INCOG 2.0 Guidelines for Cognitive Rehabilitation Following Traumatic Brain Injury, Part II: Attention and Information Processing Speed : The Journal of Head Trauma Rehabilitation

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INCOG 2.0 Guidelines for Cognitive Rehabilitation Following Traumatic Brain Injury, Part II: Attention and Information Processing Speed

Ponsford, Jennie AO, PhD, MA; Velikonja, Diana PhD, MScCP; Janzen, Shannon MSc; Harnett, Amber MSc, BSc; McIntyre, Amanda RN; Wiseman-Hakes, Catherine PhD, Reg CASLPO; Togher, Leanne PhD, BAppSc; Teasell, Robert MD, FRCPC; Kua, Ailene MSc, PMP; Patsakos, Eleni MSc; Welch-West, Penny MCLSc, SLP Reg CASLPO; Bayley, Mark Theodore MD, FRCPC

Editor(s): Bayley, Mark MD; Ponsford, Jennie AO, MA, PhD

Author Information

Monash-Epworth Rehabilitation Research Centre, Turner Institute for Brain and Mental Health, School of Psychological Sciences, Monash University, Melbourne, Australia, and Epworth Healthcare, Melbourne Australia (Dr Ponsford); Acquired Brain Injury Program, Hamilton Health Sciences, Hamilton, Ontario, Canada, and Department of Psychiatry and Behavioural Neurosciences, DeGroote School of Medicine, McMaster University, Hamilton, Ontario, Canada (Dr Velikonja); Lawson Health Research Institute, Parkwood Institute, London, Ontario, Canada (Mss Janzen, Harnett, and McIntyre and Dr Teasell); Speech Language Pathology Program, School of Rehabilitation Science, McMaster University, Hamilton, Ontario, Canada, and KITE Research Institute, Toronto Rehabilitation Institute—University Health Network, Toronto, Ontario, Canada (Drs Wiseman-Hakes and Bayley and Mss Patsakos and Kua); Faculty of Health Sciences, The University of Sydney, New South Wales, Australia, and NHMRC Centre of Research Excellence in Aphasia Rehabilitation, Australia (Dr Togher); Department of Physical Medicine and Rehabilitation, Schulich School of Medicine & Dentistry, University of Western Ontario, London, Ontario, Canada (Dr Teasell); Parkwood Institute, St Joseph's Health Care, and School of Communication Sciences and Disorders, University of Western Ontario, London, Ontario, Canada (Ms Welch-West); and Temerty Faculty of Medicine, University of Toronto, Ontario, Canada (Dr Bayley); on behalf of the INCOG Expert Panel.

Corresponding Author: Jennie Ponsford, AO, PhD, MA, Monash-Epworth Rehabilitation Research Centre, Epworth Healthcare, 89 Bridge Rd, Richmond, Victoria 3121, Australia ([email protected]).

The authors gratefully acknowledge the support of the Ministry of Health of the province of Ontario, Canada.

The project described in this manuscript was funded through the Ministry of Health of the province of Ontario, Canada (Lead: Dr Mark Bayley). The authors declare that no competing financial interests exist. The authors further declare that the funders did not participate in the organization of the project, nor the expert panel process, evidence synthesis, or formulation of the recommendations. The opinions, results and conclusions reported are those of the authors. No endorsement by the Ontario Ministry of Health is intended or should be inferred.

The authors declare no conflicts of interest.

This is an open-access article distributed under the terms of the Creative Commons Attribution-Non Commercial-No Derivatives License 4.0 (CCBY-NC-ND), where it is permissible to download and share the work provided it is properly cited. The work cannot be changed in any way or used commercially without permission from the journal.

Journal of Head Trauma Rehabilitation 38(1):p 38-51, January/February 2023. | DOI: 10.1097/HTR.0000000000000839
  • Open

