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Social functioning and health-related quality of life trajectories in people with epilepsy after epilepsy surgery
YEBEH-106849; No of Pages 6 Epilepsy & Behavior xxx (xxxx) xxx
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Social functioning and health-related quality of life trajectories in people with epilepsy after epilepsy surgery Po-Tso Lin a, Hsiang-Yu Yu a,b,⁎, Yi-Jiun Lu c, Wei-Han Wang d, Chien-Chen Chou a,b, Sanford P.C. Hsu b,c, Chun-Fu Lin b,c, Cheng-Chia Lee b,c a
Department of Neurology, Neurological Institute, Taipei Veterans General Hospital, Taipei, Taiwan Institute of Brain Science, Brain Research Center, National Yang-Ming University, Taipei, Taiwan Department of Neurosurgery, Neurological Institute, Taipei Veterans General Hospital, Taipei, Taiwan d Department of Psychology, Chung Shan Medical University, Taichung, Taiwan b c
a r t i c l e
i n f o
Article history: Received 14 October 2019 Revised 27 November 2019 Accepted 7 December 2019 Available online xxxx Keywords: Social functioning Quality of life Epilepsy Epilepsy surgery People with epilepsy
a b s t r a c t Objective: An improvement in quality of life (QoL) over time after epilepsy surgery has been demonstrated in people with epilepsy; however, social functioning has been less investigated. We conducted this study to examine whether postsurgical improvement is parallel between QoL and social functioning in patients with epilepsy. Methods: We retrospectively reviewed patients who underwent epilepsy surgery. All participants completed a comprehensive neuropsychological assessment, the Quality of Life in Epilepsy Inventory (QOLIE-89) questionnaire, and the Social and Occupational Functioning Scale for Epilepsy (SOFSE) before surgery and at 3 months, 6 months, and 1 year after surgery. Demographic and epilepsy-related information was also collected. Generalized estimating equations with identity links were used to model the QOLIE-89 and SOFSE over time and possible associated factors. A p b 0.05 was considered statistically significant. Results: A total of 76 patients, including 36 males and 43 females aged 18 to 62 years were collected. Both total QOLIE-89 and overall SOFSE improved over time after epilepsy surgery (adjusted p value b 0.001 and 0.002, respectively, with Bonferroni's correction). Total QOLIE-89 improved 3 months after surgery, while overall SOFSE showed no significant improvement until 6 months after surgery. The presurgical Full-Scale Intelligence Quotient (FSIQ) of the Wechsler Adult Intelligence Scale-III and years of education were significantly associated with time-dependent improvement for both total QOLIE-89 and overall SOFSE (p value b 0.001). At one year after surgery, overall SOFSE and total QOLIE-89 scores were significantly higher in the seizure-free group than in the nonseizure-free group (p value = 0.040 and 0.032, respectively). Conclusion: Social functioning significantly improved in people with epilepsy after surgery as QoL, but it took more time to exhibit improvement. People with better FSIQ and more years of education had better improvement in social functioning over time. The early intervention of rehabilitation programs after epilepsy surgery might be necessary to facilitate the improvement in social functioning. © 2019 Elsevier Inc. All rights reserved.
1. Introduction Epilepsy is among the most common neurologic problems. The purpose of epilepsy surgery in people with epilepsy (PWE) is to stop seizures or greatly reduce the seizure frequency [1]. However, people with or without good seizure control may have problems managing life after surgery. People's predominated aim for epilepsy surgery is in Abbreviations: PWE, people with epilepsy; HRQoL, health-related quality of life; QoL, quality of life; QOLIE, Quality of Life in Epilepsy Inventory; SOFSE, Social and Occupational Functioning Scale for Epilepsy; FSIQ, Full-Scale Intelligence Quotient; SF, seizure-free; NSF, nonseizure-free. ⁎ Corresponding author at: Neurological Institute, Taipei Veterans General Hospital, No. 201, Sec. 2, Shih-Pai Road, Taipei 11217, Taiwan. E-mail address: [email protected] (H.-Y. Yu).
the changes of social process [1]. It is mostly reflected by one's affective, psychosocial, and behavioral state [2]. As a result, apart from good seizure control, mitigation of psychosocial burden is also an utmost goal in epilepsy surgery. Health-related quality of life (HRQoL) has been suggested to greatly improve early after epilepsy surgery [3]. However, quality of life (QoL) could only partially reflect one's psychosocial status and not the whole picture [4]. Gois and colleagues [5] demonstrated that only the cognitive function domain of QoL was significantly correlated with social adjustment, not other domains. They revealed differences between QoL and social functioning. In addition, there was a gap between the improvement in QoL and social functioning after epilepsy surgery [6]. Social functioning might be overlooked in the postoperative follow-up if we focused only on
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Please cite this article as: P.-T. Lin, H.-Y. Yu, Y.-J. Lu, et al., Social functioning and health-related quality of life trajectories in people with epilepsy after epi..., Epilepsy & Behavior, https://doi.org/10.1016/j.yebeh.2019.106849
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the QoL [7]. In fact, social functioning substantially reflects the ability to be employed and maintains interpersonal relationships (IR) and therefore an independent life [8,9]. Once we notice the delayed improvement in social functioning after surgery [6], it is worth finding a solution to speed up the process of improvement. The early introduction of a rehabilitation program for PWE following surgery could help patients perceive a better psychosocial outcome [10]. Previous data focused on general social functioning in PWE following surgery, mostly based on the social function domain within the Quality of Life in Epilepsy Inventory (QOLIE), and the results were variable [11]. While some studies revealed no differences in general social functioning between surgical and nonsurgical patients [12,13], others reported significant improvement regardless of seizure status following surgery [14]. Most of the studies were cross-sectional research studies, and the time of assessment was variable and not sequentially recorded [15–18]. We would like to conduct this study to investigate the trajectories of improvement in QoL and social functioning after epilepsy surgery and possible factors affecting the improvement. 2. Methods
functioning in PWE in Taiwan. It comprises 6 dimensions, including IR, social activities (SA), communication (C), leisure activities (LA), instrumental living skill (ILS), and occupation (O). The total score is a summation of these 6 subscales and ranges from 0 to 100. Higher scores reflect better social functioning [19]. The SOFSE can also be used for a social outcome follow-up after an intervention. (2) The QOLIE
The QOLIE-89 [20] consists of 89 items within 17 subscales, including the overall QoL; emotional well-being; role limitations: emotional; social support; social isolation; energy/fatigue; seizure worry; medication effects; health discouragement; work/driving/social function; attention/concentration; language; memory; physical function; pain; role limitations: physical; and health perceptions. The total scores are further standardized to T scores ranging from 0 to 100, and higher scores indicate a better QoL. The Taiwanese version of QOLIE-89 has been shown to be a valid and reliable indicator of the QoL in PWE [21]. (3) The Intelligence Test
