Abstract
There is a relevant risk of psychosocial as well as cognitive impairments in epilepsy patients with resective surgery in the left temporal lobe. Surgery in the speech-dominant hemisphere can be associated with deterioration of speech related functions including verbal memory. There are only limited studies addressing the impact of occupational therapy in postoperative rehabilitation of epilepsy patients.Method: In this study, a mixed-methods design based on the grounded theory concept was administered. Seven patients with left temporal lobe epilepsy and a risk profile for postoperative cognitive decline were investigated over various time points. Neuropsychological assessments occurred before surgery, 1 week, 3 months, and 6 months postoperatively. According to our rehabilitation concept, every patient started occupational therapy 1 month before surgery. Therapy lasted for at least 6 months after surgery. For all patients, extensive qualitative interviews with the occupational therapists and anamnestic data were analyzed.Results: In all patients, postoperative psychosocial difficulties emerged. Language and memory tests showed a decline after 6 months specifically for name retrieval. Occupational therapy was adapted to find individual solutions for the patients problems and to implement effective coping strategies.Conclusion: Cognitive training lead to consistent improvements over time. The results show that occupational therapy can be an efficient tool in the treatment of psychosocial and cognitive impairments after epilepsy surgery.
Introduction
Verbal memory and object-naming ability are two of the modalities with the highest risk of decline after epilepsy surgery (Helmstaedter et al., 2000). The majority of previous research on epilepsy has neglected the role of neuropsychological rehabilitation and has focused on determining impairments in cognitive performance, as well as their reasons. Research on cognitive rehabilitation is so far scarce, especially after resective surgery in the left temporal lobe (De Vasconcelos Geraldi et al., 2017).
In epilepsy patients, substantial cognitive deficits are evident as part of the underlying pathology and epileptic syndrome (e.g., hippocampal sclerosis). Consequently, rehabilitative procedures beginning after resective surgery are considered too late and should be initiated preoperatively. In this sense, Wilson et al. (2001) and Koorenhof et al. (2012) recommend initialization of preoperative cognitive training specifically for patients with planned epilepsy surgery.
Moreover, up until now only very few studies have approached the question of how occupational therapy (OT) can contribute to the postsurgical rehabilitation process in epilepsy patients. The relationship between OT and cognitive measures has been investigated in other neurological illnesses, such as stroke and multiple sclerosis (Khan et al., 2017; Reuster et al., 2008). However, there is only limited data for patients with left temporal epilepsy, who have a particularly high risk of cognitive impairments after surgery (Mazur-Mosiewicz et al., 2015).
In this study, we specifically favored a therapy setting with OT. Occupational therapists are capable of treating potential cognitive, affective and motor impairments that can occur with a chronic illness. OT focuses specifically on social, mental and occupational abilities and adjusts the methods according to the individual needs of patients (Clerico, 1989).
Methods
Patients
This study was reviewed and approved by the local research ethics committee (2016). The study was performed in accordance with the code of ethics of the World Medical Association (Declaration of Helsinki) for experiments involving humans. Written informed consent was obtained from all participants after receiving an explanation of the study. Seven patients with pharmacoresistant epilepsy from the Erlangen Epilepsy Center (EEC) were included in this study, all of whom were scheduled for epilepsy surgery and were diagnosed with a left temporal lobe epilepsy (LTLE). Patients were included with a focal epilepsy in the left temporal lobe due to hippocampal sclerosis and clear left-hemispheric dominance for speech processing and verbal memory. All patients exhibited a limited ability to compensate speech- and memory-relevant deficits based on preoperative neuropsychological results and the Wada test.
All patients received OT before and after surgery, respectively. Treatments (45 min) were administered in an outpatient setting two times a week. Patients received cognitive behavior training, which is a structured therapy directed toward solving current problems and teaching skills to modify dysfunctional thinking and behavior. Each patient received at least four therapy sessions preoperatively in order to establish a therapeutic relationship and to determine a therapy goal. The therapy focus was set in accordance with the cognitive deficits and client limitations. OT was implemented at least 6 months postoperatively. In case of increased psychosocial difficulties (e.g., dysphoric mood and anxiety), patients received specific psychoeducational support (structured information on the deficits and treatment options) from the practitioner.
