• 1

    Sithithaworn P, Haswell-Elkins M, 2003. Epidemiology of Opisthorchis viverrini.Acta Trop 88 :187–194.

  • 2

    Keiser J, Utzinger J, 2005. Emerging foodborne trematodiasis. Emerg Infect Dis 11 :1507–1514.

  • 3

    Kaewpitoon N, Kaewpitoon SJ, Pengsaa P, 2008. Opisthorchiasis in Thailand: review and current status. World J Gastroenterol 14 :2297–2302.

    • Search Google Scholar
    • Export Citation
  • 4

    Traub RJ, Macaranas J, Mungthin M, Leelayoova S, Cribb T, Murrell KD, Thompson RC, 2009. A new PCR-based approach indicates the range of Clonorchis sinensis now extends to central Thailand. PLoS Negl Trop Dis 3 :e367.

    • Search Google Scholar
    • Export Citation
  • 5

    Sripa B, Kaewkes S, Sithithaworn P, Mairiang E, Laha T, Smout M, Pairojkul C, Bhudhisawasdi V, Tesana S, Thinkamrop B, Bethony JM, Loukas A, Brindley PJ, 2007. Liver fluke induces cholangiocarcinoma. PLoS Med 4 :e201.

    • Search Google Scholar
    • Export Citation
  • 6

    Sriamporn S, Pisani P, Pipitgool V, Suwanrungruang K, Kamsa-ard S, Parkin DM, 2004. Prevalence of Opisthorchis viverrini infection and incidence of cholangiocarcinoma in Khon Kaen, Northeast Thailand. Trop Med Int Health 9 :588–594.

    • Search Google Scholar
    • Export Citation
  • 7

    Jongsuksuntigul P, Imsomboon T, 2003. Opisthorchiasis control in Thailand. Acta Trop 88 :229–232.

  • 8

    Upatham ES, Viyanant V, Kurathong S, Rojborwonwitaya J, Brockelman WY, Ardsungnoen S, Lee P, Vajrasthira S, 1984. Relationship between prevalence and intensity of Opisthorchis viverrini infection, and clinical symptoms and signs in a rural community in north-east Thailand. Bull World Health Organ 62 :451–461.

    • Search Google Scholar
    • Export Citation
  • 9

    Kurathong S, Lerdverasirikul P, Wongpaitoon V, Pramoolsinsap C, Upatham ES, 1987. Opisthorchis viverrini infection in rural and urban communities in northeast Thailand. Trans R Soc Trop Med Hyg 81 :411–414.

    • Search Google Scholar
    • Export Citation
  • 10

    Kato K, Miura M, 1954. Comparative examinations. Jap J Parasitol 3 :35.

  • 11

    Truant AL, Elliott SH, Kelly MT, Smith JH, 1981. Comparison of formalin-ethyl ether sedimentation, formalin-ethyl acetate sedimentation, and zinc sulfate flotation techniques for detection of intestinal parasites. J Clin Microbiol 13 :882–884.

    • Search Google Scholar
    • Export Citation
  • 12

    Jongsuksuntigul P, Imsomboon T, 1997. The impact of a decade long opisthorchiasis control program in northeastern Thailand. Southeast Asian J Trop Med Public Health 28 :551–557.

    • Search Google Scholar
    • Export Citation
  • 13

    Sithithaworn P, Yongvanit P, Tesana S, Pairojkul C, 2007. Liver flukes. Murrell KD, Fried B, eds. Food Borne Parasitic Zoonoses: Fish and Plant-Borne Parasites. New York: Springer, 3–52.

  • 14

    Lengeler C, Utzinger J, Tanner M, 2002. Questionnaires for rapid screening of schistosomiasis in sub-Saharan Africa. Bull World Health Organ 80 :235–242.

    • Search Google Scholar
    • Export Citation
  • 15

    Steinmann P, Zhou XN, Li YL, Li HJ, Chen SR, Yang Z, Fan W, Jia TW, Li LH, Vounatsou P, Utzinger J, 2007. Helminth infections and risk factor analysis among residents in Eryuan county, Yunnan province, China. Acta Trop 104 :38–51.

    • Search Google Scholar
    • Export Citation
  • 16

    Sayasone S, Odermatt P, Phoumindr N, Vongsaravane X, Sensombath V, Phetsouvanh R, Choulamany X, Strobel M, 2007. Epidemiology of Opisthorchis viverrini in a rural district of Southern Lao PDR. Trans R Soc Trop Med Hyg 101 :40–47.

    • Search Google Scholar
    • Export Citation
  • 17

    Vichasri S, Viyanant V, Upatham ES, 1982. Opisthorchis viverrini intensity and rates of infection in cyprinoid fish from an endemic focus in northeast Thailand. Southeast Asian J Trop Med Public Health 13 :138–141.