2.1. Patient selection and evaluation This study was approved by the institutional ethics committee of the Taipei Veterans General Hospital (TPEVGH). The data were collected from patients aged 18 years and above who underwent epilepsy surgery between April 2012 and May 2018 at TPEVGH. Our presurgical evaluation included video-electroencephalography (video-EEG), high-resolution magnetic resonance imaging (MRI), F-fluorodeoxyglucose-position emission tomography, and a comprehensive neuropsychologic assessment. The decision to perform surgery was made after a multidisciplinary seizure conference in most cases. When all data were concordant with an epileptogenic lesion on neuroimage (hippocampal atrophy, tumors, vascular malformation, or focal cortical dysplasia), a resective surgery would be arranged. Intracranial EEG studies, whether subdural grids/ strips or stereo-EEG, would be suggested before resection if there was no obvious lesion on the brain MRI, or the presumed epileptogenic region inside the eloquent cortex. The epilepsy surgery included selective amygdalohippocampectomy, corticoamygdalohippocampectomy, corticetomy, and lesionectomy according to the conclusion of presurgical evaluation. In our epilepsy surgery program, patients were asked to complete the baseline and postoperative relevant questionnaires for clinical use. We retrospectively reviewed those who completed the baseline, postoperative 3-month, 6-month, and 1-year follow-up social functioning and QoL assessment. A total of 131 PWE aged 18 years and above who were literate and able to fulfill the social functioning and QoL questionnaires were reviewed in the beginning. Among them, 56 patients were excluded because of incomplete baseline data, active psychiatric problems, progressive neurological disorder, or severe concurrent medical illness. A total of 76 patients were qualified for this analysis. Demographic information, seizure-related factors, and the Full-Scale Intelligence Quotient (FSIQ) were obtained for analysis. Seizure outcomes and whether antiepileptic medication was discontinued were assessed at 1 year after surgery. Patients were classified into two groups based on one-year seizure outcome: a seizure-free (SF) group (Engel classes IA and IB) and a nonseizure-free (NSF) groups (Engel classes IC to VIB). The location of epilepsy surgery was categorized as temporal only and extratemporal with/without temporal lobe involvement. The following three assessments were used in the study. (1) The Social Functioning Scale The Social and Occupational Functioning Scale for Epilepsy (SOFSE) [19] is a validated and psychometrically sound tool for evaluating social
The Wechsler Adult Intelligence Scale – Third edition (WAIS-III) Taiwanese version [22] is used in the present study to evaluate the FSIQ as an index of general intellectual functioning. The FSIQ is calculated using ten of the WAIS-III subtests, including Picture Completion, Vocabulary, Digit Symbol Substitution, Similarities, Block Design, Arithmetic, Matrix Reasoning, Digit Span, Information, and Symbol Searching. 2.2. Statistical analysis Analyses were performed using the International Business Machines Statistical Package for the Social Sciences (IBM SPSS) 22 program. Categorical variables were indicated as the number and percentage. For intergroup comparisons, Pearson's chi-squared, Fischer's exact, and nonparametric Mann–Whitney U tests were applied when appropriate. Longitudinal data were analyzed to investigate the changes in both overall SOFSE and total HRQoL over time within a year after epilepsy surgery by using generalized estimating equations (GEE) with identity links. The scores of each of the six dimensions of SOFSE were standardized by linear conversion to a scale of 0–100 [19] and were analyzed for changes over time with GEE as well. We further determined whether demographic and disease-related factors such as gender, the age of epilepsy onset, the duration from seizure onset to surgery, the location of epilepsy surgery, years of education, and FSIQ were associated with the magnitudes of changes. The result of the analysis was considered statistically significant when p b 0.05. 3. Results A total of 76 patients received epilepsy surgery and completed presurgical baseline SOFSE and QOLIE-89 questionnaires. All patients followed up for at least one year after epilepsy surgery. Out of 76 qualified subjects, 35 were males, and 41 were females; the average age was 31.84 (range: 18 to 62). There were some missed or incomplete SOFSE or QOLIE-89 questionnaires in the following 3 months, 6 months, or 1 year after surgery. The number of patients with postoperative 3month, 6-month and 1-year eligible SOFSE scores was 57, 65, and 60, respectively, and was 64, 69, and 58 for QOLIE-89 scores, respectively (Little's test of missing completely at random [MCAR] test with p value = 0.081 and 0.774, respectively). In these 76 patients, there were 10 patients with headache, 7 patients with hypertension, and 1 patient with type II diabetes mellitus.
Please cite this article as: P.-T. Lin, H.-Y. Yu, Y.-J. Lu, et al., Social functioning and health-related quality of life trajectories in people with epilepsy after epi..., Epilepsy & Behavior, https://doi.org/10.1016/j.yebeh.2019.106849
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3.1. Seizure outcome Eighteen patients (23.7%) had recurrent seizures 1 year after surgery (NSF group); fifty-eight patients (76.3%) became SF (SF group). In the NSF group, 15 patients had improvement in seizure control compared to their condition before surgery (Engel classes IIA to IIIA). In our program, we usually started to taper off antiepileptic drugs (AEDs) after 2-year freedom from seizures. Only 4 patients discontinued antiepileptic medication in the SF group, none in the NSF group. A younger age of epilepsy onset and a longer duration of epilepsy were associated with seizure recurrence after surgery (p value = 0.031 and 0.003, respectively). There was no significant difference in baseline overall SOFSE and total QOLIE scores between groups (p value = 0.153 and 0.345, respectively). Gender, education, baseline FSIQ, surgery location (temporal only vs. extratemporal with/without temporal lobe), and the side of surgery were not different between patients with or without SF (Table 1).
3.2. Changes in social functioning and QoL over time Both total QOLIE-89 and overall SOFSE scores improved over time after epilepsy surgery (Bonferroni adjusted p value b 0.001 and 0.002, respectively). The total QOLIE-89 significantly improved at 3, 6, and 12 months after surgery (all p value b 0.001) and improved most at the 3-month follow-up; however, the overall SOFSE showed no significant improvement until 6 months after surgery (p value = 0.903, 0.009, and 0.001, respectively, at 3, 6, and 12 months after surgery) (Fig. 1). Baseline FSIQ and years of education were significantly associated with the time-dependent improvement in both total QOLIE-89 and overall SOFSE (p value b 0.001). Gender, the age of epilepsy onset, the duration from epilepsy onset to surgery, and surgery location showed no significant relationship with improvement in QoL or social functioning. Table 1 The demographic and epilepsy-related data of the cohort. Group
Gender Male (%) Female (%) Age of epilepsy onset (years) Mean Median Range Duration epilepsy to surgery (years) Mean Median Range Surgery location Temporal lobe only (%) Extratemporal with/without temporal lobe (%) Side of location Right side (%) Left side (%) Education (years) Mean Range Baseline Full-Scale IQ Mean Range Overall SOFSE score Mean Range Total QOLIE-89 T score Mean Range SF: seizure-free, NSF: nonseizure-free. ⁎ p value b 0.05.
