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DOI: 10.1055/s-0044-1791657
Validation to Brazilian Portuguese of the coma recovery scale-revised
Validação para o português brasileiro da escala de recuperação do coma-revisadaAbstract
Background To improve the diagnostic accuracy of the state of consciousness of patients with severe brain injury, Giacino et al. introduced the Coma Recovery Scale (CRS) in 1991, which underwent revision in 2004, resulting in the revised CRS scale (CRS-R).
Objective To determine the concurrent validity, as well as inter- and intrarater agreement of the CRS-R's adaptation to Brazilian Portuguese.
Methods This study involved a sample of 30 patients with severe brain injury. Concurrent evaluations were also performed with the Glasgow Coma Scale (GCS) and the Full Outline of UnResponsiveness (FOUR) scale. A total of seven rehabilitation experts were recruited to assess the inter- and intrarater reliability agreement.
Results Interrater reliability was moderate to high for auditory, visual, motor, verbal, communication, and arousal subscales (Cohen weighted kappa = 0.765 to 0.892; p < 0.001). Significant inter and intrarater intraclass correlation coefficients were observed for the total CRS-R scores, all of which were statistically significant (p < 0.001). Also, total CRS-R scores exhibited a high correlation with the total GCS and FOUR scores, indicating acceptable concurrent validity (p < 0.001).
Conclusion The Brazilian Portuguese version of CRS-R can be reliably administered by trained examiners. This study demonstrated substantial to almost perfect interrater agreement for the total score and subscales, as well as high concurrent validity between the Brazilian Portuguese version of CRS-R and the other two standardized behavioral scales.
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Resumo
Antecedentes Para melhorar a acurácia diagnóstica do estado da consciência de pacientes com lesão cerebral severa, foi desenvolvida a Escala de Recuperação do Coma em 1991, que passou por revisão em 2004, resultando na escala revisada (CRS-R).
Objetivo Determinar a validade concorrente, concordância inter- e intraexaminador da adaptação da CRS-R para o português do Brasil.
Métodos Este estudo envolveu uma amostra de 30 pacientes com lesão cerebral grave. As avaliações concorrentes foram realizadas com a Escala de Coma de Glasgow (ECG) e a escala Full Outline of UnResponsiveness (FOUR). Um total de sete especialistas em reabilitação foram recrutados para avaliar a concordância de confiabilidade inter- e intraexaminador.
Resultados A confiabilidade interexaminador foi de moderada a alta para as subescalas auditiva, visual, motora, verbal, comunicação e alerta (kappa ponderado de Cohen = 0,765 a 0,892; p < 0,001). Foram observados coeficientes de correlação intraclasse intra- e interexaminador significativos para os escores totais da CRS-R, todos estatisticamente significativos (p < 0,001). Adicionalmente, os escores totais da CRS-R apresentaram alta correlação com os escores ECG e FOUR totais, indicando validade concorrente aceitável (p < 0,001).
Conclusão A versão em português do Brasil da CRS-R pode ser administrada de forma confiável por examinadores treinados. Este estudo demonstrou uma concordância de confiabilidade interexaminador substancial a quase perfeita para os escores total e de subescalas, assim como alta validade concorrente entre a versão brasileira do CRS-R e as outras duas escalas comportamentais.
