You are on page 1of 14

J Head Trauma Rehabil

Vol. 38, No. 1, pp. 38–51


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

INCOG 2.0 Guidelines for Cognitive


Rehabilitation Following Traumatic
Downloaded from http://journals.lww.com/headtraumarehab by BhDMf5ePHKav1zEoum1tQfN4a+kJLhEZgbsIHo4XM
i0hCywCX1AWnYQp/IlQrHD3i3D0OdRyi7TvSFl4Cf3VC4/OAVpDDa8KKGKV0Ymy+78= on 07/07/2023

Brain Injury, Part II: Attention and


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

Introduction: Moderate to severe traumatic brain injury (MS-TBI) commonly causes disruption in aspects of
attention due to its diffuse nature and injury to frontotemporal and midbrain reticular activating systems. Attentional
impairments are a common focus of cognitive rehabilitation, and increased awareness of evidence is needed to
facilitate informed clinical practice. Methods: An expert panel of clinicians/researchers (known as INCOG) reviewed
evidence published from 2014 and developed updated guidelines for the management of attention in adults, as well
as a decision-making algorithm, and an audit tool for review of clinical practice. Results: This update incorporated
27 studies and made 11 recommendations. Two new recommendations regarding transcranial stimulation and an
herbal supplement were made. Five were updated from INCOG 2014 and 4 were unchanged. The team recommends
screening for and addressing factors contributing to attentional problems, including hearing, vision, fatigue, sleep-
wake disturbance, anxiety, depression, pain, substance use, and medication. Metacognitive strategy training focused
on everyday activities is recommended for individuals with mild-moderate attentional impairments. Practice on de-
contextualized computer-based attentional tasks is not recommended because of lack of evidence of generalization,
but direct training on everyday tasks, including dual tasks or dealing with background noise, may lead to gains
for performance of those tasks. Potential usefulness of environmental modifications is also discussed. There is
insufficient evidence to support mindfulness-based meditation, periodic alerting, or noninvasive brain stimulation

Author Affiliations: Monash-Epworth Rehabilitation Research Centre, The authors gratefully acknowledge the support of the Ministry of Health of the
Turner Institute for Brain and Mental Health, School of Psychological province of Ontario, Canada.
Sciences, Monash University, Melbourne, Australia, and Epworth
The project described in this manuscript was funded through the Ministry
Healthcare, Melbourne Australia (Dr Ponsford); Acquired Brain Injury
of Health of the province of Ontario, Canada (Lead: Dr Mark Bayley).
Program, Hamilton Health Sciences, Hamilton, Ontario, Canada, and
The authors declare that no competing financial interests exist. The authors
Department of Psychiatry and Behavioural Neurosciences, DeGroote
further declare that the funders did not participate in the organization of the
School of Medicine, McMaster University, Hamilton, Ontario, Canada
project, nor the expert panel process, evidence synthesis, or formulation of the
(Dr Velikonja); Lawson Health Research Institute, Parkwood Institute,
recommendations.The opinions, results and conclusions reported are those of
London, Ontario, Canada (Mss Janzen, Harnett, and McIntyre and Dr
the authors. No endorsement by the Ontario Ministry of Health is intended or
Teasell); Speech Language Pathology Program, School of Rehabilitation
should be inferred.
Science, McMaster University, Hamilton, Ontario, Canada, and KITE
Research Institute, Toronto Rehabilitation Institute—University Health This is an open-access article distributed under the terms of the Creative
Network, Toronto, Ontario, Canada (Drs Wiseman-Hakes and Bayley Commons Attribution-Non Commercial-No Derivatives License 4.0
and Mss Patsakos and Kua); Faculty of Health Sciences, The University of (CCBY-NC-ND), where it is permissible to download and share the work
Sydney, New South Wales, Australia, and NHMRC Centre of Research provided it is properly cited. The work cannot be changed in any way or used
Excellence in Aphasia Rehabilitation, Australia (Dr Togher); Department commercially without permission from the journal.
of Physical Medicine and Rehabilitation, Schulich School of Medicine &
Dentistry, University of Western Ontario, London, Ontario, Canada (Dr The authors declare no conflicts of interest.
Teasell); Parkwood Institute, St Joseph’s Health Care, and School of
Corresponding Author: Jennie Ponsford, AO, PhD, MA, Monash-Epworth
Communication Sciences and Disorders, University of Western Ontario,
Rehabilitation Research Centre, Epworth Healthcare, 89 Bridge Rd, Rich-
London, Ontario, Canada (Ms Welch-West); and Temerty Faculty of
mond, Victoria 3121, Australia (jennie.ponsford@monash.edu).
Medicine, University of Toronto, Ontario, Canada (Dr Bayley); on behalf
of the INCOG Expert Panel. DOI: 10.1097/HTR.0000000000000839
38
INCOG 2.0 Guidelines for Cognitive Rehabilitation Following Traumatic Brain Injury, Part II 39

for alleviating attentional impairments. Of pharmacological interventions, methylphenidate is recommended to


improve information processing speed. Amantadine may facilitate arousal in comatose or vegetative patients but
does not enhance performance on attentional measures over the longer term. The antioxidant Chinese herbal
supplement MLC901 (NeuroAiD IITM) may enhance selective attention in individuals with mild-moderate TBI.
Conclusion: Evidence for interventions to improve attention after TBI is slowly growing. However, more controlled
trials are needed, especially evaluating behavioral or nonpharmacological interventions for attention. Key words:
Downloaded from http://journals.lww.com/headtraumarehab by BhDMf5ePHKav1zEoum1tQfN4a+kJLhEZgbsIHo4XM

attention, cognitive rehabilitation, information processing, traumatic brain injury


i0hCywCX1AWnYQp/IlQrHD3i3D0OdRyi7TvSFl4Cf3VC4/OAVpDDa8KKGKV0Ymy+78= on 07/07/2023

A TTENTION IS A COMPLEX and multidimen-


sional construct. Component processes identified
in theoretical models include arousal, selective atten-
METHODS

Updated INCOG guideline


tion, speed of information processing, and strategic con-
The reader is referred to the Methods article of
trol of attention, including sustained attention, shifting,
this series (INCOG 2.0: Methods, Overview, and
and dividing of attention and working memory.1 Trau-
Principles)29 for a complete review of the strategies
matic brain injury (TBI) may disrupt any or all of these
used for the updated literature review (after 2014)
processes, given its diffuse nature and high frequency of
and development of the recommendations and other
injury to neural networks and neurotransmitter systems
tools. The Updated INCOG (with INCOG being an
in the frontotemporal and midbrain reticular activating
acronym standing for “International Cognitive”) Guide-
systems.2 Among individuals with TBI, experimental
line follows a thorough search, review, and critical
studies have confirmed the presence of slowed infor-
evaluation of currently published studies in adults
mation processing,3–5 working memory difficulties,6,7
for each domain including principles of assessment,
impaired vigilance or sustained attention,8,9 diffi-
posttraumatic amnesia, attention, memory, executive
culty dividing attention with high working memory
functions, and cognitive communication. An inter-
load,5,10,11 behavioral distraction,12 and problems with
national expert panel comprising TBI cognitive re-
goal-directed allocation of attention.13,14 Attention rep-
habilitation researchers and clinicians from the first
resents an important component of executive function,
version of INCOG formed the authors. In prepara-
memory, and communication,15 and the reader is
tion, a detailed internet and MEDLINE search was
therefore also referred to the INCOG reviews of in-
conducted to identify new published TBI and cognitive
terventions for executive functions,16 memory,17 and
rehabilitation evidence-based guidelines (after 2014).
cognitive-communication difficulties.18 Attentional dif-
A systematic search (2014 to July 2021) of multiple
ficulties are reported by more than 60% of individuals
databases (MEDLINE, EMBASE, Cochrane, CINAHL,
with moderate to severe traumatic brain injury (MS-
PsycINFO) was also conducted to identify TBI arti-
TBI) over 10 or more years postinjury19–21 and are
cles and reviews. Research articles meeting inclusion
also common following mild TBI.22 Attentional im-
but published after July 2021 were added on the ba-
pairments contribute to difficulty with work, study,
sis of the discretion of the expert panel. Two authors
and social interaction.19 They may also be associated
independently aligned the research articles within the
with impairments of hearing, including central audi-
existing INCOG guidelines and flagged areas where new
tory processing23 or vision, or with anxiety,24 fatigue,25
guidelines may be warranted on the basis of the re-
and sleep-wake disturbances.26 Therefore, improving
search evidence. This synopsis of evidence for attention
or maximizing attention represents an important re-
was distributed to the INCOG 2022 attention working
habilitation goal. A recent survey of 115 allied health
group. During the series of videoconference meetings,
professionals worldwide identified that addressing at-
the working group examined the recommendations ma-
tentional impairments was the second most commonly
trix and updated some recommendations based on new
reported focus of cognitive rehabilitation.27 However,
evidence, articulated novel recommendations based on
increased awareness of up-to-date evidence is needed
the evidence available, and considered the clinical ap-
to facilitate informed clinical practice. As such, the
plicability of recommendations to enhance outcomes
purpose of this article was to evaluate the effective-
for individuals with TBI. For each recommendation,
ness of specific approaches to ameliorating attentional
the cumulative evidence (studies used in the original
difficulties, including pharmacologic interventions, to
guidelines and new articles) was evaluated by the panel
provide an update to the INCOG 2014 guidelines
in terms of study design and study quality to deter-
for the management of attention in individuals with
mine the level of evidence grading (see Table 1). All
TBI.28
relevant references from 2014 were consolidated into

