INCOG Recommendations for Management of Cognition Following Traumatic Brain Injury, Part V: Memory

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J Head Trauma Rehabil Vol. 29, No. 4, pp. 369–386 Copyright c 2014 Wolters Kluwer Health Lippincott Williams & Wilkins ⃝ | INCOG Recommendations for Management of Cognition Following Traumatic Brain Injury, Part V: Memory

Diana Velikonja, PhD; Robyn Tate, PhD; Jennie Ponsford, PhD; Amanda McIntyre, MSc; Shannon Janzen, MSc; Mark Bayley, MD, FRCPC, on behalf of the INCOG Expert Panel

Introduction: Traumatic brain injury results in complex cognitive sequelae. Impairments in memory are among the most common sequelae resulting in significant functional problems. An international team of researchers and clinicians (known as INCOG) was formed to develop recommendations for the management of impairments in memory. Methods: The experts met to select appropriate recommendations and then reviewed available literature to ensure recommendations were current. Decision algorithms incorporating the recommendations based on inclusion and exclusion criteria of published trials were developed. The team then prioritized recommendations for implementation and developed audit criteria to evaluate adherence to the best practice recommendations. Results: The recommendations for rehabilitation of memory impairments support the integration of internal and external compensatory strategies implemented using appropriate instructional techniques that consider functional relevance and important patient characteristics. Restorative strategies have regained significant popularity, given broader access to computer technology; however, evidence for efficacy of these techniques remains weak and the choice in using these should be guided by special considerations. Conclusion: There is good evidence for the integration of internal and external compensatory memory strategies that are implemented using instructional procedures for rehabilitation for memory impairments. The evidence for the efficacy of restorative strategies currently remains weak. Key words: cognitive rehabilitation, guidelines, knowledge translation, memory, neuropsychology, rehabilitation, therapeutic approaches for the treatment of central nervous system injury, traumatic brain injury

Author Affiliations: Neuropsychology, Acquired Brain Injury Program, ROM AN INFORMATION-PROCESSING per- Hamilton Health Sciences, Hamilton, Ontario, Canada (Dr Velikonja); Department of Psychiatry and Behavioural Neurosciences, DeGroote F spective, memory reflects processes of encoding, School of Medicine, McMaster University, Hamilton, Ontario, Canada storing, and retrieving information from short- and (Dr Velikonja); NHMRC Centre of Research Excellence in Traumatic long-term memory systems.1 Impairments in memory Brain Injury Psychosocial Rehabilitation, Sydney, New South Wales, Australia (Drs Tate and Ponsford); Royal Rehabilitation Centre, Sydney, following traumatic brain injury (TBI) are among the New South Wales, Australia (Dr Tate); Centre for Rehabilitation most common cognitive deficits, typically manifested Research, Kolling Institute, Sydney Medical School–Northern, University as problems learning new information.2 They can have of Sydney, Sydney, New South Wales, Australia (Dr Tate); School of 3 Psychology and Psychiatry, Monash University and Epworth Hospital, debilitating functional consequences. The literature on Melbourne, Victoria, Australia (Dr Ponsford); National Trauma Research rehabilitative approaches directed at managing mem- Institute, Monash University and the Alfred Hospital, Melbourne, ory impairments following TBI can be broadly divided Victoria, Australia (Dr Ponsford); Lawson Health Research Institute, St. Joseph’s Parkwood Hospital, London, Ontario, Canada (Mss McIntyre into compensatory strategies and restorative techniques. and Janzen); and Neuro Rehabilitation Program, Toronto Rehabilitation Compensation approaches emphasize the use of the Institute, University of Toronto, Toronto, Ontario, Canada (Dr Bayley). residual cognitive strengths of patients with brain injury The authors gratefully acknowledge the support of the Victorian Transport to minimize the functional impact of their memory im- Accident Commission through its Victorian Neurotrauma Initiative, Monash pairment in the course of performing daily tasks. Com- University, and the Ontario Neurotrauma Foundation for their support of this project. pensatory strategies are typically separated into internal and external strategies. With internal memory compen- The INCOG developers, contributors, and supporting partners shall not be liable for any damages, claims, liabilities, costs, or obligations arising from satory strategies, the performance of a task is modi- the use or misuse of this material, including loss or damage arising from any fied to increase conscious effort during the encoding claims made by a third party. The authors declare no conflicts of interest. Wellington St North, Hamilton, ON L8L 0A4, Canada (dvelikonja@ svapsych.ca). Corresponding Author: Diana Velikonja, PhD, Acquired Brain Injury Program, Regional Rehabilitation Centre, Hamilton Health Sciences, 300 DOI: 10.1097/HTR.0000000000000069 369