Abstract

ATTENTION IS A COMPLEX and multidimensional construct. Component processes identified in theoretical models include arousal, selective attention, speed of information processing, and strategic control of attention, including sustained attention, shifting, and dividing of attention and working memory.1 Traumatic brain injury (TBI) may disrupt any or all of these processes, given its diffuse nature and high frequency of injury to neural networks and neurotransmitter systems in the frontotemporal and midbrain reticular activating systems.2 Among individuals with TBI, experimental studies have confirmed the presence of slowed information processing,3–5 working memory difficulties,6,7 impaired vigilance or sustained attention,8,9 difficulty dividing attention with high working memory load,5,10,11 behavioral distraction,12 and problems with goal-directed allocation of attention.13,14 Attention represents an important component of executive function, memory, and communication,15 and the reader is therefore also referred to the INCOG reviews of interventions for executive functions,16 memory,17 and cognitive-communication difficulties.18 Attentional difficulties are reported by more than 60% of individuals with moderate to severe traumatic brain injury (MS-TBI) over 10 or more years postinjury19–21 and are also common following mild TBI.22 Attentional impairments contribute to difficulty with work, study, and social interaction.19 They may also be associated with impairments of hearing, including central auditory processing23 or vision, or with anxiety,24 fatigue,25 and sleep-wake disturbances.26 Therefore, improving or maximizing attention represents an important rehabilitation goal. A recent survey of 115 allied health professionals worldwide identified that addressing attentional impairments was the second most commonly reported focus of cognitive rehabilitation.27 However, increased awareness of up-to-date evidence is needed to facilitate informed clinical practice. As such, the purpose of this article was to evaluate the effectiveness of specific approaches to ameliorating attentional difficulties, including pharmacologic interventions, to provide an update to the INCOG 2014 guidelines for the management of attention in individuals with TBI.28

METHODS

Updated INCOG guideline

The reader is referred to the Methods article of this series (INCOG 2.0: Methods, Overview, and Principles)29 for a complete review of the strategies used for the updated literature review (after 2014) and development of the recommendations and other tools. The Updated INCOG (with INCOG being an acronym standing for “International Cognitive”) Guideline follows a thorough search, review, and critical evaluation of currently published studies in adults for each domain including principles of assessment, posttraumatic amnesia, attention, memory, executive functions, and cognitive communication. An international expert panel comprising TBI cognitive rehabilitation researchers and clinicians from the first version of INCOG formed the authors. In preparation, a detailed internet and MEDLINE search was conducted to identify new published TBI and cognitive rehabilitation evidence-based guidelines (after 2014). A systematic search (2014 to July 2021) of multiple databases (MEDLINE, EMBASE, Cochrane, CINAHL, PsycINFO) was also conducted to identify TBI articles and reviews. Research articles meeting inclusion but published after July 2021 were added on the basis of the discretion of the expert panel. Two authors independently aligned the research articles within the existing INCOG guidelines and flagged areas where new guidelines may be warranted on the basis of the research evidence. This synopsis of evidence for attention was distributed to the INCOG 2022 attention working group. During the series of videoconference meetings, the working group examined the recommendations matrix and updated some recommendations based on new evidence, articulated novel recommendations based on the evidence available, and considered the clinical applicability of recommendations to enhance outcomes for individuals with TBI. For each recommendation, the cumulative evidence (studies used in the original guidelines and new articles) was evaluated by the panel in terms of study design and study quality to determine the level of evidence grading (see Table 1). All relevant references from 2014 were consolidated into a reference library that was made available to the author teams as they drafted the article and finalized the recommendations accordingly. Consensus of the working group was reached when members unanimously agreed to the wording and evidence grading assignment of all the recommendations. By the end, the team added 27 new references related to attention from 2014 and after for inclusion in the recommendations in this article. The clinical algorithm and audit tool was updated accordingly in the management area of attention.

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 relevant control group.
B: Recommendation supported by cohort studies that at minimum have a comparison group (includes small randomized controlled trials) and well-designed single case experimental designs.
C: Recommendation supported primarily by expert opinion based on their experience though uncontrolled case studies or series may also be included here.

LIMITATIONS OF USE AND DISCLAIMER

These guidelines are informed by evidence for TBI cognitive rehabilitation interventions published up to time of review. Relevant evidence published after the INCOG guideline could influence the recommendations contained herein. Clinicians must also consider their own clinical judgment, patient preferences, and contextual factors such as resource availability in their decision-making processes about implementation of these recommendations.

The INCOG developers, contributors, and supporting partners shall not be liable for any damages, claims, liabilities, costs, or obligations arising from the use or misuse of this material, including loss or damage arising from any claims made by a third party.

RESULTS

Recommendations and literature review

The expert panel made 11 recommendations, with 2 new recommendations, 5 updated from INCOG 2014, and 4 remaining unchanged from INCOG 2014. Six recommendations are based on level A evidence, 3 on level B, and 2 on level C evidence. Since 2014, there have been 27 studies published in this area. Table 2 sets out the recommendations and supporting evidence for each.

