Abstract
Zoonotic parasites are animal parasites that can infect humans. The major zoonotic protozoa in the Republic of Korea are Babesia bovis, Chilomastix mesnili, Cryptosporidium parvum, Endolimax nana, Entamoeba coli, Entamoeba hitolytica, Giardia lamblia, Iodamoeba bütschlii, Pneumocystis carinii, Sarcocystis cruzi, and Toxoplasma gondii. The major zoonotic helminths in Korea include trematodes, cestodes, and nematodes. Trematodes are Clonorchis sinensis, Echinostoma hortense, Echinostoma spp., Fasciola hepatica, Heterophyes nocens, Metagonimus yokogawai, and Paragonimus westermani. Cestodes are Diphyllobothrium latum, Dipylidium caninum, Echinococcus granulosus, Hymenolepis nana, Raillietina tetragona, sparganum (Spirometra spp.), Taenia saginata, T. solium, and T. asiatica. Nematodes are Ancylostoma caninum, Brugia malayi, Capillaria hepatica, Dirofilaria immitis, Gnathostoma dololesi, Gnathostoma spinigerum, Loa loa, Onchocerca gibsoni, Strongyloides stercoralis, Thelazia callipaeda, Trichinella spiralis, Trichostrongylus orientalis, Trichuris trichiura, and Trichuris vulpis. The one arthropod is Sarcoptes scabiei. Many of these parasites have disappeared or were in decline after the 1990's. Since the late 1990's, the important zoonotic protozoa have been C. parvum, E. nana, E. coli, E. hitolytica, G. lamblia, I. buetschlii, P. carinii and T. gondii. The important zoonotic helminths have been C. sinensis, H. nocens, M. yokogawai, P. westermani, D. latum, T. asiatica, sparganum, B. malayi, T. orientalis, T. callipaeda and T. spiralis. However, outbreaks of these parasites are only in a few endemic areas. The outbreaks of Enterobius vermicularis and head lice, human parasites, have recently increased in the kindergartens and primary schools in the Republic of Korea.
-
Key words: zoonotic parasite, animal, human, protozoa, helminth
WHAT ARE ZOONOTIC PARASITES?
Zoonotic parasites are separated into 4 categories, such as direct-zoonotic, meta-zoonotic, cyclo-zoonotic, and sapro-zoonotic parasites. Direct zoonotic parasites infect humans directly from animals, such as, Entamoeba hitolytica, Cryptosporidium parvum, Toxoplasma gondii, Hymenolepis nana, Trichinella spiralis, and Sarcoptes scabiei. Meta-zoonotic parasites can infect humans from invertebrate intermediate hosts, such as, Babesia bovis, Babesia divergens, Plasmodium schwetzi, Clonorchis sinensis, Fasciola hepatica, Paragonimus westermani, Diphyllobothrium latum, Dipylidium caninum, Dirofilaria immitis, Brugia malayi, Onchocerca gibsoni, and Polymorphus boschadis. Cyclo-zoonotic parasites have vertebrate intermediate hosts, such as, Taenia multiceps, Echinococcus granulosus, Taenia saginata, Taenia solium, sparganum (Spirometra spp.), Porrocaecum crassum, Contracaecum osculatum, Capillaria hepatica, and Gnathostoma spinigerum. Sapro-zoonotic parasites mean that parasites can be infected to humans from soil or water, such as, Ancylostoma caninum, Ascaris suum, Capillaria hepatica, Strongyloides stercoralis, Trichuris vulpis, and Hypoderma bovis. Many of carnivorous parasites are zoonotic parasites because dogs and cats have lived with humans for a long period of time. On the other hand, anthroponotic parasites mean that the parasites can be transmitted from humans to animals. Some examples of these are E. histolytica, C. sinensis, D. latum, and Trichuris trichiura.
PREVALENCE OF ZOONOTIC PARASITES IN KOREA
Major zoonotic protozoa
There are about 65,000 species of protozoan parasites in the world. Unicellular organisms, almost all protozoa, live by holozoic nutrition. Protozoa are divided into 5 phyla, Sarcomastigophora, Apicomplexa, Microspora, Myxozoa, and Ciliophora. Sarcomastigophora have flagella or pseudopodia for locomotive organs, reproduce by binary fission, and include
Trichomonas spp.,
Giardia spp., and amoeba. Apicomplexa do not have special locomotive organs and reproduce by multiple fission and gamogony; the examples are coccidia, malaria, and piroplasma. Microspora are spore forming obligatory intracellular parasites and also reproduce by binary or multiple fissions, which include
Encephalitozoon spp. and
Nosema spp. Myxozoa have ameboid germinal elements (sporoplasms) and intracellular parasitism, and includes
Myxosoma spp. Ciliophora have cilia as locomotive organs, reproduce by binary fission and conjugation, and include
Balantidium coli,
Buxtonella sulcata, and lumen ciliates [
1].
The prevalence of amoebae (including
Endolimax nana,
Entamoeba coli,
E. histolytica, and
Iodamoeba bütschlii),
Giardia lamblia, and
Trichomonas hominis in the Republic of Korea (= Korea) declined overall from the 1960s to 1990s, and became 0% nowadays, but those of handicapped people were very high. However, these are not the most severe zoonotic protozoans in Korea. The most important zoonotic protozoa recently are
T. gondii,
C. parvum, and
Pneumocystis carinii [
2-
4] (
Table 1).
Among the residents of Chorwon-gun, Kangwon-do, 9 (1.9%) of the 461 fecal samples were positive for
C. parvum oocysts in 2001 [
5]. The oocyst positive rate was 7.9% (248/3,146) in 1995, but the rate was remarkably different between Seoul and Chollanam-do, 0.5% (4/853) and 10.6% (244/2,293), respectively [
3]. Re-surveying the same village of Hwasun-gun in 1995, 44 (35.2%) of 125 villagers and 14 (93.3%) of 15 cattle examined were positive for
C. parvum oocysts [
3]. The prevalence of
C. parvum infection and its seasonality were studied in a small rural village occupied predominantly by aged people in Hwasun-gun, Chollanam-do, Korea [
6]. Fecal samples were collected monthly from November 1996 to October 1997 and examined for enteric parasites. To detect oocysts of
C. parvum, the modified acid-fast stain was applied. To determine effects of climatic factors, local weather reports were collected. The overall oocyst prevalence during 1 year from November 1996 to October 1997 was 57.0% (77 of 135), and significantly higher prevalence was noted among those aged 50-59 years (80.0%) and 60-69 years (69.0%) than in younger groups [
6].
