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2011 28: 27 originally published online 21 October 2010Journal of Pediatric Oncology NursingKristina K. Hardy, Victoria W. Willard and Melanie J. Bonner

Computerized Cognitive Training in Survivors of Childhood Cancer: A Pilot Study  

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Computerized Cognitive Training in Survivors of Childhood Cancer: A Pilot Study

Kristina K. Hardy, PhD1, Victoria W. Willard, MA1,and Melanie J. Bonner, PhD1

Abstract

The objective of the current study was to pilot a computerized cognitive training program, Captain’s Log, in a small sample of survivors of childhood cancer. A total of 9 survivors of acute lymphoblastic leukemia and brain tumors with attention and working memory deficits were enrolled in a home-based 12-week cognitive training program. Survivors returned for follow-up assessments postintervention and 3 months later. The intervention was associated with good feasibility and acceptability. Participants exhibited significant increases in working memory and decreases in parent-rated atten-tion problems following the intervention. Findings indicate that home-based, computerized cognitive intervention is a promising intervention for survivors with cognitive late effects; however, further study is warranted with a larger sample.

Keywords

computerized cognitive training, intervention, childhood cancer, survivorship, attention problems

Cure rates for childhood cancer have increased markedly over the last 50 years to nearly 80% (American Cancer Society, 2008). Despite the favorable prognosis for survival, patients are at high risk for both acute and late-occurring sequelae associated with their disease and treatments. In particular, children diagnosed with acute lymphoblastic leukemia (ALL) and primary brain tumors (BTs) who are treated with therapies that affect the central nervous system (CNS; ie, intrathecal methotrexate, cranial radiation, neu-rosurgery) are at the highest risk for cognitive, social, and psychological late effects. Indeed, various studies have shown that 40% to 100% of survivors of BT (see Mulhern & Palmer, 2003) and at least 30% of survivors of ALL (see Campbell et al., 2007) will evidence some sort of cognitive deficit. The impact of both the disease and its treatments can have deleterious effects on the brain and the cognitive functioning of these survivors, with younger age at diag-nosis, longer time since diagnosis, and female sex increasing the risk of neurocognitive late effects (Mulhern, Merchant, Gajjar, Reddick, & Kun, 2004).

Findings from the last decade suggest that declines in intelligence and achievement observed in survivors are secondary to specific deficits in attention, short-term memory, speed of processing, visuomotor coordination, and/or sequencing abilities (Campbell et al., 2007; Mulhern & Palmer, 2003). Attentional deficits are perhaps the most

prevalent (Anderson, Godber, Smibert, Weiskop, & Ekert, 2004; Langer et al., 2002; Lockwood, Bell, & Colegrove, 1999; Merchant et al., 2002; Reeves et al., 2006) and involve difficulty with shifting of attention and sustained attention. Moreover, these deficits are significantly correlated with problems in higher-order cognitive processes such as mem-ory and learning tasks and may be particularly influential in the academic environment (Reeves et al., 2006).

Based on this evidence of robust attention and working memory deficits, researchers have begun to investigate the efficacy of empirically supported treatments for these impairments, including pharmacotherapy and cognitive remediation (Butler & Mulhern, 2005). Specifically, the psychostimulant methylphenidate (MPH; commonly known as Ritalin) has contributed to improved functioning in sur-vivors (Conklin et al., 2007; Conklin et al., 2010; Mulhern, Khan, et al., 2004; Thompson et al., 2001). In the largest trial, Mulhern, Khan, et al. (2004) found statistically sig-nificant and clinically meaningful results for the use of

1Duke University Medical Center and Duke University,Durham, NC, USA

Corresponding Author:Kristina K. Hardy, Division of Neuropsychology, Children’s National Medical Center, 111 Michigan Ave., NW Washington, DC, 20010, USAEmail: kkhardy@cnmc.org

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28 Journal of Pediatric Oncology Nursing 28(1)

MPH with survivors, including a reduction in attentional and social deficits over a 3-week trial. Despite the initial positive findings for the use of psychostimulants, there are some concerns, including adverse effects in a small group of participants (Mulhern, Khan, et al., 2004), unknown long-term effects (Jasper et al., 2008), and potential reluc-tance on the part of parents to administer more medication to their already “medically fragile” survivors.