www.headtraumarehab.com
40 Journal of Head Trauma Rehabilitation/January–February 2023

TABLE 1 INCOG level of evidence- have been 27 studies published in this area. Table 2 sets
out the recommendations and supporting evidence for
grading system each.
A: Recommendation supported by at least 1
meta-analysis, systematic review, or Nonpharmacological strategies to enhance attention
randomized controlled trial of appropriate
Downloaded from http://journals.lww.com/headtraumarehab by BhDMf5ePHKav1zEoum1tQfN4a+kJLhEZgbsIHo4XM

size with relevant control group. Attention no. 1: Clinicians should screen for and address
B: Recommendation supported by cohort factors that impact attention including hearing, vision, fatigue,
i0hCywCX1AWnYQp/IlQrHD3i3D0OdRyi7TvSFl4Cf3VC4/OAVpDDa8KKGKV0Ymy+78= on 07/07/2023

studies that at minimum have a sleep-wake disturbance, anxiety, depression, pain, substance
comparison group (includes small
randomized controlled trials) and use, and medication (updated from INCOG 2014,28 (p326)
well-designed single case experimental Attention 4). Level C evidence.
designs. Other factors, some of which may be related to
C: Recommendation supported primarily by the brain injury, may exacerbate attentional difficul-
expert opinion based on their experience ties, including hearing and central auditory processing
though uncontrolled case studies or series
may also be included here. disorder, vision, fatigue, sleep-wake disturbances, anx-
iety, depression, pain, substance use, and medication.
Therefore, this recommendation has been expanded to
a reference library that was made available to the au- cover this broader range of symptoms that may affect
thor teams as they drafted the article and finalized the attention. It is important to screen for the potential
recommendations accordingly. Consensus of the work- impact of these factors while assessing attention us-
ing group was reached when members unanimously ing neuropsychological measures and rating scales and
agreed to the wording and evidence grading assign- address them wherever possible. It is imperative that
ment of all the recommendations. By the end, the accommodations are made for sensory loss or distur-
team added 27 new references related to attention from bance, including availability of eyeglasses and hearing
2014 and after for inclusion in the recommendations aids to ensure accurate assessment and interventions
in this article. The clinical algorithm and audit tool (in attention). Methylphenidate may be used to treat
was updated accordingly in the management area of fatigue, resulting in increased speed of information
attention. 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
LIMITATIONS OF USE AND DISCLAIMER there have been no controlled trials evaluating the
These guidelines are informed by evidence for TBI impact of nonpharmacological interventions for sleep-
cognitive rehabilitation interventions published up to wake disturbance on attention after TBI. We failed to
time of review. Relevant evidence published after the identify any study that formally evaluated the impact
INCOG guideline could influence the recommenda- of interventions for anxiety, depression, pain, substance
tions contained herein. Clinicians must also consider use, and medication changes on attention in individuals
their own clinical judgment, patient preferences, and with TBI. Nevertheless, it is our expert opinion that
contextual factors such as resource availability in their such factors should be considered and addressed before
decision-making processes about implementation of implementing other forms of intervention.
these recommendations. Attention no. 2: Metacognitive strategy training using func-
The INCOG developers, contributors, and supporting tional everyday activities should be considered for individuals
partners shall not be liable for any damages, claims, with TBI, especially those with mild-moderate attention deficits
liabilities, costs, or obligations arising from the use or (updated from INCOG 2014,28 (pp324–325) Attention 1). Level
misuse of this material, including loss or damage arising A evidence.
from any claims made by a third party. This recommendation has been updated from
INCOG 2014. In the INCOG 2014 guideline, we
reported level A evidence that strategies may be
RESULTS
developed, practiced, and applied to compensate for
attentional problems, specifically speed of information
Recommendations and literature review
processing. This evidence came from the work of Fasotti
The expert panel made 11 recommendations, with 2 et al32 in trialing time pressure management (TPM) to
new recommendations, 5 updated from INCOG 2014, enhance coping with slowed information processing.
and 4 remaining unchanged from INCOG 2014. Six The 3-step training program facilitates awareness of
recommendations are based on level A evidence, 3 on manifestations of mental slowness in daily activities
level B, and 2 on level C evidence. Since 2014, there and encourages the development of managing steps
i0hCywCX1AWnYQp/IlQrHD3i3D0OdRyi7TvSFl4Cf3VC4/OAVpDDa8KKGKV0Ymy+78= on 07/07/2023
Downloaded from http://journals.lww.com/headtraumarehab by BhDMf5ePHKav1zEoum1tQfN4a+kJLhEZgbsIHo4XM

TABLE 2 INCOG 2.0 guideline recommendations for attention and information-processing speed and new supporting
a
evidence
Guideline recommendation Grade Reviews RCTs Other
Nonpharmacological interventions for attention/information processing speed
Attention Clinicians should screen for and address factors that impact C Johansson et al30
no. 1 attention including hearing, vision, fatigue, sleep-wake
disturbance, anxiety, depression, pain, substance use, and
medication (updated from INCOG 2014,28(p326) Attention 4).
Attention Metacognitive strategy training using functional everyday A Cicerone et al50 Dymowski et al35
no. 2 activities should be considered for individuals with TBI, Roitsch et al40
especially those with mild-moderate attention deficits Virk et al36
(updated from INCOG 2014,28(pp324–325) Attention 1).
Attention Computer-based de-contextualized attentional tasks for B Bogdanova et al41 Dundon et al51
no. 3 individuals with TBI are NOT recommended because of lack Cicerone et al50 Straudi et al42
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).
Attention Training in dual tasking for individuals with TBI can be used to A
no. 4 improve dual-task performance, only on tasks similar to
those trained (INCOG 2014,28(p325) Attention 2).
Attention Training with periodic random auditory alerting tones is not B Dymowski et al35
no. 5 recommended for addressing attentional deficits following
TBI (INCOG 2014,28(p327) Attention 7).
Attention Training in mindfulness-based meditation techniques is not A
no. 6 recommended for remediation of attention deficits (INCOG
2014,28(pp327–328) Attention 8).
Attention Alterations to the environment and tasks may be used to C Dymowski et al35
no. 7 reduce the impact of attentional deficits on daily activities
for individuals with TBI (INCOG 2014,28(p326) Attention 5).
Attention The use of repetitive transcranial magnetic stimulation (rTMS) B Ahorsu et al65 Lee and Kim64 Boissonault et al67
no. 8 and transcranial direct current stimulation (tDCS) to Nousia et al66 Neville et al63
ameliorate attention following TBI is not recommended Rushby et al61
outside of the context of a research trial protocol (INCOG Sacco et al62
INCOG 2.0 Guidelines for Cognitive Rehabilitation Following Traumatic Brain Injury, Part II