SF (n = 58)
NSF (n = 18)
26 (44.8%) 32 (55.2%)
9 (50.0%) 9 (50.0%)
19.84 17.00 2–58
12.72 12.50 2–24
11.31 9.00 0–45
19.06 17.00 3–49
51 (87.9%) 7 (12.1%)
12 (66.7%) 6 (33.3%)
25 (43.1%) 33 (56.9%)
7 (38.9%) 11 (61.1%)
13.72 6–18
12.94 6–16
87.67 43–111
81.18 63–106
64.16 15–87
57.83 23–82
p value 0.701
0.031⁎
0.002⁎
0.067
0.752
0.408
0.074
0.153
0.345 47.30 43.61 21.53–80.16 18.66–71.66
3
The overall SOFSE and the IR, C, and ILS dimensions of the SOFSE revealed no significant improvement at 3 months after surgery but became significant over time thereafter (p value = 0.016, 0.021, and 0.001 at 6 months after surgery in the IR, C, and ILS, respectively). The O dimension showed significant improvement at 1 year (p value = 0.046). However, SA and LA did not change significantly over time (p value = 0.807 and 0.292, respectively), but there was a trend of improvement. The dimensions of the SOFSE did not improve in a parallel pattern (Fig. 2). 3.3. Social functioning and QoL between the SF and NSF groups At one year after surgery, the overall SOFSE and total QOLIE-89 scores were significantly higher in the SF group than in the NSF group (p value = 0.040 and 0.032, respectively). In addition, O was the only dimension of SOFSE that had significantly higher scores in the SF group than in the NSF group (p value = 0.011) (Table 2). However, in the GEE model, seizure outcome was not associated with time-dependent improvement in either overall SOFSE or total QOLIE-89 (p value = 0.069 and 0.106, respectively). 4. Discussion In this study, 76.3% of participants became SF one year after epilepsy surgery. The outcomes were comparable to most of the published data [3,11,12,18,23–25]. The earlier introduction of epilepsy surgery in PWE could obtain a better outcome [26]. In our study, patients with an older age of epilepsy onset and a shorter duration from epilepsy onset to surgery had significantly higher chances of being SF, as with many other reports, which supported the hypothesis that people with shorter epilepsy duration were more likely to be SF at follow-up [24,26,27]. The social functioning and QoL both improved after surgery in our cohort. We found that QoL improved over time following surgery as early as 3 months, but as for social functioning, not as observed in QoL, our analysis revealed no significant improvement in overall SOFSE scores at 3 months after surgery. There was a disparity in the speed of improvement between HRQoL and social functioning. Susan S. Spencer and colleagues [3] reported that QOLIE-89 scores increased significantly within 6 months after surgery, and Sarah J. Wilson and colleagues [6] noted the greatest improvement in HRQoL at 3 months after epilepsy surgery on average. Health-related quality of life scores improved over time soon after the surgery. However, self-perceived psychosocial adjustment changes after surgery did not appear until after 1 year on average [6]. Other studies reported that self-perceived improvements in social functioning among PWE required longer than 2 years to develop [17,28]. Accordingly, we suggested that the improvement in QoL might prevail in social functioning in PWE following surgery. This phenomenon is most likely due to one's psychosocial features of the adjustment that needed more time to improve, which cannot be explained by HRQoL [7]. There are six dimensions within SOFSE scores, and each one stands for the different aspects of social functioning [19]. From the subscales of our study, IR, C, ILS, and O improved over time, but there was a time difference. The significant improvement in occupational status occurred as late as 1 year. We speculated that this improvement in occupational status requires the ability to spend time in a structured and meaningful way, including gainful employment, household work, or studying [29]. This requires more time to achieve. We also noted that SA and LA did not change significantly over time, but there was a trend of improvement. Mary Lou Smith and colleagues [12] explored psychosocial outcomes in PWE, which revealed significant effects on the social and social problems subscales approximately 2 years after surgery but no changes at one year after surgery [12,30]. Among the dimensions of social functioning, the improvement speed after surgery varies, which implies that postoperative interventions, like rehabilitation, need to be
Please cite this article as: P.-T. Lin, H.-Y. Yu, Y.-J. Lu, et al., Social functioning and health-related quality of life trajectories in people with epilepsy after epi..., Epilepsy & Behavior, https://doi.org/10.1016/j.yebeh.2019.106849
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Fig. 1. Comparison of overall SOFSE scores and total QOLIE-89 T scores. The trajectories between overall SOFSE and total QOLIE-89 after surgery increased over time but were not parallel. ‡: p value b 0.05.
comprehensive and targeted different social functioning dimensions with a certain time schedule. We investigated possible clinical and demographic variables affecting the time-dependent improvement in overall SOFSE and total HRQoL following surgery. Baseline FSIQ and years of education were significant factors. Previous literature has revealed that total HRQoL is significantly correlated with FSIQ both before and after surgery [14,31]. FSIQ also demonstrated a positive correlation with overall SOFSE scores [32]. With more years of education, such as for college-educated subjects, patients could obtain more benefits to alleviate cognitive distress within HRQoL [3]. There were few former reports describing the correlation of the magnitude of improvement in QoL and social functioning with FSIQ and years of education. Via schooling, the intelligence of people between 10 and 20 years could increase [33], and with better intelligence, people obtain more processing skills and psychomotor coordination to assist in adjusting to a major life change [34]. Seizure outcome did not influence the time-dependent improvement in HRQoL and social functioning in our study. This result suggested that the speed of improvement after surgery was not related to seizure freedom. Previous longitudinal investigations comparing PWE before
and after surgery suggested that improvements in HRQoL can be observed only in completely SF patients [25], while other reports indicated that children who have Engel class II and III outcomes could experience similar HRQoL changes as children with Engel class I outcomes, and the cognitive functioning and emotional functioning stay the same [14]. Shehryar Sheikh and colleagues [35] demonstrated that relative seizure reduction with a mean value of 73% could predict postoperative QoL just as strongly as seizure freedom. This meant that any degree of improvement in seizures was associated with QoL improvement. Most of the patients in the NSF group in this study showed worthwhile improvement in seizure control, which supported the idea that whether the outcome was SF or not, both social functioning and QoL could improve over time. In the SF groups, there were higher total QOLIE-89 and overall SOFSE scores than in the group with recurrent seizures at one year after surgery, especially on the subscales of O. A favorable employment status was associated with seizure freedom and presurgical employment, which is consistent with other studies [36–38]. As a result, this study strengthened the benefit of surgical intervention to obtain a good seizure outcome and subsequent employment status. According to the published data, the early rehabilitation program had the same impact
Fig. 2. Comparison of 6 dimensions of SOFSE score. Each dimension score was standardized. The speed of improvement varied among dimensions. C: communication, ILS: instrumental living skill, IR: interpersonal relationships, LA: leisure activities, O: occupation, SA: social activities. ‡: p value b 0.05.
Please cite this article as: P.-T. Lin, H.-Y. Yu, Y.-J. Lu, et al., Social functioning and health-related quality of life trajectories in people with epilepsy after epi..., Epilepsy & Behavior, https://doi.org/10.1016/j.yebeh.2019.106849
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Table 2 Summary of different scales at one year after epilepsy surgery between the SF and NSF groups. Group
Overall SOFSE
SOFSE_IR
SOFSE_C
SOFSE_SA
SOFSE_LA
SOFSE_ILS
SOFSE_O
Total QOLIE-89
SF (n = 58) NSF (n = 18) p value
66.62 58.62 0.040⁎
79.82 76.11 0.353
61.22 58.50 0.640
59.76 50.28 0.136
62.14 56.32 0.352
80.55 71.10 0.136
70.41 58.70 0.011⁎
54.09 47.34 0.032⁎
SF: seizure-free, NSF: nonseizure-free, C: communication, ILS: instrumental living skill, IR: interpersonal relationships, LA: leisure activities, O: occupation, SA: social activities. ⁎ p value b 0.05.
as seizure freedom on vocational outcomes [39]. Further investigation of the early rehabilitation program in PWE after surgery on vocational and other psychosocial outcomes is warranted. The limitations of our study included the small sample size and the short follow-up duration. Trajectories beyond 2 or 3 years might give us more information. There were some missed data; however, the missed data were acceptable in our statistical analysis. Another limitation was that we evaluated the social functioning mainly based on the SOFSE questionnaire, and other social determinants of functioning such as personal income, social support, and access to care were not available. We included only patients who could complete the questionnaires. For those who could not read, relatively patients with disability, we were not able to assess their psychosocial change after surgery. 5. Conclusion Our study revealed that social functioning significantly improved in PWE after epilepsy surgery compared with health-related QoL, but they had different trajectories. People with epilepsy with higher baseline FSIQ and more years of education had greater time-dependent improvement in these two scales. In addition, we found that older epilepsy onset age and shorter duration from epilepsy onset to surgery were significantly associated with better seizure outcomes following surgery. Taken as a whole, the results of this study confirm the beneficial impact of epilepsy surgery on social functioning and HRQoL, with the evidence of more time needed to improve social functioning. Therefore, early intervention of rehabilitation programs in these patients might facilitate the improvement in social functioning. Ethical publication statement We confirm that we have read the journal's position on issues involved in ethical publication and affirm that this report is consistent with those guidelines. Acknowledgments This study was supported in parts by a grant from the National Science Council of Taiwan (102-2314-B-075-073) and Taipei Veterans General Hospital (V103C-107 and V108C-193). Declaration of competing interest The authors declare no potential conflicts of interest with respect to the research, authorship, and/or publication of this article. References [1] Taylor DC, McMacKin D, Staunton H, Delanty N, Phillips J. Patients' aims for epilepsy surgery: desires beyond seizure freedom. Epilepsia 2001;42(5):629–33. [2] Wilson SJ, Bladin PF, Saling MM. The burden of normality: a framework for rehabilitation after epilepsy surgery. Epilepsia 2007;48(Suppl. 9):13–6. [3] Spencer SS, Berg AT, Vickrey BG, Sperling MR, Bazil CW, Haut S, et al. Health-related quality of life over time since resective epilepsy surgery. Ann Neurol 2007;62(4): 327–34. [4] Whitcomb JJ. Functional status versus quality of life: where does the evidence lead us? ANS Adv Nurs Sci 2011;34(2):97–105.
