Abstract
Individuals with TBI are vulnerable to a range of cognitive impairments that can interact with psychological comorbidities to lead to chronic challenges with social and occupational functioning in the community. Epilepsy is similarly associated with cognitive difficulties that can be further undermined by the medical, psychological, and psychosocial sequelae of the illness. Although there are limited empirical studies specifically examining cognition in PTE to date, emerging evidence suggests that the development of seizures after TBI may result in a “double hit” to cognitive functioning. This chapter outlines the cognitive sequelae of TBI and epilepsy, and presents a model of cognitive impairment in PTE. It reviews the scant literature on the cognitive consequences of PTE, highlighting current gaps in the literature. Finally, it describes an approach to cognitive rehabilitation in PTE, based on the well-established principles in TBI adapted to accommodate the unique challenges of PTE.
Introduction
In a small number of people, the shock and disability that stems from having incurred a traumatic brain injury (TBI) is compounded by the emergence of post-traumatic epilepsy (PTE). As detailed in earlier chapters of this book, PTE is defined as one or more unprovoked seizures that manifest at least a week after TBI.1 Risk factors encompass TBI-related features such as injury severity, intracerebral haemorrhage, penetrating injuries and early post-traumatic seizures, as well as factors related to the individual such as older age at the time of injury, a family history of epilepsy, genetic features like the ApoE-ε4 allele of apolipoprotein E and premorbid psychiatric illness.2, 3
There is growing speculation that the emergence of PTE after a head injury represents a ‘double hit’ to cognitive functioning, whereby the neurocognitive substrates or networks damaged by the primary trauma are further undermined by a disease characterised by acute-on-chronic disturbance to these same systems (see Semple et al., 20194 for a recent review). There remains, however, a limited number of sources empirically delineating the cognitive and behavioural sequelae of PTE specifically. As such this chapter integrates findings from the parallel neuropsychology literatures investigating TBI and epilepsy to supplement our review of the extant PTE research.
Presented here is a model of cognitive decrement in adults with PTE that is framed in terms of diffuse disruption to neurocognitive brain networks caused by the primary TBI and in some cases then additionally undermined by the development of epilepsy. In light of the scarcity of empirical studies, it is reasonable to assume that the secondary mechanism for neurocognitive decrement attributable to the epilepsy is multifactorial. As in primary epilepsy, cognitive impairment in PTE could stem from seizures and interictal epileptic discharges kindling and propagating along the same neurocognitive networks damaged by the TBI,5, 6 changes to the topography or connectivity of networks hijacked by seizures,7, 8 or perhaps even a shared genetic mechanism underlying vulnerability to PTE and neurocognitive deficits. There may also be significant secondary psychosocial consequences of PTE exacerbated by behavioural difficulties accompanying TBI, such as disruption to educational, vocational and social development, further impacting cognition.
This chapter also outlines an approach to cognitive remediation for people with PTE adapted from the well-established principles of neuropsychological rehabilitation for TBI and supplemented by the more circumscribed epilepsy rehabilitation literature. In recognition of the multidetermined nature of cognitive deficits in PTE, this rehabilitation approach takes into account the relative contributions of structural brain damage, functional network dysfunction and neurological and psychiatric symptomatology, as well as the psychological and social adjustment processes that commonly accompany this condition.
Primary Cognitive Consequences of TBI
As introduced in earlier chapters, TBI occurs due to blunt head trauma in which the head is struck or moved violently. This physical force triggers a range of complex pathophysiological mechanisms that exert differential effects on neurological injury and repair. Primary effects occur at the time of the acute injury when tissues and blood vessels are damaged, compressed, stretched or torn, and they also include processes of neuronal cell death and Wallerian degeneration.9 These primary effects trigger a complex cascade of secondary pathophysiological effects that evolve over time and space, further altering neuronal activity and connections.10 The resulting damage can be both focal and diffuse in nature, impacting key brain structures as well as widespread networks that underpin a range of cognitive functions.
