Neuropsychology Review https://doi.org/10.1007/s11065-018-9367-7

REVIEW

Memory Rehabilitation in Patients with Epilepsy: a Systematic Review Samantha Joplin 1,2 & Elizabeth Stewart 1,2 & Michael Gascoigne 1,2,3 & Suncica Lah 1,2 Received: 25 November 2016 / Accepted: 21 January 2018 # Springer Science+Business Media, LLC, part of Springer Nature 2018

Abstract Memory failure is a common clinical concern of patients with epilepsy and is associated with significant functional impairments. Thus, memory rehabilitation is of critical clinical importance. In this article, we aimed to systematically evaluate the efficacy of memory rehabilitation in patients with epilepsy. The Preferred Items for Systematic Reviews and Meta-Analyses (PRISMA) was used to guide searches, extraction and reporting of data in this review. PsycINFO, Medline and PsychBITE searches yielded 95 studies. Twelve papers met inclusion criteria, reporting outcomes of cognitive or behavioural interventions that specifically targeted the rehabilitation of memory in patients with epilepsy. Methodological rigour was rated using the Single-Case Experimental Design (SCED) scale for single-case studies and a modified version of the Downs and Black checklist for group studies. Twelve prospective studies, nine group (six pre-post design, one waitlist crossover, two randomised controlled trials) and three single-case studies were identified. Eleven of the studies included adults, eight of which involved adults with temporal lobe epilepsy (TLE). One paediatric study was identified. The quality of group studies ranged from 36% (poor) to 72% (good), using the modified Downs and Black checklist. Single-case studies were assessed using the SCED scale and assessed to range in quality from four to seven out to 11. Overall, memory rehabilitation was associated with improved memory function in all studies. Verbal memory outcomes were most commonly examined and associated with improvements. This review found that the level of evidence available to support rehabilitation of memory in patients with epilepsy was generally weak and inconsistent. Nevertheless, studies conducted to date, albeit of limited methodological quality, offer preliminary evidence that memory rehabilitation is associated with improvements in verbal memory in patients with temporal lobe epilepsy. Little is known about the efficacy of memory rehabilitation in patients with nonTLE, children, and other aspects of memory difficulties. Guidelines for future research are proposed. Keywords Rehabilitation . Compensation . Restoration . Seizures . Surgery . Memory

Memory failure is a common clinical concern raised by patients with epilepsy, irrespective of the presence of brain lesions or the use of anti-epileptic medication (Giovagnoli et al. 1997; Thompson and Corcoran 1992). Memory failure is associated with significant functional deficits. For example, forgetting names, appointments, and autobiographical information. Such functional deficits place patients at risk of social, educational and vocational disadvantage (Blake et al. 2000;

Corcoran and Thompson 1992; Vermeulen et al. 1993). Patients with epilepsy perceive value from involvement in memory intervention (Wedlund et al. 2013). With the potential to improve cognition, social well-being, and community participation, the research and practice of such interventions should be paramount in this population. Despite the need for interventions, it seems that research and practice of memory rehabilitation in people with epilepsy lags behind research conducted in other neurological populations, such as traumatic brain injury (TBI; for reviews see Cicerone et al. 2011; Rees et al. 2007; for recommendations see Velikonja et al. 2014).

* Suncica Lah [email protected] 1

School of Psychology, University of Sydney, Sydney, NSW 2006, Australia

Memory Rehabilitation

2

ARC Centre of Excellence in Cognition and its Disorders, Macquarie University, Sydney, Australia

3

Australian College of Applied Psychology, Sydney, Australia

The ultimate aim of memory rehabilitation is to improve everyday functioning, reduce disability and increase community and vocational participation. Memory rehabilitation aims to teach

Neuropsychol Rev

patients how to compensate for memory deficits or to restore memory functions. Compensatory approaches to memory rehabilitation utilize internal and external strategies and rely on preserved functions. An example of an internal strategy used for memory rehabilitation is mindful attention, which involves increased effort during encoding of new information at the time of learning. Mindful attention has been reported to facilitate longterm (episodic) memory function in non-clinical populations (Brown et al. 2016). External memory strategies involve physical systems, such as diaries and electronic devices. External memory strategies have demonstrated efficacy in reducing memory failure in patients post TBI or stroke (Cicerone et al. 2011; Radford et al. 2011; Wall et al. 2013; Wilson et al. 2005). A restorative approach to memory rehabilitation relies on the neuroplasticity of cognitive functions to facilitate change. This approach often uses exercises that involve repetitive drills that are sometimes computerised. Findings regarding the efficacy of computerised restorative programs have been inconclusive (i.e. for reviews see Klingberg 2010; Melby-Lervag and Hulme 2013; Shipstead et al. 2010). In some studies, improvements are seen on trained tasks, with little evidence of transfer to either untrained tasks that involve the skills targeted by the training (near transfer: Jaeggi et al. 2010; Owen et al. 2010) or other untrained tasks that involved skills not targeted by training (far transfer: Holmes et al. 2009). In other instances however, improvements are found on completion of computerized working memory training on untrained measures of working memory and reading both immediately and at three months posttraining (Phillips et al. 2016). However, it is unclear whether gains obtained in training are maintained long-term (MelbyLervag and Hulme 2013). Interestingly, qualitative research has indicated that concomitant use of external (i.e. note taking) and internal (i.e. mental imagery) strategies is perceived as highly important for overcoming everyday memory difficulties (Wedlund et al. 2013).

Epilepsy Factors that Need to be Considered in Memory Rehabilitation In patients with epilepsy, memory rehabilitation needs to consider epilepsy-related factors that are not present in patients with other non-progressive neurological diseases, such as TBI or stroke, which impact memory and can influence responsiveness to intervention. For example, in TBI, an insult to the brain is caused by an external force, whereas in epilepsy, seizures originate from the brain itself (Fisher et al. 2014). In epilepsy, seizures themselves may interfere with initial memory acquisition and consolidation (Kapur 1997) and disrupt already established memory stores or access to these memory stores (Lah et al. 2006). Moreover, the location of epilepsy foci impacts the risk, gravity, and pattern of memory deficits. It has been known for some time that mesial temporal lobe epilepsy is associated with

impaired learning and retention of newly learned material (i.e., Milner 1975; Smith and Milner 1989) and that the side of epilepsy focus impacts the pattern of memory deficits (Milner 1968). While patients with left (language dominant) mesial TLE present with impaired learning and retention of verbal materials, patients with right TLE present with impaired learning and retention of visual materials (Golby et al. 2001; Jeyaraj et al. 2013; Willment and Golby 2013). In TBI, the acute (typically one-off) injury is followed by a period of recovery during which patients’ memory functions improve, albeit often remain impaired relative to controls (i.e., Millis et al. 2001; Vanderploeg et al. 2014). In epilepsy, seizures typically require ongoing pharmacological treatment and in some cases surgery, as seizures are inadequately controlled with pharmacotherapy in approximately 20 to 30% of patients (Elger and Schmidt 2008; Schmidt and Schachter 2014; Kwan and Brodie 2000). Both pharmacological treatment (especially Topiramate) and surgery, in particular left temporal lobectomy, carry a risk of memory decline (i.e., Baxendale et al. 2006 and Sommer et al. 2013, respectively). Several studies have shown that these epilepsy-related factors can impact the efficacy of memory interventions. For example, in one study, while patients with a left-hemisphere seizure focus (left-TLE) did not benefit from memory rehabilitation, patients with right-TLE did (Bresson et al. 2007). In another study, patients who were on polytherapy made smaller gains in rehabilitation relative to patients who were on monotherapy for epilepsy (Radford et al. 2011). It was proposed that several other epilepsy-related factors, such as early age of seizure onset, higher seizure frequency, and surgery for epilepsy could also have an adverse impact on the efficacy of memory rehabilitation (Hendriks et al. 2004; Mazarati 2008; Motamedi and Meador 2003; Radford et al. 2012). Furthermore, epilepsy often begins in childhood and is associated with a considerable risk of memory deficits even at this early age (i.e., Nolan et al. 2004). As memory is critical for learning and development, memory impairments at this early age may have far reaching consequences. Children with epilepsy may fail to acquire new skills and knowledge, or experience a slower rate of knowledge acquisition. Therefore, it is imperative to develop and provide age-appropriate memory interventions not only to adults, but also to children with epilepsy.

Aims of the Current Study The overall purpose of this study was to conduct a systematic review of the literature on the effectiveness of memory rehabilitation interventions in patients with epilepsy. Specific aims of the study were to systematically review memory intervention publications in patients with epilepsy for the (i) level of methodological rigor, (ii) identification of salient techniques and modes of delivery, and (iii) outcome evidence including

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effectiveness, transfer or generalization, and maintenance. In addition, we aimed to explore relations between epilepsy variables and outcomes.

Methods The Preferred Items for Systematic Reviews and MetaAnalyses (PRISMA; Moher et al. 2009) was used to guide our searches, extraction and reporting of data in this review.