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INTRODUCTION
Severe brain injuries from trauma, infections/inflammation, or vascular events significantly impact patients and their families, resulting in the need for complex care and prompting transformative changes in their lives. With improved access to care resources like emergency services and rehabilitation departments, the survival rates of patients bearing sequelae of such injuries have increased. One of the foremost clinical challenges for these patients is evaluating consciousness, especially in those who appear nonresponsive.[1]
Although most patients with brain injuries emerge from coma within days, some can progress to a complete loss of brain functions. Furthermore, others may display varying degrees of interaction with their surroundings or undergo different recovery phases before achieving complete or partial restoration of consciousness.[2] [3] [4] [5]
Disorders of Consciousness (DoC) are typically described as extended states of altered consciousness, evident after 28 days postbrain injury.[6] [7] The spectrum includes conditions ranging from coma to full consciousness. For instance, individuals described as being in a vegetative state (VS) or unresponsive wakefulness syndrome (UWS) are conscious but unaware.[6] [7] [8] Minimally conscious state (MCS) individuals exhibit limited but consistent awareness of themselves or their environment. Those in the minimally conscious state minus (MCS-) only show voluntary responses to nociceptive stimuli and can visually fixate on objects without localization.[9] [10] Conversely, minimally conscious state plus (MCS + ) patients can follow commands, produce intelligible speech, and establish purposeful communication.[11] Emergence from MCS (eMCS) signifies a functional use of objects and communication abilities.[6] [7] The locked-in syndrome is characterized by awareness of one's surroundings, sustained eye-opening, and specific eye movements as a communication means.[11] [12] [13] In rarer cases, a dissociated cognitive state, for example, the functional locked-in syndrome, manifests when patients do not seem to follow commands yet demonstrate brain activity in complementary exams, such as somatosensory potential and video-electroencephalogram.[11] [12] [13]
Preserving a patient's autonomy is paramount. However, envision a scenario where an individual cannot eat, drink, speak, or communicate. If even their families are uncertain about their state of consciousness, the situation becomes profoundly distressing. This underscores the importance of detecting consciousness in noncommunicative patients with severe brain injuries. Misdiagnoses can be catastrophic. To enhance diagnostic accuracy, several scales have been developed. Notably, Giacino et al. introduced the coma recovery scale (CRS) in 1991, which underwent revision in 2004, resulting in a revised scale (CRS-R).[14] [15]
The CRS-R is a comprehensive tool that evaluates various consciousness states, aiding in both diagnosis and prognosis. Standardizing data fosters consistent information sharing and comparative studies across nations. The scale evaluates auditory, visual, verbal, and motor functions, communication, and arousal levels. Its total score can range from 0 (worst) to 23 (best).[15]
This research endeavors to translate and validate the 2004 version of CRS-R for the Brazilian Portuguese language.
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METHODS
Translation and back translation
The original scale's creators authorized its translation from English to Brazilian Portuguese. The initial version was done by three independent bilingual translators. Subsequently, they collaborated to formulate a consensus version of the scale, which was then back-translated by two additional bilingual translators. Upon completing the backwards translation, both the original authors and the research group reviewed it for accuracy, culminating in the development of the CRS-R or, in Portuguese, Escala de Recuperação do Coma-Revisada (ERC-R) ([Supplementary Material S1] - https://www.arquivosdeneuropsiquiatria.org/wp-content/uploads/2024/07/ANP-2023.0315-Supplementary-Material.docx, online only).
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Participants
Individuals were recruited from a Brazilian network of rehabilitation hospitals during their rehabilitation programs. Inclusion criteria were a diagnosis of brain injury and a suspected altered state of consciousness. Those with neurological disorders unrelated to brain injury were excluded. A total of 30 consecutive patients with severe brain injuries were included in the study. Clinical and epidemiological data were extracted from medical records. Legal guardians of all participants provided written consent, following approval from the ethical review board of the Network of Rehabilitation Hospitals (CAAE 35466920.7.1001.0022) in Belo Horizonte, Brazil.
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Procedures
There were seven professionals from three units of a Brazilian Network of Rehabilitation Hospitals centers who participated to assess interrater agreements, with three from Belo Horizonte, two from, and two from Rio de Janeiro. The group consisted of internal medicine physicians (n = 3), a physiotherapist (n = 1), and neurologists (n = 3). These professionals underwent training in using the CRS-R scale, utilizing a video ([Supplementary Material S2] - https://www.sralab.org/sites/default/files/downloads/2020-09/Training_Modules_20200831_v1.pdf) that demonstrated the administration procedures for each item with real patients (online only).