Prefrontal structures, especially those on the orbital surfaces, are particularly vulnerable to focal damage due to their proximity to bony protuberances inside the skull.11, 12 The orbitofrontal region plays a key role in inhibitory control, social awareness and judgement and understanding of the consequences of behaviour.13, 14 Consequently, many individuals with TBI have difficulty anticipating the consequences of their actions and monitoring and adjusting behaviour in line with goals and social expectations in complex ‘real-world’ situations.15–19 This can be compounded by deficits in ‘cold’ executive functions, including planning, problem-solving, idea generation, cognitive flexibility and abstract thinking, that can emerge following damage to dorsolateral prefrontal cortex and associated networks.20, 21
Diffuse axonal injury (DAI) occurs when there is stretching and shearing of axons due to acceleration–deceleration forces, leading to widespread damage to white matter tracts.22 The extent of the damage depends on the nature and severity of the injury, with more pronounced white matter volume loss resulting from more severe injuries.23 Cognitively, DAI can disconnect broadly distributed networks that underpin complex functions including attention, memory and executive function, as well as undermine speed of information processing, contributing to poorer functional outcomes.24, 25 As such, the typical cognitive picture after severe TBI with DAI is of slow and effortful information processing that is vulnerable to distraction and highly susceptible to fatigue.26
In addition to cognitive deficits in attention, memory, speed of information processing and executive functioning, TBI can also lead to problems recognising emotions,27–31 identifying and labelling one’s own emotions,32–34 and understanding others’ emotions, affective states and feelings (i.e. affective theory of mind or cognitive empathy).35–37 This likely reflects damage to a broadly distributed fronto-temporo-parietal network involved in social cognition, which is vulnerable to disruption after TBI.11, 12, 38–40 These difficulties can have a profound impact on a person’s daily life, leading to misinterpretation of the behaviours and actions of others34, 42, 43 and socially inappropriate behaviours,44 particularly when executive problems such as disinhibition and impulsivity are also present.45 Impaired self-awareness further complicates this picture, with many individuals unable to recognise changes in their emotions and behaviour,46 ultimately contributing to growing social disconnection and loneliness.
For instance, these difficulties can negatively impact an individual’s ability to maintain close relationships and interact appropriately with carers, family, friends and colleagues.47 A previously caring father and husband might be described as aloof and dismissive post injury; some partners liken it to having another child in the family.48 Individuals with TBI may start to withdraw from others because socialising is stressful and tiring, with family reporting that they are spending most of the day alone in their room or watching television for hours on end.26 Others may find this behaviour difficult to understand, contributing to further relationship breakdown.49 Friends may gradually make less of an effort to maintain friendships, and social networks can shrink over time, leading to social isolation.50 The case vignette of ‘Shane’ illustrates some of the social and occupational challenges that can arise after severe TBI.
Case Vignette 1: ‘Shane’ Executive dysfunction and social problems after severe TBI
Medical and psychosocial history. Shane is a 61-year-old man who was working full-time as the director of a successful mechanic business prior to his injury. He is married with two adult children. His medical history includes hypertension and moderate alcohol use.
Injury details. Shane sustained a severe TBI following an alleged assault in a bar, in which his head struck the concrete pavement. Glasgow Coma Scale score at the scene was 7. Shane’s acute injuries included a right subdural haemorrhage with 2 mm midline shift, a small right frontal and temporal sub-arachnoid haemorrhage, fractured right petrous temporal bone and multiple cerebral contusions. He spent 16 days in the acute hospital, including 13 days in ICU, before being transferred to a specialist acquired brain injury inpatient rehabilitation unit for four weeks. Total duration of post-traumatic amnesia was 30 days. During his inpatient stay, he was noted to be verbose and tangential in conversation, becoming fixated on specific topics. He was also observed to make inappropriate comments to female staff about their appearance.
Cognitive assessment. Brief neuropsychological assessment during Shane’s inpatient admission (five weeks post-injury) revealed attentional variability, slowed speed of information processing and pronounced executive deficits including difficulty with self-monitoring, verbal reasoning, shifting set and mental flexibility. On repeat neuropsychological assessment 8 months post-injury, while there was evidence of some improvement in cognitive functioning, Shane demonstrated ongoing mild to moderate reductions in attention, processing speed and executive functioning (reasoning, problem-solving, self-monitoring, inhibition and flexible thinking).
Social and occupational functioning post-discharge. On discharge, Shane had no residual physical impairments. However, he was not medically cleared to drive or return to work due to his cognitive difficulties. Shane had minimal insight into the extent of his cognitive changes or their impact on his day-to-day functioning. During the first few months post-discharge, he spent most of his time at home. His family took over the daily operations and financial management of the business. Shane expressed frustration and resentment towards his family for keeping him ‘trapped’ and ‘on a leash’. When he did attend social events, Shane’s wife reported that he was ‘blunt’ in his interpersonal style and would say inappropriate and hurtful things to family and friends. He was also noted to have difficulty regulating his emotions, including managing anger. He did not appear to notice the impact that this had on his relationships.
In response to concerns raised by Shane’s wife, he was referred to a specialist brain injury behaviour management programme. This intervention initially focused on supporting Shane’s wife, including providing her with education about his behaviour and cognitive changes, possible triggers for his behaviours and appropriate management strategies. Shane was subsequently referred to outpatient neuropsychology for ongoing management and support. He attended regular therapy sessions with a neuropsychologist, which focused on learning strategies to support his cognitive deficits and psychological interventions such as relaxation for managing stress.
After 6 months, Shane returned to work in a limited capacity. This involved accompanying his daughter to the business site, where he would sit and observe the day’s activities. Initially, Shane reported feeling frustrated that even though he was back at work, he still wasn’t allowed to run his own business. However, he soon realised that being back at work was exhausting, even in this limited capacity. With time, and with ongoing support from his treating neuropsychologist, Shane expressed less frustration with his family and the perceived restrictions on his life. His family reported that his mood was improved, and he gradually became more appropriate in his interactions with others. Though he was not able to return to his previous level of occupational functioning, he came to enjoy his new role and the sense of purpose and routine of attending work each day.