Inclusion and Exclusion Criteria All studies needed to meet the following inclusion criteria (i) peer-reviewed, (ii) published in the English language, (iii) empirical in nature, (iv) conducted with patients diagnosed with epilepsy or a history of seizures, (v) reported findings relating to patients with epilepsy separately from findings of other patient groups (when applicable), and (vi) involved a cognitive or behavioural intervention targeting memory. Studies were included irrespective of the year of publication or design. Both single-case studies and group studies were deemed acceptable due to the paucity of research in this field. Exclusion criteria were (i) review articles or meta- analyses, (ii) editorials, (iii) conference or meeting abstracts, even if published in peer reviewed journals, as they typically do not contain a sufficient amount of detail to be critically evaluated, (iv) unpublished conference papers, and (v) dissertations.

Search Strategy Studies were identified through a computerised search of PsychBITE, PsycINFO and PubMed. The search terms employed were Bmemory^ and Bepilepsy^, with different combinations of Brehabilitation^, Bintervention^, Btraining^, Bremediation^ and Btreatment^ (Table 1). The searches were limited to English language and peer-reviewed published articles. Citation tracking was also used to identify relevant papers. The initial search that was conducted on May the 6th 2015 was updated on May the 29th 2016.

Study Selection Two reviewers (SJ and ES) discussed pre-determined inclusion or exclusion criteria and independently screened all the titles from the initial searches against these criteria. Discrepancies were resolved through discussion. When agreement could not be reached on the basis of titles, abstracts and full texts of manuscripts were retrieved and reviewed. A full list of excluded papers and corresponding exclusion criteria are presented in Appendix-3.

Quality Analysis The quality of group studies was evaluated using a modified version of the Downs and Black checklist (Downs and Black 1998; Appendix-1). The Downs and Black checklist is used for assessing the methodological quality of both randomised and non-randomised studies. The checklist provides an overall index of study quality, using four subscales to assess reporting, external quality, internal validity-bias, and internal validity-confounding. The original checklist contained 27 items, assessing (i) reporting, (ii) external validity, (iii) internal validity, and (iv) bias, respectively. Questions 8, 13 and 19 were omitted for the purpose of this review for three reasons. First, memory rehabilitation strategies are not likely to be associated with significant adverse effects. Second, memory rehabilitation is not part of routine clinical patient care. Thus, it was not possible to determine if the intervention was Brepresentative of that used in the source population^, Third, non-compliance would likely manifest as patient attrition, as we are not aware of any validated measure of compliance with memory rehabilitation (i.e., use of memory strategies) in the population of interest. For item five, principle confounding variables were operationally defined as (i) epilepsy classification or subtype, (ii) lateralisation, (iii) seizure status, (iv) medication status, (v) baseline cognitive function and (vi) pre- or postsurgery status, as these epilepsy factors may affect the efficacy of memory interventions. Item five was allotted values of 0, 1 or 2, where 0 would be given when <3 of the pre-determined principle confounding variables were reported, 1 where ≥3 were reported, and 2 points where all six were reported. Item 27 was modified to represent values of either 0 or 1. The Single-Case Experimental Design Scale (SCED: Tate et al. 2008) was used to assess the methodological rigor of single-case studies. The SCED Scale was specifically designed for the evaluation of the methodological quality of single-case study designs and n-of-1 trials. The SCED contains 11 items (scored as 1 or 0) that assess methodological quality of single-case studies against six domains of validity. The SCED scale demonstrates good content validity and excellent inter-rater reliability (Tate et al. 2008). Quality ratings were conducted by two independent reviewers (SJ and ES). Inter-rater reliability indices were κ = .758, p < .001 and κ = .530, p < .001 for the Downs and Black checklist and SCED scale, respectively. Discrepancies between the ratings were resolved collaboratively. Downs and Black score ranges were arbitrarily grouped into the following four overall quality indicators: Excellent (0.90 to 1), good (0.71 to 0.89), fair (.54 to .70), and poor (less than .53).

Neuropsychol Rev Table 1

Databases accessed and corresponding search terms

Database and search terms

PsycINFO via OvidSP host 1. Memory AND epilepsy AND rehabilitation

2. Memory AND epilepsy AND training 3. Memory AND epilepsy AND remediation

Medline via OvidSP (1950-present) 1. Memory AND epilepsy AND rehabilitation

2. Memory AND epilepsy AND training

3. Memory AND epilepsy AND remediation

PsychBite 1. Memory AND epilepsy AND rehabilitation

2. Memory AND epilepsy AND training

3. Memory AND epilepsy AND remediation

Limitations specified

Number of papers found

Number of papers excluded

Papers included

Field: Key concepts English Language Peer-reviewed Humans Field: Key concepts English Language Peer-reviewed Field: Key concepts English Language Peer-reviewed Humans

n=3

1

1. Koorenhof et al. (2012) 2. Helmstaedter et al. (2008)

n=6

4

1. Radford et al. (2011) 2. Caller et al. (2015)

n=2

1

1. Anuradha et al. (2014)

n = 34

32

1. Gess et al. (2014) 2. Gupta and Naorem (2003)

n = 29

29

n=3

3

n=8

8

n=8

8

n=3

3

Keywords Include all subheadings Humans Peer-reviewed Humans English Language Keywords Include all subheadings Humans Peer-reviewed Humans English Language Keywords Include all subheadings Humans Peer-reviewed Humans English Language Keywords Neurological group: epilepsy/seizures/convulsions English Language Keywords Neurological group: epilepsy/seizures/convulsions English Language Keywords Neurological group: epilepsy/seizures/convulsions English Language

Citation Tracking 1. Schefft et al. (2008) 2. Mosca et al. (2014) 3. Jones (1974) 4. Bresson et al. (2007) 5. Kerr and Blackwell (2015)

Results Study Selection Figure 1 provides a flow chart depicting the study selection process. Inter-rater reliability indices for titles and abstracts indicated moderate agreement, (κ = .56, p < .001). The initial search yielded a total of 95 citations, 71 of which were duplicate titles. Four relevant articles fulfilling the study selection criteria were subsequently identified from reviewing manuscript reference lists. After applying the study selection criteria, a total of 12 full text articles were reviewed. The main reasons for exclusion at this stage were studies that pooled epilepsy outcomes with other neurological groups and

utilisation of neither cognitive nor behavioural strategies (Appendix-3). Twelve studies were ultimately included for review. Eleven utilised adult patients while one utilised a peadiatric sample.

Study Characteristics Details of the studies included in this review are presented in Table 2. Of the 12 studies, nine were group studies and three were single-case studies. All studies were prospective. The majority of group studies had a pre- and post-measurement study design (n = 6), two studies involved a randomised controlled trial and one study utilised a waitlist cross-over design (Table 3).

Neuropsychol Rev Fig. 1 PRISMA (Preferred Reporting Items for Systematic Reviews and Meta-Analyses) flow diagram depicting the study search and selection process

Follow-up times ranged from 4 to 12 weeks, with 12 weeks being the most commonly employed follow-up interval. Group studies involved a total of 549 participants. Sample sizes ranged from 30 to 112 (Anuradha et al. 2013; Helmstaedter and Elger 2009, repsectively) with mean sample size of 61 (SD = 28.23). The mean ages of patients ranged from 10.5 to 45.8, with the majority of patients being in their 30s (Mode = 36). Inspection of epilepsy-related factors indicated that six group studies included patients diagnosed with TLE, either pre-surgery only (Bresson et al. 2007), post-surgery only (Helmstaedter et al. 2008), pre- and post-surgery (Jones 1974; Koorenhof et al. 2012; Radford et al. 2011), or of unspecified surgical status (Schefft et al. 2008). Four group studies did not specify the type of epilepsy (Anuradha et al. 2013; Caller et al. 2015; Kerr and Blackwell 2015). Other types of epilepsy syndromes included were amnesic syndrome (bilateral mesial temporal: Jones 1974), frontal lobe epilepsy (Radford et al. 2011; Schefft et al. 2008), extratemporal (Radford et al. 2011), parietal (Radford et al. 2011), thalamic (Radford et al. 2011), and psychogenic non-epileptic seizures (Schefft et al. 2008). Eight of the nine group studies reported other epilepsyrelated variables, such as side of seizure focus, seizure frequency or status, surgical status, medication, age at onset, and duration of illness (Bresson et al. 2007; Caller et al.

2015; Helmstaedter et al. 2008; Jones 1974; Kerr and Blackwell 2015; Koorenhof et al. 2012; Radford et al. 2011; Schefft et al. 2008).

Methodological Quality Methodological quality ratings of group studies are presented in Appendix-1. Overall methodological quality scores on the modified version of the Downs and Black checklist from 36% (poor, n = 3) to 72% (good, n = 1). A further three papers were considered to be of Bfair^ quality (56–68%). A review of scores obtained across the scale items identified several common limitations of the studies. No study reported any of the following items (i) an attempt to blind study participants to the intervention (item 14), (ii) an attempt to blind those measuring the main outcomes of the intervention (item 15), and (iii) whether randomised interventions were concealed both from patients and health-care staff until completion of recruitment (item 24). Three studies employed a randomised intervention (item 23). In contrast, most studies described or identified clearly the principal confounders (n = 7, item 5), however, these confounding variables were only partially reported by the majority of studies (n = 5). Methodological quality ratings of single-case studies are provided in Appendix-2. The three single-case studies also varied in quality, with scores on the Single-

Sample (n, total)

Design

Overview of group studies included in this review Recruitment source Source not specified.