2022). Ulam et al60


(continues)

www.headtraumarehab.com
41
i0hCywCX1AWnYQp/IlQrHD3i3D0OdRyi7TvSFl4Cf3VC4/OAVpDDa8KKGKV0Ymy+78= on 07/07/2023
Downloaded from http://journals.lww.com/headtraumarehab by BhDMf5ePHKav1zEoum1tQfN4a+kJLhEZgbsIHo4XM

42

TABLE 2 INCOG 2.0 guideline recommendations for attention and information-processing speed and new supporting
a
evidence (Continued)
Guideline recommendation Grade Reviews RCTs Other
Pharmacological management for attention/information-processing speed
Attention Methylphenidate (initiated at a dose of approximately A Barnett and Reid74 Dorer e al72
no. 9 0.10 mg/kg and increased gradually to a target of 0.25- Chien et al76 Dymowski et al73
0.30 mg/kg bid) is recommended in adults with TBI to Huang et al75 Jenkins et al78
enhance speed of information processing (updated from Johansson et al30
INCOG 2014,28(p328) Attention 9). Manktelow et al71
Moreno-Lopez70
Zhang and
Wang69
Attention While amantadine may enhance arousal in patients in a A Hammond et al84
no. 10 minimally conscious state, it should not be used to enhance
attentional functions following emergence from coma
(updated from INCOG 2014,28(p328) Attention 10).
Attention The traditional Chinese medicine MLC901 (NeuroAiD IITM) A Theadom et al86
no. 11 may enhance complex attention in individuals with
mild-moderate TBI (INCOG 2022).
Journal of Head Trauma Rehabilitation/January–February 2023

Abbreviations: RCTs, randomized controlled trials; TBI, traumatic brain injury.


a Refer to Ponsford et al28 for evidence contributing to the recommendations prior to 2014.
INCOG 2.0 Guidelines for Cognitive Rehabilitation Following Traumatic Brain Injury, Part II 43

before or during task performance to reduce time These exercises are predominantly computer-mediated
pressure.32 There have been no additional controlled and decontextualized, delivered on the premise that
studies of TPM among TBI published since that by training underlying components of attention will result
Fasotti et al.32 in improved attentional performance in other contexts.
Evidence regarding the use of strategy training (eg, Bogdanova et al41 reviewed 28 studies using comput-
chunking, pacing) to alleviate problems with working erized, cognitive interventions targeting attention and
Downloaded from http://journals.lww.com/headtraumarehab by BhDMf5ePHKav1zEoum1tQfN4a+kJLhEZgbsIHo4XM

memory and divided attention in everyday life after TBI executive functions in adults with acquired brain in-
remains confined to 2 case series studies: by Cicerone33 jury. The review reported significantly greater gains in
i0hCywCX1AWnYQp/IlQrHD3i3D0OdRyi7TvSFl4Cf3VC4/OAVpDDa8KKGKV0Ymy+78= on 07/07/2023

in mild TBI and by Vallat-Azouvi et al34 in 2 highly computerized retraining groups in 8 of 11 TBI-only
motivated individuals with severe TBI. studies. The gains reported were on neuropsychological
A case series (n = 3) by Dymowski et al35 examined measures only, with a few studies additionally including
effects of 3 to 4 weeks of individualized strategy training self-report measures. There was no objective evidence
on attention, relative to that of computerized atten- of generalization to everyday attentional behaviors.
tion training using Attention Process Training (APT-III) The authors noted many methodological limitations of
after severe TBI. Variability in attentional deficits and these studies, including the absence of control groups,
everyday attentional requirements necessitated individ- ecologically valid outcome assessments, and long-term
ualized goals and approaches and highlighted the need follow-up. One further study by Straudi et al42 similarly
to address the interplay of fatigue, mood, memory, found positive impacts of video game performance on
and executive dysfunction with attentional behavior. selective attention measures only.
All participants achieved individual goals after strategy Attention Process Training is a widely used computer-
training (eg, stay on task, complete a full day of work, ized attention training program that has been evaluated
manage anxiety, pay attention during introductions). in studies with variable methodological rigor and small
Improvements in speed of processing occurred in both samples.43–47 Repeated practice on any task may facil-
conditions but were greatest following strategy train- itate the development of strategies that improve task
ing. Although limited generalization was evident on performance.48 Although the most recent version of
participant self-ratings of attention, close-other ratings APT (APT-III) includes increased emphasis on devel-
of attentional behavior improved more after strategy opment of compensatory strategies within training, we
training than APT. Individualized strategy training was argue that strategy development may be more effec-
also generally preferred by participants over computer- tive if applied and practiced directly in the context of
ized training. The work by Dymowski et al35 highlights real-world activities, rather than on decontextualized
the need for metacognitive strategy training to be in- tasks. Consistent with this premise, Park and Ingles49
dividualized and to accommodate the impact of other concluded from an earlier meta-analysis that training
impairments on attention such as mood and fatigue. in specific skills can result in improvements in that
A systematic review and meta-analysis by Virk et al36 skill, which may also be evident on tasks similar to
found no evidence of significant overall improvement in those trained, but it cannot be assumed that under-
attention in response to intervention, but this was based lying attentional mechanisms are being restored. The
on 4 disparate studies with a TBI population.32,37–39 A INCOG recommendation deviates from that of the
quality appraisal of systematic reviews for behavioral updated review of studies conducted from 2009 to 2014
treatments of attention disorders after TBI by Roitsch by Cicerone et al,50 who supported working memory
et al40 concluded that effects of direct attention training training based on a single case study in stroke and
are minimal and limited to training tasks, with more did not clearly differentiate repeated drill practice from
evidence supporting training in strategy use to reduce strategy development.
the impact of attentional impairments. One well designed study by Dundon et al51 studied
Attention no. 3: Computer-based de-contextualized atten- training in capacity to focus attention on speech in
tional tasks for individuals with TBI are not recommended noisy or distracting environments. After recruiting in-
because of lack of demonstrated impact on everyday attentional dividuals with post–acute TBI who self-reported being
functions. Everyday task-specific training should be considered easily distracted, they demonstrated a linear decline in
but cannot be expected to generalize beyond trained or similar dichotic listening performance with the presence of a
tasks (updated from INCOG 2014,28 (pp326–327) Attention 6). second stream of irrelevant speech. The cognitive train-
Level B evidence. ing procedure based on APT included graded exposure
This recommendation has been updated to reflect to irrelevant noise in adaptive and nonadaptive training
a continuing lack of evidence of generalization be- schedules as compared with no treatment. Both types of
yond the specifically trained attentional tasks. There training resulted in improvements in dichotic listening
continues to be a significant focus on the use of train- and naturalistic tasks of performance in noise, and mea-
ing exercises to ameliorate impairments of attention.27 sures of selective attention and event-related potentials
www.headtraumarehab.com
44 Journal of Head Trauma Rehabilitation/January–February 2023

linked to target processing. There were, however, no have reported benefits from self-instructional and mind-
self-reported gains in everyday distractibility. Although fulness techniques,55–57 an RCT by McMillan et al38
Dundon et al.51 demonstrated that specific training can found that a brief mindfulness meditation technique,
result in changes that generalize to performance of sim- involving audiotape training to control attention by
ilar measures, it does not generalize more broadly to concentrating on breathing over extended periods, did
impact everyday activities. not reduce cognitive failures or improve attention,
Downloaded from http://journals.lww.com/headtraumarehab by BhDMf5ePHKav1zEoum1tQfN4a+kJLhEZgbsIHo4XM