The expected clinical course of cognitive recovery after TBI is one of gradual improvement. In cases of mild TBI, where there is only a transient alteration of consciousness, any cognitive difficulties usually recover to baseline levels within the first few weeks or months post-injury.51–54 Moderate and severe TBI is associated with more pronounced cognitive impairment, with the most spontaneous improvement likely during the first 6 to 12 months post-injury when neuroplastic changes can facilitate some restoration of cognitive function.55, 56 This tends to reach a plateau at around 2 years.57, 58 While some gradual ongoing improvement after this time is possible, studies of long-term follow-up have found cognitive difficulties can persist beyond 10 years post-injury.59
Secondary Cognitive Consequences of TBI
In addition to the primary effects of a TBI on cognitive functioning, diverse neurological, psychological and psychosocial sequelae of a TBI can further undermine cognitive integrity.
Mood
TBI is associated with an increased risk of mood and anxiety disorders.60 Meta-analytic findings indicate that between 27% and 38% of adults with TBI develop clinically significant symptoms of depression,61 and 37% develop anxiety disorders.62–64 Aetiology is likely multifactorial, including neurobiological factors (i.e. susceptibility of frontal and limbic regions to traumatic injury), psychological factors (i.e. adjustment to the impact of the injury) and psychosocial factors (i.e. social support).65, 66 A pre-injury history of mental health disorder increases the risk for the development of mood and anxiety disorders after TBI.67, 68
Symptoms of mood disturbance and anxiety are independently associated with cognitive difficulties in healthy and clinical populations, particularly affecting the same domains of attention, memory, information processing speed and executive function.69–72 Thus, in the setting of TBI, emotional comorbidities can magnify the primary cognitive effects of the brain injury, leading to more pronounced and disabling symptoms.68 Critically, however, these secondary cognitive consequences are potentially reversible, with emerging evidence that cognitive problems associated with low mood and anxiety may be remediated with treatment in healthy adults73 and in TBI specifically.74 Thus, careful monitoring of mood is recommended to facilitate early detection and treatment of potential mood disturbance after TBI.
Fatigue
Fatigue is common after brain injury, with prevalence estimates ranging from 30% to 70%.75 The experience of fatigue after TBI can be both cognitive and physical and can affect individuals across the spectrum of injury severity from mild to severe.76, 77 Individuals with TBI may describe it as ‘hitting a wall’, beyond which they can no longer engage in continued cognitive or physical effort.78 This can be particularly pronounced following sensory stimulation or prolonged engagement in cognitive tasks.79 Post-TBI fatigue is commonly cited as a significant barrier to returning to valued activities in the community and can have a major impact on quality of life.41 It can also be chronic, persisting for many years post-injury.80, 81
In terms of mechanisms, it has been proposed that the effort required to compensate for slowed processing speed and attentional problems to achieve an adequate level of function in day-to-day life is a significant contributor to fatigue after TBI.75 This is supported by findings from empirical studies of subjective fatigue and cognitive performance.82, 83 Additionally, functional MRI studies have shown that, compared to healthy controls, individuals with TBI demonstrate increased activation in task-related brain regions while performing a cognitive task, suggestive of increased cerebral effort required to complete the task.84 The relationship between fatigue and cognition is reciprocal, with cognitive difficulties not only contributing to this picture, but being further exacerbated by fatigue. In particular, greater subjective cognitive fatigue after TBI is associated with slower processing speed and more errors on tasks of complex attention.75, 85–87 Fatigue also interacts with other common sequelae of TBI, including sleep disturbance, pain, depression and anxiety.88, 89 As such, timely and appropriate management of these conditions is important.
Primary Cognitive Sequelae of Epilepsy
The peak global body for epilepsy care and research, the International League Against Epilepsy, defines epilepsy as a disease whose hypersynchronous electrical activity entrains and is propagated along the networks that organise the brain.90 This leads to both paroxysmal disruption of networks specialised for neurocognitive processing, as well as chronic abnormalities in the topography, structure and functioning of these same networks stemming from interictal epileptic discharges and epilepsy-related pathologies.7,8,91–94 Some degree of cognitive impairment can thus be detected in many people with epilepsy,95 and cognitive comorbidities are now considered to be an intrinsic feature of the disease.96 Cognitive comorbidities are a major economic and psychological burden on people with epilepsy, with self-report ratings indicating that cognitive deficits significantly reduce day-to-day functioning and quality of life, and may limit employability.97
Research focusing on delineating the clinical factors that contribute to the development of cognitive dysfunction in people with epilepsy variously emphasise the deleterious role of seizure frequency and severity, frequency of subclinical interictal epileptiform activity, seizure-induced head strikes, long duration of epilepsy and the age at onset of seizures.5, 98 The influence of the latter, however, is nuanced. In childhood-onset disease, epileptiform activity and gross brain pathology can skew the normal development of cognitive networks, resulting in either impaired cognitive function or the transfer of cognitive hubs proximal to the seizure focus to intact regions of the brain.99 The development of seizures in adult-onset epilepsy can not only lead to focalised impairments equivalent to those seen in childhood-onset cases when they are associated with brain pathology or depression,100 but may also accelerate senility due to the ‘double hit’ of aging on cognitive networks already compromised by epilepsy.101
More broadly, cognitive impairments in people with epilepsy have been conceptualised as an intrinsic feature of the underlying network disease; that is, the disease process that gives rise to seizures also gives rise to cognitive impairment.102 Supporting this, severe memory impairments in focal epilepsy patients with no MRI-resolvable brain lesion can be similar to those in patients with gross pathology, like hippocampal sclerosis or tumours.103 Moreover, the finding that cognitive impairments may be evident in untreated patients with newly diagnosed seizures104, 105 suggests that the disease can disrupt the healthy development of cognitive networks in the absence of overt seizures. This means that abnormal neurocognitive function in epilepsy may not be purely a consequence of damage secondary to seizures and pathology, as was traditionally believed.
