• View in gallery

    Map showing Heterophyes nocens and Pygidiopsis summa infections in the surveyed areas of Korea. A total of 4,179 fecal specimens collected from 45 coastal islands were examined. Egg-positive cases of H. nocens were found on 43 of 45 islands and those of P. summa on 12 of 45 islands. •* = positive for both H. nocens and P. summa eggs; • = positive for only H. nocens eggs; ○ = negative for both H. nocens and P. summa eggs. DMZ = demilitarized zone with North Korea.

  • View in gallery

    Age and sex prevalence of Heterophyes nocens and Pygidiopsis summa infections among residents on the surveyed islands. Adults showed a higher prevalence (P < 0.05) than children for both species of flukes. Women showed a slightly higher (P > 0.05) egg-positive rates (257/2,260 = 11.4% for H. nocens and 29/2,260 = 1.3% for P. summa) than men (202/1,918 = 10.5% for H. nocens and 20/1,918 = 1.0% for P. summa).

  • View in gallery

    Photomicrographs of fluke specimens recovered from an infected person residing on Imchado (area code 16; Table 1 and Figure 1). A, Wet specimens of Heterophyes nocens (Hn), Pygidiopsis summa (Ps) and Gymnophalloides seoi (Gs) expelled in diarrheic stool (CKE in Table 2) after washing with water (bar = 0.5 mm). B, Acetocarmine-stained specimen of H. nocens, showing its unique organs and structures (bar = 0.2 mm). C, Aacetocarmine-stained specimen of P. summa, demonstrating its peculiar shape (bar = 0.2 mm).

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PREVALENCE OF HETEROPHYES NOCENS AND PYGYDIOPSIS SUMMA INFECTIONS AMONG RESIDENTS OF THE WESTERN AND SOUTHERN COASTAL ISLANDS OF THE REPUBLIC OF KOREA

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  • 1 Department of Parasitology and Tropical Medicine, Seoul National University College of Medicine, and Institute of Endemic Diseases, Seoul National University Medical Research Center, Seoul, Korea; Department of Parasitology, Kangwon National University College of Medicine, Chunchon, Korea; Korea Association of Health Promotion, Seoul, Korea

To determine the distribution and prevalence of heterophyid fluke infections on coastal islands of the Republic of Korea, fecal specimens were collected from 4,179 people residing on 45 islands in the West (Yellow) and South Seas and examined using the formalin-ether and Kato-Katz techniques. Eggs of Heterophyes nocens were found in 459 (11.0%) residents of 42 islands, with an average number of eggs per gram (epg) of feces of 79.6. Eggs of Pygidiopsis summa were found in 49 (1.2%) on 12 islands, with an average epg of 253.0. The egg-positive rate for H. nocens was the highest on Chungdo (32.6%), followed by Imchado (27.3%); P. summa was most prevalent on Imchado (15.2%). The majority (78.9% [362 of 549] of those infected with H. nocens and 81.6% [40 of 49] of those infected with P. summa) of those infected were adults more than 40 years old. Adult flukes of these species were recovered from residents of Imchado by treatment with praziquantel and purgation. Our results indicate that H. nocens and P. summa are indigenous to the southern and western coastal islands of the Republic of Korea.

INTRODUCTION

Members of the family Heterophyidae (heterophyids) are a group of minute intestinal trematodes infecting avian and mammalian hosts. Worldwide, more than 22 heterophyid species are known to infect humans.1,2 Among these, 10 species, namely, Metagonimus yokogawai, M. takahashii, M. miyatai, Heterophyes nocens, Heterophyopis continua, Centrocestus armatus, Pygidiopsis summa, Stellantchasmus falcatus, Stictodora fuscata, and S. lari have been reported to be indigenous in the Republic of Korea.3–8 Because of its wide geographic distribution and high prevalence in riverside areas, public health attention has focused upon M. yokogawai.3,4 However, with regard to the other heterophyids, particularly H. nocens and P. summa, which are distributed in brackish water areas,9–13 comparatively little has been done to determine their geographic distributions and prevalences.