Mean age (years) LTLE = 36.2; RTLE =27.2; BMT = 46.0; HC1 = 26.6; HC2 = 27.6

Intervention

Jones (1974)

Total n = 76 TLE, n = 36 (LTLE, n = 18; RTLE, n = 18); Amnesic syndrome (bilateral mesial temporal, n = 2); HC, n = 36 (2 groups: 1 underwent training and 1 did not; n = 18 each)

Mixed factorial design: within subjects (pre-post training) and between subjects (LTLE, RTLE, HC)

Aim: to improve the verbal memory of patients with LTL lesions in a paired-associate test, using visual imagery as a mnemonic aid. Computerised training: nil used. Internal strategies: mnemonic imagery (abstract and concrete words) External strategies: pictures to facilitate imagery encoding. Other: nil reported. Bresson et al. (2007) Total n = 46 Mixed factorial design: within subjects LTLE = 31; Referrals for evaluation for epilepsy Aim: to investigate the compensatory impact of TLE, n = 30 (LTLE, n = 14; (pre-post training) and between RTL = 35; surgery (source/meth-od not cognitive aids on TLE surgical candidates with RTLE, n = 16); subjects (LTLE, RTLE, HC) HC =32 specified) verbal memory deficits. HC (n = 16) Computerised training: nil used. Internal strategies: depth of processing, elaboration, retrieval. External strategies: nil used. Other: nil reported. Schefft et al. (2008) Total n = 87 Mixed factorial design: within subjects Epileptic seizures = 38.1; A large university hospital (name Aim: to compare the efficacy of a self-generation LTLE, n = 25; (pre-post training) and between PNES = 29.5 unspecified). encoding procedure vs. didactic presentation in RTLE, n = 29; subjects (LTLE, RTLE, FLE, PNES) facilitating encoding/retrieval of verbal FLE, n = 8; memories in individuals with seizure disorders. PNES, n = 25 Computerised training: nil used. Internal strategies: self-generation learning condition. External Strategies: external aids such as cued recall and recognition. Other: nil reported. Helmstaedter et al. (2008) Total n = 112 Mixed factorial design: within subjects No rehab = 36.4; Aim: investigate the short-term effects of University of Bonn Epilepsy (pre-post training) and between cognitive rehabilitation on memory outcomes Rehab = 36.2 Department; the University of TLE, n = 112, subjects (LTLE, RTLE, Intervention after TLE surgery. Freiburg Epilepsy Department. (LTLE, n = 57, RTLE, n = 55) group) Computerised training: Computer-based cognitive Subdivided into two groups: exercises. - No Rehabilitation, n = 57 Internal strategies: mnemonic strategies - Rehabilitation, n = 55 External Strategies: nil reported. Other: Metacognitive therapy, psychoeducation, exercises for attention and problem solving, lifestyle aspects, occupational therapy, counseling, sociotherapy, group exercises. Waitlist cross over. ET = 39.7;LT = 47.7 Neuropsychol-ogy Unit at Royal Prince Aim: to determine the effectiveness of a Radford et al. (2011) Total n = 31 Alfred Hospital; direct referrals; group-based strategy training program for History of seizure disorder, community support groups patients with epilepsy who had memory divided into two groups: (stroke/epilep-sy) complaints. - Early Treatment, n = 17 Computerised training: nil used - Late Treatment, n = 14 Internal strategies: story rehearsal, method of loci, clustering. External Strategies: diaries, electronic device reminders. Other: Memory psychoeducation, life-style components, group exercises, homework. Controls: staff employed,people visiting Aim: To assess the short term impact of a memory Mixed factorial design: within subjects LTLE = 36.3; Koorenhof et al. (2012) Total n = 42 rehabilitation programme on verbal memory HC = 43.4 the headquarters of a national (pre-post training) and between 20 LTLE surgical patients; test performance and subjective ratings of epilepsy charity. subjects (pre−/post-surgical status, 22 HC memory in everyday life.

Citation

Table 2

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Delivery: unspecified No. of sessions (length)/ frequency not specified

Bresson et al. (2007)

Intervention

Objective: Verbal memory. Lists of paired- associate words lists containing pairs of concrete and pairs of abstract words - recall of paired associates (i) immediate (trials 1–3) and (ii) delayed (2 h) Subjective: NA Follow-up: NA Objective: Verbal memory. Lists of single words or word pairs that required either shallow (phonetic) processing or deep (semantic) processing (free and cued recall of words). Subjective: NA

Cognitive strategies differentially benefited patients with TLE. Patients with LTLE benefited from deep processing, while patients with RTLE benefited from being provided with retrieval cues. Transfer was not examined.

Improvements found in recall of concrete (but not abstract) word pair associates in all groups. No effect of group was found. Transfer was not examined.

Overall findings and transfer of the effects of the treatments

Computerised training: Lumosity Internal strategies: story rehearsal, method of loci, mental elaboration, mnemonic strategies. External Strategies: calendars, watch/phone alarms, pill dispensers. Other: psychoeducation, behavioural tasks, homework. BTwo major hospitals^, names not Aim: to develop and assess the efficacy of specified. cognitive remedial measures for patients with epilepsy. Computerised training: nil used. Internal strategies: word associations. External Strategies: nil used. Other: nature unspecified. Aim: to investigate the efficacy of a WM The Hospital for Sick Children intervention program in improving cognitive (Toronto, Canada); referrals from functions in children with symptomatic local epilepsy associations epilepsy. Computerised training: CogMed BRoboMemo^ Internal strategies: nil used. External Strategies: nil used. Other: nil reported. Dartmouth Hitchcock Epilepsy Center Aim: To assess the feasibility of a (DHEC) at the Dartmouth-Hitchcock self-management intervention targeting Medical Center (DHMC), (level 4 cognitive dysfunction to improve quality of life epilepsy center) and reduce memory-related disability in adults with epilepsy. Computerised training: Nintendo DS® handheld console and the Brain Age© program. Internal strategies: problem-solving therapy (PST) External Strategies: day planner. Other: memory tools, relaxation techniques. HOBSCOTCH comprised internal, external and other strategies. HOBSCOTCH Plus included HOBSCOTCH and Brain Age program.

Recruitment source

Outcomes (objective and subjective) and length of follow up

45.8

Mixed factorial design: within subjects (pre-post training) and between subjects (Epilepsy, HC, Intervention (i.e HOBSCOTCH/ HOBSCOTCH Plus)

Delivery: group No. of sessions (length)/ frequency: 3 x exposures, subsequent delayed recall delivered two hours later.

Total n = 48 Intervention: Epilepsy, not otherwise specified treatment group: 13 HC treatment group: 14 Other: unclear

Caller et al. (2015)

Waitlist = 10.6; Interven-tion = 11.1

Epilepsy = 31.3; HC = 30.2

Mean age (years)

RCT; waitlist controlled

Jones (1974)

Total n = 77 Children with symptomatic epilepsy, not otherwise specified.

Kerr and Blackwell (2015)

Mixed factorial design: (pre-post training) and between subjects (Epilepsy, HC)

Intervention: mode of delivery (group or individual) and duration

Total n = 30 Epilepsy, not otherwise specified: 15 HC: 15

Anuradha et al. (2014)

half HC and LFE undertook computerised brain training)

Design

Citation

Sample (n, total)

Citation

Table 2 (continued)

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Intervention: mode of delivery (group or individual) and duration

Delivery: unspecified No. of sessions (length)/ frequency 3× practice trials.

Delivery: Both group and individual No. of sessions (length)/ frequency: Commenced three to 15 days post-surgery. Mean duration = 29.3 days.

Delivery: Group delivery No, of sessions (length)/ frequency: 6 x weekly 2 h sessions

Delivery: Both group and individual No. of sessions (length)/ frequency: 4 h over 3 x sessions +40 free Lumosity sessions.

