Tropical Medicine and International Health
doi:10.1111/tmi.12338
volume 19 no 9 pp 1096–1104 september 2014
Control of clonorchiasis in Korea: effectiveness of health education for community leaders and individuals in an endemic area Jin-Kyoung Oh1, Min Kyung Lim1, E. Hwa Yun1, Heeyoun Cho1, Eun Young Park1, Min-Ho Choi2, Hai-Rim Shin3 and Sung-Tae Hong2 1 Division of Cancer Prevention, National Cancer Control Institute, National Cancer Center, Gyeounggi-do, Korea 2 Department of Parasitology and Tropical Medicine and Institute of Endemic Diseases, Seoul National University College of Medicine, Seoul, Korea 3 Noncommunicable Diseases and Health Promotion, World Health Organization Western Pacific Regional Office, Manila, Philippines
Abstract
objectives To develop effective intervention programmes to control Clonorchis sinensis infection, three interventions were evaluated in a clonorchiasis-endemic area of Korea. methods Four thousand two hundred and sixty-seven voluntary participants in Sancheong county were tested at baseline and two follow-up surveys after 1 and 3 years. Faecal samples were examined for C. sinensis eggs using the Kato-Katz method. Participants were divided into three intervention groups by areas and year recruited: national prevention programme only (mass health campaign and praziquantel treatment) for Group A; health education for community leaders added for Group B; and individual health education added for Group C. results The prevalence of C. sinensis infection fell substantially in all three intervention groups between baseline and 3-year follow-up: from 31.1% to 14.9% in Group A, from 29.6% to 6.8% in Group B and from 21.9% to 8.6% in Group C. The control effectiveness was highest in Group B with 76.8%. The new infection rate was 16.3%, 12.8% and 7.6% in Group A, B and C, respectively. The reinfection rate was lower in Group B (3.8%) than Group C (12.2%). conclusions To control C. sinensis infection in endemic areas of Korea, health education for community leaders or individuals on prevention of C. sinensis infection should be added to national control programmes. keywords Clonorchis sinensis, control effectiveness, endemicity, field intervention, health education, praziquantel
Introduction Clonorchis sinensis is a liver fluke that infects humans and is widely prevalent in East Asia. An estimated 20 million people are infected (Hong & Fang 2012), 1 million of whom live in Korea (Kim et al. 2009a). Clonorchiasis is an inflammatory disease of the biliary tract, but most cases are asymptomatic. Only a fraction of people suffer from subjective symptoms, such as bile duct obstruction, stone formation, pyogenic cholangitis, abscess formation and biliary cirrhosis (Hong 2003a; Hong & Fang 2012). C. sinensis has also been classified as carcinogenic to humans by the International Agency for Research on Cancer (Group 1 biological agent; Bouvard et al. 2009); its most serious outcome is cholangiocarcinoma. In Korea, approximately 10% of 1096
cholangiocarcinomas are caused by chronic C. sinensis infection (Shin et al. 2010). The introduction of chemotherapy for C. sinensis infection using praziquantel in the 1980s was expected to control clonorchiasis in Korea (Rim et al. 1981; Hong 2003a). However, despite the effective use of praziquantel treatment (Seo et al. 1983), C. sinensis infection remains common in Korea. Nationwide surveys of intestinal parasitic infections revealed no drop in the average prevalence of C. sinensis infection (i.e., 2.6% in 1981 and 2.4% in 2004; Kim et al. 2009b). In some areas of the river basins in Korea, the prevalence is especially high around 30% (Lim et al. 2006; Shin et al. 2010). As a national control programme, mass health campaigns aimed at changing risk behaviours for C. sinensis infection, such as raw freshwater fish intake, have been
© 2014 John Wiley & Sons Ltd
Tropical Medicine and International Health
volume 19 no 9 pp 1096–1104 september 2014
J.-K. Oh et al. Clonorchis sinensis control in Korea
implemented, and praziquantel treatment is offered for infected cases, which were identified in mass screening with the stool examination on eggs of C. sinensis, in endemic areas of Korea. However, the effectiveness of these control measures of clonorchiasis is questionable, and the intervention programmes that have been implemented are in need of evaluation in order to improve intervention programmes to control C. sinensis infection. In this context, we conducted two intensive health education programmes, one to community leaders, and the other to individuals, which focused on the risks associated with repeated C. sinensis infection, including cholangiocarcinoma and praziquantel treatment, and compared their effects with the reference group, in which only praziquantel treatment and mass health campaigns with posters were used as a national control programme.
