In addition to behavioural problems, childhood ABI is associated with significant cognitive sequelae (Taylor et al. 2002; Yeates et al. 2002). Common cognitive consequences of childhood ABI include deficits in attention, memory, problem-solving, communication, decreased speed of information processing, and academic difficulties (Sohlberg 2001). Children with moderate to severe TBIs have worse communication skills then those with a mild TBI (Rivara et al. 2011). Children with lower communication scores at 3 months post-injury were found to have normal scores 9 months later. Those with more severe injuries continued to have difficulties at the 12 months (Rivara et al. 2011). Younger children benefit more from behaviour-based approaches to remediate communication skills whereas older adolescents benefit from reasoning strategies (Shaw 2016).
Cognitive therapies encompass a variety of interventions designed to help individuals with brain injury improve upon or compensate for cognitive deficits. There is a substantial body of research investigating the effectiveness of different rehabilitation techniques for improving or compensating cognitive deficits following brain injury in adults. However, research on the effectiveness of cognitive rehabilitation for the paediatric population is lacking. Compensatory assistance in academic settings can reduce the cognitive demands of reading and writing. Examples of compensatory assistance tools include audiobooks, text-to-speech and speech-to-text software, educational assistants, and proof-reading programs. Interdisciplinary support such as ophthalmology, audiology, sleep management and pain management services can help to address cognitive-communicative disorders (Krause et al. 2015).
REMEDIATION OF ATTENTIONAL DEFICITS
Evaluating the efficacy of remediation or rehabilitation of attention deficits following a brain injury is complicated by a number of factors. First, there is no consensus regarding a definition of attention. Some define it as a general construct whereas others suggest it may reflect more specific sub-components or systems of functioning (e.g. sustained, divided, focused, selective, vigilance, speed of information processing, etc). Second, interventions targeting remediation of attentional deficits have used the same or similar tests to measure different aspects of attention. Often throughout a study, the same outcome measures are used repeatedly, thereby confounding practice and treatment effects (e.g. PASAT performance increases significantly with repeated exposure to the test). Finally, studies may not consider and account for the rate of spontaneous recovery following brain injury (i.e., would participants naturally show recovery of function in the absence of treatment? (Welch-West et al. 2013).
Interventions to Remediate Attentional Deficits
There is currently a scarcity of interventions to target the remediation of attention in children that have sustained an ABI. As previously mentioned, attention is difficult to assess and is a multifaceted construct. However, attentional deficits in children can be detrimental to proper academic, social, and psychological function (Park et al. 2009). Therefore, it is imperative to determine effective interventions to target attentional deficits.
Four studies evaluated the effectiveness of the Amsterdam Memory and Training for children (AMAT-c) intervention (Catroppa et al. 2015; Hooft et al. 2005; van't Hooft et al. 2003; van 't Hooft et al. 2007). Three important aspects of cognitive function were evaluated in all four studies: sustained and selective attention and memory. Sustained attention was not improved for children in the AMAT-c group when compared to baseline (Catroppa et al. 2015) and to an interactive control group (Hooft et al. 2005; van 't Hooft et al. 2007). However, in a study with three participants, van’t Hooft et al. (2003) report that sustained attention improved in all participants following AMAT-c. The results for improvement in selective attention was conflicting. Three studies (2 RCTs and a case series) reported that selective attention improved in the AMAT-c intervention (Hooft et al. 2005; van't Hooft et al. 2003) and was maintained by 6 month follow-up (van 't Hooft et al. 2007). One pre-post study reported that selective attention was not improved following treatment (Catroppa et al. 2015). The third outcome measured by the AMAT-c, memory, was improved in all studies, with particular aspects of memory improving more than others.