Neuropsychological measures
Neuropsychological testing and assessment of hemispheric dominance was administered by the neuropsychologist of the EEC. In all patients, preoperative neuropsychological testing occurred 3–6 months before surgery. To examine object-naming ability, the Boston Naming Test was administered (Kaplan et al., 1983). The task requires confrontation naming of 60 objects of increasing difficulty. A naming failure is noticed if the patient’s response deviated from the target name either semantically or phonologically. Overall test performance was calculated as the sum score of all incorrectly named items.
The Regensburger Wortflüssigkeits test was applied in order to detect differences in verbal fluency performance (Aschenbrenner et al., 2000). Tasks (2 min testing per task) included semantic fluency for animals (e.g., how many animal species can a person think of from the animal kingdom) and the ability to switch from one category to another (e.g., sports vs. fruits).
Verbal memory performance was measured with the Berliner Amnesie test (Metzler et al., 2010). Memory testing required the recall of word lists, as well as the recognition of learned words in a short text. Apart from assessing the test performance using individual subtests, a global score for verbal memory performance was calculated, indicating the overall performance on the different subtests. Short-term memory was examined with a digit span test.
For evaluation of depression, the Beck Depression Inventory (Beck at al., 2008) was administered pre- and postoperatively (6 months after surgery).
Assessment of hemispheric dominance
In all patients, speech and memory dominance was determined by the Intracarotid Sodium Amytal Test (IAT). After selective anaesthetization of the left or right hemisphere, speech and memory testing of the isolated awake hemisphere was performed. Tasks included automatic speech (e.g., counting), naming (pictures and real objects), reading, comprehension, and repetition of words and sentences. After the anaesthetization patients were asked to memorize as many of the presented pictures and real objects as possible. For each hemisphere, a sum score of all remembered items was calculated. Left-sided speech dominance was defined by global aphasia during left hemispheric anaesthetization and unimpaired receptive and expressive speech functions during right hemispheric anaesthetization. To assess memory dominance for each patient, a laterality index (LI) was calculated (memory score left hemisphere − memory score right hemisphere/memory score left hemisphere + memory score right hemisphere * 100). Accordingly, the LI varied between −100 and +100 with a positive score indicating a left sided dominance.
Mixed-methods approach
This study utilized a sequential mixed methods design combining qualitative and quantitative data. Neuropsychological assessments occurred at four time points: preoperatively (T0), 1 week (T1), 3 months (T2), and 6 months (T3) postoperatively. Quantitative data was analyzed by comparing pre- and postoperative neuropsychological mean scores.
Qualitative data was based on repeated patient anamnesis (four time points) and interviews of the occupational therapists during the first 6 months after surgery. For each patient, two interviews with the therapists were conducted 3 months and 6 months after surgery, respectively. Every interview was carried out by the neuropsychologist of the EEC. Our goal was to explore patients’ experiences and perceptions in the aftermath of the surgery aside from pure neuropsychological measures. Accordingly, a semi-structured interview was conducted with all occupational therapists. Questions addressed the current cognitive status of the patients (memory, language, and executive functions), psychosocial aspects (family, job, and leisure activities) and the structure of the OT process (methods and strategies). Therapists could give additional information.
All interviews were analyzed according to grounded theory paradigm (Glaser and Strauss, 1967), which is an inductive method for analyzing qualitatively generated data. The GTM aims to differentiate between multiple data types and is a method for both descriptive and exploratory studies. Grounded theory is a qualitative approach to generate theory from inductive analysis of data collected via multiple qualitative data collection procedures. The assessment of quantitative and qualitative data allowed for a triangulation of these different data types, which typically increases the credibility of methodological approaches (Shah and Corley, 2006).
