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Stigma and quality of life at long-term follow-up after surgery for epilepsy in Uganda
Epilepsy & Behavior 52 (2015) 128–131
Contents lists available at ScienceDirect
Epilepsy & Behavior journal homepage: www.elsevier.com/locate/yebeh
Brief Communication
Stigma and quality of life at long-term follow-up after surgery for epilepsy in Uganda Anita Fletcher a, Helen Sims-Williams b, Angela Wabulya c, Warren Boling d,⁎ a
University of Louisville School of Medicine, Louisville, KY 40202, USA Sheffield Teaching Hospitals NHS Foundation Trust, South Yorkshire, UK Department of Neurology, University of North Carolina School of Medicine, 170 Manning Drive, Chapel Hill, NC 27599, USA d Department of Neurosurgery, University of Louisville, 220 Abraham Flexner Way, Louisville, KY 40202, USA b c
a r t i c l e
i n f o
Article history: Received 7 June 2015 Revised 29 August 2015 Accepted 3 September 2015 Available online 27 September 2015 Keywords: Intractable epilepsy Temporal lobe Developing world Epilepsy surgery Sub-Saharan Africa
a b s t r a c t Epilepsy is a worldwide health problem with a 10-fold greater prevalence in the developing world. Commonly, the seizure focus is in the temporal lobe, and seizures in about 30% of people with epilepsy are intractable to medication. For these individuals, surgery for intractable temporal lobe epilepsy (iTLE) is more effective than medication alone and may be the only option for cure. Intractable temporal lobe epilepsy is associated with elevated morbidity and mortality, reduced quality of life (QOL), and associated stigma particularly occurring in the developing world. Individuals with intractable epilepsy who participated in an earlier Uganda pilot study were selected for the current study based on their undergoing previous surgery for iTLE or having comparable seizure type who did not have surgery. At long-term follow-up, 10 who underwent surgery for iTLE in addition to 9 patients with focal dyscognitive type epilepsy who did not have surgery were evaluated in the current study. Tests were administered to look at various outcome parameters: seizure severity, QOL, stigma, and self-esteem. Stigma and selfesteem were additionally evaluated in the parent/caregiver. Seventy-percent of surgical resection patients were seizure-free at 8 years postsurgery. The QOLIE-31 scores were higher in surgical patients. Child/patient and parent/proxy surveys identified lower stigma in seizure-free patients. The results suggest that surgery for iTLE is an effective treatment for epilepsy in the developing world and provides an opportunity to reduce stigma and improve QOL. © 2015 Elsevier Inc. All rights reserved.
1. Introduction Epilepsy represents 0.7% of the global burden of disease [1]. The incidence of epilepsy in the developing world is approximately 10 times higher than in the developed world with incidence of epilepsy in the lowest income countries ranging from 49 to 215 per 100,000 people [2]. While prevalence rates vary among regions of Africa, an overall prevalence of 14 in 1000 has been described for sub-Saharan Africa (SSA) [2], with Uganda reported to have a high incidence of epilepsy compared with other low income countries. Specific risk factors attributable to this elevated prevalence are parasitic and other infections, perinatal events, traumatic brain injuries, HIV, and developmental or genetic etiologies of epilepsy [3]. In addition to elevated prevalence, Abbreviations: iTLE, intractable temporal lobe epilepsy; QOL, quality of life; SSA, subSaharan Africa; PWE, people with epilepsy; CCHU, Cure Children's Hospital of Uganda. ⁎ Corresponding author at: Frazier Rehab and Neuroscience Bldg., 15th floor, University of Louisville, Department of Neurosurgery, 220 Abraham Flexner Way, Louisville, KY 40202, USA. Tel.: +1 502 407 3226; fax: +1 502 899 7970. E-mail addresses: anita.m.fl[email protected] (A. Fletcher), [email protected] (H. Sims-Williams), [email protected] (W. Boling).
http://dx.doi.org/10.1016/j.yebeh.2015.09.002 1525-5050/© 2015 Elsevier Inc. All rights reserved.