Stool examination and treatment Individual faecal samples were microscopically examined using the Kato-Katz method to detect and count C. sinensis eggs (Hong et al. 2003b). Clonorchis sinensis infection was confirmed by the detection of C. sinensis eggs. Eggs per gram of faeces (EPG) was used as an index of intensity of infection: light (EPG 1–500), moderate (EPG 501–2000) and heavy (EPG 2001 or more; Choi et al. 2005). Staff at the public health centre in Sancheong-gun distributed three doses of praziquantel (25 mg/kg, Distocideâ; Shin Poong Pharmaceutical Co., Ltd., Seoul, Korea) to the infected participants for free and explained how to take the drug according to the standard regimen for clonorchiasis (i.e. that doses were to be taken at 5-h intervals; Rim et al. 1981). The praziquantel treatment at baseline and followup was part of the ongoing national intervention programme for the prevention of C. sinensis infection.
Methods Study area and participants Sancheong County, with a population of 35 015 (16 994 male) of mainly farmers, in Gyeongsangnam Province is a rural area in the southeastern part of the Korea. The Nakdong River is one of Korea’s largest rivers, and its several branches flow through Sancheong. Most of these river basins provide good habitats for intermediate hosts of C. sinensis. Freshwater fish are the second intermediate host of C. sinensis, with water snails being the first intermediate host. The prevalence of C. sinensis infection in the population residing by the river basins of the Nakdong-gang was 40.2% in 1980 (Seo et al. 1981) and 30.6% in 2006 (Cho et al. 2008). In 2004–2010, we recruited and followed up 4681 inhabitants aged 30 years or over and residing in Sancheong as a part of population-based prospective cohort study, the details of which have been described previously (Yoo et al. 2002; Oh et al. 2012). All study subjects voluntarily participated in this study and signed an informed consent form. A trained research assistant interviewed each participant using a structured questionnaire, by which information on demographic characteristics, habits of alcohol drinking and tobacco smoking, dietary habits including raw freshwater fish intake and disease history was collected. Faecal samples were also collected for laboratory examination. After excluding 414 participants without a C. sinensis test result at baseline, 4267 participants (1660 men and 2607 women) were included in the final analysis. The study protocol was approved by the Institutional Review Board of the National Cancer Center of Korea.