With respect to toxplasmosis, 19 out of 1,019 (1.9%) cases in general patients, 11 out of 1,030 (1.07%) cases in asthma patients in Kangnam St. Mary's Hospital, and 45 out of 780 (5.77%) cases in Cheju patients showed positive indirect latex agglutination (ILA) test titers [
7]. Several local surveys during the past 20-30 years have shown that the antibody positive rates of patients in general hospitals ranged from 1.9% to 7.2% [
8]. When the sera were screened for antibodies against
Toxoplasma by ILA test, 76 cases (3.8%) were positive. In the paired CSF samples, no positive reactions were observed.
When ELISA was performed using PBS extract of Percoll purified tachyzoites as the antigen, the cut-off absorbance was determined as 0.40 and 0.27 for serum and CSF tests, respectively [
9]. The antibody positive rates by ELISA were 7.0% in serum and 5.6% in CSF [
9]. Thirty-nine cases (4.3%) among 899 sera from pregnant women and 4 out of 218 sera from middle school students had a positive reaction (1.8%) by ELISA [
10]. Two outbreaks of acute toxoplasmosis involving 8 adult patients were linked to eating uncooked pork [
2]. A total of 542 children under 10 years of age, admitted to the Seoul National University Children's Hospital, were examined for antibody titers of
T. gondii using ILA test [
11]. Among them, 7.7% had positive titers higher than 1:32, without significant difference between males (7.3%) and females (8.5%). The sera of local students from 18 high schools (boys 2,110, girls 2,460) and those of adults (474 admitted to Cheju Chungang General Hospital) were collected and checked for IgG antibody titers against
T. gondii [
12]. Serum samples collected from both the students and adults showed seropositive rate of 5.5% and 12.9%, respectively [
12]. Among sera of 1,109 inhabitants of the rural area Okcheon-gun, Korea, 6.9% were seropositive to
T. gondii by ELISA [
13].
A total of 1,008
Apodemus agrarius, a dominant species of field rodents in Korea, were trapped at various locations around the country, and their serum antibody (IgG) levels to
T. gondii were examined by ELISA. The mean absorbance was 0.11, and 15 samples (1.5%) showed positive titers from 0.18 to 0.59. The seropositive samples were analyzed by immunoblot, of which 5 had reactive bands to
T. gondii water soluble antigens of 30, 35, and 43 kDa [
14].
In the survey of
P. carinii infection in Korea, 40.0% of the 145 sera from Korean children were positive with any of the antigenic protein bands of
P. carinii [
15]. Forty-four percent of 2,580 sera from Seoul National University Hospital patients were positive for
P. carinii [
16].
The epidemiological and clinical patterns of HIV infection/AIDS in Korea were investigated retrospectively by analyzing the medical records of 176 HIV-infected persons who visited 2 major referral hospitals of AIDS in Korea from 1985 to April 2000. The
P. carinii pneumonia was 15.9% and among death cases, 25.7% [
19]. The medical records of 173 HIV-infected patients were reviewed to determine the frequency and types of major opportunistic diseases in patients with HIV infection in South Korea. The patients were seen from 1985 to 1998 at a referral hospital for AIDS in South Korea and the positive rate of
P. carinii pneumonia was 10% among 173 HIV-infected patients [
18].
There are 3 kinds of trematodes, such as monogenean, aspidogastrean, and digenean trematodes, with digenean being the only zoonotic trematodes. The characteristics of digenean trematodes are dorsoventrally flattened, unsegmented, and leaf-like worms and have 1 or 2 suckers (oral and ventral suckers), rarely armed with hooks or clamps. All digenean trematodes have 1 or 2 intermediate hosts and first intermediate hosts are molluscs. Almost all zoonotic trematodes have the 2nd intermediate hosts, such as cyprinoid freshwater fish or crustacea [
1].
The prevalence of zoonotic trematodes was reduced below 0.1% in all Korean people after the 1990s, but in some river-side and coastal areas it was as high as 10.0%. There were 30.8% and 14.5% rates of
C. sinensis and
Metagonimus yokogawai infection in 1991 along the river side areas.
C. sinensis,
M. yokogawai, and
P. westermani revealed very low infection rates (0.2, 0.9, and 0.4%, respectively) in 1970 because there were few riverside areas where the 1st and 2nd intermediate hosts lived (
Table 2).
In a survey of heterophyid trematodes,
Heterophyopsis continua,
Pygidiopsis summa, and
Heterophyes nocens have been shown to be infected in domestic cats in Korea [
19]. It was reported the human infections with
Heterophyes heterophyes and
H. dispar have been imported from Saudi Arabia [
20]. A highly endemic locus of human
H. nocens infection was discovered in a small coastal village of Shinan-gun, Chollanam-do, for the first time in Korea. Fecal examinations by cellophane thick smear and formalin-ether sedimentation techniques revealed 42.9% out of 98 inhabitants were positive for heterophyid eggs [
21]. Also, the egg positive rate of heterophyids was very high, 75.0%, whereas that of other parasites was comparatively lower, 0.9-3.7% by parasite species, among 108 inhabitants in a small coastal village of Muan-gun, Chollanam-do [
22].
Chai and Lee [
23] reviewed a total of 19 species of food-borne intestinal trematodes in humans in Korea in their review paper. They include 12 species of the Heterophyidae,
M. yokogawai,
M. takahashii,
M. miyatai,
H. nocens,
H. heterophyes (imported),
H. dispar (imported),
H. continua,
P. summa,
Stellantchasmus falcatus,
Centrocestus armatus,
Stictodora fuscata, and
S. lari; 4 species of the Echinostomatidae,
Echinostoma hortense,
Echinostoma cinetorchis,
Echinochasmus japonicus, and
Acanthoparyphium tyosenense; and 1 species each of the Neodiplostomidae,
Neodiplostomum seoulense, Plagiorchiidae,
Plagiorchis muris, and
Gymnophallidae,
Gymnophalloides seoi [
23].