TABLE 2 - INCOG 2.0 guideline recommendations for attention and information-processing speed and new supporting evidencea
Guideline recommendation Grade Reviews RCTs Other
Nonpharmacological interventions for attention/information processing speed
Attention no. 1 Clinicians should screen for and address factors that impact attention including hearing, vision, fatigue, sleep-wake disturbance, anxiety, depression, pain, substance use, and medication (updated from INCOG 2014,28 (p326) Attention 4). C Johansson et al30
Attention no. 2 Metacognitive strategy training using functional everyday activities should be considered for individuals with TBI, especially those with mild-moderate attention deficits (updated from INCOG 2014,28 (pp324–325) Attention 1). A Cicerone et al50 Dymowski et al35
Roitsch et al40
Virk et al36
Attention no. 3 Computer-based de-contextualized attentional tasks for individuals with TBI are NOT recommended because of lack of demonstrated impact on everyday attentional functions. Everyday task-specific training should be considered but cannot be expected to generalize beyond trained or similar tasks (updated from INCOG 2014,28 (pp326–327) Attention 6). B Bogdanova et al41 Dundon et al51
Cicerone et al50 Straudi et al42
Attention no. 4 Training in dual tasking for individuals with TBI can be used to improve dual-task performance, only on tasks similar to those trained (INCOG 2014,28 (p325) Attention 2). A
Attention no. 5 Training with periodic random auditory alerting tones is not recommended for addressing attentional deficits following TBI (INCOG 2014,28 (p327) Attention 7). B Dymowski et al35
Attention no. 6
 Training in mindfulness-based meditation techniques is not recommended for remediation of attention deficits (INCOG 2014,28 (pp327–328) Attention 8). A
Attention no. 7 Alterations to the environment and tasks may be used to reduce the impact of attentional deficits on daily activities for individuals with TBI (INCOG 2014,28 (p326) Attention 5). C Dymowski et al35
Attention no. 8 The use of repetitive transcranial magnetic stimulation (rTMS) and transcranial direct current stimulation (tDCS) to ameliorate attention following TBI is not recommended outside of the context of a research trial protocol (INCOG 2022). B Ahorsu et al65 Lee and Kim64 Boissonault et al67
Nousia et al66 Neville et al63
Rushby et al61
Sacco et al62
Ulam et al60
Pharmacological management for attention/information-processing speed
Attention no. 9 Methylphenidate (initiated at a dose of approximately 0.10 mg/kg and increased gradually to a target of 0.25-0.30 mg/kg bid) is recommended in adults with TBI to enhance speed of information processing (updated from INCOG 2014,28 (p328) Attention 9). A Barnett and Reid74 Dorer e al72
Chien et al76 Dymowski et al73
Huang et al75 Jenkins et al78
Johansson et al30
Manktelow et al71
Moreno-Lopez70
Zhang and Wang69
Attention no. 10 While amantadine may enhance arousal in patients in a minimally conscious state, it should not be used to enhance attentional functions following emergence from coma (updated from INCOG 2014,28 (p328) Attention 10). A Hammond et al84
Attention no. 11 The traditional Chinese medicine MLC901 (NeuroAiD IITM) may enhance complex attention in individuals with mild-moderate TBI (INCOG 2022). A Theadom et al86
Abbreviations: RCTs, randomized controlled trials; TBI, traumatic brain injury.
aRefer to Ponsford et al28 for evidence contributing to the recommendations prior to 2014.

Nonpharmacological strategies to enhance attention

Attention no. 1: Clinicians should screen for and address factors that impact attention including hearing, vision, fatigue, sleep-wake disturbance, anxiety, depression, pain, substance use, and medication (updated from INCOG 2014,28(p326) Attention 4). Level C evidence.

Other factors, some of which may be related to the brain injury, may exacerbate attentional difficulties, including hearing and central auditory processing disorder, vision, fatigue, sleep-wake disturbances, anxiety, depression, pain, substance use, and medication. Therefore, this recommendation has been expanded to cover this broader range of symptoms that may affect attention. It is important to screen for the potential impact of these factors while assessing attention using neuropsychological measures and rating scales and address them wherever possible. It is imperative that accommodations are made for sensory loss or disturbance, including availability of eyeglasses and hearing aids to ensure accurate assessment and interventions (in attention). Methylphenidate may be used to treat fatigue, resulting in increased speed of information processing.30 One small cohort study has shown that individualized treatment of sleep-wake disorders may result in self-reported improvements in attention,31 but there have been no controlled trials evaluating the impact of nonpharmacological interventions for sleep-wake disturbance on attention after TBI. We failed to identify any study that formally evaluated the impact of interventions for anxiety, depression, pain, substance use, and medication changes on attention in individuals with TBI. Nevertheless, it is our expert opinion that such factors should be considered and addressed before implementing other forms of intervention.

Attention no. 2: Metacognitive strategy training using functional everyday activities should be considered for individuals with TBI, especially those with mild-moderate attention deficits (updated from INCOG 2014,28(pp324–325) Attention 1). Level A evidence.

