한국의 수입 기생충 질환 : 현황과 문제점
Imported parasitic diseases in the Republic of Korea: status and issues
Article information
Trans Abstract
Background
International travel is increasing steadily worldwide. People in the Republic of Korea (Korea) tend to have an increased chance of overseas travel. As a result, various exotic diseases have been imported into the country. Among these, parasitic diseases constitute a considerable proportion of the cases. This continuing education column aims to review and introduce the status and issues related to imported parasitic diseases reported from 1965–2024 in Korea.
Current Concepts
Sixteen types of parasitic diseases (n=4,203 patients) were imported from Africa, the Asia-Pacific region, the Middle East, and North and South America. These include protozoan diseases (malaria, babesiosis, cyclosporiasis, and leishmaniasis), nematode diseases (ancylostomiasis, angiostrongyliasis, capillariasis, gnathostomiasis, larva migrans, loiasis, and syngamosis), trematode diseases (heterophyiasis and schistosomiasis), and cestode among other diseases (hydatidosis, pentastomiasis, and myiasis). Most patients were Korean, but a few were emigrants from different countries. Where necessary, indigenous cases of the above diseases, except malaria, are also briefly presented.
Discussion and Conclusion
In Korea, some parasites cannot continue their life cycles because of the absence of proper intermediate hosts or unfavorable environmental conditions. However, others, including parasites causing vivax malaria, babesiosis, cyclosporiasis, ancylostomiasis, capillariasis, gnathostomiasis, larval migrans, heterophyiasis, and hydatidosis, can establish life cycles in Korea. As the number of patients and types of imported parasitic diseases are expected to increase further, caution is needed to avoid infections with parasitic diseases while traveling abroad.
Introduction
In the Republic of Korea (henceforth referred to as Korea), human parasitic infections were highly prevalent until the 1990s. However, owing to the nationwide control activities performed mainly against soil-transmitted helminthiases, including ascariasis, trichuriasis, and hookworm infections, and to the remarkably improved socioeconomic conditions (from the aspects of environment and economy) of the Korean people, the occurrence of indigenous parasitic infections has been decreasing steadily and remarkably; the incidence now became very low or almost negligible [1-5]. However, due to the increasing overseas travel of Koreans and increased emigration of foreign people, the importation of exotic parasitic diseases from foreign countries has been continuously detected, and a part of the cases involved were reported in the literature [3,6-8]. The types of imported parasitic diseases included protozoan diseases (malaria, babesiosis, cyclosporiasis, and leishmaniasis), nematode diseases (ancylostomiasis, angiostrongyliasis, intestinal capillariasis, gnathostomiasis, larva migrans, loiasis, and syngamosis), trematode diseases (heterophyiasis and schistosomiasis), cestode disease (hydatid disease), pentastomid infection (pentastomiasis), and disease caused by fly larvae (myiasis) [3,6-12] (Table 1). The present continuing education column briefly reviews the status and issues of imported parasitic diseases in Korea (1965-2024), since the cases involved began to be recorded officially or non-officially. Two old reports which included 1 visceral leishmaniasis case (1949) and 1 schistosomiasis case (1950- 1953) were also included in the total records.
Protozoan Diseases
1. Malaria
Malaria is a febrile disease caused by the protozoan parasite of the genus Plasmodium [13]. Five species, including P. falciparum, P. vivax, P. malariae, P. ovale, and P. knowlesi, are known to infect humans. In Korea, only P. vivax has been causing indigenous malaria, and P. falciparum, P. malariae, and P. ovale, in addition to P. vivax, have been reported in imported malaria patients. Malaria is contracted by infected mosquitoes of the genus Anopheles [13]. When mosquitoes bite humans, sporozoites are introduced into the bloodstream of the patients, which go to the liver parenchyma where they develop into cryptomerozoites and merozoites during an incubation period. After the incubation, the merozoites burst into the peripheral bloodstream and infect red blood cells (RBCs) [13]. The infected RBC finally ruptures due to the development and division of the parasite. The symptoms and signs include fever, chill, anemia, headache, and hypoxic state of various organs. Hepatosplenomegaly, kidney dysfunction, and brain damage are common complications. The gold standard diagnostic method is the identification of malaria parasites in thick and thin blood smears. Chloroquine is the fundamental antimalarial drug for all species of human-infecting malaria (plus primaquine in P. vivax malaria); however, chloroquine resistance has become a big problem in many parts of the world. Artemisinin derivatives, pyrimethamine plus sulfa, atovaquone, and pyronaridine alone or in combinations are used as alternative antimalarials.
A total of 3,999 imported malaria cases have been reported from 1965 until 2024 in the literature (Table 2) [7,14-23]. The importation of malaria patients into Korea began to be reported by several earlier workers, of which the results were reviewed by Lim [14]. Among the Korean soldiers returning from the Vietnam War from November 1965 to November 1970, a total of 2,148 malaria patients were diagnosed by blood smear examinations [14]. The malaria-positive rate was 8.0% to 11.1%, and most of the cases were infected with P. falciparum, and a few were with P. vivax [14]. Separately from this review, Seo et al. [15] detected 235 blood smear-positive malaria patients evacuated from the Vietnam War between November 1965 and February 1967. The blood smear-positive rate among the malaria-suspected patients was 52.0% (235/452); most cases were due to P. falciparum alone (95.3%) or P. falciparum and P. vivax mixed infections (4.3%), and only 1 case (0.4%) due to P. vivax alone [15] (Table 3).
In 1985, Soh et al. [16] reported 80 imported malaria cases between 1970 and 1985 based on medical records from 26 hospitals in Korea. The number of cases between 1970 and 1975 was 8, between 1976 and 1980 was 30, and between 1981 and 1985 (May) was 42 [16] (Table 2). The area of acquisition was Africa (30 cases), the Middle East (18 cases), and Southeast Asia and Pacific Regions (32 cases) [16]. The species of Plasmodium detected were P. falciparum alone in 32 cases (40.0%), P. vivax alone in 7 cases (8.8%), P. falciparum+P. vivax in 3 cases (3.8%), P. vivax+P. ovale in 1 case (1.3%); the species was not identified in 37 cases (46.3%) [16]. However, these figures seem to have been underestimated compared to the real figure. From 1986 until 1993, several authors reported scattered reports of 44 imported malaria cases [17-21] (Table 2).
In 2010, Ahn [7] reviewed the records of imported malaria patients in Korea, which were reported to the Korea Centers for Disease Control and Prevention (KCDC) between 1994 and 2007 (Table 2). The number of imported malaria patients during this period was 621 (average 41.4 cases/year) [7]. The area of acquisition included Asia (46.9%, 291/621) and Africa (43.2%, 268/621) most frequently, followed by Australia (6.6%, 41/621), America (1.6%, 10/621), and Europe (0.2%, 1/621). The species of Plasmodium involved in 277 blood smear-positive cases were P. falciparum alone in 115 cases (41.5%), P. vivax alone in 102 cases (36.8%), P. malariae alone in 7 cases (2.5%), P. ovale alone in 3 cases (1.1%), P. falciparum+P. vivax in 10 cases (3.6%), and unidentified in 40 cases (14.4%).
