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Original Article
 Prevalence and Risk Factors of Clonorchiasis among the Populations Served by Primary Healthcare Posts along Five Major Rivers in South Korea
Kyung Ja Junea, Shin Hyeong Chob, Won Ja Leeb, Chunmi Kimc, Kyung-Soon Parkd
Osong Public Health and Research Perspectives 2013;4(1):21-26.
DOI: https://doi.org/10.1016/j.phrp.2012.12.002
Published online: February 28, 2013

aDepartment of Nursing, Soonchunhyang University, Asan, Korea.

bDivision of Malaria and Parasitic Diseases, Korea National Institute of Health, Osong, Korea.

cDepartment of Nursing, Sunmoon University, Asan, Korea.

dDepartment of Nursing, Chungcheong University, Cheongju, Korea.

*Corresponding author. E-mail: spring4cmk@gmail.com
1These authors equally contributed as the first authors.
• Received: December 10, 2012   • Revised: December 14, 2012   • Accepted: December 21, 2012

Copyright ©2013, Korea Centers for Disease Control and Prevention

This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/3.0) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.

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  • Objectives:
    Clonorchiasis is an infectious disease caused by the Chinese liver fluke Clonorchis sinensis. In this study, we investigated the prevalence and risk factors of clonorchiasis among the populations served by primary healthcare posts along five major rivers in South Korea.
  • Methods:
    Forty primary healthcare posts that are located less than 5 km from one of the five rivers were selected from 26 counties. For the purpose of the survey, community health practitioners selected the nearest villages from the riversides in their own catchment area. From January to May 2009, a total of 2788 stool samples were collected and examined using the formalin–ether sedimentation technique. Village inhabitants were also interviewed by means of questionnaires in order to obtain information on potential risk factors.
  • Results:
    The prevalence rates of clonorchiasis at various river basins were as follows: Seomjin River, 21.3%; Nakdong River, 13.5%; Geum River, 9.2%; Han River, 7.6%; and Yeongsan River, 4.9%. The total number of people infected with C. sinensis was 329 (11.3%). By gender, 14.3% of males and 7.6% of females were infected. In case of both males and females, the prevalence rate was highest in those in their 40s. Consumption of raw freshwater fish was confirmed as a risk factor based on a logistic regression analysis.
  • Conclusion:
    The present findings suggest that clonorchiasis is still highly prevalent among the inhabitants of riverside areas in southern Korea, and, accordingly, it is necessary to implement a systematic control program in the endemic areas.
  • Keywords: Clonorchis sinensis; prevalence; primary healthcare services; risk factors
Korea is considered to be a successful country with regard to the parasite control programs that it has implemented during the country’s period of rapid economic growth over the last 50 years. National surveys and group medication programs have been conducted periodically, and health education and campaigns have been executed widely for the prevention of parasite infection. As a consequence of these measures, the intestinal parasite infection rate decreased to 3.7% in 2004 [1]. However, the prevalence of Clonorchis sinensis has not decreased since the 1990s and has been endemic, particularly in riverside areas. According to the results of a national survey conducted using a stratified sample, the prevalence rate was 2.9% in 2004; however, a survey of endemic areas conducted in 2007 indicated that the rate was as high as 9.5% on average in the riverside areas surveyed [2].
In order to lower the C. sinensis positive rate, it is necessary to manage riverside endemic areas continuously. In the 1990s, medication was made available to 100 rural residents in Korea for 3.5 years at 6-month intervals and, as a result, the C. sinensis positive rate decreased [3]. For example, as a consequence of 6 years’ continuous management at Gokseong-gun in the Seomjin River basin, the positive rate decreased from 26.9% to 13.1% [4]. Similarly, in China, the positive rate has decreased as a consequence of annual examinations and medication programs in areas showing an average C. sinensis positive rate. However, despite these measures, cases of reinfection and unsuccessful treatment have been reported and newly infected persons have also been identified [5].