These two heterophyid species have been suggested to be prevalent in the Republic of Korea because of the common consumption of brackish water fishes including mullets (Mugil cephalus), perches (Lateolabrax japonicus), and gobies (Acanthogobius flavimanus), in a sashimi style (raw condition). However, prior to 1989, only 13 and 8 human infections of H. nocens and P. summa, respectively, had been reported from scattered localities.14–17 Since 1990, a few endemic foci of these fluke infections were discovered on a southwestern island18 and in mainland coastal areas.19,20 This information suggested that these flukes might also be prevalent on other islands, but no surveys have been conducted. Therefore, the present study was performed to determine the geographic distributions and prevalences of human H. nocens and P. summa infections on coastal islands of the Republic of Korea.

MATERIALS AND METHODS

Areas surveyed.

Of a total of 454 inhabited islands in the West (Yellow Sea) and South Seas of the Republic of Korea, 55 were randomly selected. Ten remote islands that are difficult to access were excluded, and the remaining 45 were included in this study (Table 1 and Figure 1). On each island, several coastal villages with populations of less than 300 were selected and all members of these villages were subjected to fecal examinations. More than half (55–65%) of the population were agricultural workers; a smaller proportion (10–20%) was engaged in the fishing industry. Estuaries were present near these villages, and the tidal rise and fall was large, maintaining a brackish water environment.

Fecal examinations.

A total of 4,179 fecal specimens, one specimen from each person, were collected from the 45 islands with the help of Regional Branch officers of the Korea Association of Health Promotion (Seoul, Korea), during July and August 2000. Specimens were transported to the Department of Parasitology and Tropical Medicine, Seoul National University College of Medicine (Seoul, Korea) within a week of collection and stored at 4°C until examined. Formalin-ether sedimentation and the Kato-Katz thick smear techniques were used to detect protozoan cysts and helminth eggs. Small, operculate, light brown, trematode eggs 25–28 × 14–16 μm in size with slightly pointed anterior and posterior ends were identified as H. nocens, while those 19–26 × 12–14 μm in size with an ovoid to pyriform shape, an attenuated anterior end, and a clean egg shell were identified as P. summa.4,21 Elliptical eggs 21–25 × 11–15 μm in size with a thin transparent shell were identified as those of Gymnophalloides seoi (Gymnophallidae), a new human intestinal trematode to the Republic of Korea,22 the results of which have been reported separately.23 Egg counting was done in Kato-Katz thick smears, which contained approximately 41.7 mg of fecal sample per smear.4 The number of eggs per gram (epg) of feces was calculated as epg 24 × the total number of eggs present on each Kato-Katz smear.

Worm collection.

Imchado (area code 16 in Table 1 and Figure 1) was selected as an island for adult fluke collection in view of the relatively high egg positive rate and the high epg found on this island. In December 2001, we visited this island and collected fecal specimens from 104 residents. The results obtained showed that 27.9% (29 of 104) were positive for heterophyid eggs. Ten cases were randomly selected and treated with a single dose (10 mg/kg) of praziquantel (Shinpoong Pharmaceutical Co., Seoul, Korea) and purged with magnesium salt after obtaining informed consent from each person. Whole diarrheic stools passed successively 4–5 times were collected and pooled individually. The stools were then washed several times with 10 volumes of water, sieved with a 2-mm mesh, and resuspended in water. After 10 minutes, the upper clean layer was discarded, and the lower dark layer was fixed with 0.5–1.0% neutral-buffered formalin. Samples were transported to the Department of Parasitology and Tropical Medicine, Seoul National University College of Medicine (Seoul, Korea) and examined for worm parasites under a stereomicroscope. Worms were collected using a glass pipette and washed several times in water. The number of worms collected was counted, and some were morphologically identified under a light microscope.

Ethics.

The study was reviewed and approved by the Korea Association of Health Promotion under the auspices of the Ministry of Health and Social Welfare.

Statistical analysis.

The results of the fecal examination for trematode eggs were analyzed with respect to the age, sex, and locality by using Fisher’s exact test and the chi-square test.

RESULTS

Prevalence and intensity of H. nocens infection.