Epilepsy can arise from any region of the cerebrum or cerebellum, and therefore all cognitive domains and networks are vulnerable in this population (see Helmstaedter et al., 2011 for a review95). Some cognitive deficits in epilepsy are markers of large-scale network compromise taking the form of slowed information processing speed (bradyphrenia) and attentional inefficiency, which are seen across many focal and generalised epilepsy syndromes but are especially pronounced in drug-resistant cases.95 In contrast, circumscribed, focal seizure onsets are classically associated with cognitive features attributable to dysfunction in the onset zone. For example, memory disorder in temporal lobe epilepsy (see Saling, 2009 for a review106), executive dysfunction in frontal lobe epilepsy,107–109 and language symptoms such as dysnomia or paraphasias in people with disease localised to the language-dominant hemisphere.110 Given the day-to-day personal relevance of social cognitive deficits, there is also growing evidence that relative to healthy controls both focal and generalised forms of epilepsy can be associated with deficits in theory of mind and facial emotion recognition,111, 112 with reduced social cognition linked to an earlier age at seizure onset.112
Secondary Cognitive Consequences of Epilepsy
In addition to the disturbance to neurocognitive networks by seizures and the underlying disease, people with epilepsy can also contend with various medical, psychological and psychosocial sequelae of their illness that can secondarily undermine cognitive efficiency.
Unipolar depression is the most common psychiatric symptom of epilepsy, with up to 50% of patients developing a clinically significant mood disorder at some point in their lifetime.113, 114 Symptom profiling of depression in epilepsy reveals a predominant phenotype (base rate = 17%) taking the form of a Cognitive Depression that is characterised by cognitive symptoms of depression and dysphoria. Epilepsy patients with cognitive depression also have prominent memory deficits relative to nondepressed patients or those with a somatic or vegetative phenotype of depression in epilepsy (base rate = 7%).114 Reduced new learning and delayed recall is more prominent in epilepsy patients with major depression, especially in patients with left temporal foci,115–117 with severity of depressive symptoms able to predict the scope of the memory dysfunction.118 This laterality effect has been interpreted as reflecting the depletion of cognitive reserve in people with depression exacerbating already poor verbal elaboration skills. After epilepsy surgery, temporal lobe epilepsy patients with clinically elevated depressive symptoms evidence greater verbal memory decline than nondepressed patients,119 while frontal lobe epilepsy patients with elevated depressive symptoms show greater reductions in cognitive control.120 These poor cognitive outcomes cannot be accounted for by differences in seizure outcome or post-operative mood alone, and they predict cognitive outcome beyond what can be achieved with pre-surgical memory indices. This may indicate that cognitive function after epilepsy surgery is more vulnerable in the context of depression, with the nature of the cognitive impairment shaped by the underlying focalisation of the patient’s epilepsy syndrome. Further research, however, is needed to determine whether these cognitive ‘declines’ are reversed when a patient’s psychiatric state improves.
The surgical and medical treatment of seizures can also lead to cognitive disorder. For the 30% of patients whose seizures are drug-resistant, epilepsy surgery offers the best chance of seizure freedom.121 For some patients, however, this opportunity costs them a decline in their cognitive function.122 In their review of 474 cases in the epilepsy programme at Queen’s Square, London, Baxendale and Thompson122 identified that nearly 40% of patients who underwent epilepsy surgery experienced a decline in their memory function, while 12% suffered a ‘double hit’ of cognitive decrement occurring in the context of ongoing postsurgical seizures. Initial longitudinal evidence suggests that when surgery does result in seizure freedom over the long term, memory function can recover to baseline levels, with drug load reduction specifically linked to improvements in executive functions.123 Notably, this latter study of 161 German patients did not find evidence for accelerated cognitive decline in the years after surgery over the long term. Chapter 13 of this book specifically details the iatrogenic impact of antiepileptic medications on cognition, with sedation and bradyphrenia common side effects.
