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The epidemiological and clinical characteristics study on epilepsy in 8 ethnic groups of China
Epilepsy Research 138 (2017) 110–115
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The epidemiological and clinical characteristics study on epilepsy in 8 ethnic groups of China
MARK
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ZhiPeng Yu , Kai Dong, Hong Chang, XiaoQin Huang, Yi Ren, ChunQiu Fan, QingFeng Ma, HaiQing Song, Qian Zhang, Jing Zhang, LiYuan Huang Department of Neurology, Xuanwu Hospital Capital Medical University, Beijing, 100191, PR China
A R T I C L E I N F O
A B S T R A C T
Keywords: Epilepsy Epidemiology Ethnic group
To survey the epidemiological characteristics and clinical features on epilepsy in eight ethnic groups in Yunnan province of China. Methodes: The investigation was based on the WHO questionnaire and ICBERG screening questionnaire. This study was performed through random cluster sampling and door-to-door survey. Results: A total of 76,302 individuals from eight ethnic groups were surveyed. The crude prevalence of epilepsy ranged from 1.2/1000 to 6.5/1000 in the eight ethnic groups, and the age-adjusted prevalence of epilepsy was from 2.1/1000 to 7.3/1000. The prevalence of active epilepsy varied from 1.0/1000 to 5.2/1000 in the eight ethnic groups, and the age-adjusted prevalence of active epilepsy was from 1.8/1000 to 6.7/1000. The age peak for seizures was below twenty, the patients of 61.1%-95.0% suffered from generalized seizures and 5%-21.2% had partial seizures. More than 60% of the cases in five ethnic groups, and the frequency of seizures were more than 10 events per year. More than 50% in other three ethnic groups, and the seizures had occurred less than 10 events per year. The treatment gap for active epilepsy ranged from 43.7% to 100.0% among the eight ethnic groups, while the natural remission rate varied from 5.6% to 21.0%. Conclusion: There were both disparity and similarity in the epidemiological and clinical features of epilepsy in different ethnic group communities.
1. Introduction The epidemiology of epilepsy is diverse in different countries and regions. The lifetime prevalence of epilepsy ranges from 3.5 to 10.7/ 1000 (Radhakrishnan, 2009) in developed countries, and from 0.9 to 74.4/1000 in Asia, sub-Saharan Africa, and Latin America (Mac et al., 2007; Burneo et al., 2005; Preux and Druet-Cabanac, 2005; Benamer and Grosset, 2009; Burneo et al., 2009). The prevalence of active epilepsy ranges from 1.5 to 74.4/1000 (Radhakrishnan, 2009). Similarly, the types and frequency of seizures vary in different countries and regions. More importantly, the epidemiological and clinical features of the disorder are diverse in different races and ethnicities. However, studies in the epidemiology of epilepsy are mostly conducted within one ethnicity in one country. Little has been discovered about the epidemiological and clinical features of epilepsy in different ethnicities. Thus, the epidemiological and clinical data of epilepsy in multi-ethnic groups
need further survey. The epidemiology of epilepsy in the Han nationality of Chinese has been conducted (Wang et al., 2003). However, there are 56 minorities in China. Data on the epidemiological and clinical features of epilepsy in different ethnicity groups remain undiscovered. Therefore, the major objective of this study is to establish epidemiological features in eight ethnic groups that inhabit in the rural areas in China. 2. Material and methods 2.1. Population and regional characteristics This study was conducted from January 2006 to September 2008, in the rural areas of Yunnan Province. Yunnan Province, located in the southwest of China, consists of 16 cities and autonomous regions, sharing boarders with Myanmar, Laos, and Vietnam (Fig. 1). It is the home to 26 ethnic groups, 15 of which are indigenous. Yunnan covers a
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Corresponding author at: Changchun Street, Xicheng District, Beijing, No. 45, PR China. E-mail addresses: [email protected] (Z. Yu), [email protected] (K. Dong), [email protected] (H. Chang), [email protected] (X. Huang), [email protected] (Y. Ren), [email protected] (C. Fan), [email protected] (Q. Ma), [email protected] (H. Song), [email protected] (Q. Zhang), [email protected] (J. Zhang), [email protected] (L. Huang). http://dx.doi.org/10.1016/j.eplepsyres.2017.10.020 Received 7 September 2017; Received in revised form 20 October 2017; Accepted 27 October 2017 0920-1211/ © 2017 Elsevier B.V. All rights reserved.
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Fig. 1. Study region and geographical situation of China.
2.3. Sample size
landmass of 394,000 square kilometers, accounting for 4.1% of Chinese territory, 94% of which is mountainous regions. Among the ethnic groups surveyed, the Achang, Deang, Bulang, Lahu, Nu, Jinuo, Wa, and Hani people inhabit in the rural areas in seven cities and autonomous regions. Comprising of 48 counties, the seven cities and autonomous regions cover an area of 167881 square kilometers, with a population of more than 13.95 million in 2000. The altitude of these investigated districts ranges from 1500 to 3500 m above sea level. Due to the underdeveloped infrastructure of transportation, most villages are one to ten hour’s drives away from the nearest urban area. Several villages are completely or relatively isolated from outside world, and can only be reached on foot. The air and water in these districts is unpolluted and a variety of vegetation grows in the areas. It is tropical or sub-tropical climate with rich rainfalls from June to October. The custom, religion, clothing, and physical appearance vary greatly among the eight ethnicities. Occupying different regions, every ethnic group maintains ancient and exclusive lifestyle. These people live in mountainous regions as peasants, and live on organic rice, vegetables, herbs, and meat. Every ethnic group speaks their own language and exogamy is not the norm.
Sample size was calculated using a formula n = (t2pq)/d2, of which n is the minimum sample size, t is the score on a gaussian distribution correspondent with a certain confidence level (we used t = 1.96), p is the presumed prevalence of the disease (0.007), q = 1 − p, and d is the desired level of precision (we accepted d = p/10). Accordingly, the total sample size for the eight ethnic groups should be not less than 54496 (1.962 × 0.993 × 100/0.007). Sample size was calculated separately for each ethnic groups surveyed. 2.4. Steps of the study We did a two-phase door-to-door survey. In phase I, a screening instrument for epilepsy was administered to inhabitants of the village who agreed to participate; in phase II, the evaluation of possible epilepsy was performed among those subjects who screened positive for that condition. 2.4.1. Phase I. screening Random cluster sampling and door-to-door survey were used in the study. The field workers composed by local physicians and health workers in the survey were given a standard training. The health workers who had been trained and could understand the screening questionnaires translated them into ethnic languages and dialects, if the people surveyed could not understand the screening questionnaires written in Mandarin. Our screening questionnaire was based on the WHO screening questionnaire and ICBERG screening instrument (with
2.2. Ethical approval The study was approved by the ethical committee of the Xuanwu Hospital, Capital Medical University, Beijing, PR China.
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epilepsy not on adequate treatment, expressed as a percentage of total number with active epilepsy (Meinardi et al., 2001).
sensitivity 100% and specificity 78.5%) previously used in China (Wang et al., 2003). The screening procedure was conducted during interview so that investigators must verify that all subjects understood the questions asked in the questionnaire. Each interview was conducted by a doctor together with the native village health worker for the ethnic languages and dialects. Each adult resident in the house was interviewed. The head of the household, usually the husband, and his wife provided information about each child with age less than 14 years old. If necessary, the patients and their families were required to give a detailed demonstration of the seizure. In case of seizure history of family member(s), details were taken from the case and also from a reliable eyewitness of the ictal event. The screening was completed when all subjects in a certain area were investigated.
2.6. Statistical analysis All analyses were done by SPSS Windows version 16.0. Quantitative variables were described using the mean and standard deviation (SD). The 95% confidence interval (CI) of the crude prevalence of epilepsy and the prevalence of active epilepsy was calculated using the formulae (p ± Zα/2Sp) and Sp = p (1 − p) . p is the prevalence. Sp is the standard n error. n is the number of people surveryed. Zα/2 is 1.96. The treatment gaps were also calculated. The age group was adjusted with direct method on the 2000 China population.
2.4.2. Phase II. Diagnosis and confirmation Any individual who had a positive response to any of the screening questions was then scrutinized by a neurologist. The neurologist clinically examined these subjects at their residences, and reviewed relevant investigation reports if available. The date of onset of seizure was ascertained as accurately as possible. On the basis of these observations, the neurologist made the diagnosis of epilepsy and of other forms of seizure disorder; the neurologist also identified the false positives. A part of patients with epilepsy had clinical evaluation and EEG. CT or MRI investigation was performed in a few patients. Experts from department of neurology together discussed the patients with unascertained diagnosis. As for the case of a disagreement among senior neurologists, the clinical and EEG data of the patients were discussed together to reach a consensus.
