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Cognition, behavior, and the ILAE Classification of the Epilepsies: A view from Africa
YEBEH-04815; No of Pages 2 Epilepsy & Behavior xxx (2016) xxx–xxx
Contents lists available at ScienceDirect
Epilepsy & Behavior journal homepage: www.elsevier.com/locate/yebeh
Review
Cognition, behavior, and the ILAE Classification of the Epilepsies: A view from Africa John T. Langfitt ⁎ Dept. of Neurology, University of Rochester Medical Center, Rochester, NY, USA Dept. of Psychiatry, University of Rochester Medical Center, Rochester, NY, USA
a r t i c l e
i n f o
Article history: Received 31 January 2016 Revised 1 April 2016 Accepted 2 April 2016 Available online xxxx
a b s t r a c t Recent ILAE revisions to the definition and classification of the epilepsies have highlighted cognitive–behavioral comorbidities (CBCs). Integrating a CBC dimension within a formal classification scheme would more fully account for the burden of epilepsy. This would be technically challenging, because we use fundamentally different methods to conceptualize, define, and diagnose CBCs that require additional expertise. In low resource settings such as sub-Saharan Africa (SSA), CBC burden is high. Existing classification systems are inevitably simplified in practice, because complex classifications require training and technologies that rarely exist in these settings. This makes low-resource settings a good place to develop simple methods to integrate CBCs into existing classifications so that they ultimately will communicate the full burden of epilepsy. This article is part of a Special Issue entitled “The new approach to classification: Rethinking cognition and behavior in epilepsy”. © 2016 Elsevier Inc. All rights reserved.
“Q: How do you eat an elephant? A: One bite at a time.” — Popular African riddle Should the ILAE Classification of the Epilepsies incorporate cognitive– behavioral comorbidities (CBCs) into its evolving framework? It is useful to consider this proposal from the perspective of resource-limited settings, where ~80% of the world's people with epilepsy live. A classification system that captures the full diversity of human epilepsy would highlight environmental and population differences that could provide critical insights into epileptogenesis, epilepsy pathophysiology, and effective treatments [1]. It would be in keeping with the goals of the ILAE/WHO/IBE ‘Out of the Shadows’ initiative to “increase public and professional awareness of epilepsy, as a universal treatable brain disorder”. Classifications should validly reflect the most current and comprehensive understanding of a disease. They should be flexible enough to assimilate and accommodate knowledge and concepts as they emerge over time. To be useful in resource-limited settings, they must also be a) clinically relevant locally; b) clear, simple, and direct as possible in terminology; c) usable by nonspecialist physicians and health care workers; and d) inclusive of the critical information required for public health and health policy planning [1]. In 2005, the ILAE redefined epilepsy as “a disorder of the brain characterized by an enduring predisposition to generate epileptic seizures and (emphasis mine) by the neuro-biologic, cognitive, psychological, ⁎ Dept. of Neurology, University of Rochester Medical Center, Rochester, NY, USA.
and social consequences of this condition” [2]. In its 2010 revision, the ILAE Commission on Classification and Terminology repeatedly recognized a CBC dimension to the epilepsies [3]. It noted that 1) the historically ‘idiopathic’ epilepsies were associated with “a variety of subtle cognitive and behavioral disorders”; 2) electroclinical syndromes included “cognitive and developmental antecedents and consequences”; 3) “epileptic encephalopathy embodies the notion that the epileptic activity itself may contribute to severe cognitive and behavioral impairments”; 4) “cognitive losses (occur) over time from uncontrolled seizures”; and 5) other dimensions that may prove useful in organizing the epilepsies include “cognitive and psychiatric status”. If one accepts the ILAE statements above, it is conceptually selfevident that the burden of epilepsy would be more accurately captured by including a CBC dimension. An integrated multidimensional system could maintain the independence of CBCs and seizures at a descriptive level, while embodying their essential relatedness. Others have proposed multidimensional classifications that consider functional status and other comorbidities but not a cognitive–behavioral dimension specifically [1]. Practically, certain technical barriers would need to be overcome. In resource-rich settings, CBC classification typically requires clinical judgments that are complex, fluid, and beyond the skill sets of most users. Epilepsy classification currently relies on clinical history, diagnostic biomarkers (EEG, MRI), and seizures. Seizures are discrete, episodic, stereotyped, and unambiguously abnormal behaviors. They can be detected and classified by a trained neurologist or other professionals, based on a detailed description by an informed witness. On the other
http://dx.doi.org/10.1016/j.yebeh.2016.04.012 1525-5050/© 2016 Elsevier Inc. All rights reserved.
