7

Attention

OVERVIEW

Deficits in attention are more commonly found among individuals with more severe traumatic brain injuries (TBI), and may encompass delayed reaction time, reduced speed of information processing, or challenges with concentration, forgetfulness, or doing more than one thing at a time (e.g., walking and talking). This chapter presents cognitive rehabilitation therapy (CRT) interventions aimed to restore attentional capacity, divided by phase of recovery following moderate-severe TBI (i.e., subacute and chronic). Controlled studies are described in detail within these sections, divided by treatment comparator arm, followed by descriptions of the noncontrolled studies. The committee’s conclusions are presented at the end of the chapter.

The committee reviewed six randomized controlled trials (RCTs), including two crossover studies, of treatments intended to improve attention. All six involved modular treatment directed at one or more attentional processes. All used decontextualized treatment materials, and all were categorized as restorative. The trials involved a total of 264 study participants; treatment group sizes in individual trials ranged from 7 to 43 patients. Nearly all of the patients suffered moderate-severe injuries 6 weeks to many months prior to study enrollment. Study participants were generally in their late 20s to early 30s.

The committee did not identify any nonrandomized, controlled parallel group designs of treatments for attention deficits, however it did review two pre-post single group studies and one single-subject, multiple baseline experiment. These studies also employed primarily modular restorative



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7 Attention OVERVIEW Deficits in attention are more commonly found among individuals with more severe traumatic brain injuries (TBI), and may encompass delayed reaction time, reduced speed of information processing, or challenges with concentration, forgetfulness, or doing more than one thing at a time (e.g., walking and talking). This chapter presents cognitive rehabilitation therapy (CRT) interventions aimed to restore attentional capacity, divided by phase of recovery following moderate-severe TBI (i.e., subacute and chronic). Controlled studies are described in detail within these sections, divided by treatment comparator arm, followed by descriptions of the noncontrolled studies. The committee’s conclusions are presented at the end of the chapter. The committee reviewed six randomized controlled trials (RCTs), in- cluding two crossover studies, of treatments intended to improve attention. All six involved modular treatment directed at one or more attentional processes. All used decontextualized treatment materials, and all were cat- egorized as restorative. The trials involved a total of 264 study participants; treatment group sizes in individual trials ranged from 7 to 43 patients. Nearly all of the patients suffered moderate-severe injuries 6 weeks to many months prior to study enrollment. Study participants were generally in their late 20s to early 30s. The committee did not identify any nonrandomized, controlled paral- lel group designs of treatments for attention deficits, however it did review two pre-post single group studies and one single-subject, multiple baseline experiment. These studies also employed primarily modular restorative 125

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126 COGNITIVE REHABILITATION THERAPY FOR TBI treatments, and all were delivered to patients in the chronic phase with moderate-severe injuries. The committee did not identify any studies assess- ing CRT interventions for attention in patients with mild TBI. Table 7-1 presents a summary of all included studies in this review. MODERATE-SEVERE TBI Subacute Phase of Recovery Comparator Group: Non-CRT Content Gray et al. (1992) compared approximately 17 hours of computer administered modules stressing various dimensions of attention to about 12 hours of recreational computing that excluded externally paced tasks or tasks that required rapid processing and responding. This study found a positive effect of training on psychometric measures of attention, par- ticularly the type that require numerical manipulation in working memory. These effects grew in significance in follow-up compared to the immediate posttreatment measures. This pattern is of some concern, since the median time postinjury was 20 weeks, a point at which natural recovery may be ongoing; therefore, imbalance in the acuity of injury between groups might produce such a result. However, time postinjury was statistically controlled for, and measures of functions unrelated to attention did not show greater improvement in the treatment group, lending some specificity to the find- ings. In this study nearly half of the subjects had nontraumatic injuries, but the authors report no interaction between diagnosis and treatment benefit. The credibility of this study is compromised due to its nonreport- ing of sample sizes for analysis posttreatment, especially at the 6-month follow-up. Furthermore, standard deviations of the outcomes were not provided. Comparator Group: Other CRT Content Novack et al. (1996) studied participants who were 3 to 6 months postinjury. This study was conducted in an acute inpatient rehabilitation population approximately 3 to 6 weeks postinjury, a time when many of the patients were confused and highly impaired. One group received a structured program of attention training. The other group received a variety of other rehabilitation interventions that involved cognitive rehabilitation components that did not specifically focus on attention. Outcomes were assessed with respect to several psychometric measures of attention as well as the Functional Independence Measure (FIM). Both groups improved significantly from pre- to posttreatment, but to a comparable degree.

