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Original Article

Prevalence of Clonorchiasis in Southern Endemic Areas of Korea in 2006

Shin-Hyeong Cho1, Ki-Yeon Lee1, Byung-Chul Lee1, Pyo-Yun Cho1, Hyeong-Il Cheun1, Sung-Tae Hong2, Woon-Mok Sohn3, Tong-Soo Kim1,4
The Korean Journal of Parasitology 2008;46(3):133-137.
Published online: September 20, 2008

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Corresponding author (tongsookim@inha.ac.kr)
• Received: July 21, 2008   • Accepted: August 13, 2008

Copyright © 2008 by The Korean Society for Parasitology

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  • This study was performed to investigate prevalence of clonorchiasis among the inhabitants living in villages along the 4 major rivers, Nakdong-gang (= river), Seomjin-gang, Youngsan-gang, and Guem-gang in southern Korea. From January to December 2006, a total of 24,075 stool samples (1 sample per an inhabitant) were collected in 23 localities and examined by the formalin-ether sedimentation technique. Of the inhabitants examined, 3,441 (14.3%) were found to harbor various types of intestinal parasite eggs, cysts or larvae. Numbers of infected people were 2,661 (11.1%) for Clonorchis sinensis, 431 (1.8%) for heterophyids, 226 (0.9%) for Entamoeba spp., 57 (0.2%) for Giardia lamblia, 30 (0.1%) for Trichuris trichiura, and 18 (0.07%) for echinostomes. Prevalence rates of clonorchiasis according to the river basin were 17.1% in Nakdong-gang, 11.2% in Seomjin-gang, 5.5% in Youngsan-gang and 4.6% in Guem-gang. Of the 2,661 C. sinensis egg-positive cases, 57.7% was male. The present findings suggest that clonorchiasis is still highly prevalent among inhabitants in the riverside areas of southern Korea, and it is necessary to implement a systematic control program in the endemic areas.
  • Key words: Clonorchis sinensis, prevalence, fecal examination
Human helminthiasis has been highly endemic in Korea for a long time. In the past, it was distributed along most major river basins over the country. A rapid decrease in the overall prevalence of intestinal parasites during the past decade is attributed by continuous efforts for nationwide control programs undertaken by the Korean government to reduce the prevalence of soil-transmitted nematode infections and to improve hygiene and sanitary conditions of Koreans. However, despite this remarkable control of soil-transmitted nematode infections, the prevalence of fish-borne trematode infections such as with C. sinensis and Metagonimus spp. has maintained at relatively high levels, particularly in riverside areas [1].
Clonorchiasis is endemic in East Asian countries with estimated infections of 35 million people [2]. National surveys revealed egg positive rates of C. sinensis in general population as 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 2.9% in 2004 [3]. The infection of C. sinensis is contracted by eating undercooked fishes which harbor the metacercariae. Contaminated fishes are mainly found from streams and rivers where the freshwater snails, Parafossarulus manchouricus thrive. Especially, many endemic foci of C. sinensis were located along the 7 major rivers of South Korea. In 1981, the egg positive rates of people living in those river basins differed considerably; 40.2% in Nakdong-gang (= river), 30.8% in Yeongsan-gang, 17.3% in Seomjin-gang, 15.7% in Han-gang, 15.9% in Tamjin-gang, 12.0% in Geum-gang, and 8.0% in Mangyeong-gang [4]. The liver fluke in the biliary passage provokes severe pathological changes therein, such as bile duct dilatation, ductal wall thickening, ductal inflammation, biliary mucosal hyperplasia, and biliary cirrhosis [1]. C. sinensis was found to induce cholangiocarcinoma in experimental hamsters as a promoter [5]. Clonorchiasis has been recognized as one of risk factors of development of cholangiocarcinoma in humans [6-8].
The present survey on the prevalence and distribution of human clonorchiasis endemic in Korea is one of the prerequi-sites for the government to implement its national control measures. Although some local data are previously available on this issue, no nationwide surveys have been conducted to determine the breadth of the problem. In this study, we evaluated the prevalence and distribution of clonorchiasis in a large scale survey and compared the endemicity among the endemic areas scattered in the southern part of Korean Peninsula.