Attention no. 4: Training in dual-tasking for individuals memory, or psychological adjustment more than physi-
with TBI can be used to improve dual-task performance, cal fitness training or no treatment.
i0hCywCX1AWnYQp/IlQrHD3i3D0OdRyi7TvSFl4Cf3VC4/OAVpDDa8KKGKV0Ymy+78= on 07/07/2023

only on tasks similar to those trained (updated from INCOG Attention no. 7: Alterations to the environment and tasks
2014,28 (p325) Attention 2). Level A evidence. may be used to reduce the impact of attentional deficits on daily
This recommendation remains unchanged, with no activities for individuals with TBI (updated from INCOG
new evidence. The evidence supporting this recommen- 2014,28(p326) Attention5). Level C evidence.
dation comes from 2 small lower-quality unblinded This recommendation is also unchanged. Individuals
randomized controlled trials (RCTs). The first RCT by with TBI who have significant cognitive impairments
Evans et al52 provided training in combining walking and those who lack awareness of their difficulties are
with cognitive activities as compared with treatment as rarely able to initiate the use of compensatory strate-
usual. The second RCT by Couillet et al37 trained par- gies to alleviate attentional problems.58 An intervention
ticipants to divide their attention between 2 cognitive approach that does not rely on active participation by
tasks of increasing difficulty, each learned individu- the person with TBI could include making changes
ally beforehand. Both studies demonstrated significant to the environment or tasks to reduce the impact of
training effects on trained and similar tasks. These attentional problems. In the context of work or study,
findings reinforce the conclusion that individuals with this might involve removing distractions (eg, work in
TBI can benefit from training on specific tasks or a quiet room, reduce interruptions), altering tasks to
activities. To maximize functional impact from such reduce the speed, amount or complexity of information
training, it would seem most pragmatic to provide to be processed, providing information in written form
such training on tasks that need to be performed in to ensure that it is understood, or providing prompts
everyday life. to refocus or shift attention to another aspect of a
Attention no. 5: Training with periodic random auditory task. The case studies performed by Dymowski et al35
alerting tones is not recommended for addressing attentional used some of these strategies including minimizing dis-
deficits following TBI (updated from INCOG 2014,28 (p327) traction and environmental cueing, which focused on
Attention 7). Level B evidence. specific attention-related goals, alongside compensatory
This recommendation is unchanged as no further ev- strategies such as TPM. We could find no clinical tri-
idence has emerged regarding the use of self-alerting or als evaluating the use of such strategies, despite their
external alerting tones to facilitate arousal and atten- reported use in clinical settings.59
tional performances after TBI. These strategies were used Attention no. 8: The use of repetitive transcranial magnetic
by Dymowski et al35 in their single case studies to facili- stimulation (rTMS) and transcranial direct current stimu-
tate self-monitoring. Manly and colleagues53 found that lation (tDCS) to ameliorate attention following TBI is not
providing a brief auditory alerting stimulus as a cue to recommended outside of the context of a research trial protocol
consider the goal of an activity improved performance (INCOG 2022). Level B evidence.
on the “Hotel task.” A larger study by Sweeney et al54 This is a new recommendation to account for the
found that periodic auditory alerts did not improve progressive but still limited research in the field of
performance of a virtual reality prospective memory task tDCS and rTMS. Numerous studies have investigated
that simulated working in a furniture warehouse. There the impact of noninvasive brain stimulation, tDCS, and
remains insufficient evidence to suggest that periodic rTMS on attention and working memory after TBI and
alerting enhances the allocation, or switching, of atten- the findings have been mixed. Given the mixed out-
tion across complex tasks. comes and lack of evidence of generalization to everyday
Attention no. 6: Training in mindfulness-based meditation attention, the expert panel recommends that, at this
techniques is not recommended for remediation of attention time, rTMS and tDCS should not be used outside of
deficits (updated from INCOG 2014,28(pp327–328) Attention a research context.
8). Level A evidence. Ulam et al60 did not find greater gains in performance
No new evidence has been published on this topic and on tests of attention and working memory following
the recommendation remains unchanged from INCOG 20-minute sessions of tDCS daily for 10 days relative
2014. Consensus was that this intervention should not to a sham control. Rushby et al61 found no significant
be used outside of research protocols due to lack of impact of a single dose of tDCS on working memory
demonstrated evidence. Although less rigorous studies (n-back Task Measure) performance. Sacco et al62 found
INCOG 2.0 Guidelines for Cognitive Rehabilitation Following Traumatic Brain Injury, Part II 45

that 10 sessions of tDCS for more than 5 days, followed found that methylphenidate significantly improved pro-
by computer-assisted training for 40 minutes, resulted cessing speed as measured by Choice Reaction Time
in greater improvement in reaction times on a divided and Digit Symbol Coding. Reaction time was inversely
attention task than in a sham-treated control group. associated with duration of treatment; however, there
However, it is unclear whether the gains were due to the were no statistically significant effects on other mea-
tDCS or computer training, or a combined effect. Of sures of attention or working memory. With respect to
Downloaded from http://journals.lww.com/headtraumarehab by BhDMf5ePHKav1zEoum1tQfN4a+kJLhEZgbsIHo4XM

RCTs trialing rTMS, Neville et al63 found no significant adverse events, methylphenidate significantly increased
impact of 10 sessions of rTMS on performance of heart rate but did not impact blood pressure. Although
i0hCywCX1AWnYQp/IlQrHD3i3D0OdRyi7TvSFl4Cf3VC4/OAVpDDa8KKGKV0Ymy+78= on 07/07/2023

attentional and processing speed measures (ie, Trail several studies have evaluated only a single dose of
Making Test, Digit Span, Symbol Digit Modalities methylphenidate, 1 RCT by Zhang and Wang69 showed
test) or other cognitive measures. In contrast, a smaller efficacy with administration for more than 30 weeks.
RCT by Lee and Kim64 reported a positive impact of An inverted U dose-response relationship has been
rTMS (30 minutes, 5 days a week) following muscle demonstrated between prefrontal dopamine activity and
strengthening and movement therapy (2 weeks) on working memory. Stimulants at low dose increased
performance of the Trail Making Test and Stroop Color dopamine levels and enhanced arousal and attention,
Word tasks and on the Montgomery-Astberg Depression while high doses could impair them.77 In a randomized
Rating Scale in comparison with the control group. double crossover study (n = 40), Jenkins et al78 found
A recent meta-analysis combining rTMS and tDCS that patients with low caudate dopamine transporter
studies65 concluded that noninvasive brain stimulation binding, measured using single photon emission com-
has a significant positive effect on attentional measures, puted tomography, showed significant improvement
but no functional outcomes were included. It is in response speed with methylphenidate compared
important to note that tDCS and rTMS have differing with placebo, with concomitant self and caregiver-
mechanisms of action on the brain, and the INCOG reported improvements in apathy. Participants with
team felt that they should not be combined in a meta- normal dopamine transporter binding did not improve.
analysis, and the findings should be interpreted with These findings suggest that identifying the presence of a
caution. Another review by Nousia et al,66 which also hypodopaminergic state after TBI may be important for
combined these approaches, concluded that there was selecting recipients of methylphenidate therapy.
insufficient evidence to support use of noninvasive Although everyday attentional measures were not
brain stimulation for attention or any cognitive included in the Chien et al76 meta-analysis, sev-
function. Most importantly, there is no evidence eral RCTs have shown generalization of gains from
of generalization of gains from these interventions methylphenidate to everyday attentional ratings, in-
to everyday activities. Boissonnault et al67 attempted cluding the aforementioned study by Jenkins et al.78
to implement a tDCS protocol in the context of a Whyte et al79 found generalization to everyday rating
rehabilitation center but had extremely low recruitment of attentional behavior by caregivers, while Willmott
and retention, thus highlighting the limitations of and Ponsford80 found a strong trend in that direction,
application in a general rehabilitation setting. and Johansson et al30 and Zhang and Wang69 found
reductions in fatigue ratings.
Attention no. 10: While amantadine may enhance arousal
Pharmacological strategies for improving attention
in patients in a minimally conscious state, it should not be
Attention no. 9: Methylphenidate (initiated at a dose of used to enhance attentional functions following emergence from
approximately 0.10 mg/kg and increased gradually to a tar- coma (updated from INCOG 2014,28 (p328) Attention 10).
get of 0.25-0.30 mg/kg bid) is recommended in adults with Level A evidence.
TBI to enhance speed of information processing (updated from This updated recommendation on the use of amanta-
INCOG 2014,28 (p328) Attention 9). Level A evidence. dine is based on the scientific literature since INCOG
This recommendation has been updated. Traumatic 2014. Amantadine is a dopaminergic agent that acts
brain injury is associated with changes in neurotransmit- presynaptically to enhance dopamine release and de-
ter systems associated with attention. Methylphenidate, crease dopamine reuptake. It has demonstrated efficacy
a central nervous system stimulant, increases the re- in facilitating arousal and general function in patients
lease and blocks reuptake of dopamine and nora- in a comatose or vegetative state when administered
drenaline, resulting in increased synaptic and extra- over the short term (<4 weeks).81–83 However, it appears
cellular concentrations.68 Since INCOG 2014, sev- not to enhance attentional function when administered
eral new RCTs,30,69–73 1 systematic review,74 and 2 to conscious patients at longer periods after injury.
meta-analyses75,76 have been published. As such, the Hammond et al84 compared the effects of 100 mg of
recommendation was modified to reflect the new evi- amantadine twice daily or placebo in 119 individu-
dence. The most recent meta-analysis by Chien et al76 als with chronic TBI (all >6 months postinjury) and
www.headtraumarehab.com
46 Journal of Head Trauma Rehabilitation/January–February 2023