© 2014 John Wiley & Sons Ltd
Intervention strategies Baseline measures for a population-based cohort study were taken by town of residence and each year from 2004 to 2010. During and after the baseline measures, different interventions were applied to three groups which were differentiated by year of recruitment and town of residence (Figure 1). • Group A: baseline survey and stool examination conducted from 19th to 23th July in 2004, intervention with praziquantel treatment for clonorchiasis and mass health campaigns with posters which is a part of the national intervention programme aimed at decreasing C. sinensis infection (town of Saengcho). • Group B: baseline survey and stool examination conducted from 23th November to 2nd December in 2005 and from 24th July to 2nd August in 2006, intervention with health education for community leaders about prevention of C. sinensis infection added to national intervention programmes (towns of Sancheong, Geumseo and Obu). • Group C: baseline survey and stool examination conducted from 2nd to 6th July in 2007, from 30th June to 4th July in 2008, from 6th July to 25th August in 2009 and from 28th June to 2nd July in 2010, intervention with individual health education about prevention of C. sinensis infection added to national intervention programme (towns of Sinan, Samjang, Sicheon, Sindeung, Chahwang, Danseong and Saengbiryang). The health education programmes for community leaders and the individuals used in the present study focused on the risks associated with repeated C. sinensis 1097
Tropical Medicine and International Health
volume 19 no 9 pp 1096–1104 september 2014
J.-K. Oh et al. Clonorchis sinensis control in Korea
Time line
Group A Current national control program (mass health campaigns and praziquantel treatment)
Group B: Current national control program + health education for community leaders
Group C: Current national control program + health education for individuals
Voluntary participation in baseline survey for population based cohort establishment Base line (time 0)
1 year follow−up
a
b
c
2005 − 2006
b
2006 − 2007
2004
2005
c
a
b
e
2007 − 2010
c
f
d
c
2008 − 2011
a
b
c d b
b
c
Measurement of outcomes d 3 year follow−up
2007 b
c
2008 − 2009
d b
c
2010 − 2013
d b
c
Measurement of outcomes a
A structured questionnaire completed by participants to collect information on general characteristics and potential risks of C. sinensis infection at the baseline
b
Fecal samples collected from participants and examined to detect C. sinensis eggs using the Kato−Katz method
b
Fecal samples collected from participants and examined to detect C. sinensis eggs using the Kato−Katz method. However, data are not available because they were not provided by study group but by health center and county hospital as service their own.
c
Application of national control program in endemic area of Korea (mass health cam paigns and praziquantel treatment for infected cases)
d
Invitation letter for participants to have stool exam.
e
Health education for community leaders consisted of a lecture, given by experts, as well as educational materials such as leaflets and video−on−demand.
f
Individual health education conducted by trained nurses using education materials such as posters and leaflets
infection, including cholangiocarcinoma, and explained the necessity of changing behaviour, such as avoiding raw freshwater fish consumption, which would prevent C. sinensis infection. Health education for community leaders consisted of a 1-h lecture given by experts from the National Cancer Center and Seoul National University and educational materials such as leaflets and video-on-demand. Community leaders were also asked to deliver the contents of the health education programme to the residents of their community and to advocate avoiding unhealthy behaviour such as eating raw freshwater fish. Individual health education consisted of one 1098
Figure 1 Graphical depicting of three interventions for Clonorchis sinensis infection.
time face-to-face meetings for 5–10 min with nurses and public health practitioners, who were trained by experts from the National Cancer Center and Seoul National University, and posters and leaflets. Follow-up survey Follow-up was conducted among the 4267 participants 1 and 3 years after baseline survey on a voluntary basis. At each follow-up survey, faecal samples were collected and examined after delivering invitation letter by mail for participation, and praziquantel treatment was provided
© 2014 John Wiley & Sons Ltd
Tropical Medicine and International Health
volume 19 no 9 pp 1096–1104 september 2014
J.-K. Oh et al. Clonorchis sinensis control in Korea