Cognitive Profile of Post-traumatic Epilepsy
Post-traumatic Epilepsy: a ‘Double Hit’ to Cognition?
There is a paucity of empirical research that directly investigates the cognitive sequelae of PTE in humans.124, 125 However, given the above findings of elevated rates of cognitive deficits in both epilepsy and TBI, it is conceivable that PTE may serve to exacerbate the existing cognitive problems resulting from TBI alone and result in a ‘double hit’ to cognitive function.
Early work by Dikmen & Reitan (1978)126 explored whether the cognitive sequelae of PTE were attributable to structural neurological damage rather than the epilepsy per se. They did this by comparing the normal cognitive functioning of healthy controls (n = 20) to that of two subgroups of head-injured patients: one with PTE and persistent focal neurological signs (n=22) and the other with PTE uncomplicated by neurological findings (n=27). Their cross-sectional study revealed that both PTE groups showed equivalently poor cognitive functioning relative to healthy controls, suggesting that the epileptic activity associated with PTE underpins its poor cognitive outcomes rather than gross brain pathology.
More recently, to explore the ‘double hit’ hypothesis, Semple and colleagues (2019)4 reviewed both clinical and preclinical evidence pertaining to emotional, cognitive and psychosocial outcomes after PTE. Their review identified only a small handful of studies that had empirically investigated cognitive function in a cohort of people with PTE. Of these, two failed to find any evidence to support the notion that individuals with PTE experienced worse cognitive outcomes than TBI patients without seizures, after accounting for severity of TBI (N = 143 and 210)125, 127 In contrast, a longitudinal study by Raymont et al. (2010)128 assessing the cognitive outcomes of 199 Vietnam War veterans with penetrating head injuries found that PTE was predictive of a significantly greater decline in intelligence scores from pre-injury to 35-years post-injury, even when accounting for pre-injury intelligence scores and brain volume loss. Furthermore, duration of PTE was predictive of decline in intelligence scores between phase 2 to 3 of the study (i.e., between 15- and 35-years post-injury). Their findings suggest that PTE may have a cumulative, deleterious impact on general cognitive function relative to TBI alone, and it may predispose individuals to a more rapid cognitive decline later in life.128
Together, these limited studies provide tentative evidence for the hypothesis that people with PTE may be vulnerable to experiencing a ‘double hit’ to their cognition relative to people with TBI alone, although the nature and severity of their deficits relative to people with epilepsy alone remains to be clarified. More striking is the lack of extant literature, highlighting the vast gap in our existing knowledge of cognitive outcomes in PTE. Further research that systematically investigates the neuropsychological sequelae of PTE relative to both neurological populations (e.g. TBI/epilepsy) as well as healthy controls is urgently needed before stronger conclusions can be drawn.
Principles of Neuropsychological Rehabilitation for PTE
This section seeks to provide a model of cognitive rehabilitation for PTE, taking into account the secondary features of the disorder that can additionally undermine cognitive efficiency such as fatigue, sedation, depression and psychosocial restrictions. A barrier to this endeavour, however, is that there is little research into optimising cognitive rehabilitation for people with epilepsy129 and seemingly none specific to people with PTE. This is a reasonable gap in the literature given there is limited evidence to date that PTE represents a distinct neurocognitive syndrome from TBI and/or epilepsy alone, with the nature of deficits similar but potentially just more severe in the combined form. As such we base this model on the well-established principles of neuropsychological rehabilitation for TBI and adapt it to account for the issues specific to comorbid epilepsy where scientific evidence allows.
Neuropsychological rehabilitation in PTE is an interactive process between the patient, family, community and health care team. 132 It seeks to optimise the functional capabilities of people who have cognitive or behavioural limitations resulting from the TBI and/or epilepsy, for which there is no known cure. It does not emphasise full restoration of function to premorbid levels; instead it seeks to maximise patient and family quality of life despite the patient’s cognitive and behavioural limitations 130 by optimising independence and participation in the community. It achieves these aims through the use of medications, activity modifications, physical therapy, cognitive retraining, assistive devices and compensatory strategies, as well as adjunctive experiential therapy approaches involving art, animal care, music and drama.131
Remediating cognitive limitations can also be essential to patients achieving their goals with other health disciplines during the rehabilitation process. This necessitates a holistic approach to rehabilitation incorporating multi- or inter-disciplinary teamwork (see ‘Freya’ below).129 Holistic rehabilitation of cognitive impairments aims to (i) sensitively increase patient awareness of their acquired limitations; (ii) work with the patient and support network to develop compensatory skills tailored to each individual’s cognitive profile of strengths and weaknesses; (iii) provide psychoeducation, cognitive and social skills retraining and therapeutic interventions to minimise the impact of the patient’s deficits; and (iv) support family members and other carers to reduce burnout.131 The success of this endeavour broadly depends on effective goal setting, addressing the emotional sequelae of PTE, designing appropriate cognitive strategies, as well as recognising and managing the psychosocial barriers to rehabilitation that are specific to TBI and epilepsy.132, 133
Case Vignette 8.2: ‘Freya’ The role of interdisciplinary teamwork in the rehabilitation setting
Freya is a 44-year-old female who developed PTE a few weeks after sustaining a moderate TBI in a cycling race. She currently has a generalised tonic-clonic seizure around once every 8 weeks despite pharmacotherapy with sodium valproate. She also incurred numerous lower limb orthopaedic injuries in her accident, and her rehabilitation goal is to return to a much-loved pastime of jogging. Specifically, she aims to build up to a 5-kilometre jog without stopping over the coming 6 months.
