Reemergence of foot-and-mouth disease, South Korea, 2000-2011.
To better understand the risks associated with reemergence of this disease in South Korea, we examined characteristics of these outbreaks and those occurring in neighboring countries by using macroscopic analysis. We describe the outbreak patterns to enable prediction and prevention of this disease in South Korea.
Spatiotemporal analyses used data obtained from the World Organisation for Animal Health Information Database (http://www.oie.int), the Food and Agriculture Organization World Reference Laboratory for foot-and-mouth disease (http://www.wrlfmd.org), the Southeast Asia and China Foot-and-Mouth Disease Campaign (http://www.seafmd-rcu.oie.int), national reports for international meetings (Southeast Asia and China Foot-and-Mouth Disease Campaign 2013, World Organisation for Animal Health/ Japan Trust Fund on foot-and-mouth disease control in Asia 2013), and previously reported data (9-11) for Southeast Asia (Vietnam, Cambodia, Myanmar, Thailand, Laos, Malaysia, and the Philippines) and eastern Asia (South Korea, Japan, China, Mongolia, Russia, North Korea, Hong Kong, and Taiwan) regions for 1999-2013. Statistical analysis was performed by using paired or unpaired f-tests, and correlation were made by using GraphPad InStat version 3.05 (Graph Pad Software, La Jolla, CA, USA). A phylogenetic tree was inferred by using the neighbor-joining method, and analysis was conducted by using MEGA version 6 (http://www.megasoftware.net/).
Comparative analysis of outbreaks in neighboring countries over the past 15 years showed a high incidence of outbreaks at 2- to 5-year intervals (2000, 2005, 2010-2011, and 2013) (Figure 1, panels A and F, http://wwwnc.cdc.gov/EID/article/20/12/13-0518-F1.htm). Analysis of outbreak serotypes and cases in neighboring countries (Figure 1, panels A-C) showed that type O foot-and-mouth disease virus has been predominant every year for the past 15 years. Outbreaks in eastern Asia and South Korea over the past 15 years showed a strong relationship with each other (r = 0.725) (Figure 1, panels D-H). Given the overall trend in Asia, serotype Asia 1 was predominant in 2005 (Figure 1, panels A, B). The situation for foot-and-mouth disease in Asia was regarded as serious during 2010-2011 because of the increased numbers of outbreaks (Figure 1, panels A, C-F). In 2013, the number of type A outbreaks increased, and outbreaks caused by types O and A viruses were still considered a threat (Figure 1, panels A, B).
Of 5 outbreaks in South Korea during 2000-2011, 4 were caused by type O virus, 2 were caused by the Middle East-South Asia topotype, and 2 were caused by the Southeast Asia topotype. One of the 5 outbreaks was caused by type A virus (ASIA topotype, Sea-97 lineage) (Table; Figure 1, panel I). Middle East-South Asia topotype viruses that caused outbreaks in 2000 and 2002 were related to PanAsia lineage viruses, which were detected during 19992000 in China, Taiwan, Japan, and Thailand; the causative viruses had high genetic similarity (12). We assume that these viruses, which have predominated in these regions since 1998 (12), were introduced to South Korea in 2000 and 2002. Serotype O viruses that caused outbreaks in 2010 were identified as SEA type, Mya-98 lineage. This virus type was detected in 2010 in Asia, including Russia, Japan, China, Hong Kong, and Vietnam, and the genetic similarity of these viruses was high (Figure 1, panel I). Type A virus (ASIA topotype, Sea-97 lineage) was detected in South Korea in January 2010. This virus is similar to those detected in 2009 in China and Vietnam. Genetic analyses of all viruses detected in South Korea showed a correlation with viruses that predominated in neighboring countries (Figure 1, panel I).
Major putative factors for inter-regional or inter-farm virus transmission during the 5 foot-and-mouth disease outbreaks in South Korea were movement of humans or vehicles (Table). The 5 outbreaks that occurred since 2000 were analyzed by province (Figure 2, panel A). The disease occurred most frequently in Gyeonggi Province (5 times), followed by Chungbuk Province (4 times) and Chungnam Province (3 times). Therefore, these 3 provinces, which had the highest risk for infection, were characterized by a high density of pig and cattle farms. On the basis of analysis of 4 outbreaks, the second round of outbreaks occurred 8.0 [+ or -] 2.0 days after the first infected group had been identified (Figure 2, panel B). In the most recent outbreak in November 2010, the initial diagnosis was delayed for 1 week; many concurrent infections were detected, and no unique aspects of transmission after the first detection of the disease had been identified (Figure 2, panel B). Most infections occurred [less than or equal to] 25 days after the initial case, after which occurrence was intermittent (Figure 2, panel B).