In a recent survey of metagonimiasis in Korea, the egg positive rate of
M. yokogawai was 29.7%, showing a remarkable difference between males (46.6%) and females (16.3%) from 165 fecal samples around Osib stream, Gangwon-do (province) in an east-northern coastal area in Korea during 1997-1998 [
24]. Similarly, the average infection rate of the inhabitants in several small streams of Gangwon-do was 7.8%; 11.4% in males and 3.2% in females [
25]. Meanwhile, the eggs of
Metagonimus spp. were detected from 15 (9.7%) out of 154 people examined in Umsong-gun, a side of the Namhan River [
26].
During an investigation of intestinal flukes among house rats in Yangyang-gun, Gangwon-do, a total of 6 species of trematodes belonging to 3 families; the Echinostomatidae (
E. hortense,
E. cinetorchis,
E. revolutum and
Echinoparyphium recurvatum), the Neodiplostomidae (
N. seoulense; under the name
Fibricola seoulensis) and the Plagiorchiidae (
P. muris), were recovered from 2 adult rats.
E. revolutum and
E. recurvatum were new trematode faunae of rats in Korea [
27].
In Korea, there are no natural infections of
Schistosoma spp., but an imported case of cerebral schistosomiasis caused by
Schistosoma mansoni was reported in a 40-year-old man who had worked in Yemen [
28].
There are 2 kinds of cetodes, such as
Eucestoda and
Cotyloda. Cestodes are hermaphroditic and endoparasitic worms with an elongated flat body without a body cavity or alimentary canal. Their bodies are comprised of 3 parts, such as, scolex, neck, and strobila.
Eucestoda have 1 intermediate host, but
Cotyloda have 2 or more intermediate hosts [
1].
After zoonotic cestodes were reported by Matsumoto in 1915 in Taegu, Korea, many Japanese and Korean researchers reported cestodes in various places around Korea until 1943. After 1949, the incidences of cestodes reported were from 0% (0/147 and 0/5,251) in Gyeongsangnam-do [
29] and Seoul [
30] to 12.7% (402/3,169) in Cheju. Cheju was an endemic area of cestodes (10.2%, 452/4,449) in Korea at that time. However, the prevalence of cestodes in Cheju was reduced to 3.9% (50/1,280) in 1985. Cheju had the highest incidence of
Taenia spp. infection out of different provinces in Korea. This is in accordance with the traditional habits and environments of Cheju. Many years ago, the pigsty was located below the toilet, so that pigs were raised to eat the stool and infected with the eggs of
Taenia spp. Humans were habituated to eat raw pork products, especially the liver, so they became infected with the metacestodes of
Taenia spp.,
T. solium and
Taenia asiatica. Eom and Rim [
31] reported the incidence of metacestodes (
Cysticercus) to be 1.0% in pigs. Seong et al. [
32] reported a 65.1% incidence of cestodes in Chunchon,
Taenia taeniaeformis metacestodes surveyed in rats.
Zoonotic cestodes were important parasites in Korea until many years ago. But nowadays the prevalence of cestodes in humans is very low because the environment has changed very fast according to the change of the economic situation and education. Some zoonotic cestodes, such as, D. latum, a parasite with freshwater fish as the intermediate host, occasionally infect people who frequently eat raw freshwater fish.
During earlier years, the prevalences of cestodes in Pyeongbuk and Hamkyeong provinces (now located in North Korea) were reported by Japanese researchers until 1945. The prevalences of cestodes in Korea were 0.78% (3,285/419,942) from 1915 to 1998. The incidence of cestodes in Gyeonggi-do were higher (2.8%, 204/7,352) than any other provinces except Cheju. This was because the majority of the data (2.9%, 201/7,000) were those already reported many years ago by Mills in 1927. Patients with other zoonotic cestodes, such as,
E. granulosus,
Hymenolepis diminuta and
Hymenolepis nana, have been reported. About 30 cases of hydatid diseases (due to
E. granulosus) were reported, but all but 1 case were imported from other endemic countries [
33] (
Tables 3-
5).
An imported case of hepatic unilocular hydatid disease was reported by Chai et al. [
33]. A huge hepatic cyst was found by sonography and computerized tomography. Removing the cyst, an exploratory laparotomy was performed under the impression of hydatid disease. The cyst was successfully removed. This was the 16th case of hydatid disease reported in Korea [
33]. The first human case of
Diplogonoporus balaenopterae (Cestoda: Diphyllobothriidae) infection was reported in 1995 [
34]. A part of cestode strobila was isolated from a 41-year-old male. The results of laboratory examinations were within normal limits except for slight eosinophilia (6%) and extraordinarily high serum IgE levels (10,182 IU/ml) [
34]. Chung et al. [
35] reported infection of
D. latum in 3 men who had eaten the brackish water fish,
Liza haematocheila. They were treated with praziquantel and an adult worm was collected from each of them. One had a 310 cm strobila with scolex, another had a 340 cm strobila with scolex, and the other had a 100 cm strobila without scolex [
35]. Infections of pigs with
T. asiatica metacestodes in their livers was surveyed among Korean domestic pigs [
36,
37]. A total of 256 livers (1.01%) of 25,358 pigs in Korea were found infected with 1-96 (mean 2.5 per pig) metacestodes. Most of the metacestodes were either calcified (87.1%) or highly degenerated (12.9%). Living metacestodes were present in only 0.015% (3/25,358) of the examined livers [
36,
37]. Out of 189 stool specimens, 2.6% were positive for
Taenia spp. among inhabitants of 2 islands of Tongyeong-gun, Gyeongsangnam-do, examined by Kato's cellophane thick smear and formalin-ether sedimentation techniques [
38]. Other reports on zoonotic cestode infections have been published [
39-
44].
Seven cases of
D. latum infection were reported by Lee et al. [
41]. A total of 12 worms (1-3 worms/patient) were isolated and identified by the morphology, such as, the worm size (85-423 cm in length), characteristic rosette-shape uterus in their gravid proglottids, egg size (61.0-65.3 × 41.7-46.1 µm), yellowish brown color of eggs, and ovoid to elliptical shape of eggs. This was reported as the 28th case of
D. latum infection in Korea at that time. Min [
42] reported a review paper on cestode infections in Korea, such as, the Pseudophyllidea, i.e.,
D. latum,
Diphyllobothrium yonagoense, sparganum of
Spirometra erinacei, and the Cyclophyllidea, i.e.,
H. diminuta,
H. nana,
Mesocestoides lineatus,
T. saginata,
T. solium, and
E. granulosus. He reported that the plerocercoid larva of
Spirometra spp. (= sparganum) infects humans through 16 kinds of animal hosts, such as, snakes, frogs, and so on.