Surveyed area
Twenty-three counties were selected in 4 river basins which were located near or alongside the major rivers of Korea, for this study with reference to the nationwide survey in 2004 [3] (Fig. 1). A total of 24,075 inhabitants (male 11,090 and female 12,985) were screened of their intestinal parasites in the selected localities (Table 1). This study was undertaken for 1 yr from January to December, 2006.
Stool collection and examination
Stool specimens were collected in plastic containers and transferred to the laboratory of National Institute of Health (NIH). The subjects for stool sampling were recruited from villages 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 fecal 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.
Statistical analysis
Comparisons of the prevalence parameters were assessed by the Student's t-test. Due to the distribution of the data for statistical significance by variation of intensity of infection was analyzed using the non-parametric analysis of variance. P < 0.05 was considered significant.
Positive rate of intestinal parasites
Of 24,075 examined stool samples, 3,441 (14.3%) were found to contain various intestinal parasite eggs, cysts or larvae. The helminth eggs detected were C. sinensis 2,661 (11.05%), heterophyids 431 (1.79%), echinostomes 18 (0.075%), Trichuris trichiura 30 (0.125%), Hookworms 5 (0.021%), Ascaris lumbricoides 4 (0.017%), Trichostrongylus orientalis 3 (0.012%), Taenia sp. 3 (0.012%), and Diphyllobothrium latum 1. Protozoan cysts were observed, Giardia lamblia from 57 (0.237%) and Entamoeba spp. from 221 (0.918%) individuals (Table 2).
Prevalence of C. sinensis by river basin
The positive rates of C. sinensis eggs by rivers, localities and sexes were summarized in Table 3. The overall egg positive rate of C. sinensis was 11.1%. The highest rate was observed in river basin of Nakdong-gang 17.1%, from 7.4% to 30.6% by counties: 30.6% in Sancheong-gun, 27.9% in Jinju-si, 26.7% in Changwon-si, 17.3% in Sangju-si, 13.5% in Miryang-si, 13.0% in Haman-gun, and 7.4% in Changnyong-gun (Table 3). In river basin of Seomjin-gang, the egg positive rate varied from 6.5% to 15.3%. In river basin of Youngsan-gang, the egg positive rate varied from 3.6% to 7.5%, and the rate varied from 0.4% to 13.9% in the river basin of Guem-gang. The overall egg positive rate of male inhabitants was 13.6% ranging from 0.4% to 36.5% by river basin, and that of females was 8.9% in average with a range from 0.5% to 25.0% (P < 0.05).
Positive rate of C. sinensis eggs by age group
To evaluate the prevalence of C. sinensis by age group, a total of 23,979 cases of the 24,075 whole examined individuals were subjected to analysis. The positive rate of C. sinensis was highest in 50-59 yr group (12.8%), followed by the order of 60-69 (12.6%), 40-49 (11.5%) and 70-79 (9.9%), whereas it decreased in those aged below 40 yr (Table 4).
The present study recognized that the overall prevalence of intestinal parasites was 14.3%, and 3,117 individuals were infected with trematodes, 42 with nematodes, 4 with cestodes and 283 with protozoa. This result is considerably higher than that of a previous nationwide survey previously performed in 2004 [3]. KCDC and KAHP (2004) surveyed intestinal helminth infections nationwidely, and observed a 4.3% egg positive rate [3]. The nationwide survey in 2004 included subjects according to a statistical stratified sampling method upon population census, however, the present study subjected all available residents in villages where clonorchiasis is endemic or suspected. That is the main reason of the higher egg positive rate (11.1%) of C. sinensis of the present study than that (2.9%) of the nationwide survey in 2004. In this context, it is more reasonable to compare the present results with those of Seo et al. (1981). That is because Seo et al. (1981) recovered helminth eggs from residents along the major rivers in Korea.
In 1981, the egg positive rate of C. sinensis was 15.7% at theriver basin of Han-gang, 12.0% at the Geum-gang river basin,8.0% at the Mangyeong-gang river basin, 30.8% at the Yeongsan-gang river basin, 17.3% at the Seomjin-gang river basin, and 40.2% at the Nakdong-gang river basin [4]. The egg positive rate of the present study was 4.6% at the Geum-gang river basin, 5.5% at the Yeongsan-gang river basin, 11.2% at the Seomjin-gang river basin, and 17.1% at the Nakdong-gang river basin. The egg positive rates at the individual river basins decreased remarkably compared with those at the same river basins in 1981 [4]. However, clonorchiasis is regarded as a persisting helminthiasis in Korea because almost all of other past prevalent helminthiases have disappeared throughout the country [1]. Especially the river basins of Nakdong-gang and Seomjin-gang are still endemic.
