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Trends in Epidemiological Aspects and Features by Age-Specific of Japanese Encephalitis in Korea for the Last Two Decades
Won-Hak Kim, M.D.1, Myeong-Jin Lee, Ph.D.2, Won-Chang Lee, Ph.D.3, Young Hwan Kwon, M.D.4
1Department of Nephrology, Asan Medical Center, Ulsan University, Seoul, Korea, 2Faculty of Health and Nutrition, Otemae University, Osaka, Japan, 3College of Veterinary Medicine, Konkuk University,
4Aeromedical Center, Korean Air, Seoul, Korea
The objective of this study concerns trends in the epidemic pattern and aspects of Japanese encephalitis (JE) in Korea over the last two decades between the 1980s (1980~1988) and 2000s (2004~2013). There were a total of 1,641 nationwide cases and 68 deaths of JE with a cumulative incidence rate (CIR) and cumulative mortality rate (CMR) of 0.431 and 0.018 per 100,000 populations in the 1980s, and a total of 88 cases and 17 deaths of JE with a CIR and CMR was 0.19 and 0.003 in the 2000s. The CIR and CMR in the 1980s was tended to decreased to the 2000s, (P＜0.01). However, the case-fatality rate (CFR) in the 1980s (4.1%) was increased from the 1980s to 2000s (19.3%), (P＜0.01). The age distribution of JE cases was as follows; an 87.3% of the JE cases involved those younger than 19-years old in the 1980s and an 87.5% of the cases in the 2000s involved those over 40-years old; these were the trending changes from the 1980s to the 2000s, (P＜0.01). Consideration should be given to an adult such as swineherd workers or livestock farmers, so that the immunization policy in Korea can benefit them for the better planning of future control strategies.
Key words: Japanese encephalitis, Epidemiologic studies, Republic of Korea
Received: December 7, 2016, Accepted: December 21, 2016
Correspondence: Young Hwan Kwon, Aeromedical Center, Korean Air, 260 Haneul-gi, Gangseo-gu, Seoul 07505, Korea Tel: 82-2-2656-7150, Fax: 82-2-2656-3848 E-mail: [email protected]
I. INTRODUCTION
Japanese encephalitis (JE), once a major zoonosis of the public health problems in Republic of Korea, has declined since the 1980s, as a result of improved living conditions, a mosquito eradication program, and a national JE vaccination program for all children [1,2], and gilts in swinery endemic areas for swine [3].
Although JE has traditionally been regarded as a childhood disease the majority of cases now occur in adults in countries where strong immunization program exit, such as in Korea [1]. Culex tritaeniorhynchus is the primary vector of Japanese encephalitis virus (JEV) in a member of the genus Flavivirus of the family Flaviviridae, a leading cause of encephalitis in the Asia zone. JEV is transmitted in an enzootic cycle involving large wading birds as the reservoirs and swine as the amplifying hosts. The JEV was isolated for the first time from an American soldier in 1946 [2,4,5], and was also
recovered from Korean patients who died in the epidemic in 1949, when 5,548 cases with 2,429 deaths were reported [2,6]. In 1954, when the Communicable Disease Control Act (Reg. 308) was enacted, JE was classified as a first-class notifiable communicable disease [2]. Thereafter, the largest recorded JE epidemic, involving 6,897 reported cases, occurred in 1958 [7]. Consequently, in 1963, JE was reclassified as a second-class notifiable disease in Korea [8].
Historically, JE has previously been recognized as a childhood infection in Korea. However, recently in Korea, the trend of the JE cases show that the majority of cases now occur in adults who have not had a vaccination; the elderly, however, do not seem to contract it [1,2,8-13]. To address this, the aim of the epide- miological study was to summarize the data extraction of JE cases in the Republic of Korea that reported to the Korea Center for Disease Control and Prevention (KCDC) over the last two decades between the 1980s (1980~1988) and 2000s (2004~2013).
This study provides a comprehensive epidemic pattern, and aspects and an overview of JE during the past two decades in Korea to shed insight on how to more effectively plan future strategies.
