Literature DB >> 24159439

Prevalence of Clonorchis sinensis Infections Along the Five Major Rivers in Republic of Korea, 2007.

Hyun-Kyung Kim1, Hyeng-Il Cheun, Byung-Suk Cheun, Ki-Yeon Lee, Tong-Soo Kim, Sang-Eun Lee, Won-Ja Lee, Shin-Hyeong Cho.   

Abstract

OBJECTIVES: The prevalence of Clonorchis sinensis infection was investigated among residents of the five major river basins, that is, Hangang, Nakdonggang, Seomjingang, Yeongsangang, and Geumgang River basins in Korea.
METHODS: From January to December 2007, a total of 31,268 stool samples were collected from 29 localities and examined by the formalin-ether sedimentation technique.
RESULTS: Intestinal parasite eggs and/or protozoan cysts were detected from 2957 (9.5%) inhabitants. Number of residents harbouring helminth eggs in the faeces was 2542 (8.1%) for C. sinensis, 255 (0.8%) for Heterophyes spp., 36 (0.1%) for Echinostoma spp., 30 (0.1%) for Trichuris trichiura, 8 (0.03%) for Ascaris lumbricoides, 7 (0.02%) for Gymnophalloide seoi, and 50 (0.02%) for Trichostrongylus orientalis. Number of residents harbouring protozoan cysts in the faeces was 133 (1.3%) for Entamoeba spp. and 50 (0.2%) for Giardia lamblia. The positive rates of C. sinensis in Nakdonggang, Seomjingang, Yeongsangang, Geumgang, and Hangang River basins were 12.2%, 9.5%, 3.3%, 3.0%, and 1.0%, respectively. The egg positive rate of C. sinensis was higher in male (10.6%) than in female (6.1%), and the age group of 50s had the highest positive rate (10.4%).
CONCLUSION: The result of this study revealed little decrease in positive rate of C. sinensis compared with the result of southern endemic areas of Korea in 2006.

Entities:  

Keywords:  Clonorchis sinensis; five major rivers; intestinal parasites; prevalence

Year:  2010        PMID: 24159439      PMCID: PMC3766887          DOI: 10.1016/j.phrp.2010.12.010

Source DB:  PubMed          Journal:  Osong Public Health Res Perspect        ISSN: 2210-9099


Introduction

Intestinal parasitic infections were highly prevalent until 1970s in Korea, especially among residents of major river basins of the country. During the past decade, a rapid decrease in the overall prevalence of intestinal parasites has been observed and is attributed mainly by nationwide control programs and health education undertaken by the Korean government along with increases in living conditions and quality of life among people living in Korea. Despite the remarkable decrease in soil-transmitted nematode infections, however, the prevalence of fish-borne trematode infections such as with Clonorchis sinensis and Metagonimus yokogawai has been maintained at relatively high level. The liver fluke, C. sinensis, is currently the most important parasite infecting humans in Korea. Egg positive rates of C. sinensis in general population were 4.6% in 1971, 1.8% in 1976, 2.6% in 1981, 2.7% in 1986, 2.2% in 1992, 1.4% in 1997, and 2.4% in 2004. In 1981, the egg positive rates of people living in those river basins differed considerably; 40.2% in Nakdonggang, 30.8% in Yeongsangang, 17.3% in Seomjingang, 15.7% in Hangang, 15.9% in Tamjingang, 12.0% in Geumgang, and 8.0% in Mangyeonggang Rivers. The infection of C. sinensis is contracted by eating undercooked fishes that harbour the metacercariae. Contaminated fishes are mainly found from streams and rivers where the freshwater snail Parafossarulus manchouricus thrive. The liver fluke in the biliary passage provokes severe pathologic changes therein, such as bile duct dilatation, ductal wall thickening, ductal inflammation, biliary mucosal hyperplasia, and biliary cirrhosis. The infection with C. sinensis was also found to induce cholangiocarcinoma in experimental hamsters acting as a promoter. Clonorchiasis has been recognized as one of several factors of cholangiocarcinoma in humans. Although some local data are previously available on this issue, no nationwide surveys have been conducted. The present survey on the prevalence and distribution of human clonorchiasis is one of the prerequisites for the government to implement its national control measures.