[5] Gois J, Valente K, Vicentiis S, Moschetta S, Kuczynski E, Fiore L, et al. Assessment of psychosocial adjustment in patients with temporal lobe epilepsy using a standard measure. Epilepsy Behav 2011;20(1):89–94. [6] Wilson SJ, Wrench JM, McIntosh AM, Bladin PF, Berkovic SF. Profiles of psychosocial outcome after epilepsy surgery: the role of personality. Epilepsia 2010;51(7):1133–8. [7] Wilson S, Bladin P, Saling M. The "burden of normality": concepts of adjustment after surgery for seizures. J Neurol Neurosurg Psychiatry 2001;70(5):649–56. [8] Bosc M. Assessment of social functioning in depression. Compr Psychiatry 2000;41 (1):63–9. [9] Steiger BK, Jokeit H. Why epilepsy challenges social life. Seizure 2017;44:194–8. [10] Martin R. The burden of normality in the epilepsy postsurgery setting: out with the old and in with the new (…roles). Epilepsy Curr 2016;16(6):375–7. [11] Braams O, Maher C, Jennekens-Schinkel A, Braun K, van Nieuwenhuizen O, van Schooneveld M, et al. Social functioning of children after epilepsy surgery: a literature review. Epilepsy Behav 2019;96:210–8. [12] Smith ML, Elliott IM, Lach L. Cognitive, psychosocial, and family function one year after pediatric epilepsy surgery. Epilepsia 2004;45(6):650–60. [13] Puka K, Smith ML. Predictors of long-term quality of life after pediatric epilepsy surgery. Epilepsia 2015;56(6):873–81. [14] Titus JB, Lee A, Kasasbeh A, Thio LL, Stephenson J, Steger-May K, et al. Health-related quality of life before and after pediatric epilepsy surgery: the influence of seizure outcome on changes in physical functioning and social functioning. Epilepsy Behav 2013;27(3):477–83. [15] Suurmeijer TP, Reuvekamp MF, Aldenkamp BP. Social functioning, psychological functioning, and quality of life in epilepsy. Epilepsia 2001;42(9):1160–8. [16] Wilson SJ, Bladin PF, Saling MM, Pattison PE. Characterizing psychosocial outcome trajectories following seizure surgery. Epilepsy Behav 2005;6(4):570–80. [17] Hum KM, Smith ML, Lach L, Elliott IM. Self-perceptions of social function 2 years after pediatric epilepsy surgery. Epilepsy Behav 2010;17(3):354–9. [18] Kemp S, Garlovsky J, Reynders H, Caswell H, Baker G, Shah E. Predicting the psychosocial outcome of epilepsy surgery: a longitudinal perspective on the 'burden of normality'. Epilepsy Behav 2016;60:149–52. [19] Wang WH, Yu HY, Yen DJ, Lin YY, Kwan SY, Chen C, et al. The Social and Occupational Functioning Scale for Epilepsy (SOFSE): a brief measure of functional status in a Taiwanese sample with epilepsy. Epilepsia 2013;54(5):888–97. [20] Devinsky O, Vickrey BG, Cramer J, Perrine K, Hermann B, Meador K, et al. Development of the quality of life in epilepsy inventory. Epilepsia 1995;36(11):1089–104. [21] Zhao Y, Ding C, Wang Y, Li Z, Zhou Y, Huang Y. Reliability and validity of a Chinese version of the Quality of Life in Epilepsy Inventory (QOLIE-89). Epilepsy Behav 2007;11(1):53–9. [22] HY CJC. Wechsler Adult Intelligence Scale. . 3rd ed.Taipei: Chinese Behavioral Science Corp.; 2002 (Chinese) [Manual]. [23] Vakharia VN, Duncan JS, Witt JA, Elger CE, Staba R, Engel Jr J. Getting the best outcomes from epilepsy surgery. Ann Neurol 2018;83(4):676–90. [24] Jayalakshmi S, Vooturi S, Vadapalli R, Somayajula S, Madigubba S, Panigrahi M. Outcome of surgery for temporal lobe epilepsy in adults – a cohort study. Int J Surg 2016;36:443–7. [25] Sabaz M, Lawson JA, Cairns DR, Duchowny MS, Resnick TJ, Dean PM, et al. The impact of epilepsy surgery on quality of life in children. Neurology 2006;66(4):557–61. [26] Bjellvi J, Olsson I, Malmgren K, Wilbe Ramsay K. Epilepsy duration and seizure outcome in epilepsy surgery: a systematic review and meta-analysis. Neurology 2019; 93(2):e159–66. [27] Meguins LC, Adry RA, Silva-Junior SC, Araujo Filho GM, Marques LH. Shorter epilepsy duration is associated with better seizure outcome in temporal lobe epilepsy surgery. Arq Neuropsiquiatr 2015;73(3):212–7. [28] van Empelen R, Jennekens-Schinkel A, van Rijen PC, Helders PJ, van Nieuwenhuizen O. Health-related quality of life and self-perceived competence of children assessed before and up to two years after epilepsy surgery. Epilepsia 2005;46(2):258–71. [29] Saraswat N, Rao K, Subbakrishna DK, Gangadhar BN. The Social Occupational Functioning Scale (SOFS): a brief measure of functional status in persons with schizophrenia. Schizophr Res 2006;81(2–3):301–9. [30] Elliott IM, Lach L, Kadis DS, Smith ML. Psychosocial outcomes in children two years after epilepsy surgery: has anything changed? Epilepsia 2008;49(4):634–41. [31] Clary LE, Vander Wal JS, Titus JB. Examining health-related quality of life, adaptive skills, and psychological functioning in children and adolescents with epilepsy presenting for a neuropsychological evaluation. Epilepsy Behav 2010;19(3):487–93. [32] Wang WH, Shih YH, Yu HY, Yen DJ, Lin YY, Kwan SY, et al. Theory of mind and social functioning in patients with temporal lobe epilepsy. Epilepsia 2015;56(7):1117–23. [33] Brinch CN, Galloway TA. Schooling in adolescence raises IQ scores. Proc Natl Acad Sci U S A 2012;109(2):425–30. [34] Jacob L, Smith L, Thoumie P, Haro JM, Stickley A, Koyanagi A. Association between intelligence quotient and disability: the role of socioeconomic status. Ann Phys Rehabil Med 2019. https://doi.org/10.1016/j.rehab.2019.07.010.
Please cite this article as: P.-T. Lin, H.-Y. Yu, Y.-J. Lu, et al., Social functioning and health-related quality of life trajectories in people with epilepsy after epi..., Epilepsy & Behavior, https://doi.org/10.1016/j.yebeh.2019.106849
6
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[35] Sheikh S, Thompson N, Bingaman W, Gonzalez-Martinez J, Najm I, Jehi L. (Re)defining success in epilepsy surgery: the importance of relative seizure reduction in patient-reported quality of life. Epilepsia 2019;60(10):2078–85. [36] Asztely F, Ekstedt G, Rydenhag B, Malmgren K. Long term follow-up of the first 70 operated adults in the Goteborg Epilepsy Surgery Series with respect to seizures, psychosocial outcome and use of antiepileptic drugs. J Neurol Neurosurg Psychiatry 2007;78(6):605–9.
[37] Edelvik A, Flink R, Malmgren K. Prospective and longitudinal long-term employment outcomes after resective epilepsy surgery. Neurology 2015;85(17):1482–90. [38] Chin PS, Berg AT, Spencer SS, Sperling MR, Haut SR, Langfitt JT, et al. Employment outcomes following resective epilepsy surgery. Epilepsia 2007;48(12):2253–7. [39] Thorbecke R, May TW, Koch-Stoecker S, Ebner A, Bien CG, Specht U. Effects of an inpatient rehabilitation program after temporal lobe epilepsy surgery and other factors on employment 2 years after epilepsy surgery. Epilepsia 2014;55(5):725–33.