Copyright © 2014 Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited. 370 JOURNAL OF HEAD TRAUMA REHABILITATION/JULY–AUGUST 2014 phase of memory processing by increasing an individ- the Appraisal of Guidelines for Research and Evaluation ual’s ability to monitor his or her task performance. Ex- (AGREE II) instrument.10,11 The ADAPTE process ternal memory strategies integrate a physical system of involves extracting recommendations from these CPGs compensation.4 Restorative techniques aim to improve to allow easy comparison (eg, all recommendations the specific impaired cognitive function through re- about executive function were tabulated together). peated exercises or massed training trials5 and derive The Evidence-based Review of Acquired Brain Injury evidence for their efficacy based upon the plasticity of (ERABI: http://www.abiebr.com) synopses of evidence cortical functions in the motor and sensory domains for each topic area were also distributed to the panel.12 following such training.6 The initial expert panel meeting was scheduled for The INCOG guidelines include 7 recommendations convenience just prior to the World Congress of Neu- for the best practice in the application of rehabilitation rorehabilitation in Melbourne, Australia, in May 2012. strategies for memory impairments following TBI. The Some members attended via Web conferencing from recommendations are based on a review the evidence the United States and Canada. This panel examined the related to compensatory and restorative approaches to recommendations matrix and selected suitable recom- the rehabilitation of memory, as well as the instructional mendations from existing guidelines or articulated novel strategies that should be considered when attempting to recommendations based on the evidence available. teach new information or procedures to the patient with This yielded an initial draft set of recommendations; brain injury. There is considerable variability across the however, to ensure the recommendations were updated studies regarding reporting of severity of memory im- according to the most current evidence, the research pairments, with varying descriptors used to define the team prepared synopses of large systematic reviews, the level of memory impairment. Few studies have used GEM (Global Evidence Mapping) Initiative13 based in standardized measures to define impairment ranges. Australia (www.evidencemap.org), the Evidence-based Selection criteria often exclude comorbidities such as Review of Acquired Brain Injury12 and PsycBITE alcohol, neurodegenerative diseases, and neurodevelop- (http://www.psycbite.com).14 Furthermore, the refer- mental conditions. Many patients have injury-related ence sections of all eligible cognitive rehabilitation comorbidities such as problems with executive skills, CPGs were extracted. All relevant references were con- attention, processing speed, and affect at varying lev- solidated into a reference library that was made available els of impairment. Most studies include patients with to the author teams as they drafted the manuscripts and brain injury in the post–acute phase of recovery. The finalized the recommendations accordingly. By the end, evidence should be viewed with these caveats in mind. the team completed the evidence review of more than The methodology of studies reviewed is broadly dis- 600 references found in this search process. This task cussed with an accompanying reference table if further has resulted in a comprehensive mapping of evidence to clarification is required. all previously and newly developed recommendations. The tables will be made available as online content on METHODS the Web site of the Journal of Head Trauma Rehabilitation. With the updated literature search in mind, the experts The Guidelines Adaptation and Development graded the evidence. As various systems for determining (ADAPTE) process was used to develop the INCOG the level of evidence were used across the CPGs, the guidelines.7,8 An international expert panel was formed INCOG team standardized this by using the grading through invitations of authors of previously published system outlined in Table 1, which was based upon cognitive rehabilitation guidelines and contacts of the that used in previous guideline development projects.15 team. In preparation, a detailed Internet and MEDLINE These final recommendations were presented to the search was conducted to identify published TBI and entire team for approval and then the expert panel evidence-based cognitive rehabilitation guidelines.9 The used modified Delphi voting technique to prioritize quality of the development process for each eligible the recommendations from the INCOG guideline for clinical practice guideline (CPG) was evaluated using

TABLE 1 INCOG level of evidence grading system

A. Recommendation supported by at least 1 meta-analysis, systematic review, or randomized controlled trial of appropriate size with a relevant control group B. Recommendation supported by cohort studies that at minimum have a comparison group, well-designed single-subject experimental designs, or small sample size randomized controlled trials C. Recommendations supported primarily by expert opinion based on their experience through uncontrolled case series without comparison groups that support the recommendations are also classiﬁed here.

Copyright © 2014 Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited. INCOG Recommendations for Management of Cognition Following TBI 371 audit. Each of the experts was asked in this exercise to LIMITATIONS OF USE AND DISCLAIMER vote for his or her top 15 recommendations considering These recommendations are informed by evidence both the importance to practice and feasibility of for TBI cognitive rehabilitation interventions that was auditing the recommendations. current at the time of publication. Relevant evidence For each cognitive rehabilitation domain of posttrau- published after the INCOG guideline could influence matic amnesia, attention, memory, executive function, the recommendations contained herein. Clinicians must and cognitive communication, a clinical algorithm was also consider their own clinical judgment, patient pref- developed to help clinicians decide to whom the rec- erences, and contextual factors such as resource avail- ommendations applied (see Figure 1). To finalize the ability in their decision-making processes about imple- algorithm, evidence tables were reviewed to find the in- mentation of these recommendations. clusion and exclusion criteria for the study populations that were used. By understanding the subpopulations of TBI patients to whom the evidence applies, it is possible RECOMMENDATIONS AND LITERATURE to understand what treatments are appropriate for each REVIEW patient. In contrast to other guidelines, the INCOG team has identified recommendations that could be au- The 7 INCOG guidelines for recommendations for dited from clinical charts to determine adherence to the best practices regarding the rehabilitation of memory best practice guidelines in each section. This is known impairments are accompanied by a review of the re- as the INCOG audit tool. More detailed version of the lated current evidence (see Tables 2 and 3). There is a Methods is available in the third article of the series.16 combination of grade A and B evidence to support the

Figure 1. Algorithm: Memory. www.headtraumarehab.com

continues ( 29 O’Neil-Pirozzi Glasgow Wright et al Gentry et al, Thoene and 27 37 Fleming et al, 57 35 McKerracher 36 43,44 Hersh and 45 124 Bergquist et al, 50 55 Grilli and McFarland, Potvin et al, Raskin and Sohlberg, Van den Broek et al, 24 22 34 32 56 et al, Freeman et al, Manasse et al, Schefft et al, Fleming et al, Hart et al, Zencius et al Treadgold, et al, et al, Glisky et al, Dowds et al, Bergman, Wade and Troy, 53 25 30 59 Wilson Ryan 54 23 Lemoncello McDonald 46 46 Shum et al, Schmitter- McDonald et al, 38 53 52 48 Edgecombe et al Twum and Parente Ownsworth and McFarland, et al et al, et al, et al, Fish et al, Fish et al, 39 79 A Kaschel et al, A Sohlberg et al B Lynch 16 INCOG / Guideline 40(p672) recommendation Grade Reviews RCTs Other 17(p523) /EFNS 16 16 other memory devices; weaknesses; (eg, executive cognitive skills); and Age; Severity of impairment; Premorbid use of electronic and Cognitive strengths and Physical comorbidities. • • • • • be used for TBI patientsimpairments. who These have strategies memory include instructional and/or metacognitive strategies (eg, visualization/visual imagery, repeated practice, retrieval practice, PQRST, self-cueing, self-generation, self-talk). Their use tends to be mostwho effective have with mild patients to moderateimpairments range and/or some preserved executive cognitive skills. Usingstrategies multiple is considered effective, and strategies can be taughtgroup individually format. or in a recommended for TBI patients whomemory have impairment, and most especially with those who have severeimpairment (eg, memory NeuroPage, mobile/smartphones, SIRI, PDA, notebooks, whiteboards). Patients with TBI andcaregivers their must be trained inthese how external supports. to use take into account the followingregarding considerations persons with TBI: Cicerone et al INCOG INCOG INCOG guideline recommendations: Memory Memory #1 Teaching internal compensatory strategies may Memory #2 Environmental supports and reminders are Memory #3 The selection of external memory aids should TABLE 2