Jeon et al. [22] analyzed data on imported malaria cases reported to the Korea Disease Control and Prevention Agency (KDCA, formerly KCDC) between 2009 and 2018 (Table 2). According to this report, the number of imported malaria patients during this period was 601, averaging 60.1/year [22]. Death occurred in 14 cases (2.3%). The age distribution showed that the cases were mostly between 20 to 59 years of age (89.5%), and only a few were younger than 19 years (4.3%) or older than 60 years (6.2%) [22]. The nationality was 460 (76.5%) Koreans, and 141 (23.5%) non-Koreans; visiting countries included those in Africa (414 cases, 68.9%), Asia (179 cases, 29.8%), followed by Oceania (6 cases, 1.0%), and America (2 cases, 0.3%) [22]. The most frequent Plasmodium species was P. falciparum in 335 cases (55.7%), followed by P. vivax in 182 cases (30.3%), P. ovale in 17 cases (2.8%), P. malariae in 12 cases (2.0%), P. falciparum+P. vivax mixed infections in 5 cases (0.8%), P. falciparum+P. ovale mixed in 1 case (0.2%) [22] (Table 3) [7,15,22,24].
Most P. falciparum cases were imported from Equatorial Guinea, Ghana, Uganda, Nigeria, and Sierra Leone, and some other P. falciparum cases were from Cambodia and India [22]. P. vivax cases were mostly originated from Asian countries, including Pakistan, India, the Philippines, and Cambodia [22]. KDCA then reported 74, 29, 20, 38, 74, and 35 imported malaria cases in 2019, 2020, 2021, 2022, 2023, and 2024, respectively [22] (Table 2).
Meanwhile, imported malaria was analyzed in a single center, Samsung Medical Center, Seoul, Korea, from January 1995 to December 2007 [24]. Among the total 49 imported malaria patients, P. falciparum infection alone was the most frequent (71.4%), followed by P. vivax alone (16.3%), P. falciparum+P. vivax (2.0%), P. falciparum+P. ovale (2.0%), and unidentified (8.2%) [24].
Overall, 3,999 imported malaria patients have been reported in the literature and/or to the KDCA. Excluding 1965- 1970, when veterans evacuated from the Vietnam War were analyzed, the annual number of imported malaria patients in Korea averaged 29.9/year from 1971 to 2024. However, there is a trend that the number of imported malaria cases increased according to time; 3.8 cases/year (1971-1980), 36.2/year (1981-2000), 40.8 cases/year (2001-2010), and 57.7 cases/year (2011-2024) (Table 2). The decreased number of cases between 2020 and 2022 is considered due to the remarkably decreasing number of overseas travels due to the COVID-19 global epidemic. From 2023, the number of imported malaria cases increased again (Table 2); thus, preventive measures against mosquito bites and chemoprophylaxis should be strengthened for overseas travelers.
2. Babesiosis
Human babesiosis is an acute febrile illness caused by a tick bite [25-36]. The clinical pictures of this disease as well as the morphology of the parasite on blood smears are so much like those of malaria that it is often misdiagnosed as malaria. It is primarily a disease of domestic and wildlife animals caused by various (>100) species of Babesia. However, humans can be infected with several of them, including B. microti, B. divergens, B. duncani, B. venatorum, B. crassa-like agents, and B. motasi-like agent [36].
In Korea, the 1st case of human babesiosis was reported in 1988 in a 43-year-old United States of America (USA) male citizen who complained of persistent high fever and chill [25] (Table 4). He had lived in Ivory Coast for the past 7 to 8 years and had a history of suffering from malaria-like disease a year before coming to Korea. His blood smear showed characteristic features, including small ring forms, marginal ring forms, ameboid forms, double ring forms (but no tetrad forms), no gametocytes, and no pigment within the RBC and parasites [25]. He was diagnosed with babesiosis and successfully treated with a combined therapy with quinine and clindamycin [25]. The 2nd case was a child (male) aged 8 years [26]. He lived in Ivory Coast for the past 2 years and returned to Korea. His blood picture was similar to the first case, and small ring forms, vacuolated ring forms, and tear-drop-shaped ring forms were observed [26]. He was diagnosed with babesiosis and also successfully treated with quinine and clindamycin [26]. The 3rd [27] and the 4th [28] cases were imported from Ethiopia-Uganda and Angola, respectively. In these cases, the typical ‘tetrad form’ was found in the blood smear. The 5th case was a 56-year-old Korean woman who worked in Tanzania as a missionary [29]. She suffered from a fever, chill, diarrhea, nausea, and muscle pain on 1 day after returning to Korea, and antimalarial medication showed no effects [29]. Her blood smears showed small ring forms, protruded ring forms, and ameboid forms; however, no tetrad forms were identified, and a differential diagnosis with falciparum malaria was needed [29]. However, treatment with quinine and clindamycin was effective in this patient; thus, babesiosis was suggested [29]. The 6th case, a 28-year-old Korean man, was diagnosed with a mixed infection with babesiosis (probably due to B. microti) and P. malariae malaria [30]. The patient had been to Gabon as a missionary for 3 months and on return to Korea developed febrile illness [30].
The 7th imported case was a 62-year-old man who had been in New Jersey, USA for 2 months [31]. He developed a fever and chill, and his peripheral blood showed intracellular parasites seemingly Babesia sp.; polymerase chain reaction (PCR) reaction against P. falciparum was negative [31]. In 2007, a babesiosis case occurred in a 75-year-old Korean woman who had no history of having been abroad; pyriform, double, tear-drop-like ring forms were found in the RBC [32]. Nested PCR with sequencing analysis of 18S rRNA was performed on her peripheral blood which appeared positive for Babesia sp. reported from a sheep in Hebei, China. The parasite was designated as Babesia sp. (KO1), which was later identified as B. motasi [35]; this case was considered the first indigenous case of human babesiosis in Korea [32]. The 8th imported case was a probable mixed infection with severe falciparum malaria and babesiosis in a 48-year-old Korean man who had been to Benin, West Africa [33]. The 9th and 10th imported cases were reported in 50-year-old and 72-year-old women, respectively [34]. These patients visited New Jersey and Boston, USA, respectively, and developed a fever with chill initially thought of as malaria [34]. However, their blood smears revealed the tetrad forms in RBC, typical of babesiosis, and they were found to be co-infected with Lyme disease [34]. In 2019, a second indigenous case was reported in a 70-year-old Korean man with clinical complaints of dizziness and general weakness [35]. His blood picture showed typical forms of parasites in RBCs, including the tetrad form; molecular analysis of his blood sample revealed that the parasite was a species of Babesia close to B. motasi [35]. Two more imported cases, the 11th and 12th, were reported in 2023 [36]. The patients were a 56-year-old man and a 67-year-old woman who visited the USA; their peripheral blood revealed the tetrad forms and other typical morphology of Babesia sp. [36]. In the latter patient, molecular analysis was performed using the sequences of the 18S rRNA; the parasite was identified as B. microti [36].
Summarizing the results, the number of imported human babesiosis cases in Korea since 1988 was 12. Two other babesiosis patients are regarded as indigenous cases (Table 4) [25-36].
3. Cyclosporiasis
Cyclospora cayetanensis is a newly recognized coccidian protozoan associated with diarrheal illness [37]. This parasite can cause acute watery diarrhea accompanied by abdominal pain, nausea, and low-grade fever [10]. As this parasite is common in developing countries, cyclosporiasis is regarded as one of the causes of travelers’ diarrhea [37]. The main source of infection includes water contaminated with oocysts and various kinds of green vegetables and fruits. The diagnosis can be made in fecal examinations to detect oocysts using the modified acid-fast staining or molecular identification of 18S rDNA sequences [37]. Trimethoprim-sulfamethoxazole can be used to treat cyclosporiasis [13].