Following training, the professionals' assessment protocol was:
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Day 1: Rater A and Rater B independently administered the Brazilian-Portuguese version of the scale (∼1 hour apart) to evaluate inter-rater reliability.
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Day 2: Rater A (or Rater B) re-administered the Brazilian-Portuguese version to assess test-retest reliability.
Raters A and B were blinded to each other's evaluations during this process.
The CRS-R total scores were compared with total scores from the Glasgow coma scale (GCS) and full outline of unresponsiveness (FOUR) scale to determine concurrent validity.
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Data analysis
Data analysis was conducted using the R software (R Foundation for Statistical Computing, Vienna, Austria), version 4.1.2, with a significance level of 0.05. Descriptive statistics were employed to describe the clinical and epidemiological characteristics of the participants. Interrater reliability was assessed using the Cohen kappa tests.[16] This test measured the reproducibility of CRS-R's total and subscale scores across different raters. The agreement coefficients resulting from the kappa tests were categorized as follows: poor < 0; slight = 0.01 to 0.19; fair = 0.20 to 0.39; moderate = 0.40 to 0.59; substantial = 0.60 to 0.79; and almost perfect = 0.80 to 1.00.[16] For concurrent validity, scores from the three scales (CRS-R, GCS, and FOUR) were analyzed using Spearman correlation. The alpha level was 0.05.
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RESULTS
A total of 30 patients with severe brain injury, suspected of having altered states of consciousness, were evaluated. Of these patients, 70% were male, with an average age of 29.5 ± 9.8 years. In terms of states of consciousness, 34.4% patients were diagnosed with a VS/UWS, 41.3% as MCS -, 6.8% as MCS +, and five patients had emerged from MCS. On average, the duration since brain injury onset, or ictus, was 12 months.
Trauma was the cohort's leading cause of brain injury, accounting for 70%, followed by anoxia with 23.3% of cases. Surgical intervention, either in the form of a craniotomy or craniectomy, was undergone by 23.3% of the patients. Neurologically, 89.5% of the patients exhibited reactive pupils, 98.6% had a corneal reflex, 68.1% displayed skew or conjugate deviation, 20.6% showed abnormal flexion, and 96.4% presented spasticity. Other accompanying symptoms included constipation (50%), seizures (30%), pain (26.6%), sleep disturbances (53%), and sialorrhea (12.5%). Further details can be found in [Table 1].
Abbreviations: CRS-R, Coma Recovered Scale Revised; eMCS, emergence from minimally conscious state; FOUR, Full Outline of UnResponsiveness; MCS-, minimally conscious state minus; MCS + , Minimally Conscious State Plus; SD, standard deviation; VS/UWS, vegetative state/unresponsive wakefulness syndrome. Notes: † In months. ‡ Day 1, rater A.
Intrarater reliability for CRS-R auditory, visual, motor, oromotor/verbal, communication, and arousal subscales ranged from strong to almost perfect (weighted kappa: 0.828–0.993; p < 0.001). The total score also demonstrated significant reliability with a kappa value of 0.97. In the interrater analysis, the subscales showed moderate to strong (weighted kappa: 0.69–0.87; p < 0.001), with the total score having a kappa value of 0.96. Considering all the collected data, the total CRS-R scores exhibited a high correlation (0.50–0.70) with total GCS (Spearman rho = 0.680; p < 0.001) and total FOUR (Spearman rho = 0.644; p < 0.001), indicating an acceptable concurrent validity.
Detailed results are presented in [Tables 2], [3], [4], and [5].
Abbreviations: CI, confidence interval; CRS-R, Coma Recovered Scale Revised; FOUR, Full Outline of UnResponsiveness; ICC, intraclass correlation.
Notes: †n = 29 pairs. ‡ ICC (3.1), two-way mixed models, single measurement, absolute agreement. For the assessment of concurrent validity, scores from the three scales (CRS-R, GCS, and FOUR) were analyzed using Intraclass Correlation Coefficients (ICC) (two-way mixed models, single measurement and absolute agreement) for inter-rater and intra-rater reliability.