International trade and globalization have recently been indicated as major factors for transmission of infectious diseases associated with livestock (6). Multiple sources of serotypes O, A, and Asia 1 of foot-and-mouth disease viruses, which have caused recent outbreaks in eastern Asia, are endemic to Southeast Asia (13). Incursion of these viruses from Southeast Asia into eastern Asia has been suggested because of the porous nature of borders (13). However, the Korean Peninsula is surrounded by water on 3 sides and shares its only land border with North Korea. We believe that inflow of illegal live animals and livestock products, which is generally the highest risk factor for foot-and-mouth disease (14), is negligible in the regions around South Korea. Access to suspected infectious materials from countries with outbreaks is fundamentally blocked by shipping regulations.
Although no evidence for confirmation of introduction is available, results of epidemiologic investigations have indicated that the 5 foot-and-mouth disease outbreaks in South Korea were related primarily to indirect transmission by humans who came into contact with suspected infectious animals or livestock products from countries in Asia to which the virus is endemic (Table) (2-7). In addition, imported hay or other imported animal products were probable sources of virus in March 2000 and January 2010 (Table) (2,4,8), and the viruses were transmitted to persons who had contact with these materials directly or indirectly. On the basis of the national mandatory reporting system for foreign workers (http://www.kahis.go.kr), we found that the number of persons from Vietnam, Cambodia, Thailand, and China who work on farms in South Korea has been increasing since 2005. The recent situation can be regarded as conducive for an increased risk for foot-and-mouth disease.
The outbreak pattern of foot-and-mouth disease in South Korea was more strongly correlated with outbreaks in countries in eastern Asia than with outbreaks in Southeast Asia. Outbreaks every 15 years caused by type O foot-and-mouth disease virus are predominant in Asia. The greatest risk for infection is currently by type O and A viruses, followed by type Asia 1 virus.
In summary, type O foot-and-mouth disease virus was responsible for 4 outbreaks in South Korea and type A virus accounted for 1 outbreak. South Korea might be at risk for foot-and mouth disease, given the high incidence of this disease at 2- to 5-year intervals (2000, 2005, 20102011, and 2013) in eastern Asia. Foot-and-mouth disease outbreaks in neighboring countries were a probable major source of introduction of this disease into South Korea. Once this disease is introduced, prevention of domestic transmission should include extensive restriction of movement of humans or vehicles during an outbreak.
We thank the staff of the Animal and Plant Quarantine Agency for providing assistance during the study.
This study was supported by a grant from the Animal and Plant Quarantine Agency National Animal Disease Research Project.
Dr Park is a research scientist at the Animal and Plant Quarantine Agency, Gyeonggi-do, South Korea. His research interests are diagnosis and surveillance of foot and mouth disease, and development of vaccines and antiviral agents against this disease.