    • Search Google Scholar
    • Export Citation
  • 18

    World Health Organization, 1995. Control of foodborne trematode infections. Report of a WHO Study Group. World Health Organ Tech Rep Ser 849 :1–157.

    • Search Google Scholar
    • Export Citation
  • 19

    Migasena P, 1982. Liver flukes relationship to dietary habits and development programs in Thailand. Patrice Jellife EF, Jellife DB, eds. Adverse Effects of Foods. New York: Plenum Press, 307–311.

  • 20

    Kruatrachue M, Chitramvong YP, Upatham ES, Vichasri S, Viyanant V, 1982. Effects of physico-chemical factors on the infection of hamsters by metacercariae of Opisthorchis viverrini.Southeast Asian J Trop Med Public Health 13 :614–617.

    • Search Google Scholar
    • Export Citation
  • 21

    Sukontason K, Methanitikorn R, Piangjai S, Choochote W, 1998. Viability of metacercariae in northern Thai traditional foods. Southeast Asian J Trop Med Public Health 29 :714–716.

    • Search Google Scholar
    • Export Citation

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

Incidence and Risk Factors of Opisthorchis viverrini Infections in a Rural Community in Thailand

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  • 1 Department of Military and Community Medicine, and Department of Parasitology, Phramongkutklao College of Medicine, Bangkok, Thailand

Opisthorchis viverrini infection is one of the major public health problems in Thailand. Although information about transmission of this parasite to humans is well established, infections are still prevalent in the northern and northeastern Thailand. Thus, prospective epidemiologic information is needed for developing more effective public health interventions. A cohort study to identify incidence and risk factors of O. viverrini infection was conducted in a rural community in Thailand during December 2002–February 2004. The incidence rate of opisthorchiasis was 21.6/100 person-years. The independent factors associated with opisthorchiasis were an age > 60 years and consuming chopped raw fish salad (Koi pla). Thus, avoiding this raw fish salad should be emphasized in the national control program.

INTRODUCTION

Human liver fluke infections, opisthorchiasis is caused by Opisthorchis viverrini and O. felineus. Clonorchiasis is an infection with Clonorchis sinensis. These liver fluke infections remain a major public health problem in different areas. Opisthorchis viverrini infection is endemic in Southeast Asia, especially in Thailand, Lao PDR, Vietnam, and Cambodia; O. felineus infection is prevalent in eastern Europe. Countries in eastern Asia including China, Japan, Korea, Taiwan, and northern Vietnam are the endemic areas of C. sinensis. 1,2 In Thailand, approximately six million persons harboring O. viverrini live in the northern and northeastern regions.3 Clonorchis sinensis infection was recently reported in central Thailand.4 Chronic infection of O. viverrini may lead to cholangiocarcinoma.5 The reported incidence of cholangiocarcinoma ranged from 93.8 to 317.6 per 100,000 person-years in Khon Kaen in northeastern Thailand, the area in which O. viverrini infection is endemic.6 An epidemiologic survey in Thailand showed that the average prevalence of opisthorchiasis in 2001 was relatively high, ranging from 9.6% to 19.3%.7 In addition, a study conducted in 2004 showed that the average prevalence of O. viverrini infection was 24.5%, ranging from 2.1% to 70.8% in various districts of Khon Kaen.6

Persons in these areas have consumed undercooked or raw animal products, in particular freshwater fish.79 Although information about fish-borne transmission of O. viverrini is well established, the outcome of public health prevention and control programs for opisthorchiasis during the past decade has not been succesful.7 Opisthorchiasis prevention campaigns focusing on avoiding the consumption of undercooked or raw freshwater fish may not be sustainably effective in Thailand. Prevalences have not been substantially reduced in highly endemic areas. Changing food consumption behaviors among the at-risk population is a difficult task in public health interventions. Several undercooked fish foods are still common among populations in northern and northeastern Thailand. Several reported risk factors showed a significant association of non-specific undercooked fish foods and acquiring O. viverrini infection. To develop more effective intervention strategies, information related to specific food consumption habits that increase the risk of acquiring opisthorchiasis is required.

Most studies of opisthorchiasis in Thailand were conducted using a cross-sectional study design, which may place limitations on obtaining unbiased risk factors. To obtain the incidence and associated risk factors of opisthorchiasis in this community, we conducted a cohort study was performed during December 2002–February 2004. The purpose of this study was to obtain information on risks associated with opisthorchiasis, including social behavior of people in the disease-endemic area.

MATERIALS AND METHODS

Study area and population.

The study was conducted at Baan Nayao village in a rural area of Chacheongsao Province, Thailand, 228 km east of Bangkok. The population of the study area was 1,524 in 2004. The village is surrounded by ponds and reservoirs, which harbor snail and fish intermediate hosts of O. viverrini. Most of the population migrated from northeastern Thailand and has lived in this area for more than 30 years. They have maintained their northeastern-style habits of eating undercooked and raw freshwater fish.