irritability. They evaluated behavioral and cognitive dis- of environmental supports, and factors that may be ex-
turbance over 60 days of treatment or placebo and found acerbating attentional problems, including hearing and
no significant impact on attentional measures at any vision disruptions, anxiety, depression, fatigue, sleep
time point up to 60 days. disturbance, pain, medication, and substance use.
Attention no. 11: The traditional Chinese medicine To alleviate attentional problems, there is evidence
MLC901 (NeuroAiD IITM) may enhance complex attention in support of training in metacognitive strategies ap-
Downloaded from http://journals.lww.com/headtraumarehab by BhDMf5ePHKav1zEoum1tQfN4a+kJLhEZgbsIHo4XM

in individuals with mild-moderate TBI (INCOG 2022). plied directly to everyday attentional difficulties, such
Level A evidence. as TPM. Given evidence of learning on trained tasks,
i0hCywCX1AWnYQp/IlQrHD3i3D0OdRyi7TvSFl4Cf3VC4/OAVpDDa8KKGKV0Ymy+78= on 07/07/2023

Based on research conducted since the INCOG 2014 training may be provided on specific tasks such as dual
review, a recommendation has been added to reflect tasking or dealing with background noise, but given a
use of traditional Chinese medicine MLC901. MLC901 lack of evidence of generalization, training should be
(NeuroAiD IITM) is a traditional Chinese herbal focused on everyday tasks rather than decontextualized
supplement with antioxidant properties shown to im- computer tasks. Modifications to the task (reducing
prove survival, recovery, and cognitive functioning attentional demands) or environment (removing dis-
in rodents after ischemic injury.85 Among humans, traction) may be helpful, although evaluation of such
Theadom et al86 conducted a 9-month pilot randomized strategies is needed.
placebo controlled trial involving 78 individuals aged Methylphenidate, administered at 0.3 mg/kg in
18 to 65 years, 1 to 12 months after mild-moderate divided doses, may increase speed of information
TBI (97% mild). They found that participants receiv- processing, enhance everyday attentional behavior, or
ing MLC901 (0.8-g capsules, 3 times daily) showed reduce fatigue in individuals aged 16 to 60 years who
greater gains on the CNS Vital Signs complex attention have no history of attention deficit hyperactivity disor-
measure (P = .04, d = 0.6) at 6 months relative to con- der, previous stimulant use, drug or alcohol dependence,
trols. There were no group differences for self-reported or other psychiatric disorder. Amantadine may facilitate
neurobehavioral sequelae, mood, fatigue, physical dis- arousal over the short term in individuals in vegetative
ability, or overall quality of life at 6 months. No serious state or emerging from coma, but there is no evidence of
adverse events were reported. Replication of this finding positive impact of amantadine on attention in chronic
is needed. TBI. The traditional Chinese medicine MLC901
(NeuroAiD IITM) in 0.8-g capsules 3 times daily may
Algorithm enhance complex attention in individuals with mild
Clinicians are encouraged to follow the decision TBI, although replication of this finding is needed.
algorithm in Figure 1 that highlights how to navi- Research investigating behavioral interventions for
gate through this series of guidelines for managing attention, in the context of the everyday life of the
attentional problems, further elaborated in the section individual with TBI, including both metacognitive
“Discussion.” strategies and environmental modifications remains
very limited in quantity, quality, and scope. There
Audit tool is a growing body of research supporting the use of
contextualized approaches to rehabilitation,87 and the
Table 3 sets out the audit tool items recommended
findings from our reviews support this. Unfortunately,
by the INCOG panel for examining management of
clinicians continue to use computerized attention
attentional problems in clinical settings. Clinicians and
training27 despite there being no clear evidence of
organizational leaders are encouraged to use these tools
generalization to everyday activities. The current
in review or audit of individual patient charts to de-
guideline was limited to studies conducted in adults.
termine degree of adherence to the recommendations.
Similar reviews are needed for pediatric TBI. There is
This is most successful in changing practice when these
an enormous need for further RCTs and well-designed
audit results are fed back to the team for discussion of
single case studies in both adults and children that
opportunities for improvement.
evaluate the impact of real-world interventions not only
DISCUSSION on attentional impairments but also more importantly
on the individual’s daily life and to identify what works
Given the high frequency of attentional problems in and for whom. Many methodological challenges must
individuals with TBI, it is recommended that all individ- be overcome to achieve this, including the development
uals with MS-TBI have a neuropsychological assessment and more universal use of attentional outcome measures
to determine the nature of their attentional difficulties that reflect lived experience of everyday attentional
and also assess their everyday manifestations. It is also function and are psychometrically sound and sensitive
important to identify and address the attentional de- to change. Qualitative feedback from individuals
mands of the injured individual’s lifestyle, availability receiving the interventions is also needed.
INCOG 2.0 Guidelines for Cognitive Rehabilitation Following Traumatic Brain Injury, Part II 47
Downloaded from http://journals.lww.com/headtraumarehab by BhDMf5ePHKav1zEoum1tQfN4a+kJLhEZgbsIHo4XM
i0hCywCX1AWnYQp/IlQrHD3i3D0OdRyi7TvSFl4Cf3VC4/OAVpDDa8KKGKV0Ymy+78= on 07/07/2023

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.
www.headtraumarehab.com
i0hCywCX1AWnYQp/IlQrHD3i3D0OdRyi7TvSFl4Cf3VC4/OAVpDDa8KKGKV0Ymy+78= on 07/07/2023
Downloaded from http://journals.lww.com/headtraumarehab by BhDMf5ePHKav1zEoum1tQfN4a+kJLhEZgbsIHo4XM

48

TABLE 3 Audit guidelines for priority recommendations: Attentiona


Intervention (guideline Specific activities, Assessment of need
recommendation) devices, or tools and effectiveness Patient characteristics Discipline
Attention training  Combined with metacognitive  Assessment for need  Mild to moderate at-  OT
“Metacognitive strategy training using executive strategy training conducted tention deficit  PT
functional everyday activities should  Functional everyday activities  Training provided  SLP
be considered, especially in patients  Use of checklists  MD
with mild-moderate attention  Other  Neuro
deficits” (Attention no. 2).  Other
Training may be conducted on tasks in  Functional everyday activities  Assessment for need  Mild, moderate, or se-  OT
real-world contexts (eg, dual tasks, conducted vere attention deficit  PT
background noise) without  Training provided  SLP
expectation of generalization  MD
(Attention nos. 3 and 4).  Neuro
 Other
“Alterations to the environment and  Functional everyday activities  Assessment for need  Mild, moderate, or se-  OT
tasks may be used to reduce the  Environmental manipulation conducted vere deficit  PT
impact of attentional problems on  Use of checklists  Environmental  SLP
daily activities” (Attention no. 7).  Other alterations made  MD
 Neuro
 Other
Pharmaceutical interventions: Attention
Drug Used Indication Patient characteristics Found in
Methylphenidate Yes No  Attentional function  Mild, moderate, or se-  Drug charts
Journal of Head Trauma Rehabilitation/January–February 2023