Treble-Barna et al. (2016) used a computerized program to administer the attention intervention in adolescents in the chronic phase of TBI recovery. Children that received the intervention improved in sustained, but not selective attention compared to controls. However, there was no follow-up to determine the long-term effects of such intervention on attention. Another intervention used attention and neurological training within adolescents an average of 7-9 months post-injury (Galbiati et al. 2009). Adolescents in the intervention improved significantly in cognitive performance, attention skills, and adaptive behavioural skills. Authors conclude that improvements in attention positively influenced everyday adaptive behaviours (Galbiati et al. 2009).
There is Level 1b evidence that a memory and training program improves selective, but not sustained attention, and memory in children following an ABI.
There is Level 2 evidence that computerized attention skills training programs improve sustained, but not selective, attention compared to healthy controls.
There is Level 2 evidence that specific remediation programs for attention improve attention performance.
Cognitive rehabilitation programs are beneficial for the improvement of attention and memory for children following brain injury.
Methylphenidate to Remediate Attentional Deficits
Pharmacotherapy is another viable treatment option for children with attention deficits post-ABI. Methylphenidate, a psychomotor stimulant, is often used in the treatment of attention deficit/hyperactivity disorder (ADHD) in children; however, it is also used with children who have sustained a brain injury. It is believed that those with ADHD and those who have sustained a brain injury have similar characteristics including: attention deficits, hyperactivity and impulsivity (Leonard et al., 2004). 4-methylphenidate has been shown to improve memory and attention in those with ADHD (Kempton et al. 1999).
The effect of methylphenidate for children post-TBI is conflicting; one RCT found improvement in all measures of cognition and attention (Mahalick et al. 1998), whereas another RCT found no improvements in behaviour, memory, speed of processing, or attention following methylphenidate treatment (Williams et al. 1998). Both RCTs utilized a placebo comparison group with a cross-over design. Methodological differences may have contributed to the conflicting findings. Mahalick et al. (1998) administered methylphenidate for all children at a dosage of 0.3mg/kg, whereas Williams et al. (1998) administered a standard dose based on body weight category (i.e., <20kg, 21-29kg, >30kg). Mahalick et al. (1998) administered methylphenidate for 2 weeks, whereas Williams et al. (1998) treated for only 4 days, with a 3 day washout period between weeks. Further, Williams et al. (1998) included children that varied greatly in time post injury. Six subjects were within the first two years post injury when rapid change is more likely and four were more than two years post injury. Given the difficulties in determining the extent of injury (mild versus severe), the differences in the length of time since injury, and the small sample size, the results of this study should be interpreted with caution (Williams et al. 1998).
The findings of Hornyak et al., (1997), suggest that the introduction of methylphenidate (unreported dosing) resulted in improved cognitive and behavioural function in children post TBI. These improvements were associated with increased participation in therapy at school and improvements in behaviours at home (Hornyak et al. 1997). Finally, Nikles et al. (2014) found that stimulants (methylphenidate or dexamphetamine) had a small effect on improvement of ADHD symptoms, such as attention and concentration. Although reported as an improvement, the difference compared to the placebo phase was not statistically significant (Nikles et al. 2014). Additionally, only children with ADHD-like behaviours were analyzed, which is a subset of the overall TBI population, limiting generalizability. Future RCTs are needed to determine the effectiveness of amantadine on attention for pediatric TBI.
There is conflicting evidence that methylphenidate interventions improved cognitive behavioural function compared to placebo, in children following a TBI.
Evidence regarding the efficacy of methylphenidate to improve cognitive and behavioural function following a pediatric TBI is conflicting.
REMEDIATION OF Learning Memory
Memory impairment is one of the most debilitating symptoms following brain injury and it is estimated that time and cost of care would be reduced if effective medical treatments were found to improve memory (Hooft et al. 2005; McLean et al. 1991).