Abbreviations: CI, confidence interval; CRS-R, Coma Recovered Scale Revised; FOUR, Full Outline of UnResponsiveness; ICC, intraclass correlation.
Notes: †n = 29 pairs. ‡ ICC (3.1), two-way mixed models, single measurement, absolute agreement. For the assessment of concurrent validity, scores from the three scales (CRS-R, GCS, and FOUR) were analyzed using ICC - Intraclass Correlation Coefficients (two-way mixed models, single measurement and absolute agreement) for inter-rater and intra-rater reliability.
Abbreviations: CI, confidence interval; CRS-R, Coma Recovered Scale Revised; FOUR, Full Outline of UnResponsiveness; ICC, intraclass correlation.
Notes: †n = 29 pairs. ‡ ICC (3.1), two-way mixed models, single measurement, absolute agreement. For the assessment of concurrent validity, scores from the three scales (CRS-R, GCS, and FOUR) were analyzed using ICC - Intraclass Correlation Coefficients (two-way mixed models, single measurement and absolute agreement) for inter-rater and intra-rater reliability.
Abbreviations: CI, confidence interval; CRS-R, Coma Recovered Scale Revised; FOUR, Full Outline of UnResponsiveness; ICC, intraclass correlation.
Notes: †n = 29 pairs. ‡ ICC (3.1), two-way mixed models, single measurement, absolute agreement. For the assessment of concurrent validity, scores from the three scales (CRS-R, GCS, and FOUR) were analyzed using ICC - Intraclass Correlation Coefficients (two-way mixed models, single measurement and absolute agreement) for inter-rater and intra-rater reliability.
[Table 6] illustrates the detection of signs of consciousness using CRS-R compared with GCS and FOUR for 30 patients. Visual pursuit and/or fixation were not detected in seven cases (23.3%) with GCS. Meanwhile, the FOUR did not detect visual fixation in two patients (6.7%).
Abbreviations: CRS-R, Coma Recovery Scale Revised; eMCS, emergence from minimally conscious state; FOUR, FOUR, Full Outline of UnResponsiveness; GCM, Glasgow Coma Scale; MCS-, minimally conscious state minus; MCS + , minimally conscious state plus; VS/UWS, vegetative state/unresponsive wakefulness syndrome.
Notes: †Day 1, rater A.
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DISCUSSION
Assessing patients with brain injuries and suspected DoC is challenging. Utilizing a structured clinical assessment is crucial to avoid misdiagnoses.[6] [7] The findings from this study suggest that the CRS-R's Brazilian Portuguese translation provides reproducible results across different examiners. There was substantial to almost perfect interrater agreement observed for the total score and subscales. Furthermore, high concurrent validity was established between the Brazilian Portuguese Version of CRS-R and two other standardized behavioral scales, namely GCS and FOUR.[17] [18]
The interrater reliability, as denoted by the correlation coefficient between total scores (K = 0.96), was similar to what has been observed in other validation studies with Latin languages: European Portuguese at 0.87,[19] French at 0.80,[20] Italian at 0.81,[21] and Spanish at 0.97.[22]
The CRS-R demonstrated superior detection of signs of consciousness compared with GCS and FOUR. Specifically, visual pursuit and/or fixation were no detected in seven cases (23.3%) using GCS, and two patients (6.7%) with FOUR. This is noteworthy, as GCS does not have visual pursuit and fixation criteria, and FOUR doesn't assess visual fixation.[23] These findings underscore the scale's heightened sensitivity in detecting signs of consciousness, confirming the American[6] and European[7] guidelines that endorse CRS-R as the gold standard for DoC assessment.
Potential limitations of this study include the possible inexperience of the professionals involved. Nevertheless, diagnostic changes were noted in just four instances, underscoring the overall reliability of the tool. Another limitation was the inclusion of some patients who presented with pain, seizures, and sleep problems, since treatment with drugs for these conditions can influence the results as factors such as age, number of days postinjury, and time of the day when the scale was completed can influence the result.