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Epilepsy & Behavior journal homepage: www.elsevier.com/locate/yebeh
Social functioning and health-related quality of life trajectories in people with epilepsy after epilepsy surgery Po-Tso Lin a, Hsiang-Yu Yu a,b,⁎, Yi-Jiun Lu c, Wei-Han Wang d, Chien-Chen Chou a,b, Sanford P.C. Hsu b,c, Chun-Fu Lin b,c, Cheng-Chia Lee b,c a
Department of Neurology, Neurological Institute, Taipei Veterans General Hospital, Taipei, Taiwan Institute of Brain Science, Brain Research Center, National Yang-Ming University, Taipei, Taiwan Department of Neurosurgery, Neurological Institute, Taipei Veterans General Hospital, Taipei, Taiwan d Department of Psychology, Chung Shan Medical University, Taichung, Taiwan b c
a r t i c l e
i n f o
Article history: Received 14 October 2019 Revised 27 November 2019 Accepted 7 December 2019 Available online xxxx Keywords: Social functioning Quality of life Epilepsy Epilepsy surgery People with epilepsy
a b s t r a c t Objective: An improvement in quality of life (QoL) over time after epilepsy surgery has been demonstrated in people with epilepsy; however, social functioning has been less investigated. We conducted this study to examine whether postsurgical improvement is parallel between QoL and social functioning in patients with epilepsy. Methods: We retrospectively reviewed patients who underwent epilepsy surgery. All participants completed a comprehensive neuropsychological assessment, the Quality of Life in Epilepsy Inventory (QOLIE-89) questionnaire, and the Social and Occupational Functioning Scale for Epilepsy (SOFSE) before surgery and at 3 months, 6 months, and 1 year after surgery. Demographic and epilepsy-related information was also collected. Generalized estimating equations with identity links were used to model the QOLIE-89 and SOFSE over time and possible associated factors. A p b 0.05 was considered statistically significant. Results: A total of 76 patients, including 36 males and 43 females aged 18 to 62 years were collected. Both total QOLIE-89 and overall SOFSE improved over time after epilepsy surgery (adjusted p value b 0.001 and 0.002, respectively, with Bonferroni's correction). Total QOLIE-89 improved 3 months after surgery, while overall SOFSE showed no significant improvement until 6 months after surgery. The presurgical Full-Scale Intelligence Quotient (FSIQ) of the Wechsler Adult Intelligence Scale-III and years of education were significantly associated with time-dependent improvement for both total QOLIE-89 and overall SOFSE (p value b 0.001). At one year after surgery, overall SOFSE and total QOLIE-89 scores were significantly higher in the seizure-free group than in the nonseizure-free group (p value = 0.040 and 0.032, respectively). Conclusion: Social functioning significantly improved in people with epilepsy after surgery as QoL, but it took more time to exhibit improvement. People with better FSIQ and more years of education had better improvement in social functioning over time. The early intervention of rehabilitation programs after epilepsy surgery might be necessary to facilitate the improvement in social functioning. © 2019 Elsevier Inc. All rights reserved.
1. Introduction Epilepsy is among the most common neurologic problems. The purpose of epilepsy surgery in people with epilepsy (PWE) is to stop seizures or greatly reduce the seizure frequency [1]. However, people with or without good seizure control may have problems managing life after surgery. People's predominated aim for epilepsy surgery is in Abbreviations: PWE, people with epilepsy; HRQoL, health-related quality of life; QoL, quality of life; QOLIE, Quality of Life in Epilepsy Inventory; SOFSE, Social and Occupational Functioning Scale for Epilepsy; FSIQ, Full-Scale Intelligence Quotient; SF, seizure-free; NSF, nonseizure-free. ⁎ Corresponding author at: Neurological Institute, Taipei Veterans General Hospital, No. 201, Sec. 2, Shih-Pai Road, Taipei 11217, Taiwan. E-mail address: [email protected] (H.-Y. Yu).
the changes of social process [1]. It is mostly reflected by one's affective, psychosocial, and behavioral state [2]. As a result, apart from good seizure control, mitigation of psychosocial burden is also an utmost goal in epilepsy surgery. Health-related quality of life (HRQoL) has been suggested to greatly improve early after epilepsy surgery [3]. However, quality of life (QoL) could only partially reflect one's psychosocial status and not the whole picture [4]. Gois and colleagues [5] demonstrated that only the cognitive function domain of QoL was significantly correlated with social adjustment, not other domains. They revealed differences between QoL and social functioning. In addition, there was a gap between the improvement in QoL and social functioning after epilepsy surgery [6]. Social functioning might be overlooked in the postoperative follow-up if we focused only on
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Please cite this article as: P.-T. Lin, H.-Y. Yu, Y.-J. Lu, et al., Social functioning and health-related quality of life trajectories in people with epilepsy after epi..., Epilepsy & Behavior, https://doi.org/10.1016/j.yebeh.2019.106849
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the QoL [7]. In fact, social functioning substantially reflects the ability to be employed and maintains interpersonal relationships (IR) and therefore an independent life [8,9]. Once we notice the delayed improvement in social functioning after surgery [6], it is worth finding a solution to speed up the process of improvement. The early introduction of a rehabilitation program for PWE following surgery could help patients perceive a better psychosocial outcome [10]. Previous data focused on general social functioning in PWE following surgery, mostly based on the social function domain within the Quality of Life in Epilepsy Inventory (QOLIE), and the results were variable [11]. While some studies revealed no differences in general social functioning between surgical and nonsurgical patients [12,13], others reported significant improvement regardless of seizure status following surgery [14]. Most of the studies were cross-sectional research studies, and the time of assessment was variable and not sequentially recorded [15–18]. We would like to conduct this study to investigate the trajectories of improvement in QoL and social functioning after epilepsy surgery and possible factors affecting the improvement. 2. Methods
functioning in PWE in Taiwan. It comprises 6 dimensions, including IR, social activities (SA), communication (C), leisure activities (LA), instrumental living skill (ILS), and occupation (O). The total score is a summation of these 6 subscales and ranges from 0 to 100. Higher scores reflect better social functioning [19]. The SOFSE can also be used for a social outcome follow-up after an intervention. (2) The QOLIE
The QOLIE-89 [20] consists of 89 items within 17 subscales, including the overall QoL; emotional well-being; role limitations: emotional; social support; social isolation; energy/fatigue; seizure worry; medication effects; health discouragement; work/driving/social function; attention/concentration; language; memory; physical function; pain; role limitations: physical; and health perceptions. The total scores are further standardized to T scores ranging from 0 to 100, and higher scores indicate a better QoL. The Taiwanese version of QOLIE-89 has been shown to be a valid and reliable indicator of the QoL in PWE [21]. (3) The Intelligence Test
2.1. Patient selection and evaluation This study was approved by the institutional ethics committee of the Taipei Veterans General Hospital (TPEVGH). The data were collected from patients aged 18 years and above who underwent epilepsy surgery between April 2012 and May 2018 at TPEVGH. Our presurgical evaluation included video-electroencephalography (video-EEG), high-resolution magnetic resonance imaging (MRI), F-fluorodeoxyglucose-position emission tomography, and a comprehensive neuropsychologic assessment. The decision to perform surgery was made after a multidisciplinary seizure conference in most cases. When all data were concordant with an epileptogenic lesion on neuroimage (hippocampal atrophy, tumors, vascular malformation, or focal cortical dysplasia), a resective surgery would be arranged. Intracranial EEG studies, whether subdural grids/ strips or stereo-EEG, would be suggested before resection if there was no obvious lesion on the brain MRI, or the presumed epileptogenic region inside the eloquent cortex. The epilepsy surgery included selective amygdalohippocampectomy, corticoamygdalohippocampectomy, corticetomy, and lesionectomy according to the conclusion of presurgical evaluation. In our epilepsy surgery program, patients were asked to complete the baseline and postoperative relevant questionnaires for clinical use. We retrospectively reviewed those who completed the baseline, postoperative 3-month, 6-month, and 1-year follow-up social functioning and QoL assessment. A total of 131 PWE aged 18 years and above who were literate and able to fulfill the social functioning and QoL questionnaires were reviewed in the beginning. Among them, 56 patients were excluded because of incomplete baseline data, active psychiatric problems, progressive neurological disorder, or severe concurrent medical illness. A total of 76 patients were qualified for this analysis. Demographic information, seizure-related factors, and the Full-Scale Intelligence Quotient (FSIQ) were obtained for analysis. Seizure outcomes and whether antiepileptic medication was discontinued were assessed at 1 year after surgery. Patients were classified into two groups based on one-year seizure outcome: a seizure-free (SF) group (Engel classes IA and IB) and a nonseizure-free (NSF) groups (Engel classes IC to VIB). The location of epilepsy surgery was categorized as temporal only and extratemporal with/without temporal lobe involvement. The following three assessments were used in the study. (1) The Social Functioning Scale The Social and Occupational Functioning Scale for Epilepsy (SOFSE) [19] is a validated and psychometrically sound tool for evaluating social