The average egg positive rate of C. sinensis among males was 13.6% which ranged from 0.4% to 36.5% by riverside areas, and that among females was 8.9% with a range from 0.5% to 25.0%. The age-specific egg positive rate increased as age increased, reaching a maximum of 12.8% in the 50-59 yr group. The egg positive rate of C. sinensis in men was more remarkable that of whole population, highest in 50-59 yr (12.8%), fol-lowed in order by 60-69 (12.6%), 40-49 (11.5%), and 70-79 (9.9%). The prevalence of C. sinensis by age showed one peak at the age of 40-49 or 50-59 yr in the past [9]. In every endemic area under natural equilibrium of clonorchiasis, the egg positive rate and the infection intensity increase linearly by age up to the 50s or 60s and make a peak, and then rapidly decrease afterwards. Since the life span of C. sinensis is known 30 yr or more, the peak is explained as an accumulation effect of life-long re- or super-infection with age. Human body develops no protective impact to re- or super-infection. However, the egg positive rate decreases after the peak in spite of the cumulative effect in the aged groups of 60s or more. This decreasing phenomenon in senior groups may suggest the possibility of shorter life span of residents with clonorchiasis than that of uninfected ones at the endemic areas [10]. Our data updated recent status of clonorchiasis in endemic areas of Korea as reduced egg positive rate and lower intensity of infection compared with those of previous reports [4,9,11,12]. Whole and age-specific egg positive rates have decreased, and the age-specific peak moves to 60s from 40s or 50s. This movement is an outcome of low endemicity by praziquantel medication. In other words, clonorchiasis in the endemic area in Korea is under continuous anthelminthic intervention, and the intervention makes the peak movement. The intervention has reduced also frequencies of complications of clonorchiasis as well as egg positive rate and intensity of infection [13].
Our findings reveal several other helminth eggs than C. sinensis, such as heterophyids, Gymnophalloides seoi, Echinostoma spp., Fasciola hepatica, A. lumbricoides, T. trichiura, hookworms, T. orientalisand D. latum. These various helminths have been prevalent in whole Korea in the past but most of them are now rapidly disappearing. In most of the southern parts of Korea, however, especially the fish-mediated helminths are still remaining as well as C. sinensis [14]. The localities of the helminthic infections are agricultural areas and the environment is well-preserved with minimum pollution.
In conclusion, we confirmed the presence of light to moderate endemicity of clonorchiasis and also observed other intestinal helminths in southern localities of Korea in 2006. Continuous and repeated praziquantel medication is necessary in the endemic areas in Korea.
This study was supported by an Endemic Diseases Control Program of the National Institute of Health, Ministry of Health and Welfare, Republic of Korea (NIH-4800-4847-302).
    Fig. 1
    The surveyed areas (•) and 4 major rivers located in southern parts of Korea.
    kjp-46-133-g001.jpg
    Table 1.
    The subject of investigation by the riverside, locality and sex
    Table 1.
    Riversides Localitya No. of residents examined
    Total Male Female
    Nakdong-gang (River) 1 1,761 853 908
    2 863 377 486
    3 549 232 317
    4 1,001 308 693
    5 397 142 255
    6 1,081 453 628
    7 967 420 547
    8 1,526 815 711
    9 1,032 512 520
    Subtotal 9,177 4,112 5,065
    Seomjin-gang (River) 10 1,506 726 780
    11 1,150 563 587
    12 872 387 485
    13 1,046 523 523
    14 981 396 585
    Subtotal 5,555 2,595 2,960
    Youngsan-gang (River) 15 1,202 485 717
    16 1,478 671 807
    17 1,277 541 736
    18 1,001 523 478
    Subtotal 4,958 2,220 2,738
    Guem-gang (River) 19 921 471 450
    20 811 409 402
    21 692 421 271
    22 849 378 471
    23 1,112 484 628
    Subtotal 4,385 2,163 2,222
    Total 24,075 11,090 12,985