“Methylphenidate is recommended to  Speed of cognitive pro- vere attention deficit  MD notes


enhance speed of information cessing  Other
processing” (Attention no. 9)  Sustained attention/
vigilance
 Other (please specify):

a Theaudit 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.
INCOG 2.0 Guidelines for Cognitive Rehabilitation Following Traumatic Brain Injury, Part II 49

REFERENCES

1. Whyte J, Ponsford J, Watanabe T, Hart T. Traumatic brain injury. 18. Togher L, Douglas J, Turkstra LS, et al. INCOG 2.0
In: Frontera WR, Delisa JD, Gans BM, Walsh NA, Robinson guidelines for cognitive rehabilitation following traumatic
Downloaded from http://journals.lww.com/headtraumarehab by BhDMf5ePHKav1zEoum1tQfN4a+kJLhEZgbsIHo4XM

L, eds. Delisa’s Physical Medicine and Rehabilitation: Principles and brain injury, part IV: cognitive-communication and social
Practice. 5th ed. Wolters Kluwer, Lippincott Williams and Wilkins; cognition disorders. J Head Trauma Rehabil. 2023;38(1):65-82.
i0hCywCX1AWnYQp/IlQrHD3i3D0OdRyi7TvSFl4Cf3VC4/OAVpDDa8KKGKV0Ymy+78= on 07/07/2023

2010:575–623. doi:10.1097/HTR.0000000000000835
2. Povlishock J, Katz DI. Update of neuropathology and neurological 19. Ponsford JL, Downing M, Olver J, et al. Longitudinal follow-
recovery after traumatic brain injury. J Head Trauma Rehabil. 2005; up of patients with traumatic brain injury: outcome at 2,
20(1):76–94. doi:10.1097/00001199-200501000-00008 5, and 10-years post-injury. J Neurotrauma. 2014;31(1):64–77.
3. Ponsford JL, Kinsella G. Attentional deficits following closed- doi:10.1089/neu.2013.2997
head injury. J Clin Exp Neuropsychol. 1992;14(5):822–838. 20. Himanen L, Portin R, Isoniemi H, Helenius H, Kurkj T,
doi:10.1080/01688639208402865 Tenovuo O. Longitudinal cognitive changes in traumatic brain
4. Spikman JM, van Zomeren AH, Deelman BG. Deficits of injury: a 30-year follow-up study. Neurology. 2006;66(2):187–192.
attention after closed-head injury: slowness only? J Clin Exp Neu- doi:10.1212/01.wnl.0000194264.60150.d3
ropsychol. 1996;18(5):755–767. doi:10.1080/01688639608408298 21. Hoofien D, Gilboa A, Vakil E, Donovick PJ. Traumatic brain
5. Willmott C, Ponsford J, Hocking C, Schönberger M. Factors con- injury 10-20 years later: a comprehensive outcome study of
tributing to attentional impairments following traumatic brain in- psychiatric symptomatology, cognitive abilities, and psychoso-
jury. Neuropsychology. 2009;23(4):424–432. doi:10.1037/a0015058 cial functioning. Brain Inj. 2001;15(3):189–209. doi:10.1080/
6. Vallat-Azouvi C, Weber T, Legrand L, Azouvi P. Working memory 026990501300005659
after severe traumatic brain injury. J Int Neuropsychol Soc. 2007; 22. Carroll LJ, Cassidy JD, Peloso PM, et al. Prognosis for mild
13(5):770–780. doi:10.1017/S1355617707070993 traumatic brain injury: results of the WHO Collaborating Centre
7. Dunning DL, Westgate B, Adlam A. A meta-analysis of Task Force on Mild Traumatic Brain Injury. J Rehabil Med. 2004(43
working memory impairments in survivors of moderate-to- suppl):84–105. doi:10.1080/16501960410023859
severe traumatic brain injury. Neuropsychology. 2016;30(7):811– 23. Papesh M, Theodoroff SM, Gallun FJ. Traumatic brain injury and
819. doi:10.1037/neu0000285 auditory processing. In: Fagelson M, Baguley DM, eds. Hyperacusis
8. Ziino C, Ponsford J. Vigilance and fatigue following trau- and Disorders of Sound Intolerance: Clinical and Research Perspectives.
matic brain injury. J Int Neuropsychol Soc. 2006;12(1):100–110. Plural Publishing Inc; 2018.
doi:10.1017/S1355617706060139 24. Gould KR, Ponsford JL, Spitz G. Contributions of cogni-
9. Robertson IH, Manly T, Andrade H, Baddeley BI, Yiend J. ’Oops!’ tive impairments to anxiety disorder following traumatic brain
Performance correlates of everyday attentional failures in trau- injury. J Clin Exp Neuropsychol. 2014;36(1):1–14. doi:10.1080/
matic brain injured and normal subjects. Neuropsychologia. 1997; 13803395.2013.863832
35(6):747–758. doi:10.1016/s0028-3932(97)00015-8 25. Ziino C, Ponsford J. Selective attention deficits and subjective
10. Asloun S, Soury S, Couillet J, et al. Interactions between divided fatigue following traumatic brain injury. Neuropsychology. 2006;
attention and working-memory load in patients with severe trau- 20(3):383–390. doi:10.1037/0894-4105.20.3.383
matic brain injury. J Clin Exp Neuropsychol. 2008;30(4):481–490. 26. Bloomfield ILM, Espie CA, Evans JJ. Do sleep difficulties exac-
doi:10.1080/13803390701550144 erbate deficits in sustained attention following traumatic brain
11. Azouvi P, Vallat-Azouvi C, Belmont A. Cognitive deficits after injury? J Int Neuropsychol Soc. 2010;16(1):17–25. doi:10.1017/
traumatic coma. Prog Brain Res. 2009;177:89–110. doi:10.1016/ S1355617709990798
S0079-6123(09)17708-7 27. Nowell C, Downing M, Bragge P, Ponsford J. Current practice
12. Whyte J, Fleming M, Polansky M, Cavallucci C, Coslett HB. of cognitive rehabilitation following traumatic brain injury: an
The effects of visual distraction following traumatic brain in- international survey. Neuropsychol Rehabil. 2020;30(10):1976–1995.
jury. J Int Neuropsychol Soc. 1998;4(2):127–136. doi:10.1017/ doi:10.1080/09602011.2019.1623823
s1355617798001271 28. Ponsford J, Bayley M, Wiseman-Hakes C, et al. INCOG
13. Shallice T, Burgess PW. Deficits in strategy application follow- recommendations for management of cognition following TBI
ing frontal lobe damage in man. Brain. 1991;114(pt 2):727–741. Part II: attention and information processing speed. J Head Trauma
doi:10.1093/brain/114.2.727 Rehabil. 2014;29(4):321–337. doi:10.1097/HTR.000000000000
14. Renison B, Ponsford J, Testa R, Richardson B, Brownfield K. The 0072
ecological and construct validity of a newly developed measure of 29. Bayley M, Janzen S, Harnett A, et al. INCOG 2.0 guidelines for
executive function: the Virtual Library Task. J Int Neuropsychol Soc. cognitive rehabilitation following traumatic brain injury: methods,
2012;18(3):440–450. doi:10.1017/S1355617711001883 overview and principles. J Head Trauma Rehabil. 2023;38(1):7-23.
15. VanSolkema M, McCann C, Barker-Collo S, Foster A. Atten- doi:10.1097/HTR.0000000000000838
tion and communication following TBI: making the connection 30. Johansson B, Wentzel AP, Andrell P, Mannheimer C, Rönnbäck L.
through a meta-narrative systematic review. Neuropsychol Rev. Methylphenidate reduces mental fatigue and improves processing
2020;30(3):345–361. doi:10.1007/s11065-020-09445-5 speed in persons suffered a traumatic brain injury. Brain Inj. 2015;
16. Jeffay E, Ponsford J, Harnett A, et al. INCOG 2.0 guidelines 29(6):758–765. doi:10.3109/02699052.2015.1004747
for cognitive rehabilitation following traumatic brain injury, part 31. Wiseman-Hakes C, Murray BJ, Moineddin R, et al. Evaluating
III: executive function. J Head Trauma Rehabil. 2023;38(1):52-64. the impact of treatment for trauma related sleep/wake disor-
doi:10.1097/HTR.0000000000000834 ders on recovery of cognition and communication in adults
17. Velikonja D, Ponsford J, Janzen S, et al. INCOG 2.0 guide- with chronic TBI. Brain Inj. 2013;27(12):1364–1376. doi:10.3109/
lines for cognitive rehabilitation following traumatic brain injury, 02699052.2013.823663
part V: memory. J Head Trauma Rehabil. 2023;38(1):83-102. 32. Fasotti L, Kovacs F, Eling PATM, Brouwer WH. Time pres-
doi:0.1097/HTR.0000000000000837 sure management as a compensatory strategy training after

