reliability was good for total CRS-R scores (Cronbach ¼ 0.973, p ¼ 0.001). Sub-scale analysis showed moderate-to-high inter-rater agreement. Total CRS-R scores correlated significantly (p50.05) with total GCS (r ¼ 0.74) and DRS (r ¼ 0.54) scores, indicating acceptable concurrent validity. Conclusions: The Spanish version of CRS-R can be administered reliably by trained and experienced examiners. CRS-R appears capable of differentiating patients in Emergence from Minimally Conscious State (EMCS) or in Minimally Conscious State (MCS) from those in a Vegetative State (VS).
Assessment scale, coma, Coma-Recovery Scale revised, disorders of consciousness, minimally conscious state, vegetative state
Introduction In recent years, improvements in intensive care patient management have increased the number of individuals surviving severe acute brain injuries. Although most patients recover from coma within the first days of head trauma, others remain in ‘wakeful unawareness’ or in a vegetative state (VS). Clinically, recognizing unambiguous signs of conscious perception of the environment or of the self in such patients can be extremely challenging. This difficulty is reflected in frequent misdiagnosis of the condition and in confusion between vegetative state and other related conditions such as minimally conscious state (MCS) and locked-in syndrome [1–4]. Several scales have been developed to assess the degree of consciousness. Among the most widely used are: the Glasgow Coma Scale, the Disability Rating Scale and the Wessex Head Injury Matrix (WHIM). The Glasgow Coma Scale was developed to evaluate patients during acute stages following severe head trauma, to determine the extent of brain injury. The WHIM monitors patient recovery from coma until consciousness and the Disability Rating Scale measures progress over time during recovery from coma up until community integration [5]. Correspondence: Mercedes Tamashiro, FLENI Institute, Ruta 9 Km 52,5 (B1625XAF) Escobar, Pcia de Buenos Aires, Argentina. Tel/Fax: +5411 3488 410000. E-mail: [email protected]
History Received 24 October 2013 Revised 9 May 2014 Accepted 20 July 2014 Published online 29 September 2014
In 1991 Giacino et al. [6] published the Coma Recovery Scale. An updated version of the scale was later published by Giacino and Kalmar [7] in 2004 as the Coma Recovery ScaleRevised. CRS-R is based on Aspen Work Group criteria. It is a reliable tool, able to distinguish between patients in MCS and VS. Psychometric properties of the scale have also been studied. Inter-rater reliability is good, indicating reproducibility between examiners. Test–re-test reliability is also good, indicating stability after a 36-hour interval between evaluations. Concurrent validity was established in relation to the Disability Recovery Scale [8]. Use of the Coma Recovery Scale-Revised is recommended when diagnosing disorders of consciousness after coma, rather than performing an unstructured clinical assessment. The scale has been shown to be more sensitive than other previously developed scales for assessing patients with disorders of consciousness [5]. This study considers a reliable and valid Spanish version of CRS-R is needed for use in clinical practice and research. The scale is currently available in English, French and Italian [7, 9, 10] but not in Spanish. A version for Spanish-speaking countries following the same criteria used in the original would be beneficial to clinicians. The present study, therefore, explored concurrent validity, inter-rater agreement and diagnostic sensitivity of a Spanish version of CRS-R and compared it to other coma scales, namely GCS and DRS.
Spanish version of the CRS-R
DOI: 10.3109/02699052.2014.947621
Methods Translation The original CRS-R was translated into Spanish by experienced and trained clinicians, with back translation completed by a registered medical English translator based on the final Spanish version (See Spanish version of CRS-R in Appendix 1).
Brain Inj Downloaded from informahealthcare.com by Nyu Medical Center on 06/19/15 For personal use only.
Subjects A convenience sample of 35 inpatients was included. Participants were actively involved in a Sensory–Motor Stimulation Programme (SSMP). Inclusion criteria required were the absence of centrally acting drugs, neuromuscular blockers or sedation within 24 hours prior to evaluation and diagnosis established according to international criteria consistent with: (a) vegetative state or (b) minimally conscious state. Table I describes patient characteristics. Diagnoses included 24 patients with sustained TBI, six with hypoxicischaemic brain injury, four with stroke and one tumour. Median age was 30 (range ¼ 18–62 years) and 23 were men. Median time elapsed since occurrence of trauma was 146 days (range ¼ 28–1154). Mean CRS-R score was 9.31 (SD ¼ 4.4) and mean DRS ¼ 23.20 (SD ¼ 1.9). The Institutional Ethics Committee approved the research protocol and informed consent was obtained from each subject and/or legal guardian. Procedure Two professionals, a physiotherapist (PT) and an occupational therapist (OT), from FLENI Escobar Rehabilitation Center were recruited to assess inter-rater agreement. Both had extensive experience working with post-coma patients as well as applying the CRS-R. Nevertheless, prior to participation in this reliability study, raters were re-trained in CRS-R scale use. Videotapes on administration procedure for each item, as well as observations with real patients, were used for re-training, after which a scoring exercise conducted from videos, showing three patients being administered each item successively. Participants were asked to score each item administered. Table I. Demographic characteristics of patients. Characteristic
Median
Age (y) Days postinjury
30 146 n
Gender Males Females Etiology TBI Anoxia Tumor Stroke CRS-R total score DRS total score SD, standard deviation.