Copyright © 2014 Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited. INCOG Recommendations for Management of Cognition Following TBI 373 ) 87 71 69 85 109 67, 68 Silver 89 80 Masanic 86 114 continues 113 ( 70 O’Neil- 107 Svoboda Haslam 72,73 Glisky Khateb Evans et al, 99 81 82 Quemada 22 65 111 Walker et al, 110 74 Kalla et al, 34 Goldstein et al, 88 106 Kaye et al, Morey et al, Taverni et al, Hunkin and Parkin, Riley et al, Tailby and Haslam 75–77 83 62 66 108 112 105 Constantinidou and Neils, Ehlhardt et al, Glasgow et al, Gordon Hayman et al, Goverover et al, Hux et al, Melton and Bourgeois, Molloy et al, Sumowski et al, et al, et al, et al, Tenovuo, Whelan et al Pirozzi et al et al, et al, et al, et al, Baddeley and Wilson, Evans and Wilson, Bourgeois et al, 78 98 104 97 Eakman and Tenovuo et Powell et al 63 122 Thickpenny-Davis 103 Zhang et al 59 102 al, and Barker-Collo Schmitter-Edgecombe et al, Nelson, Dou et al, 60 (Continued) A Ehlhardt et al BKimetal, BJennettandLincoln, 16 Guideline /INCOG recommendation Grade Reviews RCTs Other 17(p523) 60(p326) 100(p98) breaking down tasks into smaller components such as task analysistraining multistep when procedures; practice; stimuli/information being presented (eg, multiple exemplars, practical tasks); effortful processing of information/ imagery); relevant to the patientvalidity); (ie, and ecologically errors (eg, errorless, spaced retrieval) when acquiring new or relearning information and procedures. Clearly define intervention goals; Integrate methodologies that allow for Allow sufficient time and opportunity for Use principles of distributedTeach practice; strategies using variations in the Promote strategies that allow for more Selection of and train to goals that are Use teaching strategies that constrain stimuli (eg, verbal elaboration; visual • • • • • • • • practices that can promote learningindividuals for with memory impairments,include: which for remediation of mild todeficits moderate following memory TBI. donepezil, rivastigmine) may befor considered adults with TBI whomemory. have The deficits effects of in theshould medication be assessed usingfunctional objective measures. and Cicerone et al NZGG 6.1.6, Ehlhardt et al INCOG guideline recommendations: Memory Memory #4 There are a number of key instructional Memory #5 Group-based interventions may be considered Memory #6 A trial of acetylcholinesterase inhibitors (eg, TABLE 2

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recommendations related to the use of compensatory approaches. Weak, but consistent, evidence (grade B) was found supporting choice of various instructional strategies. The ﬁnal recommendation addresses the efﬁ- cacy of current computer-based restorative approaches in improving general memory processing, with primar- Johansson and ily grade B and C evidence. The recommendations and 118 a summary of the supporting evidence are presented in 123 the following text:

Memory #1. Teaching internal compensatory strategies may be used for TBI patients who have memory impairments. Tornmalm

Fernandez et al, These strategies include instructional and/or metacognitive

raumatic brain injury. strategies (eg, visualization/visual imagery, repeated practice, retrieval practice, PQRST, self-cueing, self-generation, self-talk, etc). Their use tends to be most effective with patients who have mild to moderate range impairments and/or some preserved executive cognitive skills. Utilizing multiple strategies is considered effective and strategies can be taught individually or in a group format. (Adapted from Cicerone et al,17(p523) 122 INCOG16)

Historically, the use of internal compensatory mem- Dou et al ory strategies started with the teaching of techniques such as mnemonics,18 visual imagery,19 and self- 117 instructional methods.20 In general, such techniques focus on directing attention to and elaborating in some meaningful way upon the information to be remem- bered, with the aim of facilitating subsequent retrieval.21 The studies have been largely conducted in experimen-

(Continued) tal settings, with outcome assessed in terms of performance on standardized neuropsychological tests. For example, instruction in the PQRST (Preview, Question,

B-C Gontkovsky et al Read, Self-Recitation, Test) method has been associated with improvement in performance on standardized verbal memory measures.22 Similarly, patients instructed in techniques for creating visual imagery and verbal elaboration to assist them to remember new information generally performed better on standardized tests of verbal and visual memory than performed by untreated controls.23–26 The use of structured visual imagery has also been applied to learning of more practical information in a “real-world” setting with positive results.27 Studies integrating self-instructional methods have

Guideline been more often applied to prospective memory tasks. Prospective memory represents the ability to remem- recommendation Grade Reviews RCTs Other ber future events and perform tasks that need to be completed.28 For example, training in visual imagery techniques to strengthen the association be- computer-based training show no evidence in enhancing sustained memory performance. Guidelines in using such techniques indicateshould that only it be consideredadjunct to develop memory rehabilitation strategies with evidence-based instructional and compensatory strategies, and only ifconjunction developed in with a therapistfocus with on a strategy development and transfer to functional tasks. tween prospective cues and intended actions has been associated with reduced forgetting of daily tasks.29 INCOG guideline recommendations: Memory Self-awareness techniques that have focused upon improving the patient’s knowledge of the manifesta- tions of memory impairments, combined with compen-