    aLocality designated in Fig. 1.

    Table 2.
    Results of stool examination according to administrative regions
    Table 2.
    Localitya No. of exam. No. of positive cases by parasite
    		 Total no. (%) of positive
    Cs Heterophyids Echinostomes Tt Al Gl E sp. Others
    1 1,761 538 100 6 3 0 3 3 8 661 (37.5)
    2 863 241 56 0 1 0 3 4 0 305 (35.3)
    3 549 95 0 1 0 0 9 2 3 110 (19.9)
    4 1,001 81 14 0 0 0 0 0 0 95 (9.5)
    5 397 106 0 0 4 0 0 1 0 111 (28.0)
    6 1,081 140 21 0 2 0 0 9 1 173 (16.0)
    7 967 131 8 0 1 0 4 2 1 147 (15.2)
    8 1,526 158 8 0 4 0 6 7 0 183 (12.0)
    9 1,032 76 10 0 0 0 0 6 0 92 (8.9)
    10 1,506 159 15 1 1 1 8 21 1 207 (13.7)
    11 1,150 75 4 3 0 0 0 9 2 93 (8.1)
    12 872 99 85 0 0 1 3 13 0 201 (23.1)
    13 1,046 160 24 4 3 1 2 16 1 211 (20.2)
    14 981 130 12 1 0 0 3 8 0 154 (15.7)
    15 1,202 43 43 0 0 0 2 66 0 159 (13.2)
    16 1,478 111 5 0 5 0 4 10 0 135 (9.1)
    17 1,277 63 4 2 3 1 3 10 2 88 (6.9)
    18 1,001 54 1 0 0 0 1 11 0 67 (6.7)
    19 921 128 14 0 1 0 1 3 0 147 (16.0)
    20 811 26 3 0 1 0 3 7 0 40 (4.9)
    21 692 22 1 0 0 0 1 4 0 28 (4.0)
    22 849 20 3 0 1 0 1 4 0 29 (3.4)
    23 1,112 5 0 0 0 0 0 5 0 10 (0.9)
    Total 24,075 2,661 431 18 30 4 57 221 19 3,441 (14.3)

    Cs, Clonorchis sinensis; Tt, Trichuris trichiura; Al, Ascaris lumbricoides; Gl, Giardia lamblia; E sp, Entamoeba.

    aLocality designated in Fig. 1.

    Table 3.
    Positive rates of Clonorchis sinensis eggs according to riversides, localities, and sexes
    Table 3.
    Riversides Localitya No. of exam. No. (%) of positive cases in
    Male Female Total
    Nakdong-gang 1 1,761 311 227 538 (30.6)
    2 863 134 107 241 (27.9)
    3 549 47 48 95 (17.3)
    4 1,001 39 42 81 (8.1)
    5 397 49 57 106 (26.7)
    6 1,081 70 70 140 (13.0)
    7 967 63 68 131 (13.5)
    8 1,526 105 53 158 (10.4)
    9 1,032 47 29 76 (7.4)
    Subtotal 9,177 865 701 1,566 (17.1)
    Seomjin-gang 10 1,506 80 79 159 (10.6)
    11 1,150 52 23 75 (6.5)
    12 872 48 51 99 (11.4)
    13 1,046 81 79 160 (15.3)
    14 981 76 54 130 (13.3)
    Subtotal 5,555 337 286 623 (11.2)
    Youngsan-gang 15 1,202 21 22 43 (3.6)
    16 1,478 73 38 111 (7.5)
    17 1,277 35 28 63 (4.9)
    18 1,001 32 22 54 (5.4)
    Subtotal 4,958 161 110 271 (5.5)
    Guem-gang 19 921 98 30 128 (13.9)
    20 811 18 8 26 (3.2)
    21 692 14 8 22 (3.2)
    22 849 15 5 20 (2.4)
    23 1,112 2 3 5 (0.4)
    Subtotal 4,385 147 54 201 (4.6)
    Total 24,075 1,510 (13.6) 1,151 (8.9) 2,661 (11.1)

    aLocality designated in Fig. 1.