When evaluating intervention strategies to improve memory performance following brain injury, the literature indicates that there are two main approaches to rehabilitation: restoration or retraining of the function and compensation. Compensation includes “training strategies or techniques that aim to circumvent any difficulty that arises as a result of the memory impairment.” Compensatory techniques include internal aids, which are “mnemonic strategies that restructure information that is to be learned” (McLean et al. 1991). Individuals with lower working memory capacity post-TBI are at a greater risk of encountering academic difficulties (Krause et al. 2015). Various interventions are designed to address this concern and support the literacy skills of adolescents with TBI. Reading interventions, such as flashcards and repeated oral readings, can improve word recognition. Metacognitive strategies such as note-taking, focusing attention on new information, building referential relationships across texts, and ensuring that performance and goal attainment are monitored may be associated with improvements in academic ability (Krause et al. 2015).
Several different interventions to remediate memory and learning post-TBI have been evaluated. Memory aids are one intervention tool that may be used to improve memory deficits in children post-TBI. Wilson et al. (2009) used a pager as a memory aid to help children remember and attain their everyday tasks more efficiently. All participants improved in their percent of targeted behaviours achieved throughout the day when using the pager. Although not as significant as with the pager, participants were able to maintain their improvement in memory when the pager was removed (Wilson et al. 2009). Another memory aid that has been tested is the use of a diary, along with self-instructional training that focused on developing self-regulation and self-awareness skills (Ho et al. 2011). Children improved in their daily memory deficits post-intervention; however, unlike the pager system, the improvements were not maintained at follow-up. The number of diary entries was significantly correlated to improvement in memory deficits. Ho et al. (2011) report that memory impairments are associated with internalizing behaviours and speed and attention to information processing.
In a different approach, Melchers et al. (1999) used sensory stimulation while children were in a coma and cognitive neuropsychological rehabilitation upon awakening to remediate learning deficits post-TBI. Although only reporting preliminary results, the authors report that children had greater improvements in intellectual development, approaching age appropriate levels, one year post-injury compared to controls who further declined from pre-treatment levels. However, due to lack of equal distribution of injury severity between groups, the results should be cautioned for generalizability (Melchers et al. 1999).
In a case series completed by Brett and Laatsch (1998), 10 school aged children were offered biweekly session of cognitive rehabilitation for 20 weeks. Pre- and post-testing revealed a modest improvement in memory skills only. This was attributed to engagement in a variety of verbal memory strategies (repetition, clustering, and semantic processing). In the one case study included in this section, improvement was also reported for selective attention, memory and academic performance (Glang et al. 1992).
There is Level 2 evidence supporting using a pager system to improve memory and planning activities in adolescents with a TBI.
There is Level 4 evidence that rehabilitation focused around diary entries and self-instructional training improves memory deficits in children post-TBI.
There is Level 2 evidence that sensory stimulation paired with cognitive neuropsychological rehabilitation improves intellectual development in children with severe TBI.
There is Level 2 evidence that intellectual function is significantly increased with cognitive rehabilitation.
Cognitive rehabilitation can improve intellectual function for children following brain injury.
Memory aids may be effective at reducing memory deficits after an ABI.
Remediation of executive functioning
Executive functions refer to higher-level cognitive functions that are primarily mediated by the frontal lobes. These functions include insight, awareness, judgment, planning, organization, problem solving, multi-tasking and working memory (Lezak 1983). Executive deficits are particularly relevant following traumatic brain injury from both a pathophysiologic as well as a psychosocial perspective. The frontal lobes tend to be one of the brain areas most likely to be injured following trauma (Greenwald et al. 2003). Frequently, bilateral frontal lobe injury occurs following TBI in contrast to typical unilateral insults following vascular injury. Not only direct contusion to the frontal and temporal lobes but also diffuse axonal injury sustained as a result of TBI affect executive functioning. Patients with a TBI often present with cognitive and behavioral deficits in the presence of little physical impairment.