mortality of intractable epilepsy is high, particularly in SSA. Uganda is reported to have a standardized mortality ratio of 7.2, among the highest in poor areas of the world [4]. Etiologies of mortality in people with epilepsy (PWE) are largely not known. However, current evidence points to injuries sustained during seizures in addition to sudden unexplained death in epilepsy. Epilepsy-associated mortality of children in Africa is closely associated with poorly controlled epilepsy, which results in more childhood death related to status epilepticus, drowning, and burns when compared with other continents [5]. In SSA, fractures, drowning, and burns are common injuries; in fact, burn scars are viewed as a mark of intractable epilepsy. Furthermore, poverty, inadequate healthcare delivery, and stigmatizing behavior such as a widespread belief in witchcraft or demonic causes of epilepsy contribute to a severe treatment gap in SSA [6,7]. Worldwide, social stigma contributes substantially to the suffering of PWE. In the developed world, progressive emergence of positive public attitudes toward PWE and public education campaigns have the potential to reduce discriminatory behavior [8]. Unfortunately, however, in the developing countries, epilepsy continues to be a highly stigmatizing condition [9–11]. Compounding the burdensome stigma of
A. Fletcher et al. / Epilepsy & Behavior 52 (2015) 128–131
epilepsy on PWE and society itself is the treatment gap worldwide in adequately addressing intractable epilepsy with effective surgical treatments [12], and this treatment gap is widest in the developing world [13]. Medically intractable epilepsy is a chronic, disabling, and dangerous disease. However, surgery for epilepsy will stop the seizures in the majority of carefully selected individuals, and seizure freedom will reduce the elevated mortality risk of epilepsy to that of age-matched controls [14]. Quality of life, as well, has been demonstrated to improve with seizure freedom [15,16]. These outcome measures identified in developed world studies of epilepsy underpin an emphasis to surgically treat intractable epilepsy when a clear opportunity for seizure freedom exists. However, these treatment outcomes of epilepsy need further clarification in the developing world. Because of the many differences between high and low resource countries, extrapolating experience in high resource areas to under-resourced areas may not be reliable. For example, patients may encounter quite diverse environments. Etiologies of disease may be dissimilar. There are differences in the type of care that can be delivered due to resource limitations of the region. Education levels are lower in severely under-resourced regions of the world. One important difference between high and low resource countries is the severe stigma associated with epilepsy in the developing world. It is likely that stigma would need to be overcome in order for quality of life to improve with treatment of epilepsy in the developing world [17]. The “low hanging fruit” of intractable epilepsy treatment is surgery of TLE. Temporal lobe epilepsy is the most common surgically treated epilepsy. Surgery of TLE is a highly effective treatment that has proven benefit in the developed world for the majority of people with epilepsy (PWE) whose seizures are not controlled on medication [18]. Boling et al. demonstrated that surgery for medically intractable TLE can be delivered with high quality in the developing world as well [19]. Additionally, our pilot study underscored the requirements to effectively and sustainably provide medical treatment in an under-resourced environment. The aim of the current study was to evaluate QOL, stigma, and selfesteem in PWE who participated in a pilot study of surgical intervention for intractable TLE in Uganda [19]. We sought to determine if there was
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a difference in the QOL, stigmatization, or self-esteem between the patients who underwent surgery and the patients who were not surgical candidates by administering validated measures evaluating these outcome parameters. Of the 49 patients who participated in the earlier pilot study, a subset of 10 individuals who had undergone surgery for iTLE and 9 patients without surgery identified to have focal dyscognitive type epilepsy were recruited for this approximately 8-year follow-up study (Table 1). Caregivers of the patients in this study were interviewed as well, using a parent/proxy version of the stigma questionnaire and an identical self-esteem scale. The authors are not aware of other studies addressing the impact of surgery for epilepsy on the stigma of epilepsy in the developed or developing world. 2. Materials and methods Patient and disease-specific data were gathered from individuals with pharmacoresistant epilepsy who had been evaluated at Cure Children's Hospital of Uganda (CCHU). Previously, patients with intractable epilepsy had been evaluated for surgery based on seizure presentation, EEG, and CT imaging [19]. The appropriate candidates with iTLE subsequently underwent surgery to resect the seizure focus. We recruited for this study 24 individuals, of whom 10 patients were treated surgically and 14 individuals had findings of focal dyscognitive epilepsy who were not candidates for surgery. These individuals were contacted by CCHU staff and offered study participation. All 10 operated individuals participated in the study. Five individuals who were not operated were lost to follow-up (Table 1). One was found to have died because of reasons unrelated to epilepsy (due to being poisoned according to patient's mother). Two could not be contacted. In one patient, the parents were unwilling to travel to CCHU, and one confirmed participation but did not arrive at CCHU for testing. Travel to and from CCHU and home village was organized by CCHU staff, and all expenses of subjects were reimbursed. A 20 US$ compensation was paid to each participant for their inconvenience due to travel to CCHU for the study. In order to assess important outcome parameters impacting QOL of patients with epilepsy and their parent or guardian, we chose multiple inventory tools that have undergone peer review and validity testing, albeit in English speaking developed world countries. The measures
Table 1 Patients evaluated at long-term follow-up with and without temporal lobe resection to treat intractable epilepsy. Age (yrs)
Sex
District
CT imaging
EEG results
Surgery
Seizure severity score
21 22 28 22 25 24 22
F F F F F F F F F M F M M M M M F M M
Tororo Tororo Tororo Tororo Tororo Tororo Tororo Tororo Mpigi Mbale Mbale Kumi Kumi Mbale Kumi Tororo Mbale Tororo Apac
No lesion Left temporo-occipital cyst/scar Enlarged right occipital horn Left temporo-occipital cyst/scar No lesion Right frontal cortical scar, BIL temporal horn enlargement Enlarged right temporal horn No CT No lesion No CT Enlarged right temporal horn No lesion No lesion left temporal horn more prominent Bilateral posterior scar Enlarged left temporal horn BIL temporal horn enlarged Left temporal atrophy No lesion Enlarged left temporal horn
Left temporal Left temporal Left temporal Left temporal Left temporal Right temporal Right temporal Left temporal Right frontal Right temporal Right frontal Multifocal Bilateral, more left posterior Left temporal Left temporal Left temporal Left temporal Left temporal
No No Left CAH No Left CAH No Right CAH No Left CAH No Right CAH No No No Left CAH No Left CAH Left CAH Left CAH
22 21 27 23 0 21 0 19 0 23 18 21 25 22 0 34 0 0 0
Right hemisphere atrophy No CT Left midtemporal cyst No lesion Left posterior temporal occipital cyst/scar
Left temporal posterior Multifocal Right frontal Left posterior temporal Left temporal
No No No No No
Parents not willing to travel to CCHU Contacted but no show for follow-up Unable to contact Unable to contact Deceased
19 20 24 17 18 20 26 18 21 26 22
Patients lost to follow-up 25 F Tororo 23 M Kampala 21 M Bushenyi-Kabwohe 18 F 28 F
CAH = corticoamygdalohippocampectomy.