    Table 4.
    Number of egg positive cases of Clonorchis sinensis according to riversides and age groups
    Table 4.
    Riversides No. of exam. No. (%) of egg positive cases by age group
    		 Total (%)
    < 19 20-29 30-39 40-49 50-59 60-69 70-79 Over 80 NKa
    Nakdong-gang 9,177 6 12 38 195 384 543 286 37 65 1,566 (17.1)
    Seomjin-gang 5,555 11 10 15 78 141 186 128 23 30 622 (11.2)
    Youngsan-gang 4,958 2 5 12 45 53 87 56 10 1 271 (5.5)
    Guem-gang 4,385 1 2 3 14 42 75 55 9 1 202 (4.6)
    Total (%) 24,075 20 (2.4) 29 (5.1) 68 (6.3) 332 (11.5) 620 (12.8) 891 (12.6) 525 (9.9) 79 (8.0) 97 (17.8) 2,661 (11.1)

    aNot exactly known.

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    Prevalence of Clonorchiasis in Southern Endemic Areas of Korea in 2006
    Korean J Parasitol. 2008;46(3):133-137.   Published online September 20, 2008
    DOI: https://doi.org/10.3347/kjp.2008.46.3.133
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    Prevalence of Clonorchiasis in Southern Endemic Areas of Korea in 2006
    Korean J Parasitol. 2008;46(3):133-137.   Published online September 20, 2008
    DOI: https://doi.org/10.3347/kjp.2008.46.3.133
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    Prevalence of Clonorchiasis in Southern Endemic Areas of Korea in 2006
    Image
    Fig. 1 The surveyed areas (•) and 4 major rivers located in southern parts of Korea.