The Wechsler Adult Intelligence Scale – Third edition (WAIS-III) Taiwanese version [22] is used in the present study to evaluate the FSIQ as an index of general intellectual functioning. The FSIQ is calculated using ten of the WAIS-III subtests, including Picture Completion, Vocabulary, Digit Symbol Substitution, Similarities, Block Design, Arithmetic, Matrix Reasoning, Digit Span, Information, and Symbol Searching. 2.2. Statistical analysis Analyses were performed using the International Business Machines Statistical Package for the Social Sciences (IBM SPSS) 22 program. Categorical variables were indicated as the number and percentage. For intergroup comparisons, Pearson's chi-squared, Fischer's exact, and nonparametric Mann–Whitney U tests were applied when appropriate. Longitudinal data were analyzed to investigate the changes in both overall SOFSE and total HRQoL over time within a year after epilepsy surgery by using generalized estimating equations (GEE) with identity links. The scores of each of the six dimensions of SOFSE were standardized by linear conversion to a scale of 0–100 [19] and were analyzed for changes over time with GEE as well. We further determined whether demographic and disease-related factors such as gender, the age of epilepsy onset, the duration from seizure onset to surgery, the location of epilepsy surgery, years of education, and FSIQ were associated with the magnitudes of changes. The result of the analysis was considered statistically significant when p b 0.05. 3. Results A total of 76 patients received epilepsy surgery and completed presurgical baseline SOFSE and QOLIE-89 questionnaires. All patients followed up for at least one year after epilepsy surgery. Out of 76 qualified subjects, 35 were males, and 41 were females; the average age was 31.84 (range: 18 to 62). There were some missed or incomplete SOFSE or QOLIE-89 questionnaires in the following 3 months, 6 months, or 1 year after surgery. The number of patients with postoperative 3month, 6-month and 1-year eligible SOFSE scores was 57, 65, and 60, respectively, and was 64, 69, and 58 for QOLIE-89 scores, respectively (Little's test of missing completely at random [MCAR] test with p value = 0.081 and 0.774, respectively). In these 76 patients, there were 10 patients with headache, 7 patients with hypertension, and 1 patient with type II diabetes mellitus.
Please cite this article as: P.-T. Lin, H.-Y. Yu, Y.-J. Lu, et al., Social functioning and health-related quality of life trajectories in people with epilepsy after epi..., Epilepsy & Behavior, https://doi.org/10.1016/j.yebeh.2019.106849
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3.1. Seizure outcome Eighteen patients (23.7%) had recurrent seizures 1 year after surgery (NSF group); fifty-eight patients (76.3%) became SF (SF group). In the NSF group, 15 patients had improvement in seizure control compared to their condition before surgery (Engel classes IIA to IIIA). In our program, we usually started to taper off antiepileptic drugs (AEDs) after 2-year freedom from seizures. Only 4 patients discontinued antiepileptic medication in the SF group, none in the NSF group. A younger age of epilepsy onset and a longer duration of epilepsy were associated with seizure recurrence after surgery (p value = 0.031 and 0.003, respectively). There was no significant difference in baseline overall SOFSE and total QOLIE scores between groups (p value = 0.153 and 0.345, respectively). Gender, education, baseline FSIQ, surgery location (temporal only vs. extratemporal with/without temporal lobe), and the side of surgery were not different between patients with or without SF (Table 1).
3.2. Changes in social functioning and QoL over time Both total QOLIE-89 and overall SOFSE scores improved over time after epilepsy surgery (Bonferroni adjusted p value b 0.001 and 0.002, respectively). The total QOLIE-89 significantly improved at 3, 6, and 12 months after surgery (all p value b 0.001) and improved most at the 3-month follow-up; however, the overall SOFSE showed no significant improvement until 6 months after surgery (p value = 0.903, 0.009, and 0.001, respectively, at 3, 6, and 12 months after surgery) (Fig. 1). Baseline FSIQ and years of education were significantly associated with the time-dependent improvement in both total QOLIE-89 and overall SOFSE (p value b 0.001). Gender, the age of epilepsy onset, the duration from epilepsy onset to surgery, and surgery location showed no significant relationship with improvement in QoL or social functioning. Table 1 The demographic and epilepsy-related data of the cohort. Group
Gender Male (%) Female (%) Age of epilepsy onset (years) Mean Median Range Duration epilepsy to surgery (years) Mean Median Range Surgery location Temporal lobe only (%) Extratemporal with/without temporal lobe (%) Side of location Right side (%) Left side (%) Education (years) Mean Range Baseline Full-Scale IQ Mean Range Overall SOFSE score Mean Range Total QOLIE-89 T score Mean Range SF: seizure-free, NSF: nonseizure-free. ⁎ p value b 0.05.
SF (n = 58)
NSF (n = 18)
26 (44.8%) 32 (55.2%)
9 (50.0%) 9 (50.0%)
19.84 17.00 2–58
12.72 12.50 2–24
11.31 9.00 0–45
19.06 17.00 3–49
51 (87.9%) 7 (12.1%)
12 (66.7%) 6 (33.3%)
25 (43.1%) 33 (56.9%)
7 (38.9%) 11 (61.1%)
13.72 6–18
12.94 6–16
87.67 43–111
81.18 63–106
64.16 15–87
57.83 23–82
p value 0.701
0.031⁎
0.002⁎
0.067
0.752
0.408
0.074
0.153
0.345 47.30 43.61 21.53–80.16 18.66–71.66
3
The overall SOFSE and the IR, C, and ILS dimensions of the SOFSE revealed no significant improvement at 3 months after surgery but became significant over time thereafter (p value = 0.016, 0.021, and 0.001 at 6 months after surgery in the IR, C, and ILS, respectively). The O dimension showed significant improvement at 1 year (p value = 0.046). However, SA and LA did not change significantly over time (p value = 0.807 and 0.292, respectively), but there was a trend of improvement. The dimensions of the SOFSE did not improve in a parallel pattern (Fig. 2). 3.3. Social functioning and QoL between the SF and NSF groups At one year after surgery, the overall SOFSE and total QOLIE-89 scores were significantly higher in the SF group than in the NSF group (p value = 0.040 and 0.032, respectively). In addition, O was the only dimension of SOFSE that had significantly higher scores in the SF group than in the NSF group (p value = 0.011) (Table 2). However, in the GEE model, seizure outcome was not associated with time-dependent improvement in either overall SOFSE or total QOLIE-89 (p value = 0.069 and 0.106, respectively). 4. Discussion In this study, 76.3% of participants became SF one year after epilepsy surgery. The outcomes were comparable to most of the published data [3,11,12,18,23–25]. The earlier introduction of epilepsy surgery in PWE could obtain a better outcome [26]. In our study, patients with an older age of epilepsy onset and a shorter duration from epilepsy onset to surgery had significantly higher chances of being SF, as with many other reports, which supported the hypothesis that people with shorter epilepsy duration were more likely to be SF at follow-up [24,26,27]. The social functioning and QoL both improved after surgery in our cohort. We found that QoL improved over time following surgery as early as 3 months, but as for social functioning, not as observed in QoL, our analysis revealed no significant improvement in overall SOFSE scores at 3 months after surgery. There was a disparity in the speed of improvement between HRQoL and social functioning. Susan S. Spencer and colleagues [3] reported that QOLIE-89 scores increased significantly within 6 months after surgery, and Sarah J. Wilson and colleagues [6] noted the greatest improvement in HRQoL at 3 months after epilepsy surgery on average. Health-related quality of life scores improved over time soon after the surgery. However, self-perceived psychosocial adjustment changes after surgery did not appear until after 1 year on average [6]. Other studies reported that self-perceived improvements in social functioning among PWE required longer than 2 years to develop [17,28]. Accordingly, we suggested that the improvement in QoL might prevail in social functioning in PWE following surgery. This phenomenon is most likely due to one's psychosocial features of the adjustment that needed more time to improve, which cannot be explained by HRQoL [7]. There are six dimensions within SOFSE scores, and each one stands for the different aspects of social functioning [19]. From the subscales of our study, IR, C, ILS, and O improved over time, but there was a time difference. The significant improvement in occupational status occurred as late as 1 year. We speculated that this improvement in occupational status requires the ability to spend time in a structured and meaningful way, including gainful employment, household work, or studying [29]. This requires more time to achieve. We also noted that SA and LA did not change significantly over time, but there was a trend of improvement. Mary Lou Smith and colleagues [12] explored psychosocial outcomes in PWE, which revealed significant effects on the social and social problems subscales approximately 2 years after surgery but no changes at one year after surgery [12,30]. Among the dimensions of social functioning, the improvement speed after surgery varies, which implies that postoperative interventions, like rehabilitation, need to be
Please cite this article as: P.-T. Lin, H.-Y. Yu, Y.-J. Lu, et al., Social functioning and health-related quality of life trajectories in people with epilepsy after epi..., Epilepsy & Behavior, https://doi.org/10.1016/j.yebeh.2019.106849
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Fig. 1. Comparison of overall SOFSE scores and total QOLIE-89 T scores. The trajectories between overall SOFSE and total QOLIE-89 after surgery increased over time but were not parallel. ‡: p value b 0.05.