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TABLE 7-1 Evidence Table: Attention TBI Severity Study N Level Brief Narrative Comparator Outcome Measures Findings RCT Gray et al. 31 Mild, Patients with attentional Y • Psychometric measures: Significant differences 1992 moderate, deficits randomized ▪ Paced Auditory Serial between groups severe to two groups. The Non-CRT Addition Test (PASAT) on psychometric treatment group received Content: ▪ Wechsler Adult Intelligence measures of attention computerized attention Recreational Scale-Revised (WAIS-R) at immediate and six- training including: computing • Frontal functions: month follow-up. • Reaction time training ▪ Wisconsin Card Sorting Test • Rapid number (WCST) comparison ▪ Finger tapping • Digit symbol transfer ▪ Word fluency • Alternating Stroop • Other attentional functions: program ▪ Letter cancellation • Divided attention tasks ▪ Picture completion ▪ Time estimation McMillan 145 Moderate Sessions of supervised Y • Test of Everyday Attention Between-group et al. 2002 mindfulness practice using • Adult Memory and comparison not an audiotape obtained No or Non-CRT Information Processing Battery significant for any from Jon Kabat-Zinn. Content: • PASAT measure. Participants were asked • Group with • Trail Making Test to practice daily with this therapist • Self-reported: tape in the intervening contact and ▪ Sunderland Memory periods. physical Questionnaire exercise (PE) ▪ Cognitive Failures • Group with Questionnaire no treatment ▪ Hospital Anxiety and Depression Questionnaire 127 continued

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TABLE 7-1 Continued 128 TBI Severity Study N Level Brief Narrative Comparator Outcome Measures Findings ▪ General Health ▪ Rivermead Post- Concussional Symptoms Questionnaire Niemann 26 Moderate- Computerized attention Y • Attention Authors report et al. 1990 Severe training with visual, ▪ Test d2 attention group auditory, and divided (i.e., Other CRT ▪ PASAT-R improved significantly both) training components, Content: ▪ Divided Attention Test more than control on further subdivided into Memory training ▪ Trail Making Test, Part B the three measures focused and alternating of equivalent • Memory of attention; memory attention tasks duration and ▪ Rey Auditory Verbal group improved more Training accompanied intensity Learning Test-Modified than attention group on by feedback and strategy (RAVLT-M) one measure. teaching ▪ Block Span Learning Test Novack 44 Severe Hierarchical training of Y • Wechsler Memory Scale- Between-group et al. 1996 attention skills for lowest Revised (WMS-R) comparison not level of functioning Other CRT • Single reaction time significant for any involved focused and Content: • Choice reaction time measure. sustained attention, more Unstructured • Functional Independence challenging tasks requiring stimulation Measure (FIM)—Activities of selective attention, program Daily Living alternating attention, and • FIM—Cognition divided attention. Each • Neuropsychological tests: level of the hierarchy ▪ Logical Memory I and II included multiple tasks. ▪ Sentence Repetition Test

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▪ Judgment of Line Orientation ▪ Trail Making Test ▪ Wide-Range Achievement Test-Revised (WRAT-R), arithmetic subtest ▪ Visual imperception Ruff et al. 15 Severe Two groups received two Y • Attention Attention measures 1994 treatments (attention ▪ Ruff 2 & 7 Selective at posttreatment did and memory training) Other CRT Attention test not show significant delivered via THINKable, Content: Group ▪ WAIS-R Digit Symbol between-group a computer-based, multi- A received ▪ Continuous Performance comparison. media program. attention Test training, then • Memory memory training. ▪ Rey Auditory Verbal Group B received Learning Test memory training, ▪ Corsi Block Learning Test then attention • Behavioral assessments training. 129 continued