Adolescents that underwent a counsellor assisted problem solving programs (CAPS) were compared to a control group given standard internet resources. Older adolescents (≥14yrs) had significant improvement in executive function, specifically behavioural regulation and metacognition compared to controls (Kurowski et al. 2013). Adolescents in grade 9-12 improved the most in executive function after the intervention according to primary care giver’s raters 12 months post-injury. Upon further analyses, Kurowski et al. (2014) found that older adolescents maintain improvement in executive functioning at 18 months post-intervention. Younger adolescents did not significantly improve in care-giver’s ratings of executive function relative to the controls, even as they aged over the 18 month follow-up. Older adolescents may be more capable of using the training program than younger, and age of intervention may be important (Kurowski et al. 2013). Two other moderating variables were reported. Adolescents that sustained a severe, but not moderate, TBI had greater improvements in executive functioning post-intervention than the control group (Wade et al. 2010). Adolescents with poor vocabulary improved in metacognitive abilities when in the CAPS group compared to the control group (Karver et al. 2014). Linden et al. (2016) conducted a meta-analysis that confirmed that the CAPS intervention was beneficial in remediating executive functioning but only a small-medium effect size was found. A clinically important effect on the patients was deemed to be unlikely.
Other interventions have been developed to target development of metacognitive strategies for children post-TBI. In one intervention, children were paired with psychology students and given the opportunity to use their metacognitive strategies and cooperative learning in daily activities and games (Braga et al. 2012). Post-treatment, children decreased of use of ineffective metacognitive behaviours and increased in beneficial ones such as planning, regulating, and monitoring behaviours (Braga et al. 2012). Treble-Barna et al. (2016) had similar goals, but used a computerized program to deliver metacognitive instruction and attention tasks. Parent ratings of executive functioning improved significantly, suggesting that children improve in everyday executive functioning tasks, metacognitive skills, and regulation of behaviours after metacognitive training. Krasny-Pacini et al. (2014) used a goal management intervention with metacognitive strategies and coaching guides. By the end of the study, all children decreased in cognitive executive impairments for assigned tasks and parental ratings of executive function overall improved (Krasny-Pacini et al. 2014). However, when a new task was introduced 6 months post-intervention, the children fell back to pre-treatment levels of performance, suggesting a lack of generalizability.
Catroppa et al. (2009) developed a pilot intervention program with three participants, requiring children to attend instructional sessions on cognitive behavioural and psychosocial skill developments post-TBI. Preliminary results indicate that cognitive inflexibility was significantly improved in 2 participants; however, all other measures were non-significant or only one participant had a significant effect (Catroppa et al. 2009). An increase in participants is needed before conclusions can be drawn. Furthermore, Cook et al. (2014) used a “SMART” program for adolescents post-TBI. The SMART program focused on top-down executive function training whereas the control memory group focused on bottom-up processing. The SMART program was more effective to remediate deficits in high order cognition compared to the memory group. Specifically, adolescents in their chronic phase of recovery were able to abstract meaning from complex information. This improvement in top-down processing may in turn influence bottom-up processing, such as recall ability (Cook et al. 2014).
A few studies have targeted problem solving in order to improve executive functioning in children post-ABI. Chan and Fong (2011) examined a problem solving intervention that emphasized metacognition to improve executive function compared to usual care. Children with an ABI in the chronic recovery phase performed better in regards to abstract reasoning, metacomponential function, and perceived themselves as having better performance in everyday tasks. Importantly, the problem solving intervention was targeted to relate to everyday skills and situations, thereby increasing generalizability and potential usefulness of the increased behaviours (Chan & Fong 2011). In a case series 5 children, under the age of 12, participated in a computer based training program to decrease undesirable behaviours, and improve positive cognitive behavioural outcomes. Results indicated that participants improved in their overall ability to problem solve (Suzman et al. 1997). Similarly, Missuina et al. (2012) used an individualized treatment program (CO-OP) to teach children cognitive strategies and problem solving skills that are necessary for successful occupational performance. Children overall improved in functional performance, with increased ability to perform their own identified goals. This improvement was maintained at 4 month follow-up. Authors suggest that perhaps adaptation to the CO-OP program may be necessary to further enhance effects.
There is Level 1a evidence supporting the use of online counsellor assisted problem solving programs to improve executive function in adolescents who have sustained a TBI.