Freya’s capability to achieve this physical goal is currently undermined by her cognitive difficulties. She is finding it hard to concentrate and follow instructions in her physiotherapy sessions, and secondary to some attentional impairments, she has trouble remembering the at-home exercises prescribed by the physiotherapist. This means Freya is not making as much physical progress as she had hoped. Freya has also identified an emotional barrier to achieving her goal; namely, she is scared of having a seizure whilst out jogging in the community and ‘being taken advantage of’ by an opportunistic sexual predator.
To assist Freya, the neuropsychologist is working collaboratively with Freya and her physiotherapist to develop tailored compensatory and environmental strategies to circumvent her attentional difficulties in her physio sessions, to allow her to physically achieve her goal. This includes reducing distractions by shifting her sessions to a quieter time of day, as well as writing down all instructions relevant to her at-home programme. The neuropsychologist is also working therapeutically with Freya to identify cognitive and behavioural strategies for her seizure-related anxiety, including systematic desensitisation of her ‘nightmare scenario’ and organising a roster of friends and family to accompany her as she builds up her jogging confidence.
Goal-focused. A cornerstone of cognitive rehabilitation with any patient population is the development of ‘SMART’ goals from the outset of patient engagement.131
SMART goals are:
Specific: describe exactly what the patient wants to be able to do, in their own words;
Measurable: decide how you will know when the goal is met. This may require setting multiple sub-goals in order to reach the major goal;
Achievable: is this a realistic endeavour?
Relevant: is this goal important to the patient and his/her values?
Timely: decide in what time frame the goal will be achieved.
In the second Case Vignette of Freya, her SMART goal is to return to jogging (S); namely to be able to jog for 5 kilometres non-stop (M). This is deemed (A)chievable given her prognosis for physical recovery and her premorbid aptitude for the same activity, and it is an endeavour that brings her a sense of mindfulness and achievement (R). Finally, Freya hopes to attain this goal in 6 months (T).
The collaboration between the patient, team and support network in delineating rehabilitation goals is essential in empowering patients to take control of their own disability and to ensure that the goals set are relevant to the life they want to live. Amongst the health care team, a multidisciplinary approach is emphasised to co-ordinate the rehabilitation goals of patients.129 In the case of Freya, interventions designed to compensate for her cognitive impairments were a key element in achieving her specific goal with physiotherapy to improve her lower limb function sufficiently to be able to jog a medium distance. It is also important for the patient and carers to identify potential barriers to achieving goals, such as financial barriers, cognitive or physical disability or lack of transport.
Cognitive Strategies
Prior to implementation of specific cognitive strategies, a comprehensive neuropsychological assessment is recommended. By integrating data from a range of sources, including performance on formal cognitive tasks, interviews with the patient and informant, measures of day-to-day functioning and behavioural observations, this assessment can be used to build a comprehensive profile of the individual’s cognitive strengths and weaknesses. It is important to consider the person’s strengths and skills, how the cognitive deficits are manifesting in everyday life, the day-to-day cognitive demands placed on the person and specific goals (as outlined in the section above) when selecting strategies for cognitive rehabilitation. In the absence of literature investigating the efficacy of cognitive strategies in PTE, the following sections draw upon the most up-to-date evidence-based practice recommendations available for cognitive rehabilitation after brain injury.