Range 18–62 28–1154
23 12 24 6 1 4 Mean (SD) 9.31 (4.39) 23.20 (1.89)
1745
Videotape assessment scoring was used in the present study. Inter-rater agreement: CRS-R was administered to all patients by the same two raters. Both the PT and OT were senior staff members, with over 7 years experience in coma rehabilitation [11]. Each rater recorded patient responses independently during the examination and scored CRS-R sub-scales immediately on completion. Raters also entered diagnoses of VS, MCS or EMCS based on the CRS-R Response Profile. Concurrent validity: To investigate validity, total CRS-R scores were compared to total DRS and GCS scores. GCS scores represent the sum of three sub-scores (eye opening subscale, motor sub-scale and verbal response scale) and results range from 3 for worst to 15 for best clinical outcome [12]. The DRS scale was originally developed to accurately measure general functional changes over the course of recovery, in individuals with moderate-to-severe traumatic brain injury (TBI). One advantage of the DRS is its ability to track individual patient course from coma right up until re-insertion into the community. The maximum score a patient can obtain on the DRS is 29 (extreme vegetative state). A person with no disability would score zero. DRS is a widely used scale in rehabilitation settings and its psychometric characteristics have been well-described [13]. CRS-R consists of 29 hierarchically organized items divided into six sub-scales addressing auditory, visual, motor, oromotor, communication and arousal processes. The lowest item on each sub-scale represents reflexive activity and the highest item cognitively mediated behaviour. Scoring is based on presence or absence of specific responses to standardized stimuli. Total scores range from 0 as the worst and 23 points as the best result. Statistical analyses Concurrent validity was determined by comparing total CRS-R scores to total GCS and DRS scores. Inter-correlation between scores of the three scales was calculated by applying the Spearman rank correlation method. To investigate interrater reliability, a Cronbach -test was used to determine reproducibility of total CRS-R and a Cohen for sub-scale scores. Kappa scores significance is established at values of 0.4 or less for poor results, 0.4–0.6 for fair-to-moderate, 0.6–0.8 for good and 40.8 for excellent inter-rater agreement. Total Cohen scores could not be calculated in this sample because of the low frequency or absence of some scores, as evidenced in the data distribution histogram. Additionally, the Paired Samples t-test was calculated to compare total scores obtained by different raters. Diagnostic agreement was also calculated using Kappa analysis to establish the degree to which raters agreed patient responses were indicative of VS or MCS. Chi-square analysis was performed to compare divergent diagnosis frequency between raters.
Results Concurrent validity (18–27)
Total CRS-R scores were correlated with total GCS and DRS scores to establish concurrent validity. Spearman coefficients were significant between CRS-R and GCS (r ¼ 0.74,
1746
M. Tamashiro et al.
Brain Inj, 2014; 28(13–14): 1744–1747
p50.001) as well as between CRS-R and DRS (r ¼ 0.54, p ¼ 0.001).
However, there were 14 cases in which CRS-R diagnosis was indicative of MCS, whereas DRS diagnosis was indicative of VS (see Table IV).
Brain Inj Downloaded from informahealthcare.com by Nyu Medical Center on 06/19/15 For personal use only.
Inter-rater agreement No significant difference in total scores obtained by different rates (p ¼ 0.81) was observed. Inter-rater reliability for total CRS-R score was high (Cronbach ¼ 0.973, p ¼ 0.001), indicating the scale yields reproducible findings across examiners. For inter-rater reliability analysis of each subscale, mean kappa values were obtained. Kappa values were good for auditory ( ¼ 0.78), visual ( ¼ 0.77) and communication ( ¼ 0.78) sub-scales; moderate for motor ( ¼ 0.56) and poor for oromotor ( ¼ 0.36) sub-scales. However, the Kappa coefficient could not be calculated due to infrequent scoring results available on the arousal sub-scale (Table II). Diagnoses established by raters A and B showed significant correlation ( ¼ 0.79, p50.001), indicating examiners clearly distinguished between VS, MCS and MCS+ using CRS-R. Raters agreed on diagnosis in 31 of 35 patients examined. Of the four cases in which raters disagreed on diagnosis, two involved a discrepancy between MCS and EMCS and two between VS and MCS. 2 ¼ 37.54; p50.001 (Table III). Frequency of diagnostic agreement between CRS-R and DRS is shown in Table IV. In six of 35 patients assessed, both scales indicated diagnosis of MCS. An additional 15 patients were diagnosed as VS by both scales. There were no cases in which DRS favoured MCS diagnosis, but CRS-R did not. Table II. Inter-rater reliability of CRS-R sub-scale scores. CRS-R subscale
Kappa Coef.
p Value
Auditive Visual Motor Oromotor/verbal Communication Arousal
0.78 0.77 0.57 0.37 0.78 *n/a
0.000 0.000 0.000 0.001 0.000 *n/a
*Not applicable.