Table 1. Comparative observation of the epidemiological indices of Japanese encephalitis in Korea between two decades
Item 1980s (1980~1989) 2000s (2004~2013)
Cases Rate (95% CI) Cases Rate (95% CI)
Total No. of patients 1,641 88
CIR per 100,000 0.431 (0.411~0.452)* 0.019 (0.015~0.023)
Total No. of deaths 68 17
CMR per 100,000 0.018 (0.014~0.022)* 0.003 (0.002~0.004)
Case-fatality rate (%) 4.1 (3.2~5.1) 19.3 (11.1~27.6)*
Remarks: CIR (Cumulative Incidence Rate) and CMR (Cumulative Mortality Rate) per 100,000 populations; Case-fatality rate in %; 95%
CI; Confidence Interval of 95% of rate. Statistical significant levels set at *P＜0.01.
II. MATERIALS AND METHODS 1. Data
It is our intention to study the outbreaks of JE for the epidemic patterns and aspects in Korea over the last two decades (1980s:
1980~1989 and 2000s: 2004~2013) under the following six headings; cumulative incidence rate (CIR), cumulative mortality rate (CMR), cases-fatality rate (CFR) for the epidemic indices, and the epidemic aspects including the age distribution, monthly and seasonality and geographically distribution of JE surveillances.
In this present descriptive study, we investigated a total of 1,641 patients and 68 fatal cases of JE from 1980 to 1989 (1980s), and those of 88 and 17 cases from 2004 to 2013 (2000s). We utilized the raw data of JE cases from the National Disease Surveillance System (website) and the Infectious Diseases Sur- veillance Yearbooks of Korea Center for Disease Control and Prevention (KCDC), 1980~2013, the Ministry of Health and Welfare, Republic of Korea [8].
2. Statistical analysis
In this study, the CIR and CMR of JE cases per 100,000 populations were estimated by the criteria that the World Health Organization (WHO) established and the upper and lower limits of 95% confidence interval (CI) of rates were calculated. Statis- tically significant differences between the epidemiological aspects and risk factors were determined using the Chi-square test or the paired t-test, and the data analyses were carried out using the statistical system software, Microsoft Excel 2007. The results were considered to be statistically significant at P＜0.05 and P＜0.01.
III. RESULTS
Trends in the epidemic indices including the CIR, CMR and CFR of JE in Korea between 1980s (1980~1989) and 2000s (2004~2013) were compared by nationwide, as shown in Table 1. There were a total of 1,641 nationwide patients and 68 fatal cases of JE with an CIR and CMR of 0.431 and 0.018 per 100,000 populations in the 1980s, and a total of 88 cases and 17 deaths of JE with an IR and MR of 0.019 and 0.003 in the 2000s; both the CIR and CMR of JE decreased by much more than those in the 2000s, respectively, (P＜0.01). However, the CFR of JE in the 2000s (19.3%) was significantly higher than in the 1980s (4.1%), (P＜0.01).
In Table 2, one of the epidemic aspects of JE cases, the percentage distribution by age groups in the 1980s was as follows:
in age groups of younger than 9, 10~19, 20~29, 30~39, 40~49, 50~59 and over 60 years, the cases of JE were 43.1%, 44.2%, 8.2%, 2.5%, 1.8%, 0%, and 0%, respectively, (P＜0.01). However, the JE cases in the 2000s were greatly changes as follows: 2.3%, 1.1%, 2.3%, 6.8%, 34.1%, 31.8%, and 21.6%, respectively (P＜
0.01), (Fig. 1). In the 1980s, the pediatric age group had a high prevalence rate, and in the 2000s, the adult age group had a relatively high prevalence rate. Moreover, the epidemic pattern of age distribution of JE cases show that the overall incidence of outbreaks resulting by the age group including younger than 9 (−40.8%), 10~19 (−43.1%), 20~29 (−5.9%), 30~39 (＋
4.2%), 40~49 (＋32.3%), 50~59 (＋31.8%) and over 60 years old (＋21.6%) tended to be changes from 1980s to 2000s (P＜
0.01).