3. Results
2.5. Diagnostic criteria
3.1. Crude prevalence and age-adjusted prevalence of epilepsy and active epilepsy
A total of 77,352 people (about 2.76% of all the population of the studied areas) were screened. 76302 (98.6%) people gave response to the screening question, of which 46.7% were Hani people, 13.8% were Wa people, 14.0% were Lahu people, 6.2% were Bulang people, 5.9% were Jinuo people, 5.3% were Achang people, 4.1% were Deang people, and 4.0% were Nu people. 293 (0.38%) subjects gave a positive response to possible or probable seizures. Of these, 43(14.7%) were diagnosed with single unprovoked seizures, and 71 (24.2%) had syncope, other types of unconsciousness, seizures due to acute illness, and nonepileptic abnormal movements. 179 (61.1%) screened positive people were confirmed as definitive epilepsy, 153 (85.5%) of which met the criteria for active epilepsy.
According to the guidelines for epidemiologic studies on epilepsy (Commission, 1989; Commission, 1993), epilepsy was defined as the condition characterized by recurrent (two or more) epileptic seizures, unprovoked by any immediate identified cause. Multiple seizures occurring in a 24-h period were considered a single event. Single epileptic seizures, febrile convulsions, and epileptic seizures with an obvious precipitant were excluded. Prevalence was a diagnosis of epilepsy (recurrent unprovoked seizures) at some point prior to the prevalence period or date. A prevalent case of active epilepsy was defined as a person with epilepsy who has had at least one seizure in the previous 5 years, regardless of antiepileptic drug treatment. Seizures were classified in accordance with the international classification of epileptic seizures of ILAE (Commission, 1989; Commission, 1993), based on the clinical history; age at onset; seizure patterns; evolution of the disease; and clinical, EEG and neuroradiologic examinations. A seizure was considered partial seizure on the basis of clinical evidence of focal onset, regardless of whether it was secondarily generalized. Natural remission referred to when epilepsy patients who have never been treated with any antiepileptic drugs were free of seizures for five years or more. Treatment gap was the number of people with active
The number of response to the screening questions ranged from 3072 Nu people (1584 men and 1488 women) to 35,609 Hani people (19,005 men and 16,604 women). A range of patients with epilepsy from sixteen in Deang people to forty-four in Hani people were identified. The crude prevalence varied from the highest in Nu people (6.5/ 1000; 95% CI 4.8–8.5/1000) to the lowest in Hani people (1.2/1000; 95% CI 0.8–1.6/1000). The age-adjusted prevalence of epilepsy also ranges from the highest in Nu people (7.3/1000; 95% CI 6.4–8.1) to the lowest in Hani people (2.1/1000; 95% CI 2.0–2.2/1000) (Table 1). The crude prevalence of active epilepsy varied from the lowest in Hani people (1.0/1000; 95% CI 0.6–1.4/1000) to the highest in Nu people (5.9/1000; 95% CI 3.9–7.9/1000). The age-adjusted prevalence of active epilepsy also ranges from the lowest in Hani people (1.8/1000; 95% CI 1.7–1.9/1000) to the highest in Nu people (5.7/1000; 95% CI 5.9–7.5/1000) (Table 1). 3.2. Gender-specific crude prevalence and age-adjusted prevalence of epilepsy The highest crude prevalence of epilepsy in both man (8.4/1000;
Table 1 Crude and Age-adjusted Prevalence of Each Ethnicity. Ethnicity
No. of people sampled
No. of patient with epilspsy
Crude prevalence (95% CI)
Age-adjusted prevalence (95% CI)
No. of patient with epilspsy
Crude prevalence (95% CI)
Age-adjusted prevalence (95% CI)
Achang Deang Bulang Lahu Nu Jinuo Wa Hani
4065 3102 4705 10687 3072 4465 10597 35609
17 16 19 25 20 18 20 44
4.2(2.2–6.2) 5.2(3.2–7.2) 4.0(2.2–5.8) 2.3(1.3–3.3) 6.5(4.5–8.5) 4.0(2.2–5.8) 1.9(1.1–2.7) 1.2(0.8–1.6)
4.3(3.7–4.9) 5.3(3.4–7.9) 4.4(4.0–4.8) 3.1(2.9–3.3) 7.3(6.4–8.1) 4.5(3.6–4.9) 2.9(2.7–3.1) 2.1(2.0–2.2)
14 14 18 19 18 16 18 36
3.4 (1.6–5.1) 4.5(2.5–6.5) 3.8(2.0–5.6) 1.8(1.0–2.6) 5.9(3.9–7.9) 3.6(1.8–5.4) 1.7(0.9–2.4) 1.0(0.6–1.4)
3.5(2.9–4.1) 4.4(3.5–5.3) 4.2(3.8–4.6) 2.5(2.3–3.8) 6.7(5.9–7.5) 4.0(3.2–4.8) 2.6(2.4–2.8) 1.8(1.7–1.9)
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Table 2 Gender-specific Crude and Age-adjusted Prevalence of Each Ethnicity. Ethnicity
No. of male sampled (%)
No. of male patient with epilepsy
Crude prevalence (95% CI)
Age-adjusted prevalence (95% CI)
No.of female sampled
No. of female patient with epilepsy
Crude prevalence (95% CI)
Age-adjusted prevalence (95% CI)
Achang Deang Bulang Lahu Nu Jinuo Wa Hani
2089 (51.4%) 1600 (51.6%) 2612 (55.5%) 5901(55.2%) 1584 (51.6%) 2434 (54.5%) 5611 (52.9%) 19005 (53.3%)
8 9 14 12 11 12 15 28
3.8(1.8–5.8) 5.6(3.6–7.6) 5.4(3.4–7.4) 2.0(0.4–3.6) 6.9(3.0–10.8) 4.9(2.9–6.9) 2.7(1.3–4.1) 1.5(0.9–2.1)
4.0(3.0–5.0) 5.5(4.0–7.0) 5.3(4.7–5.9) 2.5(2.3–2.7) 8.4(7.2–10.0) 5.7(4.3–7.0) 3.7(3.4–4.0) 2.6(2.5–2.7)
1976 (48.5%) 1502 (48.4%) 2093 (44.5%) 4786 (44.8%) 1488 (48.4%) 2031(45.5%) 4986(48.1%) 16604(46.7%)
9 7 5 13 9 6 5 16
4.6(2.0–6.6) 4.7(2.7–6.7) 2.4(0.4–4.4) 2.7(1.1–4.3) 6.1(2.2–10.0) 3.0(1.0–5.0) 1.0(0.2–2.0) 1.0(0.4–1.6)
4.5 (3.5–5.5) 4.3(3.0–5.6) 3.4(2.9–3.9) 3.7(3.4–3.9) 6.4(5.2–7.6) 3.4(2.8–4.0) 1.9(1.7–2.1) 1.6(1.5–1.7)
95% CI 7.2–10.0/1000) and woman (6.4/1000; 95% CI 5.2–7.6/1000) derived from Nu people. The lowest crude prevalence of epilepsy in man was in Hani people (1.5/1000; 95% CI 0.9–2.1/1000). The lowest age-adjusted prevalence of male with epilepsy was in Lahu people (2.5/ 1000; 95% CI 2.3–2.7/1000). The lowest crude prevalence of epilepsy in woman was in Hani and Wa people. The lowest age-adjusted prevalence of in woman was in Hani people (1.6/1000; 95% CI 1.5–1.7/ 1000). With the exception of the Achang and Lahu people, the crude prevalence of epilepsy and age-adjusted prevalence in male subjects were higher than that in female subjects (Table 2).
Table 4 Seizure Types.
3.3. Patient age, age at first seizure and duration of epilepsy There was a range of the average age of all epilepsy patients among the eight ethnic groups. The first seizure occurred before the age of 10 years in 25.0%–48.0% of cases, and before 20 years in 50.0%–95.0% of cases. The proportion of the cases steadily declined after the fifth decade of life among the eight ethnic groups. With the exception of the Hani patients, there were two peaks of age for first seizure, one in childhood, the other in young adulthood. The duration of epilepsy varied among the eight ethnic groups, ranging from 7.2 ± 6.4 (Lahu and Hani patients) to 17.6 ± 10.8 years (Jinuo patients) (Table 3).
Table 3 Patient Age, Age at First Seizure and Duration of Epilepsy.