to infected participants. For Group A, 1-year follow-up of free stool examination and praziquantel treatment were not provided by the study group but by health centres and a county hospital as service of their own. Therefore, the results of stool examination for the 1-year follow-up of Group A were not available to us. Statistical analysis The effectiveness of the three interventions was defined according to the equation for control effectiveness proposed by Choi et al. 2010: [(prevalence at baseline prevalence at follow-up)/prevalence at baseline]. To identify the risk factor of C. sinensis infection among all participants and to compare the effectiveness of each intervention relative to that of Group A, the prevalence, odds ratios (OR) and 95% confidence intervals (CI) were calculated using a multivariate logistic regression model, adjusted for age, sex and all other variables at baseline. New C. sinensis infection was defined as the infection detected at 1-year or 3-year follow-up among participants without C. sinensis infection at baseline, respectively. Clonorchis sinensis reinfection was defined as the infection detected at 3-year follow-up among participants who were infected with C. sinensis at baseline, but showed no evidence of infection at 1-year follow-up. Statistical analyses were performed using SAS software for Windows version 9.2 (SAS Institute, Cary, NC, USA). Results Table 1 shows the general characteristics of the study participants. They are mostly farmers and only 14.4% of them were educated in high school or more. The rate of C. sinensis infection at baseline, ever history of C. sinensis infection and ever experience of raw freshwater fish intake was 28.1%, 24.4% and 21.0%, respectively. Of the 4267 participants included at baseline, 33.6% and 44.7% participated in 1- and 3-year follow-up, respectively (Table 1). The general characteristics of participants such as age, sex, education, occupation and the rate of C. sinensis infection were different between baseline and follow-up (P = 0.015). The differences between participants’ general characteristics such as education, smoking, alcohol drinking, occupation, history of C. sinensis infection, raw freshwater fish intake and C. sinensis infection at the baseline are compared between intervention groups in Table 2. Table 3 shows ORs for C. sinensis infection by sex, age, alcohol consumption, raw freshwater fish intake and intervention group at the baseline. Significantly increased ORs were found for male sex (OR = 1.7; 95% © 2014 John Wiley & Sons Ltd
CI = 1.4–2.1), age group 50–60 years (OR = 1.3; 95% CI = 1.1–1.7) and 60–70 (OR = 1.4; 95% CI = 1.1–1.7) years, drinking 24 g of alcohol or more per day (OR = 1.3; 95% CI = 1.0–1.6), raw freshwater fish intake (OR = 1.6; 95% CI = 1.3–1.9) and belonging to intervention Group A (OR = 1.5; 95% CI = 1.2–2.0) and B (OR = 1.4; 95% CI = 1.2–1.7) Multiple logistic regression analyses, adjusting for age and all other listed variables, were applied as appropriate. Table 4 shows the age-standardised prevalence of C. sinensis infection by intervention group at baseline, 1- and 3-year follow-up. The prevalence of C. sinensis infection fell substantially in all intervention groups. At the 3-year follow-up, the prevalence of C. sinensis infection was highest in Group A and lowest in Group B. In Group C, the prevalence was lower than in Group A or Group B at 1-year follow-up, but slightly increased at the 3-year follow-up (Table 4). Even though high prevalence of C. sinensis infection was shown among study participants, the intensity of infection was relatively low. Of participants, 86.4% with C. sinensis had light infection (i.e., EPG ≤ 500), and the mean EPG among infected participants dropped to 81.6 in group B and 79.6 in group C at the 3-year follow-up. In Groups A, B and C, 16.3%, 12.8% and 7.6%, respectively, showed new infections. As shown in Figure 2, the new infection rate was significantly higher in participants who reported raw freshwater fish intake than in participants who did not (P < 0.001). In addition, the new infection rate decreased much more among participants who reported no raw freshwater fish consumption when health education programmes were applied. Among participants who reported no raw freshwater fish intake, the new infection rate was the lowest when the individual health education programme was applied. The reinfection rate was lower in Group B (3.8%) than Group C (12.2%) and was not significantly different by history of raw freshwater fish intake (data not shown). Discussion Parasitic infection has been dramatically decreased in Korea, due to an improved social infrastructure, national economy, environmental and individual sanitation and government-driven mass chemotherapy. In particular, the successful control of helminth, as demonstrated by the reduction of overall positivity for intestinal helminth eggs from 84.3% (Ascaris lumbricoides 58.2%, Trichuris trichiura 65.4%, and hookworms 10.7%) in 1971 to 4.3% (A. lumbricoides 0.03%, T. trichiura 0.02%, and hookworms 0%) in 2004, suggested that the mass health 1099
Tropical Medicine and International Health
volume 19 no 9 pp 1096–1104 september 2014
J.-K. Oh et al. Clonorchis sinensis control in Korea
Table 1 General characteristics and presence of Clonorchis sinensis eggs at baseline and follow-up Baseline