Delivery: unspecified No. of sessions (length)/ frequency 30× sessions

Citation

Schefft et al. (2008)

Helmstaedter et al. (2008)

Radford et al. (2011)

Koorenhof et al. (2012)

Anuradha et al. (2014)

Table 2 (continued)

Objective: Verbal memory. Rey Auditory Verbal Learning Test; total learning and delayed recall scores, Prospective memory. Royal Prince Alfred Prospective Memory Test; total score, Appointment Memory, Comprehensive Assessment of Prospective Memory. Subjective: Everyday Memory Questionnaire, self-reported number of internal/mental and external aid strategies used. Follow-up: 3 assessments × 12 week intervals. Objective: Verbal memory. BIRT Memory Information Processing Battery: Story Recall (free recall and delayed recall),List Learning subtests (total number of words recalled from the five trials), parallel versions. Lumosity progress (Brain Performance Index.), Subjective: Everyday Memory Failures Questionnaire; Hospital Anxiety and Depression Scale Follow-up: 4 weeks Objective: Verbal & visual memory. Lists of words and common objects; immediate and delayed recall. Attention/speed of processing. Number Connection Tasks, Digit Symbol Substitution Task, Executive. Category Fluency, n-back task, Tower of London, Wisconsin Card Sorting test, Stroop task, Subjective: nil reported Follow-up: 45 days

Follow-up: NA Objective: Verbal memory. 100 verbal paired associates categorised into two 50-word lists (associate, category, synonym, rhyme and opposite pairs) presented in didactic or self-generate condition, (free recall, cued recall and recognition) Subjective: NA Follow-up: NA Objective: Verbal memory. Verbaler Lern und Merkfähigkeitstest; verbal learning, verbal memory, recognition. Visual memory. Diagnostikum für Zerebralschädigung,; last learning trial. Psychomotor speed/attention. Letter cancellation test; total number correct less errors, reassessed with parallel forms. Subjective: NA Follow-up: 12 weeks

Outcomes (objective and subjective) and length of follow up

Verbal learning and recognition (i) remained stable or improved in patients who received cognitive rehabilitation, but (ii) decreased in patients who did not receive rehabilitation post-surgery. Improvements were observed on all verbal memory outcomes in post-surgical patients with RTLE, but not in patients with LTLE patients whose scores decreased post-surgically, irrespective of cognitive intervention. No significant change in visual memory in relation to either surgery or treatment. Attention improved in patients who did not receive rehabilitation, especially after right lesionectomy Transfer was not reported Improvements attributable to training were found in verbal learning, delayed recall and appointment memory. These findings were corroborated by self- reported prospective memory (EMQ; CAPM). Participants also reported an increase in repertoire of internal and external compensatory strategies. Transfer was evident in the self-reported increase in strategy use and improved prospective memory in day to day life. Maintenance of strategy use was also found for verbal anterograde memory (learning and delayed recall: RAVLT) at a 3-month follow-up. Improvements in verbal memory were observed in LTLE and HC groups. Brain Performance Index improved in LTLE and HC groups. Increased training (i.e. number of sessions completed) were associated with greater gains. The relationship between changes in the Lumosity Brain Performance Index and memory outcomes was not significant for the LTLE group. Outcomes were independent of surgical status. Transfer was evident on improved patients’ ratings of their own memory in everyday life. Subjective improvements were reported in verbal and visual memory. Transfer was not reported

The self-generate encoding strategy > didactic training in patients with (i) LTLE & RTLE in free recall and cued recall and (ii) LTLE & RTLE in recognition, but LTLE showed greater benefits than LTLE for recognition. . Transfer was not examined.

Overall findings and transfer of the effects of the treatments

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Delivery: Group No, of sessions (length)/ frequency: 5 × 30-45 min WM training sessions per week. The programme ran over 5–7 consecutive weeks in total.

Delivery: Group No. of sessions (length)/ frequency HOBSCOTCH: 8 × 45 to 60-min sessions HOBSCOTCH Plus additional Brain Age: 20–40 min per day, 5 days per week for 8 weeks

Kerr and Blackwell (2015)

Caller et al. (2015)

Objective: Working memory. Working Memory Test Battery for Children: Digit Recall Forward, Digit Recall Backward, Listening Recall, Counting Recall; Wechsler Intelligence Scale for Children IV – Integrated: Spatial Span Forward, Spatial Span Backward, Visual Digit Span. Attention. Test of Everyday Attention for Children: Creature Counting (accuracy) Score! Attentional Capacity Test; Continuous Performance Test II, omissions, variability of standard error, Score! Subjective: The Conners’ ADHD/DSM-IV Scales of the Conners Rating Scales-Revised Follow-up: 7 weeks Objective: Completion rate, compliance with computerized programme (downloading Brain Age profile). Subjective: focus group adherence to treatment (checklist) Follow-up: 8 weeks

Outcomes (objective and subjective) and length of follow up

Completion rate: 4/6 HOBSCOTCH and 6/7 HOBSCOTCH plus participants completed the study. All 10 patients completed 8 HOBSCOTCH sessions. Of the 6 patients whose programme also included computerized training 3 used the programme at the minimum requirement for 40 days. Subjective data indicated that participants were satisfied with the HOBSCOTCH intervention (especially memory tools, relaxation technique and day planner). Participants reported mixed feelings about the Brain Age program; 2 reported difficulties using the device, one became anxious because of perceived time pressure and one felt worse about her memory on participating in the Brain Aging program. No quantitative memory outcome data was reported. Transfer effects were not reported.

A significant treatment effect was found for the intervention group in visual attention span, auditory WM, and visual-verbal WM. Near transfer effects were found for untrained tasks of visual attention span, auditory working memory, and visual-verbal working memory. However, no evidence of far transfer was found.

Overall findings and transfer of the effects of the treatments

ACT, Attentional Capacity Test; BMT, Bilateral Medial Temporal; CAPM, Comprehensive Assessment of Prospective Memory; CPT-II, Continuous Performance Test-II; ET Early Treatment; EMQ, Everyday Memory Questionnaire; HC, Healthy Controls; HOBSCOTCH, HOme Based Self-management and COgnitive Training CHanges lives; LT, Late Treatment; LTLE, Left Temporal Lobe Epilepsy; MMSE, Mini Mental Status Examination; PNES, Psychogenic Non- Epileptic Seizures; RCT, Randomised Controlled Trial; RTLE, Right Temporal Lobe Epilepsy; TLE, Temporal Lobe Epilepsy; TEA-Ch, Test of Everyday Attention for Children; TMT, Trail Making Test; WAIS, Wechsler Adult Intelligence Scale; WMTB-C, WM Test Battery for Children

Intervention: mode of delivery (group or individual) and duration

Citation

Table 2 (continued)

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n = 1LTL (dysnomia)

Gess et al. (2014)

52

Nil Specified

Nil Specified

Nil Specified

Aim: to compare implicit (errorless Not clearly reported learning) and explicit (rote rehearsal) approaches to retraining face–name associations in a patient who was status post–amygdalo-hippocampectomy for refractory complex partial seizures Computerised training: nil used. Internal strategies: implicit (errorless learning), and explicit (rote rehearsal), name associations. External Strategies: nil reported.

Objective: Select tests from: Grober and Buschke test, MEM III, BEM, Verbal working memory — WAIS III, Doors test, Warrington recognition test for faces, Rey figure, Stroop, TMT, D2, verbal fluency, fMRI assessments. Subjective: everyday quality of life. Follow-up: 12 months Objective: Boston Naming test, Verbal (lists and paired associates) and visuospatial (complex figure) memory, Grandchildren’s names Subjective: N/A Follow-up: 1 week.

Objective: MMSE, Digit cancellation task, Digit span, Rivermead Behavioural Memory Test, Memory checklist, Shopping list, Verbal fluency task, TMT Subjective: interview questionnaire (memory, concentration, affect, family, time spent). Follow-up: post treatment, every 3 months for 3 years.

Intervention: Mode of Outcomes (objective and delivery and duration subjective) and length of follow up

1 h weekly × 6 weeks Aim: to assess the relative changes in the targeted skill areas after cognitive retraining in a patient with epilepsy Computerised training: nil used. Internal strategies: categorisation, chunking, imagery External Strategies: external memory aids including a diary and calendar book were encouraged. Other: supportive therapy, deep breathing relaxation exercises. A regular home intervention programme was conducted simultaneously. Aim: to demonstrate the use of a tailored 2 x session/week, for 3 months (total 12) rehabilitation program to improve visual and verbal memory abilities of non-structured material Computerised training: nil used. Internal strategies: visual mental imagery (i.e stacking method) External Strategies: Nil reported.

Intervention

Both strategies (errorless learning; rote learning) were associated with improved recall at baseline. However, the errorless learning resulted in more robust and enduring changes at a ten-minute and one week follow-up. Transfer effects were not reported.

A global improvement in functioning (including memory, attention, executive skills and emotional status) was found on completion of training (on both objective and subjective measures). The skills acquired during the training programme were found to transfer; the participant reported using learnt skills to ameliorate specific memory difficulties encountered in day to day life. The patient reported transfer of the strategies to everyday memory tasks on a one year follow-up, suggesting that gains made in treatment were maintained over time.

Overall findings and transfer of the effects of the treatments

ACT, Attentional Capacity Test; CPT-II, The Continuous Performance Test-II; D2, D2 Test of Attention; fMRI, functional Magnetic Resonance Imaging; MMSE, Mini Mental Status Examination; PNES, Psychogenic Non- Epileptic Seizures; TMT, Trail Making Test; WAIS, Wechsler Adult Intelligence Scale; WMTB-C, WM Test Battery for Children

Single Baseline, two delays.

n=1 Pre- and postLeft mesial TLE Single.