This recommendation has been updated from INCOG 2014. In the INCOG 2014 guideline, we reported level A evidence that strategies may be developed, practiced, and applied to compensate for attentional problems, specifically speed of information processing. This evidence came from the work of Fasotti et al32 in trialing time pressure management (TPM) to enhance coping with slowed information processing. The 3-step training program facilitates awareness of manifestations of mental slowness in daily activities and encourages the development of managing steps before or during task performance to reduce time pressure.32 There have been no additional controlled studies of TPM among TBI published since that by Fasotti et al.32

Evidence regarding the use of strategy training (eg, chunking, pacing) to alleviate problems with working memory and divided attention in everyday life after TBI remains confined to 2 case series studies: by Cicerone33 in mild TBI and by Vallat-Azouvi et al34 in 2 highly motivated individuals with severe TBI.

A case series (n = 3) by Dymowski et al35 examined effects of 3 to 4 weeks of individualized strategy training on attention, relative to that of computerized attention training using Attention Process Training (APT-III) after severe TBI. Variability in attentional deficits and everyday attentional requirements necessitated individualized goals and approaches and highlighted the need to address the interplay of fatigue, mood, memory, and executive dysfunction with attentional behavior. All participants achieved individual goals after strategy training (eg, stay on task, complete a full day of work, manage anxiety, pay attention during introductions). Improvements in speed of processing occurred in both conditions but were greatest following strategy training. Although limited generalization was evident on participant self-ratings of attention, close-other ratings of attentional behavior improved more after strategy training than APT. Individualized strategy training was also generally preferred by participants over computerized training. The work by Dymowski et al35 highlights the need for metacognitive strategy training to be individualized and to accommodate the impact of other impairments on attention such as mood and fatigue.

A systematic review and meta-analysis by Virk et al36 found no evidence of significant overall improvement in attention in response to intervention, but this was based on 4 disparate studies with a TBI population.32,37–39 A quality appraisal of systematic reviews for behavioral treatments of attention disorders after TBI by Roitsch et al40 concluded that effects of direct attention training are minimal and limited to training tasks, with more evidence supporting training in strategy use to reduce the impact of attentional impairments.

Attention no. 3: Computer-based de-contextualized attentional tasks for individuals with TBI are not recommended because of lack of demonstrated impact on everyday attentional functions. Everyday task-specific training should be considered but cannot be expected to generalize beyond trained or similar tasks (updated from INCOG 2014,28(pp326–327) Attention 6). Level B evidence.

This recommendation has been updated to reflect a continuing lack of evidence of generalization beyond the specifically trained attentional tasks. There continues to be a significant focus on the use of training exercises to ameliorate impairments of attention.27 These exercises are predominantly computer-mediated and decontextualized, delivered on the premise that training underlying components of attention will result in improved attentional performance in other contexts. Bogdanova et al41 reviewed 28 studies using computerized, cognitive interventions targeting attention and executive functions in adults with acquired brain injury. The review reported significantly greater gains in computerized retraining groups in 8 of 11 TBI-only studies. The gains reported were on neuropsychological measures only, with a few studies additionally including self-report measures. There was no objective evidence of generalization to everyday attentional behaviors. The authors noted many methodological limitations of these studies, including the absence of control groups, ecologically valid outcome assessments, and long-term follow-up. One further study by Straudi et al42 similarly found positive impacts of video game performance on selective attention measures only.

Attention Process Training is a widely used computerized attention training program that has been evaluated in studies with variable methodological rigor and small samples.43–47 Repeated practice on any task may facilitate the development of strategies that improve task performance.48 Although the most recent version of APT (APT-III) includes increased emphasis on development of compensatory strategies within training, we argue that strategy development may be more effective if applied and practiced directly in the context of real-world activities, rather than on decontextualized tasks. Consistent with this premise, Park and Ingles49 concluded from an earlier meta-analysis that training in specific skills can result in improvements in that skill, which may also be evident on tasks similar to those trained, but it cannot be assumed that underlying attentional mechanisms are being restored. The INCOG recommendation deviates from that of the updated review of studies conducted from 2009 to 2014 by Cicerone et al,50 who supported working memory training based on a single case study in stroke and did not clearly differentiate repeated drill practice from strategy development.