The 1st imported case was a 14-year-old girl who complained of watery diarrhea and nausea for 5 days after visiting Bali and Jakarta, Indonesia [37]. Her fecal smears revealed large, round, red-stained oocysts on modified acid-fast stained smears under high-power light microscopy or Nomarski differential interference contrast microscopy [37]. Molecular analysis of the 18S rRNA gene revealed 100% identity with C. cayetanensis registered in GenBank [37]. The 2nd to 9th imported cases were reported in a group of Korean people (n=8) who visited Nepal for 9 days and developed gastrointestinal symptoms, including diarrhea [10]. Three cases were molecularly confirmed to be C. cayetanensis infection [10]. Thus far, 9 imported cases of cyclosporiasis have been reported in Korea (Table 5) [10,37].
4. Leishmaniasis (cutaneous and visceral)
Leishmaniasis is a clinically diverse disease, with symptoms ranging from cutaneous lesions to mucocutaneous and visceral manifestations [13]. The parasite species include Leishmania tropica, L. major, L. donovani, and L. aethiopica for the old-world cutaneous leishmaniasis, L. mexicana, L. amazonensis, and L. braziliensis for the new-world cutaneous leishmaniasis, and L. donovani, L. infantum, and L. chagasi for visceral leishmaniasis [38]. However, recently, L. infantum was also reported to be able to cause cutaneous leishmaniasis [38]. The diagnosis is based on recovering the amastigote form in the biopsy specimen of the lesion (macrophages), the promastigote form in cultured fluid, or PCR and sequencing of nuclear genes [38]. The drugs for leishmaniasis include sodium stibogluconate (Pentostam), pentavalent antimony compounds, meglumine antimoniate, amphotericin B, and miltefosine [13].
1) Visceral leishmaniasis
In Korea, 6 visceral leishmaniasis (kala-azar) cases were imported including the first 3 cases in 1949 [11,39-41] (Table 6). The 1st patient was a 24-year-old Korean soldier who had been to China (Qingdao and Beijing), and returning home he suddenly developed severe chill and fever followed by dyspnea, digestive symptoms, periorbital edema, and gingival hemorrhage [11]. Amastigotes (Leishman-Donovan bodies) were confirmed in bone marrow hepatosplenic biopsy specimens [11]. The 2nd patient was a 25-year-old soldier who worked in China, and the diagnosis was confirmed by the recovery of amastigotes in bone marrow and spleen biopsy [11]. The 3rd patient was a 23-year-old Korean male merchant who had been to China, and amastigotes were found in a bone marrow biopsy [11]. Pentavalent and trivalent antimony compounds were medicated to them with considerable effects [11]. The 4th imported patient was diagnosed in a 26-year-old Korean man who had visited Saudi Arabia; after returning home he developed abdominal distention and felt prostration with easy fatigue [39]. The amastigote forms were confirmed in liver biopsy specimens under light and transmission electron microscopic observations; sodium antimony gluconate was prescribed [39]. The 5th imported case was a 38-year-old Korean man who had traveled to Egypt [40]. His bone marrow samples showed amastigotes, and serum samples revealed strong positive reactions against L. donovani antigen [40]. The 6th imported case was a child (girl) aged 9 months [41]. She had been to Argentina with her family and showed signs of diarrhea and upper respiratory tract infections [41]. Her accessory spleen and regional lymph nodes were biopsied and amastigotes of L. donovani were confirmed; amphotericin B was given which was effective for the treatment of this patient [41].
2) Cutaneous leishmaniasis
The first 2 imported cases were reported in 1978 by Yoo et al. [42] who had been to Jordan and Saudi Arabia, respectively (Table 6). The patients complained of chronic ulcerative skin lesions, and amastigote forms were detected in the ulcer juice or ulcer margin smears; the lesions were cured spontaneously or after oral chloroquine and topical povidone-iodine wet dressing treatment, respectively [42]. The 3rd imported case was a 36-year-old man who had been to Saudi Arabia as a road construction laborer [43]. Pinhead-sized erythematous pruritic spots appeared on both inner sides of the forearms; the lesion gradually enlarged and ulcerated in 5 months [43]. Numerous Leishman bodies were observed in the cytoplasm of histiocytes in skin biopsy, and he was treated with oral doses of tetracycline and topical application of antibiotics [43]. The 4th and 5th imported cases were 37-year-old and 45-year-old men with multiple ulcerated skin lesions and edema on the foot, leg, and upper and lower extremities, respectively, who had travel histories to Saudi Arabia [44]. Parasites were found in the biopsy specimens of the ulcer; they were successfully treated with trimethoprim-sulfamethoxazole, metronidazole, and local application of dextran monomer [44]. The 6th to 23rd imported cases were Korean patients who traveled to Saudi Arabia, Jordan, or other Middle East countries having skin problems, including ulceration [45-51]. The 24th and 25th imported cases were a 24-year-old man with erythematous papulonodules on the right arm and left leg and a 27-year-old female presenting with erythematous papulonodules on the face and neck; both patients had been to Israel [52]. Leishman bodies were identified at the lesions and treatment was successful with itraconazole, a new synthetic antileishmanial and antifungal drug [52]. The 26th imported case was a 25-year-old man who complained of a skin ulcer on the right arm and left lower extremity after travel to Sudan; amastigote forms were identified in histiocytes, and multinucleated giant cells from the skin lesions; itraconazole was also effective in this patient [53]. An interesting case of indigenous cutaneous leishmaniasis was described in a 70-year-old Korean male patient who had never been abroad; the lesion was on the face and the parasite was found in local macrophages, and he was treated with cryosurgery for 2 months with satisfactory effects [54]. The 27th imported case was a 23-year-old female who had been to Afghanistan, Pakistan, and India, and erythematous plaque with itching occurred on the left forearm and left ankle when she was in Afghanistan; the lesion progressed to her face [55]. Amastigotes were positive in skin biopsy specimens, and she was treated successfully with oral metronidazole and meglumine antimoniate intralesional injection [55]. The 28th case was diagnosed in a university hospital in Seoul; no details on the patient are available [56]. The 29th imported patient was a 37-year-old man who visited Brazil (Amazon region); this case was a new-world cutaneous leishmaniasis caused by L. mexicana or L. braziliensis [57]. The lesion was on the postauricular area near the neck and on the left upper arm and Leishman-Donovan bodies were found in the histological samples from the lesion; the treatment was successful with intralesional injection of pentavalent antimony compound [58]. The 30th imported case was a 78-year-old woman who visited Spain [38]. The parasite was molecularly analyzed and confirmed to be L. infantum which more frequently causes visceral-type leishmaniasis; the treatment was successful with oral liposomal amphotericin B for 15 days [58].
Summarizing the results, the number of imported leishmaniasis in Korea since 1949 was 36 cases comprising 6 visceral and 30 cutaneous cases. One patient [54] is considered an indigenous case (Table 6) [11,38-57].
Nematode Diseases
1. Ancylostomiasis
Ancylostomiasis caused by Ancylostoma duodenale and necatoriasis caused by Necator americanus are the 2 major human hookworm diseases [13]. These nematode parasites have the capacity of blood sucking in the small intestine, and the patient, particularly children, may undergo severe anemia, malnutrition, and growth retardation [13]. The diagnosis is based on recovering the eggs in fecal specimens, and treatment can be successful using anthelmintics such as albendazole and mebendazole [13].
One male patient, aged 32 years, had traveled to Southeast Asia and, after returning home, developed abdominal pain, diarrhea, and weight loss [58]. His fecal specimens revealed eggs of hookworms. At sigmoidoscopy, 3 adult hookworms (2 females and 1 male worm) were recovered; the worms were morphologically identified as A. duodenale [58].