Attention and Processing Speed
Evidence from a recent systematic review134 and recommendations from an international panel of experts (INCOG)135 support the use of metacognitive strategy training for addressing problems with attention and information processing on everyday functional tasks, particularly for deficits in the mild to moderate range.134, 135 This includes simple strategies, such as breaking information down into smaller, meaningful ‘chunks’, as well as formal training approaches such as Time Pressure Management (TPM) strategy training, developed by Fasotti and colleagues.136 TPM aims to increase the individual’s awareness of the effects of slowed processing speed and supports the use of self-instructional techniques or other steps to reduce time pressure (e.g. asking a person to repeat themselves, or recording information and playing it back later). Evidence from a randomised control trial (RCT) supports the use of this approach for improving coping with slowed information processing.136
There is also evidence from RCTs to support the use of cognitive training on dual tasks of attention, with improvements most likely on tasks similar to those trained.134, 135 Environmental modifications that aim to reduce task attentional demands and maximise functioning (e.g. minimising distractions in the environment or using prompts to shift attention to another component of the task) are also frequently used in clinical practice.137 However, more research evidence is required to support these recommendations.135 The sole use of computer-based programs for improving attention and working memory is not recommended, due to findings of a lack of generalisation beyond the trained tasks to everyday functioning.134, 138 Rather, this may be considered one part of a comprehensive rehabilitation program delivered under the guidance of a clinical neuropsychologist to build awareness and support the generalisation of learnings.134
Memory
Compensatory memory strategies aim to maximise the individual’s everyday function via internal or external strategies. Internal strategies require conscious effort to improve memory encoding, for example, by grouping a shopping list into different semantic categories, such as fruit, vegetables and meat.139 External strategies are those that rely on support beyond the self, and these include the use of diaries, notebooks, smartphones and whiteboards. There is good quality evidence for the effectiveness of internal and external strategy instruction in the rehabilitation of memory impairments after TBI.134 For effective implementation, internal strategies require the person to have a degree of intact executive function and self-awareness, and thus they tend to be more effective for mild to moderate memory problems.134, 140 Individuals with severe memory impairment after TBI typically benefit more from external supports and reminders, particularly when there is a support person available to prompt the use of these aids.141 In choosing the most appropriate external memory aid, consideration should be given to the person’s age, prior experience with technology, premorbid use of memory devices, cognitive profile and any physical comorbidities.134, 141 Overall, compensatory memory strategies that align closely with a person’s everyday tasks and activities are most likely to be used and therefore be successful.142
Executive Function
Metacognitive strategy training is recommended as a practice standard for addressing problems with executive function amongst adults with brain injury, based on evidence from several systematic reviews and meta-analyses.134, 143–146 Metacognitive instructive techniques are particularly recommended for addressing problems with planning, organization and problem-solving, with an emphasis on targeting improvement on everyday functional tasks.143 Interventions are typically multifaceted, including components such as goal setting, goal management training, time pressure management, self-monitoring and direct feedback.147 Direct feedback interventions, which seek to build the person’s awareness and self-regulation skills through verbal, visual and/or experiential feedback, have been shown to be particularly useful for improving self-awareness of deficits after brain injury.148–150
There is also evidence to support the use of strategies promoting the analysis, assimilation and synthesis of complex material for improving reasoning skills after brain injury.134, 143 For example, in an RCT of their Strategic Memory and Reasoning Training (SMART) Group programme, Vas and colleagues151 trained adults with TBI to use a range of strategies, including filtering, focusing and chunking, linking, zooming and generalising, to extract meaning from complex material such as movies and news reports. This 12-session intervention resulted in significant improvements in reasoning, working memory and community participation, which were maintained 6 months post-completion of the programme. These interventions are less effective for individuals with severe cognitive impairment, however, as they require the individual to have sufficient self-awareness to identify the need for a strategy.143 For those with pronounced impairments, additional environmental supports and structure in the way of external aids and prompts are recommended.
Social Cognition
Social cognition has emerged more recently as a target for treatment after brain injury. In a recent systematic review, Vallat-Azouvi and colleagues152 identified 16 studies reporting treatment for social cognitive deficits after TBI, of which nine were RCTs. The majority of studies to date have examined the efficacy of specific training programmes to improve facial affect recognition, with mixed but promising results.153–156 These interventions typically encourage the person to attend to areas of the face involved in emotional expression via verbal prompts, computer programs or video-based observation and instruction. Findings of the efficacy of interventions addressing other specific aspects of social cognition, such as theory of mind, have also been mixed.157 These treatments aim to improve the individual’s ability to infer what another person is thinking or feeling through the use of stories, cartoons, picture series, videos or role plays. There is some evidence for treatments targeting emotion regulation after TBI. For example, Aboulafia-Brakha and Ptak158 found that a group anger management intervention could increase the use of coping strategies and reduce anger levels.
Combined treatment approaches that target multiple domains of social cognition have shown the most promising findings.159 For example, Westerhof-Evers and colleagues160 developed a multifaceted treatment for impairments in social cognition and emotion regulation (T-ScEmo) that includes compensatory strategies to improve emotion recognition, theory of mind and social skills, delivered in weekly 1-hour sessions for 16–20 weeks. The findings from this RCT showed that, when compared to a computerised cognitive training program, T-ScEmo resulted in significant improvements on tests of emotion recognition and theory of mind, ratings of empathic behaviour and participation in society for individuals with TBI, and these gains were maintained at 5-month follow-up.
Overall, although this field is still in its infancy, there are encouraging findings of the efficacy of some treatment approaches. Given problems with low sample sizes and inconsistent findings regarding generalisation to everyday functioning, further high quality studies are needed. Treatment programmes that hold most promise for generalisation of skills to day-to-day functioning are those that have an experiential basis, take a collaborative approach and are contextualised.161
Addressing Emotional Comorbidities to Achieve Cognitive Goals
As outlined earlier, depression and anxiety are highly prevalent and can contribute to cognitive deficits and reduced quality of life in PTE.162 Individuals with PTE report that seizures have a negative impact on their ability to cope with the effects of the brain injury and act as a barrier to engaging in social activities in the community, which may further undermine emotional and cognitive functioning.163 As such, a comprehensive and multidisciplinary approach to cognitive rehabilitation in PTE should include assessment and management of any emotional comorbidities.