Materials and Methods

Surveyed area

Twenty-nine counties (Figure 1 and Table 1) were selected in five major river basins, which were located near or alongside the major rivers of Korea with reference to the nationwide survey in 2004. The study was undertaken for 1 year from January to December 2007.
Figure 1

The surveyed areas and five major rivers located in Korea.

Table 1

The subject of investigation according to localities and sex.

Locality (river basin)No. of residents examined
Total*MaleFemale
Hangang11,029477550
2988453535
Subtotal2,0179301,085
Guemgang31,038480558
4868390478
51,120532588
61,056528528
71,076467609
Subtotal5,1582,3972,761
Seomjingang81,213547666
92,4241,1201,304
101,193545648
111,072508563
12922411511
Subtotal6,8243,1313,692
Youngsangang131,256468788
141,098426672
151,009397612
161,049503546
Subtotal4,4121,7942,618
Nakdonggang17836349486
18919430489
191,001359642
201,002334668
21936414522
221,175515660
231,165589575
24880371509
251,172670502
26695302393
27953397556
281,163526637
29960421539
Subtotal12,8575,6777,178



Total31,26813,92917,334

Sex unidentified: five.

Stool collection and examination

Stool specimens were collected in plastic containers and transferred to the laboratory of National Institute of Health. A total of 31,268 subjects were recruited from villages for stool collection by a random household sampling method to assess the prevalence of parasitic infection. The formalin-ether sedimentation technique was used to examine helminth eggs, larvae, and protozoan cysts. One gram of each faecal sample was fixed with 10% neutral formalin in a 10-mL test tube. The formalin-fixed stool specimen was further processed by the formalin-ether concentration technique and examined for parasites in the laboratory. Parasite-positive individuals were treated with praziquantel and other appropriate anti-parasitic drugs at the end of the study.

Results

Number of positive cases of total intestinal parasites

Of 31,268 stool samples examined, 2957 (9.5%) were found to contain various intestinal parasite eggs, cysts, or larvae. Eggs of C. sinensis, Heterophyes spp., Echinostoma spp., Trichuris trichiura, Ascaris lumbricoides, Gymnophalloide seoi, and Trichostrongylus orientalis were detected from 2542 (8.1%), 255 (0.8%), 36 (0.1%), 30 (0.1%), 8 (0.03%), 7 (0.02%), and 5 (0.02%) individuals, respectively. Protozoan cysts were detected from 133 (1.3%) individuals for Entamoeba spp. and 50 (0.2%) for Giardia lamblia (Table 2).
Table 2

Positive cases of intestinal helminths and protozoa according to locality and parasites species

Locality (river basin)No. of ExaminedNo. of Positive (%)Helminth
Protozoa
Others*
Cs (%)HetEchGsAlTtToAmGl
Hangang11,02921 (2.0)19 (1.8)100000020
298812 (1.2)2 (0.2)100100413
Subtotal2,01733 (1.6)21 (1.0)200100433
Geumgang31,0389 (0.9)3 (0.3)000010311
486845 (5.2)41 (4.7)000020111
51,12037 (3.3)30 (2.7)000030410
61,05658 (5.5)48 (4.5)000040330
71,07645 (4.2)37 (3.4)500110001
Subtotal5,158194 (3.8)159 (3.1)50011101163
Seomjingang81,21396 (7.9)83 (6.8)500000723
92,424284 (11.7)247 (10.2)43100001132
101,193124 (10.4)111 (9.3)400012720
111,072109 (10.2)77 (7.2)16012001450
12922182 (19.7)133 (14.4)50000001120
Subtotal6,824795 (11.7)651 (9.5)1181121250145
Youngsangang131,256101 (8.0)40 (3.2)37330010710
141,09858 (5.3)44 (4.0)312010820
151,00941 (4.1)30 (3.0)1001000510
161,04956 (5.3)31 (3.0)7010311230
Subtotal4,412256 (5.8)145 (3.3)573440513270
Nakdonggang17836109 (13.0)99 (11.8)1000000000
18919141 (15.3)141 (15.3)500000000
191,00163 (6.3)59 (5.9)400000000
201,00280 (8.0)73 (7.3)500020000
21936149 (15.9)142 (15.2)101020210
221,175150 (12.8)138 (11.7)400011440
231,165154 (13.2)145 (12.4)600010260
24880101 (11.5)98 (11.1)300000000
251,17257 (4.9)33 (2.8)0012101901
26695103 (14.8)94 (13.5)1400020000
27953211 (22.1)198 (20.8)310031271
281,163131 (11.3)124 (10.7)1000010300
29960230 (24.0)222 (23.1)800200422
Subtotal12,8571,679 (13.1)1,566 (12.2)7312413236204
Total31,2682,957 (9.5)2,542 (8.1)25536783051335015