In the following inductive research process, data of the single cases were analyzed by the neuropsychologist of the EEC and a psychology student, independently. At the beginning, a first case was analyzed and findings were then compared to the next cases whereby thematic key aspects were identified and modified. Subsequently, similarities and differences were assessed according to the principles of open, axial, and selective coding. Regarding open coding we classified data material according to the emerging key categories (units of meaning). After this step, axial coding took place, whereby categories were compared and grouped into main- and subcategories. Finally, using selective coding, the central theme of each main category was extracted. After coding, relations between the main categories were fixed in reference to current scientific research. In this way, a final theoretical model was generated.
Results
Quantitative analysis
Patient data.
Pre- and postoperative mean scores for the neuropsychological measures are shown in Figure 1. Left temporal lobe resection led to significant naming decline. For verbal memory and word fluency, a slight deterioration was evident 1 week and 3 months after surgery. For both functional domains, 6 months testing revealed improved results comparable to the baseline. In most patients, 6 months testing showed relatively lower scores for depression compared to the baseline (see Table 1). Neuropsychological results. Preoperative and postoperative neuropsychological results (group mean scores). Scores are z-scores.
Qualitative analysis
Four interrelated categories emerged from the data: Components of occupational therapy, preoperative mental focusing, postoperative crisis, and crisis solution (
Figure 2
).
Main categories. Main categories based on the qualitative analysis.
Preoperative mental focusing
In all patients, subjective concerns about the surgical risks were evident (e.g., “I am heavily concerned with the operation,” “poor sleep,” “I am stuck in thoughts,” “thoughts about disability and death,” “feeling paralyzed,” “I pondered a lot”). In addition, cognitive impairments were a source of concern (“What happens if I lose my mental capabilities?”). Lack of information on the course of rehabilitation fueled anxious thoughts in two patients (“I do not understand the relationship between the exercises and the brain’s ability to restructure”).
Postoperative crisis
Postoperative crisis is the main category considered most relevant. Crisis was defined in this context as a difficult or unstable mental or psychsocial situation involving a desire for change. Within this category, a subjective concept of immobility was evident (e.g., “lack of privacy,” “not being able to work,” “not having a purpose,” “surgical scar problems”). In addition, psychological problems were identified as a result of loss of identity (e.g., “I feel like I am no longer who I used to be”), depersonalization (“to perceive oneself as unrealistic”) and an increase in psychopathological symptoms (e.g., “general dissatisfaction,” “worries,” “depressive mood”). Furthermore, an increased perception of cognitive impairments was shown (e.g., “reduced word finding,” “I have the words right on the tip of my tongue,” “I forget everything too quickly”). All patients expressed a desire for functional improvements. In one patient, a state of euphoria occurred after surgery due to seizure freedom followed by a psychosocial crisis (“What should I do with my life”).
Solution of the crisis
In all patients, specific factors could be identified that were associated with the onset of the crisis solution. An improved mental well-being (e.g., “solved,” “calm,” “more stable,” “relatively satisfied with the new living situation”), the regaining of a structure of everyday life (e.g., “he started working in a supermarket”) or the discovery of new leisure activities (e.g., “went to the gym more often”) were reported. In these cases, therapists observed improved behavior change strategies (e.g., “regular diary entries,” “he/she learned to think quietly”).
Components of occupational therapy
This category emerged from the interviews with the therapists. Accordingly, OT covered three therapeutic areas. Psychoeducation can be understood as a corner stone (e.g., “therapist explains what occupational therapy is,” “explanation of therapeutic techniques,” “clarifying goals,” “the patient had difficulties figuring out what will happen in the next few months”). In addition, mindfulness training (e.g., relaxation skills, autogenous training, identification of stressful events, focus on positive aspects of life, and motivation to seek social support) shaped the therapy process. In this regard, the following therapeutic approaches were adopted: (1) Worksheets: Dialectical method (“Positive things in life versus stressful life events”) with accentuation of positive life aspects, listing of subjectively important activities in the foreseeable future (e.g., hobby, sports, and job perspective). (2) Creativity techniques: These techniques were mainly administered for stress reduction and the maintenance of self-esteem. Indicators were sleep disturbances, a high level of uncertainty regarding functional deficits (“I just want my old self back”) and correspondingly, a poor self-image. Therapeutic approaches consisted of paintings, making a collage with magazine pictures (e.g., “Just let your imagination go and paint/make whatever you want”) and visual mental imagery (“seeing with the mind’s eye”). (3) Motivational techniques: Fixation of concrete, realistic life plans (e.g., intensify social communication and social interactions), utilization of mind-maps (e.g., depiction of the current emotional state, delineation of solutions for individual problems).