A multicenter, randomized clinical trial has also been conducted with cognitive remediation (Butler et al., 2008). This program focused on the acquisition of strategies designed to improve performance on cognitive and aca-demic outcomes, including attentional skills, and consisted of sessions with a therapist every week for 4 to 6 months. Results with 161 survivors yielded parent reports of increased attention and academic achievement over the course of the intervention (Butler et al., 2008). However, effect sizes were small, albeit comparable with those in other interventions using similar methodologies with other patient groups. A similar intervention using problem-solving skills training was recently piloted in a small group (n = 12) of survivors (Patel, Katz, Richardson, Rimmer, & Kilian, 2009). This intervention focused on cognitive, learning, and problem-solving skills for 15 weekly training sessions, with the majority of participants completing at least 70% of the intervention. Of note, families who did not complete treatment cited the inconvenience of travel-ling to the medical center every week (this was also the primary reason given for not enrolling in the intervention). Despite this limitation, the program showed preliminary efficacy, with participants completing the intervention making gains, albeit not significant ones, on each outcome measure (Patel et al., 2009). Results from both interventions suggest that the mode of treatment may make it impractical for larger groups of survivors who live far away from a medical center that could provide the intensive program. Therefore, it is critical that effective short-term and home-based interventions be developed so as to be applicable to a wide range of survivors, which will not be limited by time, distance, or cost.

One such intervention is computerized cognitive training programs that have been developed to target attention prob-lems, primarily in children and adolescents diagnosed with attention-deficit hyperactivity disorder (ADHD). Most consist of a series of attention/short-term memory tasks of increasing complexity, and there is emerging support for their efficacy with the ADHD population (Bangirana et al., 2009; Kerns, Eso, & Thomson, 1999; Klingberg et al., 2005; Rabiner, Murray, Skinner, & Malone, 2010; Slate, Meyer, Burns, & Montgomery, 1998). Furthermore, such programs can be completed at home with limited formal supervision by a mental health professional, making them particularly attractive for a survivor population. One study in particular

(Klingberg et al., 2005) assessed the efficacy of a home- and/or school-based cognitive training program targeting work-ing memory skills. Results were robust, indicating that chil-dren who completed the intervention improved significantly on numerous working memory tasks as well on parent-rated reports of ADHD symptoms (Klingberg et al., 2005). What was important was that improvements in the ADHD sample were maintained, or even increased, after a 3-month follow-up period.

In summary, neurocognitive late effects in survivors of CNS-affecting childhood cancer are well established in the literature. Specifically, deficits in attention and working memory appear to impede survivors’ ability to acquire new information at developmentally appropriate rates. Existing interventions, including pharmacotherapy and cognitive remediation, have shown promise but are likely to be impractical or ineffective for a sizable propor-tion of children. Computerized cognitive training pro-grams developed to address inattention in children with ADHD have recently shown good efficacy in a limited number of trials. As such, the current study piloted the use of one of these programs, Captain’s Log, with a small sample of survivors of childhood cancer who demonstrated treatment-related attention and/or working memory dif-ficulties. We hypothesized that the home-based computer-ized attention training program would be feasible and acceptable for survivors of pediatric cancer as measured by parent and child report of technical ease of use and satisfaction and program records of treatment compliance. It was also predicted that participants who successfully completed the intervention would show increases in atten-tion and working memory of moderate effect size at the end of the intervention period as compared with baseline functioning. Furthermore, these increases would be main-tained after a 3-month follow-up period.

MethodsParticipants and Procedures

Participants included survivors of CNS-affecting cancer (ALL, n = 3; BT, n = 6) aged 10 to 17 years who were at least 1 year posttreatment. We assessed the intervention in both illness populations given the possibility of their dif-ferent cognitive and physical deficits. Specifically, survivors of ALL generally have less severe cognitive and physical limitations compared with survivors of BTs; therefore, it is possible that the acceptability of, and response to, the intervention may differ between groups. As such, participants were recruited from the divisions of pediatric hematology/oncology and pediatric neuro-oncology at a large medical center in the Southeast United States. A letter explaining the purpose of the study was sent to parents who were

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Hardy et al. 29

invited to contact study personnel for a thorough review of the study and to schedule a screening appointment.

After obtaining written informed consent and assent (from parents and child, respectively), screening procedures included administration of an abbreviated intellectual test battery, 2 working memory tasks, and several questionnaire measures regarding adaptive, behavioral, emotional, and attentional functioning (see list of measures below). Based on data from the screening visit, enrollment in the interven-tion was determined by either of the following: (1) A T-score greater than the 75th percentile on either the Cognitive Problems/Inattention or the DSM-IV Inattention subscales of the Conners’ Parent Rating Scale (CPRS) and (2) one or more standard deviations (SDs) below the mean on the Work-ing Memory Index (WMI) of the Wechsler Intelligence Scale for Children–4th edition (WISC-IV) or a WMI that is one or more SDs below the participant’s estimated IQ. These criteria were based on the eligibility criteria used in a trial of MPH with survivors of childhood cancer (Mulhern, Khan, et al., 2004). Additionally, participants who were taking stimulant medications (stable dose for at least 30 days) for attentional difficulties were allowed to participate.