comprehensive and targeted different social functioning dimensions with a certain time schedule. We investigated possible clinical and demographic variables affecting the time-dependent improvement in overall SOFSE and total HRQoL following surgery. Baseline FSIQ and years of education were significant factors. Previous literature has revealed that total HRQoL is significantly correlated with FSIQ both before and after surgery [14,31]. FSIQ also demonstrated a positive correlation with overall SOFSE scores [32]. With more years of education, such as for college-educated subjects, patients could obtain more benefits to alleviate cognitive distress within HRQoL [3]. There were few former reports describing the correlation of the magnitude of improvement in QoL and social functioning with FSIQ and years of education. Via schooling, the intelligence of people between 10 and 20 years could increase [33], and with better intelligence, people obtain more processing skills and psychomotor coordination to assist in adjusting to a major life change [34]. Seizure outcome did not influence the time-dependent improvement in HRQoL and social functioning in our study. This result suggested that the speed of improvement after surgery was not related to seizure freedom. Previous longitudinal investigations comparing PWE before
and after surgery suggested that improvements in HRQoL can be observed only in completely SF patients [25], while other reports indicated that children who have Engel class II and III outcomes could experience similar HRQoL changes as children with Engel class I outcomes, and the cognitive functioning and emotional functioning stay the same [14]. Shehryar Sheikh and colleagues [35] demonstrated that relative seizure reduction with a mean value of 73% could predict postoperative QoL just as strongly as seizure freedom. This meant that any degree of improvement in seizures was associated with QoL improvement. Most of the patients in the NSF group in this study showed worthwhile improvement in seizure control, which supported the idea that whether the outcome was SF or not, both social functioning and QoL could improve over time. In the SF groups, there were higher total QOLIE-89 and overall SOFSE scores than in the group with recurrent seizures at one year after surgery, especially on the subscales of O. A favorable employment status was associated with seizure freedom and presurgical employment, which is consistent with other studies [36–38]. As a result, this study strengthened the benefit of surgical intervention to obtain a good seizure outcome and subsequent employment status. According to the published data, the early rehabilitation program had the same impact
Fig. 2. Comparison of 6 dimensions of SOFSE score. Each dimension score was standardized. The speed of improvement varied among dimensions. C: communication, ILS: instrumental living skill, IR: interpersonal relationships, LA: leisure activities, O: occupation, SA: social activities. ‡: p value b 0.05.
Please cite this article as: P.-T. Lin, H.-Y. Yu, Y.-J. Lu, et al., Social functioning and health-related quality of life trajectories in people with epilepsy after epi..., Epilepsy & Behavior, https://doi.org/10.1016/j.yebeh.2019.106849
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Table 2 Summary of different scales at one year after epilepsy surgery between the SF and NSF groups. Group
Overall SOFSE
SOFSE_IR
SOFSE_C
SOFSE_SA
SOFSE_LA
SOFSE_ILS
SOFSE_O
Total QOLIE-89
SF (n = 58) NSF (n = 18) p value
66.62 58.62 0.040⁎
79.82 76.11 0.353
61.22 58.50 0.640
59.76 50.28 0.136
62.14 56.32 0.352
80.55 71.10 0.136
70.41 58.70 0.011⁎
54.09 47.34 0.032⁎
SF: seizure-free, NSF: nonseizure-free, C: communication, ILS: instrumental living skill, IR: interpersonal relationships, LA: leisure activities, O: occupation, SA: social activities. ⁎ p value b 0.05.
as seizure freedom on vocational outcomes [39]. Further investigation of the early rehabilitation program in PWE after surgery on vocational and other psychosocial outcomes is warranted. The limitations of our study included the small sample size and the short follow-up duration. Trajectories beyond 2 or 3 years might give us more information. There were some missed data; however, the missed data were acceptable in our statistical analysis. Another limitation was that we evaluated the social functioning mainly based on the SOFSE questionnaire, and other social determinants of functioning such as personal income, social support, and access to care were not available. We included only patients who could complete the questionnaires. For those who could not read, relatively patients with disability, we were not able to assess their psychosocial change after surgery. 5. Conclusion Our study revealed that social functioning significantly improved in PWE after epilepsy surgery compared with health-related QoL, but they had different trajectories. People with epilepsy with higher baseline FSIQ and more years of education had greater time-dependent improvement in these two scales. In addition, we found that older epilepsy onset age and shorter duration from epilepsy onset to surgery were significantly associated with better seizure outcomes following surgery. Taken as a whole, the results of this study confirm the beneficial impact of epilepsy surgery on social functioning and HRQoL, with the evidence of more time needed to improve social functioning. Therefore, early intervention of rehabilitation programs in these patients might facilitate the improvement in social functioning. Ethical publication statement We confirm that we have read the journal's position on issues involved in ethical publication and affirm that this report is consistent with those guidelines. Acknowledgments This study was supported in parts by a grant from the National Science Council of Taiwan (102-2314-B-075-073) and Taipei Veterans General Hospital (V103C-107 and V108C-193). Declaration of competing interest The authors declare no potential conflicts of interest with respect to the research, authorship, and/or publication of this article. References [1] Taylor DC, McMacKin D, Staunton H, Delanty N, Phillips J. Patients' aims for epilepsy surgery: desires beyond seizure freedom. Epilepsia 2001;42(5):629–33. [2] Wilson SJ, Bladin PF, Saling MM. The burden of normality: a framework for rehabilitation after epilepsy surgery. Epilepsia 2007;48(Suppl. 9):13–6. [3] Spencer SS, Berg AT, Vickrey BG, Sperling MR, Bazil CW, Haut S, et al. Health-related quality of life over time since resective epilepsy surgery. Ann Neurol 2007;62(4): 327–34. [4] Whitcomb JJ. Functional status versus quality of life: where does the evidence lead us? ANS Adv Nurs Sci 2011;34(2):97–105.
