Focused Issue of This Month Emerging Parasitic Diseases in Korea JongYil Chai, MD Department of Parasitology and Tropical Medicine, Seoul National University College of Medicine Email : cjy@snu.ac.kr J Korean Med Assoc 2007; 50(11): 946-958 Abstract Parasitic diseases of the Korean people have remarkably changed in terms of the kinds of major parasites and the prevalence of each parasite species. In particular, after the 1970~ 80s, the prevalence of soiltransmitted nematode infections became very low, and instead, those diseases that had been veiled by the soiltransmitted nematodes became unveiled and attention is paid to these parasitic infections. It is also of note that various kinds of new parasitic infections emerged, and malaria that disappeared in the late 1970s reemerged after 1993. The number of parasite species that emerged or reemerged since 1980 is at least 36 species. Among them, protozoan species include Acanthamoeba spp., Babesia spp., Plasmodium vivax, Cryptosporidium hominis, and Cryptosporidium parvum. Nematode species are Capillaria hepatica, Toxocara canis, Toxocara cati, Ancylostoma caninum, Ancylostoma braziliense, Mammomonogamus laryngeus, Pseudoterranova decipiens, Trichinella spiralis, and Capillaria philippinensis. The emerged trematode species include Centrocestus armatus, Stictodora lari, Heterophyopsis continua, Metagonimus miyatai, Plagiorchis vespertilionis, Neodiplostomum seoulense, Stellantchasmus falcatus, Heterophyes nocens, Echinostoma cinetorchis, Clinostomum complanatum, Echinochasmus japonicus, Stictodora fuscata, Plagiorchis muris, Gymnophalloides seoi, Pygidiopsis summa, Metagonimus takahashii, Acanthoparyphium tyosenense, and Echinostoma hortense. Cestode species newly reported from humans are Spirometra erinacei, Taenia asiatica, Diphyllobothrium yonagoense, and Mesocestoides lineatus. Most of these species are, with the exception of P. vivax and several others, foodborne parasites. For prevention of these parasitic infections, consumption of wellcooked food is essential. Keywords : Emerging parasitic diseases; Foodborne parasites 946
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Chai JY Table 1. Parasites reported from humans after 1980 in the Republic of Korea and the source of infection Year Parasite species (common name) Infection source 1980 Echinostoma cinetorchis loach, large snail 1981 Heterophyes nocens mullet, goby 1981 Pygidiopsis summa mullet, goby 1982 Neodiplostomum seoulense snake, frog 1983 Echinostoma hortense freshwater fish, loach 1984 Spirometra erinacei snake, frog 1984 Stellantchasmus falcatus mullet, goby 1984 Heterophyopsis continua perch 1984 Pseudoterranova decipiens sea fish, codfish 1985 Echinochasmus japonicus freshwater fish, carps 1986 Toxocara spp. polluted soil, vegetables 1988 Stictodora fuscata mullet, goby 1988 Centrocestus armatus freshwater fish, minnow 1988 Diphyllobothrium yonagoense sea fish 1991 Babesia spp. tick 1992 Mesocestoides lineatus chicken, snake 1992 Acanthamoeba spp. contact lens and container 1993 Taenia asiatica pig liver 1993 Capillaria hepatica cat feces 1993 Plamodium vivax anopheline mosquito 1993 Capillaria philippinensis freshwater fish 1993 Gymnophalloides seoi oyster 1993 Cryptosporidium parvum polluted water, cattle feces 1995 Clinostomum complanatum freshwater fish 1995 Ancylostoma spp. polluted soil 1996 Plagiorchis muris freshwater fish, naiads of dragonfly 1997 Metagonimus takahashii freshwater fish, carps 1997 Metagonimus miyatai common minnow 1997 Trichinella spiralis pig, wild animals (muscle, viscera) 1998 Mammomonogamus laryngeus wild animals 2001 Acanthoparyphium tyosenense mud bivalve, gastropod 2002 Stictodora lari mullet, goby 2006 Cryptosporidium hominis polluted water, human-human 207 Plagiorchis verpertilionis insect(?) 948