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Jong-Hyeon Park, Kwang-Nyeong Lee, Su-Mi Kim, Hyang-Sim Lee, Young-Joon Ko, Dong-Seob Tark, Yeun-Kyung Shin, Min-Goo Seo, and Byounghan Kim
Author affiliation: Animal and Plant Quarantine Agency, Gyeonggi-do, South Korea
Address for correspondence: Jong-Hyeon Park, Animal and Plant Quarantine Agency, 175 Anyang-ro, Manan gu, Anyang City, Gyeonggido 430-757, South Korea; email: email@example.com
Table. Characteristics of 5 outbreaks of foot-and mouth-disease, South Korea, 2000-2011 * Characteristic 2000 Mar 2002 May Disease status No. cases 15 16 No. virus-positive cases 15 16 Duration virus detected, 22 52 d Period of virus Mar 24-Apr 15 May 2-Jun 23 detection Host tropism Ruminant Pig (cattle) Serotype O O (ME-SA/PanAsia) (topotype/lineage) (ME-SA/PanAsia) No. affected provinces 3 (6) 2 (4) (cities or counties) Economic losses, US$, 300 143 millions Date of disease-free 2001 Sep 16 2002 Nov 29 status Control measures Eradication policy Culling, Culling vaccination No. cattle culled 2,021 1,372 No. pigs culled 63 158,708 No. other animals culled 132 75 Total culled 2,216 160,155 Area of culling, km radius 0.5 (all) 0.5 (all), 3 (pigs) Vaccine strain O Manisa NA No. animals vaccinated 1st: 860,700, NA booster: 661,700 Vaccination range, 10 NA km radius Serosurveillance area, 20 10 km radius Restricted zones, km radius Management NA NA Surveillance 10-20 3-10 Protection 0-10 0-3 Putative sources Regions in Asia as Northeastern Northeastern possible sources Major sources of first International Overseas travel, outbreak travelers, foreign workers imported hay Low possibility sources Windborne spread Swill, saw dust, of first outbreak of contaminated wild animals and yellow sand, wild birds, yellow sand birds Possible transmission Imported hay Humans and vehicles factor for domestic regions References ([dagger]) (2,8) (3) Characteristic 2010 Jan 2010 Apr Disease status No. cases 7 13 No. virus-positive cases 7 29 Duration virus detected, 28 29 d Period of virus Jan 2-Jan 29 Apr 8-May 6 detection Host tropism Ruminant Ruminant, pig Serotype A (ASIA/SEA-97) O (SEA/Mya-98) (topotype/lineage) No. affected provinces 1 (2) 4 (4) (cities or counties) Economic losses, US$, 29 124 millions Date of disease-free 2010 Sep 27 2010 Sep 27 status Control measures Eradication policy Culling Culling No. cattle culled 2,905 10,858 No. pigs culled 2,953 38,274 No. other animals culled 98 742 Total culled 5,956 49,874 Area of culling, km radius 0.5 0.5, 3 (on 2 farms) Vaccine strain NA NA No. animals vaccinated NA NA Vaccination range, NA NA km radius Serosurveillance area, 10 10 km radius Restricted zones, km radius Management 10-20 10-20 Surveillance 3-10 3-10 Protection 0-3 0-3 Putative sources Regions in Asia as Northeastern Northeastern possible sources Major sources of first Foreign workers, Overseas travel outbreak international parcels Low possibility sources Overseas travel, Imported forage, of first outbreak imported forage, TMR feed tMr feed, saw dust Possible transmission Humans Vehicles, humans factor for domestic (veterinarians, regions meetings, animal feeding) References ([dagger]) (4) (6) 2010 Nov- Characteristic 2011 Apr Disease status No. cases 153 No. virus-positive cases 3,700 Duration virus detected, 145 d Period of virus Nov 28-2011 detection Apr 21 Host tropism Ruminant, pig Serotype O (SEA/Mya-98) (topotype/lineage) No. affected provinces 11 (75) (cities or counties) Economic losses, US$, 3,000 millions Date of disease-free 2014 May 29 status Control measures Eradication policy Culling, vaccination No. cattle culled 150,864 No. pigs culled 3,318,298 No. other animals culled 10,800 Total culled 3,479,962 Area of culling, km radius 0.5 Vaccine strain O Manisa No. animals vaccinated All susceptible animals Vaccination range, Nationwide km radius Serosurveillance area, 10 km radius Restricted zones, km radius Management 10-20 Surveillance 3-10 Protection 0-3 Putative sources Regions in Asia as Southeastern possible sources Major sources of first Overseas travel outbreak Low possibility sources Foreign workers, of first outbreak illegal livestock products Possible transmission Vehicles, humans factor for domestic regions References ([dagger]) (5,7) * ME-SA, Middle East-South Asia; USD, US dollars; TMR, total mixed ration; NA, not applicable. ([dagger]) Data were obtained from national epidemiology investigation reports on the 5 foot-and-mouth disease outbreaks in South Korea and the references.
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|Author:||Park, Jong-Hyeon; Lee, Kwang-Nyeong; Kim, Su-Mi; Lee, Hyang-Sim; Ko, Young- Joon; Tark, Dong-Seob; S|
|Publication:||Emerging Infectious Diseases|
|Date:||Dec 1, 2014|
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