Achang Deang Bulang Lahu Nu Jinuo Wa Hani
29.9 31.7 28.6 29.8 35.4 34.9 27.0 26.1
± ± ± ± ± ± ± ±
21.1 16.6 18.6 21.1 20.9 13.3 17.5 14.3
Age at First Seizure ≤19 years (%)
Duration of Epilepsy (y)
21.4 18.4 18.0 17.5 23.1 16.7 14.9 14.9
29.4 25.0 36.8 48.0 35.0 33.3 40.0 45.5
52.9 50.0 52.6 72.0 50.0 61.1 95.0 75.0
9.5 ± 8.9 12.4 ± 10.3 9.8 ± 9.2 7.2 ± 6.4 10.3 ± 8.1 17.6 ± 10.8 10.9 ± 10.6 7.2 ± 6.4
± ± ± ± ± ± ± ±
17.2 13.3 15.2 20.1 22.4 12.2 11.4 13.9
Partial Seizure
Other Seizures
Achang Deang Bulang Lahu Nu Jinuo Wa Hani
12 13 12 19 16 11 17 31
1 0 3 0 0 0 2 4
13 13 15 19 16 11 19 35
3 2 4 2 2 2 1 5
1 1 0 4 2 5 0 4
(70.6%) (81.2%) (63.2%) (76.0%) (80.0%) (61.1%) (85.0%) (70.4%)
(5.8%) (0.0%) (15.8%) (0.0%) (0.0%) (0.0%) (10.0%) (9.1%)
(76.4%) (81.2%) (79.0%) (76.0%) (80.0%) (61.1%) (95.0%) (79.5%)
(17.6%) (12.5%) (21.1%) (8.0%) (10.0%) (11.1%) (5.0%) (11.4%)
(5.8%) (6.3%) (0.0%) (16.0%) (10.0%) (27.8%) (0.0%) (9.1%)
To our knowledge, this is the first door-to-door and populationbased epidemiological and clinical characteristics of epilepsy study from eight ethnic groups in rural areas of China. Our study supplies data of the epidemiological and clinical characteristics on epilepsy in 8 ethnic groups of China. The eight ethnic groups live in the same area for generations. Therefore, the data has value for the knowledge of epilepsy both in these ethnic groups and these areas. We found disparities of the crude prevalence and age-adjusted prevalence among the eight ethnic groups. Though, the ethnic groups lived closely in the same mountainous regions for generations, they have their own lifestyle. We thought that the genetic heterogeneity might mainly contribute to the difference. First, compared with the other seven ethnic groups and the data from Asia community (6.0/ 1000), the crude prevalence (6.5/1000) and age-adjusted prevalence (7.3/1000) in Nu people appeared higher but in line with the previous report about Han ethnic groups (7.0/1000) in five provinces in China (Mac et al., 2007; Wang et al., 2003). Secondly, compared with Lahu, Wa and Hani people, the crude prevalence in Achang, Deang, Bulang, and Jinuo people (3.8–5.2/1000) appeared higher but in accordance with some Asia population (3.5–6.0/1000) (Mac et al., 2007). Finally, the lower crude prevalence in Lahu, Wa and Hani people is close to Taiwan (2.4/1000) and Hongkong Chinese population (1.5/1000), and Arab people (2.3/1000) (Mac et al., 2007; Benamer and Grosset, 2009). Apart from Nu people, the age-adjusted prevalence in other seven
The frequency of seizure in Deang, Lahu, Jinuo, Wa and Hani subjects was different from Achang, Bulang and Nu cases. In former
Age at First Seizure ≤9 years (%)
Total Generalized Seizure
4. Discussion
3.5. Seizure frequency, natural remission rate, treatment gap and average per capita income per year
Age at First Seizure
Absence Seizures
ethnics, more than sixty percent cases had more than 10 events per year, whereas in the latter, more than fifty percent of patients had less than10 events per year. Among the eight ethnic groups, there was a different nature remission rate. Furthermore, all patients who were in natural remission had GTCSs. The treatment gap, except Jinuo subjects (43.8%), took up more than two-thirds cases with active epilepsy. The Jinuo subjects with lowest treatment gap had highest average per capita income per year (1327 Yuan) (Table 5).
Generalized seizures (from 61.1% in Jinuo subjects to 95.0% in Wa subjects), including generalized tonic-clonic seizures (GTCSs) and absence seizure, were the most prominent type in each ethnic group. The majority of these were GTCSs. A minority of these in each ethnic group met the standard of partial seizures and other seizures (Table 4).
Age(y)
GTCS
Note: GTCS generalized tonic-clonic seizures.
3.4. Seizure types
Ethnicity
Ethnicity
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Table 5 Seizure Frequency, Natural Remission Rate, Treatment Gap and Average Per Capita Income Per Year. Ethnicity
Seizure frequency ≥10 events/y
Seizure frequency < 10 events/y
No. of active epilepsy
Nature remission rate
No. of Treatment
Treatment Gap
Average per capita income per year (Yuan)
Achang Deang Bulang Lahu Nu Jinuo Wa Hani
8 (47.1%) 10 (62.5%) 8 (42.1%) 17 (68.0%) 9 (45.0%) 13 (72.2%) 13 (65.0%) 28 (63.6%)
9 (52.9%) 6 (37.5%) 11(57.8%) 8 (32.0%) 11 (55.0%) 5 (27.8%) 7 (35.0%) 16 (36.4%)
14 14 18 19 18 16 18 36
3 2 1 6 2 2 2 8
1(7.1%) 3(21.4%) 1(5.6%) 3(15.8%) 0(0.0%) 9(56.3%) 0(0.0%) 7(19.4%)
92.9% 76.9% 94.4% 84.2% 100.0% 43.8% 100.0% 80.6%
1182 1028 819 899 839 1327 1250 828
(17.6%) (12.5%) (5.2%) (24.0%) (10.0%) (16.7%) (10.0%) (18.2%)
1000), south Tanzania (8.6/1000), and Cameroon (105/1000) (Burneo et al., 2005; Noronha et al., 2007; Bartolini et al., 2011; Dent et al., 2005; Prischich et al., 2008). Our findings showed that more than half of patients had their first seizure before 20 years old, among the eight ethnic groups, and the proportion gradually decreased after fifth decade of life. This suggested that both children and juvenile might be prone to epilepsy. Furthermore, there was no remarkable difference in age distribution of epilepsy between our results and those studies from Asia, sub-Saharan Africa, some Arab countries, northern Tanzania, and Honduras (Mac et al., 2007; Preux and Druet-Cabanac, 2005; Benamer and Grosset, 2009; Noronha et al., 2007; Bartolini et al., 2011). Our results showed that generalized seizures, especially GTCSs, constituted the majority of cases, as other authors have previously noted, which lacked any significant difference in the proportion of generalized seizure between different ethnic groups (Mac et al., 2007; Preux and Druet-Cabanac, 2005; Winkler et al., 2009; Noronha et al., 2007; Djibuti and Shakarishvili, 2003). Similarly, GTCSs account for about 97% of cases in some Arab countries, and 95.8% in south Tanzania (Benamer and Grosset, 2009; Dent et al., 2005). Moreover, a report from twenty-five studies also showed a higher proportion of epilepsy was generalized seizure (Banerjee et al., 2009). Together, these data suggest that the seizure types in our study match the reports from some racial/ethnical groups, but contrast the results from Honduras, Europe, and Cameroon, which have been reported that partial seizures was more common type (Medina et al., 2005; Forsgren et al., 2005; Prischich et al., 2008). However, we could not preclude that the only use of clinical examination, without access to electroencephalographic data, could lead to the underreporting of partial seizures and the overrepresentation of generalized seizures. While there were some variations in the seizure frequency among the eight ethnic groups, and the majority of cases had more frequency seizures. The age of range of epilepsy onset among the eight ethnic groups ranged from 7.0 ± 8.4 to 17.6 ± 10.8 years. The severity of seizures was reflected by their frequency and duration. Patients with very frequent seizures were in much higher risk of mental retardation than those with the general epilepsy (Djibuti and Shakarishvili, 2003). This indicates that reduction of seizure frequencies should be noticed among these ethnic groups. Moreover, high seizure frequency also affects the economic situation of patients, qualities of life, treatment and prognosis. In fact, the average per capita income per year was very low (from 819 Yuan to 1327 Yuan). While the natural remissions had taken place in each ethnic group, the natural remission rate among the eight ethnic groups was low. Moreover, we had also noted that it was true that generalized seizures in natural remission were associated with a better prognosis (Nicoletti et al., 2009). The low natural remission rate in the eight ethnic groups was possibly due to the different definition for natural remission, or racial/ethnical factors (Tuan et al., 2008; Forsgren et al., 2005; Nicoletti et al., 2009; Placencia et al., 1994). For example, natural remission previously reported from Europe or Ecuad referred to free of seizures for one years or more (Forsgren et al., 2005; Placencia et al.,
ethnic groups was same as that in developed countries (2.5–5.3/1000) (Jappon, 2002). Similar reports with heterogeneity from the different races/ethnic groups have been presented in the North American and Asia (Mac et al., 2007; Burneo et al., 2009). On the other hand, the crude prevalence and age-adjusted prevalence in each ethnic group had a similar feature, which is not consistent with some developing countries, with a very high prevalence conducted by door-to-door (Burneo et al., 2005; Preux and Druet-Cabanac, 2005; Winkler et al., 2009; Noronha et al., 2007; Medina et al., 2005). This suggests that there were some common characteristics in the crude prevalence and ageadjusted prevalence among the eight ethnic groups. In sum, the eight ethnic groups in the crude prevalence and age-adjusted prevalence of epilepsy have both different and similar features: in accordance with Asian countries but lower than some developing countries (Bartolini et al., 2011). However, we cannot exclude that the study might underestimate the true prevalence, especially in Lahu, Wa and Hani people, although the number of response to screening questions from the interviewers was big. The lower both the crude prevalence and ageadjusted prevalence are attributed to concealment of epilepsy, because of the fear of shame, the negative attitudes towards this condition, under-ascertainment of cases with minor seizures and/or rare seizures. Furthermore, patients with partial seizures or less frequent seizures, elderly onset of seizures, and with remissive seizures might be also under-represented here. Nevertheless, our findings provided a reasonably reliable estimate of the crude prevalence and age-adjusted prevalence of the eight ethnic groups. The information about the crude prevalence and age-adjusted prevalence by gender distribution were also different in our study. We found higher the crude prevalence and age-adjusted prevalence of women in Achang and Lahu people. Consistent results from northern Tanzania and Honduras have been reported (Winkler et al., 2009; Medina et al., 2005). Moreover, we also found there is no different for higher the crude prevalence in men subjects among Deang, Bulang, Nu, Jinuo, Wa and Hani people, which is in line with Asia, sub-Saharan Africa as well as Arab population (Mac et al., 2007; Preux and DruetCabanac, 2005; Benamer and Grosset, 2009). Apart from Nu people, the age-adjusted prevalence in men subjects among Deang, Bulang, Jinuo, Wa and Hani people was similar. The age-adjusted prevalence in women subjects was similar, except for Wa and Hani people. These differences by gender could represent gender-dependent risk factors (Winkler et al., 2009). We noted that there was a difference in the crude prevalence of active epilepsy among the eight ethnic groups. Compared with Lahu, Wa and Hani people, the crude prevalence of active epilepsy in Achang, Deang, Bulang, Nu and Jinuo people were high but were similar to those results carried out in China (4.6/1000), Vietnam (4.4/1000) or Europe (3.3–7.8/1000) (Wang et al., 2003; Tuan et al., 2008; Forsgren et al., 2005). However, apart from Hani people, age-adjusted prevalence of active epilepsy in other seven groups was similar. In addition, the crude and age-adjusted prevalence of active epilepsy in each ethnic group in our study was lower than those results from Latin America (12.4/1000), northern Tanzania (8.7/1000), Honduras (15.4/ 114