Memory #7 Restorative techniques such as satory prospective cueing techniques, have also been TABLE 2 Abbreviations: PDA, personal digital assistant; PQRST, Preview, Question, Read, Self-recitation, Test; RCT, randomizedassociated controlled trial; TBI, t with improved performance on prospective

continues ( OT Other SLP Neuropsychology Rehabilitation OT Other SLP Neuropsychology Rehabilitation OT Other SLP Neuropsychology Rehabilitation psychology psychology psychology ! ! ! ! ! ! ! ! ! ! ! ! ! ! ! Aspects of executive cognitive functioning that may be preserved memory impairment— psychometric or functional assessment level of memory impairment— psychometric assessment memory impairment— psychometric assessment Mild to moderate Amnesia and/or severe Amnesia and/or severe ! ! ! ! a Training provided Assess transfer of Assess patients Training provided to Training provided to Assess usability or memory severity and executive cognitive skills strategy to functional tasks appropriateness for group intervention if this format is being considered ensure appropriateness of device caregivers/support staff characteristics and needs of patient caregivers/support staff functional uptake of the strategy for patient Assessment of Assessment to Assess individual ! ! ! ! ! ! ! ! ! Speciﬁc activities, Assessment of need Patient applicable aids applicable aids Smartphone PDA Notebook SIRI Other Smartphone PDA Notebook SIRI Other Paging system Paging system ! ! ! ! ! ! ! ! ! ! ! ! : : : Audit guidelines for priority recommendations: Memory memory devices (eg, executive cognitive skills) Severity of impairment Age Premorbid use of electronic and other Cognitive strengths and weaknesses Physical comorbidities • recommended for TBI patients who have memory impairment, and most especially with those whomemory have impairment—(eg, severe NeuroPage, mobile/smartphones, SIRI, PDA, notebooks, whiteboards, etc) Patients with TBI and their caregivers/support staff must be trained inthese how external to supports. use may be used for TBImemory impairments. patients who These strategies have include instructional and/or metacognitive strategies (eg, visualization/visual imagery, repeated practice, retrieval practice, PQRST, self-cueing, self-generation, self-talk). Their use tends to bewith most patients effective who havemoderate mild range to impairments and/or some preserved executive cognitive skills. Using multiple strategiesconsidered is effective, and strategies can be taught individually orformat. in a group should take into accountconsiderations the regarding following the person with a TBI: • • • • Environmental supports and reminders are Teaching internal compensatory strategies memory strategies strategies compensatory strategies The selection of external memory aids

Intervention (guideline recommendation)Implementing internal compensatory devices, or tools and effectiveness characteristicsExternal memory compensatory Discipline Selection of external memory TABLE 3

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continues ( SLP Neuropsychology Rehabilitation OT Other SLP Neuropsychology Rehabilitation OT Other psychology psychology ! ! ! ! ! ! ! ! ! ! memory impairment— psychometric assessment memory impairment— psychometric or functional assessment Mild to severe Mild to moderate ! ! (Continued) a Training provided Evaluation of functional integration memory and other cognitive skills suitability for group-based intervention Assessment of Assess patients ! ! ! ! activities, Assessment of need Patient Specific any structured programs being used (ie, I-MEMS, etc) group setting and materials Materials for Appropriate ! ! : Audit guidelines for priority recommendations: Memory : stimuli/information being presented (eg, multiple exemplars, practical tasks); effortful processing of information/stimuli (eg, verbal elaboration; visual imagery); relevant to the patientvalidity); (ie, and ecologically breaking down tasks into smaller components such as task analysis when training multistep procedures; for practice; Promote strategies that allow for more Selection of and train to goals that are Clearly define intervention goals; Integrate methodologies that allow for Allow sufficient time and opportunity Use principles of distributed practice; Teach strategies using variations in the • • • • • • • practices that can promote learningindividuals for with memory impairments, which include: considered for remediation of mildmoderate to memory deficits following TBI. There are a number of key instructional Group-based interventions may be patients

Intervention (guideline recommendation)Group-based instructional formats devices,Instructional or practices tools for memory-impaired and effectiveness characteristics Discipline TABLE 3

Copyright © 2014 Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited. INCOG Recommendations for Management of Cognition Following TBI 377 in Other MD Drug notes charts ! ! ! Patient SLP Neuropsychology Rehabilitation OT Other Evidence of Functional psychology deficits of memory outcomes measures administered ! ! ! ! ! ! ! aumatic brain injury. ) memory severity— psychometric or functional assessment Memory impairment Mild to moderate Other (please specify): ! ! ! Continued ( a transfer Evaluation of functional functional goals and generalization tasks Assess for key ! ! Pharmaceutical interventions: Memory Specific activities, Assessment of need Patient Therapist Yes No ! : Audit guidelines for priority recommendations: Memory errors (eg, errorless, spaced retrieval) when acquiring new or relearning information and procedures. Use teaching strategies that constrain • computer-based training show no evidence in enhancing sustained memory performance. Guidelines in using such techniques indicateshould that only it be consideredadjunct to memory develop rehabilitation strategies with evidence-based instructional and compensatory strategies, and only if developed in conjunction withtherapist a with a focus ondevelopment strategy and transfer to functional tasks. Donepezil Rivastigmine for adults with TBI whomemory. have The deficits effects of in theshould medication be assessed usingfunctional objective measures. and • • Restorative techniques such as AtrialofAChEinhibitorsmaybeconsidered Intervention (guideline recommendation) devices, or tools and effectiveness characteristics Discipline AChE inhibitors Restorative memory strategies Drug Used Indication characteristics Found The audit tool items for Memory are shown. These are the items that the panel voted as the most important for implementation. TABLE 3 Abbreviations: AChE, acetylcholinesterase; OT,a occupational therapy; PDA, personal digital assistant; SLP, speech-language pathology; TBI, tr