One well designed study by Dundon et al51 studied training in capacity to focus attention on speech in noisy or distracting environments. After recruiting individuals with post–acute TBI who self-reported being easily distracted, they demonstrated a linear decline in dichotic listening performance with the presence of a second stream of irrelevant speech. The cognitive training procedure based on APT included graded exposure to irrelevant noise in adaptive and nonadaptive training schedules as compared with no treatment. Both types of training resulted in improvements in dichotic listening and naturalistic tasks of performance in noise, and measures of selective attention and event-related potentials linked to target processing. There were, however, no self-reported gains in everyday distractibility. Although Dundon et al.51 demonstrated that specific training can result in changes that generalize to performance of similar measures, it does not generalize more broadly to impact everyday activities.

Attention no. 4: Training in dual-tasking for individuals with TBI can be used to improve dual-task performance, only on tasks similar to those trained (updated from INCOG 2014,28(p325) Attention 2). Level A evidence.

This recommendation remains unchanged, with no new evidence. The evidence supporting this recommendation comes from 2 small lower-quality unblinded randomized controlled trials (RCTs). The first RCT by Evans et al52 provided training in combining walking with cognitive activities as compared with treatment as usual. The second RCT by Couillet et al37 trained participants to divide their attention between 2 cognitive tasks of increasing difficulty, each learned individually beforehand. Both studies demonstrated significant training effects on trained and similar tasks. These findings reinforce the conclusion that individuals with TBI can benefit from training on specific tasks or activities. To maximize functional impact from such training, it would seem most pragmatic to provide such training on tasks that need to be performed in everyday life.

Attention no. 5: Training with periodic random auditory alerting tones is not recommended for addressing attentional deficits following TBI (updated from INCOG 2014,28(p327) Attention 7). Level B evidence.

This recommendation is unchanged as no further evidence has emerged regarding the use of self-alerting or external alerting tones to facilitate arousal and attentional performances after TBI. These strategies were used by Dymowski et al35 in their single case studies to facilitate self-monitoring. Manly and colleagues53 found that providing a brief auditory alerting stimulus as a cue to consider the goal of an activity improved performance on the “Hotel task.” A larger study by Sweeney et al54 found that periodic auditory alerts did not improve performance of a virtual reality prospective memory task that simulated working in a furniture warehouse. There remains insufficient evidence to suggest that periodic alerting enhances the allocation, or switching, of attention across complex tasks.

Attention no. 6: Training in mindfulness-based meditation techniques is not recommended for remediation of attention deficits (updated from INCOG 2014,28(pp327–328) Attention 8). Level A evidence.

No new evidence has been published on this topic and the recommendation remains unchanged from INCOG 2014. Consensus was that this intervention should not be used outside of research protocols due to lack of demonstrated evidence. Although less rigorous studies have reported benefits from self-instructional and mindfulness techniques,55–57 an RCT by McMillan et al38 found that a brief mindfulness meditation technique, involving audiotape training to control attention by concentrating on breathing over extended periods, did not reduce cognitive failures or improve attention, memory, or psychological adjustment more than physical fitness training or no treatment.

Attention no. 7: Alterations to the environment and tasks may be used to reduce the impact of attentional deficits on daily activities for individuals with TBI (updated from INCOG 2014,28(p326) Attention5). Level C evidence.

This recommendation is also unchanged. Individuals with TBI who have significant cognitive impairments and those who lack awareness of their difficulties are rarely able to initiate the use of compensatory strategies to alleviate attentional problems.58 An intervention approach that does not rely on active participation by the person with TBI could include making changes to the environment or tasks to reduce the impact of attentional problems. In the context of work or study, this might involve removing distractions (eg, work in a quiet room, reduce interruptions), altering tasks to reduce the speed, amount or complexity of information to be processed, providing information in written form to ensure that it is understood, or providing prompts to refocus or shift attention to another aspect of a task. The case studies performed by Dymowski et al35 used some of these strategies including minimizing distraction and environmental cueing, which focused on specific attention-related goals, alongside compensatory strategies such as TPM. We could find no clinical trials evaluating the use of such strategies, despite their reported use in clinical settings.59

Attention no. 8: The use of repetitive transcranial magnetic stimulation (rTMS) and transcranial direct current stimulation (tDCS) to ameliorate attention following TBI is not recommended outside of the context of a research trial protocol (INCOG 2022). Level B evidence.

This is a new recommendation to account for the progressive but still limited research in the field of tDCS and rTMS. Numerous studies have investigated the impact of noninvasive brain stimulation, tDCS, and rTMS on attention and working memory after TBI and the findings have been mixed. Given the mixed outcomes and lack of evidence of generalization to everyday attention, the expert panel recommends that, at this time, rTMS and tDCS should not be used outside of a research context.