In 52,552 out- and in-patients, 0.05% (28), 0.03% (18), and 0.004% (2) were reported to be infected with
Taenia spp.,
H. nana, and
D. latum, respectively, in the Seoul Paik Hospital (1984-1992) [
43]. Two rare cases of human infections with the parvum (dwarf) type of
D. latum [syn.
D. parvum (Stephens, 1908)] were discovered by Lee et al. [
43] in Korea. A complete strobila with a scolex, 120 cm in total length, was recovered from a woman treated with praziquantel [
43]. A chain of tapeworm proglottids, 15 cm in length, was also collected from a 22-year-old medical student. They had eaten raw fish. Kim et al. [
44] reported 112 cases of cysticercosis and 1 of sparganosis among 80,947 biopsied materials of humans from 1980 to 1989 in Gwangju and Chollanam-do.
Nematodes are characterized as free-living or parasitic, unsegmented, cylindrical, and elongated round worms with a body cavity and alimentary canal. Almost all nematodes are sex-separated and their life cycles are direct or indirect [
1]. The major intestinal nematodes among Koreans were
Ascaris lumbricoides (roundworm),
Enterobius vermicularis (pinworm), hookworms,
Trichuris trichiura (whipworm),
Trichostrongylus orientalis, and
Strongyloides stercoralis. The incidences of these nematodes were reduced to below 1.0% without special endemic areas after the middle of the 1980s. Almost all of these gastrointestinal nematodes disappeared in Korea after the 1990s, but
Enterobius vermicularis has been recurrent [
45-
51] (
Table 6).
Lymphatic filariasis due to
Brugia malayi infection was endemic in several areas of South Korea; however, at present, it has been completely eradicated from Korea. In the 1960s, to determine the prevalence of filariasis in Korea, a night blood survey was carried out among inhabitants over 1 year in 15 villages throughout Cheju-do [
52]. Blood films from 2,139 people were examined and 183 (8.6%) had microfilariae, with the incidences varying from 0.8 to 19.5% according to geographical sources [
52]. Among 24,816 draftees from all over the country in the army recruitment camp, 155 (0.63%) were found to be infected with the microfilariae of
B. malayi between 1964 and 1967. Cheju-do residents had the highest microfilaria rate (3.5%), followed by Gyongsangbuk-do (1.4%) and Chollanam-do (1.2%) [
53]. The microfilaria positive rate among inhabitants of 5 villages in Yeongpung-gun, Gyeongsangbuk-do became 2.2% on average (male: 1.6%, female: 2.8%) among 370 persons examined in June 1980 [
54].
To discover its recent situation, a small-scale survey was performed on the Heugsan Islands in September 2000 [
55]. A total of 378 people, 151 males and 227 females, living in 8 villages (6 on Daeheugsan-do, 1 on Daejang-do, and 1 on Yeongsan-do) were subjected to a night blood survey for microfilaremia, and physical examination for elephantiasis in the extremities. There were 6 (1.6%) cases positive for microfilariae, and 3 patients with swollen legs were found [
55]. Thereafter, microfilaremia has not been found even in previously endemic areas.
As imported zoonotic nematode infections, 2 loiasis cases due to
Loa loa were reported [
56,
57]. As indigenous infections, there have been several human
Thelazia callipaeda infections [
58-
65]. The reservoir hosts of
T. callipaeda were examined. The eyes of 76 dogs reared at a farm, 78 military dogs (shepherds), 96 cattle, and 105 pigs were investigated for the presence of the eyeworm. Among them, 6
T. callipaeda worms were collected from 2 farm-raised dogs (2.7%) and 188 worms from 26 shepherd dogs (33.5%). No worms were recovered from the cattle or pigs. These results suggested that the dogs, especially the military dogs, serve as an important reservoir host of
T. callipaeda in Korea [
66]. Three cases of human infections with
Trichinella spiralis were first confirmed by detecting encysted larvae in the biopsied muscle in December 1997 [
67]. The patients were all men aged 35 years (1 man) and 39 years (2 men) residing in Gochang-gun, Gyongsangnam-do. They had a common past history of eating raw liver, spleen, blood, and muscle of a badger,
Meles meles melanogenys [
67].
Dirofilaria immitis infections are very popular among dogs in Korea; however, only 1 human
D. immitis infection has been reported [
68].
Sarcoptes scabiei, causing scabies, is the most important zoonotic arthropod in Korea and around the world. The infestation rate of human scabies in Korea peaked in 1981-1982 and was prevalent (about 10%) among outpatients of the dermatological clinic, but decreased dramatically during the past ten years and has been below 1% since 1990. However, canine scabies tends to increase recently.
Prevalence of zoonotic parasites in animals
In an epidemiological study of zoonoses in Korea, Min [
69] reported that out of 13,685 specimens of animals examined from July 1980 through August 1981, a total of 9,808 (71.7%) were positive for helminth parasites. The positive rate was 99.0% in cattle, 86.5% for sheep, 85.4% in pigs, 35.4% in dogs, and 15.1% in cats. Single infection cases showed the highest rate (60.0%), followed by double (27.5%), triple (8.1%), quadruple (2.8%), quintuple (1.5%) and hexad (0.1%) infections in the decreasing order of prevalence. In this study, 18 species of zoonotic helminths were found; 11 nematodes, 6 trematodes, and 1 cestode. In cattle, strongyles,
Neoascaris vitulorum,
Trichuris ovis,
Nematodirus sp.,
Srongyloides papillosus,
Capillaria bovis,
Paramphistomum sp.,
Fasciola hepatica, and
Eurytrema pancreaticum were reported with infection rates of 26.4%, 24.1%, 12.0%, 6.3%, 5.1%, 0.02%, 41.5%, 33.2%, and 29.7%, respectively. In sheep, 3 nematodes and 2 trematodes were reported, including strongyles (33.0%),
S. papillosus (26.9%),
Nematodirus sp. (14.6%),
F. hepatica (31.7%), and
E. pancreaticum (19.6%). In pigs, 5 nematodes and 2 trematodes were reported; strongyles (43.1%),
Ascaris suum (29.0%),
Metastrongylus apri (20.3%),
Trichuris suis (14.0%),
Strongyloides ransomi (12.1%),
Clonorchis sinensis (1.4%), and
Paragonimus westermani (0.9%). Four nematode species, 3 trematodes, and 1 cestode were reported in dogs. Those were
Toxocara canis (14.4%),
Trichuris vulpis (9.5%),
Ancylostoma caninum (8.0%),
Toxascaris leonina (4.0%),
C. sinensis (2.4%),
M. yokogawai (1.3%),
P. westermani (0.8%), and
Spirometra sp. (0.9%). Two nematode species, 3 trematodes, and 1 cestode were reported in cats. Those were
Toxocara cati (7.7%),
Ancylostoma tubaeforme (3.1%),
C. sinensis (1.9%),
P. westermani (1.4%),
M. yokogawai (1.2%), and
Spirometra sp. (0.7%) [
69].