In Brazil, accurately identifying consciousness in patients with severe brain injuries, especially those who cannot communicate, remains a formidable challenge, leading to frequent misdiagnoses. Many patients do not receive the requisite rehabilitation, adding to the severity of the problem.
Patients with DoC need specific rehabilitation and therapeutic strategies. By understanding the clinical and epidemiological profiles and insights into neurological findings and prevalent symptoms, professionals can more effectively prevent complications and tailor interventions, thereby elevating the quality of life for patients and their families.[24] [25] There is an urgent need to advocate for research on therapeutic interventions, symptom management, and preventive measures for this demographic.[26] [27] [28] The task of spreading awareness about the correct diagnosis of DoC is equally paramount, given the profound repercussions a misdiagnosis can have on patients and their families.
A secondary yet crucial purpose of this study is to emphasize the catastrophic consequences of misdiagnosis and advise Brazilian health professionals to commit to accurate and timely diagnoses.
In conclusion, when administered by trained professionals, the Brazilian Portuguese version of CRS-R is a reliable tool. It demonstrates substantial to almost perfect interrater agreement for both the total score and its subscales. Additionally, it showcases high concurrent validity when compared with two other standardized behavioral scales: GCS and FOUR. Notably, CRS-R is not limited to physicians, and can be employed by various healthcare professionals, reinforcing the tool's versatility. Training programs focusing on CRS-R are essential to improve the assessment and rehabilitation of patients with DoC in Brazil.
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Conflict of Interest
The authors have no conflict of interest to declare.
Authors' Contributions
APSC: conceptualization, data curation, investigation, methodology, project administration, supervision, writing – original draft, and writing – review & editing; TNFVS: data curation, investigation, and writing – review & editing; CMC, RCM, PSP: data curation, investigation, and writing – review & editing; LCVBC: writing – review & editing; RXSN: investigation, writing – review & editing; LSV: formal analysis.
Editor-in-Chief: Hélio A. G. Teive.
Associate Editor: Eduardo Genaro Mutarelli.
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References
- 1 GBD 2016 Traumatic Brain Injury and Spinal Cord Injury Collaborators. Global, regional, and national burden of traumatic brain injury and spinal cord injury, 1990-2016: a systematic analysis for the Global Burden of Disease Study 2016. Lancet Neurol 2019; 18 (01) 56-87
- 2 Kondziella D, Friberg CK, Frokjaer VG, Fabricius M, Møller K. Preserved consciousness in vegetative and minimal conscious states: systematic review and meta-analysis. J Neurol Neurosurg Psychiatry 2016; 87 (05) 485-492
- 3 Andrews K, Murphy L, Munday R, Littlewood C. Misdiagnosis of the vegetative state: retrospective study in a rehabilitation unit. BMJ 1996; 313 (7048) 13-16
- 4 Estraneo A, Moretta P, Loreto V, Lanzillo B, Santoro L, Trojano L. Late recovery after traumatic, anoxic, or hemorrhagic long-lasting vegetative state. Neurology 2010; 75 (03) 239-245
- 5 Luauté J, Maucort-Boulch D, Tell L. et al. Long-term outcomes of chronic minimally conscious and vegetative states. Neurology 2010; 75 (03) 246-252
- 6 Giacino JT, Katz DI, Schiff ND. et al. Comprehensive systematic review update summary: Disorders of consciousness: Report of the Guideline Development, Dissemination, and Implementation Subcommittee of the American Academy of Neurology; the American Congress of Rehabilitation Medicine; and the National Institute on Disability, Independent Living, and Rehabilitation Research. Neurology 2018; 91 (10) 461-470
- 7 Kondziella D, Bender A, Diserens K. et al; EAN Panel on Coma, Disorders of Consciousness. European Academy of Neurology guideline on the diagnosis of coma and other disorders of consciousness. Eur J Neurol 2020; 27 (05) 741-756
