Jpn. J. Infect. Dis., 64, 513-515, 2011

Short Communication Retrospective Study of Extensive Vaccination Programs for Canine Rabies Control and Public Health in Korea

Yi-Seok Joo, Joo-Ho , Kyoung-Ki Lee, Hyeong-Ae Bang1, and Won-Chang Lee2* National Veterinary Research & Quarantine Service, Ministry of Food, Agriculture & Fisheries, Anyang; 1College of Health Sciences, Korea University, ; and 2College of Veterinary Medicine, Konkuk University, Seoul, Korea (Received July 6, 2011. Accepted August 19, 2011)

SUMMARY: This retrospective study of the patterns and efforts of the extensive vaccination programs for canine rabies control (EVPCRC) compared the prevalence rate (PR) of rabies under two different vaccination programs for dogs in Korea between 1962 and 2007. A total of 753 cases of rabid dogs were reported between 1962 and 2007, and there were 350 human cases reported in the same period. There were 518 cases (PR, 4.11) of rabid dogs reported from 1962 to 1979, when the low-egg-passage Flury strain vaccine was used, and a total of 342 human cases were observed over the same period. However, there were 235 rabid dogs (PR, 0.83) identified from 1980 to 2007 when the Evelyn-Rokitnicki-Abelseth strain vaccine was used, and only 8 human cases of rabies were observed during the same period. The prevalence of rabies in dogs during the two periods was significantly different (P º 0.01). Moreover, the year with the largest outbreak, 1975, contained 91 cases, and the PR value was 6.3. In 1963, for hu- mans, there were 103 cases, and the PR value was 0.4. However, in recent years, raccoon dogs have in- creased as a reservoir of rabies in the mountain areas linking North Korea with near the demilitarized zone, reflecting areas with poor EVPCRC.

Rabies is a zoonotic disease that is caused by an RNA animals in Korea (4,6). virus, genus Lyssavirus,familyRhadoviridae.Thedis- This study compares the rabies prevalence under the ease infects both domestic and wild animals and is two vaccination programs for the EVPCRC in Korea spread to humans by contact with infected saliva from 1962 to 2007. During the period from 1962 to through bites or scratches. Rabies is present worldwide, 2007, there were 753 cases of rabid dogs that were con- except in Australia, Japan, Great Britain, most of Ocea- firmed by the National Veterinary Research and nia, some Caribbean islands, etc., but more than 95z Quarantine Service (NVRQS) in the Ministry for Food, of human deaths occur in Asia and Africa. Once sym- Agriculture, Forestry and Fisheries (MFAFF) (7,8). ptoms of the disease develop, rabies is nearly always Data on rabies vaccinations in domestic dogs through- fatal (1). In the Korean Peninsula, the first official out the whole country were obtained from the Food, report of rabies in animals was recorded in 1907 (2–4). Agriculture, Forestry and Fisheries Statistical Yearbook From 1907 to 1945, the epidemiological aspects of ra- of the MFAFF, 1962–2007 (9), and data on the human bies were first apparent with many outbreaks of rabies. cases of rabies were obtained from the Ministry of However, there were few epidemiological studies and Health and Welfare, Republic of Korea, 1962–2007 reports about the outbreaks of animal or human rabies (10,11). in Korea, except for statistical reports by the official ex- In this study, the prevalence rate (PR) of rabies cases pression, until 1960. About 4z of the dog population per 100,000 was calculated. Significant differences be- was inoculated with a phenolglycerin-inactivated rabies tween the PRs between the two vaccination programs vaccine, which was prepared from the brain tissue- were determined using the chi-square test; the levels of derived vaccine of rabbits and produced by Umeno- significance were set at P º 0.05 and P º 0.01, respec- Kondo's methods in Japan (2,5). After the tively. Data analyses were carried out using the statisti- in 1959, the National Veterinary Research Institute de- cal analysis system software, Microsoft Excel 2003. veloped an attenuated-live vaccine containing the low- Dogs in Korea were a principal vector for the trans- egg-passage (LEP) Flury strain, and this vaccine was mission of rabies to other animals and humans. Table 1 used in extensive vaccination programs for canine rabies compares the prevalence of rabies in dogs under the two control (EVPCRC) from 1960 to 1979. Thereafter, from different vaccination programs from 1962 to 2007. 1980 to the present, a tissue culture-attenuated live vac- There were a total of 518 rabid dogs with a PR of 4.11 cine containing the Evelyn-Rokitnicki-Abelseth (ERA) from 1962 to 1979 when the LEP Flury strain vaccine strain has been used for dogs and other domestic wasused(Table1);342humancasesofrabiesoccurred during the same period (Table 1). However, there were 235 rabid dogs (PR, 0.83) identified between 1980 and *Corresponding author: Mailing address: College of Veteri- 2007 when the ERA strain vaccine was used, and only 8 nary Medicine, Konkuk University, Seoul 143-701, Korea. human cases of rabies occurred during the same period. Tel: ＋82-16-223-9096, E-mail: lwcdvm＠yahoo.co.kr The PRs of rabies in dogs during the two periods were