The baseline survey of O. viverrini infection was carried out in December 2002. Of 668 stool specimens, 142 (21.3%) were positive for O. viverrini infection. Those persons who were negative for O. viverrini (n = 526, 78.7%) by stool examination were invited to be enrolled into a follow-up survey in February 2004 to identify incidence and risk factors of O. viverrini infection.

Stool collection and examination.

At the baseline and follow-up surveys, a stool specimen from each participant was examined for intestinal parasites within 6 hours after collection in the field using normal saline wet preparation and Kato thick smear method. 10 Stool specimens were then examined under a light microscope for intestinal parasites, with an emphasis on O. viverrini. These specimens were then transported to the Department of Parasitology, Phramongkutklao College of Medicine, Bangkok, for the confirmation of O. viverrini infection by experienced technicians using formalin-ethyl acetate concentration technique. 11 Opisthorchis viverrini positivity was defined as the presence of O. viverrini eggs in the stool specimen examined by at least one of three methods: normal saline wet preparation, Kato thick smear, and formalin-ethyl acetate concentration technique.

Questionnaires.

Enrolled participants were interviewed using standardized questionnaires to identify the risk factors for O. viverrini infection. The questionnaire covered demographic data, socioeconomic conditions, sanitary behavior, including cooking and eating habits of several traditional fish dishes during the past 12 months, sources of fish for food preparation, sources and treatment methods of drinking water, and a history of animals contact. The questionnaire was also designed to cover traditional fish food items, which were grouped into three categories: uncooked fish, i.e., chopped raw fish salad (Koi pla); moderately fermented fish, i.e., briefly fermented fish (Pla som) and briefly fermented fish stuffed with rice (Pla faak); and completely fermented fish in a highly concentrated salt solution, i.e., raw fermented fish (Pla ra). The villagers’ interview sessions were conducted as a process of the questionnaire development to ensure the validity of the questions asked. The questionnaire has been pre-tested and used in the other previous surveys and was found to be reliable in identifying the potential food consumption exposures.

Statistical analysis.

Incidence rate per 100 person-years of observation were calculated for each category of demographic and potential risk factor variables. The association between potential risk factors and O. viverrini infection were assessed using Pearson’s chi-square test for categorical variables. A 0.05 cut-off point was used for the P value and applied in all statistical analysis. Crude relative risk (RR) and 95% confidence intervals (CIs) were calculated for O. viverrini infection and each of the other variables in a bivariate analysis. Multivariate Poisson regression analysis was performed to obtain adjusted RR and 95% CIs. All analyses were conducted using STATA/SE for Windows version 9.2 (StataCorp LP, College Station, TX).

Ethical consideration and treatment.

The research protocol was reviewed and approved by Ethical Committee of the Medical Department of the Royal Thai Army. Written informed consents were obtained from the enrolled participants or their parents for children participants after they read the information sheet and consent form. Free proper anthelminthic treatment and health education were provided for those who had intestinal parasitic infections. Opisthorchis viverrini–infected cases were treated with a single dose of praziquantel (40 mg/kg).

RESULTS

Study population.

Of 526 enrolled O. viverrini-negative participants, 258 (49.0%) were males. Agriculture (80.0%) was the main occupation. A total of 57% had education levels less than primary school. Annual household income was obtained from each family in Thai baht and converted to U.S. dollar at the rate of 40 baht/U.S. dollar. More than 9 of 10 study participants had an annual household income below the national average. The proportion of raw or undercooked fresh-water fish eating habits were as follows: consumption of briefly fermented fish (67.5%), raw fermented fish (66.3%), chopped raw fish salad (52.4%), and briefly fermented fish stuffed with rice (16.8%).

Incidence of opisthorchiasis.

Of 526 participants who were negative for O. viverrini infection at the baseline survey in December 2002, 317 (60.3%) were enrolled in a follow-up evaluation in February 2004. Opisthorchis eggs were identified in 83 (26.2%) persons. The Kato thick smear method detected O. viverrini egg in 68 specimens, and the formalin-ethyl acetate concentration technique identified additional 15 cases. The incidence rate of opisthorchiasis was 21.6/100 person-years.

Risk factors for opisthorchiasis.

The prevalence of O.viverrini infection was significantly different when analyzed by age group (P < 0.001), education level (P = 0.047), and occupation (P < 0.001). There was no significant difference between sex and different household income groups (Table 1). Univariate analysis showed that those who consumed chopped raw fish salad (RR = 2.07, 95% CI = 1.31–3.28) and briefly fermented fish stuffed with rice (RR = 1.78, 95% CI = 1.03–2.97) had a higher risk of acquiring the infection (Table 2). In contrast, consuming raw fermented fish (Pla ra) was not associated with opisthorchiasis (RR = 0.97, 95% CI = 0.61–1.59).