According to the results of previous studies, the major risk factor of C. sinensis infection is the consumption of raw freshwater fish, and the risk of infection is highest in middle-aged men and higher in rural areas than in urban areas [6,7]. An obvious means of reducing infection would be to change such dietary habits; however, the habit of raw freshwater fish consumption cannot be changed in a short period of time. Moreover, successful administration of the drug praziquantel is difficult; it is also difficult to change the drinking habits of middle-aged men. Accordingly, accurate knowledge should be spread through health education, and control strategies should be developed continuously in order to manage drug administration for infected persons, prevent reinfection, and change community culture.
This study was conducted as a baseline survey with the aim of developing a program for continuous C. sinensis control, based on primary healthcare posts that provide primary healthcare services to residents in riverside areas where C. sinensis is endemic.
2.1. Survey areas
Among 26 counties in South Korea, we selected 40 primary healthcare posts that are located less than 5 km from one of the following five major rivers: Geum, Han, Nakdong, Seomjin, and Yeongsan. Community health practitioners selected the nearest villages from the riversides in their own catchment area. A total of 2788 participants were screened for C. sinensis and some were interviewed in selected localities. The study was undertaken from January to May 2009.
2.2. Stool collection and examination
Informed consent was obtained from all the participants, and the study protocol was approved by the IRB committee of Soonchunhyang University Hospital.
Stool specimens were collected in plastic containers and transferred to the laboratory of the National Institutes of Health. The formalin–ether sedimentation technique was used to identify the presence of the C. sinensis eggs. 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 using the formalin–ether concentration technique and examined for parasites in the laboratory.
2.3. Questionnaire survey
We also conducted a questionnaire survey of the participants. The questionnaire included questions on sociodemographic characteristics, health behaviors, consumption of raw freshwater fish, and past history of C. sinensis infection. Each participant was interviewed by a community health practitioner working in his/her village.
2.4. Statistical analysis
Descriptive statistics were applied to determine the prevalence rates of clonorchiasis. Unconditional multiple logistic regression was used to evaluate odds ratios and 95% confidence intervals of being egg positive according to various characteristics (Table 1). Statistical analyses were performed using SPSS WIN 17.0 software.
Among the 2,614 persons surveyed, 300 (11.4%) were found to be positive (Table 2). The positive rate was higher in men (14.8%) than in women (7.8%). Categorized according to riverside area, the rate was highest along the Seomjin River (21.5%), followed by the rivers Nakdong (13.8%), Geum (9.3%), Han (7.9%), and Yeongsan (4.8%). Of the primary healthcare posts, four along the Seomjin River and one by the Han River recorded a positive rate of greater than 30%, with the Geumcheon Health Center by the Seomjin River showing the highest positive rate (38.4%).
Among men, the positive rate was highest among those in their 40s (17.6%), and was higher in those with smoking experience (16.6%) than in those without it (Table 3). In addition, the positive rate was higher in those drinking four or more times a week (17.8%) than in those drinking less frequently. The rate was also higher in those who had consumed raw freshwater fish (16.3%) than in those who had not, and was somewhat higher in those who replied that they would not change their habit of consuming raw fish (16.5%) than in those who intended to change the habit. It was also somewhat higher in those with a previous experience of infection. Drinking frequency and consumption of raw freshwater fish were found to be the factors contributing to a statistically significant difference in the positive rate.
In contrast, among women, the positive rate was higher in those in their 60s (9.3%) than in those in other age groups and in those with smoking experience (14.3%) than in those without it (Table 4). With respect to drinking frequency, the positive rate was highest in those drinking two to four times a month (12.2%). Further, the rate was as high as 12.5% in those with a previous experience of infection, and was significantly higher in those with the habit of raw freshwater fish consumption and in those who indicated that they would not change the habit.
Logistic regression analysis that included all the demographic characteristics and behavioral characteristics indicated that the risk of infection was 2.58 times higher in those with the habit of raw freshwater fish consumption than in those without the habit.