Parameters Mean age, years (SD) Sex Male Female Marital status Married Widowed Other§ Education None Primary or middle school High school or more Smoking status Non-smoker Ex-smoker Current smoker Alcohol drinking Non-drinkers
doi:10.1111/tmi.12338
volume 19 no 9 pp 1096–1104 september 2014
Control of clonorchiasis in Korea: effectiveness of health education for community leaders and individuals in an endemic area Jin-Kyoung Oh1, Min Kyung Lim1, E. Hwa Yun1, Heeyoun Cho1, Eun Young Park1, Min-Ho Choi2, Hai-Rim Shin3 and Sung-Tae Hong2 1 Division of Cancer Prevention, National Cancer Control Institute, National Cancer Center, Gyeounggi-do, Korea 2 Department of Parasitology and Tropical Medicine and Institute of Endemic Diseases, Seoul National University College of Medicine, Seoul, Korea 3 Noncommunicable Diseases and Health Promotion, World Health Organization Western Pacific Regional Office, Manila, Philippines
Abstract
objectives To develop effective intervention programmes to control Clonorchis sinensis infection, three interventions were evaluated in a clonorchiasis-endemic area of Korea. methods Four thousand two hundred and sixty-seven voluntary participants in Sancheong county were tested at baseline and two follow-up surveys after 1 and 3 years. Faecal samples were examined for C. sinensis eggs using the Kato-Katz method. Participants were divided into three intervention groups by areas and year recruited: national prevention programme only (mass health campaign and praziquantel treatment) for Group A; health education for community leaders added for Group B; and individual health education added for Group C. results The prevalence of C. sinensis infection fell substantially in all three intervention groups between baseline and 3-year follow-up: from 31.1% to 14.9% in Group A, from 29.6% to 6.8% in Group B and from 21.9% to 8.6% in Group C. The control effectiveness was highest in Group B with 76.8%. The new infection rate was 16.3%, 12.8% and 7.6% in Group A, B and C, respectively. The reinfection rate was lower in Group B (3.8%) than Group C (12.2%). conclusions To control C. sinensis infection in endemic areas of Korea, health education for community leaders or individuals on prevention of C. sinensis infection should be added to national control programmes. keywords Clonorchis sinensis, control effectiveness, endemicity, field intervention, health education, praziquantel
Introduction Clonorchis sinensis is a liver fluke that infects humans and is widely prevalent in East Asia. An estimated 20 million people are infected (Hong & Fang 2012), 1 million of whom live in Korea (Kim et al. 2009a). Clonorchiasis is an inflammatory disease of the biliary tract, but most cases are asymptomatic. Only a fraction of people suffer from subjective symptoms, such as bile duct obstruction, stone formation, pyogenic cholangitis, abscess formation and biliary cirrhosis (Hong 2003a; Hong & Fang 2012). C. sinensis has also been classified as carcinogenic to humans by the International Agency for Research on Cancer (Group 1 biological agent; Bouvard et al. 2009); its most serious outcome is cholangiocarcinoma. In Korea, approximately 10% of 1096
cholangiocarcinomas are caused by chronic C. sinensis infection (Shin et al. 2010). The introduction of chemotherapy for C. sinensis infection using praziquantel in the 1980s was expected to control clonorchiasis in Korea (Rim et al. 1981; Hong 2003a). However, despite the effective use of praziquantel treatment (Seo et al. 1983), C. sinensis infection remains common in Korea. Nationwide surveys of intestinal parasitic infections revealed no drop in the average prevalence of C. sinensis infection (i.e., 2.6% in 1981 and 2.4% in 2004; Kim et al. 2009b). In some areas of the river basins in Korea, the prevalence is especially high around 30% (Lim et al. 2006; Shin et al. 2010). As a national control programme, mass health campaigns aimed at changing risk behaviours for C. sinensis infection, such as raw freshwater fish intake, have been
© 2014 John Wiley & Sons Ltd
Tropical Medicine and International Health
volume 19 no 9 pp 1096–1104 september 2014
J.-K. Oh et al. Clonorchis sinensis control in Korea
implemented, and praziquantel treatment is offered for infected cases, which were identified in mass screening with the stool examination on eggs of C. sinensis, in endemic areas of Korea. However, the effectiveness of these control measures of clonorchiasis is questionable, and the intervention programmes that have been implemented are in need of evaluation in order to improve intervention programmes to control C. sinensis infection. In this context, we conducted two intensive health education programmes, one to community leaders, and the other to individuals, which focused on the risks associated with repeated C. sinensis infection, including cholangiocarcinoma and praziquantel treatment, and compared their effects with the reference group, in which only praziquantel treatment and mass health campaigns with posters were used as a national control programme.