Please cite this article as: Langfitt JT, Cognition, behavior, and the ILAE Classification of the Epilepsies: A view from Africa, Epilepsy Behav (2016), http://dx.doi.org/10.1016/j.yebeh.2016.04.012
2
J.T. Langfitt / Epilepsy & Behavior xxx (2016) xxx–xxx
hand, CBCs reflect extreme ends of a wide range of continuous, latent traits. They manifest quite variably across individuals and environments. Clinical history is helpful but often nonspecific. There are currently no diagnostic biomarkers that provide reliable classifications at an individual level. Cognitive–behavioral comorbidities are defined by a patient crossing a normatively based threshold of subjective symptoms or objective performance that is detected by time-consuming psychometric measures. Most medical professionals or field investigators are not trained to administer or interpret them. From this perspective, implementing a CBC dimension would further complicate an already-complex and resource-intensive system. Paradoxically, this is actually less likely to be true in resource-limited settings, because most of the complexity of the current classification system falls away in the face of the same resource limitations. Most persons with epilepsy in sub-Saharan Africa (SSA) who have nonconvulsive seizures, a specific electroclinical syndrome, and/or a structural/ metabolic etiology cannot be accurately classified. Studies in SSA have mostly addressed convulsive epilepsy because nonconvulsive epilepsy may not be noticed by family members and thus is not well captured in surveys [4]. Over half the population do not have access to any clinical care. There are ~ 6 neurologists providing epilepsy care per 10 M Africans [5], so those who do have access are mostly seen by nonspecialist physicians, clinical officers or nonprofessional health care workers. Zambia (pop. 15.5 M) and Malawi (pop. 17.7 M) have one MRI scanner each. Therefore, in routine clinical or epidemiologic use, the classification is effectively limited to distinguishing between persons with and without epilepsy and those with focal vs. generalized seizures. This is not to suggest that this situation is any way acceptable. It is to acknowledge that adding information to the current classification in resource-limited settings may be less burdensome than would initially appear. Another barrier is that diagnosis of CBCs requires appropriatelytrained psychologists and well-developed psychological instruments. These are costly and scarce resources, even in wealthy countries. However, this diagnostic standard cannot be applied in most resourcelimited settings where trained psychologists and valid, culturally appropriate instruments are so rare as to be effectively nonexistent at a population level. Again, this is not to accept the situation but simply to recognize that “the perfect is the enemy of the very good” in such settings. Simpler field measures often suffice where CBCs are common, many are clinically obvious, and an important initial goal is to describe the general scope of the problem. In a large epidemiologic study of convulsive epilepsy across 5 SSA countries, 31% of cases with focal epilepsy and 19% of cases with generalized epilepsy had cognitive impairment, as determined simply from their orientation to time, place, and person and ability to follow instructions during a neurologic examination [6]. Brief, epidemiologic surveys of disruptive and adaptive behavior would improve precision of these estimates at a fairly low cost. Several, such as the Strengths and Difficulties Questionnaire and the WHO Disability Adjustment Schedule 2.0, have been adapted and validated in SSA [7,8]. Novel reaction time measures are sensitive to mild cognitive dysfunction in wealthy countries, can be constructed of local materials, and have been applied in resourcelimited settings with initial promise [9]. Ultimately, practitioners and researchers in SSA will need more precise, graded, and culturally appropriate CBC measures for clinical evaluations and for assessing outcomes of interventions. For example, a measure that was developed within the local culture identified new developmental delays in cerebral malaria survivors [10]. However, in the same study, a simple translation of the Child Behavior Checklist (CBCL) failed to discriminate cases from controls, despite severe behavior abnormalities reported by parents of 11% of cases. In part, this may be because cultures differ in the behaviors that are considered disruptive [11]. A positive response to the CBCL item ‘sets fires’ captures a behavior that is highly disruptive in Western cultures but reflects obedience and competence in a rural African boy. In the meantime, we can provide a more accurate estimate of epilepsy burden by