Intervention Design and ProceduresThe intervention program, Captain’s Log (http://www .braintrain.com), consists of 33 multilevel, entertaining, game-like “brain-training” exercises aimed at improving memory, attention, concentration, listening skills, self-control, patience, and processing speed and are in use in more than 650 US schools. The exercises are designed to develop, improve, and remediate attention, concentration, memory, hand–eye coordination, fundamental numerical concepts, and basic problem solving/reasoning skills. Pro-gram complexity and difficulty ranges are such that the exercises are appropriate for use with children as young as age 6 through adulthood. In addition, the program is adapt-able for home use, with minimal training and support.

Although no “best dose” has been established for this intervention, we were interested in assessing the program when used at least 50 minutes per week for 12 weeks, a level that is consistent with outpatient rehabilitation pro-grams, including the 2 prior cognitive interventions assessed with survivors (Butler et al., 2008; Patel et al., 2009). To promote compliance and maintain children’s interest, par-ticipants earned gift cards after weeks 4, 8, and 12. Addition-ally, all families had weekly phone-based check-ins with study personnel to ensure compliance and to address prob-lems (eg, adverse events, technical difficulties) efficiently.

Participants returned to the clinic following completion of the intervention and 3 months later for follow-up testing; this interval has been used in prior research to demonstrate maintenance of attentional improvements following cognitive

training in children with ADHD (Klingberg et al., 2005). In all, 8 of 9 participants (88.9%) completed all follow-up visits (1 survivor did not return for the 3-month visit).

MeasuresScreening Measures

Wechsler Abbreviated Scale of Intelligence (Wechsler, 1999). This is a brief measure of intelligence usable with people aged 6 to 89 years and yields estimation of a full-scale IQ, verbal IQ, and performance IQ. Wechsler Abbreviated Scale of Intelligence scores were used in the screening phase to verify that survivors had adequate intellectual functioning (IQ > 70).

Child Behavior Checklist (CBCL; Achenbach, 1991). This is a well-known parent-completed measure of the emotional/behavioral functioning of children. Parents respond to a num-ber of open-ended and forced-choice questions describing their child’s social, academic, behavioral, and emotional functioning across home and school domains. CBCL scores were used in the screening phase to assess participants’ behavioral and psychiatric functioning.

Outcome MeasuresWechsler Intelligence Scale for Children, 4th Edition. The

WISC-IV (Wechsler, 2003) is a widely used measure of intellectual functioning in children aged 6 to 16. For the purposes of the proposed study, only the subtests from the WMI (ie, Digit-Span and Letter-Number Sequencing) were used. The WMI was our primary outcome measure and was administered during the screening, postintervention, and 3-month follow-up assessments.

Conners’ Parent Rating Scale (Conners, 1997). The CPRS is a parent-reported measure of children and adolescents’ attention and behavioral functioning. The measure has been widely used with ADHD and community samples in research and clinical settings, and the factor structure is similar for ADHD and cancer survivor samples (Helton, Corwyn, Bonner, Brown, & Mulhern, 2006). Parents com-pleted the questionnaire at all 3 time points: screening, postintervention, and 3-month follow-up.

Feasibility and acceptability questionnaire. There is no standardized measure of feasibility and acceptability for use with this type of intervention. Therefore, we developed a 15-item survey for parents and children assessing techni-cal feasibility, adherence, satisfaction, and ease of use. The questionnaire was completed by phone during week 4 and week 8 of the intervention and during the postintervention assessment by either the survivor or the parent.

Analytical Plan. To assess feasibility and acceptability, we used descriptive and summary statistics to report parent and child ratings of the intervention’s technical feasibility, ease of use, and satisfaction, as well as to detail the number

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30 Journal of Pediatric Oncology Nursing 28(1)

and type of adverse events and the number of sessions completed by each participant. In our analysis of prelimi-nary efficacy, we used linear mixed models to determine changes in attentional functioning postintervention and after a 3-month follow-up.