513 significantly different (P º 0.01). Moreover, the use of the cases, and rabid dogs caused the other 6 (7,8). All the ERA vaccine with the EVPCRC (average vaccina- rabies cases, including 6 human cases, occurred at the tion rate, 47.1z) appeared to have reduced the preva- border of the DMZ (8). In Korea, rabies was geographi- lence of canine rabies much more than the LEP Flury cally distributed along the mountain range during the strain vaccine did (37.1z). In 1975, the year with the 1960s, but, in the beginning of the 1970s, rabies began largest outbreak, there were 91 cases, and the PR was to appear in regions of the Gyeonggi and Gangwon 6.3 (Fig. 1). In 1963, there were 103 cases and a PR provinces, near the DMZ (3,6–8). value of 0.4 for humans (Fig. 1). However, in recent As reported by the NVRQS for the period from 1993 years, there has been an increase in the number of rabid to 2007, rabies most frequently occurred in winter with dogs and raccoon dogs (Nyctereutes procyonoides)in 36.0z of the total of 417 cases, while 28.8z were diag- the mountain areas linking North Korea with South nosed in spring, 20.1z in autumn, and 15.1z in sum- Korea near the demilitarized zone (DMZ) (8,12). Since mer (8). 1945, South Korea has been isolated by this zone, which In most endemic countries, stray dogs are the main divides the Korean Peninsula into two, and, thus, it is source of human rabies infection (11,13,14). Rabies, not surprising that the rabies epidemics in Korea are which is a preventable viral disease of mammals, is most similar to those of an island country (3,4). For example, often transmitted through the bite of a rabid animal over the 27-year period from 1980 to 2007, 8 human (1,6–8,11–14). In Korea, the period from 1907 to the deaths from rabies were reported, with 1 death each in present can be divided into four separate phases on the 1982, 1984, 1999, 2001, 2002, and 2005 and 2 deaths in basis of the epidemiological aspects of rabies. The first 2003 (Fig. 1). Bites by rabid raccoon dogs caused 2 of phase, named the endemic period of rabies, occurred between 1907 and 1945. At that time, there were many outbreaks of rabies in Korea; from 1926 to 1938, Table 1. Canine and human rabies prevalence under the two 241,806 stray dogs were killed in order to prevent rabies different extensive vaccination programs for rabies control in (15). During that period, the number of canine rabies Korea, 1962–2007 cases varied from 491 to 881 per year (2,6). The second Vaccine strain phase, called the decrease period of rabies, lasted from the end of the 1950s to 1984, when an average of 24 Item LEP Flury ERA (1962–1979) (1980–2007) cases of rabies occurred annually. The third phase, named the elimination period of rabies, spanned from Total no. of dogs (A) 20,071,708 53,635,674 1985 to 1992, when there were no outbreaks of rabies No. of vaccinated dogs (B) 7,453,357 25,271,719 for 8 years. The fourth phase, named the recurrence No. of susceptible dogs (A－B) 12,618,351 28,363,955 period of rabies, began in 1993. The disease reemerged No. of rabid dogs 518* 235 in 1993 after 8 years of no reported cases, and it showed Prevalence rate per 100,000 4.11* 0.83 a sylvatic form of rabies in different wildlife species No. of human rabies cases 342* 8 with mainly raccoon dogs acting as carriers and/or Chi-square analysis indicated a significant difference from total transmitters near the DMZ in the Korean Peninsula value. (3,4,6,12,16). Therefore, annual oral vaccinations using *P º 0.01. the vaccinia-rabies glycoprotein (V-RG; Merial Ltd., LEP, low-egg-passage; ERA, Evelyn-Rokitnicki-Abelseth. Duluth,Ga.,USA)baitvaccine,hasbeenimplemented

