DEVELOPMENTAL MEDICINE & CHILD NEUROLOGY

INVITED REVIEW

Cognitive–communication disorders in children with traumatic brain injury LYN S TURKSTRA 1

| ADAM M POLITIS 1 | ROB FORSYTH 2

1 Department of Communication Sciences and Disorders, University of Wisconsin-Madison, Madison, WI, USA. 2 Institute of Neuroscience, Newcastle University, Newcastle, UK. Correspondence to Lyn S Turkstra at Department of Communication Sciences and Disorders, University of Wisconsin-Madison, Willow Drive, Madison, WI 53562, USA. E-mail: [email protected]

PUBLICATION DATA

Accepted for publication 10th August 2014. Published online ABBREVIATION

TBI

Traumatic brain injury

Children with moderate to severe traumatic brain injury (TBI) are at risk of developing cognitive–communication disorders that have devastating effects on their school life, family life, and social life. These problems can be difficult for families to describe and may be overlooked by community-based providers who are unfamiliar with TBI sequelae. To support the identification and management of cognitive–communication disorders, we review the common signs and symptoms of these disorders in children with TBI and discuss principles of assessment and intervention.

Traumatic brain injury (TBI) is common among children and adolescents.1 Current incidence and prevalence statistics are thought to underestimate the true incidence of TBI in these age groups, as most injuries are mild and many are not reported.1 Emerging international standards for evaluation and management of mild TBI2 and growing awareness of potential long-term morbidity after mild TBI3 mean that it is likely that the accuracy of incidence and prevalence estimates will be improved in the coming years. After discharge from hospital, it is likely that children with TBI will be cared for by community-based care providers who have little specialized knowledge of TBI and its sequelae. Thus, children and adolescents with TBI may lack a long-term ‘medical home’4 because they lack a physician or other care providers who understand the implications of TBI as a chronic disease. Community-based care providers play a critical role in this long-term stage not only by managing chronic postinjury health, social, and educational problems, but also as a source of referral to appropriate therapies and other services. The aim of this paper is to provide a resource for community care providers in both of these roles. In this paper, we review one aspect of outcome from paediatric TBI: long-term impairments in what is referred to as cognitive–communication ability.5 While language disorders such as aphasia can result from paediatric TBI, the more common clinical finding is a communication disorder due to underlying impairments in cognitive functions, such as attention, working memory, declarative learning, executive functions, and social cognition.6,7 Cognitive impairments can affect any communication modality (listening, speaking, gesturing, reading, or writing); and any language domain (phonology, morphology, syntax, semantics, or pragmatics).5 © 2014 Mac Keith Press

We chose to focus on cognitive–communication disorders in this paper because they can be less obvious than gross sensory or motor impairments, and thus might be missed in a clinical examination. It can also be difficult for families to describe signs of a cognitive–communication disorder clearly to a care provider. Communication impairments in general are a major source of stress and burden for families,8 and may affect long-term outcomes in school life7 and social life.9 Thus, it is important to recognize cognitive–communication challenges in children and adolescents with TBI and refer them for appropriate services. This paper relates primarily to children with moderate or severe injuries, that is children who had a loss of consciousness for at least 30 minutes or a brief loss of consciousness with evidence of an intracranial lesion. We begin with an overview of the common cognitive impairments associated with childhood TBI as a foundation for discussing the communication problems that arise from these impairments. We then summarize known communication problems and offer suggestions for evaluation and referral.