The estimation of the seasonal pattern of outbreaks of JE- infection patients in the 1980s, in the order of spring, summer, autumn and winter were 0%, 7.4%, 92.6% and 0%, respectively, (P＜0.01), and the outbreaks of JE in the 2000s were similar to those in the 1980s. Additionally, the main epidemic period of JE outbreaks was between August and October (over 90% of the total
Table 2. Comparison of trends in epidemiological aspects and features of Japanese encephalitis in Korea between two decades
Item 1980s (1980~1989) 2000s (2004~2013) Change rate
Cases % (95% CI) Cases % (95% CI) (%)
Age distribution
＜9 707 43.1 (40.7~45.5) 2 2.3 (−0.8~5.4) −40.8**
10~19 726 44.2 (41.8~46.6) 1 1.1 (−1.1~3.3) −43.1**
20~29 135 8.2 (7.0~9.5) 2 2.3 (−0.8~5.4) −5.9*
30~39 42 2.6 (2.1~3.7) 6 6.8 (1.5~12.1) ＋4.2*
40~49 29 1.8 (1.2~2.4)) 30 34.1 (24.2~44.0) ＋32.3**
50~59 0 0 28 31.8 (22.9~41.5) ＋31.8**
＞60 0 0 19 21.6 (13.0~30.2) ＋21.6**
Total 1,641 88
Season
Spring 0 0 1 - -
Summer 122 7.4 (6.1~8.7) 4 4.5 (0.2~8.8) −2.9
Autumn 1,519 92.6 (91.3~93.9) 81 92.1 (86.5~97.7) −0.5
Winter 0 0 2 -
Total 1,641 88
Geographically
Northern region 439 26.8 (24.9~29.2) 36 40.9 (30.6~51.2) ＋14.1**
Central region 376 22.9 (21.1~25.1) 17 19.3 (11.1~27.5) −3.6
Southern region 782 47.7 (45.3~50.1) 35 39.8 (29.6~50.0) −7.9
Jeju 30 1.8 (1.2~2.4) - - -
Unknown 14 0.9 (0.4~0.5) - - -
Total 1,641 88
Footnotes are in Table 1.
Fig. 1. Trends in distribution rate (%) by the age-specific of Japanese encephalitis cases in Korea for the last two decades.
cases) regardless of the epidemic size.
The epidemiological aspects of JE cases that occurred in Korea between 1980s and 2000s were analyzed by association with the geographical risks. A summary of incidence cases of JE in relation to geography reveals that the percentage distribution of the significant outbreaks for the Northern, Central, Southern and Jeju
(island) regions were 26.8%, 22.9%, 47.7% and 0.9% in the 1980s, respectively. However, the JE cases in the 2000s trended to be changes as follows: 40.9%, 19.3%, 39.3% and 0%, respec- tively (P＜0.01).
IV. DISCUSSION
JE is an arbovirosis by mosquito-borne zoonosis, and it has been recently recognized to be reemerging as it has expended in Korea from 2001 up to now [8,9]. In the case reports of the 1960s in Korea, several thousand cases of JE were reported annually until 1968, with the exception of 1963, when only 19 cases were reported [2,9]. The last large epidemic was reported in 1982, when 1,197 cases and 40 deaths (CFR: 3.34%) were reported [2,9,11-14]. Thus, JE outbreaks which were once a public health problem in Korea, have declined since the 1980s, as a result of improved living conditions, a mosquito eradication program related to the extensive use of pesticides in rice farming, which led to a marked decrease of Culex tritaeniorhynchus in rural habitats, and a national JE vaccination program, which includes an annual booster vaccine for all children [1,2,10,13], and in the vaccination of
young breading gilts and boars in swinery areas of the JE endemic the mosquito season starts; this vaccination is commonly done with attenuated vaccine but inactivated vaccine are also available [3].
Moreover, the Animal, Plant and Fisheries Quarantine Inspection Agency (QIA) of Korea has vaccinated a total of over 21 million for gilts and boars in swinery between 2001 and 2012 [3].
However, in the recent years in Korea, the trend of the JE cases from 2005 to 2013 show that the number of JE patients in Korea tended to increase year after year from 6 case in 2005 to 26 cases in 2010, when it was at its peak [8,9]. In the cases of Korea, since the CFR of JE screening test came into force in 1966, the CFR of JE cases in Korea has increased from 26.6% in 1966 to 30.0% in 1967 and peaked at 32.3% in 1968. However, the outbreaks of JE cases have decreased from the 1970s to now [8-11]. Thus in Korea, CIR, CMR and CFR of JE have declined since the 1983 after great outbreaks of JE, as a result of improved environmental conditions for living, a mosquito eradication pro- gram, and a national JE vaccination program for both children under 12 years of age, and gilts and boars in swinery as the amplifying hosts of JEV [1,2,8,10,13]. However, the majority of JE cases now occur in human adults in countries without immu- nization programs, such as in the swinery areas [1,8]. This is believed to be due to the different responsibilities that men have in their jobs and the various activities that are characteristics to the livestock fields such as a pigsty in swineherd [1,8,9,10].