Fig. 1. Chronological observation of the prevalence of rabies in human and dogs under the two different vaccina- tion programs in Korea, 1962–2007. LEP, low-egg-passage; ERA, Evelyn-Rokitnicki-Abelseth; VRG, vaccinia-ra- bies glycoprotein.

514 for wild animals, including raccoon dogs, foxes, and tion of dogs and the results of its practical application. Kitasato wild cats, in the vicinity of the DMZ in South Korea Arch. Exp. Med., 19, 281–293. 6. Hwang, E.K. (1995): Outbreak and control of rabies in animals in since 2002 (8,12). Korea: a review. Korean J. Vet. Public Health, 19, 281–293. The results of this comparison of the prevalence pat- 7. National Veterinary Research and Quarantine Service (NVRQS) terns of rabies under the two vaccination programs for (2007): Surveillance of Rabies. NVEQS, Ministry for Food, the EVPCRC in South Korea from 1962 to 2007 indicate Agriculture, Forestry and Fisheries, Republic of Korea (in that the prevention of rabies in human beings depends Korean). 8. National Veterinary Research and Quarantine Service (NVRQS) upon the management of animal rabies by the (2007): Special Operation Practice (SOP) for Rabies. NVRQS, EVPCRC, as well as the control of stray dogs and Ministry for Food, Agriculture, Forestry and Fisheries, Republic wildlife. of Korea (in Korean). Finally, the development of a public health education 9. Ministry for Food, Agriculture, Forestry and Fisheries (MFAFF) system for rabies prevention and improvement of the (1962–2007): Rabies. MFAFF Statistical Yearbook, 1962–2007 (in Korean). living environment will aid in reducing the number of 10. Ministry of Health and Welfare (1962–2007): Rabies. Yearbook cases of human rabies. of Health and Welfare, 1962–2007 (in Korean). 11. Korea Center for Disease Control (2009): Animal bite cases oc- Conflict of interest None to declare. curred in high-risk region of rabies in 2009. Public Health Wkly. Rep., 3, 225–228 (in Korean). 12. Kim, C.H., Lee, C.G., Yoon, H.C., et al. (2006): Rabies, an REFERENCES emerging disease in Korea. J. Vet. Med. B53, 111–115. 13. World Health Organization (1999): World Survey of Rabies. 1. World Health Organization: Rabies. Fact Sheet N999. Online at number 33 for the year 1997. WHO/CDS/CSR/APH/99.4. p. 〈http://www.who.int/mediacentre/factsheets/fs099/en/〉. 1–5. 2. Lee, H.S. (1967): Rabies. p. 55–62. History of Preventive Medi- 14. Centers for Disease Control and Prevention (2011): Rabies in the cine of Domestic Animals. Korean Veterinary Medical Associa- U.S. and around the World. April 22, 2011. Online at〈http:// tion, Seoul. www.cdc.gov/rabies/〉. 3. Lee, W.C., Chung, C.S., Yun, K.B., et al. (1970): An observation 15. Yamagiwa, S. (1944): Rabies. Epizootiology. p. 21–22. Booneido, on the incidence of rabies in Korea, 1958–1969. Korean Central J. Tokyo. Med., 19, 201–208. 16. Moon, W.K., Won, C.M., Lee, S.S., et al. (2001): Rabies Eradi- 4. Lee, J.H., Lee, M.J., Lee, J.B. et al. (2001): Review of canine ra- cation Plan Using Bite Vaccine in Korea. Report of National bies prevalence under two different vaccination programmes in Veterinary Research and Quarantine Service. The Ministry of Korea. Vet. Rec., 148, 511–512. Agriculture and Forestry, Korea. 5. Umeno, S. and Doi, Y. (1921): A study on the antirabic inocula-

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