- 8 Laureys S, Celesia GG, Cohadon F. et al; European Task Force on Disorders of Consciousness. Unresponsive wakefulness syndrome: a new name for the vegetative state or apallic syndrome. BMC Med 2010; 8: 68
- 9 Schnakers C, Vanhaudenhuyse A, Giacino J. et al. Diagnostic accuracy of the vegetative and minimally conscious state: clinical consensus versus standardized neurobehavioral assessment. BMC Neurol 2009; 9 (35) 35
- 10 Giacino JT, Ashwal S, Childs N. et al. The minimally conscious state: definition and diagnostic criteria. Neurology 2002; 58 (03) 349-353
- 11 Thibaut A, Bodien YG, Laureys S, Giacino JT. Minimally conscious state “plus”: diagnostic criteria and relation to functional recovery. J Neurol 2020; 267 (05) 1245-1254
- 12 Schnakers C, Perrin F, Schabus M. et al. Detecting consciousness in a total locked-in syndrome: an active event-related paradigm. Neurocase 2009; 15 (04) 271-277
- 13 Formisano R, D'Ippolito M, Catani S. Functional locked-in syndrome as recovery phase of vegetative state. Brain Inj 2013; 27 (11) 1332
- 14 Giacino JT, Kezmarsky MA, DeLuca J, Cicerone KD. Monitoring rate of recovery to predict outcome in minimally responsive patients. Arch Phys Med Rehabil 1991; 72 (11) 897-901
- 15 Giacino JT, Kalmar K, Whyte J. The JFK Coma Recovery Scale-Revised: measurement characteristics and diagnostic utility. Arch Phys Med Rehabil 2004; 85 (12) 2020-2029
- 16 Landis JR, Koch GG. The measurement of observer agreement for categorical data. Biometrics 1977; 33 (01) 159-174
- 17 Jennett B. The history of the Glasgow Coma Scale: an interview with professor Bryan Jennett. Interview by Carole Rush. Int J Trauma Nurs 1997; 3 (04) 114-118
- 18 Wijdicks EF, Bamlet WR, Maramattom BV, Manno EM, McClelland RL. Validation of a new coma scale: The FOUR score. Ann Neurol 2005; 58 (04) 585-593
- 19 Simões JF, Jesus LM, Voegeli D, Sá-Couto P, Fernandes J, Morgado M. Assessment of comatose patients: a Portuguese instrument based on the Coma Recovery Scale - revised and using nursing standard terminology. J Adv Nurs 2011; 67 (05) 1129-1141
- 20 Schnakers C, Majerus S, Giacino J. et al. A French validation study of the Coma Recovery Scale-Revised (CRS-R). Brain Inj 2008; 22 (10) 786-792
- 21 Teasdale G, Jennett B. Assessment of coma and impaired consciousness. A practical scale. Lancet 1974; 2 (7872) 81-84
- 22 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 Inj 2011; 25 (05) 488-495
- 23 Tamashiro M, Rivas ME, Ron M, Salierno F, Dalera M, Olmos L. A Spanish validation of the Coma Recovery Scale-Revised (CRS-R). Brain Inj 2014; 28 (13-14): 1744-1747
- 24 Bodien YG, Carlowicz CA, Chatelle C, Giacino JT. Sensitivity and Specificity of the Coma Recovery Scale–Revised Total Score in Detection of Conscious Awareness. Arch Phys Med Rehabil 2016; 97 (03) 490-492.e1
- 25 Nakase-Richardson R, Whyte J, Giacino JT. et al. Longitudinal outcome of patients with disordered consciousness in the NIDRR TBI Model Systems Programs. J Neurotrauma 2012; 29 (01) 59-65
- 26 Katz DI, Polyak M, Coughlan D, Nichols M, Roche A. Natural history of recovery from brain injury after prolonged disorders of consciousness: outcome of patients admitted to inpatient rehabilitation with 1-4 year follow-up. Prog Brain Res 2009; 177: 73-88
- 27 Thonnard M, Gosseries O, Demertzi A. et al. Effect of zolpidem in chronic disorders of consciousness: a prospective open-label study. Funct Neurol 2013; 28 (04) 259-264
- 28 Ghate PS, Bhanage A, Sarkar H, Katkar A. Efficacy of Amantadine in Improving Cognitive Dysfunction in Adults with Severe Traumatic Brain Injury in Indian Population: A Pilot Study. Asian J Neurosurg 2018; 13 (03) 647-650
Address for correspondence
Publikationsverlauf
Eingereicht: 19. Januar 2024
Angenommen: 25. Juli 2024
Artikel online veröffentlicht:
20. November 2024
© 2024. The Author(s). This is an open access article published by Thieme under the terms of the Creative Commons Attribution 4.0 International License, permitting copying and reproduction so long as the original work is given appropriate credit (https://creativecommons.org/licenses/by/4.0/)
Thieme Revinter Publicações Ltda.