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1993. Guidelines for epidemiologic studies on epilepsy. Epilepsia 34, 592–596. Dent, W., Helbok, R., Matuja, W.B., Scheunemann, S., Schmutzhard, E., 2005. Prevalence of active epilepsy in a rural area in South Tanzania: a door-to-door survey. Epilepsia 46, 1963–1969. Djibuti, M., Shakarishvili, R., 2003. Influence of clinical, demographic, and socioeconomic variables on quality of life in patients with epilepsy: findings from Georgian study. J. Neurol. Neurosurg. Psychiatry 74, 570–573. Forsgren, L., Beghi, E., Oun, A., Sillanpaa, M., 2005. The epidemiology of epilepsy in Europe - a systematic review. Eur. J. Neurol. 12, 245–253. Jappon, P., 2002. Epilepsy and epileptic disorders, an epidemiological marker? Contribution of descriptive epidemiology. Epileptic. Disord. 4, 1–13. Mac, T.L., Tran, D.S., Quet, F., Odermatt, P., Preux, P.M., Tan, C.T., 2007. Epidemiology, aetiology, and clinical management of epilepsy in Asia: a systematic review. Lancet Neurol. 6, 533–543. Mbuba, C.K., Ngugi, A.K., Newton, C.R., Carter, J.A., 2008. The epilepsy treatment gap in developing countries: a systematic review of the magnitude, causes, and intervention strategies. Epilepsia 49, 1491–1503. Medina, M.T., Duron, R.M., Martinez, L., Osorio, J.R., Estrada, A.L., Zúniga, C., Cartagena, D., Collins, J.S., Holden, K.R., 2005. Prevalence, incidence, and etiology of epilepsies in rural Honduras: the Salama Study. Epilepsia 46, 124–131. Meinardi, H., Scott, R.A., Reis, R., JW;1, Sander, 2001. The treatment gap in epilepsy: the current situation and ways forward. Epilepsia 42, 136–149. Nicoletti, A., Sofia, V., Vitale, G., Bonelli, S.I., Bejarano, V., Bartalesi, F., Tran, D.S., Preux, P.M., Zappia, M., Bartoloni, A., 2009. Natural history and mortality of chronic epilepsy in an untreated population of rural Bolivia: a follow-up after 10 years. Epilepsia 50, 2199–2206. Noronha, A.L., Borges, M.A., Marques, L.H., Zanetta, D.M., Fernandes, P.T., Boer, H., Espíndola, J., Miranda, C.T., Prilipko, L., Bell, G.S., Sander, J.W., Li, L.M., 2007. Prevalence and pattern of epilepsy treatment in different socioeconomic classes in Brazil. Epilepsia 48, 880–885. Placencia, M., Sander, J.W., Roman, M., Madera, A., Crespo, F., Cascante, S., Shorvon, S.D., 1994. The characteristics of epilepsy in a largely untreated population in rural Ecuador. J. Neurol. Neurosurg. Psychiatry 57, 320–325. Preux, P.M., Druet-Cabanac, M., 2005. Epidemiology and aetiology of epilepsy in subSaharan Africa. Lancet Neurol. 4, 21–31. Prischich, F., De Rinaldis, M., Bruno, F., Egeo, G., Santori, C., Zappaterrenob, A., Fattouchd, J., Bonaventurad, C.D., Badae, J., Russoc, G., Pizzuti, A., Cardonaa Francesco Sa’a Vullo, V., Giallonardod, A.T., Erasmob, E.D’, Pellicciai, A., Vanacorej, N., 2008. High prevalence of epilepsy in a village in the Littoral Province of Cameroon. Epilepsy Res. 82, 200–210. Radhakrishnan, K., 2009. Challenges in the management of epilepsy in resource-poor countries. Nat. Rev. Neurol. 5, 323–330. Tuan, N.A., Cuong, L.Q., Allebeck, P., Chuc, N.T., Persson, H.E., Tomson, T., 2008. The prevalence of epilepsy in a rural district of Vietnam: a population-based study from the EPIBAVI project. Epilepsia 49, 1634–1637. Tuan, N.A., Tomson, T., Allebeck, P., Chuc, N.T., Cuong, L.Q., 2009. The treatment gap of epilepsy in a rural district of Vietnam: a study from the EPIBAVI project. Epilepsia 50, 2320–2323. World Health Organization, 2001. Epilepsy: Epidemiology, Aetiology and Prognosis. WHO Factsheet, pp. 165. Wang, W.Z., Wu, J.Z., Wang, D.S., Dai, X.Y., Yang, B., Wang, T.P., Yuan, C.L., Scott, R.A., Prilipko, L.L., Boer, H.M., Sander, J.W., 2003. The prevalence and treatment gap in epilepsy in China: an ILAE/IBE/WHO study. Neurology 60, 1544–1545. Winkler, A.S., Kerschbaumsteiner, K., Stelzhammer, B., Meindl, M., Kaaya, J., Kaaya, J., Schmutzhard, E., 2009. Prevalence, incidence, and clinical characteristics of epilepsya community-based door-to-door study in northern Tanzania. Epilepsia 50, 2310–2313.
1994). Treatment gap is a severe problem in developing countries. Our study showed that a large proportion of patients with epilepsy, except Jinuo subjects, did not receive treatment. No patient in the Wa and Nu ethnic groups had even received any antiepileptic treatment before, in particular. This situation, which was consistent with that of developing countries, was much worse than the situation reported in China (Wang et al., 2003; Noronha et al., 2007; Mbuba et al., 2008; Tuan et al., 2009). The high treatment gap among different ethnic subjects could be contributed to some factors: (1) geography; (2) misconception of epilepsy, that the epilepsy was untreatable and the treatment was ineffective; (3) low socioeconomic status in the eight ethnic groups, except for Jinuo people whose average per capita income per year was highest and whose treatment gap was lowest, whose average per capita income per year made antiepileptic drugs unaffordable; (4) deprivation of physical strength, which prevented the patient from working and earning a living; (5) seeking treatment from traditional healers. The major limitation of our study was the lack of electroencephalogram and neuroimaging in some patients, allowed diagnosis on clinical grounds alone. In addition, though there are 26 ethnic groups in Yunnan province, we selected the 8 ethnic groups who inhabit the rural areas in seven cities and autonomous regions and population are relatively low. We will further study other ethnic groups in the future. 5. Conclusions There were both disparity and similarity in the epidemiological and clinical features of epilepsy in different ethnic group communities. References Banerjee, P.N., Filippi, D., Allen, H.W., 2009. The descriptive epidemiology of epilepsy-a review. Epilepsy Res. 85, 31–45. Bartolini, E., Bell, G.S., Sander, J.W., 2011. Multicultural challenges in epilepsy. Epilepsy Behav. 20, 428–434. Benamer, H.T., Grosset, D.G., 2009. A systematic review of the epidemiology of epilepsy in Arab countries. Epilepsia 50, 2301–2304. Burneo, J.G., Tellez-Zenteno, J., Wiebe, S., 2005. Understanding the burden of epilepsy in Latin America: a systematic review of its prevalence and incidence. Epilepsy Res. 66, 63–74. Burneo, J.G., Jette, N., Theodore, W., Begley, C., Parko, K., Thurman, D.J., Wiebe, S., 2009. Disparities in epilepsy: report of a systematic review by the North American Commission of the International League Against Epilepsy. Epilepsia 50, 2285–2295. Commission on Classification and Terminology of the International League Against Epilepsy, 1989. Proposal for revised classification of epilepsies and epileptic syndromes. Epilepsia 30, 389–399. Commission on Epidemiology and Prognosis, International League Against Epilepsy,
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Epilepsy Research journal homepage: www.elsevier.com/locate/epilepsyres
The epidemiological and clinical characteristics study on epilepsy in 8 ethnic groups of China
MARK
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ZhiPeng Yu , Kai Dong, Hong Chang, XiaoQin Huang, Yi Ren, ChunQiu Fan, QingFeng Ma, HaiQing Song, Qian Zhang, Jing Zhang, LiYuan Huang Department of Neurology, Xuanwu Hospital Capital Medical University, Beijing, 100191, PR China
A R T I C L E I N F O
A B S T R A C T
Keywords: Epilepsy Epidemiology Ethnic group
To survey the epidemiological characteristics and clinical features on epilepsy in eight ethnic groups in Yunnan province of China. Methodes: The investigation was based on the WHO questionnaire and ICBERG screening questionnaire. This study was performed through random cluster sampling and door-to-door survey. Results: A total of 76,302 individuals from eight ethnic groups were surveyed. The crude prevalence of epilepsy ranged from 1.2/1000 to 6.5/1000 in the eight ethnic groups, and the age-adjusted prevalence of epilepsy was from 2.1/1000 to 7.3/1000. The prevalence of active epilepsy varied from 1.0/1000 to 5.2/1000 in the eight ethnic groups, and the age-adjusted prevalence of active epilepsy was from 1.8/1000 to 6.7/1000. The age peak for seizures was below twenty, the patients of 61.1%-95.0% suffered from generalized seizures and 5%-21.2% had partial seizures. More than 60% of the cases in five ethnic groups, and the frequency of seizures were more than 10 events per year. More than 50% in other three ethnic groups, and the seizures had occurred less than 10 events per year. The treatment gap for active epilepsy ranged from 43.7% to 100.0% among the eight ethnic groups, while the natural remission rate varied from 5.6% to 21.0%. Conclusion: There were both disparity and similarity in the epidemiological and clinical features of epilepsy in different ethnic group communities.