Out of 102 stray dogs examined in Ejungbu City of Gyonggi-do, Korea, 72 were infected with at least more than 1 species of helminthes [
70]. The common helminths found were
Dipylidium caninum (47%),
A. caninum (26%),
T. leonina (16%), and
Toxocara canis (13%). Also,
Taenia pisiformis (9%),
Echinostoma hortense (4%),
E. cinetorchis (2%), and
Spirometra mansoni (2%) were found. One dog was incidentally found to be infected with
Clonorchis sinensis [
70]. In the feces of 245 dogs, 99 (40.4%) contained parasite eggs [73]. The infection rate of
A. caninum was 17.1%, whereas
T. vulpis,
T. canis,
Isospora canis, and
T. leonina, were 16.7%, 8.2%, 3.3%, and 2.0%, respectively [
71].
CONCLUSION
Recently, direct-zoonotic parasites, such as, C. parvum, T. gondii, and P. carinii have been prevalent in endemic areas of the Republic of Korea. Meta-zoonotic parasites, like C. sinensis, H. nocens, M. yokogawai, P. westermanii, and sparganum (Spirometra spp.), are also prevalent among people who consume raw freshwater fish or crabs in endemic areas. Cyclo-zoonotic parasites, such as, T. saginata, T. solium, and T. asiatica, were prevalent in humans who consumed raw cattle or pig meat; however, these parasites are decreasing nowadays in Korea.
References
- 1. Soulsby EJL. Helminths, Arthropods and Protozoa of Domesticated Animals. 1982, 7th ed. London, England. Bailliere Tindall; p 809.
- 2. Choi WY, Nam HW, Kwak NH, Huh W, Kim YR, Kang MW, Cho SY, Dubey JP. Foodborne outbreaks of human toxoplasmosis. J Infect Dis 1997;175:1280-1282.
- 3. Chai JY, Lee SH, Guk SM, Lee SH. An epidemiological survey of Cryptosporidium parvum infection in randomly selected inhabitants of Seoul and Chollanam-do. Korean J Parasitol 1996;34:113-119.
- 4. Hong ST. Serologic response to Pneumocystis carinii of Seoul National University Hospital patients. Korean J Parasitol 1991;29:355-361.
- 5. 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 1991;39:201-203.
- 6. Chai JY, Kim NY, Guk SM, Park YK, Seo M, Han ET, Lee SH. High prevalence and seasonality of cryptosporidiosis in a small rural village occupied predominantly by aged people in the Republic of Korea. Am J Trop Med Hyg 2001;65:518-522.
- 7. Choi WY, Nam HW, Youn JH, Kim WS, Kim WK. Toxoplasma antibody titers by indirect latex agglutination test in patients of Kangnam St. Mary's Hospital and Cheju Medical Center. Korean J Parasitol 1989;27:171-175.
- 8. Choi WY. Diagnosis and epidemiology of toxoplasmosis in Korea. Korean J Parasitol 1990;28:41-44.
- 9. Choi WY, Nam HW, Youn JH, Kim DJ, Kong Y, Kang SY, Cho SY. Detection of antibodies in serum and cerebrospinal fluid to Toxoplasma gondii by indirect latex agglutination test and enzymelinked immunosorbent assay. Korean J Parasitol 1992;30:83-90.
- 10. Ryu JS, Min DY, Ahn MH, Choi HG, Rho SC, Shin YJ, Choi B, Joo HD. Toxoplasma antibody titers by ELISA and indirect latex agglutination test in pregnant women. Korean J Parasitol 1996;34:233-238.
- 11. Kook J, Lee HJ, Kim BI, Yun CK, Guk SM, Seo M, Park YK, Hong ST, Chai JY. Toxoplasma gondii antibody titers in sera of children admitted to the Seoul National University Children's Hospital. Korean J Parasitol 1999;37:27-32.
- 12. Yang HJ, Jin KN, Park YK, Hong SC, Bae JM, Lee SH, Choi HS, Hwang HS, Chung YB, Lee NS, Nam HW. Seroprevalence of toxoplasmosis in the residents of Cheju island, Korea. Korean J Parasitol 2000;38:91-93.
- 13. Lee YH, Noh HJ, Hwang OS, Lee SK, Shin DW. Seroepidemiological study of Toxoplasma gondii infection in the rural area Okcheon-gun, Korea. Korean J Parasitol 2000;38:251-256.
- 14. Jeon SH, Yong TS. Serological observation of Toxoplasma gondii prevalence in Apodemus agrarius, a dominant species of field rodents in Korea. Yonsei Med J 2000;41:491-496.
- 15. Moon HN, Hong ST, Lee SH. Serologic response of normal Korean children to Pneumocystis carinii as observed by immunoblot. Korean J Parasitol 1995;33:101-106.
- 16. Hong ST, Lee SH, Kim SI. A human case of Thelazia callipaeda infection with reference to its internal structures. Korean J Parasitol 1991;26:137-140.
- 17. Kim JM, Cho GJ, Hong SK, Chang KH, Chung JS, Choi YH, Song YG, Huh A, Yeom JS, Lee KS, Choi JY. Epidemiology and clinical features of HIV infection/AIDS in Korea. Yonsei Med J 2003;44:363-370.
- 18. Oh MD, Park SW, Kim HB, Kim US, Kim NJ, Choi HJ, Shin DH, Lee JS, Choe K. Spectrum of opportunistic infections and malignancies in patients with human immunodeficiency virus infection in South Korea. Clin Infect Dis 1999;29:1524-1528.