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A. Fletcher et al. / Epilepsy & Behavior 52 (2015) 128–131
included: the Liverpool seizure severity scale [20], QOLIE-31 [21], child and parent stigma scale [22], and the Rosenberg self-esteem scale [23]. The patient and caregiver were interviewed separately to reduce bias in the responses offered by patient or caregiver, although 3 patients in the nonsurgical group required assistance by their caregivers during questioning due to low cognitive function and poor language skills. Language interpreters were present and assisted with interviews in all patients to translate test tools and conduct interviews as needed into a variety of Ugandan languages: Itesot, Luteso, Kiswahili, Munyoli, Atesot, Ateso, Japhadola, Swahili, Luganda, Lugisu, and Langi. The study protocol was reviewed and approved by the local IRB at CCHU. The α-level of significance was set at p = 0.05. Data were analyzed using Student's t-test and Pearson product-moment correlation. Descriptive statistics were recorded as means and corresponding standard deviation. For statistical computation, IBM SPSS version 22 was used. 3. Results Nineteen patients participated and were included in this study. Study subjects were 11 females and 8 males with age range of 17–28 years. Ten had prior surgery performed for iTLE, and 9 had prior evaluations confirming focal dyscognitive epilepsy but did not have surgery because of extratemporal lesions on imaging, unclear localization of seizure focus on EEG video telemetry, or parent not consenting to surgery. In addition to the 19 study participants, five individuals who were subjects in our earlier pilot study with focal dyscognitive epilepsy and not operated were invited to participate but were lost to follow-up (see Table 1). Seventy percent of patients who underwent surgical resection for iTLE at CCHU were seizure-free at approximately 8 years after surgery. One individual who had experienced 3 seizures in 2 years postsurgery had been seizure-free for over 5 years at this long-term follow-up. Of the 10 patients who were surgically treated for iTLE, 7 were seizurefree and free of medication, 1 reported a reduction in seizure frequency and severity, 1 reported a reduction in seizure severity, and 1 reported no change. The Liverpool seizure severity scale showed a significant difference in seizure severity between the surgical treatment group (M = 6.8, SD 11.20) and nonsurgical control group (M = 23.10, SD 4.40, t(1) = 4.10, p = b .001). Quality-of-life epilepsy inventory (QOLIE-31) contains seven multiitem scales and a single item that assesses overall health. Internal consistency reliability is reported for the multi-item scales to range from 0.77 to 0.85 [21]. In study subjects, the QOLIE-31 identified a significantly higher QOL for patients in the surgical treatment group (M = 76.15, SD 12.38) compared with nonsurgical patients (M = 55.6, SD 13.01, t(1) = 3.30, p = .002). The Austin stigma measure has two scales, one for testing the child with epilepsy and another for the parent. The parents respond to five items on a 5-point scale from 1 (strongly disagree) to 5 (strongly agree). To score, the five items are summed and divided by the number of items. A higher score reflects greater perceptions of stigma associated with their child having epilepsy. The coefficient alpha has been demonstrated to be 0.79 for the chronic epilepsy sample [22]. The child responds to 8 questions that ask to rate how often they felt or acted in the ways described in the items on a 5-point scale from 1 (never) to 5 (very often). To score, the items are summed and divided by the number of items. A higher score reflects greater perceptions of stigma [22]. The coefficient alpha was reported to be 0.81 [22]. In our study subjects, there was a significantly lower perceived stigma, based on the Austin child/patient survey, in the seizure-free patients (M = 10.14, SD 2.73) compared with those who continued with epilepsy (M = 14.30, SD = 3.68, t(1) = 2.53, p = .02). The Austin parent/proxy survey likewise revealed lower perceived stigma in seizure-free patients (M = 11.43, SD = 5.16) compared with those that still had seizures (M = 19.16, SD = 3.19, t(1) = 4.07, p = .001). Additionally, patients in the
surgical group (M = 14.00, SD = 6.46) had lower perceived stigma compared with the nonsurgical patients (M = 18.90, SD = 2.42, t(1) = 2.13, p = 0.04). Both the Austin parent/proxy and Rosenberg self-esteem evaluations of the caregiver were administered to a parent of the 10 patients. In others, testing was administered to a sibling, cousin, grandmother, or friend. The Rosenberg self-esteem scale is scored as a Likert scale. The 10 items are answered on a 4-point scale ranging from strongly agree to strongly disagree. The scale has high reliability: test–retest correlations are reported to be in the range of 0.82 to 0.88, and Cronbach's alpha for various samples in the range of 0.77 to 0.88 [24]. The Rosenberg selfesteem scale data from both patient and caregiver interviews did not identify a difference in surgical treatment vs nonsurgical control groups. In fact, all respondents reported high or normal self-esteem (p = 0.26 and p = 0.43, respectively) (Rosenberg self-esteem child: seizure group mean = 22.80, SD = 2.74; seizure-free group mean = 22.14, SD = 3.76) (Rosenberg self-esteem parent/caregiver: seizure group mean = 20.64, SD = 4.63; seizure-free group mean = 20.14, SD = 3.29). Pearson product-moment correlation was determined among seizure severity results, QOLIE-31, and Austin child/patient stigma scale for control and surgical treatment groups. A significant inverse relationship was found between seizure severity and QOL (r = −0.754, p = .0005) indicating an increased QOL as seizure severity decreased. The patients' perceived stigma of epilepsy correlated with seizure severity such that a lower seizure severity score was related to a reduction in perceived stigma (r = 0.52, p = 0.032). 