1. Introduction The epidemiology of epilepsy is diverse in different countries and regions. The lifetime prevalence of epilepsy ranges from 3.5 to 10.7/ 1000 (Radhakrishnan, 2009) in developed countries, and from 0.9 to 74.4/1000 in Asia, sub-Saharan Africa, and Latin America (Mac et al., 2007; Burneo et al., 2005; Preux and Druet-Cabanac, 2005; Benamer and Grosset, 2009; Burneo et al., 2009). The prevalence of active epilepsy ranges from 1.5 to 74.4/1000 (Radhakrishnan, 2009). Similarly, the types and frequency of seizures vary in different countries and regions. More importantly, the epidemiological and clinical features of the disorder are diverse in different races and ethnicities. However, studies in the epidemiology of epilepsy are mostly conducted within one ethnicity in one country. Little has been discovered about the epidemiological and clinical features of epilepsy in different ethnicities. Thus, the epidemiological and clinical data of epilepsy in multi-ethnic groups
need further survey. The epidemiology of epilepsy in the Han nationality of Chinese has been conducted (Wang et al., 2003). However, there are 56 minorities in China. Data on the epidemiological and clinical features of epilepsy in different ethnicity groups remain undiscovered. Therefore, the major objective of this study is to establish epidemiological features in eight ethnic groups that inhabit in the rural areas in China. 2. Material and methods 2.1. Population and regional characteristics This study was conducted from January 2006 to September 2008, in the rural areas of Yunnan Province. Yunnan Province, located in the southwest of China, consists of 16 cities and autonomous regions, sharing boarders with Myanmar, Laos, and Vietnam (Fig. 1). It is the home to 26 ethnic groups, 15 of which are indigenous. Yunnan covers a
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Corresponding author at: Changchun Street, Xicheng District, Beijing, No. 45, PR China. E-mail addresses: [email protected] (Z. Yu), [email protected] (K. Dong), [email protected] (H. Chang), [email protected] (X. Huang), [email protected] (Y. Ren), [email protected] (C. Fan), [email protected] (Q. Ma), [email protected] (H. Song), [email protected] (Q. Zhang), [email protected] (J. Zhang), [email protected] (L. Huang). http://dx.doi.org/10.1016/j.eplepsyres.2017.10.020 Received 7 September 2017; Received in revised form 20 October 2017; Accepted 27 October 2017 0920-1211/ © 2017 Elsevier B.V. All rights reserved.
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Fig. 1. Study region and geographical situation of China.
2.3. Sample size
landmass of 394,000 square kilometers, accounting for 4.1% of Chinese territory, 94% of which is mountainous regions. Among the ethnic groups surveyed, the Achang, Deang, Bulang, Lahu, Nu, Jinuo, Wa, and Hani people inhabit in the rural areas in seven cities and autonomous regions. Comprising of 48 counties, the seven cities and autonomous regions cover an area of 167881 square kilometers, with a population of more than 13.95 million in 2000. The altitude of these investigated districts ranges from 1500 to 3500 m above sea level. Due to the underdeveloped infrastructure of transportation, most villages are one to ten hour’s drives away from the nearest urban area. Several villages are completely or relatively isolated from outside world, and can only be reached on foot. The air and water in these districts is unpolluted and a variety of vegetation grows in the areas. It is tropical or sub-tropical climate with rich rainfalls from June to October. The custom, religion, clothing, and physical appearance vary greatly among the eight ethnicities. Occupying different regions, every ethnic group maintains ancient and exclusive lifestyle. These people live in mountainous regions as peasants, and live on organic rice, vegetables, herbs, and meat. Every ethnic group speaks their own language and exogamy is not the norm.
Sample size was calculated using a formula n = (t2pq)/d2, of which n is the minimum sample size, t is the score on a gaussian distribution correspondent with a certain confidence level (we used t = 1.96), p is the presumed prevalence of the disease (0.007), q = 1 − p, and d is the desired level of precision (we accepted d = p/10). Accordingly, the total sample size for the eight ethnic groups should be not less than 54496 (1.962 × 0.993 × 100/0.007). Sample size was calculated separately for each ethnic groups surveyed. 2.4. Steps of the study We did a two-phase door-to-door survey. In phase I, a screening instrument for epilepsy was administered to inhabitants of the village who agreed to participate; in phase II, the evaluation of possible epilepsy was performed among those subjects who screened positive for that condition. 2.4.1. Phase I. screening Random cluster sampling and door-to-door survey were used in the study. The field workers composed by local physicians and health workers in the survey were given a standard training. The health workers who had been trained and could understand the screening questionnaires translated them into ethnic languages and dialects, if the people surveyed could not understand the screening questionnaires written in Mandarin. Our screening questionnaire was based on the WHO screening questionnaire and ICBERG screening instrument (with
2.2. Ethical approval The study was approved by the ethical committee of the Xuanwu Hospital, Capital Medical University, Beijing, PR China.
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epilepsy not on adequate treatment, expressed as a percentage of total number with active epilepsy (Meinardi et al., 2001).
sensitivity 100% and specificity 78.5%) previously used in China (Wang et al., 2003). The screening procedure was conducted during interview so that investigators must verify that all subjects understood the questions asked in the questionnaire. Each interview was conducted by a doctor together with the native village health worker for the ethnic languages and dialects. Each adult resident in the house was interviewed. The head of the household, usually the husband, and his wife provided information about each child with age less than 14 years old. If necessary, the patients and their families were required to give a detailed demonstration of the seizure. In case of seizure history of family member(s), details were taken from the case and also from a reliable eyewitness of the ictal event. The screening was completed when all subjects in a certain area were investigated.
2.6. Statistical analysis All analyses were done by SPSS Windows version 16.0. Quantitative variables were described using the mean and standard deviation (SD). The 95% confidence interval (CI) of the crude prevalence of epilepsy and the prevalence of active epilepsy was calculated using the formulae (p ± Zα/2Sp) and Sp = p (1 − p) . p is the prevalence. Sp is the standard n error. n is the number of people surveryed. Zα/2 is 1.96. The treatment gaps were also calculated. The age group was adjusted with direct method on the 2000 China population.
2.4.2. Phase II. Diagnosis and confirmation Any individual who had a positive response to any of the screening questions was then scrutinized by a neurologist. The neurologist clinically examined these subjects at their residences, and reviewed relevant investigation reports if available. The date of onset of seizure was ascertained as accurately as possible. On the basis of these observations, the neurologist made the diagnosis of epilepsy and of other forms of seizure disorder; the neurologist also identified the false positives. A part of patients with epilepsy had clinical evaluation and EEG. CT or MRI investigation was performed in a few patients. Experts from department of neurology together discussed the patients with unascertained diagnosis. As for the case of a disagreement among senior neurologists, the clinical and EEG data of the patients were discussed together to reach a consensus.