COMMON COGNITIVE IMPAIRMENTS AFTER PAEDIATRIC TBI Paediatric TBI is associated with impairments in attention (sustaining, shifting, and dividing attention);10 speed of thinking;11 verbal and visuospatial working memory,12 particularly in dual-task conditions (e.g. asking the child to simultaneously recall words and categorize them);13 declarative learning;14 and executive functions (e.g. control of thoughts, feelings, and behaviour; abstract thinking).15 Although declarative learning (i.e. explicit learning) is impaired, learning of new procedures and habits (i.e. implicit learning) is thought to be intact.16 TBI, likewise, may DOI: 10.1111/dmcn.12600 1

have little effect on previously learned knowledge and skills,16 although impairments in executive functions and attention may limit the child’s ability to access previously learned information quickly and effectively. A relatively new finding in the literature is that children with TBI may be impaired in social cognition, specifically in recognizing emotions and mentalization (i.e. Theory of Mind). Several studies have shown deficits in children with moderate–severe injury on social cognition tasks requiring emotion recognition from facial affect17,18 and inferences about feelings and intents of others.19 Children with TBI also may show impaired social problem-solving,20 which might reflect a combination of executive function and social cognition impairments. The results of several recent long-term outcome studies21–23 provide strong evidence that cognitive effects persist into adulthood, particularly in children with severe TBI. Cognitive impairments may look different at different developmental stages, depending on the cognitive processes maturing at each stage and cognitive demands at that stage. For example, executive functions continue to mature well into the third decade of life and impairments may become noticeable only as demands increase over time. In one study,24 in the first few days after injury, children with TBI exhibited impairments in control of attention, which is a simple executive function, whereas 10 years after their injury they showed impairments of metacognition, a complex executive function. Late effects of learning problems also may be seen. A common finding is that IQ raw scores decline after injury, at least in the first few years.25,26 The decline in scores does not always indicate a decline in IQ, but rather may reflect a lag in development compared with age expectations, as learning and executive function impairments affect the rate at which new knowledge is acquired. Children with TBI may be slower to develop aspects of language that depend on declarative memory and executive functions, such as receptive and expressive vocabulary,7 and also may show qualitatively different patterns of skills. For example, because of underlying cognitive impairments, a child might know literal meanings but not abstract meanings,27 or may be unable to generalize learning from one context to another.28 Thus, standardized test scores may overestimate the child’s ability to use language flexibly in everyday school life, home life, and social life.29 Although preinjury cognitive problems play a role in postinjury outcomes, they account for only a portion of postinjury impairments.30,31 It is important to recognize this, as there might be a tendency to dismiss some postinjury signs and symptoms as exaggerations of preinjury problems, particularly when TBI effects are not evident until cognitive demands increase several years after injury. Executive function impairments, in particular, might not be evident until demands for self-control and abstract thinking increase in late childhood and adolescence. This poses a challenge in diagnosis, as parents might not automatically link the new problems to a past injury and thus might not think to mention to health care providers the 2 Developmental Medicine & Child Neurology 2014

• • •

What this paper adds This review summarizes the cognitive and communication impairments associated with paediatric traumatic brain injury (TBI). It also describes general principles of intervention for cognitive–communication disorders after paediatric TBI. The limitations of typical clinical assessment methods are presented and improvements to the referral and management of children with TBI are suggested.

injury sustained at an earlier age. TBI-related cognitive impairments in the chronic stage also can resemble cognitive limitations seen in children with developmental disabilities. The distinction between acquired and developmental disorders is important for intervention, as strategies that are effective for children who are impaired in using an existing knowledge base or skills differ from effective strategies for children who never had that knowledge or skills. For example, social communication may be a problem for children with autism, language learning disabilities, or TBI, but differences in life experiences of these children may necessitate different management approaches (e.g. learning about others’ perspectives vs catching up with peers vs coping with a changed skill set).32