The overall positive rate in the survey areas of the present study is similar to that recorded in a 2007 survey conducted in endemic areas in the basins of four major South Korean rivers [2]. As a result of continuous management at Gokseong-gun in the basin of the Seomjin River, the positive rate was reported to have decreased from 25.05% in 1999 to 10.4% in 2005 [4]; however, in the present study, the rate exceeded 30% at four of the primary healthcare posts along the Seomjin River. Moreover, although the positive rate was found to be 2.1% in Chuncheon by the Bukhan River and 7.8% in Chungju by the Namhan River [7], there was an area in the present study where the positive rate exceeded 30%. Thus, there were significant differences among different river basins and even among areas within the same river basin. This is probably because, in contrast to previous studies, our study sampled residents living close to the rivers and examined only a small number of individuals based on their proximity to primary healthcare posts [8]. Accordingly, in order to survey the current state of C. sinensis infection, it is considered more desirable to select high-risk areas showing a markedly high positive rate among the primary healthcare posts of cities, counties, and wards, and to monitor changes in the positive rate of the same areas continuously, than to compare the average positive rates of various river basins.
As in previous studies, the positive rate was higher in men than in women [8]. This may be related to the Korean culture, in which drinking alcohol and consumption of raw freshwater fish are more common among men than among women; men participate in social activities that involve drinking and raw freshwater fish consumption more frequently than women [6–8]. Differences among age groups were not significant; however, attention should be paid to the finding that those in their 40s showed a somewhat higher positive rate. Because the survival period of C. sinensis is over 30 years, if infected persons are not treated adequately, they are highly likely to experience reinfection or complications [2]. Those in their70s also showed a high positive rate, probably because of unsuccessful treatment in the past or repeated reinfections. A positive rate of approximately 16% in those with a previous experience of infection indicates the possibility of reinfection. Previous studies have also reported that the positive rate is higher among the aged and, as a result of treatment effect, highest among those in their 50s and 60s, but decreases thereafter [2,6]. In both men and women, the C. sinensis positive rate varies significantly among people depending on whether they have the habit of consuming raw freshwater fish or not. This is consistent with previous reports and confirms that continuous efforts should be made to change the habit of raw freshwater fish consumption in order to prevent C. sinensis infection [2,6]. Consistently, the results of logistic analysis indicated that the habit of raw freshwater fish consumption increased the risk of C. sinensis infection by approximately 2.5 times, which is higher than that previously reported [6]. Accordingly, in community health surveys, we need to consider using the habit of raw freshwater fish consumption as a screening tool to select high-risk areas or individuals susceptible to C. sinensis infection [9,10].
According to the results presented above, prevention of C. sinensis infection may be achieved by changing individuals’ health behaviors and improving the awareness of communities. Specifically, because C. sinensis infection is closely related to the habits of drinking and raw fish consumption, it would be effective to adopt a comprehensive approach as part of the health promotion programs. Further, in order to reduce the chance of reinfection in C. sinensis-positive persons, it is necessary to enhance their compliance with treatment regimens and change their health behaviors through regular education and consultation after medication.
To date, C. sinensis control has been conducted through demonstration projects limited to some localities or nationwide centering on examination, medication, and campaigns by public health centers at the county level. However, these efforts have not succeeded in persuading residents in endemic areas to change their habit of raw fish consumption, and, consequently, they have not been successful in decreasing the C. sinensis positive rate continuously. On the basis of the results of this study, we suggest developing a program for primary healthcare posts in the high-risk areas of the five major rivers surveyed to control C. sinensis infection, execute such control programs continuously, and evaluate the effect.
Acknowledgements
This work was supported by a grant from the Korea National Institute of Health (2008-E00410-00), Ministry of Health and Welfare, Republic of Korea.