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Copyright © 2014 Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited. 378 JOURNAL OF HEAD TRAUMA REHABILITATION/JULY–AUGUST 2014 memory tasks30 and found to be superior to rote re- tion and later checking what tasks they need to per- hearsal in facilitating the subsequent completion of form led to the introduction of paging systems.26,41,45 tasks.31 Greater long-term use of paging devices was associated Implementation of structured training procedures in with built-in prompting systems,26 as well as with pa- the use of multiple internal mnemonic strategies has tients who had better executive cognitive skills, regard- been associated with improvements in recall of prospec- less of the level of memory impairment.46 tive tasks when delivered both in an individualized Individuals with brain injury and good executive func- format32,33 and in group instruction. For example, the tioning scores have been shown to achieve a large per- Internal Memory Strategies (I-MEMS)34 is a protocol in- centage of attained target behaviors when trained to use volving a 12-week structured program in which multiple a mobile phone with individualized prompts. In gen- internal compensatory strategies (eg, visualization, asso- eral, paging systems and personal voice organizers that ciations) were delivered in a group format. Delivery of provide a system of cues or prompts have been shown this protocol was associated with improvements on stan- to improve the ability of individuals with brain injury to dardized verbal learning and behavioral memory tasks, effectively achieve target behaviors, reduce the number including tests of prospective memory.34 Instruction in of therapy sessions missed, and complete more person- several concurrent strategies integrating self-awareness of ally meaningful tasks within the home and at work.47,48 memory deficits, customized cueing strategies, as well as The use of such devices has also resulted in improve- organizational strategies also resulted in improved per- ment in the individual’s quality of life and sense of formance on prospective memory tasks.30,35,36 well-being.49,50 The use of PDAs programed to pro- Evidence suggests that combining compensatory vide prompting has been associated with self-ratings memory techniques with self-instructional strategies that of increased participation in daily activities and satis- emphasize the use of executive skills to monitor their faction in occupational performance.51 An assistive de- use enhances their efficacy.37 The need for use of ex- vice that provided specific prospective memory prompts ecutive cognitive skills in implementing these strategies was associated with much greater task completion than may explain why individuals with less severe cognitive that by assistive devices that did not incorporate such deficits have shown more benefit from internally based prompting.52 Programming a computer-based calendar memory training than those with more severe deficits.38 system with prompts was shown to enhance prospective Evidence of the generalizability of these techniques in memory performance and reduce the need for monitor- reducing the daily functional problems experienced by ing when compared with the use of a standard diary.53 patients with memory impairment has been equivocal, The expense of electronic devices may be prohibitive due to the inclusion of people with more severe memory for some people, and there may also be issues with learn- impairment and additional executive cognitive deficits, ing how to use such technology, particularly for older which significantly limit their capacity to apply these people who have little experience with technology, or techniques.4 Therefore, the application of such strate- patients who do not have someone who can program gies must include assessment of the capacity of the per- the device for them. Hence, diary systems may be more son with brain injury to implement strategies taught in helpful in certain cases. Studies have examined ways everyday contexts, including knowing when to use such of increasing the use of diary systems. When training strategies. Thus, combining the integration of internal in diary use was combined with cueing, learning, and and external compensatory strategies may enhance the self-instructional techniques, greater improvements in effectiveness of remedial interventions for memory.39 performance on prospective memory tasks was found than those by instruction in diary use alone.35 Such Memory #2. Environmental supports and reminders are training has also resulted in an increased use of com- recommended for TBI patients who have memory impair- pensatory strategies.54 Modifications to a standard diary ment and most especially with those who have severe mem- that better suited the individual needs of patients and ory impairment—(eg, NeuroPage, mobile/smartphones, SIRI, their functional application have also been associated PDA, notebooks, whiteboards, etc). Patients with TBI and their 55,56 caregivers/support staff must be trained in how to use these with improved prospective memory performance. 40(p672) 16 external supports. (Adapted from EFNS, INCOG ) Memory #3. The selection of external memory aids should take into account the following considerations regarding the The evidence supporting the use of external compen- person with a traumatic brain injury: satory strategies in reducing some of the daily prob- Age lems associated with impaired memory has been exten- Severity of impairment 4,39,41 r sively reviewed. The range of external aids includes r Premorbid use of electronic and other memory devices diaries, notebooks, customized memory books, organiz- r Cognitive strengths and weaknesses (eg, executive cogni- 42–44 ers, and planners. Difficulties with severe memory- r tive skills) impaired patients remembering to write down informa- Physical comorbidities. (Adapted from INCOG16) r