Cs, Clonorchis sinensis; Het, Heterophyes spp.; Ech, Echinostoma spp.; Gs, Gymnophalloides seoi; Al, Ascaris lumbricoides; Tt, Trichuris trichiura; To, Trichostrongylus orientalis; Am, Entamoeba spp.; Gl, Giardia lamblia.

Hook worm, Diphyllobothrium latum, Enterobius vermicularis, Paragonimus westermani

Egg positive cases of C. sinensis by river basin and gender

Infection rates of C. sinensis by river basin, locality, and gender are summarized in Table 3. The overall egg positive rate of C. sinensis was 8.1%. The highest rate was observed in the Nakdonggang River basin, which showed an average infection rate of 12.2%, ranging from 2.8% to 23.1% by counties. Yecheon-gun showed the highest rate at 23.1%, followed by Sangju-si (20.8%). The next highest rate was observed in the Seomjingang River basin with an average infection rate of 9.5%, ranging from 6.8% to 14.4%. The lowest infection rate was observed in the Hangang River basin, which showed an average of 1.0%.
Table 3

Positive rates of C. sinensis according to localities and gender.

Locality (river basin)Total
Male
Female
No. of ExaminedNo. of Positive (%)No. of ExaminedNo. of Positive (%)No. of ExaminedNo. of Positive (%)
Hangang11,02919 (1.8)47713 (2.7)5506 (1.1)
29882 (0.2)4531 (0.2)5351 (0.2)
Subtotal2,01721 (1.0)93014 (1.5)1,0857 (0.6)
Guemgang31,0383 (0.3)4802 (0.4)5581 (0.2)
486841 (4.7)39023 (5.9)47818 (3.8)
51,12030 (2.7)53224 (4.5)5886 (1)
61,05648 (4.5)52833 (6.3)52815 (2.8)
71,07637 (3.4)46728 (6)6099 (1.5)
Subtotal5,158159 (3.1)2,397110 (4.6)2,76149 (1.8)
Seomjingang81,21383 (6.8)54761 (11.2)66622 (3.3)
92,424247 (10.2)1,120149 (13.3)1,30498 (7.5)
101,193111 (9.3)54571 (13)64840 (6.2)
111,07277 (7.2)50840 (7.9)56336 (6.4)
12922133 (14.4)41177 (18.7)51156 (11)
Subtotal6,824651 (9.5)3,131398 (12.7)3,692252 (6.8)
Youngsangang131,25640 (3.2)46824 (5.1)78816 (2)
141,09844 (4.0)42628 (6.6)67216 (2.4)
151,00930 (3.0)39716 (4)61214 (2.3)
161,04931 (3.0)50323 (4.6)5468 (1.5)
Subtotal4,412145 (3.3)1,79491 (5.1)2,61854 (2.1)
Nakdonggang1783699 (11.8)34949 (14)48650 (10.3)
18919141 (15.3)43073 (17)48968 (13.9)
191,00159 (5.9)35931 (8.6)64228 (4.4)
201,00273 (7.3)33436 (10.8)66837 (5.5)
21936142 (15.2)41474 (17.9)52268 (13)
221,175138 (11.7)51581 (15.7)66057 (8.6)
231,165145 (12.4)58997 (16.5)57548 (8.3)
2488098 (11.1)37156 (15.1)50942 (8.3)
251,17233 (2.8)67024 (3.6)5029 (1.8)
2669594 (13.5)30258 (19.2)39336 (9.2)
27953198 (20.8)39791 (22.9)556107 (19.2)
281,163124 (10.7)52678 (14.8)63746 (7.2)
29960222 (23.1)421120 (28.5)539102 (18.9)
Subtotal12,8571,566 (12.2)5,677868 (15.3)7,178698 (9.7)
Total31,2682,542 (8.1)13,9291,481 (10.6)17,3341,060 (6.1)