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Emerging Parasitic Diseases 11. Cho HK, Moon YS, Lee HK, Park AJ, Cho SI. Acanthamoeba keratitis (case report). J Korean Ophthalmol Soc 1992; 33: 538-543 (in Korean). 12. Park YM, Hahn TW, Choi SH, Lee JS, Lee JE. Acanthamoeba keratitis related to cosmetic contact lenses. J Korean Ophthalmol Soc 2007; 48: 991-994 (in Korean). 13. Lee JE, Hahn TW, Yu HS, Lee JS. Acanthamoeba keratitis related to orthokeratology contact lens. J Korean Ophthalmol Soc 2007; 48: 328-331 (in Korean). 14. Kim HT, Song YW, Choe KW, Chai JY, Lee SH. An imported case of human babesiosis in Korea. Korean J Int Med 1988; 35: 569-573 (in Korean). 5. Sim JG, Park HS, Ahn DH, Kho WG, Chai JY. A case of babesiosis in an eight year old Korean boy. J Korean Pediatr 1991; 34: 1417-1421 (in Korean). 16. Lee SS, Yang SY, Cho YK, Kim E, Kim YS, Woo JH, Ryu J, Chai JY. An imported case of babesiosis. Korean J Infec Dis 1997; 29: 49-52 (in Korean). 17. Park JH, Guk SM, Han ET, Shin EH, Kim JL, Chai JY. Genotype analysis of Cryptosporidium spp. prevalent in a rural village in Hwasungun, Republic of Korea. Korean J Parasitol 2006; 44: 27-33. 18. Chai JY, Lee SH, Guk SM, Lee SH. Epidemiological survey of Cryptosporidium parvum infection in randomly selected inhabitants of Seoul and Chollanamdo. Korean J Parasitol 1996; 34: 113-119. 19. Guk SM, Seo M, Park YK, Oh MD, Choe KW, Kim JL, Choi MH, Hong ST, Chai JY. Parasitic infections in HIVinfected patients who visited Seoul National University Hospital during the period 1995-2003. Korean J Parasitol 2005; 43: 1-5. 10. Chai IH, Lim GI, Yoon SN, Oh WI, Kim SJ, Chai JY. Occurrence of tertian malaria in a male patient who has never been abroad. Korean J Parasitol 1994; 32: 195-200 (in Korean). 11. Cho SY, Kong Y, Park SM, Lee JS, Lim YE, Chae SL, Kho WG, Lee JS, Shim JC, Shin HK. Two vivax malaria cases detected in Korea. Korean J Parasitol 1994; 32: 281-284. 12. Han ET, Lee DH, Park KD, Seok WS, Kim YS, Tsuboi T, Shin EH, Chai JY. Reemerging vivax malaria: changing patterns of annual incidence and control programs in the Republic of Korea. Korean J Parasitol 2006; 44: 285-294. 13. Chai JY. Reemerging Plasmodium vivax malaria in the Republic of Korea. Korean J Parasitol 1999; 37: 129-143. 14. Kho WG, Jang JY, Hong ST, Lee HW, Lee WJ, Lee JS. Border malaria characters of reemerging vivax malaria in the Republic of Korea. Korean J Parasitol 1999; 37: 71-76. 15. Lee JS, Kho WG, Lee HW, Seo M, Lee WJ. Current status of vivax malaria among civilians in Korea. Korean J Parasitol 1998; 36: 241-248. 16. Kwak YH, Choi SE, Na SY, Lee HJ, Chai JY. Two cases of re emerging indigenous malaria in Korean children. J Korean Pediatr 1997; 4: 288-292. 17. Jeong IK, Oh MD, Chai JY, Lee HW, Lee WJ, Lee JS, Seo DH, Choi KW. A case of transfusioninduced malaria presenting as fever of unknown origin. Korean J Inf Dis 1999; 31: 41-45. 18. Park JH, Kim HJ, Guk SM, Shin EH, Kim JL, Rim HJ, Lee SH, Chai JY. A survey of cryptosporidiosis among 2,541 residents of 25 coastal islands in Jeollanamdo (Province), Republic of 955