3. Results
2.5. Diagnostic criteria
3.1. Crude prevalence and age-adjusted prevalence of epilepsy and active epilepsy
A total of 77,352 people (about 2.76% of all the population of the studied areas) were screened. 76302 (98.6%) people gave response to the screening question, of which 46.7% were Hani people, 13.8% were Wa people, 14.0% were Lahu people, 6.2% were Bulang people, 5.9% were Jinuo people, 5.3% were Achang people, 4.1% were Deang people, and 4.0% were Nu people. 293 (0.38%) subjects gave a positive response to possible or probable seizures. Of these, 43(14.7%) were diagnosed with single unprovoked seizures, and 71 (24.2%) had syncope, other types of unconsciousness, seizures due to acute illness, and nonepileptic abnormal movements. 179 (61.1%) screened positive people were confirmed as definitive epilepsy, 153 (85.5%) of which met the criteria for active epilepsy.
According to the guidelines for epidemiologic studies on epilepsy (Commission, 1989; Commission, 1993), epilepsy was defined as the condition characterized by recurrent (two or more) epileptic seizures, unprovoked by any immediate identified cause. Multiple seizures occurring in a 24-h period were considered a single event. Single epileptic seizures, febrile convulsions, and epileptic seizures with an obvious precipitant were excluded. Prevalence was a diagnosis of epilepsy (recurrent unprovoked seizures) at some point prior to the prevalence period or date. A prevalent case of active epilepsy was defined as a person with epilepsy who has had at least one seizure in the previous 5 years, regardless of antiepileptic drug treatment. Seizures were classified in accordance with the international classification of epileptic seizures of ILAE (Commission, 1989; Commission, 1993), based on the clinical history; age at onset; seizure patterns; evolution of the disease; and clinical, EEG and neuroradiologic examinations. A seizure was considered partial seizure on the basis of clinical evidence of focal onset, regardless of whether it was secondarily generalized. Natural remission referred to when epilepsy patients who have never been treated with any antiepileptic drugs were free of seizures for five years or more. Treatment gap was the number of people with active
The number of response to the screening questions ranged from 3072 Nu people (1584 men and 1488 women) to 35,609 Hani people (19,005 men and 16,604 women). A range of patients with epilepsy from sixteen in Deang people to forty-four in Hani people were identified. The crude prevalence varied from the highest in Nu people (6.5/ 1000; 95% CI 4.8–8.5/1000) to the lowest in Hani people (1.2/1000; 95% CI 0.8–1.6/1000). The age-adjusted prevalence of epilepsy also ranges from the highest in Nu people (7.3/1000; 95% CI 6.4–8.1) to the lowest in Hani people (2.1/1000; 95% CI 2.0–2.2/1000) (Table 1). The crude prevalence of active epilepsy varied from the lowest in Hani people (1.0/1000; 95% CI 0.6–1.4/1000) to the highest in Nu people (5.9/1000; 95% CI 3.9–7.9/1000). The age-adjusted prevalence of active epilepsy also ranges from the lowest in Hani people (1.8/1000; 95% CI 1.7–1.9/1000) to the highest in Nu people (5.7/1000; 95% CI 5.9–7.5/1000) (Table 1). 3.2. Gender-specific crude prevalence and age-adjusted prevalence of epilepsy The highest crude prevalence of epilepsy in both man (8.4/1000;
Table 1 Crude and Age-adjusted Prevalence of Each Ethnicity. Ethnicity
No. of people sampled
No. of patient with epilspsy
Crude prevalence (95% CI)
Age-adjusted prevalence (95% CI)
No. of patient with epilspsy
Crude prevalence (95% CI)
Age-adjusted prevalence (95% CI)
Achang Deang Bulang Lahu Nu Jinuo Wa Hani
4065 3102 4705 10687 3072 4465 10597 35609
17 16 19 25 20 18 20 44
4.2(2.2–6.2) 5.2(3.2–7.2) 4.0(2.2–5.8) 2.3(1.3–3.3) 6.5(4.5–8.5) 4.0(2.2–5.8) 1.9(1.1–2.7) 1.2(0.8–1.6)
4.3(3.7–4.9) 5.3(3.4–7.9) 4.4(4.0–4.8) 3.1(2.9–3.3) 7.3(6.4–8.1) 4.5(3.6–4.9) 2.9(2.7–3.1) 2.1(2.0–2.2)
14 14 18 19 18 16 18 36
3.4 (1.6–5.1) 4.5(2.5–6.5) 3.8(2.0–5.6) 1.8(1.0–2.6) 5.9(3.9–7.9) 3.6(1.8–5.4) 1.7(0.9–2.4) 1.0(0.6–1.4)
3.5(2.9–4.1) 4.4(3.5–5.3) 4.2(3.8–4.6) 2.5(2.3–3.8) 6.7(5.9–7.5) 4.0(3.2–4.8) 2.6(2.4–2.8) 1.8(1.7–1.9)
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Table 2 Gender-specific Crude and Age-adjusted Prevalence of Each Ethnicity. Ethnicity
No. of male sampled (%)
No. of male patient with epilepsy
Crude prevalence (95% CI)
Age-adjusted prevalence (95% CI)
No.of female sampled
No. of female patient with epilepsy
Crude prevalence (95% CI)
Age-adjusted prevalence (95% CI)
Achang Deang Bulang Lahu Nu Jinuo Wa Hani
2089 (51.4%) 1600 (51.6%) 2612 (55.5%) 5901(55.2%) 1584 (51.6%) 2434 (54.5%) 5611 (52.9%) 19005 (53.3%)
8 9 14 12 11 12 15 28
3.8(1.8–5.8) 5.6(3.6–7.6) 5.4(3.4–7.4) 2.0(0.4–3.6) 6.9(3.0–10.8) 4.9(2.9–6.9) 2.7(1.3–4.1) 1.5(0.9–2.1)
4.0(3.0–5.0) 5.5(4.0–7.0) 5.3(4.7–5.9) 2.5(2.3–2.7) 8.4(7.2–10.0) 5.7(4.3–7.0) 3.7(3.4–4.0) 2.6(2.5–2.7)
1976 (48.5%) 1502 (48.4%) 2093 (44.5%) 4786 (44.8%) 1488 (48.4%) 2031(45.5%) 4986(48.1%) 16604(46.7%)
9 7 5 13 9 6 5 16
4.6(2.0–6.6) 4.7(2.7–6.7) 2.4(0.4–4.4) 2.7(1.1–4.3) 6.1(2.2–10.0) 3.0(1.0–5.0) 1.0(0.2–2.0) 1.0(0.4–1.6)
4.5 (3.5–5.5) 4.3(3.0–5.6) 3.4(2.9–3.9) 3.7(3.4–3.9) 6.4(5.2–7.6) 3.4(2.8–4.0) 1.9(1.7–2.1) 1.6(1.5–1.7)
95% CI 7.2–10.0/1000) and woman (6.4/1000; 95% CI 5.2–7.6/1000) derived from Nu people. The lowest crude prevalence of epilepsy in man was in Hani people (1.5/1000; 95% CI 0.9–2.1/1000). The lowest age-adjusted prevalence of male with epilepsy was in Lahu people (2.5/ 1000; 95% CI 2.3–2.7/1000). The lowest crude prevalence of epilepsy in woman was in Hani and Wa people. The lowest age-adjusted prevalence of in woman was in Hani people (1.6/1000; 95% CI 1.5–1.7/ 1000). With the exception of the Achang and Lahu people, the crude prevalence of epilepsy and age-adjusted prevalence in male subjects were higher than that in female subjects (Table 2).
Table 4 Seizure Types.
3.3. Patient age, age at first seizure and duration of epilepsy There was a range of the average age of all epilepsy patients among the eight ethnic groups. The first seizure occurred before the age of 10 years in 25.0%–48.0% of cases, and before 20 years in 50.0%–95.0% of cases. The proportion of the cases steadily declined after the fifth decade of life among the eight ethnic groups. With the exception of the Hani patients, there were two peaks of age for first seizure, one in childhood, the other in young adulthood. The duration of epilepsy varied among the eight ethnic groups, ranging from 7.2 ± 6.4 (Lahu and Hani patients) to 17.6 ± 10.8 years (Jinuo patients) (Table 3).
Table 3 Patient Age, Age at First Seizure and Duration of Epilepsy.