Ulam et al60 did not find greater gains in performance on tests of attention and working memory following 20-minute sessions of tDCS daily for 10 days relative to a sham control. Rushby et al61 found no significant impact of a single dose of tDCS on working memory (n-back Task Measure) performance. Sacco et al62 found that 10 sessions of tDCS for more than 5 days, followed by computer-assisted training for 40 minutes, resulted in greater improvement in reaction times on a divided attention task than in a sham-treated control group. However, it is unclear whether the gains were due to the tDCS or computer training, or a combined effect. Of RCTs trialing rTMS, Neville et al63 found no significant impact of 10 sessions of rTMS on performance of attentional and processing speed measures (ie, Trail Making Test, Digit Span, Symbol Digit Modalities test) or other cognitive measures. In contrast, a smaller RCT by Lee and Kim64 reported a positive impact of rTMS (30 minutes, 5 days a week) following muscle strengthening and movement therapy (2 weeks) on performance of the Trail Making Test and Stroop Color Word tasks and on the Montgomery-Astberg Depression Rating Scale in comparison with the control group. A recent meta-analysis combining rTMS and tDCS studies65 concluded that noninvasive brain stimulation has a significant positive effect on attentional measures, but no functional outcomes were included. It is important to note that tDCS and rTMS have differing mechanisms of action on the brain, and the INCOG team felt that they should not be combined in a meta-analysis, and the findings should be interpreted with caution. Another review by Nousia et al,66 which also combined these approaches, concluded that there was insufficient evidence to support use of noninvasive brain stimulation for attention or any cognitive function. Most importantly, there is no evidence of generalization of gains from these interventions to everyday activities. Boissonnault et al67 attempted to implement a tDCS protocol in the context of a rehabilitation center but had extremely low recruitment and retention, thus highlighting the limitations of application in a general rehabilitation setting.

Pharmacological strategies for improving attention

Attention no. 9: Methylphenidate (initiated at a dose of approximately 0.10 mg/kg and increased gradually to a target of 0.25-0.30 mg/kg bid) is recommended in adults with TBI to enhance speed of information processing (updated from INCOG 2014,28(p328) Attention 9). Level A evidence.

This recommendation has been updated. Traumatic brain injury is associated with changes in neurotransmitter systems associated with attention. Methylphenidate, a central nervous system stimulant, increases the release and blocks reuptake of dopamine and noradrenaline, resulting in increased synaptic and extracellular concentrations.68 Since INCOG 2014, several new RCTs,30,69–73 1 systematic review,74 and 2 meta-analyses75,76 have been published. As such, the recommendation was modified to reflect the new evidence. The most recent meta-analysis by Chien et al76 found that methylphenidate significantly improved processing speed as measured by Choice Reaction Time and Digit Symbol Coding. Reaction time was inversely associated with duration of treatment; however, there were no statistically significant effects on other measures of attention or working memory. With respect to adverse events, methylphenidate significantly increased heart rate but did not impact blood pressure. Although several studies have evaluated only a single dose of methylphenidate, 1 RCT by Zhang and Wang69 showed efficacy with administration for more than 30 weeks. An inverted U dose-response relationship has been demonstrated between prefrontal dopamine activity and working memory. Stimulants at low dose increased dopamine levels and enhanced arousal and attention, while high doses could impair them.77 In a randomized double crossover study (n = 40), Jenkins et al78 found that patients with low caudate dopamine transporter binding, measured using single photon emission computed tomography, showed significant improvement in response speed with methylphenidate compared with placebo, with concomitant self and caregiver-reported improvements in apathy. Participants with normal dopamine transporter binding did not improve. These findings suggest that identifying the presence of a hypodopaminergic state after TBI may be important for selecting recipients of methylphenidate therapy.

Although everyday attentional measures were not included in the Chien et al76 meta-analysis, several RCTs have shown generalization of gains from methylphenidate to everyday attentional ratings, including the aforementioned study by Jenkins et al.78 Whyte et al79 found generalization to everyday rating of attentional behavior by caregivers, while Willmott and Ponsford80 found a strong trend in that direction, and Johansson et al30 and Zhang and Wang69 found reductions in fatigue ratings.

Attention no. 10: While amantadine may enhance arousal in patients in a minimally conscious state, it should not be used to enhance attentional functions following emergence from coma (updated from INCOG 2014,28(p328) Attention 10). Level A evidence.

This updated recommendation on the use of amantadine is based on the scientific literature since INCOG 2014. Amantadine is a dopaminergic agent that acts presynaptically to enhance dopamine release and decrease dopamine reuptake. It has demonstrated efficacy in facilitating arousal and general function in patients in a comatose or vegetative state when administered over the short term (<4 weeks).81–83 However, it appears not to enhance attentional function when administered to conscious patients at longer periods after injury. Hammond et al84 compared the effects of 100 mg of amantadine twice daily or placebo in 119 individuals with chronic TBI (all >6 months postinjury) and irritability. They evaluated behavioral and cognitive disturbance over 60 days of treatment or placebo and found no significant impact on attentional measures at any time point up to 60 days.