2. Angiostrongyliasis
Angiostrongyliasis is a disease caused by the parasitic nematode Angiostrongylus cantonensis for which humans are an accidental host; in human infections, cerebral involvement may occur which is manifested histopathologically as eosinophilic meningitis [13]. The natural definitive host is rats in which the parasite inhabits the lungs, and land snails and slugs are intermediate hosts [13]. Angiostrongyliasis is distributed in Southeast Asian countries, including China, Thailand, Taiwan, and the Pacific Islands, but not in Korea [13].
One report is available on the imported angiostrongyliasis cases in Korea. The number of patients diagnosed was 10 out of 15 Korean sailors who disembarked in Samoa; they bought Achatina fulica snails from the natives and ate them raw [59]. They had cerebral symptoms, and the cerebrospinal fluid revealed signs of eosinophilic meningitis; 1 patient died in Samoa [59]. Nine patients were successfully treated with thiabendazole for 3 days [59].
3. Capillariasis (paracapillariasis)
Calodium hepaticum (formerly Capillaria hepatica), Paracapillaria philippinensis (formerly Capillaria philippinensis), and Eucoleus aerophilus (Capillaria aerophila) are the 3 capillarid species causing human capillariasis [60]. Among them, P. philippinensis is the only species reported from imported cases in Korea (Table 7). P. philippinensis is a long, slender nematode parasitizing the small intestine of humans and fish-eating animals, originally reported in the Philippines [13]. Infection with this nematode (=intestinal capillariasis) can cause protein-losing enteropathy, including chronic diarrhea, borborygmus, abdominal discomfort, weight loss, and emaciation [13]. The diagnosis can be made by detecting the eggs in feces, and treatment can be successfully done using albendazole [13].
Four indigenous and 4 imported cases of intestinal capillariasis have been reported in Korea (Table 7) [9,61-66]. The first indigenous case was a 41-year-old man who had never been abroad and complained of chronic diarrhea, lethargy, and weight loss; he enjoyed eating raw meat of game animals and fish [61]. Unfortunately, no fecal examination was performed before the patient underwent an open surgical biopsy of the ileum in which sections of a nematode parasite consistent with P. philippinensis were found [61]. Postsurgical fecal examination revealed P. philippinensis eggs; he was medicated with albendazole and cured [61]. The second indigenous case, a 78-year-old man complaining of intractable diarrhea, was diagnosed by finding the eggs in feces; several juvenile worms were recovered after anthelmintic treatment and purging [62]. The 1st imported case was a 41-year-old man who traveled to Indonesia for 2 years; he had symptoms, including chronic diarrhea sustaining for 8 months, and looked ill and emaciated [62]. He was treated with albendazole for 4 weeks and cured [62]. The 2nd and the 3rd imported cases were 42-year-old and 31-year-old men who had traveled to Saipan (USA) 6 months before or lived in Saipan for 10 years, respectively, and both consumed raw fish; watery diarrhea, and abdominal pain developed, and albendazole therapy was successful [63,64]. Two more indigenous intestinal capillariasis cases were diagnosed; one was a 52-year-old woman with gastric infection and the other was a 37-year-old man complaining of intestinal infection with protein-losing enteropathy; both recalled that they ate raw freshwater fish but had no history of travel abroad [65,66]. The 4th imported case was a 42-year-old man who had lived in the Philippines for 9 years [9]. He used to consume raw fish and experienced a 2-year-long intractable diarrhea; biopsy specimens from the distal ileum revealed sections of a nematode characteristic of P. philippinensis, and albendazole was prescribed [9].
4. Gnathostomiasis
Human gnathostomiasis is caused by diverse species of the genus Gnathostoma around the world, which include G. spinigerum, G. hispidum, G. nipponicum, G. doloresi, G. malaysiae, and G. binucleatum [13,67]. The disease is clinically characterized by migratory creeping eruptions or erythematous indurated plaques; in some instances, the brain, eyes, lungs, and gastrointestinal tract are affected [13,67]. Infection occurs through ingestion of infected freshwater fish (snakehead fish, catfish, loach, and carps), crustaceans (crabs), amphibians (frogs, toads, and salamanders), or reptiles (snakes) [13]. Skin biopsy and serological tests are important diagnostic measures, and albendazole for 14 to 21 days can be used as a medical treatment regimen [13].
A total of 43 imported gnathostomiasis cases have been reported in Korea (Table 8). In addition, 2 indigenous cases were detected; however, in 1 of the these 2 cases, the locality of infection was uncertain (in Korea or China). The 1st imported case was a young Thai woman having clinical signs of meningoencephalitis since she lived in Thailand [68]. In a hospital in Korea, she underwent neurosurgery, and a coiled nematode parasite was removed from the brain; it was morphologically identified as a male worm of G. spinigerum [68]. The 2nd imported case was a 41-year-old man who had been to Myanmar where he consumed raw freshwater fish; he developed erythematous indurated plaques on the trunk accompanied with fever and muscle pain [69]. The diagnosis was based on positive serological reactions against Gnathostoma antigen; the patient was given albendazole for 3 weeks [69]. The 3rd to 40th imported cases occurred as a group infection; the patients were Korean emigrants living in Yangon, Myanmar who complained of migratory swellings and creeping eruptions [70]. They consumed the raw flesh of freshwater fish in a Korean restaurant in Yangon; 38 out of 60 people who consumed the fish developed symptoms of gnathostomiasis [70]. Later, many of these patients returned to Korea and thus were regarded as imported cases. Serum samples of 38 symptomatic and 22 asymptomatic people, and 50 healthy controls, were examined for immunoglobulin (Ig) G antibodies against Gnathostoma antigen, and all 38 patients showed positive reactions [70]. The fish the patients recalled having eaten were examined for Gnathostoma larvae, and 2 G. spinigerum larvae were detected in 2 catfish examined; thus, the diagnosis was given as G. spinigerum infection in these patients [70]. The 41st imported case was a 44-year-old Korean man who had visited Sri Lanka 6 weeks previously and developed migratory, erythematous, and subcutaneous swellings on his face; the lesion was migratory and painful but not pruritic [71]. The serum antibody test using enzyme-linked immunosorbent assay (ELISA) was positive for Gnathostoma antigen (the specific diagnosis was not given), and the treatment with ivermectin was successful [71]. The 42nd imported case was a 74-year-old Korean man who had lived in China; he noted an erythematous skin lesion on his back 1 to 2 years before he returned to Korea [72]. The lesion moved within a limited region and persisted; a skin biopsy revealed sections of a G. hispidum larva showing characteristic internal structures, including the number of intestinal cells of about 30 and each cell having a single nucleus [72]. The 43rd imported case was a 15-year-old boy who had visited Vietnam for 1 week and ate wild boar meat and lobsters; 8 months later, he felt blurred vision in his right eye for 2 weeks [73]. Serum antibodies were strongly positive against G. nipponicum antigen by western blot assay; albendazole was prescribed with successful results [73]. Two indigenous cases of gnathostomiasis were reported [74,75]. One was a 32-year-old Korean woman who had a lesion on the upper lip; she felt a painful migratory swelling near the left nasolabial fold area for a year which moved to the upper lip [74]. The lesion was surgically removed and showed sections of a 3rd-stage larva; the larva had 25 intestinal cells each with multiple nuclei (3 to 6 nuclei) compatible with G. spinigerum [74]. The other case was a 54-year-old Chinese woman who complained of voice change; she consumed the raw flesh of a conger a few weeks before the voice change, but it was uncertain whether she was infected in Korea or in China [75]. A round and red cystic lesion was seen in the anterior part of the right vocal cord which was removed; section slides showed a nematode larva having 27 to 28 intestinal cells with 0 to 4 nuclei in each cell compatible with G. nipponicum or G. hispidum [75].