4. Discussion Many facets of life are impacted by epilepsy. Personal health security is threatened by the risk of injury and elevated mortality associated with intractable epilepsy. Fear of injury, concern regarding the social consequences of having a seizure, and the stigma related to having a diagnosis of epilepsy all lead to social isolation, which impacts QOL. Stigma appears to be a driver of QOL in many regions of the world, and how stigma manifests itself can vary from region to region. Additionally, stigma can take more than one form. Baskin and Birbeck have described three types of stigma associated with epilepsy: enacted, felt, and courtesy [25]. Enacted stigma occurs when the source of discrimination is another person. Felt stigma results from a fear of being discriminated against. Courtesy stigma occurs when someone close to a PWE, in relation or proximity, feels stigmatized. Stigmatization, in all forms, limits personal, educational, and social opportunities, leading to a significant impact on the QOL of both the PWE and family members. Sub-Saharan Africa is one region where all forms of stigma are common [25]. In our study, QOL was higher in patients who were seizure-free after surgery for iTLE. In addition, the QOLIE-31 measure was highly correlated with seizure severity, pointing to increased QOL resulting from decreased seizure severity, a relationship that has been identified in developed world populations [15]. Patients anecdotally reported, in addition to the standard questions of the QOLIE-31, that epilepsy led to interpersonal and relationship problems, for example, an inability to marry or to bear children. Difficulties with societal and familial obligations such as cooking, cleaning, and farming were expressed by both patients and caregivers as a consequence of intractable seizures. Stigma was lower in our seizure-free patients; perceived stigma was lower in the parent/proxy of seizure-free patients as well. Correlation analysis of the seizure severity and the Austin child stigma scale identified that higher levels of perceived stigma were correlated with an increased seizure severity. As stigma is a driver of overall QOL, it is not surprising that both are affected by seizure severity. However, what is not clear at this point is the relative contribution of stigma on QOL in this developing world patient population. The WHO and the ILAE/IBE set forth global goals in the “Out of the Shadows” campaign. The goals include, among others, treatment and
A. Fletcher et al. / Epilepsy & Behavior 52 (2015) 128–131
education to increase the awareness of epilepsy as a noncommunicable, biophysical manifestation of disease [26]. Educating communities on the biological basis of epilepsy may decrease enacted stigma in PWE and increase the number of PWE that seek medical treatment. Experience in a southwest Ethiopia epilepsy clinic showed that patient education can positively shift knowledge of the cause of epilepsy [27]. Additionally, a significant positive correlation was found between treatment at a comprehensive epilepsy center and a positive attitude toward epilepsy, suggesting that increased accessibility and patient education can lead to a more positive outlook. A similar self-esteem reported by individuals in our study who currently have seizures and those who are seizure-free may reflect that felt stigma is often reported to be less severe than enacted stigma [25]. Alternatively, the patient population in this study is a subset of PWE who were educated in the biophysical nature of their illness during the surgical evaluation. It is feasible that such education resulted in patients who were less burdened with the stigma-laden traditional beliefs of seizure origin. Also, high selfesteem may be secondary to a positive influence of the support structure at home or school. Self-esteem in PWE in developing countries has rarely been studied and would benefit from a more in-depth analysis.
5. Conclusion Intractable TLE is a chronic disabling neurological disease that in many cases can be cured with surgery. In our Ugandan patients, QOL was higher, and stigma was significantly lower in seizure-free patients compared with those with continued epilepsy. In addition, perceived stigma was lower in the parents or parent proxy of iTLE patients seizure-free after surgery. This study identified that in a very low resource setting, surgical treatment for iTLE can result in higher QOL and lower perceived stigma in patients with iTLE as well as their parents and caregivers. The main limitations of this study are a small sample size of evaluated subjects and number of patients lost to follow-up. Additionally, the outcome measures administered to evaluate QOL, stigma, and self esteem are not validated in an East African culture or local languages. However, we encountered no obstacles in reliably conveying questions and gathering responses in multiple languages, and objective test results appeared congruent with subjective assessments of QOL, selfesteem, and stigma perception.
Acknowledgments The authors acknowledge Cure Uganda for providing facilities and the staff who contributed their time and resources that made this study possible. Particular thanks go to executive director Derek Johnson, Dr. John Mugamba, Dr. Peter Ssenyonga, Peter Sagabo, and Brian Kaaya. Juliet Mayeku provided valuable assistance in testing and evaluating patients. Disclosures None of the authors has any conflict of interest to disclose.
