jkma Journal of the Korean Medical Association J Korean Med Assoc 1975-8456 2093-5951 Korean Medical Association 10.5124/jkma.2019.62.8.437 jkma-62-437 Continuing Education Column Status of common parasitic diseases in Korea in 2019 HuhSunMD Department of Parasitology and Institute of Medical Education, College of Medicine, Hallym University, Chuncheon, Korea Corresponding author: Sun Huh E-mail: shuh@hallym.ac.kr 82019 1782019 628 437456 05082019 07082019 Copyright © 2019 Korean Medical Association 2019 This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/3.0/) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited. Abstract

This study aimed to determine the status of common parasitic disease in Korea in 2019. Twelve parasitic diseases were selected: toxocariasis, anisakiasis, paragonimiasis, sparganosis, cysticercosis, toxoplasmosis, clonorchiasis, enterobiasis, trichuriasis, trichomoniasis, cryptosporidiosis, and malaria. Their biology, epidemiology, pathogenesis, symptoms and signs, diagnosis, treatment, and prognosis were evaluated. Of the parasitic diseases, toxocariasis was the most prevalent according to serological results. Anisakiasis should be considered when acute gastrointestinal symptoms occur with a recent past history of raw seafood ingestion. Paragonimiasis, sparganosis, and cysticercosis can be diagnosed using an enzyme-linked immunosorbent assay; thus, enzyme-linked immunosorbent assay needs to be performed for suspected cases. Toxoplasmosis and cryptosporidiosis are opportunistic infections. The symptoms and signs are aggravated under immunocompromised conditions. Although the egg positivity rate of Clonorchis sinensis is higher than that of other intestinal parasitic diseases, encountering patients with complaints of symptoms caused by clonorchiasis is rare because the worm burden is low. Trichomoniasis is usually managed by gynecologists; therefore, it should be included in the differential diagnoses of vaginal diseases. The annual number of malaria cases has decreased, although it remains at approximately 500 cases per year. Malaria should be suspected when symptoms such as intermittent fever, headache, and splenomegaly are noted especially when the patients reside near demilitarized zones. Although the prevalence and number of reported cases of parasitic diseases have decreased in Korea, we should consider parasitic diseases in the list of differential diagnoses.