Sex unidentified: five

The egg positive rate of C. sinensis was higher in male (10.6%) than in female (6.1%). The highest rate of male residents infected with C. sinensis was observed in the Nakdonggang River basin, which showed an average infection rate of 15.3%, ranging from 3.6% to 28.5%. Male residents living in Yecheon-gun showed the highest infection rate at 28.5%, followed by Sangju-si (22.9%). The next highest rate was observed in the Seomjingang River basin (12.7%), followed by the Yeongsangang (5.1%) and the Geumgang (4.6%) River basins. The overall egg positive rate of female residents was 6.1%. The highest female egg positive rate was also observed in the Nakdonggang River basin with an average of 9.7%, ranging from 1.8% to 19.2%. The next highest rate was in the Seomjingang River basin (6.8%), followed by Yeongsangang (2.1%), Geumgang (1.8%), and Hangang (0.6%) River basins.

Egg positive cases of C. sinensis by age group

Among the 31,268 cases examined by age group, the positive rate of C. sinensis was highest in the age group between 50 and 59 years (10.4%), followed by the order of 40–49 (8.7%), 60–69 (8.3%), and 70–79 (7.7%) years (Table 4).
Table 4

Positive rates of C. sinensis according to localities and age groups

Age group (yr)
Locality (river basin)Total
1–19
20–29
30–39
40–49
50–59
60–69
70–79
Over 80
Unknown
No. of ExaminedNo. of Positive (%)No. of ExaminedNo. of Positive (%)No. of ExaminedNo. of Positive (%)No. of ExaminedNo. of Positive (%)No. of ExaminedNo. of Positive (%)No. of ExaminedNo. of Positive (%)No. of ExaminedNo. of Positive (%)No. of ExaminedNo. of Positive (%)No. of ExaminedNo. of Positive (%)No. of ExaminedNo. of Positive (%)
Hangang11,02919 (1.8)650 (0.0)180 (0.0)440 (0.0)1675 (3.0)2496 (2.4)2443 (1.2)1531 (0.7)282 (7.1)612 (3.3)
29882 (0.2)390 (0.0)190 (0.0)461221220 (0.0)1921 (0.5)3240 (0.0)1981 (0.5)420 (0.0)60 (0.0)
Subtotal2,01721 (1.0)1040 (0.0)370 (0.0)900 (0.0)2895 (1.7)4417 (1.6)5683 (0.5)3512 (0.6)702 (2.9)672 (3.0)
Guemgang31,0383 (0.3)100 (0.0)150 (0.0)420 (0.0)1221 (0.8)1940 (0.0)2751 (0.4)2951 (0.3)690 (0.0)160 (0.0)
486841 (4.7)910 (0.0)391 (2.6)462 (4.3)1168 (6.9)13712 (8.8)20511 (5.4)1887 (3.7)350 (0.0)110 (0.0)
51,12030 (2.7)00 (0.0)331 (3.0)622 (3.2)1145 (4.4)2509 (3.6)3205 (1.6)2878 (2.8)460 (0.0)80 (0.0)
61,05648 (4.5)780 (0.0)240 (0.0)550 (0.0)1615 (3.1)25713 (5.1)23322 (9.4)1656 (3.6)342 (5.9)490 (0.0)
71,07637 (3.4)940 (0.0)140 (0.0)383 (7.9)1247 (5.6)17912 (6.7)31110 (3.2)2444 (1.6)721 (1.4)00 (0.0)
Subtotal5,158159 (3.1)2730 (0.0)1252 (1.6)2437 (2.9)63726 (4.1)1,01746 (4.5)1,34449 (3.6)1,17926 (2.2)2563 (1.2)840 (0.0)
Seomjingang81,21383 (6.8)481 (2.1)131 (7.7)501 (2.0)13610 (7.4)19417 (8.8)34925 (7.2)34023 (6.8)815 (6.2)20 (0.0)