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Contents lists available at ScienceDirect
Epilepsy & Behavior journal homepage: www.elsevier.com/locate/yebeh
Brief Communication
Stigma and quality of life at long-term follow-up after surgery for epilepsy in Uganda Anita Fletcher a, Helen Sims-Williams b, Angela Wabulya c, Warren Boling d,⁎ a
University of Louisville School of Medicine, Louisville, KY 40202, USA Sheffield Teaching Hospitals NHS Foundation Trust, South Yorkshire, UK Department of Neurology, University of North Carolina School of Medicine, 170 Manning Drive, Chapel Hill, NC 27599, USA d Department of Neurosurgery, University of Louisville, 220 Abraham Flexner Way, Louisville, KY 40202, USA b c
a r t i c l e
i n f o
Article history: Received 7 June 2015 Revised 29 August 2015 Accepted 3 September 2015 Available online 27 September 2015 Keywords: Intractable epilepsy Temporal lobe Developing world Epilepsy surgery Sub-Saharan Africa
a b s t r a c t Epilepsy is a worldwide health problem with a 10-fold greater prevalence in the developing world. Commonly, the seizure focus is in the temporal lobe, and seizures in about 30% of people with epilepsy are intractable to medication. For these individuals, surgery for intractable temporal lobe epilepsy (iTLE) is more effective than medication alone and may be the only option for cure. Intractable temporal lobe epilepsy is associated with elevated morbidity and mortality, reduced quality of life (QOL), and associated stigma particularly occurring in the developing world. Individuals with intractable epilepsy who participated in an earlier Uganda pilot study were selected for the current study based on their undergoing previous surgery for iTLE or having comparable seizure type who did not have surgery. At long-term follow-up, 10 who underwent surgery for iTLE in addition to 9 patients with focal dyscognitive type epilepsy who did not have surgery were evaluated in the current study. Tests were administered to look at various outcome parameters: seizure severity, QOL, stigma, and self-esteem. Stigma and selfesteem were additionally evaluated in the parent/caregiver. Seventy-percent of surgical resection patients were seizure-free at 8 years postsurgery. The QOLIE-31 scores were higher in surgical patients. Child/patient and parent/proxy surveys identified lower stigma in seizure-free patients. The results suggest that surgery for iTLE is an effective treatment for epilepsy in the developing world and provides an opportunity to reduce stigma and improve QOL. © 2015 Elsevier Inc. All rights reserved.
1. Introduction Epilepsy represents 0.7% of the global burden of disease [1]. The incidence of epilepsy in the developing world is approximately 10 times higher than in the developed world with incidence of epilepsy in the lowest income countries ranging from 49 to 215 per 100,000 people [2]. While prevalence rates vary among regions of Africa, an overall prevalence of 14 in 1000 has been described for sub-Saharan Africa (SSA) [2], with Uganda reported to have a high incidence of epilepsy compared with other low income countries. Specific risk factors attributable to this elevated prevalence are parasitic and other infections, perinatal events, traumatic brain injuries, HIV, and developmental or genetic etiologies of epilepsy [3]. In addition to elevated prevalence, Abbreviations: iTLE, intractable temporal lobe epilepsy; QOL, quality of life; SSA, subSaharan Africa; PWE, people with epilepsy; CCHU, Cure Children's Hospital of Uganda. ⁎ Corresponding author at: Frazier Rehab and Neuroscience Bldg., 15th floor, University of Louisville, Department of Neurosurgery, 220 Abraham Flexner Way, Louisville, KY 40202, USA. Tel.: +1 502 407 3226; fax: +1 502 899 7970. E-mail addresses: anita.m.fl[email protected] (A. Fletcher), [email protected] (H. Sims-Williams), [email protected] (W. Boling).
http://dx.doi.org/10.1016/j.yebeh.2015.09.002 1525-5050/© 2015 Elsevier Inc. All rights reserved.