Mosca et al. (2014)

57

32 Pre- and post- multiple baseline design

n=1 Epilepsy, classification unspecified

Gupta and Naorem (2003)

Age Recruitment source

Design

Sample

Overview of single case studies included in this review

Citation

Table 3

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Case Experimental Design (SCED) Scale ranging from 4 to 7 out to 11. Inspections of ratings made against the SCED criteria indicated that all studies (i) clearly described the clinical history, (ii) operationally defined target behaviours, and (iii) conducted sufficient sampling during the treatment phase. In contrast, no study reported statistical analyses, demonstrated replicability of findings (due to insufficiently described methods) or the independence of assessors (i.e. assessors were not blinded to the treatment).

Qualitative Summary and Synthesis Techniques Used for Memory Rehabilitation in Group Studies The studies included in this review implemented a wide range of internal and external rehabilitation and compensation techniques. While three of the reviewed studies used primarily compensatory approaches to enhancing m e m o r y, f o u r s t u d i e s e m p l o y e d p r e d o m i n a n t l y restitution-oriented therapies, and three studies implemented compensation and restitution approaches simultaneously (Anuradha et al. 2013; Bresson et al. 2007; Gess et al. 2014; Gupta and Naorem 2003; Helmstaedter et al. 2008; Jones 1974; Koorenhof et al. 2012; Mosca et al. 2014; Radford et al. 2012; Schefft et al. 2008). One study used a restitution approach alone (Kerr and Blackwell 2015). This study used computerised repetitive exercises with increasing levels of difficulty d u r i n g t h e c o u r s e o f t r a i n i n g , n m e l y, C o g m e d BRoboMemo^ to enhance working memory. Another study reported qualitative data suggestive of high satisfaction with the intervention and subjective improvement in cognitive functioning in everyday life (Caller et al. 2015). In studies that used compensatory approaches to rehabilitation, internal techniques involved mnemonic strategies (i.e. mental imagery), association strategies, the method of loci, elaborative encoding repetition-clustering, staggered rehearsal, self-prompting, depth of processing, and self-generation encoding (Helmstaedter et al. 2008; Jones 1974; Koorenhof et al. 2012; Radford et al. 2011). Compensatory external techniques included cueing with visual aids (such as photographs or illustrations), calendars, diaries, and lists or notes (Radford et al. 2011; Schefft et al. 2008; Jones 1974). Use of electronic devices, such as mobile phones and alarms, was also encouraged (Koorenhof et al. 2012; Radford et al. 2011). Three of the reviewed studies employed a range of external and internal techniques simultaneously (Jones 1974; Koorenhof et al. 2012; Radford et al. 2011). In four studies, restorative

techniques were employed, namely, computerised training (Caller et al. 2015; Helmstaedter et al. 2008; Kerr and Blackwell 2015; Koorenhof et al. 2012). Helmstaedter et al. and Koorenhof et al. also employed computerized training as an adjunct to other strategies. Finally, two studies also reported incorporating psychoeducation into their rehabilitation programs (Koorenhof et al. 2012; Radford et al. 2011). Mode of delivery was reported in six studies. Four studies used group interventions (Caller et al. 2015; Jones 1974; Kerr and Blackwell 2015; Radford et al. 2011). Two studies delivered the intervention both in groups and individually (Helmstaedter et al. 2008; Koorenhof et al. 2012). The remaining four studies did not specify whether intervention was delivered individually or in a group. Six studies conducted follow-up assessment to determine maintenance of gains over time (Anuradha et al. 2013; Caller et al. 2015; Helmstaedter et al. 2008; Kerr and Blackwell 2015; Koorenhof et al. 2012; Radford et al. 2011). The length of follow-up ranged from four weeks to 36 weeks (see Table 2).

Group Study Outcomes Treatment Outcomes All nine group studies reported benefits from memory interventions. Four of the nine group studies measured memory outcomes using standardised clinical tests, including the Brain Injury Rehabilitation Trust (BIRT) Memory Information Processing Battery, Rey Auditory Verbal Learning Test, Royal Prince Alfred Prospective Memory Test, and the verbal subtests from the Wechsler Memory Scale-III (as shown in Table 2). Helmstaedter et al. (2008) used adaptations of German memory scales. Kerr and Blackwell (2015) examined improvement indices to assess outcomes from Cogmed training. Caller et al. (2015) employed HOBSCOTCH Plus cognitive training using the Brain Age© software on a Nintendo DS® handheld console. Two studies used free-recall performance on non-standardised, paired-associate lists to assess outcomes (Jones 1974; Schefft et al. 2008). Several studies also developed their own measures of memory performance. One study developed its own measure of memory, which purported to target and assess elaborative encoding, spatial encoding, temporal encoding and frequency encoding (Anuradha et al. 2013). Another study investigated Appointment Memory using incidental assessment of behaviour and performance on several to-beremembered tasks assessing memory for time-and-eventbased information (Radford et al. 2011). Verbal memory outcomes were reported in eight of the nine group studies (Anuradha et al. 2013; Bresson et al. 2007;

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Helmstaedter and Elger 2009; Jones 1974; Kerr and Blackwell 2015; Koorenhof et al. 2012; Radford et al. 2011; Schefft et al. 2008). All studies found improvements in one or more aspects of verbal memory, including (i) working memory (ii) learning of word list or word pairs or (iii) recall of newly learned information after a delay. Only two of the nine group studies reported on visual memory outcomes. While one study reported improvements in spatial encoding on a non-standardised task on which participants were presented with visual representations of common objects (Anuradha et al. 2013), another study found no changes on a revised version of a German figural design list-learning test (Helmstaedter et al. 2008). Evidence of Transfer One study examined whether gains made in training transfer to tasks that closely resemble the trained task a phenomenon known as near transfer (Kerr and Blackwell 2015). This study found significant treatment effects on untrained tasks of visual attention span, auditory working memory, and visual-verbal working memory. No other group studies explicitly examined near transfer effects. Several studies examined far transfer using rating scales. Kerr and Blackwell (2015) found no evidence of far transfer on the parental ratings of their children’s behaviour in everyday life on The Conners’ ADHD/ DSM-IV Scales of the Conners Rating Scales-Revised (Conners 1999) on completion of Cogmed training. Radford et al. (2011) used several indicators of far transfer, including participants’ subjective rating of Bstrategy use,^ prospective memory ratings (participants and significant others), and an everyday memory questionnaire (participants and significant others). The study found significant improvements in participants’ ratings of strategy use and prospective memory, but not an improved overall rating of everyday memory post-training. Significant others’ subjective ratings of the participants’ memory also improved post-training. Koorenhoof et al. (2012) also observed a significant improvement on patients’ ratings of their own memory on everyday memory questionnaires completed by participants themselves post-training. One study used an objective measure to assess memory functioning in day to day life, an incidental assessment of behaviour (Appointment Memory), which contained items assessing the capacity to remember time or place of appointments during a phone call that occurred a day after training, arriving to appointment on time, and remembering to bring specified items to the appointment (i.e., mailed questionnaires: Radford et al. 2011). Appointment memory was improved on completion of training relative to pre-training. Two of the studies that included tasks or strategies that were expected to facilitate transfer of skills into everyday life

did not report on transfer (Anuradha et al. 2013; Helmstaedter et al. 2008). Maintenance Over Time Radford et al. (2011) found that gains on completion of training were maintained at a three month follow-up on objective measures of verbal anterograde memory (learning and delayed recall), but not on a measure of incidental behaviour that required memory (Appointment Memory). Training related gains on self-report measure of day-to-day prospective memory were maintained over time. Other group studies included only one short-term follow-up assessment (M = 8.49 weeks, SD = 3.51) in their design, precluding inspection of maintenance over time. Koorenhof et al. (2012) indicated that further follow-up was planned, but no subsequent studies reporting on subsequent follow-ups have been published at the time of this review. Epilepsy-Related and Demographic Factors Associated with Rehabilitation Effectiveness Six of the nine group studies specifically investigated or commented on relations between side of epilepsy focus and the effect on strategy efficacy. Jones (1974) found improvements in recall of concrete, but not abstract, word-pair associates in all groups undergoing the training, which involved using visual imagery to enhance learning and recall. While the LTLE improved as much as the RTLE and healthy control groups, the LTLE obtained significantly lower scores relative to the RTLE and controls pre- and post-training. Given that no effect of group was found, it is not possible to make inferences regarding the impact of side of seizure focus on gains made in training. Similarly, Radford et al. (2011) found no impact of lateralisation of seizure focus on outcome of memory rehabilitation. Schefft et al. (2008) offered partial support for the differential impact of seizure focus on training outcomes. When taught to deploy self-generated strategies to learn verbal pairs, it was shown that LTLE patients experienced more benefit from this strategy training than did patients with RTLE or FLE in recognition memory, although not for free recall or cued recall. There was no evidence of any group benefiting more from the didactic learning condition. Bresson et al. (2007) found that controls as well as patients with epilepsy improved when provided with compensatory memory strategies (i.e., depth of processing, elaboration, and retrieval). Nevertheless, this study also documented a differential impact of compensatory strategies on recall of verbal material in patients with