 Parasitic diseases Prevalence Diagnosis Therapeutics Republic of Korea REFERENCES Choi EJ Anisakis worm from the school lunch meal in Incheon, Korea Yonhap News. 2019 Jun 24 [cited 2019 Jul 25]. Available from: https://www.yna.co.kr/view/AKR20190624169200065 Cho SH Jeong BS Lee SE National survey of intestinal parasitic infections in Korea, 8th report (2013) [Internet] Cheongju: Korea Centers for Disease Control and Prevention [cited 2019 Jul 25]. Available from: http://www.cdc.go.kr/CDC/cms/content/mobile/52/24152_view.html Korea Centers for Disease Control and Prevention Infectious disease portal [Internet] Cheongju: Korea Centers for Disease Control and Prevention [cited 2019 Jul 25]. Available from: http://www.cdc.go.kr/npt/biz/npp/nppMain.do Bahk YY Park YK Na BK Sohn WM Hong SJ Chai JY Kim TS Survey on intestinal helminthic infection status of students in two counties, Hadong-gun and Goseong-gun, Korea Korean J Parasitol 201856 335339 Cheun HI Shin HE Ma DW Hong SH Kim TY Lee SE Ju J Park YK Kim TS Cho SH Follow-up study of patients previously diagnosed with lymphatic filariasis in Korea Osong Public Health Res Perspect 20178 421424 Kim C June KJ Cho SH Park KS Lee HS Park JY Prevalence and related factors of Clonorchiasis among five major river-sideresidents in South Korea J Korean Acad Community Health Nurs 201627 346357 Goo YK Shin WS Yang HW Joo SY Song SM Ryu JS Lee WM Kong HH Lee WK Lee SE Lee WJ Chung DI Hong Y Prevalence of Trichomonas vaginalis in women visiting 2 Obstetrics and Gynecology Clinics in Daegu, South Korea Korean J Parasitol 201654 7580 Kim YE Huh HJ Hwang YY Lee NY A survey of intestinal parasite infection during a 10-year period (2003-2012) Ann Clin Microbiol 201316 134139 Park HY Lee SU Huh S Kong Y Magnaval JF A seroepide-miological survey for toxocariasis in apparently healthy residents in Gangwon-do, Korea Korean J Parasitol 200240 113117 Kim HS Jin Y Choi MH Kim JH Lee YH Yoon CH Hwang EH Kang H Ahn SY Kim GJ Hong ST Significance of serum antibody test for toxocariasis in healthy healthcare examinees with eosinophilia in Seoul and Gyeongsangnam-do, Korea J Korean Med Sci 201429 16181625 Kim YH Huh S Chung YB Seroprevalence of yoxocariasis among healthy people with eosinophilia Korean J Parasitol 200846 2932 Huh S Toxocariasis [Internet] New York Medscape 2016 [cited 2019 Jul 27]. Available from: https://emedicine.medscape.com/article/229855-overview Kwon HH Toxocariasis: a rare cause of multiple cerebral infarction Infect Chemother 201547 137141 Kim SH Park CW Kim SK Won S Park WK Kim HR Nam KW Lee GS A case of anisakiasis invading the stomach and the colon at the same time after eating anchovies Clin Endosc 201346 293296 Song H Jung BK Cho J Chang T Huh S Chai JY Molecular identification of Anisakis larvae extracted by gastrointestinal endoscopy from health check-up patients in Korea Korean J Parasitol 201957 207211 Sohn WM Na BK Kim TH Park TJ Anisakiasis: report of 15 gastric cases caused by Anisakis type I larvae and a brief review of Korean anisakiasis cases Korean J Parasitol 201553 465470 Park SE Song B Hwang JY Pulmonary paragonimiasis misdiagnosed with pulmonary tuberculosis Pediatr Infect Vaccine 201724 178182 Lee MK Hong SJ Kim HR Seroprevalence of tissue invading parasitic infections diagnosed by ELISA in Korea J Korean Med Sci 201025 12721276 Seok H Sohn TS Peck KR A Paragonimiasis mimicking gastric submucosal tumor J Korean Med Sci 201934 e45 Kim JY Park MK Lee YJ Huh S Cho KY A case of pulmonary paragonimiasis with chronic abdominal pain and erythematous rash in a 6-year-old girl Pediatr Infect Vaccine 201825 5459 Oh CR Kim MJ Lee KH A case of intra-abdominal paragonimiasis mimicking metastasis of lung cancer diagnosed by endoscopic ultrasound-guided fine needle aspiration Korean J Gastroenterol 201566 4145 Jeon KN Park MJ Bae K Choi HY Choi HC Na JB Choi DS Kim HC Jang IS Kim DC Paragonimiasis: a pictorial essay J Korean Soc Radiol 201369 365371 Oh MY Kim KE Kim MJ Chu A Lee JY Park JH Kim J Hwang KT Breast sparganosis presenting with a painless breast lump: report of two cases Korean J Parasitol 201957 179184 Kim JG Ahn CS Sohn WM Nawa Y Kong Y Human sparganosis in Korea J Korean Med Sci 201833 e273 Jeong YH Lee YS Eun DC Byun CW Intradural extramedullary cysticercosis involving the thoracolumbar spinal canal in a patient with cerebral cysticercosis J Korean Orthop Assoc 201853 369373 Ahn CS Kim JG Huh S Kang I Kong Y Advances in serological diagnosis of Taenia solium neurocysticercosis in Korea Genomics Inform 201917 e7 Chai JY Praziquantel treatment in trematode and cestode infections: an