Attention no. 11: The traditional Chinese medicine MLC901 (NeuroAiD IITM) may enhance complex attention in individuals with mild-moderate TBI (INCOG 2022). Level A evidence.

Based on research conducted since the INCOG 2014 review, a recommendation has been added to reflect use of traditional Chinese medicine MLC901. MLC901 (NeuroAiD IITM) is a traditional Chinese herbal supplement with antioxidant properties shown to improve survival, recovery, and cognitive functioning in rodents after ischemic injury.85 Among humans, Theadom et al86 conducted a 9-month pilot randomized placebo controlled trial involving 78 individuals aged 18 to 65 years, 1 to 12 months after mild-moderate TBI (97% mild). They found that participants receiving MLC901 (0.8-g capsules, 3 times daily) showed greater gains on the CNS Vital Signs complex attention measure (P = .04, d = 0.6) at 6 months relative to controls. There were no group differences for self-reported neurobehavioral sequelae, mood, fatigue, physical disability, or overall quality of life at 6 months. No serious adverse events were reported. Replication of this finding is needed.

Algorithm

Clinicians are encouraged to follow the decision algorithm in Figure 1 that highlights how to navigate through this series of guidelines for managing attentional problems, further elaborated in the section “Discussion.”

F1
Figure 1.:
Algorithm: Attention.Following the identification of attentional impairments using neuropsychological assessment and consideration of their everyday manifestations, it is important to consider factors that may be exacerbating attentional problems, including hearing and vision disruptions, fatigue, sleep-wake disturbance, anxiety, depression, pain, medication effects, and substance use, and address these wherever possible. It is also important to consider the individual's level of motivation, self-awareness, memory, and executive functions to determine capacity for adopting strategies, as well as the degree of support from close others and other factors in the environment. To alleviate attentional problems with individuals with mild-moderate impairment and some degree of self-awareness, there is evidence in support of training in metacognitive strategies applied directly to everyday attentional difficulties. Time pressure management may be used to address impaired speed of information processing. Given evidence of learning on trained tasks, training may be provided on specific tasks such as dual tasking or dealing with background noise, but given a lack of evidence of generalization, training should be focused on everyday tasks rather than decontextualized computer tasks. An additional approach that may be used in these individuals as well as those with severe attentional impairment and poor awareness and executive function is modifications to the task (reducing attentional demands) or environment (removing distraction) may be helpful, although studies evaluating these approaches are much needed. Studies evaluating these approaches have included people with mild to severe injuries, generally aged between 16 and 60 years, and having adequate visual acuity, hand function and cognitive function to perform the assessment, and training tasks. Participants were generally excluded if they had other neurological or developmental issues or preexisting psychiatric or substance use problems. They received training between 3 months and many years after injury. Screening measures included a broad range of neuropsychological tests of attention, including the PASAT, Trail Making Test, cancellation, Digit Span and Digit Symbol substitution tasks, and many others. These tasks have also been used to evaluate the outcome of interventions. Outcomes have also been measured in terms of subjectively reported changes and performance on real-world data entry tasks and activity and participation scales. Methylphenidate, administered at 0.3 mg/kg in divided doses, may increase speed of information processing as measured on measures of reaction time and the Symbol Digit Modalities Test and on a Rating Scale of Attentional Behaviour in individuals aged 16 to 60 years who are in acute stages of recovery from mild to severe TBI or longer than 6 months postinjury, have no history of attention deficit hyperactivity disorder previous stimulant use, drug or alcohol dependence, or other psychiatric disorder. Amantadine may facilitate arousal and function on the Disability Rating Scale over the short term in inpatients in vegetative state or emerging from coma, but there is no evidence of positive impact of amantadine on attention following emergence from coma.

Audit tool

Table 3 sets out the audit tool items recommended by the INCOG panel for examining management of attentional problems in clinical settings. Clinicians and organizational leaders are encouraged to use these tools in review or audit of individual patient charts to determine degree of adherence to the recommendations. This is most successful in changing practice when these audit results are fed back to the team for discussion of opportunities for improvement.

TABLE 3 - Audit guidelines for priority recommendations: Attentiona
Intervention (guideline recommendation) Specific activities, devices, or tools Assessment of need and effectiveness Patient characteristics Discipline
Attention training
“Metacognitive strategy training using functional everyday activities should be considered, especially in patients with mild-moderate attention deficits” (Attention no. 2).