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LTLE and RTLE. For example, while patients with LTLE benefited from deep processing, patients with RTLE benefited from retrieval cues. For phonetic processing, patients with LTLE did not benefit from compensatory memory strategies, while patients with RTLE did when information was elaborated. For semantic processing, patients with LTLE improved on provision of semantic information and patients with RTLE on cued recall. Helmstaedter et al. (2008) reported differential benefits of a memory rehabilitation program encompassing psychoeducation, specific cognitive exercises and computerbased training for the two epilepsy groups. In patients with RTLE, this training appeared to attenuate the verbal memory impairments engendered by surgical intervention. In contrast, LTLE patients benefitted less from the post-surgical intervention, indicating that surgery may result in too great a loss of cognitive capacity in this patient group for them to cope with the demands of rehabilitation. Importantly, the relative risk of decline in verbal learning abilities was approximately 3.4 times higher for patients who did not receive any rehabilitative training than for those who did. No improvements to visual memory were evident in either group. Conversely, Koorenhof et al. (2012) investigated the effectiveness of a short-term rehabilitation program for patients with LTLE and controls utilising both internal (imagery, the method of loci, the story method) and external (mobile phones and computers) memory rehabilitation techniques. Verbal memory improvement was observed in both groups, although there was no effect of group. Patients with LTLE patients demonstrated gains irrespective of surgical status. With respect to epilepsy medication, polytherapy was associated with worse rehabilitation outcomes relative to monotherapy in the only study that examined the impact of anti-epilepsy medication on rehabilitation outcomes (Radford et al. 2011). Timing of intervention (pre- or post-surgery) rendered mixed findings. Koorenhof et al. (2012) found that in patients with LTLE, benefits from training were observed irrespective of surgical status. In contrast, Helmstaedter et al. (2008) found that patients with LTLE conferred fewer gains from a post-surgical memory intervention relative to patients with RTLE. Lastly, Radford et al. (2011) found no impact of surgery status on training outcome. However, these results were obtained in the context of a comparatively small number of patients who had undergone a resection. Given these mixed findings, whether pre-operative intervention carries greater benefit in offsetting surgical effects remains uncertain. Two studies examined the impact of background variables on rehabilitation outcomes. Younger age and lower levels of education were associated with greater bene f it s i n a d u l t s w h o at t en d ed a g ro u p m em ory

rehabilitation programme (Radford et al. 2011). In children, Kerr and Blackwell (2015) failed to identify any relations between demographic or clinical variables (i.e. sex, IQ, AEDs, age of epilepsy onset, duration of epilepsy, seizure frequency, and topography of the epileptogenic area) and outcomes following Cogmed training.

Single-Case Study Outcomes All three single-case studies reported improvements in patients’ memory upon completion of training. Nevertheless, none of the studies employed statistical methods to assess the significance of memory improvements. The single-case studies included in this review explored the utility of different rehabilitation approaches that were focused on remediation of difficulties in everyday life. The first study involved a 52 year old patient with a history of traumatic brain injury following which she developed complex partial seizures and underwent amygdalohippocampectomy (Gess et al. 2014). She had multiple memory deficits in everyday life, including difficulties retrieving the names of her six grandchildren, which she reported to have developed post-surgery and found particularly distressing. Two different techniques were used to teach her the names of her grandchildren. The names were randomly divided into one of two lists. One list was trained using rote learning. Another list was trained using errorless learning. Both techniques resulted in 100% accuracy on completion of training. At follow-ups of 10-min and 1 week, recall was maintained at 100% for names acquired through errorless learning, but returned to baseline (1/3) for the rote learned names. The second study included a 57 year old patient who underwent left temporal lobe surgery that spared the hippocampus, to treat epilepsy (Mosca et al. 2014). The patient developed verbal memory problems postsurgery, including word finding difficulties in conversations, and forgetting verbal information at work. Neuropsychological assessment was suggestive of persistent difficulties with encoding and retrieval, but not storage, of unstructured verbal materials, and low average memory for structured verbal material. Visual memory was high average to superior. Patient rehabilitation relied on preserved cognitive skills. It involved visual mental imagery that used the stacking method, as it enables visualisation and structuring of unstructured verbal materials. Memory and fMRI assessments were conducted before, and on completion, of the training. Posttraining assessment revealed an increase in the verbal memory test score and a shift in activation from the anterior to the posterior brain regions was observed.

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Moreover, the patient reported improvement in everyday quality of life. On a one year follow-up, the patient reported continuing to use mental imagery in daily living. The third study concerned a 32 year old patient with an eight year history of epilepsy during which time he noticed a slow decline in his concentration and memory (Gupta and Naorem 2003). These concentration and memory problems adversely impacted his social life and work performance. He underwent attention and memory training that included several techniques aimed at improving memory, including categorisation, chunking and imagery. Pre- to post-training assessments showed improvements on scores obtained on memory tests and on an everyday memory checklist. Furthermore, improvements were also documented on tests of executive skills, emotional status and independence in everyday activities. Follow-up evaluations were conducted every three months for a period of three years.

Discussion Principal Findings We undertook a systematic review of the literature on the effectiveness of memory rehabilitation in patients with epilepsy and evaluated this literature for the level of methodological rigor, techniques, and modes of delivery used for memory rehabilitation. In addition, we evaluated the effectiveness of memory rehabilitation with respect to training-related gains, transfer or generalization, and maintenance of gains made in rehabilitation. Finally, we explored relations between epilepsy variables and outcomes. Twelve studies were identified, with only one of the twelve studies including children. The identified studies used either group or single-case designs. The studies employed a wide range of compensatory and restorative approaches alone or in combination. This heterogeneity of study designs and techniques used for memory rehabilitation precluded the conducting of a meta-analysis. Only one group study was deemed to be of a ‘good’ quality. While keeping in mind limited quality and heterogeneity of the reviewed studies, we note that an overarching preliminary finding across all group and single-case studies is of patients with epilepsy gaining some benefits from memory rehabilitation on completion of training. It is unknown whether these gains were maintained, as the longest follow-up period was 3 months. Studies that examined whether epilepsy factors were related to the gains made in rehabilitation most commonly examined the impact of the laterality of epilepsy

focus and surgical status, while the impact of other epilepsy and patient factors remained largely neglected. With respect to the laterality of seizure focus, some studies provided preliminary evidence of differential efficacy of specific compensatory strategies in relation to the side of TLE (Bresson et al. 2007; Schefft et al. 2008; Helmstaedter et al. 2008). Other studies found no evidence of the side of epilepsy focus having an impact on outcomes of memory rehabilitation (Jones 1974; Radford et al. 2011). In these later studies patients were taught a range of strategies and could selfselect strategies. It is not known whether the laterality of epilepsy focus impacted the selection of strategies. Hence, patients could use different strategies to achieve the same benefits on completion of rehabilitation. Epilepsy surgery could compromise patients’ cognitive reserve and consequently limit potential benefits to be gained from memory rehabilitation. Two studies that delivered memory rehabilitation to patients with epilepsy, irrespective of the surgical treatment, found no evidence of surgical status impacting outcomes of rehabilitation (Koorenhof et al. 2012; Radford et al. 2011). One study examined whether provision of memory training post-surgery improves memory outcomes. While one group of patients underwent memory rehabilitation post-surgery, another group did not. On followup, verbal memory scores of patients who did not undergo memory rehabilitation post-surgery were significantly below their pre-surgical scores. In contrast, verbal memory scores of patients who underwent memory rehabilitation post-surgery were comparable to their presurgical scores. Taken together, these findings suggest that Brehabilitation counteracted verbal memory decline^ (Helmstaedter et al. 2008, p. 408). Nevertheless, the patients who underwent left temporal lobectomy benefited less than patients who underwent right temporal lobectomy. We note that in this last study, the rehabilitation program was implemented during the early stages of recovery, 3 to 15 days post-surgery and was completed within a month. It is possible that such an early implementation and rapid completion of memory rehabilitation may not have been optimal for patients who underwent left temporal lobectomy. The ultimate aim of memory rehabilitation is to improve everyday functioning. Thus, it is important to determine whether skills gained in memory rehabilitation transfer to functional gains in everyday life and are maintained over time. Single-case and group studies differed with respect to examination of transfer effects. All three single-case studies were primarily motivated by clearly described, specific memory deficits that interfered with daily living of participants involved in the studies. All single-case studies developed theoretically

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driven interventions and examined whether interventions resulted in meaningful functional gains. Conversely, group studies provide little information about functional difficulties patients with memory deficits experienced prior to the training. Some rehabilitation programs actively promoted transfer of skills learned in rehabilitation to everyday life by including tailored homework tasks (Radford et al. 2011) and by training specific everyday life skills (Anuradha et al. 2013). Evidence of far-transfer and reduction in memory-related disability in daily life is extremely limited and relies on self-report rather than on objective evidence of transfer.