incorporating data from brief, culturally validated CBC screening measures, even if the estimate is not as precise as we might like. The CBC burden associated with epilepsy in SSA is likely to be much greater than in wealthy countries, so it is all the more critical to account for it. Uncontrolled seizures, status epilepticus, and structural–metabolic etiologies (e.g., perinatal trauma, CNS infections, traumatic brain injury) are more common and are commonly associated with CBCs. Malnutrition may be both a cause (via reduced immune function) and an effect of epilepsy (sick children often are fed less than their siblings) and is associated with CBCs. Epilepsy remains a highly stigmatized condition in SSA, increasing CBC risk. ‘Nodding syndrome’ appears to be unique to SSA. It was described in East Africa in the 1960s but has reappeared in epidemic patterns in the last 15 years among internally displaced children in South Sudan, Uganda, and Tanzania [12]. It is characterized by daily ‘head nodding’ (brief atonic seizures), often provoked by eating or drinking, along with convulsions in over half of cases. Severe cognitive impairment is readily apparent in 30%. Infectious, nutritional, and genetic etiologies have been proposed, but the cause of Nodding Syndrome and its rapid re-emergence remain unclear. The mystery of nodding syndrome illustrates how important it is to account for CBCs in a part of the world where we are only beginning to comprehend the full extent and nature of the epilepsies. Disease classifications primarily serve a scientific purpose, but they also guide policy. They send a message. Excluding disease characteristics that have a high functional impact potentially misleads policymakers about the overall burden of the disease, diverting resources away from where they are truly needed. Simple methods exist for defining this dimension in ways that are immediately relevant, will spur further refinements, and will do justice to the true burden of epilepsy not only in resource-limited settings but worldwide. Conflict of interest The author has no conflicts of interest to declare. References [1] Birbeck GL. Revising and refining the epilepsy classification system: priorities from a developing world perspective. Epilepsia 2012;53(s2):18–21. [2] Fisher RS, Boas WE, Blume W, Elger C, Genton P, Lee P, et al. Epileptic seizures and epilepsy: definitions proposed by the International League Against Epilepsy (ILAE) and the International Bureau for Epilepsy (IBE). Epilepsia 2005;46(4):470–2. [3] Berg AT, Berkovic SF, Brodie MJ, Buchhalter J, Cross JH, Van Emde Boas W, et al. Revised terminology and concepts for organization of seizures and epilepsies: report of the ILAE Commission on Classification and Terminology, 2005–2009. Epilepsia 2010;51(4):676–85. [4] Newton CR, Garcia HH. Epilepsy in poor regions of the world. Lancet 2012; 380(9848):1193–201. [5] Dua T, De Boer HM, Prilipko LL, Saxena S. Epilepsy care in the world: results of an ILAE/IBE/WHO global campaign against epilepsy survey. Epilepsia 2006;47(7): 1225–31. [6] Kariuki SM, Matuja W, Akpalu A, Kakooza-Mwesige A, Chabi M, Wagner RG, et al. Clinical features, proximate causes, and consequences of active convulsive epilepsy in Africa. Epilepsia 2014;55(1):76–85. [7] Sharp C, Venta A, Marais L, Skinner D, Lenka M, Serekoane J. First evaluation of a population-based screen to detect emotional–behavior disorders in orphaned children in Sub-Saharan Africa. AIDS Behav 2014;18(6):1174–85. http://dx.doi.org/ 10.1007/s10461-014-0739-6. [8] Scorza P, Stevenson A, Canino G, Mushashi C, Kanyanganzi F, Munyanah M, et al. Validation of the “World Health Organization Disability Assessment Schedule for Children, WHODAS-Child” in Rwanda. PLoS ONE 2013;8(3), e57725. http://dx.doi. org/10.1371/journal.pone.0057725. [9] Aranha VP, Joshi R, Samuel AJ, Sharma K. Catch the moving ruler and estimate reaction time in children. Indian J Med Health Sci 2015;2(1). [10] Boivin MJ, Gladstone MJ, Vokhiwa M, Birbeck GL, Magen JG, Page C, et al. Developmental outcomes in Malawian children with retinopathy-positive cerebral malaria. Trop Med Int Health 2011;16(3):263–71. http://dx.doi.org/10.1111/j.1365-3156.2010.02704.x. [11] Lancy DF. The anthropology of childhood: cherubs, chattel and changelings. Cambridge, UK: Cambridge Univerity Press; 2015. [12] Sejvar JJ, Kakooza AM, Foltz JL, Makumbi I, Atai-Omoruto AD, Malimbo M, et al. Clinical, neurological, and electrophysiological features of nodding syndrome in Kitgum, Uganda: an observational case series. Lancet Neurol 2013;12(2):166–74.