Chai JY Korea. Korean J Parasitol 2006; 44: 367-372. 19. Chai JY, Shin SM, Yun CK, Yu JR, Lee SH. Experimental activation of cryptosporidiosis in mice by immunosuppression. Korean J Parasitol 1990; 28: 31-37 (in Korean). 20. Cho MH, Kim AK, Im KI. Detection of Cryptosporidium oocysts from outpatients of the Severance hospital. Korean J Parasitol 1993; 31: 193-200. 21. Choe GY, Lee HS, Seo JK, Chai JY, Lee SH, Eom KS, Chi JG. Hepatic capillariasisfirst case report in Korea. Am J Trop Med Hyg 1993; 48: 610-625. 22. Kim HY, Lee SM, Joo JE, Na MJ, Ahn MH, Min DY. Human syngamosis: the first case in Korea. Thorax 1998; 53: 717-718. 23. Seo BS, Chai JY, Lee SH, Hong ST, Seo JW, Noh SH. A human case infected by the larva of Terranova type A in Korea. Korean J Parasitol 1984; 22: 248-252. 24. Sohn WM, Seol SY. A human case of gastric anisakiasis by Pseudoterranova decipiens larva. Korean J Parasitol 1994; 22: 248-252. 25. Im KI, Shin HJ, Kim BH, Moon SI. Gastric anisakiasis cases in Chejudo, Korea. Korean J Parasitol 1995; 33: 179-186. 26. Yu JR, Seo M, Kim YW, Oh MH, Sohn WM. A human case of gastric infection by Pseudoterranova decipiens larva. Korean J Parasitol 2001; 39: 193-196. 27. Chai JY. Parasitic diseases of the gastrointestinal and biliary system. Proceedings of the 1st CME Seminar, Korean Society of Gastroenterology 1995; p 21-37. 28. Lee HC, Kim JS, Oh HY, Kim JH, Kim HG, Lee MS, Kim WJ, Kim HY. A case of trichinosis caused by eating wild badger. Korean J Med 1999; 56: 134-138 (in Korean). 29. Sohn WM, Kim HM, Chung DI, Yee ST. The first human case of Trichinella spiralis infection in Korea. Korean J Parasitol 2000; 38: 111-115. 30. Kim E, Pyun RH, Park JH, Kim KH, Choi I, Park HH, Lee YH, Yong TS, Hong SK. Family outbreak of trichinosis after eating a raw meat of wild swine. Infec Chemo 2003; 35: 180-184 (in Korea). 31. Choi JS, Kim HJ. A case of presumed ocular toxocariasis. J Korean Ophthalmol Soc 1986; 27: 861-865 (in Korean). 32. Kim YJ, Kyung SY, An CH, Lim YH, Park JW, Jeong SH, Lee SP, Choi DC, Jeong YB, Kang SY. The characteristics of eosinophilic lung diseases caused by Toxocara canis larval infestation. Tuberc Respir Dis 2007; 62: 19-26 (in Korean). 33. Jung JK, Jung JT, Lee CH, Kim EY, Kwon JG, Kim BS. A case of hepatic abscess caused by Toxocara. Korean J Hepatol 2007; 13: 409-413 (in Korean). 34. Kwon IH, Kim HS, Lee JH, Choi MH, Chai JY, Nakamura- Uchiyama F, Nawa Y, Cho KH. A serologically diagnosed human case of cutaneous larva migrans caused by Ancylostoma caninum (case report). Korean J Parasitol 2003; 41: 233-237. 35. Jang IK, Lee DW, Cho BK. A case of cutaneous larva migrans. Korean J Dermatol 1995; 33: 396-400 (in Korean). 36. Kim TH, Lee BS, Sohn WM. Three clinical cases of cutaneous larva migrans. Korean J Parasitol 2006; 44: 145-149. 37. Sohn JH, Park HR, Song KY, Cho SY. Cutaneous infection of larval Strongyloides stercoralis manifesting pseudolymphomatous reactions. Korean J Pathol 1996; 30: 466-469 (in Korean). 38. Lee SH, Hong ST, Chai JY, Kim WH, Kim YT, Song IS, Kim SW, Choi BI, Cross JH. A case of intestinal capillariasis in the Republic of Korea. Am J Trop Med Hyg 1993; 48: 542-546. 