Limitations of this Review Our review is limited in scope for two main reasons. Firstly, we included only studies published in the English language. Secondly, we included only studies published in peer reviewed journals, excluding abstracts and dissertations, which may have produced more data. This second limitation, however, can also be viewed as a strength, as all included studies have undergone a rigorous peer review process, which is likely to have resulted in the inclusion of higher quality studies in this review. With respect to assessment of single-case studies methodological quality, this review used the SCED scale, which was considered to be Bthe only psychometrically validated tool for assessing the rigor of SCED methodology^ (Smith 2012, p. 512). Recently, however, the Equator-SCRIBE scale (Tate et al. 2017) was commissioned to cater for the broader range of singlecase experimental designs used in the behavioural sciences. While a useful addition to the literature, there is significant overlap between the two scales. Our review is also limited by the small quantity and heterogeneity of the published studies reporting on memory rehabilitation in patients with epilepsy. Inclusion of both group and case studies increases the heterogeneity of the review. Nevertheless, inclusion of both group and case studies offers a richer account of approaches to memory rehabilitation and strategies that have demonstrated efficacy in a very understudied field. No study involved a randomized, controlled design, which represents a significant limitation of studies published to date and limits the strength of conclusions that could be drawn from the review. Only one study employed a manualised treatment program (Radford et al. 2011), which allows for replication, independent evaluation of the findings and utilisation of this memory rehabilitation in clinical settings. Many studies omitted reporting important details, such as the types of epilepsy, limiting the extent to which findings could be

replicated, generalized and utilised in clinical practice. The research is largely limited to adults with TLE.

Directions for Future Research Our review highlights the disparity between a high clinical need for memory rehabilitation, contrasted against a limited and weak level of evidence for the efficacy of memory rehabilitation in patients with epilepsy, despite memory rehabilitation being overwhelmingly advocated in the field (Anuradha et al. 2013; Bresson et al. 2007; Gess et al. 2014; Gupta and Naorem 2003; Helmstaedter et al. 2008; Jones 1974; Kerr and Blackwell 2015; Koorenhof et al. 2012; Mosca et al. 2014; Ponds and Hendriks 2006; Radford et al. 2011; Schefft et al. 2008; Wedlund et al. 2013). While the weak level of evidence prevents us from drawing explicit recommendations for the implementation of specific memory rehabilitation programs, our study identifies the shortcomings of research conducted to date and provides recommendations for future research accordingly. First, future studies should examine the effectiveness of memory rehabilitation in children with epilepsy. While only one of the twelve studies included in our review involved children, memory is often found to be impaired on neuropsychological assessments of children with epilepsy (i.e., Elliott et al. 2014; Gascoigne et al. 2012, 2014; Gonzalez et al. 2012; Nolan et al. 2004). Also, memory-related functional difficulties have been reported by parents and children themselves (Smith et al. 2006). In children, memory deficits may impede acquisition of new skills and knowledge in all aspects of their life. As such, the impact of memory impairments in children may be cumulative, resulting in an ever increasing gap between children with memory impairments and their peers. Thus, the need for memory rehabilitation studies in children with epilepsy is paramount. Second, future studies should develop memory rehabilitation programs specifically designed for children, as B…children are not small adults^ (p. 68; Smith 2010). For example, memory rehabilitation programs for children with acquired brain injury address developmental aspects (Ho et al. 2011). The program used a combination of internal (self-instruction) and external (diary) strategies. Only children whose reading skills were at or above the third grade level were deemed suitable for inclusion, as this level of reading skill development was required for children to read notes made in their diary and use training materials. In addition, the authors appreciated that the materials used in the training needed to be socially appropriate, so the children did not stand out from their peers. Hence, children could choose

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to use their school diaries or a diary purchased by the researchers during memory rehabilitation training. Finally, the authors also recognized that the training needed to be of functional significance to children. Thus, children were encouraged to talk about memory difficulties they faced in everyday life, test strategies learned in the memory rehabilitation training to overcome these difficulties and discuss outcomes and develop additional strategies, if needed. Similar developmental considerations could be used in memory rehabilitation for children with epilepsy. Third, the effectiveness of memory rehabilitation needs to be investigated in patients with epilepsy other than TLE for two main reasons. One reason is that memory difficulties represent the most common clinical concern of patients with many types of epilepsy (Blake et al. 2000; Corcoran and Thompson 1992; Vermeulen et al. 1993). Another reason is that other types of epilepsy are more prevalent than TLE. For example, while TLE accounts for approximately 9 to 24% of all epilepsies, GGE accounts for 20–40% of all epilepsies (Manford et al. 1992; Semah et al. 1998; Acton 2012). Fourth, future studies need to investigate whether gains made in memory rehabilitation relate to the type of memory deficits and strategies being taught. The studies published to date often used strategies that were expected to assist with encoding in patients who presented with difficulties in new learning and material specific memory impairments, reflecting a preoccupation of the literature with patients with TLE. In contrast, much of the impairment patients experience in daily life can be attributed to difficulties with retrieval (Ponds and Hendriks 2006). As such, more attention should be paid to facilitating patients in performing systematic memory searches. In addition, rehabilitation for more recently described types of memory impairments, such as impaired autobiographical memory and accelerated long-term forgetting is missing, apart from one single-case study on rehabilitation of accelerated longterm forgetting (Jansari et al. 2010). Fifth, further research should investigate individual differences in response to memory rehabilitation in patients with epilepsy. This may facilitate selection of more receptive patients for memory rehabilitation, whilst also adapting memory rehabilitation interventions to patients’ individual needs. Such an approach will be beneficial for patients whilst allowing for the best utilization of scarce clinical resources. For example, Radford et al. (2011) found that young patients with epilepsy who had low levels of education and fewer depression symptoms made greater gains in a group memory rehabilitation program. Research that involved patients who completed memory rehabilitation after temporal

lobectomy indicated that patients who underwent left lobectomy benefited less from rehabilitation. These individual differences in gains made in memory rehabilitation highlight the need to develop rehabilitation programs that are indiviualised, but also reproducible and valid. Qualitative research confirms that individually tailored elements are important features of memory rehabilitation programs for patients with epilepsy (Wedlund et al. 2013). Indeed, several of the group studies reviewed herein also included individualised components (Caller et al. 2015; Helmstaedter et al. 2008; Koorenhof et al. 2012; Radford et al. 2011). Group programs can offer individual components through problem solving (i.e. tailored strategies for specific functiona l d i ff i c u l t i e s ) , t a i l o r e d h o m e w o r k t a s k s , a n d individualised training goals devised to suit the needs of individual patients. Sixth, given the individual differences in response to memory rehabilitation, experimental single-case study designs (Tate et al. 2017) may be more suitable than group studies for patients who are not receptive to group interventions, such as patients who require more intensive treatment, or who are identified as having a higher level of impairment. Single-case studies may also be more suitable for patients who present with recently identified forms of memory impairments (i.e., ALF, or impaired autobiographical memory), or with very specific functional impairments requiring the development of new memory rehabilitation approaches. In addition, there is a pressing need to examine a range of outcomes, particularly functional outcomes. This will allow researchers to establish whether gains made in memory rehabilitation extend to everyday life (far-transfer) and reduce memoryrelated disability. Research focusing on functional gains and maintenance of gains on completion of memory rehabilitation will provide crucial clinical data for clinicians and researchers working with this population. Finally, future studies should be of better methodological quality, should use theoretically driven, manualized treatments and randomized-controlled study designs. Ideally, future studies should be multicentered, as this would enable large sample sizes to be obtained in a timely manner. Such studies would enable more sophisticated statistical techniques to be employed to investigate the impact of many different factors than can potentially influence the outcomes of memory rehabilitation. In addition, such studies are likely to increase the validity and generalizability of findings.

Acknowledgments This research activity was funded by awards from: Nursing and Allied Health Scholarship and Support Scheme (NAHSSS) and the National Health and Medical Research Council PhD Scholarship.