Please cite this article as: Langfitt JT, Cognition, behavior, and the ILAE Classification of the Epilepsies: A view from Africa, Epilepsy Behav (2016), http://dx.doi.org/10.1016/j.yebeh.2016.04.012
Contents lists available at ScienceDirect
Epilepsy & Behavior journal homepage: www.elsevier.com/locate/yebeh
Review
Cognition, behavior, and the ILAE Classification of the Epilepsies: A view from Africa John T. Langfitt ⁎ Dept. of Neurology, University of Rochester Medical Center, Rochester, NY, USA Dept. of Psychiatry, University of Rochester Medical Center, Rochester, NY, USA
a r t i c l e
i n f o
Article history: Received 31 January 2016 Revised 1 April 2016 Accepted 2 April 2016 Available online xxxx
a b s t r a c t Recent ILAE revisions to the definition and classification of the epilepsies have highlighted cognitive–behavioral comorbidities (CBCs). Integrating a CBC dimension within a formal classification scheme would more fully account for the burden of epilepsy. This would be technically challenging, because we use fundamentally different methods to conceptualize, define, and diagnose CBCs that require additional expertise. In low resource settings such as sub-Saharan Africa (SSA), CBC burden is high. Existing classification systems are inevitably simplified in practice, because complex classifications require training and technologies that rarely exist in these settings. This makes low-resource settings a good place to develop simple methods to integrate CBCs into existing classifications so that they ultimately will communicate the full burden of epilepsy. This article is part of a Special Issue entitled “The new approach to classification: Rethinking cognition and behavior in epilepsy”. © 2016 Elsevier Inc. All rights reserved.
“Q: How do you eat an elephant? A: One bite at a time.” — Popular African riddle Should the ILAE Classification of the Epilepsies incorporate cognitive– behavioral comorbidities (CBCs) into its evolving framework? It is useful to consider this proposal from the perspective of resource-limited settings, where ~80% of the world's people with epilepsy live. A classification system that captures the full diversity of human epilepsy would highlight environmental and population differences that could provide critical insights into epileptogenesis, epilepsy pathophysiology, and effective treatments [1]. It would be in keeping with the goals of the ILAE/WHO/IBE ‘Out of the Shadows’ initiative to “increase public and professional awareness of epilepsy, as a universal treatable brain disorder”. Classifications should validly reflect the most current and comprehensive understanding of a disease. They should be flexible enough to assimilate and accommodate knowledge and concepts as they emerge over time. To be useful in resource-limited settings, they must also be a) clinically relevant locally; b) clear, simple, and direct as possible in terminology; c) usable by nonspecialist physicians and health care workers; and d) inclusive of the critical information required for public health and health policy planning [1]. In 2005, the ILAE redefined epilepsy as “a disorder of the brain characterized by an enduring predisposition to generate epileptic seizures and (emphasis mine) by the neuro-biologic, cognitive, psychological, ⁎ Dept. of Neurology, University of Rochester Medical Center, Rochester, NY, USA.
and social consequences of this condition” [2]. In its 2010 revision, the ILAE Commission on Classification and Terminology repeatedly recognized a CBC dimension to the epilepsies [3]. It noted that 1) the historically ‘idiopathic’ epilepsies were associated with “a variety of subtle cognitive and behavioral disorders”; 2) electroclinical syndromes included “cognitive and developmental antecedents and consequences”; 3) “epileptic encephalopathy embodies the notion that the epileptic activity itself may contribute to severe cognitive and behavioral impairments”; 4) “cognitive losses (occur) over time from uncontrolled seizures”; and 5) other dimensions that may prove useful in organizing the epilepsies include “cognitive and psychiatric status”. If one accepts the ILAE statements above, it is conceptually selfevident that the burden of epilepsy would be more accurately captured by including a CBC dimension. An integrated multidimensional system could maintain the independence of CBCs and seizures at a descriptive level, while embodying their essential relatedness. Others have proposed multidimensional classifications that consider functional status and other comorbidities but not a cognitive–behavioral dimension specifically [1]. Practically, certain technical barriers would need to be overcome. In resource-rich settings, CBC classification typically requires clinical judgments that are complex, fluid, and beyond the skill sets of most users. Epilepsy classification currently relies on clinical history, diagnostic biomarkers (EEG, MRI), and seizures. Seizures are discrete, episodic, stereotyped, and unambiguously abnormal behaviors. They can be detected and classified by a trained neurologist or other professionals, based on a detailed description by an informed witness. On the other
http://dx.doi.org/10.1016/j.yebeh.2016.04.012 1525-5050/© 2016 Elsevier Inc. All rights reserved.