Of the 4,179 people examined, 459 (11.0%) were egg positive for H. nocens; positive cases were found on 43 of the 45 islands surveyed (Table 1 and Figure 1). The islands with egg-positive rates greater than 20% were Chungdo (32.6%), Hauido (29.2%), Kogumdo (28.8%), Naenarodo (28.0%), Imchado (27.3%), Anchwado (23.6%), and Pikumdo (22.1%). Of the remaining 36 islands, 11 had an egg-positive rate between 10% and 19%, and 25 had a rate less than 10%. The Individual epg of H. nocens ranged from 24 to 3,216 and with a mean of 79.6 (n = 407). The highest mean epg was obtained on Pikumdo (441.6), followed by Imchado (156.0), Huksando (144.0), Chungdo (96.0), Munyodo (91.2), and Wonsando (84.0). Adults more than 20 years old had markedly higher (P < 0.05) egg-positive rates (Figure 2) and comprised 96.9% of the egg-positive cases. The egg-positive rate of women (11.4%) was slightly higher than that of men (10.5%), but this difference was not statistically significant (P > 0.05).

Prevalence and intensity of P. summa infection.

Of the 4,179 specimens, P. summa eggs were found in 49 (1.2%) on 12 of the 45 islands examined. Thus, the geographic distribution of egg-positive cases was not as wide as that of H. nocens (Table 1 and Figure 1). The highest-egg positive rate was found on Imchado (15.2%), followed by Chungdo (6.5%), Tochodo (6.3%), and Kadokdo (6.3%). With the exception of two islands (Chebudo and Kadokdo), the distribution of P. summa egg-positive cases was confined to Chollanam-do, particularly Shinangun (Figure 1). Individual epg ranged from 24 to 2,904 with a mean of 253 (n = 48). The highest mean epg was found on Imchado (1,024.8), followed by Pikumdo (816.0), Hauido (252.0), Kadokdo (240.0), and Tochodo (144.0). Of those found to be egg positive, 89.8% were more than 40 years old (P < 0.05) (Figure 2). Women had a higher egg positive rate (1.3%) than men (1.0%), but this difference was not statistically significant (P > 0.05).

Prevalence of other parasite infections.

Other helminth eggs detected by fecal examination included G. seoi22 (160 people, 3.8%) (also reported by Chai and others23) Trichuris trichiura (94, 2.2%), Metagonimus yokogawai (76, 1.8%), Clonorchis sinensis (65, 1.6%), hookworms (18, 0.43%), Ascaris lumbricoides (11, 0.26%), Taenia sp. (3, 0.07%), Echinostoma hortense4 (2, 0.05%), and Diphyllobothrium latum (1, 0.02%). Protozoan cysts found at the same time were Entamoeba coli (42, 1.0%), Giardia lamblia (3, 0.07%), Entamoeba histolytica (1, 0.02%), and Endolimax nana (1, 0.02%).

Worms collected from villagers on Imchado.

Various species of intestinal flukes were collected from the diarrheic stools of 10 Imchado residents who were treated with praziquantel and purged (Table 2 and Figure 3). A total of 42,917 adult fluke specimens, including 2,975 of H. nocens (Figure 3A and B), 32,879 of P. summa (Figure 3A and C) and 7,063 miscellaneous species (Table 2), were recovered from the 10 persons. The highest number of H. nocens collected from a single person was 1,347, and the lowest was 9, with a mean number of 228 worms collected per person. The number of P. summa collected per person ranged from 0 to 21,598, with a mean of 3,288, which was more than 10 times higher than that of H. nocens.

Other heterophyid flukes collected included Heterophyopsis continua5 (4 specimens), Stellantchasmus falcatus6 (5), Stictodora fuscata4,7(134), and S. lari8 (5). Flukes of the other families were also collected, namely, G. seoi (6,914) (Figure 3A) and Acanthoparyphium tyosenense24 (1) (Echinostomatidae) (Table 2). Further details on these fluke infections will be reported separately.

DISCUSSION

In the present study, two species of heterophyids, namely, H. nocens and P. summa, were found to be prevalent among residents of the western and southern islands of the Republic of Korea. People infected with H. nocens were found on almost all (43 of 45) of the islands tested, whereas those infected with P. summa were distributed sparsely on 12 islands, the majority of which are located in the southern West (Yellow) Sea. The prevalence of H. nocens (11.0%) was approximately 10 times higher than that of P. summa (1.2%), but its intensity of infection, as shown by the average epg, was more than three times higher. Adult flukes of H. nocens, P. summa and several others were collected from Imchado residents after treatment with praziquantel and purgation and morphologically identified.