39. Hong ST, Kim YT, Choe GY, Min YI, Cho SH, Kim JK, Kook J, Chai JY, Lee SH. Two cases of intestinal capillariasis in Korea. Korean J Parasitol 1994; 32: 43-48. 40. Lee SH, Rhee PL, Lee JH, Kee KT, Le JK, Sim SG, Lee SK, Kim JJ, Ko KC, Paik SW, Rhee JC, Choi KW, Lee NY, Cho SL, Ryu KH. A case of intestinal capillariasis: fourth case report in Korea. Korean J Gastroenterol 1999; 34: 542-546 (in Korean). 41. Kwon YM, Jung HY, Ha HK, Lee I. An imported case of intestinal capillariasis as proteinlosing enteropathy. Korean J Pathol 34: 235-238 (in Korean). 42. Hong SJ, Seo BS, Lee SH, Chai JY. A human case of Centrocestus armatus infection in Korea. Korean J Parasitol 1988; 26: 55-60. 43. Chai JY, Han ET, Park YK, Guk SM, Park JH, Lee SH. Stictodora lari (Digenea: Heterophyidae): the discovery of the first human infections. J Parasitol 2002; 88: 627-629. 44. Seo BS, Lee SH, Chai JY, Hong SJ. Studies on intestinal trematodes in Korea. XIII. Two cases of natural human infection by Heterophyopsis continua and the status of metacercarial infection in brackish water fishes. Korean J Parasitol 1984; 19: 51-60. 45. Park JH, Kim JL, Shin EH, Guk SM, Park YK, Chai JY. A new endemic focus of Heterophyes nocens and other heterophyid infections in a coastal area of Gangjingun, Jeollanamdo. Korean J Parasitol 2007; 45: 33-38. 46. Saito S, Chai JY, Kim KH, Lee SH, Rim HJ. Metagonimus miyatai sp. nov. (Digenea: Heterophyidae), a new intestinal trematode transmitted by freshwater fishes in Japan and Korea. Korean J Parasitol 1997; 35: 223-232. 47. Guk SM, Kim JL, Park JH, Chai JY. A human case of Plagiorchis verpertilionis (Digenea: Plagiorchiidae) infection in the Republic of Korea. J Parasitol 2007; 93: 1225-1227. 48. Seo BS, Rim HJ, Lee CW. Studies on the parasitic helminths in Korea. I. Trematodes of rodents. Korean J Parasitol 1964; 2: 20-26. 49. Seo BS. Fibricola seoulensis Seo, Rim et Lee, 1964 (Trematoda) and fibricoliasis in man. Seoul J Med 1990; 31: 61-96. 956
Emerging Parasitic Diseases 50. Quan F, Jiang T, Ma H, Cui C, Sun L. The first discovery of Fibricola seoulensis in China. J Yanbian Med Coll 1995; 18; 17-20 (in Chinese). 51. Kook J, Nawa Y, Lee SH, Chai JY. Pathogenicity and lethality of a minute intestinal fluke, Neodiplostomum seoulense, to various strains of mice. J Parasitol 1998; 84: 1178-1183. 52. Chai JY, Shin EH, Han ET, Guk SM, Choi MH, Lee SH. Genetic difference in susceptibility and fatality of three strains of mice experimentally infected with Neodiplostomum seoulense. J Parasitol 2000; 86: 1140-1144. 53. Seo BS, Lee SH, Chai JY, Hong SJ. Studies on intestinal trematodes in Korea. XII. Two cases of human infection by Stellantchasmus falcatus. Korean J Parasitol 1984; 22: 43-50. 54. Sohn WM, Chai JY, Lee SH. A human case of Stellantchasmus falcatus infection. Korean J Parasitol 1989; 27: 277-279. 55. Seo BS, Hong ST, Chai JY. Studies on intestinal trematodes in Korea III. Natural human infections of Pygidiopsis summa and Heterophyes heterophyes nocens. Seoul J Med 1981; 22: 228-235. 56. Chai JY, Murrell KD, Lymbery AJ. Fishborne parasitic zoonoses: status and issues. Intern J Parasitol 2005; 35: 1233-1254. 57. Chai JY, Park JH, Han ET, Shin EH, Kim JL, Guk SM, Hong KS, Lee SH, Rim HJ. Prevalence of Heterophyes nocens and Pygidiopsis summa infections among residents of the western and southern coastal islands of the Republic of Korea. Am J Trop Med Hyg 2004; 71: 617-622. 