92,424247 (10.2)371 (2.7)311 (3.2)816 (7.4)30425 (8.2)42147 (11.2)75079 (10.5)61767 (10.9)13513 (9.6)488 (16.7)
101,193111 (9.3)20 (0.0)91 (11.1)312 (6.5)9513 (13.7)21326 (12.2)36531 (8.5)38333 (8.6)825 (6.1)130 (0.0)
111,07277 (7.2)741 (1.4)441 (2.3)566 (10.7)12513 (10.4)21515 (7.0)27423 (8.4)20914 (6.7)441 (2.3)313 (9.7)
12922133 (14.4)264 (15.4)122 (16.7)366 (16.7)9416 (17.0)15628 (17.9)26737 (13.9)26935 (13.0)625 (8.1)00 (0.0)
Subtotal6,824651 (9.5)1877 (3.7)1096 (5.5)25421 (8.3)75477 (10.2)1,199133 (11.1)2,005195 (9.7)1,818172 (9.5)40429 (7.2)9411 (11.7)
Youngsangang131,25640 (3.2)360 (0.0)280 (0.0)281 (3.6)1345 (3.7)2408 (3.3)43516 (3.7)2969 (3.0)581 (1.7)10 (0.0)
141,09844 (4.0)110 (0.0)140 (0.0)251 (4.0)882 (2.3)21612 (5.6)39016 (4.1)28911 (3.8)652 (3.1)00 (0.0)
151,00930 (3.0)40 (0.0)140 (0.0)390 (0.0)911 (1.1)1549 (5.8)2787 (2.5)30310 (3.3)821 (1.2)442 (4.5)
161,04931 (3.0)90 (0.0)90 (0.0)381 (2.6)1151 (0.9)22310 (4.5)36114 (3.9)2524 (1.6)411 (2.4)10 (0.0)
Subtotal4,412145 (3.3)600 (0.0)650 (0.0)1303 (2.3)4289 (2.1)83339 (4.7)1,46453 (3.6)1,14034 (3.0)2465 (2.0)462 (4.3)
Nakdonggang1783689 (10.6)10 (0.0)40 (0.0)233 (13.0)715 (7.0)14618 (12.3)39155 (14.1)1827 (3.8)161 (6.3)20 (0.0)
18919141 (15.3)691 (1.4)40 (0.0)244 (16.7)9119 (20.9)16031 (19.4)31655 (17.4)21028 (13.3)353 (8.6)100 (0.0)
191,00159 (5.9)00 (0.0)00 (0.0)50 (0.0)585 (8.6)16411 (6.7)42223 (5.5)31718 (5.7)352 (5.7)00 (0.0)
201,00273 (7.3)00 (0.0)20 (0.0)140 (0.0)667 (10.6)12615 (11.9)35025 (7.1)38923 (5.9)553 (5.5)00 (0.0)
21936142 (15.2)181 (5.6)110 (0.0)344 (11.8)9714 (14.4)20541 (20.0)28237 (13.1)23937 (15.5)343 (8.8)165 (31.3)
221,175137 (11.7)90 (0.0)82 (25.0)180 (0.0)759 (12.0)20241 (20.3)39841 (10.3)37835 (9.3)546 (11.1)333 (9.1)
231,165145 (12.4)242 (8.3)222 (9.1)371 (2.7)14726 (17.7)30956 (18.1)34633 (9.5)24822 (8.9)303 (10.0)20 (0.0)
2488098 (11.1)150 (0.0)90 (0.0)413 (7.3)11013 (11.8)21631 (14.4)27630 (10.9)17120 (11.7)170 (0.0)251 (4.0)
251,17233 (2.8)00 (0.0)150 (0.0)850 (0.0)2025 (2.5)29814 (4.7)3077 (2.3)2077 (3.4)570 (0.0)10 (0.0)
2669594 (13.5)170 (0.0)295 (17.2)404 (10.0)6011 (18.3)12726 (20.5)18021 (11.7)18821 (11.2)526 (11.5)30 (0.0)
27953198 (20.8)624 (6.5)253 (12.0)313 (9.7)10313 (12.6)16842 (25.0)27168 (25.1)22749 (21.6)6015 (25.0)61 (16.7)
281,163124 (10.7)120 (0.0)270 (0.0)432 (4.7)12012 (10.0)21023 (11.0)33041 (12.4)31138 (12.2)746 (8.1)362 (5.6)
29960222 (23.1)30 (0.0)61 (16.7)201 (5.0)12531 (24.8)20354 (26.6)25854 (20.9)27866 (23.7)6715 (22.4)00 (0.0)
Subtotal12,8571,555 (12.1)2308 (3.5)16213 (8.0)41525 (6.0)1,325170 (12.8)2,534403 (15.9)4,127490 (11.9)3,345371 (11.1)58663 (10.8)13412 (9.0)
Total31,2682,531 (8.1)85415 (1.8)49821 (4.2)1,13256 (4.9)3,433287 (8.4)6,024628 (10.4)9,508790 (8.3)7,833605 (7.7)1,562102 (6.5)42527 (6.4)