Close morphologic similarities have been reported between the eggs of heterophyid genera and species, and between heterophyid species and C. sinensis (Opisthorchiidae),21 a common liver fluke in the Republic of Korea. The eggs of H. nocens and P. summa differ from those of C. sinensis in lacking the muskmelon eggshell patterns.4,21 The eggs of H. nocens differ from those of P. summa by their larger size and elliptical shape rather than a pyriform shape.4,21 The eggs of G. seoi are similar to those of H. nocens and P. summa, but may be distinguished from the former by their smaller size and a thin transparent eggshell, and from the latter by their elliptical form and thin eggshell.4,22 However, differentiation of the eggs of H. nocens from those of the other heterophyids, including H. continua and Stictodora spp., is difficult and problematic. Therefore, we recovered adult flukes from Imchado residents to support diagnoses made by egg examinations, and were able to confirm H. nocens, P. summa, and G. seoi infections. Small numbers of specimens of the other fluke species, namely H. continua (4 specimens), S. falcatus (5), S. fuscata (134), S. lari (5), and A. tyosenense (1), were also recovered, although their eggs were not detected in fecal examinations. A lack of egg detection is presumed to be due to low individual worm burdens (< 100 worms per person),4 even in S. fuscata-infected cases.

Since the metacercariae of H. nocens10 and P. summa11 were detected in brackish water fishes, including mullets (Mugil cephalus) and gobies (Acanthogobius flavimanus), the geographic distributions of these flukes in the Republic of Korea has been depicted based on recovery of metacercariae from fish. The metacercariae of H. nocens have been found in six areas:13,25 Yongdok-gun (eastern coast), Yeochon-gun and Haenam-gun (southern coast), and Mokpo City, Okku-gun, and Yongyu Island (western coast), and those of P. summa in five areas:13,25 Samchonpo City, Yeochon-gun, Haenam-gun, and Mokpo City (southern coast), and Okku-gun (western coast). With regard to geographic distributions, the results of the present study are comparable with the distributions determined in previous reports.13,25

Cases of human infections with H. nocens (1 case) and P. summa (8 cases) were discovered in Okku-gun (Chollanam-do) in 1981 for the first time in the Republic of Korea.14 Thereafter, human infections with H. nocens have been found sporadically in several coastal areas,15–17,26 whereas no additional human infections with P. summa were reported before 1997. However, endemic foci for H. nocens and P. summa were discovered in each of four coastal villages: Shinan-gun (Chollanam-do),18 Muan-gun (Chollanam-do),19 Puan-gun (Chollabuk-do),20 and Sachon-gun (Kyongsangnam-do).20 In the present study, human infections of H. nocens and P. summa were found to be more widely distributed than previously believed; 43 and 12 coastal islands, respectively, were found to be new endemic areas for the two species.

Despite the lower prevalence of P. summa than that of H. nocens on the islands surveyed, the intensity of infection, as determined by the average epg, was higher for P. summa. This may be related to the distribution and density of their metacercariae in the fish body; for P. summa, the majority of metacercariae are found in the gills and the density is high,13 whereas those of H. nocens are found more frequently in muscle at comparatively low densities.13 Eating of the heads, which contain the gills, of mullets and gobies seems to be an important risk factor for P. summa infection. Such practices may differ between islands. In this connection, it is of interest to note that islands with P. summa-infected cases were concentrated in the southern part of the West (Yellow) Sea, particularly on Shinan-gun. In contrast, H. nocens infection was more widely distributed and found on almost all islands surveyed.

The importance of infected people in the maintenance of the life cycles of H. nocens and P. summa is uncertain. Animal reservoir hosts, if present, may be more important than humans. Unfortunately, however, information on the reservoir hosts of these flukes is scarce; only domestic cats, obtained from a local market in Seoul, were reported to be infected with H. nocens, P. summa, and several other intestinal flukes.27 On the surveyed islands, no studies were performed on reservoir hosts, and the role of cats in maintaining the life cycles of these two fluke species remains unclear. From an ecologic point of view, birds have been suggested to be a reservoir host, but no evidence has been obtained; studies are required to further elucidate this point.