There is Level 1b evidence that the SMART program improves higher-order cognitive deficits compared to a control group with bottom-up processing training.
There is Level 1b evidence that metacognitive therapy improves learning strategies and executive function in children and adolescents with an ABI.
There is Level 4 evidence from one study supporting the use of goal management therapy to improve parental ratings of executive function in young children who have sustained a TBI.
There is Level 2 evidence that problem solving interventions improve executive function and metacognitive abilities in children post-ABI.
Counsellor assisted problem solving programs are effective at improving executive function in adolescents.
The SMART intervention improves high-order cognitive function in adolescents post-ABI.
Goal management therapy is effective to reduce parental ratings of their child’s executive function.
Metacognitive treatment programs for pre-adolescents that are assisted by therapists improve executive function and increase the use of metacognitive learning strategies.
Interventions that target problem solving are effective to improve executive function and metacognitive abilities.
Communication Deficits Post ABI
Communication has been described as the “heart of learning, living adequately in society and developing one’s unique personality” (DePompei & Hotz 2001). A TBI often results in several long-term consequences and one of these is the inability to communicate adequately (Savage et al. 2005). During childhood, language and communication skills are continuously maturing and when brain injuries occur, there may be an abnormal development delay in the emergence of skills, or a detriment to mastery levels (Didus et al. 1999). It is known that pragmatic language skills are developing until at least the age of 12 years. When these skills are impaired and proper development does not occur, it affects the child’s ability to effectively interact with peers, thus affecting social processes as well as disenabling effective communication (Didus et al. 1999; Savage et al. 2005).
Several aspects of communication have been described; among them, is the use of listening, speaking, reading, writing and gesturing to understand an idea or to express thoughts. Speech is the production of sounds that make up words and sentences; however, language implies the use of words or ideas to convey thoughts. Finally, cognitive-communication is use of language and underlying processes (attention, problem solving etc.) to communicate effectively. Children often return to their pre-injury language abilities, however there are 3 types of language abilities (receptive, expressive and pragmatic) that can be affected by a TBI (Savage et al. 2005). An injury to the brain can interfere with any one (or all) of these aspects (DePompei & Hotz 2001). Several interventions have been explored for individuals that have sustained a brain injury. The most common approach is therapy targeting accommodations, but other therapies include targeting remediation and metacognitive strategies (Turkstra et al. 2015).
Three different interventions examined the effects of language therapy for children following an ABI. The first intervention used a recording of spontaneous speech between child and examiner to determine the percent of consonants that were correct within the speech (Campbell et al. 2013). The odds of entering in the normal range for consonant production by 12 months was significantly greater for children that sustained their injury after the age of five. Such evidence adds to the literature that traumatic brain injuries severely affect language skills that have not fully consolidated by the time injury occurs (Campbell et al. 2013).
The second intervention evaluated the effectiveness of treating three teenagers with electropalatography (Morgan et al. 2007). Electropalatography (EPG) “is an instrumental treatment technique allowing visual feedback of tongue to palate movement during real time articulation”. All participants had improvement in the perceptual measure for articulation and speech intelligibility. EPG treatment may be an effective rehabilitative tool to improve speech at the level of phenomes, word, or sentence articulation (Morgan et al. 2007).
The third intervention examined the effectiveness of a peer-group training program aimed at improving pragmatic skills in adolescents with brain injury (Wiseman-Hakes et al. 1998). Following the intervention, adolescents improved in both pragmatic language behaviours (i.e., intelligibility of speech, syntax, topic, etc.) and the range of pragmatic communication abilities (i.e., conversational skills, emphasis of meaning, use of context to convey message, etc.). Despite the number of studies that have been conducted looking at the frequency and complexity of communication problems that develop post ABI in children, to date there remains little discussion on the treatments used to overcome these problems.
There is Level 5 evidence that children that sustain a brain injury after 5 years of age are more likely to return to normal consonant production, compared to children who sustain an injury prior to language skill consolidation.