ResultsParticipants

Participants included 9 children (44.4% female) diagnosed with and treated for CNS-affecting cancer: 3 (33.3%) with ALL, 4 (44.4%) with medulloblastoma/primitive neuro-ectodermal tumor, and 2 (22.2%) with ependymoma. All 3 ALL patients were treated with chemotherapy only; all 6 BT patients were treated with surgery, 5 (83.3%) with chemotherapy, and 5 (83.3%) with radiation therapy. Sur-vivors were an average of 13.3 years of age (SD = 2.44) and an average of 5.7 years (SD = 3.20; range = 1-10 years) off-therapy at screening. The demographic characteristics of the sample are listed in Table 1.

At screening, participants had average IQs of 96.1 (SD = 14.34; range = 74-114) and an average WMI of 88.0 (SD = 12.49; range = 65-107). Per parent report, participants had few emotional or behavioral difficulties on the CBCL other than attention problems (T = 60.8; SD = 7.96). Specifically, the average internalizing problems T was 53.3 (SD = 11.67), and the average externalizing problems T was 49.7 (SD = 13.31). Additionally, on the CPRS, parents reported an aver-age T score of 68.8 (SD = 11.19) on the cognitive problems subscale, 64.4 (SD = 11.43) on the ADHD index, and 66.4 (SD = 9.80) on the DSM-IV Inattention subscale.

Feasibility and AcceptabilityParticipants and their parents reported few technical prob-lems with either the computer or the intervention program over the course of the trial; no technical problems prevented

use or practice of the program. No physical, behavioral, or emotional adverse events were reported as a result of participation. Children reported good compliance with the training schedule, though computer records indicated a wide range of time spent on the intervention, from 9 to 53 sessions (mean = 28.4) and from 3.7 to 20.8 training hours (mean = 11.4).

Intervention OutcomesParticipants’ working memory scores generally increased from baseline to the follow-up assessments (see Figure 1 and Table 2). Specifically, there was a trend for the overall WMI [F(2, 15.11) = 3.16; P = .07] to increase from baseline to 3-month follow-up, with an average gain of 8.4 standard scale points. Analysis of subscale improvement indicated that only Digit-Span Forward was associated with a signifi-cant increase over time [F(2, 15.09) = 6.79; P < .01]; neither Digit-Span Backward [F(2, 15.27) = 0.10; NS] nor Letter-Number Sequencing [F(2, 15.38) = 0.40; NS] scaled scores improved significantly postintervention. However, parent-reported attention problems, as measured by the Cognitive Problems Index [F(2, 15.10) = 6.98; P < .01], significantly decreased across the 3 time points (see Figure 1).

To identify factors related to changes in working mem-ory and parent-rated attention scores, correlation coeffi-cients were computed between these variables, participants’ baseline IQ, and training variables tracked by the interven-tion program. Our study was likely underpowered to detect all but very large associations between variables; as such, these results are presented with no significance values. Changes in the WMI were modestly correlated with the amount of time children spent training (r = 0.28) and with their response accuracy (r = 0.35). Furthermore, baseline Full-Scale IQ scores were positively correlated with changes in Digit Span (r = 0.47), such that children with greater IQs had a greater improvement in their Digit Span score (Forward and Backward) over time.

Table 1. Description of Survivors of Pediatric Cancer Completing the Home-Based Cognitive Training Program

ParticipantAge

(years) Gender DiagnosisCranial Radiation

Treatment IQNumber of

Training SessionsNumber of

Training Hours

1 11.3 Male ALL No 91 53 13.82 13.3 Male ALL No 111 24 6.73 10.7 Male ALL No 114 18 8.14 12.7 Female PNET Yes 109 22 8.75 10.4 Female Ependymoma Yes 79 33 19.96 13.2 Female Medulloblastoma Yes 91 49 20.87 15.9 Male Medulloblastoma Yes 74 20 7.88 14.5 Male Ependymoma No 91 9 3.79 17.7 Female Medulloblastoma Yes 105 28 12.9

Abbreviations: ALL, acute lymphoblastic leukemia; PNET, primitive neuroectodermal tumor.

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Hardy et al. 31

Discussion

The current article describes the results of a pilot interven-tion study using a home-based, computerized cognitive training program known as Captain’s Log with a small sample of survivors of CNS-affecting cancer. Results indi-cate preliminary feasibility and efficacy for computerized cognitive training programs with survivors of pediatric cancer who evidence deficits in attention and working memory. These preliminary results are consistent with

findings from similar programs evaluated in children with ADHD (Klingberg et al., 2005). Such findings suggest that computerized cognitive training programs like Captain’s Log may provide a mechanism for improvement in cogni-tive skills, such as working memory and attention, in sur-vivors of pediatric cancer who are experiencing cognitive late effects.