Summarizing the results, the number of imported gnathostomiasis in Korea since 1988 was 43 cases; the species of Gnathostoma involved were G. spinigerum, G. nipponicum, or G. hispidum. Two patients [74,75] were considered indigenous cases (Table 8) [68-75].
5. Larva migrans (cutaneous)
Larva migrans can be defined as a human parasitic disease caused by the migration of helminth (particularly nematode) larvae in the human body; it can be divided into 2 types depending on the involved organs and tissues, i.e., visceral larva migrans (VLM) and cutaneous larva migrans (CLM) [13,67]. VLM is caused by the larvae of Toxocara canis, T. cati, Toxascaris leonina, Ascaris suum, anisakid nematodes, Gnathostoma spp., and A. cantonensis [13]. Imported cases of gnathostomiasis and angiostrongyliasis have already been described (see former sections). Imported VLM cases due to other nematodes have not yet been reported in Korea. Thus, in the present section, imported CLM cases were described. CLM is most commonly caused by the larvae of Ancylostoma braziliense and A. caninum, and less frequently by the larvae of Uncinaria stenocephala, Bunostomum phlebotomum, Strongyloides stercoralis, and G. spinigerum [13].
A 58-year-old man without any history of overseas travel complained of an S-shaped erythematous plaque on his right chest; the skin biopsy specimen revealed inflammatory reactions with numerous eosinophils and a few [76] (Table 9). He was diagnosed with CLM, although no larvae were confirmed in the lesion; this was considered an indigenous case [76]. The 1st imported case was a 26-year-old woman who had a history of travel to Thailand; she complained of erythematous serpiginous plaques on the dorsum of the left foot [77]. Biopsy revealed typical features of CLM but larvae were not found; flubendazole was prescribed and the symptoms subsided [77]. The 2nd and 3rd imported cases were 20-yearold and 28-year-old women who traveled to Thailand; they had erythematous, serpiginous, and pruritic lesions on the right forearm and back, respectively; larvae were not found in biopsy specimens, and albendazole was prescribed [78]. The 4th imported case was a 34-year-old woman who had been to Indonesia and complained of erythematous pruritic plaque on the skin near the epigastrium with a migration pattern to the left chest and shoulder [79]. In the biopsy specimen, a nematode larva-like section was found but ultimate diagnosis was not possible; albendazole cream was given for 1 week with successful results [79]. The 5th imported case was a 27-year-old woman who had been to New York, USA, and complained of an erythematous serpiginous pruritic lesion on her back [80]. A lesion biopsy revealed sections of a nematode larva seemingly A. braziliense; praziquantel was prescribed [80]. The 6th and 7th imported cases were a 4-year-old body and a 27-year-old woman; the boy had traveled to Brazil for 40 days and the woman had been to Thailand for a short time [81]. The boy developed an eruption on his palm, and the woman had a pruritic, erythematous, serpiginous eruption on her right thigh; the biopsy revealed sections of a nematode larva although a specific diagnosis was not possible; albendazole was prescribed with favorable results [81]. The 8th and 9th imported cases, 30-year-old and 26-year-old men, had a travel history to the Philippines and developed skin lesions characterized by erythematous pruritic serpiginous plaques on the back-buttock area and left thigh, respectively [82,83]. Larvae were not found in biopsy specimens, and albendazole was given for 3 days [82,83]. The 10th imported case and 1 indigenous case were reported in a 30-year-old foreign man (Caucasian) and a 1-year-old boy; they developed linear erythematous serpiginous plaques on the back and hand-trunk-leg, respectively [84]. The man had a travel history to Thailand and Vietnam, and the boy did not have any abroad travel; larvae were not found in biopsy specimens and albendazole was prescribed for both [84]. The 11th imported case was a 15-year-old boy who had been to Cambodia and developed several serpiginous thread-like lesions on the left upper extremity [85]. Serum antibodies were strongly positive against A. caninum antigen by ELISA; albendazole was prescribed with favorable effects [85]. The 12th imported and 2 indigenous cases were reported in a 36-year-old woman, a 74-year-old man, and a 62-year-old man, respectively; they had skin lesions compatible with CLM [86]. The imported case visited Thailand, and the other 2 cases did not have any overseas travel history; a nematode larva was detected in a scratched lesion specimen in the imported case which was specifically diagnosed as A. caninum larva [86]. All cases were treated with oral albendazole for 3 to 5 days and their skin lesions were gradually improved [86]. The 13th to 16th imported cases were a 52-year-old woman, a 26-year-old woman, a 38-year-old man, and a 58-year-old man, respectively; they had a history of travel to the Philippines and developed pruritic serpiginous linear eruptions on their skin [87]. Larvae were not found in biopsy specimens, and albendazole was prescribed for all patients [87]. Another indigenous CLM case was reported in a 52-year-old man who had never been abroad and developed a pruritic skin lesion on the left palm [88]. A lesion with a suspicious nematode larva was found in the skin biopsy specimens but specific determination of the larva was not possible; he was prescribed albendazole for 3 days with successful results [88]. The 17th imported case was a 55-year-old woman who had been to the Philippines; erythematous serpiginous papules and patches were developed on the buttock [89]. Sections of a seemingly nematode larva were detected in a biopsy specimen of the lesion, but no specific diagnosis of the larva was possible; praziquantel was prescribed in this case [89].
Summarizing the results, the number of imported CLM in Korea since 1995 was 17 cases; larvae were morphologically or serologically confirmed as A. caninum in a few cases [85,86]. Five patients [76,84,86,88] were considered indigenous cases (Table 9) [76-89].
6. Loiasis
Loiasis is caused by the filarial nematode Loa loa [13]. Adult worms are called ‘eye worms’ and parasitize the subcutaneous tissues in humans, and they migrate to another place, including the eyes, where the lesions are called Calabar swelling or fugitive swelling [13]. This filaria also infects monkeys and is transmitted by biting flies of the genus Chrysops [13,67]. Retinal involvement is common in humans. The diagnosis is based on fugitive swellings associated with high eosinophilia who visited endemic areas (West and Central Africa) and the identification of microfilariae in the peripheral blood during the daytime [13]. Surgical removal of the worms and medication with suramin and diethylcarbamazine are effective for treatment [13,67].
The 1st imported case was a 33-year-old man who complained of erythematous swellings (Calabar swelling) in the left hand and foot; he visited Nigeria for 2 years; his serum was strongly reactive against filarial antigen in ELISA, but no worm was identified [90] (Table 10). Diethylcarbamazine was prescribed for 1 month. After 4 months, the symptoms subsided, and the serum antibodies returned to a negative level [90]. The 2nd imported case was a 37-year-old man presenting with right arm swelling; he had been to Cameroon [91]. His serum samples tested positive against loiasis, and he was prescribed ivermectin with favorable results [91]. The 3rd imported case was a 29-year-old Mauritanian lady who complained of sudden left eyelid swelling and a sensation of motion on the left eyeball; a thread-like adult nematode (female worm) was extracted from the lesion which was morphologically identified as L. loa [92]. Currently, 3 imported loiasis cases have been reported in Korea (Table 10) [90-92].