www.headtraumarehab.com
50 Journal of Head Trauma Rehabilitation/January–February 2023

closed-head injury. Neuropsychol Rehabil. 2000;10:47–65. doi:10. 50. Cicerone KD, Goldin Y, Ganci K, et al. Evidence-based cogni-
1080/096020100389291 tive rehabilitation: systematic review of the literature from 2009
33. Cicerone KD. Remediation of “working attention” in mild trau- through 2014. Arch Phys Med Rehabil. 2019;100(8):1515–1533.
matic brain injury. Brain Inj. 2002;16(3):185–195. doi:10.1080/ doi:10.1016/j.apmr.2019.02.011
02699050110103959 51. Dundon NM, Dockree SP, Buckley V, et al. Impaired
34. Vallat-Azouvi C, Weber T, Leqrand L, Azouvi P. Rehabilitation auditory selective attention ameliorated by cognitive training
of the central executive of working memory after severe traumatic with graded exposure to noise in patients with traumatic
Downloaded from http://journals.lww.com/headtraumarehab by BhDMf5ePHKav1zEoum1tQfN4a+kJLhEZgbsIHo4XM

brain injury: two single case studies. Brain Inj. 2009;23(6):585–594. brain injury. Neuropsychologia. 2015;75:74–87. doi:10.1016
doi:10.1080/02699050902970711 /j.neuropsychologia.2015.05.012
i0hCywCX1AWnYQp/IlQrHD3i3D0OdRyi7TvSFl4Cf3VC4/OAVpDDa8KKGKV0Ymy+78= on 07/07/2023

35. Dymowski AR, Ponsford JL, Willmott C. Cognitive training ap- 52. Evans JJ, Greenfield E, Wilson BA, Bateman A. Walking
proaches to remediate attention and executive dysfunction after and talking therapy: improving cognitive-motor dual-tasking in
traumatic brain injury: a single case series. Neuropsychol Rehabil. neurological illness. J Int Neuropsychol Soc. 2009;15(1):112–120.
2016;26(5–6):866–894. doi:10.1080/09602011.2015.1102746 doi:10.1017/S1355617708090152
36. Virk S, Williams T, Brunsdon R, Suh F, Morrow A. Cognitive 53. Manly T, Hawkins J, Evans J, Woldt K, Robertson IH. Rehabili-
remediation of attention deficits following acquired brain injury: a tation of executive function: facilitation of effective goal manage-
systematic review and meta-analysis. Neurorehabilitation. 2015;36: ment on complex tasks using periodic auditory alerts. Neuropsy-
367–377. doi:10.3233/NRE-151225 chologia. 2001;41(3):271–281. doi:10.1016/s0028-3932(01)00094-x
37. Couillet J, Soury S, Leborne C, et al. Rehabilitation of di- 54. Sweeney S, Kersel DA, Morris RG, Manly T, Evans JJ. The
vided attention after severe traumatic brain injury: a randomised sensitivity of a virtual reality task to planning and prospective
trial. Neuropsychol Rehabil. 2010;20(3):321–339. doi:10.1080/ memory impairments: group differences and the efficacy of peri-
09602010903467746 odic alerts on performance. Neuropsychol Rehabil. 2010;20(2):239–
38. McMillan T, Robertson IH, Brock D, Chorlton L. Brief mindful- 263. doi:10.1080/09602010903080531
ness training for attentional problems after traumatic brain injury: 55. Wilson C, Robertson IH. A home-based intervention for at-
a randomised control treatment trial. Neuropsychol Rehabil. 2002; tentional slips during reading following head injury: a single
12(2):117–125. doi:10.1080/09602010143000202 case study. Neuropsychol Rehabil. 1992;2(3):193–205. doi:10.1080/
39. Tiersky LA, Anselmi V, Johnston MV, et al. A trial of neu- 09602019208401408
ropsychologic rehabilitation in mild-spectrum traumatic brain 56. Webster JS, Scott RR. The effects of self-instructional training on
injury. Arch Phys Med Rehabil. 2005;86:1565–1574. doi:10.1016/j attentional deficits following head injury. Clin Neuropsychol. 1983;
.apmr.2005.03.013 5(2):69–74.
40. Roitsch J, Redman R, Michalek AMP, Johnson RK, Raymer AM. 57. Novakovic-Agopian T, Chen AJ, Rome S, et al. Rehabilitation
Quality appraisal of systematic reviews for behavioral treatments of executive functioning with training in attention regulation
of attention disorders in traumatic brain injury. J Head Trauma Re- applied to individually defined goals: a pilot study bridging theory,
habil. 2018;34(4):E42–E50. doi:10.1097/HTR.0000000000000444 assessment, and treatment. J Head Trauma Rehabil. 2011;26(5):325–
41. Bogdanova Y, Yee MK, Ho VT, Cicerone KD. Computerized 328. doi:10.1097/HTR.0b013e3181f1ead2
cognitive rehabilitation of attention and executive function in 58. Sloan S, Ponsford J. Managing cognitive problems. In: JL
acquired brain injury: a systematic review. J Head Trauma Rehabil. Ponsford, S Sloan, P Snow, eds. Traumatic Brain Injury: Rehabilita-
2016;31(6):419–433. doi:10.1097/HTR.0000000000000203 tion for Everyday Adaptive Living. 2nd ed. Psychology Press; 2012:
42. Straudi S, Severini G, Charabati AS, et al. The effects of video game 99–132.
therapy on balance and attention in chronic ambulatory traumatic 59. Downing M, Bragge P, Ponsford J. Cognitive rehabilitation follow-
brain injury: an exploratory study. BMC Neurology. 2017;17(1):86. ing traumatic brain injury: a survey of current practice in Australia.
doi:10.1186/s12883-017-0871-9 Brain Impairment. 2019;20(1):24–36. doi:10.1017/BrImp.2018.12
43. Park NW, Proulx G, Towers W. Evaluation of the Attention 60. Ulam F, Shelton C, Richards L, et al. Cumulative effects of
Process training programme. Neuropsychol Rehabil. 1999;9(2):135– transcranial direct current stimulation on EEG oscillations and
154. doi:10.1080/713755595 attention/working memory during subacute neurorehabilitation
44. Sohlberg MM, Mateer CA. Effectiveness of an attention- of traumatic brain injury. Clin Neurophysiol. 2015;126(3):486–496.
training program. J Clin Exp Neuropsychol. 1987;9(2):117–130. doi:10.1016/j.clinph.2014.05.015
doi:10.1080/01688638708405352 61. Rushby JA, DeBlasio FM, Logan JA, et al. tDCS affects on
45. Sohlberg MM, McLaughliin KA, Pavese A, Heidrich A, Posner AI. task-related activation and working memory performance in
Evaluation of attention process training and brain injury education traumatic brain injury: a within group randomized controlled
in persons with acquired brain injury. J Clin Exp Neuropsychol. 2000; trial. Neuropsychol Rehabil. 2021;31(5):814–836. doi:10.1080/
22(5):656–676. doi:10.1076/1380-3395(200010)22:5;1-9;FT656 09602011.2020.1733620
46. Pero S, Incoccia C, Caracciolo B, Zoccolotti P, Formisano R. 62. Sacco K, Galetto V, Dimitri D, et al. Concomitant use of transcra-
Rehabilitation of attention in two patients with traumatic brain nial direct current stimulation and computer-assisted training for
injury by means of “attention process training.” Brain Inj. 2006; the rehabilitation of attention in traumatically brain injured pa-
20(11):1207–1219. doi:10.1080/02699050600983271 tients: behavioral and neuroimaging results. Front Behav Neurosci.
47. Murray LL, Keeton RJ, Karcher L. Treating attention in mild 2016;10:57. doi:10.3389/fnbeh.2016.00057
aphasia: evaluation of attention process training-II. J Commun 63. Neville LS, Zaninotto AL, Hayashi Y, et al. Repetitive TMS does
Disord. 2006;39(1):37–61. doi:10.1016/j.jcomdis.2005.06.001 not improve cognition in patients with TBI. Neurology. 2019;93(2):
48. Dirette DK, Hinojosa J. The effects of a compensatory in- e190–e199. doi:10.1212/WNL.0000000000007748
tervention on processing deficits of adults with acquired 64. Lee SA, Kim MK. Effect of low frequency repetitive transcranial
brain injuries. Occupational Ther J Res. 1999;19(4):223–240. magnetic stimulation on depression and cognition of patients with
doi:10.1177/153944929901900401 traumatic brain injury: a randomized controlled trial. Med Sci
49. Park NW, Ingles JL. Effectiveness of attention rehabilitation after Monit. 2018;24:8789–8994. doi:10.12659/MSM.911385
an acquired brain injury: a meta-analysis. Neuropsychology. 2001; 65. Ahorsu DK, Adjaottor ES, Lam BYH. Intervention effect of non-
15(2):199–210. doi:10.1037//0894-4105.15.2.199 invasive brain stimulation on cognitive functions among people
INCOG 2.0 Guidelines for Cognitive Rehabilitation Following Traumatic Brain Injury, Part II 51