We regret that clinicopathologic studies were not performed on people infected with H. nocens and P. summa. Thus, the pathologic aspects of these fluke infections, and the symptoms and signs of infected people are unknown. Moreover, some infected individuals had mixed infections, for example, with intestinal protozoans. Thus, specific symptoms and signs due to H. nocens or P. summa infections could not be determined. In experimental mice and rats, P. summa infection was shown to cause villous atrophy (a thickening and blunting of tips and fusion), crypt hyperplasia, and inflammation of the mucosa of the small intestine.28 However, in infected humans, the clinical manifestations of intestinal heterophyid infections are known to be generally mild and transient, and cause no serious illnesses,4 although heavily infected individuals may experience epigastric discomfort, diarrhea, indigestion, fatigue, weakness, and vomiting.4,15,29 Nevertheless, heterophyid members, namely Haplorchis, Stellantchasmus, and Procerovum, can cause fatal erratic parasitism in the heart, brain, and spinal cord30 in immunocompromised patients. Host-parasite relationships, including the immune responses of hosts, remain to be further elucidated.

Table 1

Distribution of Heterophyes nocens and Pygidiopsis summa egg-positive cases on the western and southern coastal islands of the Republic of Korea*

H. nocensP. summa
ProvinceArea of islandsCode in Figure 1No. of examinationsNo. positive (%)Average EPGRange of EPGNo. positive (%)Average EPGRange of EPG
* EPG = eggs per gram of feces.
† n = 407.
‡ n = 48.
Kyonggi-doChebudo1654 (6.2)30.024–481 (1.5)48.048
Soyado2571 (1.8)24.024.00 (0.0)
Sonchaedo3621 (1.6)24.024.00 (0.0)
Yonghungdo4661 (1.5)48.0480 (0.0)
Chungchong-nam-doAnmyondo5856 (7.1)24.024.00 (0.0)
Kodaedo6894 (4.5)24.024.00 (0.0)
Wonsando7942 (2.1)84.024–1440 (0.0)
Sapshido8871 (1.1)24.024.00 (0.0)
Chollabuk-doShinshido99316 (17.2)36.024–960 (0.0)
Sonyudo101078 (7.5)27.024–480 (0.0)
Munyodo11986 (6.1)91.224–3360 (0.0)
Chollanam-doChungdo129230 (32.6)96.024–7446 (6.5)84.024–144
Hauido139628 (29.2)48.024–2162 (2.1)252.024–456
Kogumdo1411132 (28.8)64.824–3360 (0.0)
Naenarodo1510730 (28.0)60.024–3360 (0.0)
Imchado169927 (27.3)156.024–1,58415 (15.2)1,024.824–2,904
Anchwado1711026 (23.6)57.624–2401 (0.9)48.048
Pikumdo1810423 (22.1)441.624–3,2162 (1.9)816.0816
Changdo1910921 (19.3)48.024–1920 (0.0)
Sodo2010018 (18.0)45.624–2160 (0.0)
Tolsando219316 (17.2)33.624–720 (0.0)
Pyongildo2210816 (14.8)43.224–963 (2.8)25.324–48
Oenarodo2311716 (13.7)69.924–2160 (0.0)
Tochodo249512 (12.6)52.824–966 (6.3)144.024–576
Nakwoldo259311 (11.8)38.424–1443 (3.2)72.024–120
Dallido2610411 (10.6)31.224–721 (1.0)48.048
Amtaedo279910 (10.1)31.224–480 (0.0)
Hachodo281088 (7.4)26.424–481 (0.9)24.024
Keogumdo291138 (7.1)28.824–480 (0.0)
Sangchodo301037 (6.8)36.024–720 (0.0)
Pogildo311037 (6.8)24.0240 (0.0)
Kohado32855 (5.9)24.0240 (0.0)
Sorokdo33913 (3.3)72.024–1680 (0.0)
Nopdo341022 (2.0)24.0240 (0.0)
Nohwado351092 (1.8)36.024–480 (0.0)
Huksando36901 (1.1)144.01440 (0.0)
Kyeongsang-nam-doKajodo371047 (6.7)57.624–1920 (0.0)
Tumido38623 (4.8)40.824–720 (0.0)
Sandaldo39673 (4.5)24.0240 (0.0)
Pijindo40612 (3.3)24.0240 (0.0)
Yokchido41942 (2.1)24.0240 (0.0)
Yonhwado42660 (0.0)0 (0.0)
Maemuldo43380 (0.0)0 (0.0)
Kadokdo4412817 (13.3)76.224–3368 (6.3)240.024–1,368
Cheju-doChuchado451157 (6.1)24.0240 (0.0)
    Total4,179459 (11.0)79.6†24–3,21649 (1.2)253.0‡24–2,904
Table 2