- 19. Eom KS, Son SY, Lee JS, Rim HJ. Heterophyid trematodes (Heterophyopsis continua, Pygidiopsis summa and Heterophyes heterophyes nocens) from domestic cats in Korea. Korean J Parasitol 1985;23:197-202.
- 20. Chai JY, Seo BS, Lee SH, Hong SJ, Sohn WM. Human infections by Heterophyes heterophyes and H. dispar imported from Saudi Arabia. Korean J Parasitol 1986;24:82-86.
- 21. Chai JY, Nam HK, Kook J, Lee SH. The first discovery of an endemic focus of Heterophyes nocens (Heterophyidae) infection in Korea. Korean J Parasitol 1994;32:157-161.
- 22. Chai JY, Kim IM, Seo M, Guk SM, Kim JL, Sohn WM, Lee SH. A new endemic focus of Heterophyes nocens, Pygidiopsis summa, and other intestinal flukes in a coastal area of Muan-gun, Chollanam-do. Korean J Parasitol 1997;35:233-238.
- 23. Chai JY, Lee SH. Food-borne intestinal trematode infections in the Republic of Korea. Parasitol Int 2002;51:129-154.
- 24. Chai JY, Han ET, Park YK, Guk SM, Kim JL, Lee SH. High endemicity of Metagonimus yokogawai infection among residents of Samchok-shi, Kangwon-do. Korean J Parasitol 2000;38:33-36.
- 25. Ahn YK. Intestinal flukes of genus Metagonimus and their second intermediate hosts in Kangwon-do. Korean J Parasitol 1993;31:331-340.
- 26. Chai JY, Huh S, Yu JR, Kook J, Jung KC, Park EC, Sohn WM, Hong ST, Lee SH. An epidemiological study of metagonimiasis along the upper reaches of the Namhan River. Korean J Parasitol 1993;31:99-108.
- 27. Lee SH, Sohn WM, Chai JY. Echinostoma revolutum and Echinoparyphium recurvatum recovered from house rats in Yangyang-gun, Kangwon-do. Korean J Parasitol 1990;28:235-240.
- 28. Lee YK, Choi TY, Jin SY, Lee DW. Imported CNS schistosomiasis - a case report. J Korean Med Sci 1995;10:57-61.
- 29. Seo BS, Rim HJ, Cho SY, Ahn JH, Kwak JW, Lee JW, Kang SC. The prevalence of intestinal helminths in inhabitants of Cheju Do. Korean J Parasitol 1972;10:100-108.
- 30. Min DY, Ahn MH, Kim KM, Kim CW. Intestinal parasite survey in Seoul by stool examination at Hanyang University Hospital. Korean J Parasitol 1986;24:209-212.
- 31. Eom KS, Rim HJ, Geerts S. Experimental infection of pigs and cattle with eggs of Asian Taenia saginata with special reference to the extrahepatic viscerotropism. Korean J Parasitol 1992;30:269-275.
- 32. Seong JK, Huh S, Lee JS, Oh YS. Helminths in Rattus norvegicus captured in Chunchon, Korea. Korean J Parasitol 1995;33:235-237.
- 33. Chai JY, Seo M, Suh KS, Lee SH. An imported case of hepatic unilocular hydatid disease. Korean J Parasitol 1995;33:125-130.
- 34. Chung DI, Kong HH, Moon CH, Choi DW, Kim TH, Lee DW, Park JJ. The first human case of Diplogonoporus balaenopterae (Cestoda: Diphyllobothriidae) infection in Korea. Korean J Parasitol 1995;33:225-230.
- 35. Chung PR, Sohn WM, Chung YH, Bae SH, Nam MS. The infection of Diphyllobothrium latum to 3 men eaten Liza haematocheila. Korean J Parasitol 1997;35:283-289.
- 36. Eom KS, Rim HJ. Experimental human infection with Asian Taenia saginata metacestodes obtained from naturally infected with Korean domestic pigs. Korean J Parasitol 1992;30:21-24.
- 37. Eom KS, Rim HJ. Natural infections of Asian Taenia saginata metacestodes in the livers of Korean domestic pigs. Korean J Parasitol 1992;30:15-20.
- 38. Hong SJ, Woo HC, Han JH, Seong YK. Intestinal parasite infections among inhabitants in two islands of Tongyeong-gun, Kyeongsangnam-do. Korean J Parasitol 1990;28:63-67.
- 39. Kim CH, Na YE, Kim NM, Shin DW, Chang DY. Intestinal parasite and Clonorchis sinensis infection among the inhabitants in the upper stream of Taechong Dam, Kumgang (River). Korean J Parasitol 1994;32:207-214.
- 40. Kong Y, Cho SY, Kang SY. Sparganum infections in normal adult population and epileptic patients in Korea: A seroepidemiologic observation. Korean J Parasitol 1994;32:85-92.
- 41. Lee SH, Chai JY, Hong ST, Sohn WM, Huh S, Cheong EH, Kang SB. Seven cases of Diphyllobothrium latum infection. Korean J Parasitol 1989;27:213-216.
- 42. Min DY. Cestode infections in Korea. Korean J Parasitol 1990;28:123-144.
- 43. Lee SH, Chai JY, Seo M, Kook J, Huh S, Ryang YS, Ahn YK. Two rare cases of Diphyllobothrium latum parvum type infection in Korea. Korean J Parasitol 1994;32:117-120.
- 44. Kim J, Chung WS, Cho KH. Status of parasitic infection diagnosed by surgical biopsy in Kwangju and Chollanam-do. Korean J Parasitol 1994;32:93-100.
- 45. Choi DW, Park SD, Kim JW, Ahn DH, Kim YM. Intestinal parasite survey of Kyungpook National University Hospital patients. Korean J Parasitol 1971;9:47-53.
- 46. Goo GS, Min DY, Ahn MH, Kim KM, Leem MH, Yoon HS. Status of intestinal parasitic infections in a remote island, Yondo, Jeonranam-do: province. Korean J Parasitol 1988;26:275-284.
- 47. Hong ST. A survey on intestinal parasites of soldiers in Korea. Korean J Parasitol 1986;24:213-215.
- 48. Huh S, Huh SC. Intestinal parasitic infections of Korean Army soldiers in Whachon-gun, Korea. Korean J Parasitol 1993;31:293-294.