58. Seo BS, Cho SY, Chai JY. Studies on intestinal trematodes in Korea. I. A human case of Echinostoma cinetorchis infection with an epidemiological investigation. Seoul J Med 1980; 21: 21-29. 59. Ryang YS, Ahn YK, Kim WT, Shin KC, Lee KW, Kim TS. Two cases of human infection by Echinostoma cinetorchis. Korean J Parasitol 1986; 24: 71-76 (in Korean). 60. Lee SK, Chung NS, Ko IH, Ko HI. A case of natural human infection by Echinostoma cinetorchis. Korean J Parasitol 1988; 26: 61-64 (in Korean). 61. Chung PR, Jung Y, Park YK. Segmentina hemisphaerula: a new molluscan intermediate host for Echinostoma cinetorchis in Korea. J Parasitol 2001; 87: 1169-1171. 62. Chung DI, Moon CH, Kong HH, Choi DW, Kim DK. The first human case of Clinostomum complanatum (Trematoda: Clinostomidae) infection in Korea. Korean J Parasitol 1995; 33: 219-223. 63. Seo BS, Lee SH, Chai JY, Hong SJ. Studies on intestinal trematodes in Korea. XX. Four cases of natural human infection by Echinochasmus japonicus. Korean J Parasitol 1985; 23: 214-220. 64. Chai JY, Hong SJ, Lee SH, Seo BS. Stictodora sp. (Trematoda: Heterophyidae) recovered from a man in Korea. Korean J Parasitol 1988; 26: 127-132. 65. Chai JY, Lee SH. Foodborne intestinal trematode infections in the Republic of Korea. Parasitol Int 2002; 51: 129-154. 66. Hong SJ, Woo HC, Chai JY. A human case of Plagiorchis muris (Tanabe, 1922: Digenea) infection in the Republic of Korea: Freshwater fish as a possible source of infection. J Parasitol 1996; 82: 647-649. 67. Lee SH, Chai JY, Hong ST. Gymnophalloides seoi n. sp. (Digenea: Gymnophallidae), the first report of human infection by a gymnophallid. J Parasitol 1993; 79: 677-680. 68. Chai JY, Choi MH, Yu JR, Lee SH. Gymnophalloides seoi: a new human intestinal trematode. Trends Parasitol 2003; 19: 109-112. 69. Lee SH, Chai JY, Lee HJ Hong ST, Yu JR, Sohn wn, Kho WG, Choi MH, Lim YJ. High prevalence of Gymnophalloides seoi infection in a village on a southwestern island of the Republic of Korea. Am J Trop Med Hyg 1994; 51: 281-285. 70. Park JH, Guk SM, Shin EH, Kim HJ, Kim JL, Seo M, Park YK, Chai JY. A new endemic focus of Gymnophalloides seoi infection on Aphae Island, Shinangun, Jeollanamdo. Korean J Parasitol 2007; 45: 39-44. 71. Seo M, Chun H, Ahn G, Jang KT, Guk SM, Chai JY. A case of colonic lymphoid tissue invasion by Gymnophalloides seoi in a Korean man. Korean J Parasitol 2006; 44: 87-89. 72. Chai JY, Han ET, Park YK, Guk SM, Lee SH. Acanthoparyphium tyosenense: the discovery of human infection and identification of its source. J Parasitol 2001; 87: 794-800. 73. Chai JY, Hong ST, Lee SH, Lee GC, Min YI. A case of echinostomiasis with ulcerative lesions in the duodenum. Korean J Parasitol 1994; 32: 201-205. 74. Lee SH, Chai JY, Seo BS, Cho SY. Two cases of human infection by adult of Spirometra erinacei. Korean J Parasitol 1984; 22: 66-71. 75. Eom KS, Rim HJ. Morphologic descriptions of Taenia asiatica sp. n. Korean J Parasitol 1993; 31: 1-6. 76. Korea Association of Health Promotion. Prevalence of intestinal parasitic infections in KoreaThe 7th report. Art Motion, Seoul, Korea, 2004. 77. Lee SH, Chai JY, Hong ST, Sohn WM, Choi DI. A case of Diphyllobothrium yonagoense infection. Seoul J Med 1988; 29: 391-395. 78. Eom KS, Kim SH, Rim HJ. Second case of human infection with Mesocestoides lineatus in Korea. Korean J Parasitol 1992; 30: 147-150. 957
Chai JY Peer Reviewer Commentary 958