Stool examination and treatment Individual faecal samples were microscopically examined using the Kato-Katz method to detect and count C. sinensis eggs (Hong et al. 2003b). Clonorchis sinensis infection was confirmed by the detection of C. sinensis eggs. Eggs per gram of faeces (EPG) was used as an index of intensity of infection: light (EPG 1–500), moderate (EPG 501–2000) and heavy (EPG 2001 or more; Choi et al. 2005). Staff at the public health centre in Sancheong-gun distributed three doses of praziquantel (25 mg/kg, Distocideâ; Shin Poong Pharmaceutical Co., Ltd., Seoul, Korea) to the infected participants for free and explained how to take the drug according to the standard regimen for clonorchiasis (i.e. that doses were to be taken at 5-h intervals; Rim et al. 1981). The praziquantel treatment at baseline and followup was part of the ongoing national intervention programme for the prevention of C. sinensis infection.
Methods Study area and participants Sancheong County, with a population of 35 015 (16 994 male) of mainly farmers, in Gyeongsangnam Province is a rural area in the southeastern part of the Korea. The Nakdong River is one of Korea’s largest rivers, and its several branches flow through Sancheong. Most of these river basins provide good habitats for intermediate hosts of C. sinensis. Freshwater fish are the second intermediate host of C. sinensis, with water snails being the first intermediate host. The prevalence of C. sinensis infection in the population residing by the river basins of the Nakdong-gang was 40.2% in 1980 (Seo et al. 1981) and 30.6% in 2006 (Cho et al. 2008). In 2004–2010, we recruited and followed up 4681 inhabitants aged 30 years or over and residing in Sancheong as a part of population-based prospective cohort study, the details of which have been described previously (Yoo et al. 2002; Oh et al. 2012). All study subjects voluntarily participated in this study and signed an informed consent form. A trained research assistant interviewed each participant using a structured questionnaire, by which information on demographic characteristics, habits of alcohol drinking and tobacco smoking, dietary habits including raw freshwater fish intake and disease history was collected. Faecal samples were also collected for laboratory examination. After excluding 414 participants without a C. sinensis test result at baseline, 4267 participants (1660 men and 2607 women) were included in the final analysis. The study protocol was approved by the Institutional Review Board of the National Cancer Center of Korea.