COMMON COGNITIVE-COMMUNICATION IMPAIRMENTS AFTER PAEDIATRIC TBI Impairments in language comprehension The effects of TBI on language comprehension depend on the age at which the child is injured and type of language to be understood. Children who are injured in early childhood when reading skills are developing are at risk of impairments in basic language decoding abilities, which are compounded by slow information processing speed.6 Young children with TBI-related learning problems also are at significant risk of delays in acquisition of vocabulary, which may contribute to impairments in reading and auditory comprehension.33 The finding that injury at an earlier age results in poorer outcomes has been replicated across several language-related cognitive domains (e.g. Ewing-Cobbs et al.25), and runs counter to the common perception that younger age predicts better cognitive recovery.34,35 Children with moderate–severe TBI are at high risk of impairments in both spoken and written language comprehension. The types of language commonly affected include (1) non-literal language that requires inference, including text with missing or ambiguous elements (e.g. understanding that the missing link between ‘the student studied hard’ and ‘the student was disappointed in his grade’ is that the student failed the test),36 statements of truth versus deception,37 written or spoken sarcasm38 or humour,39 and figurative language such as metaphors and idioms;40 and (2) language in complex forms (e.g. with embedded clauses) or that is presented in a way that taxes the child’s working memory (e.g. too slowly or in too large a quantity for a child to hold all the information in working memory, or too quickly for the child to process).41 As the preceding examples show, TBI-related comprehension impairments are likely to reflect underlying

problems in working memory, processing speed, social cognition, and executive functions. For example, if a parent looks around a child’s room and says, ‘If something around here doesn’t change, I’m calling the health inspector’, the child must be able to hold the initial clause in mind while comprehending the main clause in the sentence (working memory), recognize his mother’s tone of voice as showing exasperation (social cognition), shift perspectives to consider the room as his mother sees it (executive functions), make the inference that the comment is related to a messy room (executive functions and social cognition), and recognize that his mother’s intent is for him to clean his room (social cognition). All of this must be achieved in milliseconds (speed of processing), and in the presence of potentially competing internal and external stimuli (selective attention and resistance to distraction). The role of cognitive impairments in language comprehension is supported by evidence that when cognitive load is controlled (e.g. by adapting test items to reduce working memory), auditory comprehension may be within age expectations.41

Impairments in language production Children with moderate to severe TBI may have impairments in conveying word meaning (semantics), such as reduced expressive vocabulary,33 and reduced verbal fluency42 and sentence formulation43 compared with peers. Children with TBI also may produce shorter and more incomplete utterances than peers.44 By contrast, phonology (speech sounds), morphology (word forms that convey meaning), and grammar appear to be intact after TBI. Differences among language functions are likely to reflect how these functions are learned and used. For example, phonology and morphology are acquired implicitly, and implicit memory and learning do not appear to be affected by paediatric TBI.16 Grammar, similarly, is thought to be acquired through implicit learning and is likely to be intact after TBI, except perhaps when a child is attempting to produce long and complex utterances that tax working memory. The most commonly reported communication problems for children with TBI are in using language in context, an aspect of communication that is referred to as pragmatics.45 Pragmatic language often is evaluated using discourse tasks such as telling or re-telling a story, and on these tasks children with TBI may produce less information than peers,22 fail to organize information in a logical sequence,44 and take turns at odd or inappropriate times.44 Another aspect of pragmatics in which children with TBI may show impairments is using language to achieve specific goals, such as giving hints, negotiating, or conveying humour or sarcasm.38 As with basic language skills, aspects of pragmatic communication that are more automatic appear to be less impaired, including basic social greetings and non-verbal communication such as turning towards the listener when talking.46 A study by Chapman et al.47 illustrates the discourse problems that may be associated with TBI. In this study, children with severe TBI and uninjured age-peers were

asked to summarize a story and identify the main theme and lesson. The experimenters first defined a summary and lesson using two stories familiar to the children (The Lion King and Beauty and the Beast). Children were then asked to listen to a novel story and give a summary of the story, with only the main points, and state a lesson that could be learned from the story. Children in both groups could reduce stories to fewer words and identify a lesson, but there were significant differences in quality of their responses. Children with TBI were less likely to transform statements from the story into gist summaries than their peers, and more likely to restate facts from the story without abstracting meaning. Children with TBI also were more likely that their peers to produce lessons that were literal statements from the story rather than general principles (e.g. ‘Don’t steal anyone’s money’ vs ‘Money can’t make you happy’). Children injured before age 8 years, when summarization abilities develop, were more severely impaired on the task than were children who sustained a TBI at age 11 to 14 years. As with problems in language comprehension, problems in language production reflect underlying impairments in cognitive processes that support language, particularly executive functions and working memory.45 In the above example from Chapman et al.,47 summarization abilities were significantly correlated with working memory test scores but not with tests of simple verbal recall, suggesting that discourse limitations reflect impairments in the ability to use information rather than simple forgetting. Social cognition also may play a role. In one study,48 adolescents with TBI who performed poorly on a test of social cognition also used fewer ‘social thinking’ words in conversation than adolescents with TBI who had age-typical scores on the social cognition test. Vocabulary and utterance length were similar in these two groups, again supporting the notion that discourse deficits reflect more than impairments in basic language skills.