Results of worm collection from the villagers on Imchado, Chollanam-do, Republic of Korea

No. of fluke specimens collected
Villager nameAge/sexH. nocensP. summaOther species*Total
* Other species include Heterophyopsis continua (4 specimens), Stellantchasmus falcatus (5), Stictodora fuscata (134), S lari (5), Gymnophalloides seoi (6,914), and Acanthoparyphium tyosenense (1).
KSL72/M1,34721,5985,87928,824
CKE55/F6998376212,157
CYH50/F3268,398178,741
KSK65/F270639342
CBC63/M10436235375
CCH58/M93609162
KSS56/M631,38721,452
CSN66/F43498285826
JGY64/F212124
CJS70/F90514
    Total2,97532,8797,06342,917
Figure 1.
Figure 1.

Map showing Heterophyes nocens and Pygidiopsis summa infections in the surveyed areas of Korea. A total of 4,179 fecal specimens collected from 45 coastal islands were examined. Egg-positive cases of H. nocens were found on 43 of 45 islands and those of P. summa on 12 of 45 islands. •* = positive for both H. nocens and P. summa eggs; • = positive for only H. nocens eggs; ○ = negative for both H. nocens and P. summa eggs. DMZ = demilitarized zone with North Korea.

Citation: The American Journal of Tropical Medicine and Hygiene Am J Trop Med Hyg 71, 5; 10.4269/ajtmh.2004.71.617

Figure 2.
Figure 2.

Age and sex prevalence of Heterophyes nocens and Pygidiopsis summa infections among residents on the surveyed islands. Adults showed a higher prevalence (P < 0.05) than children for both species of flukes. Women showed a slightly higher (P > 0.05) egg-positive rates (257/2,260 = 11.4% for H. nocens and 29/2,260 = 1.3% for P. summa) than men (202/1,918 = 10.5% for H. nocens and 20/1,918 = 1.0% for P. summa).

Citation: The American Journal of Tropical Medicine and Hygiene Am J Trop Med Hyg 71, 5; 10.4269/ajtmh.2004.71.617

Figure 3.
Figure 3.

Photomicrographs of fluke specimens recovered from an infected person residing on Imchado (area code 16; Table 1 and Figure 1). A, Wet specimens of Heterophyes nocens (Hn), Pygidiopsis summa (Ps) and Gymnophalloides seoi (Gs) expelled in diarrheic stool (CKE in Table 2) after washing with water (bar = 0.5 mm). B, Acetocarmine-stained specimen of H. nocens, showing its unique organs and structures (bar = 0.2 mm). C, Aacetocarmine-stained specimen of P. summa, demonstrating its peculiar shape (bar = 0.2 mm).

Citation: The American Journal of Tropical Medicine and Hygiene Am J Trop Med Hyg 71, 5; 10.4269/ajtmh.2004.71.617

Authors’ addresses: Jong-Yil Chai, Jae-Hwan Park, Eun-Hee Shin, Jae-Lip Kim, Sang-Mee Guk, and Soon-Hyung Lee, Department of Parasitology and Tropical Medicine, Seoul National University College of Medicine, and Institute of Endemic Disease, Seoul National University Medical Research Center, Seoul 110-799, Korea, Telephone: 82-2-740-8342, Fax: 82-2-765-6142. Eun-Taek Han, Department of Parasitology, Kangwon National University College of Medicine, Chunchon 200-701, Korea, Telephone: 82-33-250-7941, Fax: 82-33-242-7571. Kwang-Sun Hong and Han-Jong Rim, Korea Association of Health Promotion, 1097 Hwagok-6-dong, Kangseo-gu, Seoul 157-016, Korea, Telephone: 82-2-2601-6142, Fax: 82-2-2690-4905.

Acknowledgments: We thank the staff of the branch offices of the Korea Association of Health Promotion for helping with the collection of fecal samples.

Financial support: This study was supported by a grant from the Korea Association of Health Promotion (2000), and by BK21 Human Life Sciences, Ministry of Education, Republic of Korea.

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Author Notes

Reprint requests: Jong-Yil Chai, Department of Parasitology and Tropical Medicine, Seoul National University College of Medicine, and Institute of Endemic Diseases, Seoul National University Medical Research Center, Seoul 110-799, Korea, E-mail: cjy@plaza.snu.ac.kr.
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