7. Syngamosis
Syngamosis is a disease caused by the adult nematodes of the genus Mammomonogamus laryngeus (syn. Syngamus laryngeus), a common parasite of the upper respiratory tract of cattle [67]. This nematode accidentally infects humans in the trachea by ingesting the 3rd-stage larva; however, the entire life cycle of this nematode has not been clarified [67].
One imported case of syngamosis (infection with M. laryngeus) was reported in Korea; the patient was a 61-year-old man living in northeastern China who developed fever, malaise, and purulent sputum [93]. Bronchoscopy revealed many parasites attached to the segmental and subsegmental bronchial wall, and with biopsy forceps and endobronchial suction many copulating nematodes were aspirated [93]. The worms were morphologically identified as M. laryngeus, and albendazole was prescribed for 3 days with good results [93].
Trematode Diseases
1. Heterophyiasis
Heterophyiasis is caused by the infection with minute intestinal trematodes of the genus Heterophyes. The species known to infect humans include H. nocens, H. heterophyes, and H. dispar [13]. H. nocens is distributed in the Far East, including Korea, China, and Japan, and H. heterophyes and H. dispar are found in Egypt, Sudan, Saudi Arabia, and other Middle East countries [13]. These trematode parasites are transmitted by eating brackish water fish (mullets, gobies, and perch) under raw or improperly cooked conditions, and elicit gastrointestinal troubles [13]. The diagnosis is based on recovering the eggs in feces, and treatment can be done with praziquantel [13].
Two documents are available regarding imported heterophyiasis cases in Korea (Table 11) [94,95]. One is an abstract presented at the Korean Society for Parasitology annual meeting in 1985 reporting 5 patients [94], and the other is an official publication reporting 2 additional cases [95]. In the 1st report, 5 imported cases of H. heterophyes and H. dispar infections were presented among Korean laborers returned from Sudan; they were treated with praziquantel, and diarrhea was induced using cathartics [94]. A total of 103 adult specimens (20.1 specimens per person) of H. heterophyes and a total of 1,108 adults (221.6 per person) of H. dispar were collected from the 5 patients; they consumed raw brackish water fish caught from the Red Sea when they lived in Sudan [94]. Two more imported cases were reported subsequently; 38-year-old and 40-year-old men who returned from Saudi Arabia [95]. They consumed the raw flesh of mullets caught from the Red Sea and developed abdominal discomforts after returning home. Following praziquantel treatment and purging, a total of 19 H. heterophyes and 140 H. dispar adult specimens were recovered [95]. Summing up, a total of 7 imported cases of heterophyiasis due to H. heterophyes and H. dispar mixed infections were reported who had been to Sudan or Saudi Arabia; all patients consumed mullets caught from the Red Sea [94,95].
2. Schistosomiasis (urinary and intestinal/cerebral)
Schistosoma haematobium, S. mansoni, S. japonicum, and S. mekongi are the 4 major schistosome flukes infecting humans [13,67]. The adult schistosomes reside within the blood vessels, i.e., vesical and pudendal plexuses (S. haematobium) and superior and inferior mesenteric venules (the former 3 species), and they elicit egg granuloma in the bladder wall and liver, respectively [13]. Freshwater snails of the genera Bulinus, Biomphalaria, Oncomelania, and Neotricula, respectively, for the above 4 species, serve as the intermediate host and shed cercariae; the cercariae are the infective stage to humans [13,67]. In S. haematobium infection, the urinary bladder is affected, and the symptoms include increased urinary frequency, hematuria, dysuria, bladder hypertrophy and inflammation, and in some patients, bladder cancer [13]. In infections with the latter 3 species, eggs produced within the venules are transported to the portal system and liver, where they are filtrated and undergo granuloma formation; the major symptoms include fever, chill, sweating, diarrhea, dysentery, portal hypertension, ascites, varicose vein, and hepatomegaly [13]. The eggs of the latter 3 species can invade the central nervous system (CNS), including the brain, called cerebral schistosomiasis; Jacksonian epilepsy may occur in these patients [13]. The geographical distribution of S. haematobium is mostly Africa and the Middle East, and that of S. mansoni includes Africa, the Middle East, and South America [13]. S. japonicum is distributed mainly in Southeast Asia, including China and the Philippines, and S. mekongi is found in Cambodia, Laos, and Myanmar [13].
1) Urinary schistosomiasis
The 1st imported case was a 29-year-old man who returned from Yemen; he experienced intermittent hematuria accompanied by dysuria and was clinically impressed as a bladder malignancy [96] (Table 12). However, eggs of S. haematobium were found in his urine specimen and diagnosed with urinary schistosomiasis; febendazole was prescribed, and the results were satisfactory [96]. The 2nd to 6th imported cases were 29- to 35-year-old men who returned from Yemen after several years of laboring services; they had experienced contact with water in Yemen and developed urinary symptoms [97]. Two cases revealed S. haematobium eggs in urine examinations, and 2 other cases showed S. haematobium eggs in bladder biopsy specimens; however, eggs were not detected in 1 case [97]. They were treated with praziquantel, and all patients were cured [97]. The 7th imported case was a 33-year-old man who had traveled to Yemen and returned home with clinical symptoms of painless hematuria; he was impressed as cystitis or bladder cancer [98]. However, the biopsy specimen of the bladder and his urine showed eggs of S. haematobium and diagnosed with urinary schistosomiasis; praziquantel was prescribed and 1 month later his urine was negative for S. haematobium eggs [98]. The 8th imported case was a 28-year-old man from Ghana complaining of lower abdominal pain, with no hematuria, nor pyuria, and no S. haematobium eggs in the urine but urinary bladder, ureter, and rectosigmoid bowel wall calcifications were noted [99]. However, serum antibodies were positive against both S. haematobium and S. mansoni by ELISA [99]; a mixed infection with both Schistosoma spp. should be ruled out in this case. The 9th imported case was a 23-year-old Korean woman who had been to Kenya and Malawi presenting with painless gross hematuria; calcified eggs of S. haematobium were detected in biopsy specimens of the urinary bladder [100]. Praziquantel treatment seemed effective, although serum ELISA remained positive even after the treatment [100].
2) Intestinal/cerebral schistosomiasis
The 1st imported case was a 20-year-old man who was a soldier in China or Japan; he had a renal infection with the fatty metamorphosis of the liver and died in the prisoners’ camp, sometime between 1950 and 1953; it is presumed that he suffered from S. japonicum infection [12] (Table 12). The 2nd imported case was a 40-year-old man who had been to Yemen and developed headache, dizziness, and gait disturbance; CNS surgery was performed under the impression of glioma in the cerebellum [101]. However, the eggs of S. mansoni were detected in the feces, and serum ELISA was positive against S. mansoni antigen; in addition, eggshells of S. mansoni were histopathologically detected in the granulomatous lesion in the cerebellar vermis [101]. The patient was prescribed with praziquantel for 7 days and the symptoms gradually disappeared [101]. The 3rd imported case was a 47-year-old man who visited Saudi Arabia; he was positive for a rectal polyp in colonoscopy during a routine health examination [102]. The rectal mucosa showed several granulomas with inflammatory cell infiltrations, and in the center of each granuloma, miracidium-containing S. mansoni eggs were found; praziquantel was prescribed [102]. The 4th imported case was a 40-year-old man who had been in Yemen for 6 months; he complained of headache and dizziness, with nausea, vomiting, and leg pain, and diagnosed with CNS schistosomiasis [103]. Surgical biopsies of the cerebellar vermis and the roof of the 4th ventricle showed granulomatous inflammations due to S. mansoni eggs; eggs were also found in the feces, and serum and cerebrospinal fluid were positive for antibodies against S. mansoni [103]. Praziquantel was prescribed, and follow-up examinations after 7 months showed no evidence of the disease [103]. The 5th imported case was a 39-year-old woman from the Philippines; her clinical problem was a coincidental occurrence of hepatocellular-cholangiocarcinoma with underlying schistosomiasis [104]. Surgical specimens of the liver showed pathological features of hepatocellular carcinoma and cholangiocarcinoma, and between these 2 cancer tissues schistosome eggs, possibly those of S. japonicum, were found [104]. The 6th imported case possibly due to S. japonicum was a Korean (age and sex unknown) living in Guam, USA; no detailed clinical course and treatment are available [8]. The 7th imported case was a 53-year-old man who visited the Middle East for several years; he suffered from intractable neuropathic pain accompanied by hypesthesia, motor weakness, voiding difficulty, and dizziness arising from spinal cord injury due to transverse myelitis caused by schistosomiasis, probably due to S. mansoni [105]. No details of the diagnostic methods of schistosomiasis were described; high cervical spinal cord stimulation was efficacious in reducing the pain in this patient [105].