IMPLICATIONS FOR PRACTICE Recognizing a communication problem Common communication problems in children with TBI are summarized in Table I. Although cognitive and communication problems that arise after childhood TBI are well described in the literature, recognition of these problems in clinical settings remains a challenge. As noted earlier, the cognitive and communication effects of TBI evolve over time as the child matures, which can make it difficult to connect current difficulties to a past brain injury event. The situation can be compounded if, for example, a child has changed school since the injury and a full account of the injury and its possible future consequences have not been conveyed to the new school staff. Recognition is further complicated by ‘professional turnover’ around a young person, particularly in high school, where a teacher will typically have contact with a young person for only a year or two at most, complicating recognition of slowly evolving pictures. Invited Review

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Table I: Communication problems seen after moderate-severe traumatic brain injury in children and adolescents. Adapted from Savage et al.57 Aspect of communication Language comprehension

Language production

Pragmatic communication

Communication problems Poor comprehension of vocabulary Difficulty remembering instructions or following directions Difficulty sequencing or following multiple directions Difficulty with the rate, complexity, or amount of spoken or written information presented at one time Inability to keep up with complex sentences or vocabulary Requires additional time to understand what others are saying Requests multiple repeats of information Slow reading rate Problems understanding or recalling what was read May not understand puns, sarcasm, or humour and may take what is said literally Difficulty identifying the gist of stories and/or important story elements Problems in developing and using new vocabulary Difficulty remembering the desired word when speaking or writing Uses ‘thing’ or ‘you know’ rather than the noun or verb Problems organizing thoughts to say what is on his or her mind Slower to respond to written or verbal directions or questions Unable to form response to a question in usual time allotted for students to respond, even though he or she might know the correct response or behaviour Poor spelling Difficulty writing sentences Takes turns at inappropriate times or monopolizes the conversation Talks about unrelated topics Interrupts with irrelevant ideas Unable to monitor quality of his or her own conversation Continues talking when others indicate they are uninterested Engages in lengthy, disorganized explanations Rambling conversation or written expression Minimal responses to questions with an inability to fill in details or offer other supporting information Difficulty using language to achieve specific goals, such as giving hints, negotiating, or conveying humour or sarcasm

Even if the care provider has considered the possibility that manifest difficulties relate to a previous brain injury, asking the wrong questions in a cognitive assessment or using the wrong instruments may give a misleadingly positive impression. Standard educational attainment tests are ill-suited to the task of identifying the specific deficits in executive functions and social cognition discussed in this paper. The same is true for standardized language tests. Assessments tend to emphasize old learning (e.g. literacy and numeracy skills that were acquired preinjury), and occur in highly structured one-on-one settings that 4 Developmental Medicine & Child Neurology 2014

minimize risk of distraction. Particularly in less severe injuries, professionals’ views of the relative contribution of the injury versus premorbid socio-economic disadvantage (which conveys an increased injury risk) may differ. An important response to the challenges just described is to empower families to seek appropriate assessment if they recognize problems emerging. Online sources, such as the Center on Brain Injury Research and Training (http:// cbirt.org), have excellent resources for health care providers, including lists of communication signs and symptoms often associated with TBI and indicators for referral. There is a need for validated screening instruments that physicians and other care providers can use to help identify communication problems that merit referral. In the meantime, care providers are left to screen communication informally, based on developmental expectations.