Achang Deang Bulang Lahu Nu Jinuo Wa Hani
29.9 31.7 28.6 29.8 35.4 34.9 27.0 26.1
± ± ± ± ± ± ± ±
21.1 16.6 18.6 21.1 20.9 13.3 17.5 14.3
Age at First Seizure ≤19 years (%)
Duration of Epilepsy (y)
21.4 18.4 18.0 17.5 23.1 16.7 14.9 14.9
29.4 25.0 36.8 48.0 35.0 33.3 40.0 45.5
52.9 50.0 52.6 72.0 50.0 61.1 95.0 75.0
9.5 ± 8.9 12.4 ± 10.3 9.8 ± 9.2 7.2 ± 6.4 10.3 ± 8.1 17.6 ± 10.8 10.9 ± 10.6 7.2 ± 6.4
± ± ± ± ± ± ± ±
17.2 13.3 15.2 20.1 22.4 12.2 11.4 13.9
Partial Seizure
Other Seizures
Achang Deang Bulang Lahu Nu Jinuo Wa Hani
12 13 12 19 16 11 17 31
1 0 3 0 0 0 2 4
13 13 15 19 16 11 19 35
3 2 4 2 2 2 1 5
1 1 0 4 2 5 0 4
(70.6%) (81.2%) (63.2%) (76.0%) (80.0%) (61.1%) (85.0%) (70.4%)
(5.8%) (0.0%) (15.8%) (0.0%) (0.0%) (0.0%) (10.0%) (9.1%)
(76.4%) (81.2%) (79.0%) (76.0%) (80.0%) (61.1%) (95.0%) (79.5%)
(17.6%) (12.5%) (21.1%) (8.0%) (10.0%) (11.1%) (5.0%) (11.4%)
(5.8%) (6.3%) (0.0%) (16.0%) (10.0%) (27.8%) (0.0%) (9.1%)
To our knowledge, this is the first door-to-door and populationbased epidemiological and clinical characteristics of epilepsy study from eight ethnic groups in rural areas of China. Our study supplies data of the epidemiological and clinical characteristics on epilepsy in 8 ethnic groups of China. The eight ethnic groups live in the same area for generations. Therefore, the data has value for the knowledge of epilepsy both in these ethnic groups and these areas. We found disparities of the crude prevalence and age-adjusted prevalence among the eight ethnic groups. Though, the ethnic groups lived closely in the same mountainous regions for generations, they have their own lifestyle. We thought that the genetic heterogeneity might mainly contribute to the difference. First, compared with the other seven ethnic groups and the data from Asia community (6.0/ 1000), the crude prevalence (6.5/1000) and age-adjusted prevalence (7.3/1000) in Nu people appeared higher but in line with the previous report about Han ethnic groups (7.0/1000) in five provinces in China (Mac et al., 2007; Wang et al., 2003). Secondly, compared with Lahu, Wa and Hani people, the crude prevalence in Achang, Deang, Bulang, and Jinuo people (3.8–5.2/1000) appeared higher but in accordance with some Asia population (3.5–6.0/1000) (Mac et al., 2007). Finally, the lower crude prevalence in Lahu, Wa and Hani people is close to Taiwan (2.4/1000) and Hongkong Chinese population (1.5/1000), and Arab people (2.3/1000) (Mac et al., 2007; Benamer and Grosset, 2009). Apart from Nu people, the age-adjusted prevalence in other seven
The frequency of seizure in Deang, Lahu, Jinuo, Wa and Hani subjects was different from Achang, Bulang and Nu cases. In former
Age at First Seizure ≤9 years (%)
Total Generalized Seizure
4. Discussion
3.5. Seizure frequency, natural remission rate, treatment gap and average per capita income per year
Age at First Seizure
Absence Seizures
ethnics, more than sixty percent cases had more than 10 events per year, whereas in the latter, more than fifty percent of patients had less than10 events per year. Among the eight ethnic groups, there was a different nature remission rate. Furthermore, all patients who were in natural remission had GTCSs. The treatment gap, except Jinuo subjects (43.8%), took up more than two-thirds cases with active epilepsy. The Jinuo subjects with lowest treatment gap had highest average per capita income per year (1327 Yuan) (Table 5).
Generalized seizures (from 61.1% in Jinuo subjects to 95.0% in Wa subjects), including generalized tonic-clonic seizures (GTCSs) and absence seizure, were the most prominent type in each ethnic group. The majority of these were GTCSs. A minority of these in each ethnic group met the standard of partial seizures and other seizures (Table 4).
Age(y)
GTCS
Note: GTCS generalized tonic-clonic seizures.
3.4. Seizure types
Ethnicity
Ethnicity
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Table 5 Seizure Frequency, Natural Remission Rate, Treatment Gap and Average Per Capita Income Per Year. Ethnicity
Seizure frequency ≥10 events/y
Seizure frequency < 10 events/y
No. of active epilepsy
Nature remission rate
No. of Treatment
Treatment Gap
Average per capita income per year (Yuan)
Achang Deang Bulang Lahu Nu Jinuo Wa Hani
8 (47.1%) 10 (62.5%) 8 (42.1%) 17 (68.0%) 9 (45.0%) 13 (72.2%) 13 (65.0%) 28 (63.6%)
9 (52.9%) 6 (37.5%) 11(57.8%) 8 (32.0%) 11 (55.0%) 5 (27.8%) 7 (35.0%) 16 (36.4%)
14 14 18 19 18 16 18 36
3 2 1 6 2 2 2 8
1(7.1%) 3(21.4%) 1(5.6%) 3(15.8%) 0(0.0%) 9(56.3%) 0(0.0%) 7(19.4%)
92.9% 76.9% 94.4% 84.2% 100.0% 43.8% 100.0% 80.6%
1182 1028 819 899 839 1327 1250 828
(17.6%) (12.5%) (5.2%) (24.0%) (10.0%) (16.7%) (10.0%) (18.2%)
1000), south Tanzania (8.6/1000), and Cameroon (105/1000) (Burneo et al., 2005; Noronha et al., 2007; Bartolini et al., 2011; Dent et al., 2005; Prischich et al., 2008). Our findings showed that more than half of patients had their first seizure before 20 years old, among the eight ethnic groups, and the proportion gradually decreased after fifth decade of life. This suggested that both children and juvenile might be prone to epilepsy. Furthermore, there was no remarkable difference in age distribution of epilepsy between our results and those studies from Asia, sub-Saharan Africa, some Arab countries, northern Tanzania, and Honduras (Mac et al., 2007; Preux and Druet-Cabanac, 2005; Benamer and Grosset, 2009; Noronha et al., 2007; Bartolini et al., 2011). Our results showed that generalized seizures, especially GTCSs, constituted the majority of cases, as other authors have previously noted, which lacked any significant difference in the proportion of generalized seizure between different ethnic groups (Mac et al., 2007; Preux and Druet-Cabanac, 2005; Winkler et al., 2009; Noronha et al., 2007; Djibuti and Shakarishvili, 2003). Similarly, GTCSs account for about 97% of cases in some Arab countries, and 95.8% in south Tanzania (Benamer and Grosset, 2009; Dent et al., 2005). Moreover, a report from twenty-five studies also showed a higher proportion of epilepsy was generalized seizure (Banerjee et al., 2009). Together, these data suggest that the seizure types in our study match the reports from some racial/ethnical groups, but contrast the results from Honduras, Europe, and Cameroon, which have been reported that partial seizures was more common type (Medina et al., 2005; Forsgren et al., 2005; Prischich et al., 2008). However, we could not preclude that the only use of clinical examination, without access to electroencephalographic data, could lead to the underreporting of partial seizures and the overrepresentation of generalized seizures. While there were some variations in the seizure frequency among the eight ethnic groups, and the majority of cases had more frequency seizures. The age of range of epilepsy onset among the eight ethnic groups ranged from 7.0 ± 8.4 to 17.6 ± 10.8 years. The severity of seizures was reflected by their frequency and duration. Patients with very frequent seizures were in much higher risk of mental retardation than those with the general epilepsy (Djibuti and Shakarishvili, 2003). This indicates that reduction of seizure frequencies should be noticed among these ethnic groups. Moreover, high seizure frequency also affects the economic situation of patients, qualities of life, treatment and prognosis. In fact, the average per capita income per year was very low (from 819 Yuan to 1327 Yuan). While the natural remissions had taken place in each ethnic group, the natural remission rate among the eight ethnic groups was low. Moreover, we had also noted that it was true that generalized seizures in natural remission were associated with a better prognosis (Nicoletti et al., 2009). The low natural remission rate in the eight ethnic groups was possibly due to the different definition for natural remission, or racial/ethnical factors (Tuan et al., 2008; Forsgren et al., 2005; Nicoletti et al., 2009; Placencia et al., 1994). For example, natural remission previously reported from Europe or Ecuad referred to free of seizures for one years or more (Forsgren et al., 2005; Placencia et al.,