update Infect Chemother 201345 3243 Lee SB Lee TG Toxoplasmic encephalitis in patient with acquired immunodeficiency syndrome Brain Tumor Res Treat 20175 3436 Song KJ Shin JC Shin HJ Nam HW Seroprevalence of toxoplasmosis in Korean pregnant women Korean J Parasitol 200543 6971 Yang Z Cho PY Ahn SK Ahn HJ Kim TS Chong CK Hong SJ Cha SH Nam HW A surge in the seroprevalence of toxoplasmosis among the residents of islands in Gangwha-gun, Incheon, Korea Korean J Parasitol 201250 191197 Lim H Lee SE Jung BK Kim MK Lee MY Nam HW Shin JG Yun CH Cho HI Shin EH Chai JY Serologic survey of toxoplasmosis in Seoul and Jeju-do, and a brief review of its seroprevalence in Korea Korean J Parasitol 201250 287293 Kim YH Lee JH Ahn SK Kim TS Hong SJ Chong CK Ahn HJ Nam HW Seroprevalence of toxoplasmosis with ELISA and rapid diagnostic test among residents in Gyodong-do, Inchon city, Korea: a four-year followup Korean J Parasitol 201755 247254 Lee SE Kim J Kim Y Cho SH Ahn HJ Woo HM Lee WJ Nam HW Prevalence of Toxoplasma gondii Infection in stray and household cats in regions of Seoul, Korea Korean J Parasitol 201048 267270 Park YH Nam HW Clinical features and treatment of ocular toxoplasmosis Korean J Parasitol 201351 393399 Yang YM Choi H Ryu DH Woo CG Han JH Park SM Clonorchis sinensis Infection presenting as acute cholangitis and acute cholecystitis Korean J Pancreas Biliary Tract 201924 7983 Huh S Chemotherapeutic drugs for common parasitic diseases in Korea J Korean Med Assoc 201356 513522 Huh S Parasitic diseases in children J Korean Med Assoc 200447 512520 Kim DH Cho MK Park MK Kang SA Kim BY Park SK Yu HS Environmental factors related to enterobiasis in a southeast region of Korea Korean J Parasitol 201351 139142 Kim DH Son HM Lee SH Park MK Kang SA Park SK Choi JH Park JH Yu HS Detection of head lice among orphanage children in Busan and Ulsan, Korea (2014) Korean J Parasitol 201553 497499 Huh S Pinworm (Enterobiasis) [Internet] New York Medscape 2019 [cited 2019 Jul 27]. Available from: https://emedicine.medscape.com/article/225652-overview Ok KS Kim YS Song JH Lee JH Ryu SH Lee JH Moon JS Whang DH Lee HK Trichuris trichiura infection diagnosed by colonoscopy: case reports and review of literature Korean J Parasitol 200947 275280 Huh S Is it necessary to take anthelmintics every year in Korea? J Korean Med Assoc 201861 198204 Hong ST Albendazole and praziquantel: review and safety monitoring in Korea Infect Chemother 201850 110 Kim YJ Kim SI Kim YR Choi IJ Lee MD Park YJ Nam HW Kang MW Cryptosporidiosis in a small bowel transplant recipient J Korean Soc Transplant 200822 138141 Sim S Won J Kim JW Kim K Park WY Yu JR Simultaneous molecular detection of Cryptosporidium and Cyclospora from raw vegetables in Korea Korean J Parasitol 201755 137142 Seo M Huh S Chai JY Yu JR An epidemiological survey on Cryptosporidium parvum infection of inhabitants in Chorwon-gun, Kangwon-do Korean J Parasitol 200139 201203 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 Jeollanam-Do (Province), Republic of Korea Korean J Parasitol 200644 367372 Cheun HI Cho SH Lim YY Lee BC Kim JY Ju JW Na BK Kimata I Yu JR Kim TS Cryptosporidium parvum in Korea: prevalence in individuals residing in three major river valleys and genetic characteristics of the isolates J Vet Med Sci 201072 167172 Moon S Kwak W Lee S Kim W Oh J Youn SK Epidemiological characteristics of the first water-borne outbreak of cryptosporidiosis in Seoul, Korea J Korean Med Sci 201328 983989 Kim SR Kim JH Gu NY Kim YS Hong YC Ryu JS Prevalence of trichomoniasis by PCR in women attending health screening in Korea Korean J Parasitol 201654 187190 Goo YK Shin WS Yang HW Joo SY Song SM Ryu JS Lee WM Kong HH Lee WK Lee SE Lee WJ Chung DI Hong Y Prevalence of Trichomonas vaginalis in women visiting 2 obstetrics and gynecology clinics in Daegu, South Korea Korean J Parasitol 201654 7580 Seo JH Yang HW Joo SY Song SM Lee YR Ryu JS Yoo ES Lee WK Kong HH Lee SE Lee WJ Goo YK Chung DI Hong Y Prevalence of Trichomonas vaginalis by PCR in men attending a primary care urology clinic in South Korea Korean J Parasitol 201452 551555 Ryu JS Trichomoniasis Hanyang Med Rev 201030 213222 Kim NH Lee KH Jeon YS Cho SG Kim JH Spontaneous splenic rupture in a vivax malaria case treated with transcatheter coil embolization of the splenic artery Korean J Parasitol 201553 215218 Bahk YY Park SH Lee W Jin K Ahn SK Na BK Kim TS Comparative assessment of diagnostic performances of two commercial rapid diagnostic test kits for detection of Plasmodium spp. in Ugandan patients with malaria Korean J Parasitol 201856 447452 Figures and Tables