- 49. Kim CH, Park CH, Kim HJ, Chun HB, Min HK, Koh TY, Soh CT. Prevalence of intestinal parasites In Korea. Korean J Parasitol 1971;9:25-38.
- 50. Lee J, Park GM, Lee DH, Park SJ, Yong TS. Intestinal parasite infections at an institution for the handicapped in Korea. Korean J Parasitol 2000;38:179-181.
- 51. Lee SK, Shin BM, Chung NS, Chai JY, Lee SH. Second report on intestinal parasites among the patients of Seoul Paik Hospital (1984-1992). Korean J Parasitol 1994;32:27-33.
- 52. Seo BS, Rim HJ, Seong SH, Park YH, Kim BC, Lim TB. The epidemiological studies on the filariasis in Korea. I. Filariasis in Cheju-Do (Quelpart Island). Korean J Parasitol 1965;3:139-145.
- 53. Seo BS, Rim HJ, Lim YC, Kang IK, Park YO. The epidemiological studies on the filariasis In Korea. II. Distribution and prevalence of malayian filariasis in southern Korea. Korean J Parasitol 1968;6:132-141.
- 54. Kim DC, Lee OY, Jeong EB, Jeong MG. Natural transition of endemicity of malayan flariasis in inland Korea: pattern of change in microfilaria rate among inhabitants of Yongpung (former Yongju) area during the period of the last seven years. Korean J Parasitol 1980;18:171-178.
- 55. Chai JY, Lee SH, Choi SY, Lee JS, Yong TS, Park KJ, Yang KA, Lee KH, Park MJ, Park HR, Kim MJ, Rim HJ. A survey of Brugia malayi infection on the Heugsan Islands, Korea. Korean J Parasitol 2003;41:69-73.
- 56. Chun YS, Chun SI, Im KI, Moon TK, Lee MG. A case of loiasis. Yonsei Med J 1998;39:184-188.
- 57. Min DY, Soh CT, Yoon JW. A case of calabar swelling suspected as loiasis. Korean J Parasitol 1987;25:185-187.
- 58. Choi WY, Lee WK, Lee OR, Shin HH, Shin NY. A case of human thelaziasis in Seoul. Korean J Parasitol 1977;15:127-132.
- 59. Hong ST, Lee SH, Shim YB, Choi JS, Choe JK. A human case of thelaziasis in Korea. Korean J Parasitol 1981;19:76-80.
- 60. Hong ST, Park YK, Lee SK, Yoo JH, Kim AS, Chung YH, Hong SJ. Two human cases of Thelazia callipaeda infection in Korea. Korean J Parasitol 1995;33:139-144.
- 61. Huh S, Lee SU, Huh SC. A follow-up examination of intestinal parasitic infections of the army soldiers in Whachon-gun, Korea. Korean J Parasitol 1994;32:61-63.
- 62. Choi WY, Youn JH, Nam HW, Kim WS, Kim WK, Park SY, Oh YW. Scanning electron microscopic observations of Thelazia callipaeda from human. Korean J Parasitol 1989;27:217-223.
- 63. Im KI, Ahn MH, Kim JJ, Kim HB. A case of human thelaziasis in Korea. Korean J Parasitol 1982;20:60-63.
- 64. Min HK, Chun KS. A case of human thelaziasis occurred in both eyes. Korean J Parasitol 1988;26:133-135.
- 65. Ryu JS, Im KI, Byun YJ, Kim SC. A case of human thelaziasis in Korea. Korean J Parasitol 1987;25:83-84.
- 66. Seo M, Yu JR, Park HY, Huh S, Kim SK, Hong ST. Enzooticity of the dogs, the reservoir host of Thelazia callipaeda, in Korea. Korean J Parasitol 2002;40:101-103.
- 67. 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.
- 68. Lee KJ, Park GM, Yong TS, Im KI, Jung SH, Jeong NY, Lee WY, Yong SJ, Shin KC. The first Korean case of human pulmonary dirofilariasis. Yonsei Med J 2000;41:285-288.
- 69. Min HK. An epidemiological study on zoonoses in Korea. Korean J Parasitol 1981;19:60-75.
- 70. Cho SY, Kang SY, Ryang YS. Helminthes infections in the small intestine of stray dogs in Ejungbu City, Kyunggi Do, Korea. Korean J Parasitol 1981;19:55-59.
- 71. Youn HJ, Hong KO, Lee BC, Oh HG. Prevalence of intestinal parasites in dogs and its control in Korea. Korean J Vet Publ Hlth 1995;19:257-261.
Table 1.The reported prevalence (%) of gastrointestinal zoonotic protozoa in Korea
Table 1.
|
Years (No. of tested sample) |
1962-1968 (2,414) |
1969 Jul.-1970 Dec. (2,250) |
1981 (4,116) |
1981 May-Jul. (2,735) |
1983 Aug.-1985 Dec. (2,643) |
1985 Jun.-1986 Jul. (5,251) |
1988 Feb.-May (1,011) |
1984-1992 (52,552) |
1991 Jan.-Oct. (743) |
1997 Aug. (112) |
|
Species of zoonotic protozoa |
|
Chilomastix mesnili
|
|
0.5 |
|
|
|
|
|
|
|
|
|
Dientamoeba fragilis
|
|
0.1 |
|
|
|
|
|
|
|
|
|
Endolimax nana
|
|
10.0 |
|
2.71 |
1.7 |
|
0.8 |
0.8 |
0.3 |
21.4 |
|
Entamoeba coli
|
15.3 |
20.5 |
4.9 |
5.52 |
1.4 |
|
3.3 |
1.1 |
0.7 |
25.0 |
|
Entamoeba histolytica
|
11.9 |
6.4 |
1.4 |
0.69 |
0.6 |
0.06 |
0.2 |
0.3 |
0.3 |
1.8 |
|
Enteromonas hominis
|
|
0.7 |
|
|
|
|
|
|
|
|
|
Giardia lamblia
|
|
5.1 |
1.9 |
2.23 |
0.9 |
0.13 |
1.5 |
0.3 |
0.3 |
0.9 |
|
Iodamoeba bütschlii
|
|
0.6 |
0.4 |
0.18 |
0.04 |
|
|
|
0.1 |
1.8 |
|
Trichomonas hominis
|
|
1.1 |
|
|
|
|
|
0.004 |
|
|
|
Province (area, subjects) |
Gyungpook |
Korea |
Chollanam |
Gyeonggi & Chollabuk |
Soldiers |
Seoul |
Chollanam |
Seoul |
Gumgang (Chungnam) |
Handicapped |
Table 2.The reported prevalence (%) of zoonotic trematodes in Korea
Table 2.