Rua do Matoso 170, Rio de Janeiro, RJ, CEP 20270-135, Brazil
Ana Paula Silva Champs, Thayse Nayara Freitas do Vale Santanna, Christian Marques Couto, Roberta Correa Macedo, Patricia Sola Penna, Luciana Charchar Vilas Boas Cruz, Rafael Xavier da Silva-Neto, Luiz Sérgio Vaz. Validation to Brazilian Portuguese of the coma recovery scale-revised. Arq Neuropsiquiatr 2024; 82: s00441791657.
DOI: 10.1055/s-0044-1791657
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References
- 1 GBD 2016 Traumatic Brain Injury and Spinal Cord Injury Collaborators. Global, regional, and national burden of traumatic brain injury and spinal cord injury, 1990-2016: a systematic analysis for the Global Burden of Disease Study 2016. Lancet Neurol 2019; 18 (01) 56-87
- 2 Kondziella D, Friberg CK, Frokjaer VG, Fabricius M, Møller K. Preserved consciousness in vegetative and minimal conscious states: systematic review and meta-analysis. J Neurol Neurosurg Psychiatry 2016; 87 (05) 485-492
- 3 Andrews K, Murphy L, Munday R, Littlewood C. Misdiagnosis of the vegetative state: retrospective study in a rehabilitation unit. BMJ 1996; 313 (7048) 13-16
- 4 Estraneo A, Moretta P, Loreto V, Lanzillo B, Santoro L, Trojano L. Late recovery after traumatic, anoxic, or hemorrhagic long-lasting vegetative state. Neurology 2010; 75 (03) 239-245
- 5 Luauté J, Maucort-Boulch D, Tell L. et al. Long-term outcomes of chronic minimally conscious and vegetative states. Neurology 2010; 75 (03) 246-252
- 6 Giacino JT, Katz DI, Schiff ND. et al. Comprehensive systematic review update summary: Disorders of consciousness: Report of the Guideline Development, Dissemination, and Implementation Subcommittee of the American Academy of Neurology; the American Congress of Rehabilitation Medicine; and the National Institute on Disability, Independent Living, and Rehabilitation Research. Neurology 2018; 91 (10) 461-470
- 7 Kondziella D, Bender A, Diserens K. et al; EAN Panel on Coma, Disorders of Consciousness. European Academy of Neurology guideline on the diagnosis of coma and other disorders of consciousness. Eur J Neurol 2020; 27 (05) 741-756
- 8 Laureys S, Celesia GG, Cohadon F. et al; European Task Force on Disorders of Consciousness. Unresponsive wakefulness syndrome: a new name for the vegetative state or apallic syndrome. BMC Med 2010; 8: 68
- 9 Schnakers C, Vanhaudenhuyse A, Giacino J. et al. Diagnostic accuracy of the vegetative and minimally conscious state: clinical consensus versus standardized neurobehavioral assessment. BMC Neurol 2009; 9 (35) 35
- 10 Giacino JT, Ashwal S, Childs N. et al. The minimally conscious state: definition and diagnostic criteria. Neurology 2002; 58 (03) 349-353
- 11 Thibaut A, Bodien YG, Laureys S, Giacino JT. Minimally conscious state “plus”: diagnostic criteria and relation to functional recovery. J Neurol 2020; 267 (05) 1245-1254