mortality of intractable epilepsy is high, particularly in SSA. Uganda is reported to have a standardized mortality ratio of 7.2, among the highest in poor areas of the world [4]. Etiologies of mortality in people with epilepsy (PWE) are largely not known. However, current evidence points to injuries sustained during seizures in addition to sudden unexplained death in epilepsy. Epilepsy-associated mortality of children in Africa is closely associated with poorly controlled epilepsy, which results in more childhood death related to status epilepticus, drowning, and burns when compared with other continents [5]. In SSA, fractures, drowning, and burns are common injuries; in fact, burn scars are viewed as a mark of intractable epilepsy. Furthermore, poverty, inadequate healthcare delivery, and stigmatizing behavior such as a widespread belief in witchcraft or demonic causes of epilepsy contribute to a severe treatment gap in SSA [6,7]. Worldwide, social stigma contributes substantially to the suffering of PWE. In the developed world, progressive emergence of positive public attitudes toward PWE and public education campaigns have the potential to reduce discriminatory behavior [8]. Unfortunately, however, in the developing countries, epilepsy continues to be a highly stigmatizing condition [9–11]. Compounding the burdensome stigma of
A. Fletcher et al. / Epilepsy & Behavior 52 (2015) 128–131
epilepsy on PWE and society itself is the treatment gap worldwide in adequately addressing intractable epilepsy with effective surgical treatments [12], and this treatment gap is widest in the developing world [13]. Medically intractable epilepsy is a chronic, disabling, and dangerous disease. However, surgery for epilepsy will stop the seizures in the majority of carefully selected individuals, and seizure freedom will reduce the elevated mortality risk of epilepsy to that of age-matched controls [14]. Quality of life, as well, has been demonstrated to improve with seizure freedom [15,16]. These outcome measures identified in developed world studies of epilepsy underpin an emphasis to surgically treat intractable epilepsy when a clear opportunity for seizure freedom exists. However, these treatment outcomes of epilepsy need further clarification in the developing world. Because of the many differences between high and low resource countries, extrapolating experience in high resource areas to under-resourced areas may not be reliable. For example, patients may encounter quite diverse environments. Etiologies of disease may be dissimilar. There are differences in the type of care that can be delivered due to resource limitations of the region. Education levels are lower in severely under-resourced regions of the world. One important difference between high and low resource countries is the severe stigma associated with epilepsy in the developing world. It is likely that stigma would need to be overcome in order for quality of life to improve with treatment of epilepsy in the developing world [17]. The “low hanging fruit” of intractable epilepsy treatment is surgery of TLE. Temporal lobe epilepsy is the most common surgically treated epilepsy. Surgery of TLE is a highly effective treatment that has proven benefit in the developed world for the majority of people with epilepsy (PWE) whose seizures are not controlled on medication [18]. Boling et al. demonstrated that surgery for medically intractable TLE can be delivered with high quality in the developing world as well [19]. Additionally, our pilot study underscored the requirements to effectively and sustainably provide medical treatment in an under-resourced environment. The aim of the current study was to evaluate QOL, stigma, and selfesteem in PWE who participated in a pilot study of surgical intervention for intractable TLE in Uganda [19]. We sought to determine if there was
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a difference in the QOL, stigmatization, or self-esteem between the patients who underwent surgery and the patients who were not surgical candidates by administering validated measures evaluating these outcome parameters. Of the 49 patients who participated in the earlier pilot study, a subset of 10 individuals who had undergone surgery for iTLE and 9 patients without surgery identified to have focal dyscognitive type epilepsy were recruited for this approximately 8-year follow-up study (Table 1). Caregivers of the patients in this study were interviewed as well, using a parent/proxy version of the stigma questionnaire and an identical self-esteem scale. The authors are not aware of other studies addressing the impact of surgery for epilepsy on the stigma of epilepsy in the developed or developing world. 2. Materials and methods Patient and disease-specific data were gathered from individuals with pharmacoresistant epilepsy who had been evaluated at Cure Children's Hospital of Uganda (CCHU). Previously, patients with intractable epilepsy had been evaluated for surgery based on seizure presentation, EEG, and CT imaging [19]. The appropriate candidates with iTLE subsequently underwent surgery to resect the seizure focus. We recruited for this study 24 individuals, of whom 10 patients were treated surgically and 14 individuals had findings of focal dyscognitive epilepsy who were not candidates for surgery. These individuals were contacted by CCHU staff and offered study participation. All 10 operated individuals participated in the study. Five individuals who were not operated were lost to follow-up (Table 1). One was found to have died because of reasons unrelated to epilepsy (due to being poisoned according to patient's mother). Two could not be contacted. In one patient, the parents were unwilling to travel to CCHU, and one confirmed participation but did not arrive at CCHU for testing. Travel to and from CCHU and home village was organized by CCHU staff, and all expenses of subjects were reimbursed. A 20 US$ compensation was paid to each participant for their inconvenience due to travel to CCHU for the study. In order to assess important outcome parameters impacting QOL of patients with epilepsy and their parent or guardian, we chose multiple inventory tools that have undergone peer review and validity testing, albeit in English speaking developed world countries. The measures
Table 1 Patients evaluated at long-term follow-up with and without temporal lobe resection to treat intractable epilepsy. Age (yrs)
Sex
District
CT imaging
EEG results
Surgery
Seizure severity score
21 22 28 22 25 24 22
F F F F F F F F F M F M M M M M F M M
Tororo Tororo Tororo Tororo Tororo Tororo Tororo Tororo Mpigi Mbale Mbale Kumi Kumi Mbale Kumi Tororo Mbale Tororo Apac
No lesion Left temporo-occipital cyst/scar Enlarged right occipital horn Left temporo-occipital cyst/scar No lesion Right frontal cortical scar, BIL temporal horn enlargement Enlarged right temporal horn No CT No lesion No CT Enlarged right temporal horn No lesion No lesion left temporal horn more prominent Bilateral posterior scar Enlarged left temporal horn BIL temporal horn enlarged Left temporal atrophy No lesion Enlarged left temporal horn
Left temporal Left temporal Left temporal Left temporal Left temporal Right temporal Right temporal Left temporal Right frontal Right temporal Right frontal Multifocal Bilateral, more left posterior Left temporal Left temporal Left temporal Left temporal Left temporal
No No Left CAH No Left CAH No Right CAH No Left CAH No Right CAH No No No Left CAH No Left CAH Left CAH Left CAH
22 21 27 23 0 21 0 19 0 23 18 21 25 22 0 34 0 0 0
Right hemisphere atrophy No CT Left midtemporal cyst No lesion Left posterior temporal occipital cyst/scar
Left temporal posterior Multifocal Right frontal Left posterior temporal Left temporal
No No No No No
Parents not willing to travel to CCHU Contacted but no show for follow-up Unable to contact Unable to contact Deceased
19 20 24 17 18 20 26 18 21 26 22
Patients lost to follow-up 25 F Tororo 23 M Kampala 21 M Bushenyi-Kabwohe 18 F 28 F
CAH = corticoamygdalohippocampectomy.