There is Level 4 evidence indicating the EPG treatment is effective treating the articulatory component of dysarthria post TBI in children.
There is Level 4 evidence that peer-group training of pragmatic language skills may benefit children with communication deficits following brain injury.
Pragmatic skills training may help to improve communication following brain injury.
Injury-Related Information Intervention
Children may have difficulties in understanding the extent of their brain injury. This can lead to lack of awareness of any injury-related deficits, which could result in increased anxiety or poor self-esteem. Since the parents are one of the major sources of information for children, a child understanding their injuries likely depends upon their parents’ level of understanding and knowledge about ABI. Thus, providing injury-related information to pediatric brain injury victims and their families should improve their awareness of injury-related deficits, which could indirectly improve cognitive processes.
A single RCT evaluated the effects of injury-related information interventions (Beardmore 1999). Although the intervention was not effective in improving the children’s knowledge or awareness of their deficits, self-esteem or cognitive measures, it did significantly reduce the stress experienced by their parents. Additional studies using larger sample sizes should be conducted to elucidate the effects of injury-related information interventions upon children and their families.
Based on the findings of a single RCT, there is Level 2 evidence that injury-related information interventions do not improve knowledge or awareness of injury-related deficits, memory function or behavioral problems in children.
Injury-related information provided to participants and parents has not been yet shown to have an effect upon knowledge and awareness of injury-related deficits, memory or behavioral problems in children.
Summary of Remediation of Cognitive Impairments
The present review examined several articles investigating the effectiveness of cognitive interventions in children with ABI. General limitations within the cognitive therapy literature are similar to those in the behavioural therapy literature. These include a small number of studies, a small number of children evaluated, and few studies of preschool children. Overall, it is difficult to determine the effectiveness of cognitive therapies in children with ABI. The small number of studies and small numbers of individuals therein limit the extent to which conclusions can be made at this time. As in the behavioural therapies research, the findings appear promising, although empirical support in general is limited. Further, small case studies may prove to be the most useful approach to research in this area, which require a longer time than cohort studies to compile sufficient data to make stronger conclusions. Again, while smaller case studies may prove to be a useful approach for study in this area, there is a clear need for maximizing the scientific rigour of such studies, for example by studying a larger number of individuals within one study, and through the inclusion of control comparisons.
Unlike adults, brain injuries in children occur within a context of significant cognitive development. Thus in children, a brain injury may affect the onset of a skill (i.e., skill acquisition may be delayed), the order of emergence of a skill, the rate of skill development, and/or the degree of development of a skill. While such developmental factors should be considered in any cognitive treatment plan, equating these factors across subjects or groups in a research design is problematic.
Children who sustain a brain injury often develop at a slower rate than age matched peers, therefore there may be an increased age gap between the individual who has sustained the injury (Babikian & Asarnow 2009; Fay et al. 2009). This concept of “Growing Gap” is difficult to measure and analyze. It highlights the need for long term follow up into the adult years. Unfortunately none of the studies presently reviewed addressed cognitive developmental issues in their sample.
A problem that is particularly salient to this area of research is the notion of generalizability. That is, to what extent are gains made following a cognitive training program merely a reflection of improvements in performing a particular test-related task, rather than gains in more general cognitive function such as attention or memory? One way to address this is to study how cognitive rehabilitation skills generalize to the classroom setting following therapy. Although one study presently reviewed involved a school-based intervention (Brett & Laatsch 1998), generalization of skills to the classroom was not evaluated. Some studies have reported anecdotal evidence of generalized improvements (Catroppa et al. 2009; Glang et al. 1992; Suzman et al. 1997). On a related matter, in the studies conducted thus far, it is unclear to what extent gains made in therapy are maintained over time.
An important difference between adults and children with respect to brain injury is the rehabilitation context. While interventions with adults may focus primarily on the workplace, the primary context for rehabilitation with children who have sustained brain injuries is school. Only one study presently reviewed involved school-based interventions (Brett & Laatsch 1998). It is thus important for future research in this area to implicate the school context.