Discussion

The present study indicated that the overall prevalence of intestinal parasites was 9.5% and 2957 individuals were infected with 13 species of intestinal parasites. This result, however, is considerably lower than that of 2006, which was observed a 14.3% positive rate in southern endemic areas. The positive rate of C. sinensis was the highest, covering 85.6% of all positive cases. The egg positive rate of C. sinensis (8.1%) decreased slightly compared with the result of 2006 investigation. In the nationwide surveys in 1997 and 2004, C. sinensis positive rates were 1.4% and 2.4%, respectively, and these results suggested that C. sinensis are prevalent along major river basins. The present study was mainly focused on residents of villages where clonorchiasis has been endemic or suspected. Thus, it is the main reason for the higher egg positive rate of C. sinensis of the present study (8.1%) than that (2.4%) of 2004. Clonorchiasis has been regarded as a persisting helminthiasis and has largely disappeared throughout the country. In 2006, the total egg positive rate of C. sinensis was 11.1% among residents living in the river basins of South Korea. The egg positive rates observed in the river basins of Nakdonggang, Seomjingang, Yeongsangang, and Geumgang were 17.1%, 11.2%, 5.5%, and 4.6%, respectively. In 2007, the total egg positive rate of C. sinensis was 8.1% (Table 3). The positive rates observed in the river basins of Nakdonggang, Seomjingang, Yeongsangang, Geumgang, and Hangang were 12.2%, 9.5%, 3.3%, 3.1% and 1.0%, respectively (Table 3). Especially, the river basins of Nakdonggang and Seomjingang Rivers still appear to be endemic. The average egg positive rate of C. sinensis among male was 10.6%, which ranged from 0.2% to 28.5% by river basin areas, whereas the average positive rate among female was 6.1% with a range from 0.2% to 19.2% (Table 3). Infection rates of male and female residents showed between 3.0% and 2.8% decrease compared with results of 2006. The egg positive rate increased as age increased, reaching a maximum of 10.4% in the age group of 50–59- years (Table 3), followed by 40–49 (8.4%), 60–69 (8.3%), 70–79 (7.7%), and older than 80 (6.5%) years. The infection status of C. sinensis among Koreans by age in this study showed the same peak at the 50- to 59-year-old group as compared with the result in 2006. This result appears to be the typical pattern of C. sinensis infection, showing a peak at the age group of 40–49 or 50–59 years, which is then rapidly decreased afterwards. Because the life span of C. sinensis is known to be up to 30 years, the infection peak in the age group of 50s is comprehended as an accumulation effect of reinfection or superinfection with age because epidemiologic studies indicate that humans do not develop any resistance to reinfection or superinfection by the parasites. However, the egg positive rate decreased after the peak, in spite of the cumulative effect in the age group of 60s or more. This decreasing phenomenon in senior groups has been commonly observed in previous investigations and may suggest the possibility of shorter lifespan of residents with clonorchiasis than those of uninfected ones at the endemic areas. This decrease of 27% compared with the previous year appears to be an outcome of low endemicity by praziquantel medication. The clonorchiasis in the endemic area of South Korea is under continuous anthelminthic intervention, and the intervention makes the decrease in positive rate. Our data have been updated the status of clonorchiasis in endemic area of Korea as reduced egg positive rate and lower intensity of infection compared with previous reports. In conclusion, the result of this study revealed little decrease in positive rate of C. sinensis compared with the result of southern endemic areas of Korea in 2006. Therefore, continuous and repeated praziquantel medication is necessary in the endemic in Korea.
  10 in total