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Table 1
OR and corresponding 95% CI for the presence of C. sinensis in stools according to selected characteristics
Characteristic OR 95% CI
Gender Female Reference
Male 1.501 0.838–2.691
Age (y) ≤49 Reference
50–59 0.698 0.336–1.450
60–69 0.848 0.428–1.682
≥70 1.120 0.555–2.261
Smoking Never Reference
Ex-smoker 0.885 0.490–1.599
Current smoker 1.049 0.586–1.879
Alcohol drinking Never Reference
≤1/mo 0.621 0.316–1.219
2–4/mo 1.352 0.728–2.511
2–3/wk 1.097 0.594–2.026
≥4/wk 1.353 0.725–2.527
Raw freshwater fish consumption Never Reference
Yes 2.581 1.175–5.672
Intent to change the habit of raw freshwater consumption Yes Reference
No 0.892 0.594–1.415
Past history of C. sinensis infection Never Reference
Yes 0.944 0.630–1.339

CI = confidence interval; OR = odds ratio.

Table 2
Positive rates of C. sinensis eggs categorized by river, locality, and gender
River Localities No. examined. No. (%) of positive cases
Males Females Total
Guem-gang 1 Geumji 86 5 (6.4) 0 (0.0) 5 (5.8)
2 Dosam 70 0 (0.0) 0 (0.0) 0 (0.0)
3 Dudong 66 3 (7.3) 1 (4.0) 4 (6.0)
4 Dumo 65 1 (3.3) 0 (0.0) 1 (1.5)
5 Buri 75 17 (31.5) 1 (4.8) 18 (23.7)
6 Wondong 56 12 (46.2) 2 (6.7) 14 (24.6)
7 Jangsang 74 2 (5.9) 2 (5.0) 4 (5.4)
Subtotal 492 40 (13.7) 6 (3.0) 46 (9.3)
Han-gang 8 Boktan 50 17 (38.6) 1 (16.7) 18 (36.0)
9 Geumkwan 46 7 (16.3) 1 (33.3) 8 (17.4)
10 Haho 47 4 (20.0) 1 (3.7) 5 (10.6)
11 Hwangsan 51 1 (4.5) 3 (10.3) 4 (7.8)
12 Danglim 100 4 (6.6) 1 (2.6) 5 (5.0)
13 Dukmok 50 2 (7.4) 0 (0.0) 2 (4.0)
14 Bobat 50 1 (2.9) 0 (0.0) 1 (2.0)
15 Kwangrak 54 0 (0.0) 1 (4.3) 1 (1.9)
16 Gumchun 57 0 (0.0) 0 (0.0) 0 (0.0)
17 Suhang 50 0 (0.0) 0 (0.0) 0 (0.0)
Subtotal 555 36 (10.7) 8 (3.6) 44 (7.9)
Yeongsan-gang 18 Guemkang 50 3 (15.8) 4 (12.9) 7 (14.0)
19 Walak 52 6 (12.8) 1 (20.0) 7 (13.5)
20 Kwangam 71 3 (8.8) 1 (2.7) 4 (5.6)
21 Sinhak 47 1 (4.5) 1 (4.0) 2 (4.3)
22 Bongmyong 55 1 (5.0) 1 (2.9) 2 (3.6)
23 Juksan 93 2 (5.4) 1 (1.8) 3 (3.2)
24 sinryong 49 0 (0.0) 0 (0.0) 0 (0.0)
25 Sachang 50 0 (0.0) 0 (0.0) 0 (0.0)
26 Eungok 50 0 (0.0) 0 (0.0) 0 (0.0)
Subtotal 517 16 (6.3) 9 (3.4) 25 (4.8)
Seomjin-gang 27 Geumchun 73 15 (50.0) 13 (30.2) 28 (38.4)
28 Kyesan 50 10 (37.0) 8 (34.8) 18 (36.0)
29 Dosa 57 14 (51.9) 7 (23.3) 21 (36.8)
30 Oegok 50 8 (38.1) 9 (31.0) 17 (34.0)
31 Hachun 52 5 (22.7) 7 (23.3) 12 (23.1)
32 Bumwang 100 5 (11.1) 2 (3.6) 7 (7.0)
33 Hapgang 80 3 (8.1) 2 (4.7) 5 (6.3)