    Fig. 1

    Prevalence of Clonorchiasis in Southern Endemic Areas of Korea in 2006
    Riversides Localitya No. of residents examined
    Total Male Female Nakdong-gang (River) 1 1,761 853 908 2 863 377 486 3 549 232 317 4 1,001 308 693 5 397 142 255 6 1,081 453 628 7 967 420 547 8 1,526 815 711 9 1,032 512 520 Subtotal 9,177 4,112 5,065 Seomjin-gang (River) 10 1,506 726 780 11 1,150 563 587 12 872 387 485 13 1,046 523 523 14 981 396 585 Subtotal 5,555 2,595 2,960 Youngsan-gang (River) 15 1,202 485 717 16 1,478 671 807 17 1,277 541 736 18 1,001 523 478 Subtotal 4,958 2,220 2,738 Guem-gang (River) 19 921 471 450 20 811 409 402 21 692 421 271 22 849 378 471 23 1,112 484 628 Subtotal 4,385 2,163 2,222 Total 24,075 11,090 12,985 Localitya No. of exam. No. of positive cases by parasite
    Total no. (%) of positive Cs Heterophyids Echinostomes Tt Al Gl E sp. Others 1 1,761 538 100 6 3 0 3 3 8 661 (37.5) 2 863 241 56 0 1 0 3 4 0 305 (35.3) 3 549 95 0 1 0 0 9 2 3 110 (19.9) 4 1,001 81 14 0 0 0 0 0 0 95 (9.5) 5 397 106 0 0 4 0 0 1 0 111 (28.0) 6 1,081 140 21 0 2 0 0 9 1 173 (16.0) 7 967 131 8 0 1 0 4 2 1 147 (15.2) 8 1,526 158 8 0 4 0 6 7 0 183 (12.0) 9 1,032 76 10 0 0 0 0 6 0 92 (8.9) 10 1,506 159 15 1 1 1 8 21 1 207 (13.7) 11 1,150 75 4 3 0 0 0 9 2 93 (8.1) 12 872 99 85 0 0 1 3 13 0 201 (23.1) 13 1,046 160 24 4 3 1 2 16 1 211 (20.2) 14 981 130 12 1 0 0 3 8 0 154 (15.7) 15 1,202 43 43 0 0 0 2 66 0 159 (13.2) 16 1,478 111 5 0 5 0 4 10 0 135 (9.1) 17 1,277 63 4 2 3 1 3 10 2 88 (6.9) 18 1,001 54 1 0 0 0 1 11 0 67 (6.7) 19 921 128 14 0 1 0 1 3 0 147 (16.0) 20 811 26 3 0 1 0 3 7 0 40 (4.9) 21 692 22 1 0 0 0 1 4 0 28 (4.0) 22 849 20 3 0 1 0 1 4 0 29 (3.4) 23 1,112 5 0 0 0 0 0 5 0 10 (0.9) Total 24,075 2,661 431 18 30 4 57 221 19 3,441 (14.3) Riversides Localitya No. of exam. No. (%) of positive cases in
    Male Female Total Nakdong-gang 1 1,761 311 227 538 (30.6) 2 863 134 107 241 (27.9) 3 549 47 48 95 (17.3) 4 1,001 39 42 81 (8.1) 5 397 49 57 106 (26.7) 6 1,081 70 70 140 (13.0) 7 967 63 68 131 (13.5) 8 1,526 105 53 158 (10.4) 9 1,032 47 29 76 (7.4) Subtotal 9,177 865 701 1,566 (17.1) Seomjin-gang 10 1,506 80 79 159 (10.6) 11 1,150 52 23 75 (6.5) 12 872 48 51 99 (11.4) 13 1,046 81 79 160 (15.3) 14 981 76 54 130 (13.3) Subtotal 5,555 337 286 623 (11.2) Youngsan-gang 15 1,202 21 22 43 (3.6) 16 1,478 73 38 111 (7.5) 17 1,277 35 28 63 (4.9) 18 1,001 32 22 54 (5.4) Subtotal 4,958 161 110 271 (5.5) Guem-gang 19 921 98 30 128 (13.9) 20 811 18 8 26 (3.2) 21 692 14 8 22 (3.2) 22 849 15 5 20 (2.4) 23 1,112 2 3 5 (0.4) Subtotal 4,385 147 54 201 (4.6) Total 24,075 1,510 (13.6) 1,151 (8.9) 2,661 (11.1) Riversides No. of exam. No. (%) of egg positive cases by age group
    Total (%) < 19 20-29 30-39 40-49 50-59 60-69 70-79 Over 80 NKa Nakdong-gang 9,177 6 12 38 195 384 543 286 37 65 1,566 (17.1) Seomjin-gang 5,555 11 10 15 78 141 186 128 23 30 622 (11.2) Youngsan-gang 4,958 2 5 12 45 53 87 56 10 1 271 (5.5) Guem-gang 4,385 1 2 3 14 42 75 55 9 1 202 (4.6) Total (%) 24,075 20 (2.4) 29 (5.1) 68 (6.3) 332 (11.5) 620 (12.8) 891 (12.6) 525 (9.9) 79 (8.0) 97 (17.8) 2,661 (11.1)
    Table 1. The subject of investigation by the riverside, locality and sex

    Locality designated in Fig. 1.

    Table 2. Results of stool examination according to administrative regions

    Cs, Clonorchis sinensis; Tt, Trichuris trichiura; Al, Ascaris lumbricoides; Gl, Giardia lamblia; E sp, Entamoeba.

    Locality designated in Fig. 1.

    Table 3. Positive rates of Clonorchis sinensis eggs according to riversides, localities, and sexes

    Locality designated in Fig. 1.

    Table 4. Number of egg positive cases of Clonorchis sinensis according to riversides and age groups

    Not exactly known.

    Table 1.

    Table 2.

    Table 3.

    Table 4.

    PHD : Parasites, Hosts and Diseases

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