Assessment of cognitive–communication disorders A physician should exclude any medical causes for cognitive and communication problems, considering the unlikely possibility of causes such as unrecognized seizure activity. Other medical problems such as pain, fatigue, and changes in mood can affect communication performance, and may respond to pharmacological remedies. The key to further management is a detailed evaluation of communication ability by a qualified speech–language pathologist or speech therapist who is experienced in the assessment of the issues discussed in this paper. As communication problems reflect underlying cognitive impairments, it also is important to have a neuropsychological assessment carried out by an appropriately qualified professional. The results of these evaluations will include implications for teaching styles and recommendations for additional educational support, as well as guidance for families in effective communication with the child. When evaluating a child with TBI, it is important to recognize that injury severity accounts for relatively little of the variance in long-term communication skills.7 Significant predictors of language outcomes may include socioeconomic status, preinjury language skills, and age at injury, with injuries sustained at a younger age being associated with poorer outcomes.21 Thus, assessment should consider these factors as well. Intervention In general terms, there are three approaches to intervention for cognitive–communication disorders in children and adolescents with TBI: (1) direct remediation of communication deficits; (2) metacognitive strategy instruction, for example teaching children to think about their cognition and language and use strategies to communicate effectively; and (3) accommodation. Evidence supporting direct remediation of communication deficits is limited (see Slomine and Locascio49 and Laatsch et al.50 for reviews). There is support for general intervention principles, such as providing positive everyday supports for communication,51 engaging families,52 collaborating with schools,53 and teaching new vocabulary.28 There is, however, a lack of evidence that

direct training of specific communication functions (e.g. verbal fluency or auditory comprehension) leads to generalizable improvements.49 Metacognitive strategy instruction may be helpful for older children and adolescents, to help them understand their own cognitive strength and limitations, identify the sorts of communication situations they may find challenging and why, and use compensatory strategies that will help them communicate effectively.54 In practice, accommodation may be the most common type of intervention for children with communication problems due to TBI. The main goal of accommodation is to provide an environment where the young person’s strengths and difficulties are understood and mitigated.55 Many children who have survived TBI will have a clear memory of how things were premorbidly and be acutely aware that it used to be easier for them to think and communicate. If a collapse of self-esteem is not to further complicate matters, the importance of the classroom as a ‘rehabilitation environment’ must be harnessed. Classroom strategies that play to the child’s strengths and avoid setting them up to fail are well understood,56 and can be instituted once (1) the young person’s problems have been correctly attributed to the brain injury, (2) teachers have been given in-service training to understand a particular young person’s needs, and (3) appropriate resources are secured.

CONCLUSION Children with moderate to severe TBI are at risk of developing cognitive–communication problems that have

devastating effects on school life, family life, and social life. Cognitive–communication disorders are most often apparent on complex language tasks, including tasks requiring linguistic inference, rapid comprehension or production, and adjustment of language to fit a given social context. Cognitive–communication disorders also may be evident on connected language tasks, such as discourse, that place particular demands on executive functions and working memory. Cognitive–communication disorders can be difficult for families to describe and may be overlooked by community-based providers who are unfamiliar with TBI sequelae. As a result, children who need services may not always receive them. To improve referral and management of children with cognitive–communication disorders after TBI, we recommend that neurologists and other community health care providers (1) become familiar with the ways in which the effects of an injury interact with ongoing development to create evolving communication signs and symptoms; (2) understand the typical areas of weakness after TBI (e.g. new learning, executive functions, social cognition) and recognize that the effects of these impairments on communication may not be revealed by conventional language tests; (3) find out who can provide informed assessments where you work; and (4) be prepared to advocate for children with cognitive–communication disorders, particularly in educational settings where cognitive–communication disorders may be attributed to ‘poor attitude’, ‘lack of motivation’, or other incorrect causes.

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