Review of the literature has provided strong evidence which emphasizes the need for a combination of en- that the use of external compensatory strategies is as- vironmental adaptations, external compensatory strate- sociated with reduced functional problems in daily liv- gies, and various internal strategies individualized to the ing across individuals with variable memory severity.4 patient to maximize learning in individuals with brain An important factor in the successful use of a mobile injury, was evaluated using a combination of standard- phone, which emerged from a series of case studies, ized and behavioral outcome measures. Results showed was the individual’s ability to manage the sophistication that using a combination of strategies was associated of the device, which was strongly influenced by his or with functional improvements on tasks that were rele- her age.57 One study using a randomized, controlled, vant to the daily life of patients.62 Assignment to a con- crossover design with a large sample, more than half of dition in which instructions were applied to “hands-on” whom had TBI, did demonstrate that better executive tasks or tasks of practical significance to the individual cognitive skills facilitated the integration of an exter- resulted in significantly better recall of instructions than nal device.46 Data from a within-subject design demon- when verbal instruction was provided alone.63 strated that provision of a conceptual understanding Training typically involves either teaching informa- of how to use an external memory device as well as tion (eg, names, word-lists, object names) or tasks such prior experience with technology were considered im- as data entry, programming, or learning to use an ex- portant in order for patients to gain any benefit from ternal memory aid or computer task. A number of re- such devices.58 Moreover, using a within-subject design, view articles of approaches to training individuals with electronic devices were more readily used if the indi- brain injury suggest that the goal of the training inter- vidual with brain injury had prior experience with such vention must be relevant and clearly delineated to the devices, access to appropriate supportive technology, as individual with brain injury (eg, reduce missed appoint- well as a family member available to support and moni- ments, increase daily tasks to be achieved, a computer tor the use of the device as a memory aid.53,59 In a small, program). These reviews also suggest that the use of in- randomized, controlled trial, group instruction and sup- structional techniques that carefully structure the infor- port were shown to be effective in increasing the use of a mation or steps of the task is essential to ensure the suc- memory notebook at the end of the intervention; how- cess of training.64 Specific instructional packages have ever, this effect was not sustained at 6-month follow also been developed integrating task analysis, in which up.59 Thus, there is emerging support that would indi- the steps of practical tasks are broken down into compo- cate evaluation of these factors in considering the choice nent steps, errorless learning, and an executive cognitive of technology or other memory support strategies. predictive strategy (TEACH-M; each letter represents 1 of the 7 steps of the procedure65)toteachacomplex Memory #4. There are a number of key instructional prac- e-mail task. In a pilot study using a multiple-baseline tices that can promote learning for individuals with memory approach across 9 subjects, the TEACH-M package was impairments, which include: shown to facilitate learning the sequences of steps in an Clearly define intervention goals e-mail task, with good maintenance of strategies learned r Integrate methodologies that allow for breaking down tasks into smaller components such as task analysis when and some generalization, but there was variability in r 65 training multistep procedures the number of trials required to learn the steps. Use of Allow sufficient time and opportunity for practice “theory-driven” instructional strategies incorporating er- r Use principles of distributed practice rorless learning and generalization to relevant tasks was r Teach strategies using variations in the stimuli/ shown to improve the use of a device in a single case, 66 r information being presented (eg, multiple exemplars, studied using an ABAB design. practical tasks) Randomized controlled trials have shown that the use Promote strategies that allow for more effortful process- of internal strategies that increase the depth of semantic r ing of information/stimuli (eg, verbal elaboration; visual processing and embed visual imagery into verbal infor- imagery, etc) mation is effective in enhancing recognition and cued re- Selection of and train to goals that are relevant to the call of verbal information and for improving face-name r patient (ie, ecologically validity) 67,68 Use teaching strategies that constrain errors (eg, error- recognition, with evidence of generalization. The use of internal strategies that integrate modalities, in- r less, spaced retrieval, etc) when acquiring new or relearning information and procedures. (Adapted from Ehlhardt cluding auditory and visual techniques, has been shown et al60) to be effective in improving recall in individuals with moderate and severe memory impairments in a control Studies focusing on instructional practices generally group study.69 Strategies such as vanishing cues, a form support the use of structured methods to aid learning of chaining with fading cues following an attempt at of skills or knowledge or to teach compensatory strate- identifying the target, tend to show weaker effects in in- gies. Wilson’s61 structured behavioral memory program, dividuals with severe memory impairment, presumably www.headtraumarehab.com

Copyright © 2014 Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited. 380 JOURNAL OF HEAD TRAUMA REHABILITATION/JULY–AUGUST 2014 due to the errors that are allowed in this more traditional ter acquisition of functional tasks in the context of a process.70 However, even when the capacity to make er- within-subject design.82 Meta-analytic studies evaluat- rors was eliminated from the vanishing cue trials, no ing errorless strategies have demonstrated moderate ef- advantage was found over the more conventional meth- fect sizes.83,84 The use of errorless strategies to improve ods in more severely memory-impaired individuals.71 verbal recall and functional task acquisition has resulted Using a within-subject design, vanishing cues were con- in gains with moderate effect sizes across the range of firmed to be associated with limited learning in severe severity of memory impairment,85 but stronger effect memory-impaired patients but did demonstrate greater sizes for use of errorless strategies have been found in effects in semantic learning for individuals with milder individuals with more severe memory impairment.4,86 memory impairments.72 Essentially cues could be re- One study using a counterbalanced group design found duced more rapidly in milder memory-impaired indi- that patients were able to have cues faded more rapidly viduals, whereas those with more severe impairments during errorless learning conditions when memory im- required more gradual fading.73 A series of case studies pairments were less severe.87 showed that multiple internal compensatory strategies Distributed practice is a form of spaced retrieval in delivered in a structured instructional format resulted in which training of recall strategies is provided over ex- improved recall for verbal and visual based structured panded intervals. Using a within-subject design, dis- information22 and was also effective in the context of tributed practice was shown to be effective for teach- more functional tasks.74 ing association strategies (names of known individuals) The value of using training tasks of ecological rel- when training was delivered at no greater frequency than evance to the individual with brain injury was estab- once a day.88 Positive results were found on prospective lished in a landmark study that capitalized on the rel- and episodic memory tasks when instructional practice atively intact implicit learning capacity of an amnesic was delivered during 30-minute daily phone sessions woman, facilitating her procedural and semantic learn- over 7 weeks.89 Both studies showed good acquisition ing of a computer-based task through systematic instruc- across individuals with variable severity of memory im- tion, which enabled her to be gainfully employed. On pairment, but, again, the number of acquisition trials re- these tasks, there was clearer evidence that more severe quired varied across patients because of the differences memory impairments were associated with slower rates in memory deficits. of learning.75–77 In a controlled trial study, errorless in- Spaced retrieval and errorless strategies have been struction was found to be more effective than traditional used with amnestic individuals, as the prevention of error-based learning to train the use of an external as- errors in such severe memory impairment is important sistive compensatory device.78 Lynch79 noted that tech- for learning.70 Spaced retrieval involves the systematic nology and compensatory devices were most effectively increase in intertrial intervals during learning and is con- integrated when they were individualized to the prac- sidered by some to be “effortless,” allowing for it to be a tical daily life tasks needing to be performed by the successful strategy with this severity of memory impair- individual with TBI. ment. Some consider spaced retrieval to be an errorless Constraining errors can be achieved through a vari- procedure or strategy,90 whereas others consider it to ety of techniques. It has been demonstrated that learn- be differences between the strategies and have argued ing is facilitated by errorless strategies in populations that recall memory with spaced retrieval is superior to with brain injuries because explicit memory, which is “errorless” strategies.83 the memory system believed to systematically eliminate Using errorless approaches, amnestic individuals have errors during learning, is most typically impaired, which been taught new factual information,91 novel associa- leaves the consolidation phase of learning to be more tions and remotely linked information,92 as well as face- reliant upon implicit memory that is highly susceptible name associations.87 Use of spaced retrieval with gen- to the interference caused by errors.70 One relatively eralization strategies has been shown to be effective in well-controlled study found that combining errorless teaching specific goals and strategies, with evidence of strategies with preexposure was particularly helpful in maintenance for up to 1 month following training in teaching target tasks such as name learning.80 Spaced mild to moderately impaired TBI patients.89 Spaced re- retrieval/presentation is another training method that trieval has also been shown to improve recall of words involves both reexposure and cued feedback at system- in TBI individuals with moderate to severe impairments atically increasing intervals during learning trials. This when compared with massed practice.93 Use of errorless has been shown to be more effective than conventional procedures for teaching semantic and procedural knowl- strategies where there was more potential for errors, edge and cued conditions94 is particularly effective with such as massed restudy and spaced restudy.81 In fact, those with better executive skills.95 Face-name associa- compared with just massed learning, spaced retrieval tions were also more successfully taught using errorless was shown to be more consistently associated with bet- strategies, particularly if preexposure conditions were