© 2014 John Wiley & Sons Ltd
Intervention strategies Baseline measures for a population-based cohort study were taken by town of residence and each year from 2004 to 2010. During and after the baseline measures, different interventions were applied to three groups which were differentiated by year of recruitment and town of residence (Figure 1). • Group A: baseline survey and stool examination conducted from 19th to 23th July in 2004, intervention with praziquantel treatment for clonorchiasis and mass health campaigns with posters which is a part of the national intervention programme aimed at decreasing C. sinensis infection (town of Saengcho). • Group B: baseline survey and stool examination conducted from 23th November to 2nd December in 2005 and from 24th July to 2nd August in 2006, intervention with health education for community leaders about prevention of C. sinensis infection added to national intervention programmes (towns of Sancheong, Geumseo and Obu). • Group C: baseline survey and stool examination conducted from 2nd to 6th July in 2007, from 30th June to 4th July in 2008, from 6th July to 25th August in 2009 and from 28th June to 2nd July in 2010, intervention with individual health education about prevention of C. sinensis infection added to national intervention programme (towns of Sinan, Samjang, Sicheon, Sindeung, Chahwang, Danseong and Saengbiryang). The health education programmes for community leaders and the individuals used in the present study focused on the risks associated with repeated C. sinensis 1097
Tropical Medicine and International Health
volume 19 no 9 pp 1096–1104 september 2014
J.-K. Oh et al. Clonorchis sinensis control in Korea
Time line
Group A Current national control program (mass health campaigns and praziquantel treatment)
Group B: Current national control program + health education for community leaders
Group C: Current national control program + health education for individuals
Voluntary participation in baseline survey for population based cohort establishment Base line (time 0)
1 year follow−up
a
b
c
2005 − 2006
b
2006 − 2007
2004
2005
c
a
b
e
2007 − 2010
c
f
d
c
2008 − 2011
a
b
c d b
b
c
Measurement of outcomes d 3 year follow−up
2007 b
c
2008 − 2009
d b
c
2010 − 2013
d b
c
Measurement of outcomes a
A structured questionnaire completed by participants to collect information on general characteristics and potential risks of C. sinensis infection at the baseline
b
Fecal samples collected from participants and examined to detect C. sinensis eggs using the Kato−Katz method
b
Fecal samples collected from participants and examined to detect C. sinensis eggs using the Kato−Katz method. However, data are not available because they were not provided by study group but by health center and county hospital as service their own.
c
Application of national control program in endemic area of Korea (mass health cam paigns and praziquantel treatment for infected cases)
d
Invitation letter for participants to have stool exam.
e
Health education for community leaders consisted of a lecture, given by experts, as well as educational materials such as leaflets and video−on−demand.
f
Individual health education conducted by trained nurses using education materials such as posters and leaflets
infection, including cholangiocarcinoma, and explained the necessity of changing behaviour, such as avoiding raw freshwater fish consumption, which would prevent C. sinensis infection. Health education for community leaders consisted of a 1-h lecture given by experts from the National Cancer Center and Seoul National University and educational materials such as leaflets and video-on-demand. Community leaders were also asked to deliver the contents of the health education programme to the residents of their community and to advocate avoiding unhealthy behaviour such as eating raw freshwater fish. Individual health education consisted of one 1098
Figure 1 Graphical depicting of three interventions for Clonorchis sinensis infection.
time face-to-face meetings for 5–10 min with nurses and public health practitioners, who were trained by experts from the National Cancer Center and Seoul National University, and posters and leaflets. Follow-up survey Follow-up was conducted among the 4267 participants 1 and 3 years after baseline survey on a voluntary basis. At each follow-up survey, faecal samples were collected and examined after delivering invitation letter by mail for participation, and praziquantel treatment was provided
© 2014 John Wiley & Sons Ltd
Tropical Medicine and International Health
volume 19 no 9 pp 1096–1104 september 2014
J.-K. Oh et al. Clonorchis sinensis control in Korea