Table III. Frequency of inter-rater agreement in diagnosis. Rater 1
Rater 2 VS MCS MCS+ Total
VS
MCS
MCS+
Total
13 1 0 14
1 17 2 20
0 0 1 1
14 18 3 35
Table IV. Frequency of diagnosis agreement between CRS-R and DRS. DRS CRS-R
MCS
VS
Total
MCS VS Total
6 0 6
14 15 29
20 15 35
Discussion The essential aim of this study was to determine diagnostic accuracy of a Spanish version of CRS-R. Results indicate that the translated version is reliable and generates valid measures of neurobehavioural responsiveness. Inter-rater reliability was high for total CRS-R scores. The findings showed low agreement between raters on the oromotor/verbal sub-scale, in agreement with the original version [7]. In this study cohort, no patients rated 3 (a result denoting MCS with intelligible verbalization) and low agreement (28%) was observed on reflex movements for scores of 1 and 2. Frequently, patients with disorders of consciousness may present different oromandibular movements including suction, chewing, bruxism or generating guttural vocal sounds [14]. All these responses represent forms of reflex movement and may give rise to score discrepancies, as raters may assign them 1 or 2 points on the oromotor scale. In the study on Coma Recovery Scale reliability by O’Dell et al. [15], the authors suggested that the relatively low agreement among raters on this sub-scale was due to lack of specialized training in oromotor function assessment. Investigation of individual sub-scale score reliability was limited by the restricted range of scores for some items. In the case of the arousal sub-scale, for example, it was uncommon to find high and low end scores. In the original version this sub-scale was eliminated from the analysis because arousal scores were not considered useful for differential diagnosis [7]. The present study used videotape assessments for scoring patients, eliminating any influence of arousal fluctuations as the same videotape was analysed by each rater. In this study, disagreement between VS and MCS was observed in two cases. In one case, one rater observed painful stimulus localization and the second interpreted flexion withdrawal. In the other case, one rater observed fixation and the second visual startle. In both cases patients were diagnosed as being in MCS because of their unique behavioural interaction with the external environment. Disagreement between raters on a single item of the scale, however, ultimately changed patient diagnosis. In these two cases, in which patients presented minimal level of interaction without following commands, MCS minus may be diagnosed. Recently, a proposal to sub-categorize MCS patients based on the complexity of their behaviour into two entities: ‘MCS minus’ (MCS) and ‘MCS plus’ (MCS+) [16] has been recommended. MCS+ corresponds to high level behavioural response such as command following, intelligible verbalizations or non-functional communication; and MCS shows only minimal levels of behavioural interaction characterized by non-reflex movements such as orientation of noxious stimuli, pursuit eye movements occurring in direct response to moving or salient stimuli and movements or affective behaviours occurring appropriately in relation to relevant environmental stimuli. Although the scale showed
DOI: 10.3109/02699052.2014.947621
high inter-rater reliability for diagnostic criteria, future research might consider incorporation of this MCS subcategorization, to better approximate clinical patient diagnosis. In one case, lack of agreement between raters was observed; one rater diagnosed MCS and the other EMCS. This was due to difficulty rating functional use of objects following the original scale protocol. The video shows the patient managing to make proper functional use of an object twice; however, correct use of a second object was doubtful, so that one rater scored 5 and the other 6 on the motor sub-scale. Diagnostic agreement levels between CRS-R and DRS show CRS-R is more sensitive to detect patients in MCS than DRS.
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Conclusion The steady rise in numbers of patients hospitalized in VS or MCS is a burden to health systems worldwide, requiring more specific programmes and therapeutic approaches to diagnose and treat them. The CRS-R published by Giacino et al. [7] is considered as the best tool to assess and treat different states of consciousness, because of its sensitivity in differentiating between patients in coma, VS, MCS and EMCS. Having this assessment tool available in Spanish will be useful both for future scientific research in Spanish speaking countries as well as for wider use of the scale in certain regions. This study suggests the Spanish version of the CRS-R is a valid scale for use during acute and chronic stages of patient recovery that can be administered reliably by all trained and experimented members of the rehabilitation staff.
Declaration of interest The authors report no conflicts of interest. The authors alone are responsible for the content and writing of the paper.
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