|
Years (No. of tested samples) |
1962-1968 (2,414) |
1969 Jul.-1970 Dec. (2,250) |
1970 Jul. (3,169) |
1983 Aug.-1985 Dec. (2,643) |
1985 Jun.-1986 Jul. (5,251) |
1984-1992 (52,552) |
1991 Jan.-Oct. (743) |
1992 (113) |
1993 (233) |
|
Species of trematodes |
|
Clonorchis sinensis
|
29.8 |
12.1 |
0.2 |
7.6 |
1.43 |
3.2 |
30.8 |
6.2 |
0.4 |
|
Echinostoma hortense
|
|
|
|
0.04 |
|
|
|
|
0.4 |
|
Echinostoma spp. |
|
|
|
|
|
0.03 |
|
|
|
|
Fasciolidae
|
|
0.04 |
|
|
|
|
0.7 |
|
|
|
Neodiplostomum seoulense
|
|
|
|
0.9 |
|
|
|
|
0.4 |
|
Metagonimus yokogawai
|
|
0.04 |
0.9 |
1.1 |
0.13 |
1.2 |
14.5 |
|
0.9 |
|
Metagonimus sp. |
|
|
|
|
|
|
|
2.7 |
|
|
Paragonimus westermani
|
|
1/2,250 |
0.4 |
0.08 |
|
0.02 |
|
|
|
|
Province (area, subjects) |
Gyungpook |
Korea |
Cheju |
Soldiers |
Seoul |
Seoul |
Gumgang |
Soldiers |
Soldiers |
Table 3.Prevalence of Taenia spp. infection through human coprological examinations in Korea from 1915 to 1998
Table 3.
|
Province, area, or subjects |
No. examined |
No. positive |
% |
|
Korea |
186,197 |
1,694 |
0.9 |
|
Soldier |
26,368 |
124 |
0.5 |
|
Seoul |
81,233 |
148 |
0.2 |
|
Kyeonggi |
7,352 |
204 |
2.8 |
|
Kangwon |
2,975 |
54 |
1.8 |
|
Chungbuk |
608 |
5 |
0.8 |
|
Taegu |
4,905 |
56 |
1.1 |
|
Kyeongbuk |
6,354 |
37 |
0.6 |
|
Kyeongnam |
7,389 |
72 |
1.0 |
|
Chonbuk |
5,818 |
177 |
3.0 |
|
Chonnam |
84,996 |
245 |
0.3 |
|
Cheju |
4,449 |
452 |
10.2 |
|
Pyeongbuk |
698 |
7 |
1.0 |
|
Hamkyeong |
600 |
10 |
1.7 |
|
Total |
419,942 |
3,285 |
0.8 |
Table 4.Fluctuation in the prevalence of Taenia spp. infection in humans in Korea
Table 4.
|
Periods |
No.
|
Prevalence (%) |
|
Examined |
Positives |
|
1910-1919 |
674 |
42 |
6.2 |
|
1920-1929 |
15,492 |
299 |
1.9 |
|
1930-1939 |
1,458 |
7 |
0.5 |
|
1940-1949 |
660 |
6 |
0.9 |
|
1950-1959 |
919 |
16 |
1.7 |
|
1960-1969 |
63,669 |
533 |
0.8 |
|
1970-1979 |
82,281 |
1,287 |
1.6 |
|
1980-1989 |
121,101 |
950 |
0.8 |
|
1990-Now |
133,688 |
145 |
0.1 |
|
Total |
419,942 |
3,285 |
0.8 |
|
|
1992a
|
25,552 |
256 |
1.0 |
|
1995b
|
43 |
28 |
65.1 |
Table 5.The reported prevalence (%) of zoonotic cestodes in Korea
Table 5.
|
Years (No. of tested samples) |
1969 Jul.-1970 Dec.(2,250) |
1970 Jul. (3,169) |
1983 Aug.-1985 Dec.(2,643) |
1985 Jun.-1986 Jul. (5,251) |
1988 Feb.-May (1,011) |
1984-1992 (52,552) |
Oct. (743) |
|
Species of cestodes |
|
Diphyllobothrium latum
|
|
|
|
0.02 |
|
0.004 |
|
|
Hymenolepis diminuta
|
|
|
0.04 |
|
|
|
|
|
Hymenolepis nana
|
0.7 |
1.4 |
0.2 |
0.02 |
0.4 |
0.03 |
|
|
Province (area/subjects) |
Korea |
Cheju |
Soldiers |
Seoul |
Chollanam |
Seoul |
Gumgang |
Table 6.The reported prevalence (%) of zoonotic nematodes in Korea
Table 6.
|
Years (No. of tested samples) |
1962-1968 (2,414) |
1969 Jul.7-1970 Dec. (2,250) |
1970 Jul. (3,169) |
1983 Aug.-1985 Dec. (2,643) |
1985 Jun.-1986 Jul. (5,251) |
1988 Feb.-May (1,011) |
1984-1992 (52,552) |
1991 Jan.-Oct. (743) |
1997 Aug. (112) |
|
Species of nematodes |
|
Ascaris lumbricoides
|
40.9 |
46.0 |
44.3 |
2.0 |
0.02 |
17.4 |
0.2 |
0.4 |
|
|
Enterobius vermicularis
|
|
1.6 |
|
|
|
|
0.02 |
0.1 |
20.6 |
|
Hookworms |
22.4 |
6.8 |
1.5 |
0.08 |
0.06 |
0.2 |
0.03 |
0.1 |
|
|
Trichuris trichiura
|
83.6 |
46.8 |
65.6 |
13.0 |
0.7 |
27.5 |
2.0 |
1.6 |
0.28 |
|
Trichostrongylus orientalis
|
61.6 |
7.0 |
0.8 |
0.08 |
|
0.2 |
0.1 |
|
|
|
Strongyloides stercoralis (larvae) |
|
|
|
|
|
|
0.01 |
|
|
|
Province (area/subjects) |
Gyungpook |
Korea |
Cheju |
Soldiers |
Seoul |
Chollanam |
Seoul |
Gumgang |
Handicapped, Gangwon |