Copyright © 2014 Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited. INCOG Recommendations for Management of Cognition Following TBI 381 included.80 The benefits of errorless approaches have alizing instruction and provided over 4 stages, antici- been shown to extend to route-finding tasks, suggest- pation, acquisition, application, and adaptation, with ing that this strategy can facilitate perceptual learning.96 didactic lessons and homework assignments presented Spaced retrieval strategies have also been successfully by the therapists and regularly reviewed and modifica- delivered by telephone to patients and associated with tions made as required. Generalization of skills to novel positive mastery of treatment goals, which was main- settings was also reviewed. Between-group comparison tained over time.90 There appears to be general support was conducted relative to a supportive group to examine for constraining errors, especially with those patients the effects of a group intervention alone, which alone who have more severe memory impairments. presented positive results.59

Memory #5. Group-based interventions may be considered for Memory #6. A trial of acetylcholinesterase inhibitors (eg, remediation of mild to moderate memory deficits following donepezil, rivastigmine, etc) may be considered for adults with traumatic brain injury. (Adapted from Cicerone17(p523)) traumatic brain injury who have deficits in memory. The effects of the medication should be assessed using objective and Randomized controlled trial evidence has been pro- functional measures. (Adapted from New Zealand Guidelines vided supporting the efficacy of teaching combined in- Group,100(p98) INCOG16) ternal and external compensatory memory strategies, using errorless learning, in a group format. This inter- The cholinergic system has been associated with vention was structured over 8 modules, presented in attention and memory processing and is also a sys- hour-long sessions twice a week for 4 weeks. Results tem believed to be highly vulnerable to the dam- immediately posttreatment and at 1-month follow-up age associated with TBI, as the regulatory systems showed that compared with wait-list controls, partici- tend to be diffusely spread through the forebrain and pants in the treatment group showed improvement in brainstem.101 Acetylcholinesterase (AChE) inhibitors their knowledge of memory strategies, use of memory improve cholinergic transmission and have been associ- aids, and more effortful processing and problem-solving ated with slowed decline in memory function in people strategies, as well as improvements in performance on with Alzheimer disease.101 In the TBI population, 3 ran- standardized and functional memory tasks.97 domized controlled trial studies have evaluated the ef- A group format has also been used to teach a more ficacy of 2 separate AChE medications: rivastigmine102 structured experimental intervention using the I-MEMs, and donepezil.103,104 Rivastigmine administered to pa- as referred to earlier in this article, in which multi- tients with brain injury at a maximum dose of 12 mg ple internal strategies (semantic association, elaboration, daily over 2 titration periods as well as maintenance chaining, and imagery) are taught, along with “com- period was only associated with statistically significant plementary” external strategies (memory book, PDA, improvements on self-report measures of general mem- etc) across 12 structured sessions. Training methods ory and attention functioning,102 with no effect evident combined errorless learning and metacognitive strate- on standardized cognitive measures. gies (self-generation and awareness). While gains were Donepezil administered initially at a dose of 5 mg made across all levels of memory severity, better out- for 3 weeks and then increased to 10 mg for 3 weeks, comes on both standardized and functional tasks were the standard dosing for patients with Alzheimer dis- found for mild to moderately memory-impaired pa- ease, was associated with some improvement on a stan- tients and for those with better executive cognitive dardized test of mental control, naming and short-term skills.34 This supports the findings, stated earlier, that recall, in a small randomized control trial study in- individuals with severe memory and/or executive im- volving 26 patients with brain injury compared with pairments are less able to implement internal memory matched controls. Increased cortical metabolism was strategies. also evident bilaterally across the mid frontal region, Group instruction in the practical use of memory aids posterior parietal area, and temporal and occipital lobes has also been found to increase the number of memory on FDG-PET (fludeoxyglucose positron emission to- aids used by patients compared with wait-list controls.98 mographic) scans.103 Zhang et al104 used similar dos- Group programs that have integrated external and in- ing in a randomized, placebo-controlled, double-blind, ternal strategies while also focusing on fostering social crossover trial involving a relatively small sample of 18 support among memory-impaired patients showed ad- individuals with TBI who were in the post–acute phase ditional benefits in reducing symptoms of anxiety and of recovery. Improvements were found during the pe- depression.99 Preliminary evidence for the efficacy of riod of medication administration on standardized mea- group instruction in reducing “everyday memory fail- sures of attention using the PASAT (Paced Auditory ures” was provided in a 9-week memory notebook treat- Serial Addition Test) and immediate auditory and vi- ment program that incorporated both behavioral learn- sual recall, with sustained effects through the “washout” ing principles and educational strategies for individu- phase. www.headtraumarehab.com