Conversely, JE has traditionally been regarded as a childhood disease [1,2,8-13]. However, the majority of cases of JE now occur in adults in countries where strong immunization programs exist, such as in Korea. Our findings show a significantly highest incidence of cases of confirmed JE in those aged more than 40 years in the 2000s (P＜0.01). Moreover, the age distribution of JE cases was as follows; an 87.3% of the JE cases involved those younger than 19-years old in the 1980s and an 87.5% of the cases in the 2000s involved those over 40-years old; these were the trending changes from the 1980s to the 2000s (P＜0.01). In the 1980s, the pediatric age group had a high prevalence rate, and in the 2000s, the adult age group had a relatively high prevalence rate. While JE has traditionally been regarded as a children’s disease, the majority of cases now occur in adults who vaccination programs for adults except in Korea.
The estimation of the seasonal pattern of outbreaks of JE-infection patients in the 1980s, in order of spring, summer, autumn and winter were 0%, 7.4%, 92.6% and 0%, respectively, and the outbreaks of JE in the 2000s were similar to those in the 1980s. These data strongly indicate for JE in Korea that the first cases of JE were usually reported in early August, and the
epidemics cases in late November; more than 80% were among children 8 to 15 years of age [2,7-11]. Thus, JE outbreaks which were once a public health problem in Korea, have declined since the 1980s, as a result of improved living conditions, a mosquito eradication program related to the extensive use of pesticides in rice farming, and a national JE vaccination program for all children [1,2,10,13]. In addition, historically the JE epidemic was highly incident Korea during 1965 to 1984, and a higher incidence recorded in the Southwestern areas, which are mainly under rice cultivation with large flooded rice paddies, in contrast to the mountainous Northeastern area. Vector mosquito populations were more prevalent in the Southwestern than in the Northeast areas [2,6,12]. However, the risks of JE between the Northern and Southern regions were similar in the 2000s. Thus, the occurrence of JE in Korea has declined since the 1980s, as a result of improved living environment, and a national JE vaccination program for all children.
Finally, we see from the retrospective review of the epidemic patterns of JE outbreaks in Korea that the period from 1955 to the present can be divided in to four separate phases on the basis of the epidemiology. The first phase, named the emerged period of JE, occurred between 1955 and 1966. At that time, there were many outbreaks of JE in Korea, when 22,111 cases (IR: 7.3 per 100,000) with 7,324 deaths (CFR: 33.1%) were reported [6]. The second phase, called the endemic period of JE, lasted from the end of the 1967 to 1984, when an average of 458 cases of JE occurred annually. The third phase, named the elimination period of JE, spanned from 1985 to 2000, when there were a few cases of JE for 15 years. Thereafter, the fourth phase, named the reemerging period of JE began in 2001 [8,13,15]. Moreover, the majority of JE cases now occur in adults in Korea, who are may be in immunization programs except for JE.
In conclusion, consideration should be given to an adult such as swineherd workers or livestock farmers, so that the immuni- zation policy in the near future in Korea can benefit them. This study provides an epidemiological aspect analysis of JE outbreaks in Korea between the 1980s and the 2010s and on the better planning of future control strategies. We hope that this informa- tion will be a useful for public health service as a reference for further studies on JE.
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=국문초록=
이 연구의 목적은 1980년대(1980∼1988)와 2000년대(2004∼2013) 사이의 지난 20년간 한국에서 일본뇌염의 전염 패 턴 및 경향에 관한 것이다. 총 1,641건의 전국 사례와 68건의 일본뇌염 사망자가 있었으며, 1980년대 인구 10만 명당 누적 발생률과 누적 사망률은 0.431과 0.018이었으며, 총 88건과 17건의 사망자가 발생했다. 2000년대 누적 발생률과 누적 사망률은 0.19와 0.003이었다. 1980년대의 누적 발생률과 누적 사망률은 2000년대에는 감소하는 경 향이 있었다(P＜0.01). 그러나 1980년대 4.1%였던 치사율은 2000년대에 19.3%로 증가했다(P＜0.01). 일본뇌염의 연 령 분포는 다음과 같다. 1980년대 일본뇌염 환자의 87.3%는 19세 이하였고, 2000년대의 87.5%는 40세 이상이었다.
이는 1980년대에서 2000년대로의 유의한 추세 변화였다(P＜0.01). 따라서, 돼지나 축산 농가의 어른들을 대상으로 한 예방 접종 정책은 장래의 방제 전략 수립에 도움이 될 수 있다.
중심단어: 일본뇌염, 역학 연구, 대한민국
