Reemergence of Foot-and-Mouth Disease, South Korea, 2000–2011

Five outbreaks of foot-and-mouth disease have occurred in South Korea during 2000–2011. Macro-analysis of these outbreaks showed a correlation with outbreaks in countries in eastern Asia. Genetic analyses of food-and-mouth disease viruses in South Korea showed a correlation with viruses that are prevalent in neighboring countries.

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 t-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 (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 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 ± 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 ≤25 days after the initial case, after which occurrence was intermittent ( Figure 2, panel B).

Conclusions
International trade and globalization have recently been indicated as major factors for transmission of infectious diseases associated with livestock (6).  *ME-SA, Middle East-South Asia; USD, US dollars; TMR, total mixed ration; NA, not applicable. †Data were obtained from national epidemiology investigation reports on the 5 foot-and-mouth disease outbreaks in South Korea and the references.
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) (2,4,8), 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, 2010-2011, 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.