Please cite this article as: Langfitt JT, Cognition, behavior, and the ILAE Classification of the Epilepsies: A view from Africa, Epilepsy Behav (2016), http://dx.doi.org/10.1016/j.yebeh.2016.04.012
2
J.T. Langfitt / Epilepsy & Behavior xxx (2016) xxx–xxx
hand, CBCs reflect extreme ends of a wide range of continuous, latent traits. They manifest quite variably across individuals and environments. Clinical history is helpful but often nonspecific. There are currently no diagnostic biomarkers that provide reliable classifications at an individual level. Cognitive–behavioral comorbidities are defined by a patient crossing a normatively based threshold of subjective symptoms or objective performance that is detected by time-consuming psychometric measures. Most medical professionals or field investigators are not trained to administer or interpret them. From this perspective, implementing a CBC dimension would further complicate an already-complex and resource-intensive system. Paradoxically, this is actually less likely to be true in resource-limited settings, because most of the complexity of the current classification system falls away in the face of the same resource limitations. Most persons with epilepsy in sub-Saharan Africa (SSA) who have nonconvulsive seizures, a specific electroclinical syndrome, and/or a structural/ metabolic etiology cannot be accurately classified. Studies in SSA have mostly addressed convulsive epilepsy because nonconvulsive epilepsy may not be noticed by family members and thus is not well captured in surveys [4]. Over half the population do not have access to any clinical care. There are ~ 6 neurologists providing epilepsy care per 10 M Africans [5], so those who do have access are mostly seen by nonspecialist physicians, clinical officers or nonprofessional health care workers. Zambia (pop. 15.5 M) and Malawi (pop. 17.7 M) have one MRI scanner each. Therefore, in routine clinical or epidemiologic use, the classification is effectively limited to distinguishing between persons with and without epilepsy and those with focal vs. generalized seizures. This is not to suggest that this situation is any way acceptable. It is to acknowledge that adding information to the current classification in resource-limited settings may be less burdensome than would initially appear. Another barrier is that diagnosis of CBCs requires appropriatelytrained psychologists and well-developed psychological instruments. These are costly and scarce resources, even in wealthy countries. However, this diagnostic standard cannot be applied in most resourcelimited settings where trained psychologists and valid, culturally appropriate instruments are so rare as to be effectively nonexistent at a population level. Again, this is not to accept the situation but simply to recognize that “the perfect is the enemy of the very good” in such settings. Simpler field measures often suffice where CBCs are common, many are clinically obvious, and an important initial goal is to describe the general scope of the problem. In a large epidemiologic study of convulsive epilepsy across 5 SSA countries, 31% of cases with focal epilepsy and 19% of cases with generalized epilepsy had cognitive impairment, as determined simply from their orientation to time, place, and person and ability to follow instructions during a neurologic examination [6]. Brief, epidemiologic surveys of disruptive and adaptive behavior would improve precision of these estimates at a fairly low cost. Several, such as the Strengths and Difficulties Questionnaire and the WHO Disability Adjustment Schedule 2.0, have been adapted and validated in SSA [7,8]. Novel reaction time measures are sensitive to mild cognitive dysfunction in wealthy countries, can be constructed of local materials, and have been applied in resourcelimited settings with initial promise [9]. Ultimately, practitioners and researchers in SSA will need more precise, graded, and culturally appropriate CBC measures for clinical evaluations and for assessing outcomes of interventions. For example, a measure that was developed within the local culture identified new developmental delays in cerebral malaria survivors [10]. However, in the same study, a simple translation of the Child Behavior Checklist (CBCL) failed to discriminate cases from controls, despite severe behavior abnormalities reported by parents of 11% of cases. In part, this may be because cultures differ in the behaviors that are considered disruptive [11]. A positive response to the CBCL item ‘sets fires’ captures a behavior that is highly disruptive in Western cultures but reflects obedience and competence in a rural African boy. In the meantime, we can provide a more accurate estimate of epilepsy burden by