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included: the Liverpool seizure severity scale [20], QOLIE-31 [21], child and parent stigma scale [22], and the Rosenberg self-esteem scale [23]. The patient and caregiver were interviewed separately to reduce bias in the responses offered by patient or caregiver, although 3 patients in the nonsurgical group required assistance by their caregivers during questioning due to low cognitive function and poor language skills. Language interpreters were present and assisted with interviews in all patients to translate test tools and conduct interviews as needed into a variety of Ugandan languages: Itesot, Luteso, Kiswahili, Munyoli, Atesot, Ateso, Japhadola, Swahili, Luganda, Lugisu, and Langi. The study protocol was reviewed and approved by the local IRB at CCHU. The α-level of significance was set at p = 0.05. Data were analyzed using Student's t-test and Pearson product-moment correlation. Descriptive statistics were recorded as means and corresponding standard deviation. For statistical computation, IBM SPSS version 22 was used. 3. Results Nineteen patients participated and were included in this study. Study subjects were 11 females and 8 males with age range of 17–28 years. Ten had prior surgery performed for iTLE, and 9 had prior evaluations confirming focal dyscognitive epilepsy but did not have surgery because of extratemporal lesions on imaging, unclear localization of seizure focus on EEG video telemetry, or parent not consenting to surgery. In addition to the 19 study participants, five individuals who were subjects in our earlier pilot study with focal dyscognitive epilepsy and not operated were invited to participate but were lost to follow-up (see Table 1). Seventy percent of patients who underwent surgical resection for iTLE at CCHU were seizure-free at approximately 8 years after surgery. One individual who had experienced 3 seizures in 2 years postsurgery had been seizure-free for over 5 years at this long-term follow-up. Of the 10 patients who were surgically treated for iTLE, 7 were seizurefree and free of medication, 1 reported a reduction in seizure frequency and severity, 1 reported a reduction in seizure severity, and 1 reported no change. The Liverpool seizure severity scale showed a significant difference in seizure severity between the surgical treatment group (M = 6.8, SD 11.20) and nonsurgical control group (M = 23.10, SD 4.40, t(1) = 4.10, p = b .001). Quality-of-life epilepsy inventory (QOLIE-31) contains seven multiitem scales and a single item that assesses overall health. Internal consistency reliability is reported for the multi-item scales to range from 0.77 to 0.85 [21]. In study subjects, the QOLIE-31 identified a significantly higher QOL for patients in the surgical treatment group (M = 76.15, SD 12.38) compared with nonsurgical patients (M = 55.6, SD 13.01, t(1) = 3.30, p = .002). The Austin stigma measure has two scales, one for testing the child with epilepsy and another for the parent. The parents respond to five items on a 5-point scale from 1 (strongly disagree) to 5 (strongly agree). To score, the five items are summed and divided by the number of items. A higher score reflects greater perceptions of stigma associated with their child having epilepsy. The coefficient alpha has been demonstrated to be 0.79 for the chronic epilepsy sample [22]. The child responds to 8 questions that ask to rate how often they felt or acted in the ways described in the items on a 5-point scale from 1 (never) to 5 (very often). To score, the items are summed and divided by the number of items. A higher score reflects greater perceptions of stigma [22]. The coefficient alpha was reported to be 0.81 [22]. In our study subjects, there was a significantly lower perceived stigma, based on the Austin child/patient survey, in the seizure-free patients (M = 10.14, SD 2.73) compared with those who continued with epilepsy (M = 14.30, SD = 3.68, t(1) = 2.53, p = .02). The Austin parent/proxy survey likewise revealed lower perceived stigma in seizure-free patients (M = 11.43, SD = 5.16) compared with those that still had seizures (M = 19.16, SD = 3.19, t(1) = 4.07, p = .001). Additionally, patients in the
surgical group (M = 14.00, SD = 6.46) had lower perceived stigma compared with the nonsurgical patients (M = 18.90, SD = 2.42, t(1) = 2.13, p = 0.04). Both the Austin parent/proxy and Rosenberg self-esteem evaluations of the caregiver were administered to a parent of the 10 patients. In others, testing was administered to a sibling, cousin, grandmother, or friend. The Rosenberg self-esteem scale is scored as a Likert scale. The 10 items are answered on a 4-point scale ranging from strongly agree to strongly disagree. The scale has high reliability: test–retest correlations are reported to be in the range of 0.82 to 0.88, and Cronbach's alpha for various samples in the range of 0.77 to 0.88 [24]. The Rosenberg selfesteem scale data from both patient and caregiver interviews did not identify a difference in surgical treatment vs nonsurgical control groups. In fact, all respondents reported high or normal self-esteem (p = 0.26 and p = 0.43, respectively) (Rosenberg self-esteem child: seizure group mean = 22.80, SD = 2.74; seizure-free group mean = 22.14, SD = 3.76) (Rosenberg self-esteem parent/caregiver: seizure group mean = 20.64, SD = 4.63; seizure-free group mean = 20.14, SD = 3.29). Pearson product-moment correlation was determined among seizure severity results, QOLIE-31, and Austin child/patient stigma scale for control and surgical treatment groups. A significant inverse relationship was found between seizure severity and QOL (r = −0.754, p = .0005) indicating an increased QOL as seizure severity decreased. The patients' perceived stigma of epilepsy correlated with seizure severity such that a lower seizure severity score was related to a reduction in perceived stigma (r = 0.52, p = 0.032). 