ethnic groups was same as that in developed countries (2.5–5.3/1000) (Jappon, 2002). Similar reports with heterogeneity from the different races/ethnic groups have been presented in the North American and Asia (Mac et al., 2007; Burneo et al., 2009). On the other hand, the crude prevalence and age-adjusted prevalence in each ethnic group had a similar feature, which is not consistent with some developing countries, with a very high prevalence conducted by door-to-door (Burneo et al., 2005; Preux and Druet-Cabanac, 2005; Winkler et al., 2009; Noronha et al., 2007; Medina et al., 2005). This suggests that there were some common characteristics in the crude prevalence and ageadjusted prevalence among the eight ethnic groups. In sum, the eight ethnic groups in the crude prevalence and age-adjusted prevalence of epilepsy have both different and similar features: in accordance with Asian countries but lower than some developing countries (Bartolini et al., 2011). However, we cannot exclude that the study might underestimate the true prevalence, especially in Lahu, Wa and Hani people, although the number of response to screening questions from the interviewers was big. The lower both the crude prevalence and ageadjusted prevalence are attributed to concealment of epilepsy, because of the fear of shame, the negative attitudes towards this condition, under-ascertainment of cases with minor seizures and/or rare seizures. Furthermore, patients with partial seizures or less frequent seizures, elderly onset of seizures, and with remissive seizures might be also under-represented here. Nevertheless, our findings provided a reasonably reliable estimate of the crude prevalence and age-adjusted prevalence of the eight ethnic groups. The information about the crude prevalence and age-adjusted prevalence by gender distribution were also different in our study. We found higher the crude prevalence and age-adjusted prevalence of women in Achang and Lahu people. Consistent results from northern Tanzania and Honduras have been reported (Winkler et al., 2009; Medina et al., 2005). Moreover, we also found there is no different for higher the crude prevalence in men subjects among Deang, Bulang, Nu, Jinuo, Wa and Hani people, which is in line with Asia, sub-Saharan Africa as well as Arab population (Mac et al., 2007; Preux and DruetCabanac, 2005; Benamer and Grosset, 2009). Apart from Nu people, the age-adjusted prevalence in men subjects among Deang, Bulang, Jinuo, Wa and Hani people was similar. The age-adjusted prevalence in women subjects was similar, except for Wa and Hani people. These differences by gender could represent gender-dependent risk factors (Winkler et al., 2009). We noted that there was a difference in the crude prevalence of active epilepsy among the eight ethnic groups. Compared with Lahu, Wa and Hani people, the crude prevalence of active epilepsy in Achang, Deang, Bulang, Nu and Jinuo people were high but were similar to those results carried out in China (4.6/1000), Vietnam (4.4/1000) or Europe (3.3–7.8/1000) (Wang et al., 2003; Tuan et al., 2008; Forsgren et al., 2005). However, apart from Hani people, age-adjusted prevalence of active epilepsy in other seven groups was similar. In addition, the crude and age-adjusted prevalence of active epilepsy in each ethnic group in our study was lower than those results from Latin America (12.4/1000), northern Tanzania (8.7/1000), Honduras (15.4/ 114
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1993. Guidelines for epidemiologic studies on epilepsy. Epilepsia 34, 592–596. Dent, W., Helbok, R., Matuja, W.B., Scheunemann, S., Schmutzhard, E., 2005. Prevalence of active epilepsy in a rural area in South Tanzania: a door-to-door survey. Epilepsia 46, 1963–1969. Djibuti, M., Shakarishvili, R., 2003. Influence of clinical, demographic, and socioeconomic variables on quality of life in patients with epilepsy: findings from Georgian study. J. Neurol. Neurosurg. Psychiatry 74, 570–573. Forsgren, L., Beghi, E., Oun, A., Sillanpaa, M., 2005. The epidemiology of epilepsy in Europe - a systematic review. Eur. J. Neurol. 12, 245–253. Jappon, P., 2002. Epilepsy and epileptic disorders, an epidemiological marker? Contribution of descriptive epidemiology. Epileptic. Disord. 4, 1–13. Mac, T.L., Tran, D.S., Quet, F., Odermatt, P., Preux, P.M., Tan, C.T., 2007. Epidemiology, aetiology, and clinical management of epilepsy in Asia: a systematic review. Lancet Neurol. 6, 533–543. Mbuba, C.K., Ngugi, A.K., Newton, C.R., Carter, J.A., 2008. The epilepsy treatment gap in developing countries: a systematic review of the magnitude, causes, and intervention strategies. Epilepsia 49, 1491–1503. Medina, M.T., Duron, R.M., Martinez, L., Osorio, J.R., Estrada, A.L., Zúniga, C., Cartagena, D., Collins, J.S., Holden, K.R., 2005. Prevalence, incidence, and etiology of epilepsies in rural Honduras: the Salama Study. Epilepsia 46, 124–131. Meinardi, H., Scott, R.A., Reis, R., JW;1, Sander, 2001. The treatment gap in epilepsy: the current situation and ways forward. Epilepsia 42, 136–149. Nicoletti, A., Sofia, V., Vitale, G., Bonelli, S.I., Bejarano, V., Bartalesi, F., Tran, D.S., Preux, P.M., Zappia, M., Bartoloni, A., 2009. Natural history and mortality of chronic epilepsy in an untreated population of rural Bolivia: a follow-up after 10 years. Epilepsia 50, 2199–2206. Noronha, A.L., Borges, M.A., Marques, L.H., Zanetta, D.M., Fernandes, P.T., Boer, H., Espíndola, J., Miranda, C.T., Prilipko, L., Bell, G.S., Sander, J.W., Li, L.M., 2007. Prevalence and pattern of epilepsy treatment in different socioeconomic classes in Brazil. Epilepsia 48, 880–885. Placencia, M., Sander, J.W., Roman, M., Madera, A., Crespo, F., Cascante, S., Shorvon, S.D., 1994. The characteristics of epilepsy in a largely untreated population in rural Ecuador. J. Neurol. Neurosurg. Psychiatry 57, 320–325. Preux, P.M., Druet-Cabanac, M., 2005. Epidemiology and aetiology of epilepsy in subSaharan Africa. Lancet Neurol. 4, 21–31. Prischich, F., De Rinaldis, M., Bruno, F., Egeo, G., Santori, C., Zappaterrenob, A., Fattouchd, J., Bonaventurad, C.D., Badae, J., Russoc, G., Pizzuti, A., Cardonaa Francesco Sa’a Vullo, V., Giallonardod, A.T., Erasmob, E.D’, Pellicciai, A., Vanacorej, N., 2008. High prevalence of epilepsy in a village in the Littoral Province of Cameroon. Epilepsy Res. 82, 200–210. Radhakrishnan, K., 2009. Challenges in the management of epilepsy in resource-poor countries. Nat. Rev. Neurol. 5, 323–330. Tuan, N.A., Cuong, L.Q., Allebeck, P., Chuc, N.T., Persson, H.E., Tomson, T., 2008. The prevalence of epilepsy in a rural district of Vietnam: a population-based study from the EPIBAVI project. Epilepsia 49, 1634–1637. Tuan, N.A., Tomson, T., Allebeck, P., Chuc, N.T., Cuong, L.Q., 2009. The treatment gap of epilepsy in a rural district of Vietnam: a study from the EPIBAVI project. Epilepsia 50, 2320–2323. World Health Organization, 2001. Epilepsy: Epidemiology, Aetiology and Prognosis. WHO Factsheet, pp. 165. Wang, W.Z., Wu, J.Z., Wang, D.S., Dai, X.Y., Yang, B., Wang, T.P., Yuan, C.L., Scott, R.A., Prilipko, L.L., Boer, H.M., Sander, J.W., 2003. The prevalence and treatment gap in epilepsy in China: an ILAE/IBE/WHO study. Neurology 60, 1544–1545. Winkler, A.S., Kerschbaumsteiner, K., Stelzhammer, B., Meindl, M., Kaaya, J., Kaaya, J., Schmutzhard, E., 2009. Prevalence, incidence, and clinical characteristics of epilepsya community-based door-to-door study in northern Tanzania. Epilepsia 50, 2310–2313.
1994). Treatment gap is a severe problem in developing countries. Our study showed that a large proportion of patients with epilepsy, except Jinuo subjects, did not receive treatment. No patient in the Wa and Nu ethnic groups had even received any antiepileptic treatment before, in particular. This situation, which was consistent with that of developing countries, was much worse than the situation reported in China (Wang et al., 2003; Noronha et al., 2007; Mbuba et al., 2008; Tuan et al., 2009). The high treatment gap among different ethnic subjects could be contributed to some factors: (1) geography; (2) misconception of epilepsy, that the epilepsy was untreatable and the treatment was ineffective; (3) low socioeconomic status in the eight ethnic groups, except for Jinuo people whose average per capita income per year was highest and whose treatment gap was lowest, whose average per capita income per year made antiepileptic drugs unaffordable; (4) deprivation of physical strength, which prevented the patient from working and earning a living; (5) seeking treatment from traditional healers. The major limitation of our study was the lack of electroencephalogram and neuroimaging in some patients, allowed diagnosis on clinical grounds alone. In addition, though there are 26 ethnic groups in Yunnan province, we selected the 8 ethnic groups who inhabit the rural areas in seven cities and autonomous regions and population are relatively low. We will further study other ethnic groups in the future. 5. Conclusions There were both disparity and similarity in the epidemiological and clinical features of epilepsy in different ethnic group communities. References Banerjee, P.N., Filippi, D., Allen, H.W., 2009. The descriptive epidemiology of epilepsy-a review. Epilepsy Res. 85, 31–45. Bartolini, E., Bell, G.S., Sander, J.W., 2011. Multicultural challenges in epilepsy. Epilepsy Behav. 20, 428–434. Benamer, H.T., Grosset, D.G., 2009. A systematic review of the epidemiology of epilepsy in Arab countries. Epilepsia 50, 2301–2304. Burneo, J.G., Tellez-Zenteno, J., Wiebe, S., 2005. Understanding the burden of epilepsy in Latin America: a systematic review of its prevalence and incidence. Epilepsy Res. 66, 63–74. Burneo, J.G., Jette, N., Theodore, W., Begley, C., Parko, K., Thurman, D.J., Wiebe, S., 2009. Disparities in epilepsy: report of a systematic review by the North American Commission of the International League Against Epilepsy. Epilepsia 50, 2285–2295. Commission on Classification and Terminology of the International League Against Epilepsy, 1989. Proposal for revised classification of epilepsies and epileptic syndromes. Epilepsia 30, 389–399. Commission on Epidemiology and Prognosis, International League Against Epilepsy,
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