Anisakis larva in mesentry of Anago anago (photo by Sun Huh, 2019).

(A) Chest posteroanterior radiograph in a patient with toxocariasis. (B) A computed tomography scan of the patient with toxocariasis showing multiple pulmonary nodules with surrounding ground-glass opacities at first visit (Unpublished case).

Endoscopic and endosonographic findings of the stomach. (A) An anisakid larva is penetrating into the mucosa of the lesser curvature of the gastric body. The gastric mucosa around the worm shows marked hyperemia. (B) The worm is captured by endoscopic forceps for removal. (C) On endosonography, gastric wall thickening can be seen. The most thickened layer is the submucosa (third layer of the stomach). Its character is homogenous and relatively hypodense. The 5-layered wall structure is well preserved. mp, muscularis propria; sm, submucosal layer; m, mucosal layer. Reproduced from Kim SH et al. Clin Endosc 2013;46:293-296, according to the Creative Commons license [14].

(A) Initial chest radiograph shows a subpleural nodule (arrow) in the left upper lung field with localized pleural thickening (arrowhead). Note subtle bubble-like air density within the nodule. (B) Follow-up chest radiograph after completion of antituberculosis medication reveals enlargement of the nodule with increased cavitary portion (arrow) accompanied with pulmonic infiltrates (arrowheads) in paragonimiasis. Reproduced from Park SE et al. Pediatr Infect Vaccine 2017;24:178-182, according to the Creative Commons license [17].

Intraoperative findings of sparganosis case. (A) A lesion is located between the left upper outer part of the breast and the axilla. (B) Skin incision is done over the main lesion and a worm is detected between the pectoralis muscles. (C) A close-up picture of the worm. (D) A worm is being extracted. Reproduced from Oh MY et al. Korean J Parasitol 2019;57:179-184, according to the Creative Commons license [23].

(A) Magnetic resonance imaging showing a ring-enhanced mass with mild edema in the right frontal lobe. (B) Many minute, basophilic bradyzoites fill a ruptured protozoal pseudocyst of Toxoplasm gondii with surrounding brain tissue which shows edema and infiltrating inflammatory cells (hematoxylin-eosin stain, ×200). Reproduced from Lee SB et al. Brain Tumor Res Treat 2017;5:34-36, according to the Creative Commons license [28].

Round filling defect (A, arrows) in a dilated common bile duct on endoscopic retrograde cholangiopancreatography revealed an adult worm of Clonorchis sinensis (B, arrow). Stool examination demonstrated the eggs of C. sinensis seen as yellow-brown ovoid operculation (C, ×400). Reproduced from Yang YM et al. Korean J Pancreas Biliary Tract 2019;24:79-83, according to the Creative Commons license [35].

Enterobius vemicularis eggs obtained by cellphans-tape perianal swab from student. Long diameter of eggs is 60 μm (Photo by Sun Huh).

(A) Colonoscopic finding of case 1 showing a whitish worm, Trichuris trichiura, with coiled posterior end embedded in the wall of the cecum. (B) Histologic finding of the cecal mucosa of case 1 which reveals eosinophilic infiltration in the lamina propria (hematoxylin-eosin stain, ×400). Reproduced from Ok KS et al. Korean J Parasitol 2009;47:275-280, according to the Creative Commons license [41].