[5] Gois J, Valente K, Vicentiis S, Moschetta S, Kuczynski E, Fiore L, et al. Assessment of psychosocial adjustment in patients with temporal lobe epilepsy using a standard measure. Epilepsy Behav 2011;20(1):89–94. [6] Wilson SJ, Wrench JM, McIntosh AM, Bladin PF, Berkovic SF. Profiles of psychosocial outcome after epilepsy surgery: the role of personality. Epilepsia 2010;51(7):1133–8. [7] Wilson S, Bladin P, Saling M. The "burden of normality": concepts of adjustment after surgery for seizures. J Neurol Neurosurg Psychiatry 2001;70(5):649–56. [8] Bosc M. Assessment of social functioning in depression. Compr Psychiatry 2000;41 (1):63–9. [9] Steiger BK, Jokeit H. Why epilepsy challenges social life. Seizure 2017;44:194–8. [10] Martin R. The burden of normality in the epilepsy postsurgery setting: out with the old and in with the new (…roles). Epilepsy Curr 2016;16(6):375–7. [11] Braams O, Maher C, Jennekens-Schinkel A, Braun K, van Nieuwenhuizen O, van Schooneveld M, et al. Social functioning of children after epilepsy surgery: a literature review. Epilepsy Behav 2019;96:210–8. [12] Smith ML, Elliott IM, Lach L. Cognitive, psychosocial, and family function one year after pediatric epilepsy surgery. Epilepsia 2004;45(6):650–60. [13] Puka K, Smith ML. Predictors of long-term quality of life after pediatric epilepsy surgery. Epilepsia 2015;56(6):873–81. [14] Titus JB, Lee A, Kasasbeh A, Thio LL, Stephenson J, Steger-May K, et al. Health-related quality of life before and after pediatric epilepsy surgery: the influence of seizure outcome on changes in physical functioning and social functioning. Epilepsy Behav 2013;27(3):477–83. [15] Suurmeijer TP, Reuvekamp MF, Aldenkamp BP. Social functioning, psychological functioning, and quality of life in epilepsy. Epilepsia 2001;42(9):1160–8. [16] Wilson SJ, Bladin PF, Saling MM, Pattison PE. Characterizing psychosocial outcome trajectories following seizure surgery. Epilepsy Behav 2005;6(4):570–80. [17] Hum KM, Smith ML, Lach L, Elliott IM. Self-perceptions of social function 2 years after pediatric epilepsy surgery. Epilepsy Behav 2010;17(3):354–9. [18] Kemp S, Garlovsky J, Reynders H, Caswell H, Baker G, Shah E. Predicting the psychosocial outcome of epilepsy surgery: a longitudinal perspective on the 'burden of normality'. Epilepsy Behav 2016;60:149–52. [19] Wang WH, Yu HY, Yen DJ, Lin YY, Kwan SY, Chen C, et al. The Social and Occupational Functioning Scale for Epilepsy (SOFSE): a brief measure of functional status in a Taiwanese sample with epilepsy. Epilepsia 2013;54(5):888–97. [20] Devinsky O, Vickrey BG, Cramer J, Perrine K, Hermann B, Meador K, et al. Development of the quality of life in epilepsy inventory. Epilepsia 1995;36(11):1089–104. [21] Zhao Y, Ding C, Wang Y, Li Z, Zhou Y, Huang Y. Reliability and validity of a Chinese version of the Quality of Life in Epilepsy Inventory (QOLIE-89). Epilepsy Behav 2007;11(1):53–9. [22] HY CJC. Wechsler Adult Intelligence Scale. . 3rd ed.Taipei: Chinese Behavioral Science Corp.; 2002 (Chinese) [Manual]. [23] Vakharia VN, Duncan JS, Witt JA, Elger CE, Staba R, Engel Jr J. Getting the best outcomes from epilepsy surgery. Ann Neurol 2018;83(4):676–90. [24] Jayalakshmi S, Vooturi S, Vadapalli R, Somayajula S, Madigubba S, Panigrahi M. Outcome of surgery for temporal lobe epilepsy in adults – a cohort study. Int J Surg 2016;36:443–7. [25] Sabaz M, Lawson JA, Cairns DR, Duchowny MS, Resnick TJ, Dean PM, et al. The impact of epilepsy surgery on quality of life in children. Neurology 2006;66(4):557–61. [26] Bjellvi J, Olsson I, Malmgren K, Wilbe Ramsay K. Epilepsy duration and seizure outcome in epilepsy surgery: a systematic review and meta-analysis. Neurology 2019; 93(2):e159–66. [27] Meguins LC, Adry RA, Silva-Junior SC, Araujo Filho GM, Marques LH. Shorter epilepsy duration is associated with better seizure outcome in temporal lobe epilepsy surgery. Arq Neuropsiquiatr 2015;73(3):212–7. [28] van Empelen R, Jennekens-Schinkel A, van Rijen PC, Helders PJ, van Nieuwenhuizen O. Health-related quality of life and self-perceived competence of children assessed before and up to two years after epilepsy surgery. Epilepsia 2005;46(2):258–71. [29] Saraswat N, Rao K, Subbakrishna DK, Gangadhar BN. The Social Occupational Functioning Scale (SOFS): a brief measure of functional status in persons with schizophrenia. Schizophr Res 2006;81(2–3):301–9. [30] Elliott IM, Lach L, Kadis DS, Smith ML. Psychosocial outcomes in children two years after epilepsy surgery: has anything changed? Epilepsia 2008;49(4):634–41. [31] Clary LE, Vander Wal JS, Titus JB. Examining health-related quality of life, adaptive skills, and psychological functioning in children and adolescents with epilepsy presenting for a neuropsychological evaluation. Epilepsy Behav 2010;19(3):487–93. [32] Wang WH, Shih YH, Yu HY, Yen DJ, Lin YY, Kwan SY, et al. Theory of mind and social functioning in patients with temporal lobe epilepsy. Epilepsia 2015;56(7):1117–23. [33] Brinch CN, Galloway TA. Schooling in adolescence raises IQ scores. Proc Natl Acad Sci U S A 2012;109(2):425–30. [34] Jacob L, Smith L, Thoumie P, Haro JM, Stickley A, Koyanagi A. Association between intelligence quotient and disability: the role of socioeconomic status. Ann Phys Rehabil Med 2019. https://doi.org/10.1016/j.rehab.2019.07.010.
Please cite this article as: P.-T. Lin, H.-Y. Yu, Y.-J. Lu, et al., Social functioning and health-related quality of life trajectories in people with epilepsy after epi..., Epilepsy & Behavior, https://doi.org/10.1016/j.yebeh.2019.106849
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[35] Sheikh S, Thompson N, Bingaman W, Gonzalez-Martinez J, Najm I, Jehi L. (Re)defining success in epilepsy surgery: the importance of relative seizure reduction in patient-reported quality of life. Epilepsia 2019;60(10):2078–85. [36] Asztely F, Ekstedt G, Rydenhag B, Malmgren K. Long term follow-up of the first 70 operated adults in the Goteborg Epilepsy Surgery Series with respect to seizures, psychosocial outcome and use of antiepileptic drugs. J Neurol Neurosurg Psychiatry 2007;78(6):605–9.
[37] Edelvik A, Flink R, Malmgren K. Prospective and longitudinal long-term employment outcomes after resective epilepsy surgery. Neurology 2015;85(17):1482–90. [38] Chin PS, Berg AT, Spencer SS, Sperling MR, Haut SR, Langfitt JT, et al. Employment outcomes following resective epilepsy surgery. Epilepsia 2007;48(12):2253–7. [39] Thorbecke R, May TW, Koch-Stoecker S, Ebner A, Bien CG, Specht U. Effects of an inpatient rehabilitation program after temporal lobe epilepsy surgery and other factors on employment 2 years after epilepsy surgery. Epilepsia 2014;55(5):725–33.
Please cite this article as: P.-T. Lin, H.-Y. Yu, Y.-J. Lu, et al., Social functioning and health-related quality of life trajectories in people with epilepsy after epi..., Epilepsy & Behavior, https://doi.org/10.1016/j.yebeh.2019.106849