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TABLE 7-1 Continued 130 TBI Severity Study N Level Brief Narrative Comparator Outcome Measures Findings Sohlberg et 14 Moderate- Compares Attention Y • Neuropsychological attention Training showed al. 2000 Severe Process Training (APT) tests: improvement on to education, delivered to No or Non-CRT ▪ Trail Making Test PASAT, Stroop, and two groups in a crossover Content: ▪ PASAT Trail Making Test. design. APT aims to Placebo—Brain ▪ Gordon Diagnostic Patients reported a improve memory, learning, Injury Education ▪ Controlled Oral Word significant difference in and some aspects of and Supportive Association Task (COWAT) attention and memory executive control. Listening ▪ Covert Orienting in the treatment group ▪ Continuous Performance versus education. Task Subjects with greater ▪ Stroop task changes had improved ▪ Sternberg tasks score on PASAT. • Self-report: Significant more ▪ Attention Questionnaire reports of improvement ▪ Brock Adaptive Functioning to daily life (via Questionnaire (BAFQ) questionnaires) were ▪ Dysexecutive Questionnaire given by participants (DEX) after APT. Pre-Post Single Group Park et al. 23 Moderate- Examined the use of the N • PASAT Post-testing showed 1999 Severe Attention Process Training • Consonant trigrams (Brown- significant improvement (APT) to determine if Peterson task) on PASAT and APT improves cognitive • Beck Depression Inventory Consonant trigrams. function versus learning (BDI) No significant specific skills. improvement on BDI. Results are mediated by lack of control group.

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Stathopoulou 5 Severe Included a “Captain’s N • Electroencephalogram (EEG) Sustained attention, and Lubar Log” computer training variables alternating attention, 2004 program for attention • WAIS-R and divided attention skills with tasks for • PASAT improved in three of vigilance, inattention, • Self-report measure of severity five subjects. Selective prudence, impulsivity, (of deficit) for memory and attention improved in focus, variability, and attention symptoms all subjects. Focused speed. Participants attention improved in selected, discriminated, or two of five subjects. matched visual pictures or Results are mediated by sounds. lack of control group. Single Subject, Multiple Baseline Experimental Design Gansler and 4 Severe Hierarchically organized N • Neuropsychological tests: Posttreatment test McCaffrey attention training program ▪ WMS-R results proved 1991 based on Posner’s four ▪ Trail Making Test not significant for component model of ▪ Minute Estimation Test all participants. attention. ▪ Thurstone Word Fluency Participants reported Test increase in ADLs. ▪ Grooved Pegboard Test ▪ WAIS-R • Psychological variables for depression, anxiety, and anger • Self-report of ADLs 131

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132 COGNITIVE REHABILITATION THERAPY FOR TBI Chronic Phase of Recovery Studies of chronic, moderate-severe TBI included four RCTs (McMillan et al. 2002; Niemann et al. 1990; Ruff et al. 1994; Sohlberg et al. 2000) comparing five treatment arms with patients in the chronic phase. Inter- ventions in three (Niemann et al. 1990; Ruff et al. 1994; Sohlberg et al. 2000) of these RCTs consisted of some form of attention training exercises, similar to those employed by Gray et al. (1992) (see above), and most were delivered via computer. Training ranged from 10 to 24 hours and typically involved several different attention-demanding tasks that progressed in difficulty with patient improvement. Some treatments included therapist- delivered goal setting, feedback, and review of performance, including one study of Attention Process Training (APT), a manualized treatment approach that specifies therapist feedback more systematically. The fourth RCT (McMillan et al. 2002), also the largest trial, used mindfulness train- ing. Unlike the other attention treatments, mindfulness training did not in- volve practice with attention-demanding tasks but rather separate sessions focused on breathing. Therapist-led training in this study was fewer than 4 hours for both mindfulness training and the active comparison condition, but with home practice assigned. Comparator Group: No or Non-CRT Content McMillan et al. (2002) compared the effects of instruction in mindful- ness training to comparable instruction in physical exercise (non-CRT con- tent) and a no-treatment control where participants received no therapist contact but were assessed at the same intervals. Thus, this was the only study that had a comparator arm of no treatment. Outcomes were assessed in terms of neuropsychological measures of attention as well as several self- report measures of mental health status and lapses of attention in everyday life. The mindfulness intervention outcomes on attention were no different than those of physical exercise or no intervention. Sohlberg et al. (2000) compared 24 hours of manualized APT deliv- ered over 10 weeks to 10 hours of brain injury education—a non-CRT intervention—delivered over the same time period, in an RCT with out- comes assessed at the point of crossover and again at trial completion. Outcome measures included standardized neuropsychological measures of attention, laboratory measures of information processing intended to assess the functioning of specific neural networks subserving separable attentional domains, and coded qualitative interviews regarding real-world changes re- sulting from treatment. This trial found positive effects of attention training on the Paced Auditory Serial Addition Test (PASAT), a measure of working