4. Discussion Many facets of life are impacted by epilepsy. Personal health security is threatened by the risk of injury and elevated mortality associated with intractable epilepsy. Fear of injury, concern regarding the social consequences of having a seizure, and the stigma related to having a diagnosis of epilepsy all lead to social isolation, which impacts QOL. Stigma appears to be a driver of QOL in many regions of the world, and how stigma manifests itself can vary from region to region. Additionally, stigma can take more than one form. Baskin and Birbeck have described three types of stigma associated with epilepsy: enacted, felt, and courtesy [25]. Enacted stigma occurs when the source of discrimination is another person. Felt stigma results from a fear of being discriminated against. Courtesy stigma occurs when someone close to a PWE, in relation or proximity, feels stigmatized. Stigmatization, in all forms, limits personal, educational, and social opportunities, leading to a significant impact on the QOL of both the PWE and family members. Sub-Saharan Africa is one region where all forms of stigma are common [25]. In our study, QOL was higher in patients who were seizure-free after surgery for iTLE. In addition, the QOLIE-31 measure was highly correlated with seizure severity, pointing to increased QOL resulting from decreased seizure severity, a relationship that has been identified in developed world populations [15]. Patients anecdotally reported, in addition to the standard questions of the QOLIE-31, that epilepsy led to interpersonal and relationship problems, for example, an inability to marry or to bear children. Difficulties with societal and familial obligations such as cooking, cleaning, and farming were expressed by both patients and caregivers as a consequence of intractable seizures. Stigma was lower in our seizure-free patients; perceived stigma was lower in the parent/proxy of seizure-free patients as well. Correlation analysis of the seizure severity and the Austin child stigma scale identified that higher levels of perceived stigma were correlated with an increased seizure severity. As stigma is a driver of overall QOL, it is not surprising that both are affected by seizure severity. However, what is not clear at this point is the relative contribution of stigma on QOL in this developing world patient population. The WHO and the ILAE/IBE set forth global goals in the “Out of the Shadows” campaign. The goals include, among others, treatment and
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education to increase the awareness of epilepsy as a noncommunicable, biophysical manifestation of disease [26]. Educating communities on the biological basis of epilepsy may decrease enacted stigma in PWE and increase the number of PWE that seek medical treatment. Experience in a southwest Ethiopia epilepsy clinic showed that patient education can positively shift knowledge of the cause of epilepsy [27]. Additionally, a significant positive correlation was found between treatment at a comprehensive epilepsy center and a positive attitude toward epilepsy, suggesting that increased accessibility and patient education can lead to a more positive outlook. A similar self-esteem reported by individuals in our study who currently have seizures and those who are seizure-free may reflect that felt stigma is often reported to be less severe than enacted stigma [25]. Alternatively, the patient population in this study is a subset of PWE who were educated in the biophysical nature of their illness during the surgical evaluation. It is feasible that such education resulted in patients who were less burdened with the stigma-laden traditional beliefs of seizure origin. Also, high selfesteem may be secondary to a positive influence of the support structure at home or school. Self-esteem in PWE in developing countries has rarely been studied and would benefit from a more in-depth analysis.
5. Conclusion Intractable TLE is a chronic disabling neurological disease that in many cases can be cured with surgery. In our Ugandan patients, QOL was higher, and stigma was significantly lower in seizure-free patients compared with those with continued epilepsy. In addition, perceived stigma was lower in the parents or parent proxy of iTLE patients seizure-free after surgery. This study identified that in a very low resource setting, surgical treatment for iTLE can result in higher QOL and lower perceived stigma in patients with iTLE as well as their parents and caregivers. The main limitations of this study are a small sample size of evaluated subjects and number of patients lost to follow-up. Additionally, the outcome measures administered to evaluate QOL, stigma, and self esteem are not validated in an East African culture or local languages. However, we encountered no obstacles in reliably conveying questions and gathering responses in multiple languages, and objective test results appeared congruent with subjective assessments of QOL, selfesteem, and stigma perception.
Acknowledgments The authors acknowledge Cure Uganda for providing facilities and the staff who contributed their time and resources that made this study possible. Particular thanks go to executive director Derek Johnson, Dr. John Mugamba, Dr. Peter Ssenyonga, Peter Sagabo, and Brian Kaaya. Juliet Mayeku provided valuable assistance in testing and evaluating patients. Disclosures None of the authors has any conflict of interest to disclose.
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