  1. □ Combined with metacognitive executive strategy training

  2. □ Functional everyday activities

  3. □ Use of checklists

  4. □ Other

  1. □ Assessment for need conducted

  2. □ Training provided

  1. □ Mild to moderate attention deficit

  1. □ OT

  2. □ PT

  3. □ SLP

  4. □ MD

  5. □ Neuro

  6. □ Other
Training may be conducted on tasks in real-world contexts (eg, dual tasks, background noise) without expectation of generalization (Attention nos. 3 and 4).

  1. □ Functional everyday activities

  1. □ Assessment for need conducted

  2. □ Training provided

  1. □ Mild, moderate, or severe attention deficit

  1. □ OT

  2. □ PT

  3. □ SLP

  4. □ MD

  5. □ Neuro

  6. □ Other
“Alterations to the environment and tasks may be used to reduce the impact of attentional problems on daily activities” (Attention no. 7).

  1. □ Functional everyday activities

  2. □ Environmental manipulation

  3. □ Use of checklists

  4. □ Other

  1. □ Assessment for need conducted

  2. □ Environmental alterations made

  1. □ Mild, moderate, or severe deficit

  1. □ OT

  2. □ PT

  3. □ SLP

  4. □ MD

  5. □ Neuro

  6. □ Other
Pharmaceutical interventions: Attention
Drug Used Indication Patient characteristics Found in
Methylphenidate
“Methylphenidate is recommended to enhance speed of information processing” (Attention no. 9)		 Yes No

  1. □ Attentional function

  2. □ Speed of cognitive processing

  3. □ Sustained attention/vigilance

  4. □ Other (please specify):

  1. □ Mild, moderate, or severe attention deficit

  1. □ Drug charts

  2. □ MD notes

  3. □ Other
aThe audit tool items that the panel voted as the most important for implementation are listed. It is important to note that many different strategies may be applicable and that the language used to describe these interventions is likely to vary across settings and cultures.

DISCUSSION

Given the high frequency of attentional problems in individuals with TBI, it is recommended that all individuals with MS-TBI have a neuropsychological assessment to determine the nature of their attentional difficulties and also assess their everyday manifestations. It is also important to identify and address the attentional demands of the injured individual's lifestyle, availability of environmental supports, and factors that may be exacerbating attentional problems, including hearing and vision disruptions, anxiety, depression, fatigue, sleep disturbance, pain, medication, and substance use.

To alleviate attentional problems, there is evidence in support of training in metacognitive strategies applied directly to everyday attentional difficulties, such as TPM. Given evidence of learning on trained tasks, training may be provided on specific tasks such as dual tasking or dealing with background noise, but given a lack of evidence of generalization, training should be focused on everyday tasks rather than decontextualized computer tasks. Modifications to the task (reducing attentional demands) or environment (removing distraction) may be helpful, although evaluation of such strategies is needed.

Methylphenidate, administered at 0.3 mg/kg in divided doses, may increase speed of information processing, enhance everyday attentional behavior, or reduce fatigue in individuals aged 16 to 60 years who have no history of attention deficit hyperactivity disorder, previous stimulant use, drug or alcohol dependence, or other psychiatric disorder. Amantadine may facilitate arousal over the short term in individuals in vegetative state or emerging from coma, but there is no evidence of positive impact of amantadine on attention in chronic TBI. The traditional Chinese medicine MLC901 (NeuroAiD IITM) in 0.8-g capsules 3 times daily may enhance complex attention in individuals with mild TBI, although replication of this finding is needed.

Research investigating behavioral interventions for attention, in the context of the everyday life of the individual with TBI, including both metacognitive strategies and environmental modifications remains very limited in quantity, quality, and scope. There is a growing body of research supporting the use of contextualized approaches to rehabilitation,87 and the findings from our reviews support this. Unfortunately, clinicians continue to use computerized attention training27 despite there being no clear evidence of generalization to everyday activities. The current guideline was limited to studies conducted in adults. Similar reviews are needed for pediatric TBI. There is an enormous need for further RCTs and well-designed single case studies in both adults and children that evaluate the impact of real-world interventions not only on attentional impairments but also more importantly on the individual's daily life and to identify what works and for whom. Many methodological challenges must be overcome to achieve this, including the development and more universal use of attentional outcome measures that reflect lived experience of everyday attentional function and are psychometrically sound and sensitive to change. Qualitative feedback from individuals receiving the interventions is also needed.

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Keywords:

attention; cognitive rehabilitation; information processing; traumatic brain injury

© 2023 The Authors. Published by Wolters Kluwer Health, Inc.