1 1 1 1 1 1 1 1 0

1 1 1 0 1 1 1 1 0

1 1 1 0 1 1 1 1 1

1 1 2 0 1 1 2 1 0

1 1 1 1 1 1 1 1 0

1 0 1 1 1 0 1 0 0

NA NA NA NA NA NA NA NA NA

1 0 0 0 NA NA NA 1 1

9 1 1 1 1 0 0 0 1 0

0 1 1 0 1 0 1 0 0

10 11 0 0 0 0 0 1 1 0 0

12

External validity

NA NA NA NA NA NA NA NA NA

13 0 0 0 0 0 0 0 0 0

0 0 0 0 0 0 0 0 0

1 1 1 1 1 0 1 1 1

1 1 1 1 NA NA NA 1 1

14 15 16 17 1 1 1 1 1 1 1 1 NA

18

Internal validity - bias

NA NA NA NA NA NA NA NA NA

19 1 1 1 0 1 0 1 1 NA

20 1 0 1 1 1 0 0 1 1

21 0 0 0 0 0 0 0 1 1

22 0 0 1 0 0 0 0 1 1

23 0 0 0 0 0 0 0 0 0

24 0 0 1 0 1 1 1 1 0

25 1 0 0 0 NA NA NA 1 0

26

Internal validity - confounding

0 1 1 1 1 1 1 1 0

27

β

14/25 13/25 18/25 9/25 14/22 10/22 16/22 19/27 10/25

56 52 72 36 63 45 68 70 40

Sum /Max Overall quality %

Item. 1: Is the hypothesis/aim/objective of the study clearly described? 2: Are the main outcomes to be measured clearly described in the Introduction or Methods section? 3: Are the characteristics of the patients included in the study described clearly? 4: Are the interventions of interest clearly described? 5: Are the distributions of principal confounders in each group of subjects to be compared described clearly? 6: Are the main findings of the study described clearly? 7: Does the study provide estimates of the random variability in the data for the main outcomes? 8Have all important adverse events that may be a consequence of the intervention been reported? 9: Have the characteristics of patients lost to follow-up been described? 10: Have actual probability values been reported (for example, 0.035 rather than<0.05) for the main outcomes except where the probability value is less than 0.001? 11: Were the subjects asked to participate in the study representative of the entire population from which they were recruited? 12: Were those subjects who were prepared to participate representative of the entire population from which they were recruited? 13 Were the staff, places, and facilities where the patients were treated, representative of the treatment the majority of patients receive? 14: Was an attempt made to blind study subjects to the intervention they have received? 15 Was an attempt made to blind those measuring the main outcomes of the intervention?, 16: If any of the results of the study were based on ‘data dredging’, was this made clear? 17: In trials and cohort studies, do the analyses adjust for different lengths of follow-up of patients, or in case-control studies, is the time period between the intervention and outcome the same for cases and controls? 18: Were the statistical tests used to assess the main outcomes appropriate? 19: Was compliance with the intervention/s reliable? 20: Were the main outcome measures used accurate (valid and reliable)? 21: Were the patients in different groups recruited from the same population? 22: Were study subjects recruited over the same period of time? 23: Were study subjects randomised to intervention groups? 24: Was the randomised intervention assignment concealed from both patients and health care staff until recruitment was complete and irrevocable? 25: Was there adequate adjustment for confounding in the analyses from which the main findings were drawn? 16: Were losses of patients to follow-up taken into account? 17: Did the study have sufficient power to detect a clinically important effect where the probability value for a difference being due to chance is less than 5%? NA, not applicable

β = Power. Item 5 represents values of 0, 1 or 2. All other items represent values of 0 or 1

0 1 1 1 1 1 1 1 1

1 2 3 4 5 6 7 8

Reporting

Quality assessment: Downs and black checklist (Downs and Black 1998)

Koorenhof et al. (2012) Helmstaedter et al. (2008) Radford et al. (2011) Anuradha et al. (2014) Schefft et al. (2008) Jones (1974) Bresson et al. (2007) Kerr et al. (2015) Caller et al. (2015)

Study

Table 4

Appendix 1

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Appendix 2 Table 5

Quality Assessment: The Single-Case Experimental Design (SCED) Scale

Study

Criteria

Gess et al. (2014) Gupta and Naorem (2003) Mosca et al. (2014)

Total score

Overall quality

1

2

3

4

5

6

7

8

9

10

11

/11

%

1 1 1

1 1 1

0 1 1

1 0 0

1 1 1

0 1 1

0 1 0

0 0 0

0 0 0

0 0 0

0 1 1

4 7 6

36 63 54

All items represent values of 0 or 1 Item. 1: Is clinical history clearly described? 2: Are target behaviours operationally defined, precise and repeatable? 3: is the study either an A-B-A design or a multiple baseline design? 4: Was sufficient sampling conducted in the pre- treatment phase? 5: Was sufficient sampling conducted during the treatment phase? 6: Are raw data points provided? 7: Was interrater reliability established for at least one measure of target behaviour? 8: Are assessors independent? 9: Were statistical analyses carried out? 10: Were the findings replicated either across subjects, assessors or settings? 11: Was there evidence of generalisability?

Appendix 3 Table 6

Papers excluded and corresponding reasons for exclusion

Citation

Reason for exclusion

Ponds and Hendriks (2006) Compston (2008) Lantz and Sterman (1992) Sterman and Lantz (2001) Shulman and Barr (2002) Patra et al. (2014) Pearn and O’Connor (2013) Gois et al. (2011) Baxendale and Thompson (2010) Dupont (2000) Fitzgerald et al. (2010)

Non-empirical research Non-empirical research Intervention was not Cognitive/Behavioural Intervention was not Cognitive/Behavioural Non-empirical research Memory not targeted; Intervention was not Cognitive/Behavioural Non-empirical research Non-empirical research Non-empirical research Non-empirical research Non-empirical research; No epilepsy diagnosis; Memory not targeted; Intervention was not Cognitive/Behavioural Memory not targeted; Intervention was not Cognitive/Behavioural Intervention was not Cognitive/Behavioural Non-empirical research No epilepsy diagnosis; Memory not targeted; Intervention was not Cognitive/Behavioural Non-empirical research; no epilepsy diagnosis; memory not targeted; Intervention was not cognitive/behavioural Non-empirical research; memory not targeted; intervention was not cognitive/behavioural Non-empirical research Memory not targeted; Intervention was not Cognitive/Behavioural Memory not targeted No epilepsy diagnosis; Memory not targeted; Intervention was not Cognitive/Behavioural Non-empirical research No epilepsy diagnosis; Memory not targeted; Intervention was not Cognitive/Behavioural No epilepsy diagnosis; Memory not targeted; Intervention was not Cognitive/Behavioural No epilepsy diagnosis; Memory not targeted; Intervention was not Cognitive/Behavioural Non-empirical research Intervention was not Cognitive/Behavioural No epilepsy diagnosis; Memory not targeted; Intervention was not Cognitive/Behavioural Memory not targeted; Intervention was not Cognitive/Behavioural Memory not targeted; Intervention was not Cognitive/Behavioural Memory not targeted; Intervention was not Cognitive/Behavioural No epilepsy diagnosis; Memory not targeted; Intervention was not Cognitive/Behavioural No epilepsy diagnosis Memory not targeted; Intervention was not Cognitive/Behavioural Intervention was not Cognitive/Behavioural Non-empirical Research No epilepsy diagnosis; Memory not targeted; Intervention was not Cognitive/Behavioural Intervention was not Cognitive/Behavioural Memory not targeted; Intervention was not Cognitive/Behavioural

Vigliano et al. (2009) Berger et al. (2008) Jambaque (2008) Schwartz et al. (2008) Lexell et al. (2007) Au et al. (2006) Baker and Goldstein (2004) Mazzini et al. (2003) Engelberts et al. (2002) Hawley (2001) Mauri-Llerda et al. (2006) Kowalske et al. (2000) Giovagnoli et al. (1997) Ogden et al. (1997) Emilien and Waltregny (1996) Corcoran and Thompson (1993) Schwab et al. (1993) Dikmen and Morgan (1980) Alekseeva (1979) Utin (1977) Moroni et al. (2014) Løhaugen, et al. (2014) Wang et al. (2014) Grewe et al. (2014) Pearn and O’Connor (2013) Urbain et al. (2013) Grewe et al. (2013) Deak et al. (2011)

Neuropsychol Rev Table 6 (continued) Citation

Reason for exclusion

Surmeli and Ertem (2010) Barkas et al. (2010) Gunduz et al. (2009) Fournier et al. (2008) Edin et al. (2007) Hoppe et al. (2007) Heinrich et al. (2007) Sindou and Guenot (2003) Giovagnoli and Avanzini (2000) Grafman and Wassermann (1999) Oxbury et al. (1997) Daum et al. (1993) Laurent and Arzimanoglou (2006) Chaix et al. (2006) Thaut et al. (2009). Thornton (2000). Todd and Barrow (2008) Lawson and Rice (1989)

No epilepsy diagnosis; Intervention was not Cognitive/Behavioural Memory not targeted; Intervention was not Cognitive/Behavioural No epilepsy diagnosis; Memory not targeted; Intervention was not Cognitive/Behavioural Memory not targeted; Intervention was not Cognitive/Behavioural Non-empirical Research;Intervention was not Cognitive/Behavioural Non-empirical Research Intervention was not Cognitive/Behavioural Non-empirical Research Memory not targeted; Intervention was not Cognitive/Behavioural Non-empirical Research Memory not targeted; Intervention was not Cognitive/Behavioural Memory not targeted; Intervention was not Cognitive/Behavioural No epilepsy diagnosis; Memory not targeted; Intervention was not Cognitive/Behavioural Memory not targeted; Intervention was not Cognitive/Behavioural No epilepsy diagnosis; Memory not targeted; No epilepsy diagnosis; Intervention was not Cognitive/Behavioural No epilepsy diagnosis; Intervention was not Cognitive/Behavioural No epilepsy diagnosis;

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