The third category consisted of neurocognitive tests and procedures for attention, executive functions, speech-related functions, and memory: (1) Memory: Mental visualization of verbal material, memorization of word lists and stories, thinking about the meaning of words, and digit span tasks for verbal short-term memory. (2) Language: Picture naming, brainstorming tasks, verbal description of pictures, fill-in-the-blank texts, defining the meaning of words, generation of synonyms and antonyms for words, and sorting words into categories. (3) Creativity techniques: Verbalization of body movements and interpretation of activity cards (e.g., “Which adage is depicted?”). (4) Executive functions: Sorting pictures in a logical order, verbal analysis of complex everyday activities, verbalization of action steps, and strategy transfer. (5) Attention: Computer-based tasks (e.g., stimulus-reaction incompatibility paradigm, arrows that are directed to the left or the right side are presented, depending on the direction of the arrow, the test person should respond with the right or left hand irrespective of the side on which the arrow is presented).
Overall, OT attempted to have a positive reinforcing effect through cognitive tasks and to encourage a sense of accomplishment. The goal was to facilitate emotional stabilization and maintenance of emotional balance under stressful circumstances. Furthermore, the discussion of everyday problems was adopted to support problem solving activities (“What doesn’t work’’) and to specify the next therapeutic steps. Moreover, external sources were used to take the pressure off. For example, a patient stuck name tags on objects at home, who were difficult to name, in order to strengthen word recall.
Conceptual model
Based on the results a conceptual model for neurorehabilitation after epilepsy surgery was established. The procedure was based on the Strauss (1991) coding paradigm. The central aspect is the phenomenon with its various influencing factors. The causal condition contributes to the manifestation of the phenomenon, as well as intervening conditions, behavioral strategies, and contextual variables (Figure 3). Conceptual model for the rehabilitation process.
Causal condition
Resective surgery was identified as the causal condition that led to the phenomenon of postoperative crisis.
Contextual conditions
This term features the individual epilepsy-related conditions. Contextual conditions encompass LTLE, left-sided speech dominance, and lack of compensatory capacity of the right hemisphere. Increased anxiousness right before the operation shows that patients struggle with the associated risks. Accordingly, preoperative hopes can also develop into postoperative disappointment and frustration. This is why psychosocial support in both the pre- and postoperative setting is important.
Intervening conditions
Rehabilitation measures that support coping strategies are beneficial for the solution of the postoperative crisis. Occupational therapists are able to implement individualized programs according to the patient-specific characteristics, which is more reasonable than using standardized training programs (Sturm, 2007). Wilson et al. (2001) confirmed the impact of psychosocial education in rehabilitation. In order to minimize preoperative ambiguities and false expectations, professionals should inform patients about rehabilitation methods and chances preoperatively. Jacoby et al. (2014) also emphasize the support patients with epilepsy need postoperatively. In particular, psychosocial support should address life activities and social functions, which have shown themselves to be central to subjective mental well-being. Through psychoeducation and mindfulness training coping strategies can be learned that support patients in their daily activities.
Phenomenon
Hosseini et al. (2016) notes that patients can experience loss of identity, helplessness, and self-degradation after epilepsy surgery. Wilson et al. (2001) explored the psychosocial adaptation process of patients, which are postoperatively seizure free. The authors determine the development of a healthy identity and the abandonment of dependence and passivity as one of the biggest challenges. They postulate that the less the patients master these challenges, the greater the likelihood is for persisting psychological deficits. Therefore, psychological well-being is a concept, which does not necessarily go along with an improved cognitive performance (Ozanne et al., 2016).