The remaining studies were typically open- associated with injury to the brain.5 Recently, these label trials. They included 2 studies incorporating technologies have been advocated in nonclinical larger sample sizes,105,106 5withsmallernumbers populations, with a substantially growing application of participants,107–110 and single and case series of such techniques with older adults and with children, designs.111–114 All involved donepezil titrated to 10 mg as well as with neurologically injured populations, with daily over 3 to 4 weeks. The exception to this was the the goal of improving cognitive function or, in the Tenovuo106 study, which also included description of case of older adults, slowing decline. There is, however, the effects of treatment with other central AChE in- no substantive evidence to indicate improvement in hibitors, rivastigmine and galantamine. Generally, very memory functions beyond the trained tasks. This was modest positive effects were evident on standardized demonstrated in a randomized controlled trial involving measures of memory and/or self-report of cognitive more than 11 000 viewers of a popular BBC show. Two symptoms and no significant difference was found be- experimental groups logged on and performed specific tween any of the 3 central AChE inhibitors used.113 In training tasks modeled after those commercially avail- addition, improvements in executive functioning using able, whereas the control group spent the same amount fluency and trail making tests as well as affective symp- of time answering obscure questions from 6 categories. toms were also associated with the use of donepezil.108 After 6 weeks, no improvement was found on standard- Using a block design matching procedure for control ized tests of cognitive skills, including memory.116 subjects compared with 36 patients with brain injury, Computer-based brain training as a restorative tech- donepezil treatment was associated with modest im- nique has gained clinical popularity in the brain in- provements only in cognition for the patients who jury population, with weak and mixed outcomes from were earlier in the acute rehabilitation process (about preliminary studies that are typically poorly controlled. 1month)relativetothoseclosertothe3-monthstage. One study using a within-subject pre-post design evalu- However, it was opined that the poorer results of this ated a remotely delivered series of structured exercises to study may have been related to the use of FIM (Func- patients in their homes. Variable results were found, with tional Independence Measure) change and efficiency some positive association between subjective reports of scores to assess cognition, whereby ratings are provided improvement in cognitive ability and performance on by therapists, rather than performance-based measures the Automated Neuropsychological Assessment Metrics of cognition.109 Improvement in general clinical abili- (ANAM4).5 A literature review has suggested that com- ties was also noted by therapist-raters for patients using a puter programs integrating hierarchically based training donepezil and vitamin E combination110 and when fam- in which task difficulty is increased as more basic skills ily members’ ratings of the patient were integrated.114 are demonstrated can be more effective.117 However, Currently, the evidence indicates very modest results general outcome data showing gains are confined to psy- using central AChE inhibitors to improve memory in chometric and structured therapy tasks, although there is patients with brain injury. Future studies should use also some evidence for changes in neuroimaging.118–120 more prospective, randomized, double-blind, placebo- The functionality of such changes with respect to re- controlled, clinical trials, with randomization stratified duction in disability or generalization of skills into for age, injury severity, and time since injury. daily activities has not been demonstrated, especially for independently used programs.121 In a review ar- Memory #7. Restorative techniques such as computer-based ticle, it was suggested that computer-assisted memory training show no evidence in enhancing sustained memory training is most likely to be effective if sessions are performance. Guidelines in using such techniques indicate therapist-driven, train basic memory skills, and inte- that it should only be considered to develop adjunct memory grate those skills into ecologically valid tasks, tailored rehabilitation strategies with evidence-based instructional and compensatory strategies, and only if developed in conjunction to the patient with brain injury and generalized into 122 with a therapist with a focus on strategy development and practical tasks. In a prospective cohort study, com- 123 transfer to functional tasks. puterized training (Cogmed QM), combined with coaching during the training sessions by therapists, ed- Restorative techniques differ from compensatory ucation regarding the functional integration of strate- techniques in that they focus directly on restoring gies, as well as peer support (30 minutes to exchange impaired cognitive functioning through repetitive experiences), was effective in improving functioning on exercises performed in massed practice trials. These daily tasks in a sample of participants with moderate involved paper-and-pencil tasks prior to current techno- to severe memory impairments.123 This demonstrated logical advances115 and now are generally delivered via that computer training alone was not effective in im- computer. Computer-based restorative rehabilitation proving performance on functional tasks but should techniques were developed following the concept of be combined with instructional and compensatory neural plasticity to remediate cognitive impairments strategies.

DISCUSSION use of memory aids, and the availability of a support person to facilitate the use of aids. Both errorless learning Overall, there is evidence that, while restorative mem- and spaced retrieval techniques are effective methods of ory training in itself is unlikely to be efficacious in learning in individuals with TBI. However, studies have restoring impaired memory, both internal and external consistently shown that all interventions are more likely memory strategies may be used successfully to allevi- to be effective if tailored to the individual and applied ate memory difficulties in individuals with TBI. The in the context of the individual’s daily life. More com- extent to which these may be effective depends, how- prehensive, well-designed trials incorporating appropri- ever, on a number of factors. Internal strategies are only ate blinding and use of both objective and everyday likely to be effective in individuals with sufficient moti- functional measures of memory are needed to establish vation, self-awareness, and executive function to be able the efficacy of anticholinesterase inhibitors in alleviating to identify the situations in which they are applicable memory impairments. Sufficient well-controlled studies and follow through with using them. Thus, the evidence do not exist supporting the independent use of restora- would suggest that they are more appropriate for use in tive techniques such as computer-based programs as a individuals with mild-moderate memory impairments. strategy to restore impaired memory processes. Rather, Those with more severe memory impairments are more the evidence to date suggests that such techniques may likely to benefit from external strategies, which will also be considered if used in conjunction with compen- be of assistance to people with mild-moderate memory satory techniques, occur with a therapist, are strategy- problems. The nature of the most appropriate external driven, and the skills learned are translated to functional strategy will depend on the individual’s age and previous tasks. experience with technology, his or her literacy, preinjury

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