Summarizing the results, the number of imported schistosomiasis cases in Korea since 1950-1953 was 16 cases in total, which included 9 urinary cases and 7 intestinal/cerebral cases; the parasite species involved were S. haematobium for the former, and S. mansoni or S. japonicum for the latter (Table 12) [8,12,96-105].
Cestode Disease and Others
1. Hydatid disease
Human infections with the larval stage (hydatid cyst) of Echinococcus granulosus or E. multilocularis are called echinococcosis or hydatid disease. E. granulosus causes cystic echinococcosis and E. multilocularis causes alveolar echinococcosis. The natural definitive hosts include the dog and other canine or feline hosts (wolf, jackal, dingo, hyena, puma, jaguar, fox, or cat) [67]. Humans are infected through contact with the eggs in the feces of dogs or other definitive hosts. Intermediate hosts include a wide range of domestic and wildlife animals, including sheep, cattle, pig, horse, camel, goat, monkey, baboon, lemur, elephant, antelope, reindeer, elk, moose, giraffe, gazelle, tapir, zebra, kangaroo, mongoose, and others [67]. In human infections, the liver and lungs are the most frequently affected organs, and kidneys, brain, spinal cord, muscles, spleen, eyes, heart, and bone marrow are the less frequent sites involved [13,67]. Hydatid disease is distributed almost worldwide but is especially prevalent in countries where livestock farming is frequent. The existence of its life cycle was previously acknowledged in Korea, especially on Jeju Island; however, it seems to have almost disappeared now except for a few rare cases. The diagnosis of human echinococcosis is based on detecting cystic lesions in the liver, lungs, or other organs, and treatment includes surgical excision of the cyst and anthelmintic administration [13].
The 1st to 29th imported cases were summarized by Joo [8] and Byun et al. [106] and in 2010. Two of the 31 cases (Table 13) were regarded indigenous cases because the patients had no history of overseas travel [8,106]. Among the 29 imported cases, 22 were Koreans, 6 were Uzbeks, and 1 was Mongolian; males were predominant, 93.1% (27/29), over females, 6.9% (2/29) [106]. Liver cysts were found in 15 patients, lung cysts were in 7 patients, combined liver and lung, and liver and peritoneal cavity cysts were in 2 patients each, and bladder, orbit, and spleen cysts were in 1 patient each [106]. The areas of acquisition were Saudi Arabia (11 patients), Uzbekistan (6 patients), the Middle East (5 patients), Kuwait, Pakistan, Libya, China, Brazil, Mongolia, and Vietnam (1 patient each) [106]. The 30th imported case was a 61-year-old man who traveled to several countries in Europe (France, Germany, Italy, Switzerland, and Spain); he developed a large cystic liver mass detected by ultrasonography [106]. He received a cystectomy; in histopathological samples, numerous protoscolices with suckers and hooklets of E. granulosus were detected [106]. In 2011, 2 seemingly indigenous hydatid disease cases were reported in a 41-year-old woman and a 50-year-old man who had no history of overseas travel; the former patient had a large recurrent liver mass, and the latter had a small nodular lesion in the right lower lung [107,108]. The former case was diagnosed with alveolar echinococcosis due to E. multilocularis based on histopathologic findings of the resected liver mass; this was the first case of indigenous alveolar echinococcosis in Korea [107]. The latter case was diagnosed with E. granulosus infection based on histopathological observations of the resected lung mass [108]. The 31st and 32nd imported cases were 25-year-old and 28-year-old Uzbek men who complained of a cystic mass in the liver [109,110]. The former patient had been in Korea for 3 years and complained of right upper abdominal pain for 20 days [109]. The resected hepatic mass revealed numerous scattered protoscolices of E. granulosus having suckers and calcium corpuscles; after the surgery, the patient recovered well [109]. The latter patient had a right hepatic cyst based on computed tomography (CT) of the liver; the fine needle aspiration cytology was performed and in the aspiration fluid many protoscolices with suckers and hooklets of E. granulosus were confirmed [110]. The 33rd imported patient was also an Uzbek, a 64-year-old woman, who complained of left flank pain due to a renal cyst mimicking a renal malignancy; laparoscopic radical nephrectomy was performed [111]. The resected renal mass consisted of a large unilocular cyst and multiple small cysts; histopathological findings revealed the structures of a hydatid cyst [111]. The 34th imported case was a 58-year-old Chinese man who lived in Korea for 4 years; he developed a cystic mass in the liver incidentally found on abdominal ultrasound [112]. Daughter cysts were found in the large cyst, and complete surgical removal of the cyst was performed and a brood capsule containing numerous degenerating protoscolices of E. granulosus were found; albendazole was prescribed [112]. The 35th imported patient was a 49-year-old man who had been to Uzbekistan a few years ago; he complained of epigastric discomfort on palpation and a CT image showed a round cystic mass in the hepatic lateral ligament and gastrohepatic ligament, with a daughter cyst inside [113]. The cyst ruptured spontaneously into the stomach causing gastric ulcer and peritoneal seeding; the resected mass revealed variable-sized daughter cysts and numerous protoscolices and necrotic debris [113]. The 36th imported patient was a 53-year-old Korean man who had been to China, Russia, and Kazakhstan between 2001 and 2007; he was diagnosed with a liver cyst in abdominal ultrasonography in 2011 but did not take any appropriate medical care [114]. In 2017, he complained of dizziness, dysarthria, and cough for several months, and a 2 cm cerebellar mass and an 11.8 cm liver cyst were found in magnetic resonance imaging and CT, respectively; a lung cyst was also found [114]. The ELISA test was positive for IgG antibodies against echinococcosis antigen; a prolonged treatment with albendazole was effective in this patient [114]. The 37th imported case was a 27-year-old Mongolian female who developed abdominal pain nearby the umbilicus; abdominal ultrasonography revealed a cystic mass with internal septation in the right hepatic lobe, and IgG ELISA for echinococcosis was positive [115]. Surgical excision of the liver mass was done and the resected mass contained daughter echinococcal cysts; albendazole was prescribed [115]. The 38th imported patient was a 42-year-old Kazakhstan female, and she had the clinical symptoms of epigastric discomfort that had persisted for 3 months; abdominal ultrasonography showed a thick-walled cystic lesion with rim calcifications involving segment VIII dome of the liver [116]. The serum ELISA for echinococcal IgG was positive; surgery was done on the lesion, and the resected sample showed evidence of cystic echinococcosis [116]. Albendazole was prescribed for 8 weeks [116]. The 39th imported patient was a 23-year-old Uzbek male complaining of dyspnea and right epigastric pain; abdominal ultrasonography revealed 2 huge communicating cystic lesions in the liver [117]. Laparoscopic right hemi-hepatectomy was performed and the resected samples showed diverse larval stages of E. granulosus; albendazole was prescribed [117].