incorporating data from brief, culturally validated CBC screening measures, even if the estimate is not as precise as we might like. The CBC burden associated with epilepsy in SSA is likely to be much greater than in wealthy countries, so it is all the more critical to account for it. Uncontrolled seizures, status epilepticus, and structural–metabolic etiologies (e.g., perinatal trauma, CNS infections, traumatic brain injury) are more common and are commonly associated with CBCs. Malnutrition may be both a cause (via reduced immune function) and an effect of epilepsy (sick children often are fed less than their siblings) and is associated with CBCs. Epilepsy remains a highly stigmatized condition in SSA, increasing CBC risk. ‘Nodding syndrome’ appears to be unique to SSA. It was described in East Africa in the 1960s but has reappeared in epidemic patterns in the last 15 years among internally displaced children in South Sudan, Uganda, and Tanzania [12]. It is characterized by daily ‘head nodding’ (brief atonic seizures), often provoked by eating or drinking, along with convulsions in over half of cases. Severe cognitive impairment is readily apparent in 30%. Infectious, nutritional, and genetic etiologies have been proposed, but the cause of Nodding Syndrome and its rapid re-emergence remain unclear. The mystery of nodding syndrome illustrates how important it is to account for CBCs in a part of the world where we are only beginning to comprehend the full extent and nature of the epilepsies. Disease classifications primarily serve a scientific purpose, but they also guide policy. They send a message. Excluding disease characteristics that have a high functional impact potentially misleads policymakers about the overall burden of the disease, diverting resources away from where they are truly needed. Simple methods exist for defining this dimension in ways that are immediately relevant, will spur further refinements, and will do justice to the true burden of epilepsy not only in resource-limited settings but worldwide. Conflict of interest The author has no conflicts of interest to declare. References [1] Birbeck GL. Revising and refining the epilepsy classification system: priorities from a developing world perspective. Epilepsia 2012;53(s2):18–21. [2] Fisher RS, Boas WE, Blume W, Elger C, Genton P, Lee P, et al. Epileptic seizures and epilepsy: definitions proposed by the International League Against Epilepsy (ILAE) and the International Bureau for Epilepsy (IBE). Epilepsia 2005;46(4):470–2. [3] Berg AT, Berkovic SF, Brodie MJ, Buchhalter J, Cross JH, Van Emde Boas W, et al. Revised terminology and concepts for organization of seizures and epilepsies: report of the ILAE Commission on Classification and Terminology, 2005–2009. Epilepsia 2010;51(4):676–85. [4] Newton CR, Garcia HH. Epilepsy in poor regions of the world. Lancet 2012; 380(9848):1193–201. [5] Dua T, De Boer HM, Prilipko LL, Saxena S. Epilepsy care in the world: results of an ILAE/IBE/WHO global campaign against epilepsy survey. Epilepsia 2006;47(7): 1225–31. [6] Kariuki SM, Matuja W, Akpalu A, Kakooza-Mwesige A, Chabi M, Wagner RG, et al. Clinical features, proximate causes, and consequences of active convulsive epilepsy in Africa. Epilepsia 2014;55(1):76–85. [7] Sharp C, Venta A, Marais L, Skinner D, Lenka M, Serekoane J. First evaluation of a population-based screen to detect emotional–behavior disorders in orphaned children in Sub-Saharan Africa. AIDS Behav 2014;18(6):1174–85. http://dx.doi.org/ 10.1007/s10461-014-0739-6. [8] Scorza P, Stevenson A, Canino G, Mushashi C, Kanyanganzi F, Munyanah M, et al. Validation of the “World Health Organization Disability Assessment Schedule for Children, WHODAS-Child” in Rwanda. PLoS ONE 2013;8(3), e57725. http://dx.doi. org/10.1371/journal.pone.0057725. [9] Aranha VP, Joshi R, Samuel AJ, Sharma K. Catch the moving ruler and estimate reaction time in children. Indian J Med Health Sci 2015;2(1). [10] Boivin MJ, Gladstone MJ, Vokhiwa M, Birbeck GL, Magen JG, Page C, et al. Developmental outcomes in Malawian children with retinopathy-positive cerebral malaria. Trop Med Int Health 2011;16(3):263–71. http://dx.doi.org/10.1111/j.1365-3156.2010.02704.x. [11] Lancy DF. The anthropology of childhood: cherubs, chattel and changelings. Cambridge, UK: Cambridge Univerity Press; 2015. [12] Sejvar JJ, Kakooza AM, Foltz JL, Makumbi I, Atai-Omoruto AD, Malimbo M, et al. Clinical, neurological, and electrophysiological features of nodding syndrome in Kitgum, Uganda: an observational case series. Lancet Neurol 2013;12(2):166–74.
Please cite this article as: Langfitt JT, Cognition, behavior, and the ILAE Classification of the Epilepsies: A view from Africa, Epilepsy Behav (2016), http://dx.doi.org/10.1016/j.yebeh.2016.04.012