with traumatic brain injury: a systematic review and meta-analysis. matic brain injury: a meta-analysis. Brain Sci. 2019;9(11):291.
Brain Sci. 2021;11(7):840. doi:10.3390/brainsci11070840 doi:10.3390/brainsci9110291
66. Nousia A, Martzoukou M, Liampas I, et al. The effectiveness of 77. Cools R, D’Esposito M. Inverted-U-shaped dopamine actions on
non-invasive brain stimulation alone or combined with cognitive human working memory and cognitive control. Biol Psychiatry.
training on the cognitive performance of patients with traumatic 2011;69(12):e113–e125. doi:10.1016/j.biopsych.2011.03.028
brain injury: α systematic review. Arch Clin Neuropsychol. 2022; 78. Jenkins PO, DeSimoni S, Bourke NJ, et al. Stratifying drug
37(2):497–512. doi:10.1093/arclin/acab047 treatment of cognitive impairments after traumatic brain injury
Downloaded from http://journals.lww.com/headtraumarehab by BhDMf5ePHKav1zEoum1tQfN4a+kJLhEZgbsIHo4XM

67. Boissonnault E, Higgins J, LaGarde G, Barthelemy D, Lamarre C, using neuroimaging. Brain. 2019;142(8):2367–2379. doi:10.1093/
Dagher JH. Brain stimulation in attention deficits after traumatic brain/awz149
i0hCywCX1AWnYQp/IlQrHD3i3D0OdRyi7TvSFl4Cf3VC4/OAVpDDa8KKGKV0Ymy+78= on 07/07/2023

brain injury: a literature review and feasibility study. Pilot Feasibility 79. Whyte H, Hart T, Vaccaro M, et al. Effects of methylphenidate on
Stud. 2021;7(1):115. doi:10.1186/s40814-021-00859-3 attention deficits after traumatic brain injury: a multidimensional
68. Leonard BE, McCartan D, White J, King DJ. Methylphenidate: randomized, controlled trial. Am J Phys Med Rehabil. 2004;83(6):
a review of its neuropharmacological, neuropsychological and 401–420. doi:10.1097/01.phm.0000128789.75375.d3
adverse clinical effects. Hum Psychopharmacol. 2004;19(3):151–180. 80. Willmott C, Ponsford J. Efficacy of methylphenidate in the early
doi:10.1002/hup.579 rehabilitation of attention following traumatic brain injury: a
69. Zhang W, Wang Y. Efficacy of methylphenidate for the treatment randomized, crossover, double-blind, placebo controlled trial.
of mental sequelae after traumatic brain injury. Medicine (Balti- J Neurol Neurosurg Psychiatry. 2009;80(5):552–557. doi:10.1136/
more). 2017;96(25):e6960. doi:10.1097/MD.0000000000006960 jnnp.2008.159632
70. Moreno-Lopez L, Manktelow AE, Sahakian BJ, Menon DK, 81. Loggini A, Tangonan R, El Ammar F, et al. The role of amantadine
Stamatakis EA. Anything goes: regulation of the neural pro- in cognitive recovery early after traumatic brain injury. Clin Neurol
cesses underlying response inhibition in TBI patients. Eur Neu- Neurosurg. 2020;194:105815. doi:10.1016/j.clineuro.2020.105815
ropsychopharmacol. 2017;27(2):159–169. doi:10.1016/j.euroneuro. 82. Giacino J, Whyte J, Bagiella E, et al. Placebo-controlled trial of
2016.12.002 amantadine for severe traumatic brain injury. N Engl J Med. 2012;
71. Manktelow AE, Menon DK, Sahakian BJ, Stamatakis EA. Working 366(9):819–826. doi:10.1056/NEJMoa1102609
memory after traumatic brain injury: The neural basis of improved 83. Ghalaenovi H, Fathahi A, Koohpayehzadeh J, et al. The effects of
performance with methylphenidate. Front Behav Neurosci. 2017;11: amantadine on traumatic brain injury outcome: a double -blind
163. doi:10.3389/fnbeh.2017.00058 randomized controlled clinical trial. Brain Inj. 2018;32(8):1050–
72. Dorer CL, Manktelow AE, Allanson J, et al. Methylphenidate- 1055. doi:10.1080/02699052.2018.1476733
mediated motor control network enhancement in patients 84. Hammond FH, Sherer M, Malec JF, et al. Amantadine did not
with traumatic brain injury. Brain Inj. 2018;32(8):1040–1049. positively impact cognition in chronic traumatic brain injury: a
doi:10.1080/02699052.2018.1469166 multi-site randomized controlled trial. J Neurotrauma. 2018;35(19):
73. Dymowski AR, Ponsford JL, Owens JA, Olver JH, Ponsford 2298–2305. doi:10.1089/neu.2018.5767
M, Willmott C. The efficacy and safety of extended-release 85. Heurteaux C, Gandin C, Borsotto M, et al. Neuroprotective and
methylphenidate following traumatic brain injury: a randomised neuroproliferative activities of NeuroAid (MLC601, MLC901), a
controlled pilot study. Clin Rehabil. 2017;31(6):733–741. Chinese medicine, in vitro and in vivo. Neuropharmacology. 2010;
doi:10.1177/0269215516655590 58(7):987–1001. doi:10.1016/j.neuropharm.2010.01.001
74. Barnett M, Reid L. The effectiveness of methylphenidate in im- 86. Theadom A, Barker-Collob S, Jonesa KM, Parmara P,
proving cognition after brain injury in adults: a systematic review. Bhattacharjee R, Feigin VL. MLC901 (NeuroAiD IITM ) for cogni-
Brain Inj. 2020;34(1):1–10. doi:10.1080/02699052.2019.1667538 tion after traumatic brain injury: a pilot randomized clinical trial.
75. Huang CH, Huang CC, Sun CK, Lin GH, Hou WH. Eur J Neurol. 2018;25(8):1055–1062, e1081–1082. doi:10.1111/
Methylphenidate on cognitive improvement in patients with trau- ene.13653
matic brain injury: a meta-analysis. Curr Neuropharmacol. 2016; 87. Bogner J, Dijkers M, Hade EM, et al. Contextualized treatment
14(3):272–281. doi:10.2174/1570159x13666150514233033 in traumatic brain injury inpatient rehabilitation: effects on out-
76. Chien Y, Chien Y, Liu C, Wu H, Chang C, Wu M. Effects comes during the first year after discharge. Arch Phys Med Rehabil.
of methylphenidate on cognitive function in adults with trau- 2019;100(10):1810–1817. doi:10.1016/j.apmr.2018.12.037

www.headtraumarehab.com

You might also like