Oocyst of Cryptosporidium parvum obtained from mouse stool expeirmentallly infected with C. parvum. Modified acid-fast stain (×1,000). Four trophozoites are shown as red color in the oocyst of which diameter is 5 μm (Photo by Sun Huh).

Peripheral blood smear showing a trophozoite and a macrogametocyte of Plasmodium vivax of the patient (Wright-Giemsa stain, ×1,000). Reproduced from Kim NH et al. Korean J Parasitol 2015;53:215-218, according to the Creative Commons license [54].

Classification of malaria cases from 2011 to 2018 in Korea according to origin of the infection and the target population in aboriginal cases. Data from Korea Centers for Disease Control and Prevention. Infectious disease portal [Internet]. Cheongju: Korea Centers for Disease Control and Prevention [3].

Results of 8th national survey of intestinal parasitic infection in 2012, the Republic of Korea

  Number (%)
No. of examined 23,956 100
No. of egg positive 645 2.692
No. of cumulative egg positive 664 2.772
Ascaris lumbricoides    
Unfertilized 6 0.025
Fertilized 1 0.004
Total 6 0.025
Hookworm 0 0
Trichuris trichiura 95 0.397
Trichostrongyloides orientalis 0 0
Clonorchis sinensis 479 1.999
Paragonimus westermani 0 0
Yokogawa metagonimus 60 0.25
Gymnophalloides seoi 6 0.025
Taenia spp. 10 0.042
Diphyllobothrium latum 1 0.004
Enterobius vermiculris 1 0.004
Others 0 0

Data from Cho SH et al. National survey of intestinal parasitic infections in Korea, 8th report (2013) [Internet]. Cheongju: Korea Centers for Disease Control and Prevention [2]. Data are not standardized one but raw positive data.

Parasitic diseases reported through Korea Infectious Diseases Surveillance System from 2011 to 2019

Year Ascariasis Trichuriasis Enterobiasis Clonorchiasis Paragonimiasis Intestinal trematodiasis Malaria
2011 11 287 331 2,019 4 78 826
2012 9 222 289 1,943 4 242 542
2013 10 218 301 2,479 0 309 445
2014 8 207 182 2,372 3 524 638
2015 8 142 128 1,959 1 500 699
2016 3 179 445 1,880 1 592 673
2017 2 130 218 1,618 2 408 515
2018 4 176 225 1,352 2 431 576
2019a) 5 117 193 704 0 287 301

Malaria is the 3rd group surveillance infectious disease so that it is mandatory for all medical health institute to report cases to the Korean Government. Data from Korea Centers for Disease Control and Prevention. Infectious disease portal [Internet]. Cheongju: Korea Centers for Disease Control and Prevention [3].

Data up to July 25 2019.

Imported parasitic diseases reported through Korea Infectious Diseases Surveillance System from 2010 to 2019

Year Total Leishmaniasis Babesiosis African sleeping sickness Schistosomiasis Chagas disease Angiostrongyliasis Gnathostomiasis Filariasis Echinococcosis Toxoplasmosis Dracunculiasis
2010 1 0 0 0 0 0 0 0 0 1 0 0
2011 3 0 0 0 0 0 0 0 0 1 2 0
2012 2 0 0 0 1 0 0 0 0 0 1 0
2013 2 0 0 0 0 0 0 0 0 0 2 0
2014 2 0 0 0 0 0 0 0 0 0 2 0
2015 8 1 1 0 0 0 0 0 0 0 6 0
2016 16 0 0 0 1 0 0 0 0 0 15 0
2017 5 0 0 0 0 0 0 0 0 0 5 0
2018 21 0 0 0 0 0 0 0 1 3 17 0
2019 0 0 0 0 0 0 0 0 0 0 0 0
Total 60 1 1 0 2 0 0 0 1 5 50 0

Data from Korea Centers for Disease Control and Prevention. Infectious disease portal [Internet]. Cheongju: Korea Centers for Disease Control and Prevention [3].