Crisis implications
Interdisciplinary rehabilitation concepts address the association between disease-specific parameters and the individual psychological needs and impairments (Wilson et al., 2001). The results of our study are in line with Wrench et al., (2004), who negate a simple linear positive correlation of postoperative seizure freedom and psychosocial functioning. The described loss of identity as part of the postoperative crisis is congruent with previous assumptions, that epilepsy patients show deficits in their perceived self-efficacy and self-confidence. OT can help to ensure a realistic idea of one’s own performance level (Rickertsen, 1996).
Action and interaction strategies
Action and interaction strategies describe how patients deal with a postoperative crisis. There are two distinct strategies: ignorant and motivated behavior. In our patient group, both ignorant (e.g., “he/she seems to compensate for weaknesses by laughing loudly and talking a lot,” “the patient does not see the problem and its connections”) and motivated strategies (e.g., “during therapy, the patient shows great motivation and effort,” “the patient sees tasks more as a challenge,” “the patient motivates himself with statements such as “Yes, I can do that”) were evident. Lequerica and Kortte (2010) subdivide the willingness for therapy into engagement and disengagement, which coincides with this assumption. Motivated behavior is an action strategy that can contribute to solving the crisis.
Consequence
The solution of a postoperative crisis is less a final state, but rather the beginning of perceiving positive aspects in life. This change is part of a long-term psychosocial adaptation process (Coleman et al., 2020; Katz et al., 2002; Stefan and Pauli, 2008). Our results show that OT with its specific therapeutic components can have an important influence on psychosocial disease management.
Discussion and implications
The aim of this study was to develop an understanding of the process of postoperative rehabilitation in epilepsy patients aside from pure neuropsychological measures. Quantitative and qualitative data were combined in order to encompass a more holistic picture of the rehabilitation process. We also wanted to provide an insight whether qualitative and quantitative data match or show inconsistencies.
Disease-specific questionnaires are often insufficient to assess the quality of life after epilepsy surgery. Particularly for a relatively short postoperative period of 6 months, they proved to be unsuitable for valid assessment of the psychosocial condition (McLachlan et al., 1997; Mikati et al., 2006). Accordingly, these methods give an inadequate picture of the psychosocial outcome in epilepsy patients after surgery. Psychological processes that do not manifest themselves in clinically relevant symptoms of depression and anxiety are not covered (Michaelis et al., 2019). Wilson et al. (2001) have suggested that there should be a paradigm shift in the assessment and management of psychosocial development after resective epilepsy surgery. In particular, it is currently still unclear how the patients subjectively perceive their functional abilities (Markand et al., 2000).
In this study, individual psychosocial disease perception was a major focus. Preoperatively LTLE patients showed fear of postoperative mental and physical decline. We found that OT showed effectiveness by reducing the symptoms of postoperative crisis. Quantitative analysis of the postoperative neuropsychological data showed that after left temporal lobe surgery specifically naming ability deteriorates. Regarding verbal and short-term memory capacity and word fluency, the patient group showed improvements throughout the therapy process. There is sufficient evidence on that phenomenon (Ives-Deliperi and Butler, 2017). A study by Pauli et al. (2017) found that naming deficits (as tested by the BNT) after surgery in the anterior temporal lobe are one of the cognitive dysfunctions that patients are most (consciously) aware of. Furthermore, postoperative memory deficits are well documented if parts of the hippocampus are removed (Zentner, 2016).
Our results indicate that objective psychometric test procedures are not sufficient in evaluating the rehabilitation process of epilepsy patients, whereas qualitative research methods contribute notably in minimizing the current research gap. Resective surgery in the dominant left temporal lobe can cause significant postoperative impairment that may exceed preoperative cognitive deficits.