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133 ATTENTION memory and speeded mental addition, and on the Memory for Location task, a measure of location working memory. On the Stroop task and the Trail Making Test, members of the APT group were characterized by “low vigilance” at baseline. The trial did not find such effects on verbal work- ing memory, verbal fluency, or on the laboratory tasks designed to isolate the functions of specific neural networks. Although the patients were not blinded to the content of their treatment, there were significantly more re- ports of attention improvements in daily life after the APT treatment than after brain injury education. Lending some support to the validity of these reports, reports of everyday attention benefits correlated with improvement in PASAT scores. This was a small study, with 14 participants, all with moderate-severe injuries. Two subjects were not included in the structured interview to assess improvement because they did not recall their par- ticipation in the treatment. This situation is problematic, as it reduces the sample size to 12 and raises concerns about generalization to patients with substantial memory impairment. In addition, there were several statistical tests, with no adjustment for multiple testing. Comparator Group: Other CRT Content Two trials (Neimann et al. 1990; Ruff et al. 1994) studied the impact of an attention training program, compared to a memory training program, on measures of attention; thus memory training served as the control treatment. Neimann et al. (1990) provided approximately 36 hours of training on three different aspects of attention, or a comparable amount of training on internal and external memory strategies. Neuropsychological measures of attention and memory were assessed. Based on a significant result from a MANOVA test for the four attention measures, the authors reported “partial support” for the treatment prediction that attention training would provide more robust impact on attention measures than the comparison memory training. However, in post hoc testing, only one of the attention measures differed significantly between groups. Inspection of the pattern of improvement suggests that three attention measures improved more in the group that received attention training, and one improved more in the group that received memory training. Ruff et al. (1994) conducted a similar study in which the two treat- ment groups received both attention training and memory training, but in counterbalanced order. However, the authors did not conduct statistical testing at the midpoint of treatment (when a parallel group comparison would have been possible) because of the small sample size. They report benefit in both domains at the end of combined treatment, but inspection of

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134 COGNITIVE REHABILITATION THERAPY FOR TBI the pattern of scores at the midpoint suggests that some attention measures improved more in one group and some in the other. Pre-Post Designs Park et al. (1999) studied the effects of 40 hours of APT training in 23 individuals with chronic, moderate-severe TBI using the PASAT and Consonant Trigrams tests as outcome measures, along with the Beck De- pression inventory. Stathopoulou and Lubar (2004) studied five people with severe brain injury between 1.5 and 23 years postinjury. The patients received 18 hours of attention training using “Captain’s Log,” a commer- cial computerized product that administers tasks involving various chal- lenges to verbal and visual attention and memory. Participants were tested only once pre and once post, using digit span and digit symbol subtests of the Wechsler Adult Intelligence Scale (WAIS), the PASAT, a continuous performance test, a self-report measure of severity of a number of atten- tion and memory symptoms rated on a five-point scale from “no problem” to “severe problem,” and electroencephalogram (EEG) spectral measures. These studies—all of which were conducted at a time when rapid natural recovery would be unexpected—showed improvement in some of the out- come measures relevant to treatment. However, none of these studies had an adequate control for practice on the outcome assessments themselves, which were assessed twice, so none provides strong support for a treat- ment effect. Single-Subject, Multiple Baseline Experiment Gansler and McCaffrey (1991) conducted four single-subject experi- ments in which individuals with severe TBI—4 to 27 years postinjury—re- ceived repeated testing on a set of information processing measures modeled on Posner’s attention components. The measures were administered weekly, beginning 4 weeks prior to training, during the 8 weeks of training, and at 1 month after training. Training consisted of 8 weeks of hierarchically or- ganized modules of attention totaling about 64 hours. Other psychological measures were also administered weekly and neuropsychological measures at baseline, after training, and at follow-up; participants also completed a self-assessment of ADL performance and their satisfaction with it. Improve- ment on attention measures and psychological measures was negligible for all participants, though there were larger effects on self-appraisal of ADL performance. This result could suggest that the treatment imparted compensatory skills for managing attention deficits that were evident in real-world ADL tasks but not on controlled attention processing tasks.