to infected participants. For Group A, 1-year follow-up of free stool examination and praziquantel treatment were not provided by the study group but by health centres and a county hospital as service of their own. Therefore, the results of stool examination for the 1-year follow-up of Group A were not available to us. Statistical analysis The effectiveness of the three interventions was defined according to the equation for control effectiveness proposed by Choi et al. 2010: [(prevalence at baseline prevalence at follow-up)/prevalence at baseline]. To identify the risk factor of C. sinensis infection among all participants and to compare the effectiveness of each intervention relative to that of Group A, the prevalence, odds ratios (OR) and 95% confidence intervals (CI) were calculated using a multivariate logistic regression model, adjusted for age, sex and all other variables at baseline. New C. sinensis infection was defined as the infection detected at 1-year or 3-year follow-up among participants without C. sinensis infection at baseline, respectively. Clonorchis sinensis reinfection was defined as the infection detected at 3-year follow-up among participants who were infected with C. sinensis at baseline, but showed no evidence of infection at 1-year follow-up. Statistical analyses were performed using SAS software for Windows version 9.2 (SAS Institute, Cary, NC, USA). Results Table 1 shows the general characteristics of the study participants. They are mostly farmers and only 14.4% of them were educated in high school or more. The rate of C. sinensis infection at baseline, ever history of C. sinensis infection and ever experience of raw freshwater fish intake was 28.1%, 24.4% and 21.0%, respectively. Of the 4267 participants included at baseline, 33.6% and 44.7% participated in 1- and 3-year follow-up, respectively (Table 1). The general characteristics of participants such as age, sex, education, occupation and the rate of C. sinensis infection were different between baseline and follow-up (P = 0.015). The differences between participants’ general characteristics such as education, smoking, alcohol drinking, occupation, history of C. sinensis infection, raw freshwater fish intake and C. sinensis infection at the baseline are compared between intervention groups in Table 2. Table 3 shows ORs for C. sinensis infection by sex, age, alcohol consumption, raw freshwater fish intake and intervention group at the baseline. Significantly increased ORs were found for male sex (OR = 1.7; 95% © 2014 John Wiley & Sons Ltd
CI = 1.4–2.1), age group 50–60 years (OR = 1.3; 95% CI = 1.1–1.7) and 60–70 (OR = 1.4; 95% CI = 1.1–1.7) years, drinking 24 g of alcohol or more per day (OR = 1.3; 95% CI = 1.0–1.6), raw freshwater fish intake (OR = 1.6; 95% CI = 1.3–1.9) and belonging to intervention Group A (OR = 1.5; 95% CI = 1.2–2.0) and B (OR = 1.4; 95% CI = 1.2–1.7) Multiple logistic regression analyses, adjusting for age and all other listed variables, were applied as appropriate. Table 4 shows the age-standardised prevalence of C. sinensis infection by intervention group at baseline, 1- and 3-year follow-up. The prevalence of C. sinensis infection fell substantially in all intervention groups. At the 3-year follow-up, the prevalence of C. sinensis infection was highest in Group A and lowest in Group B. In Group C, the prevalence was lower than in Group A or Group B at 1-year follow-up, but slightly increased at the 3-year follow-up (Table 4). Even though high prevalence of C. sinensis infection was shown among study participants, the intensity of infection was relatively low. Of participants, 86.4% with C. sinensis had light infection (i.e., EPG ≤ 500), and the mean EPG among infected participants dropped to 81.6 in group B and 79.6 in group C at the 3-year follow-up. In Groups A, B and C, 16.3%, 12.8% and 7.6%, respectively, showed new infections. As shown in Figure 2, the new infection rate was significantly higher in participants who reported raw freshwater fish intake than in participants who did not (P < 0.001). In addition, the new infection rate decreased much more among participants who reported no raw freshwater fish consumption when health education programmes were applied. Among participants who reported no raw freshwater fish intake, the new infection rate was the lowest when the individual health education programme was applied. The reinfection rate was lower in Group B (3.8%) than Group C (12.2%) and was not significantly different by history of raw freshwater fish intake (data not shown). Discussion Parasitic infection has been dramatically decreased in Korea, due to an improved social infrastructure, national economy, environmental and individual sanitation and government-driven mass chemotherapy. In particular, the successful control of helminth, as demonstrated by the reduction of overall positivity for intestinal helminth eggs from 84.3% (Ascaris lumbricoides 58.2%, Trichuris trichiura 65.4%, and hookworms 10.7%) in 1971 to 4.3% (A. lumbricoides 0.03%, T. trichiura 0.02%, and hookworms 0%) in 2004, suggested that the mass health 1099
Tropical Medicine and International Health
volume 19 no 9 pp 1096–1104 september 2014
J.-K. Oh et al. Clonorchis sinensis control in Korea
Table 1 General characteristics and presence of Clonorchis sinensis eggs at baseline and follow-up Baseline
Parameters Mean age, years (SD) Sex Male Female Marital status Married Widowed Other§ Education None Primary or middle school High school or more Smoking status Non-smoker Ex-smoker Current smoker Alcohol drinking Non-drinkers