34 Aprok 46 0 (0.0) 1 (3.4) 1 (2.2)
Subtotal 508 60 (26.5) 49 (17.4) 109 (21.5)
Nakdong-gang 35 Gobong 129 5 (9.8) 3 (3.8) 8 (6.2)
36 Oryong 68 8 (21.1) 0 (0.0) 8 (11.8)
37 Yulgok 50 8 (30.8) 3 (12.5) 11 (22.0)
38 Doheung 90 3 (6.5) 0 (0.0) 3 (3.3)
39 Sinsung 94 15 (33.3) 8 (16.3) 23 (24.5)
40 Yangseo 121 11 (23.4) 12 (16.2) 23 (19.0)
Subtotal 552 50 (19.8) 26 (8.7) 76 (13.8)
Total 2624 202 (14.8) 98 (7.8) 300 (11.4)
Table 3
Differences in C. sinensis positive rates according to age and behavioral characteristics among males
Characteristic Total No. negative (%) No. positive (%) χ2 p
Age (y) ≤49 204 168 (82.4) 36 (17.6) 2.773 0.428
50–59 350 299 (85.4) 51 (14.6)
60–69 454 395 (87.0) 59 (13.0)
≥70 348 293 (84.2) 55 (15.8)
Smoking Never 330 292 (88.5) 38 (11.5) 4.154 0.125
Ex-smoker 501 418 (83.4) 83 (16.6)
Current smoker 523 443 (84.7) 80 (15.3)
Alcohol drinking Never 116 105 (90.5) 11 (9.5) 10.880 0.028
≤1/mo 91 85 (93.4) 6 (6.6)
2–4/mo 190 163 (85.8) 27 (14.2)
2–3/wk 336 280 (83.3) 56 (16.7)
≥4/wk 371 305 (82.2) 66 (17.8)
Raw freshwater fish consumption Never 219 201 (91.8) 18 (8.2) 9.325 0.002
Yes 1119 937 (83.7) 182 (16.3)
Intention to change the habit of raw freshwater consumption Yes 807 694 (86.0) 113 (14.0) 1.440 0.253
No 467 390 (83.5) 77 (16.5)
Past history of C. sinensis infection Never 359 297 (82.7) 62 (17.3) 0.164 0.735
Yes 215 175 (81.4) 40 (18.6)
Table 4
Differences in C. sinensis positive rates according to age and behavioral characteristics among females
Characteristic Total No. negative (%) No. positive (%) χ2 p
Age (y) ≤49 156 143 (91.7) 13 (8.3) 2.580 0.461
50–59 305 284 (93.1) 21 (6.9)
60–69 430 390 (90.7) 40 (9.3)
≥70 367 343 (93.5) 24 (6.5)
Smoking Never 1202 1110 (92.3) 2 (6.5) 1.345 0.510
Ex-smoker 21 18 (85.7) 3 (14.3)
Current smoker 31 29 (93.5) 2 (6.5)
Alcohol drinking Never 639 593 (92.8) 46 (7.2) 5.109 0.276
≤1/mo 342 320 (93.0) 22 (6.4)
2–4/mo 139 122 (87.8) 17 (12.2)
2–3/wk 91 84 (92.3) 7 (7.7)
≥4/wk 22 20 (90.9) 2 (9.1)
Raw freshwater fish consumption Never 445 425 (95.5) 20 (4.5) 10.367 0.001
Yes 803 726 (90.4) 97 (7.8)
Intention to change the habit of raw freshwater consumption Yes 897 840 (93.6) 57 (6.4) 10.825 0.002
No 322 283 (87.9 39 (12.1)
Past history of C. sinensis infection Negative 272 248 (91.2) 24 (8.8) 1.203 0.266
Positive 112 98 (87.5) 14 (12.5)

Figure & Data

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