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135 ATTENTION However, the result is also consistent with biasing of self-reported benefit because of expectation. CONCLUSIONS: ATTENTION The committee found limited evidence from one RCT (Sohlberg et al. 2000) to support conclusions about the impact on patient-centered outcomes (quality of life, functional status) in moderate-severe TBI. The committee found limited evidence from one RCT (Gray et al. 1992) on long-term impact of treatment (6 months) in the subacute phase as assessed with psychometric measures, particularly the type requiring numerical manipulation in working memory. Considering subacute and chronic studies together, the committee found limited evidence from two studies (Grey et al. 1992; Sohlberg et al. 2000), that intensive practice of hierarchical attention-demanding tasks had a positive impact on psycho-metric measures of attention in the immediate posttreatment period and/or at follow-up. The review did not include any RCTs or other study designs on CRT for attention in mild TBI. Two studies (Gray et al. 1992; Novack et al. 1996) provided limited evidence to conclude that CRT improves attention in subacute, moderate-severe TBI patients. In studies of moderate-severe TBI patients in the chronic phase of recovery, a few, relatively small RCTs with several methodologic limitations provided mixed support for treat- ment benefit. These trials tested intensive practice of hierarchical attention- demanding tasks on some psychometric measures of attention, with positive immediate outcomes. However, none studied the durability of benefits, and only one study assessed treatment impact with respect to patient-centered outcomes (i.e., Sohlberg et al. [2000] found a preliminary association of improved psychometric measures of attention with real-world benefits). Data from pre-post designs, although consistent with some treatment ben- efit, provide weak support because of the possible confounding effect of practice on the outcome measures. Several of the RCTs with equivocal results (Niemann et al. 1990; Ruff et al. 1994) used intensive memory training as a control condition. Since all tasks requiring effort place demands on attention, it is possible that the overlap in treatment outcomes between treatment groups in such studies reflects the overlap in mental demands of treatment content, potentially attenuating or accounting for the lack of finding of differences in attention outcomes. Of note, the two studies that provided the strongest support for

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136 COGNITIVE REHABILITATION THERAPY FOR TBI the efficacy of hierarchical attention training employed non-CRT compara- tor conditions. REFERENCES Gansler, D. A., and R. J. McCaffrey. 1991. Remediation of chronic attention deficits in trau- matic brain-injured patients. Archives of Clinical Neuropsychology 6(4):335–353. Gray, J. M., I. Robertson, B. Pentland, and S. Anderson. 1992. Microcomputer-based atten- tional retraining after brain damage: A randomised group controlled trial. Neuropsycho- logical Rehabilitation 2(2):97–115. McMillan, T., I. H. Robertson, D. Brock, and L. Chorlton. 2002. Brief mindfulness training for attentional problems after traumatic brain injury: A randomised control treatment trial. Neuropsychological Rehabilitation 12(2):117–125. Niemann, H., R. M. Ruff, and C. A. Baser. 1990. Computer-assisted attention retraining in head-injured individuals: A controlled efficacy study of an outpatient program. Journal of Consulting and Clinical Psychology 58(6):811–817. Novack, T. A., S. G. Caldwell, L. W. Duke, T. F. Bergquist, and R. J. Gage. 1996. Focused versus unstructured intervention for attention deficits after traumatic brain injury. Jour- nal of Head Trauma Rehabilitation 11(3):52–60. Park, N. W., G. B. Proulx, and W. M. Towers. 1999. Evaluation of the attention process train- ing programme. Neuropsychological Rehabilitation 9(2):135–154. Ruff, R. M., R. Mahaffey, J. Engel, C. Farrow, D. Cox, and P. Karzmark. 1994. Efficacy study of THINKable in the attention and memory retraining of traumatically head-injured patients. Brain Injury 8(1):3–14. Sohlberg, M. M., K. A. McLaughlin, A. Pavese, A. Heidrich, and M. I. Posner. 2000. Evalu- ation of attention process training and brain injury education in persons with acquired brain injury. Journal of Clinical and Experimental Neuropsychology 22(5):656–676. Stathopoulou, S., and J. F. Lubar. 2004. EEG changes in traumatic brain injured patients after cognitive rehabilitation. Journal of Neurotherapy 8(2):21–51.