Unfortunately, there is little research examining the efficacy of psychological approaches for addressing emotional disturbance in PTE. However, there are psychological treatments that have been found to be effective in TBI and epilepsy, and thus may hold promise for PTE. Cognitive behaviour therapy (CBT) is an extensively researched and well-validated psychological treatment for anxiety and depression in the general population.164 CBT is a short-term, goal-oriented, structured form of psychotherapy that can be adapted to suit the needs of individuals with specific health conditions.165 A modified CBT approach has been found to be effective in reducing symptoms of depression and anxiety after TBI.166
For the patient with PTE, a CBT programme incorporating tailored, neurobiologically informed psychoeducation on the emotional and cognitive consequences of brain injury and seizures may help to frame and normalise some of the challenges. Practical modifications to accommodate for cognitive impairments include scheduling shorter therapy sessions and frequent rest breaks, ensuring repetition of key information, providing written summaries to support learning, using concrete examples to explain abstract concepts and using external memory aids such as smartphone reminders to support the completion of homework tasks or session attendance.167, 168 Psychological interventions also need to be sensitive to the ongoing challenges associated with PTE, including careful management of risk factors, activity limitations associated with seizures and the impact of anti-epileptic drug treatments.
TBI-specific Considerations for Rehabilitation
TBI has been described as a ‘silent’ or ‘hidden’ disability. Although many individuals with TBI have no physically discernible sign of disability, they can experience cognitive, social and emotional deficits that act as a major barrier to successful participation in the community, as highlighted throughout this chapter.169–171 Misconceptions about TBI have been reported amongst the general public and by some health professionals.172, 173 There is an expectation that a person who appears ‘normal’ should behave normally, and so family, friends and work colleagues may overestimate the abilities of brain-injured individuals with no overt physical signs of disability.174 The degree of visibility of injury can impact on attributions of behaviour: when there is no visible marker of disability, the individual’s actions (e.g. behaving in a way that is socially inappropriate) are more likely to be perceived as intentional rather than attributed to a neurological impairment.175, 176
The stigmatising and prejudicial attitudes held by the general public about individuals with TBI, particularly those with no overt signs of disability, may interfere with rehabilitation efforts.177, 178 In PTE, this is compounded by the stigma associated with epilepsy, as discussed in the section below. Minimisation, trivialisation or misattribution of an individual’s cognitive deficits can invalidate the person’s experience and may undermine recovery. For this reason, it is important for clinicians to be aware of the diversity of cognitive, emotional and behavioural sequelae in PTE, and the significant impact that these symptoms can have on the person’s everyday life, including the ability to work, study and maintain relationships. From the perspectives of the person with brain injury and the family, it is the emotional and behavioural symptoms that appear to have the greatest impact on the quality of life and the family’s caring burden over the long term.179
One of the most common and disabling ‘hidden’ symptoms of TBI is fatigue. As discussed earlier in this chapter, fatigue can interact with and exacerbate primary cognitive difficulties following brain injury. In PTE, poorly managed fatigue may also represent a risk factor for reduced seizure control. Thus, improved management of fatigue may represent both a target for rehabilitation and an important consideration when structuring a rehabilitation programme for a patient with PTE.
Behavioural management techniques can help the individual to manage cognitive fatigue and minimise its effects on day-to-day life. First, the rehabilitation clinician might work together with the person with PTE to monitor and record fluctuations in fatigue levels over the course of a week. By revealing patterns in fatigue levels, including changes in response to specific activities or times of day, this exercise can provide valuable information to guide subsequent interventions. Strategies can then be tailored to the individual and may include, for example, scheduling activities for the time of the day when the person typically feel at his/her best, taking frequent breaks, keeping therapy sessions brief, delegating tasks to others, engaging in one task after another rather than multi-tasking, minimising stimulation in the environment and implementing healthy sleeping habits (e.g. regular bedtime routine, minimising naps during the day).78, 180
These behavioural management strategies can be complemented by more structured psychological interventions, which have been found to be effective in treating fatigue after TBI and may hold promise in PTE. For example, an RCT of patients with TBI or stroke found that an 8-week programme of mindfulness-based stress reduction resulted in improvements in mental fatigue and cognitive performance.181 More recently, in an RCT conducted by Nguyen and colleagues182 an eight-session adapted CBT programme was found to improve sleep quality, daily fatigue levels and depression symptoms amongst adults with TBI.
Related posts:
Chapter 5 – Post-traumatic Epilepsy in Children
Chapter 6 – Sport-related Concussive Convulsions
Chapter 7 – Accidents and Injuries during Seizures
Chapter 12 – Antiepileptogenic Therapies for Post-traumatic Epilepsy: Is There Any Evidence?
Chapter 13 – Effects of Antiepileptic Drugs on Cognition
Chapter 14 – Post-traumatic Epilepsy in Low Income Countries
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