- 12 Schnakers C, Perrin F, Schabus M. et al. Detecting consciousness in a total locked-in syndrome: an active event-related paradigm. Neurocase 2009; 15 (04) 271-277
- 13 Formisano R, D'Ippolito M, Catani S. Functional locked-in syndrome as recovery phase of vegetative state. Brain Inj 2013; 27 (11) 1332
- 14 Giacino JT, Kezmarsky MA, DeLuca J, Cicerone KD. Monitoring rate of recovery to predict outcome in minimally responsive patients. Arch Phys Med Rehabil 1991; 72 (11) 897-901
- 15 Giacino JT, Kalmar K, Whyte J. The JFK Coma Recovery Scale-Revised: measurement characteristics and diagnostic utility. Arch Phys Med Rehabil 2004; 85 (12) 2020-2029
- 16 Landis JR, Koch GG. The measurement of observer agreement for categorical data. Biometrics 1977; 33 (01) 159-174
- 17 Jennett B. The history of the Glasgow Coma Scale: an interview with professor Bryan Jennett. Interview by Carole Rush. Int J Trauma Nurs 1997; 3 (04) 114-118
- 18 Wijdicks EF, Bamlet WR, Maramattom BV, Manno EM, McClelland RL. Validation of a new coma scale: The FOUR score. Ann Neurol 2005; 58 (04) 585-593
- 19 Simões JF, Jesus LM, Voegeli D, Sá-Couto P, Fernandes J, Morgado M. Assessment of comatose patients: a Portuguese instrument based on the Coma Recovery Scale - revised and using nursing standard terminology. J Adv Nurs 2011; 67 (05) 1129-1141
- 20 Schnakers C, Majerus S, Giacino J. et al. A French validation study of the Coma Recovery Scale-Revised (CRS-R). Brain Inj 2008; 22 (10) 786-792
- 21 Teasdale G, Jennett B. Assessment of coma and impaired consciousness. A practical scale. Lancet 1974; 2 (7872) 81-84
- 22 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 Inj 2011; 25 (05) 488-495
- 23 Tamashiro M, Rivas ME, Ron M, Salierno F, Dalera M, Olmos L. A Spanish validation of the Coma Recovery Scale-Revised (CRS-R). Brain Inj 2014; 28 (13-14): 1744-1747
- 24 Bodien YG, Carlowicz CA, Chatelle C, Giacino JT. Sensitivity and Specificity of the Coma Recovery Scale–Revised Total Score in Detection of Conscious Awareness. Arch Phys Med Rehabil 2016; 97 (03) 490-492.e1
- 25 Nakase-Richardson R, Whyte J, Giacino JT. et al. Longitudinal outcome of patients with disordered consciousness in the NIDRR TBI Model Systems Programs. J Neurotrauma 2012; 29 (01) 59-65
- 26 Katz DI, Polyak M, Coughlan D, Nichols M, Roche A. Natural history of recovery from brain injury after prolonged disorders of consciousness: outcome of patients admitted to inpatient rehabilitation with 1-4 year follow-up. Prog Brain Res 2009; 177: 73-88
- 27 Thonnard M, Gosseries O, Demertzi A. et al. Effect of zolpidem in chronic disorders of consciousness: a prospective open-label study. Funct Neurol 2013; 28 (04) 259-264
- 28 Ghate PS, Bhanage A, Sarkar H, Katkar A. Efficacy of Amantadine in Improving Cognitive Dysfunction in Adults with Severe Traumatic Brain Injury in Indian Population: A Pilot Study. Asian J Neurosurg 2018; 13 (03) 647-650