Summarizing the results, the total number of imported hydatid disease cases in Korea since 1983 was 39, including 38 cystic echinococcosis and 1 alveolar echinococcosis cases (Table 13) [8,106-117]. Out of the 39 patients, Koreans were 25, Uzbeks were 10, Mongolians were 2, Kazakhstan was 1, and Chinese was 1 [106]. The most predilection site was the liver followed by the lungs.
2. Pentastomiasis
Pentastomes (linguatulids or tongue worms) are members of a small group of arthropods or crustacea endoparasitic in vertebrate hosts [67]. The adults have a mouth and 2 pairs of clawed rudimentary appendages; they live in the respiratory passages and body cavities of reptiles, birds, and mammals [67]. Sheep, rabbits, and rodents are intermediate hosts. Humans are accidental hosts and are infected through eating the intermediate host; in humans, larval forms are found in the liver, spleen, lungs, or eyes [67].
One imported case of pentastomiasis was reported in Korea: the patient was a 43-year-old man who had been to Saudi Arabia and Indonesia [118]. He complained of fever, cough, sputum, and dyspnea; an open lung biopsy showed eosinophilic infiltrations with gradual granulomatous changes with sections of an encysted parasite larva [118]. The parasite was diagnosed with a pentastomid larva (the worm species was not identified) [118].
3. Myiasis
Myiasis is an infection with fly larvae that attack animals and rarely humans. In humans, intestinal, urogenital, and lung myiasis can occur; however, cutaneous, ophthalmic, nasal, and aural myiasis are more common [67]. The calliphorine fly species, including Cordylobia anthropophaga (the tumbu fly), are an important agent causing human myiasis, found mostly in tropical Africa [67]. The larvae of C. anthropophaga hatch on polluted dry sand or clothing with animal feces or urine and invade the unbroken skin of humans or animals (usually the feet) producing furuncular swellings at the site of invasion [67].
The 1st imported case was a 37-year-old man who had been to Niger and Cameroon; he had furuncular swellings on the skin of the upper and lower back and posterior thigh [119] (Table 14). A fly larva was expelled when the swollen skin around the lesion was compressed; the larva was morphologically identified as C. anthropophaga [119]. The 2nd imported case was a 27-year-old woman who had a travel history to Cameroon and developed multiple erythematous papules on the right thigh (femoral region) accompanied by pruritus, pain, and tenderness [120]. Fly larvae were extracted by pressing the swollen skin around the lesion and identified as the second stage larvae of C. anthropophaga [120]. The 3rd imported patient was a 33-year-old man who had been to Uganda and developed boil-like lesions with a small central punctum and abscess on his left leg [121]. A 3rd instar larva was extracted from the lesion which was morphologically and molecularly confirmed as C. anthropophaga [121]. The 4th imported case was a 55-year-old man presenting with painful erythematous nodules on the left buttock and upper thigh; he had been to Equatorial Guinea (Central Africa) for a month [122]. Two fly larvae were extracted from the lesion and morphologically identified as C. anthropophaga [122].
Regarding indigenous cases of myiasis, at least 11 reports are available since 1996 until 2024 [123-126]. Chung et al. [123] was the first to describe an internal myiasis case in the gastrointestinal tract due to infestation with the larvae of Lucilia sp. in a 71-year-old male. After 4 more myiasis cases were reported, a nasal myiasis case was diagnosed in a 74-year-old woman caused by the larvae of Lucilia sericata [124]. A case of ophthalmomyiasis was described in an enucleated 50-year-old male patient which was caused by Phormia sp. larvae [125], and a case of oral myiasis due to L. sericata larvae was detected in a 37-year-old man who suffered from muscular dystrophy syndrome [126].
Summarizing the results, the number of imported myiasis cases in Korea since 1990 was 4, and the fly species involved was exclusively C. anthropophaga (Table 14) [119-126]. The number of indigenous myiasis cases was at least 11 cases until 2024.
Issues
The cases of imported parasitic diseases tend to increase yearly in Korea, because of the rapid increase in overseas travel among Koreans. The types of imported parasitic diseases become more diverse because of the increased number of travelers and the remarkably advanced diagnostic techniques. One of the most important diseases is malaria. The incidence tends to increase yearly, and the species of Plasmodium involved have been, in the majority, P. falciparum, which can cause severe and malignant malaria. The government should be aware of this trend and preventive measures with health education should be undertaken for overseas travelers, especially those who visit malaria-endemic areas. Travelers should be notified that avoiding mosquito bites, including various ways of personal protection, and chemoprophylactic administration of antimalarial drugs are the most practical ways of malaria prevention.
In the case of other vector-borne diseases, travelers should be cautious about being bitten by ticks (babesiosis), sandflies (leishmaniasis), or biting flies (loiasis). Cautions should also be paid for drinking water or consumption of vegetables (cyclosporiasis and ancylostomiasis), food intake, including mollusks and fish (angiostrongyliasis, capillariasis, gnathostomiasis, syngamosis, heterophyiasis, and pentastomiasis). Exposure to the soil (CLMs and myiasis) or environmental water (schistosomiasis) should be avoided. Exposure to or contact with the dog or wildlife feces should also be avoided (hydatid disease).
Some imported parasites cannot continue their life cycles in Korea because there are no susceptible intermediate hosts or because of unfavorable environmental conditions. However, some others, for vivax malaria, babesiosis, cyclosporiasis, ancylostomiasis, capillariasis, gnathostomiasis, larva migrans, heterophyiasis, and hydatid disease, could establish their life cycles in Korea. Early diagnosis of the imported case and prompt report to the KDCA is important to prepare preventive and control measures for imported parasitic diseases.
Lastly, clinical centers and health organizations in Korea tend to have low capability for morphological and molecular diagnosis of parasitic diseases. This undoubtedly becomes a drawback to properly assessing the incidence of imported parasitic diseases. Capacity building for parasitic disease diagnosis is urgently needed among clinical centers and health organizations in Korea.
Conclusion
The status and issues of imported parasitic diseases reported from 1965-2024 in Korea have been reviewed. As the number of patients increases yearly and the types of imported parasitic diseases become diverse, health education and prophylactic measures are needed for overseas travelers to avoid getting infected with exotic parasites.
Notes
Conflict of Interest
No potential conflict of interest relevant to this article was reported.
References
Peer Reviewers’ Commentary
이 논문은 1965년부터 2024년까지 한국에서 보고된 수입 기생충 질환의 현황과 문제점을 다루고 있다. 국제 여행과 이민 증가 로 인해 다양한 외래 기생충 질환이 국내로 유입된 4,203건의 사례를 분석하여, 해외 여행자와 이민자들 사이에서 발생할 수 있는 질병의 위험을 사전에 인지하고 예방할 수 있는 기반을 제공한다. 또한, 이 논문은 보건정책 수립과 의학교육에 유용하게 활용될 수 있을 것으로 기대된다.
[정리: 편집위원회]