However, it should be mentioned that measures specifically tackling naming ability had not been one of the main goals of neurorehabilitation after surgery in the anterior temporal lobe (De Vasconcelos Geraldi et al., 2017). The results show that OT can be useful even in speech related deficits. Nevertheless, other types of therapy should be included, such as speech correction therapy.
To obtain seizure freedom in pharmacoresistant epilepsy, surgery is the method of choice (Hamer and Winkler, 2016). However, postoperative absence of seizures is not the only criterion of success since newly formed cognitive, psychiatric, and social impairments reduce quality of life considerably. Rehabilitative methods can contribute to minimizing these impairments (Wilson et al., 2001). In a study by Wilson et al. (2010), half of the patients (n = 57) reported psychosocial adaptive difficulties in the first 12 months after epilepsy surgery.
Even though our study shows limitations regarding the relatively small sample size, there is reason to assume that early rehabilitation methods constitute a suitable approach to minimize deficits in cognitive and psychosocial domains. Qiu et al. (2019) discovered that patients’ quality of life after epilepsy surgery improved with preoperative behavior-based interventions, focusing on psychological and neurocognitive deficits. Apart from these findings, an effective information exchange between neuropsychologists and occupational therapists is necessary to support patient-centered rehabilitative processes.
Giles et al. (2020) point out that functional cognition—the cognitive ability to perform daily life tasks—should be an important domain of concern for OT practice. Accordingly, apart from assessing deficits in specific cognitive domains (e.g., memory and language) it is essential to measure life tasks regarding the use of strategies, routines and environmental resources. Further evidence comes from the observation that physical exercise training improves mechanisms of neural plasticity. In humans, higher intensity of habitual exercise is associated with improved cognitive reappraisal success (Giles et al., 2017). Therefore, habitual exercise relates to improved cognitive control of neuronal information (e.g., selective attention, working memory, and reappraisal of emotional information).
Based on the results of our study, the following implications for future research arise: qualitative long-term-studies are needed in order to understand the adaptation process of patients after epilepsy surgery (Mikati et al., 2006; Ozanne et al., 2016). Moreover, further studies should be conducted investigating whether specific preoperative measures can compensate postoperative cognitive deficits (Koorenhof et al., 2012).
Conclusion
Based on the study results, there are two central conclusions:
Qualitative research leads to a more comprehensive understanding of the postoperative outcome in epilepsy patients and the associated psychosocial impairments. Apart from a deterioration in cognitive domains, the most central aspects are deficits in mental well-being.
The theoretical framework we developed serves as a guideline in order to understand the positive and negative factors during postoperative epilepsy rehabilitation. Based on this framework, it is possible to establish specific clinical interventions, serving the needs of future patients.
Key findings
• Aggravation of language and memory deficits is a typical finding after left temporal lobe surgery. • Occupational therapy is adapted to address psychosocial adaptive difficulties after brain surgery. • After left temporal lobe surgery apart from cognitive deficits, postoperative psychosocial problems are the primary focus of OT.
What the study has added
Occupational therapy after left temporal lobe surgery is adapted to specifically identify cognitive and behavioral performance problems in patients and provide individualized, goal-focused solutions. We found that an individualized approach with effective psychoeducational and cognitive training strategies can lead to improvements in task performance and patients’ satisfaction.
Footnotes
Author Contributions
MS initiated and supervised the study and gained ethical approval. He was responsible for patient recruitment, interviews with the occupational therapists, and data analysis. MS and KW were responsible for all neuropsychological assessments. LG and KS researched literature and conceived the study. BK and HH—as leading neurologists of the epilepsy center—were responsible for all epilepsy-related medical data. All authors reviewed and edited the manuscript and approved the final version of the manuscript.
Declaration of conflicting interests
The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.
Funding
The author(s) received no financial support for the research, authorship, and/or publication of this article.
Ethical approval
This study was reviewed and approved by the research ethics committee of the Friedrich-Alexander University Erlangen-Nuernberg (approval number 344_15B, year 2016).