1.  Control of clonorchiasis by repeated treatments with praziquantel.

Authors:  S T Hong; H J Rim; D Y Min; X Li; J Xu; Z Feng; S H Lee
Journal:  Korean J Parasitol       Date:  2001-12       Impact factor: 1.341

Review 2.  Clonorchiasis: an update.

Authors:  H-J Rim
Journal:  J Helminthol       Date:  2005-09       Impact factor: 2.170

Review 3.  A successful experience of soil-transmitted helminth control in the Republic of Korea.

Authors:  Sung-Tae Hong; Jong-Yil Chai; Min-Ho Choi; Sun Huh; Han-Jong Rim; Soon-Hyung Lee
Journal:  Korean J Parasitol       Date:  2006-09       Impact factor: 1.341

4.  Epidemiological study of clonorchiasis and metagonimiasis along the Geum-gang (River) in Okcheon-gun (county), Korea.

Authors:  Gye-Sung Lee; In-Sung Cho; Young-Ha Lee; Hyung-Jun Noh; Dae-Whan Shin; Sok-Goo Lee; Tae-Yong Lee
Journal:  Korean J Parasitol       Date:  2002-03       Impact factor: 1.341

5.  [Mucinous cholangiocarcinoma associated with Clonorchis sinensis infestation: a case report].

Authors:  Hyo Sup Shim; Beom Jin Lim; Myeong-Jin Kim; Woo Jung Lee; Chanil Park; Young Nyun Park
Journal:  Korean J Hepatol       Date:  2004-09

6.  Promoting role of Clonorchis sinensis infection on induction of cholangiocarcinoma during two-step carcinogenesis.

Authors:  J H Lee; H M Yang; U B Bak; H J Rim
Journal:  Korean J Parasitol       Date:  1994-03       Impact factor: 1.341

7.  Cholangiocarcinoma and Clonorchis sinensis infection: a case-control study in Korea.

Authors:  Dongil Choi; Jae Hoon Lim; Kyu Taek Lee; Jong Kyun Lee; Seong Ho Choi; Jin Seok Heo; Kee-Taek Jang; Nam Yong Lee; Seonwoo Kim; Sung-Tae Hong
Journal:  J Hepatol       Date:  2005-12-27       Impact factor: 25.083

8.  Prevalence of clonorchiasis in southern endemic areas of Korea in 2006.

Authors:  Shin-Hyeong Cho; Ki-Yeon Lee; Byung-Chul Lee; Pyo-Yun Cho; Hyeong-Il Cheun; Sung-Tae Hong; Woon-Mok Sohn; Tong-Soo Kim
Journal:  Korean J Parasitol       Date:  2008-09       Impact factor: 1.341

9.  Infection status of Clonorchis sinensis in residents of Hamyang-gun, Gyeongsangnam-do, Korea.

Authors:  Bong Jin Kim; Mee-Sun Ock; Ik Su Kim; Un Bo Yeo
Journal:  Korean J Parasitol       Date:  2002-12       Impact factor: 1.341

10.  An Epidemiologic Study On Clonorchiasis And Metagonimiasis In Riverside Areas In Korea.

Authors:  Byong Seol Seo; Soon Hyung Lee; Seung Yull Cho; Jong Yil Chai; Sung Tae Hong; In Soo Han; Jin Saeng Sohn; Byong Hwan Cho; Seok Rok Ahn; Sang Ki Lee; Sang Choon Chung; Keun Shik Kang; Hyong Soo Shim; In Soo Hwang
Journal:  Kisaengchunghak Chapchi       Date:  1981-12
  10 in total
  12 in total