Our positive findings must be discussed in light of sev-eral limitations beyond the small sample size. As this was a single-arm design, findings may be attributable to parent

Figure 1. Changes in indices of attention and working memory over the course of the intervention period

Table 2. Descriptive and Comparison Statistics for Outcome Data at Baseline, Postintervention, and 3-Month Follow-upa

Outcome Baseline Postintervention3-Month

Follow-upT (Baseline −

Postintervention) P

Working memory indexb 88.0 ± 12.49 93.6 ± 1.89 97.0 ± 15.06 −2.42 .03Digit Spanc 7.6 ± 0.30 8.9 ± 3.44 9.6 ± 3.16 −2.23 .04

Forwardd 7.3 ± 2.87 9.4 ± 2.92 9.9 ± 3.00 −3.23 .01Backwardd 8.7 ± 1.80 9.4 ± 3.13 9.6 ± 2.56 −0.44 NS

Letter-Number Sequencingc 8.4 ± 2.65 9.0 ± 2.55 9.3 ± 2.71 −0.86 NSCognitive problems/inattention indexe 68.8 ± 11.19 65.0 ± 12.77 59.5 ± 12.46 −2.15 .05

aNo significant differences were found between postintervention and 3-month follow-up scores.bStandard score (mean = 100, standard deviation [SD] = 15).cScale score (mean = 10, SD = 3).dRaw score.eT-score (mean = 50, SD = 10).

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32 Journal of Pediatric Oncology Nursing 28(1)

rating bias or to practice effects on the objective outcomes. However, analyses revealed that only parent perceptions of cognitive problems and inattention changed over the course of the intervention and not indices of anxiety, social problems, or oppositional behavior (data available on request). If changes had been observed in these other indi-ces of psychosocial functioning, then a stronger case would be made for reporting bias. In addition, observed WMI gains for our sample exceeded practice effects reported in the WISC-IV manual (Wechsler, 2003; ie, 2.6 points after a test-retest interval averaging 32 days). Finally, it should be noted that significant improvements were limited to measures of attention: parent report and Digit Span For-ward. Those measures that required the use of manipulation and higher-order working memory skills—Digit Span Back-ward and Letter-Number Sequencing—did not demonstrate large improvements over the course of the intervention. Such findings suggest that the Captain’s Log program may provide a better mechanism for training attention skills but not those required for working memory.

Findings from this pilot study suggest preliminary effi-cacy for computerized cognitive training programs with survivors of pediatric cancer who evidence deficits in atten-tion and working memory secondary to CNS-affecting treatment. Indeed, results indicate the need for implementa-tion of a larger trial, with a control group, and modifications based on the limitations and findings described above. Furthermore, a larger trial should likely add measures of processing speed, academic functioning, and imaging cor-relates to determine the effects of the intervention on other cognitive factors, academic skills, and brain functioning (including indices of white matter and functional imaging). Finally, it would be useful to examine associations between medical (eg, radiation dose, diagnosis), cognitive (eg, base-line IQ), and intervention (eg, “dose” effects) variables as moderators of any improvements in functioning over time.

Computerized cognitive training programs are a recently developed mechanism for targeting attention and working memory deficits and have been used extensively with other patient populations, including children diagnosed with ADHD and brain injury. The application of this technology to childhood cancer survivors represents a novel use of these tools and one that can be widely disseminated and incorporated into survivorship clinics.

Authors’ Note

Initial findings were presented at the National Conference on Child Health Psychology (April 2008, Miami, FL).

Declaration of Conflicting Interests

The author(s) declared no conflicts of interest with respect to the authorship and/or publication of this article.

Funding

This project was supported by a grant from the Duke Com-prehensive Cancer Center Development Funds to the first author.

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Bios

Kristina K. Hardy, PhD, is a psychologist in the Center for Neurosciences and Behavioral Medicine at Children’s National Medical Center and an assistant professor of psychiatry and behav-ioral sciences at George Washington University School of Medicine.

Victoria W. Willard, MA, is a doctoral candidate in the Depart-ment of Psychology and Neuroscience at Duke University.

Melanie J. Bonner, PhD, is an associate professor of psychiatry and behavioral science at Duke University Medical Center and of psychology and neuroscience at Duke University. She serves as the pediatric psychologist for the Preston Robert Tisch Brain Tumor Center at Duke.

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