1.  Zoonotic Intestinal Trematodes in Stray Cats (Felis catus) from Riverside Areas of the Republic of Korea.

Authors:  Sung-Shik Shin; Dae-Sung Oh; Kyu-Sung Ahn; Shin-Hyeong Cho; Won-Ja Lee; Byoung-Kuk Na; Woon-Mok Sohn
Journal:  Korean J Parasitol       Date:  2015-04-22       Impact factor: 1.341

2.  Trematode Metacercariae in Freshwater Fish from Water Systems of Hantangang and Imjingang in Republic of Korea.

Authors:  Woon-Mok Sohn; Byoung-Kuk Na; Shin-Hyeong Cho; Soon-Won Lee; Seung-Bong Choi; Won-Seok Seok
Journal:  Korean J Parasitol       Date:  2015-06-30       Impact factor: 1.341

3.  Prevalence and Risk Factors of Clonorchiasis among the Populations Served by Primary Healthcare Posts along Five Major Rivers in South Korea.

Authors:  Kyung Ja June; Shin Hyeong Cho; Won Ja Lee; Chunmi Kim; Kyung-Soon Park
Journal:  Osong Public Health Res Perspect       Date:  2013-02

4.  Prevalence and Intensity of Clonorchis sinensis Metacercariae in Freshwater Fish from Wicheon Stream in Gunwi-gun, Gyeongsangbuk-do, Korea.

Authors:  Woon-Mok Sohn; Byoung-Kuk Na; Shin-Hyeong Cho; Jung-Won Ju; Dong-Chul Son
Journal:  Korean J Parasitol       Date:  2018-02-28       Impact factor: 1.341

5.  Epidemiological and Clinical Parameters Features of Patients with Clonorchiasis in the Geum River Basin, Republic of Korea.

Authors:  Hee-Eun Shin; Myoung-Ro Lee; Jung-Won Ju; Byong-Suk Jeong; Mi-Yeoun Park; Keoung-Sook Lee; Shin-Hyeong Cho
Journal:  Interdiscip Perspect Infect Dis       Date:  2017-04-26

6.  A new method for estimating the prevalence of clonorchiasis in Korea: A proposal to replace arbitrary riverside sampling.

Authors:  Jin-Young Jeong; Jin Yong Lee; Byung-Suk Chung; Younghyun Choi; Allison Baer Alley; Hyun Joo Kim
Journal:  Medicine (Baltimore)       Date:  2017-03       Impact factor: 1.889

7.  Infection Status with Digenetic Trematode Metacercariae in Fishes from Coastal Lakes in Gangwon-do, Republic of Korea.

Authors:  Woon-Mok Sohn; Byoung-Kuk Na; Shin-Hyeong Cho; Soon-Won Lee
Journal:  Korean J Parasitol       Date:  2019-12-31       Impact factor: 1.341

8.  Prevalence and Infection Intensity of Zoonotic Trematode Metacercariae in Fish from Soyang-cheon (Stream), in Wanju-gun, Jeollabuk-do, Korea.

Authors:  Woon-Mok Sohn; Byoung-Kuk Na; Shin-Hyeong Cho; Jung-Won Ju; Cheon-Hyeon Kim; Min-Ah Hwang; Kyeong-Woo No; Jong-Ho Park
Journal:  Korean J Parasitol       Date:  2021-06-21       Impact factor: 1.341

9.  Prevalence and risk factors of clonorchiasis among residents of riverside areas in Muju-gun, Jeollabuk-do, Korea.

Authors:  Do-Soon Park; Sung-Jin Na; Shin Hyeong Cho; Kyung Ja June; Young-Chae Cho; Young-Ha Lee
Journal:  Korean J Parasitol       Date:  2014-08-29       Impact factor: 1.341

10.  Prevalence of Clonorchis sinensis Infection among Residents along 5 Major Rivers in the Republic of Korea.

Authors:  Young-Il Jeong; Hee-Eun Shin; Sang-Eun Lee; Hyeng-Il Cheun; Jung-Won Ju; Jung-Yeon Kim; Mi Yeoun Park; Shin-Hyeong Cho
Journal:  Korean J Parasitol       Date:  2016-04-30       Impact factor: 1.341

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