Multivariate Poisson regression analysis showed that age and chopped raw fish salad consumption were independently associated with opisthorchiasis (Table 2). The participants who were in 20–39, 40–59, and greater than 60 years of age were 3.1 (95% CI = 1.1–8.2), 2.7 (95% CI = 1.0–7.4), and 4.1 (95% CI = 1.5–11.8) times at greater risk of acquiring the infection compared with those of less than 20 years of age. In addition, those who consumed chopped raw fish salad had a 1.9 times higher risk of acquiring opisthorchiasis (95% CI = 1.1–3.3) than those who did not consume chopped raw fish salad after adjusting for sex, age, education level, occupation, and a history of consuming other fish food items. There was no significant association with other traditional freshwater fish food.

DISCUSSION

Our study showed a relatively high incidence rate of O. viverrini infection of 21.6/100 person-years in the study community. The infection rate was similar to that reported in Khon Kaen Province (24%), an area in northeastern Thailand in which opisthorchiasis is highly endemic. 6,7,12 We used the formalin-ethyl acetate concentration technique, which is considered to be the most sensitive and reliable method for detection of O. viverrini eggs in confirming the results of the normal saline wet preparation and the Kato thick smear method in the baseline and follow-up surveys. 13 However, we examined only a single stool sample for each participant. Thus, those persons with light infection intensities might be missed. This finding might have affected the incidence rate. Another limitation of this study might be the relatively low follow-up rate (60.3%) among those who had negative stool examination results for O. viverrini during the 2002 study. The overall incidence rate might be overestimated to some extent because the incidences of O. viverrini infection were increased in the older age group. However, most persons who did not participate in the follow-up survey in 2004 were young adults who temporarily moved out of the village to find jobs during the dry season. However, the findings regarding risk factors would not be affected because the reasons for not participating in the study were unlikely to be related to food consumption behavior and O. viverrini infection.

Another potential bias might be related to the relatively long recall period (one year) of the food consumption history. Other previous studies using questionnaires for rapid identification of schistosomiasis in Africa and for risk factors of helminthic infections in China used a much shorter recall period, usually about four weeks. 14,15 In our study, however, we noted a high seasonal variation in consumption of uncooked food in this community, especially for chopped raw fish salad consumption that usually take place during the dry season. The questionnaire was designed to cover the food consumption over the whole previous year. In addition, because we collected the exposure information at the same time of stool specimen collections, our findings on risk factors were not likely to be compromised by information bias.

In our study, the incidence of opisthorchiasis was not significantly different between sexes but was different among age groups. The higher incidences were found in the older age groups compared with those less than 19 years of age. Using a multivariate Poisson regression model, we found that those who were greater than 60 years of age had an approximately four times greater risk of acquiring opisthorchiasis. This finding is in agreement with those of previous reports. 6,8 Although health education to avoid all kind of raw or undercooked fish food has been implemented in the study area, the older population still maintained their habits of eating undercooked fish. It is apparent that recommendations that the public avoid non-specific undercooked fish dishes have not been achieved, especially among the elderly. Other reasons might be that affected people feel less concerned about the infection because it is asymptomatic and an effective treatment against the parasites (praziquantel) is available. It has been demonstrated that there is an association between chronic infection with O. viverrini and cholangiocarcinoma. Persons 65–69 years of age with chronic infections with opisthorchiasis were 2.5 times more likely to show development of cholangiocarcinoma than other age groups.6 Thus, health education regarding the threat of chronic opisthorchiasis needs to be continuously communicated to affected people. Because the older population seemed to have difficulties in changing its eating habits, health education programs to avoid raw and undercooked fish foods should be focused on young persons who would be more likely to change their behavior.

Using a cross-sectional approach, Upatham and others found that more than 90% of heavily infected persons had a history of eating chopped raw fish salad compared with 19% of uninfected persons.8 Recently, a study of opisthorchiasis in Lao PDR also showed that persons consuming raw or undercooked fish had a 2.3 times greater risk of acquiring the infection. 16 From these studies, it was concluded that eating preference, especially raw or undercooked fish dishes, enhances the risk of being infected with O. viverrini. However, eating undercooked fish and actual risks of acquiring the infection were not demonstrated in this study. Our study was the first cohort study of O. viverrini infection conducted in Thailand that identified the risks for O. viverrini infection.

There are at least 15 species of small and medium-sized cyprinoid fish that naturally harbor the infective metacercariae, and these fish being the source of infection. 17,18 More than 10 popular raw or undercooked fish dishes had been prepared and consumed throughout the year by local persons at the study site. Of the four favorite dishes of freshwater fish, multivariate Poisson regression analysis confirmed that only chopped raw fish salad consumption was significantly associated with opisthorchiasis; the others were not. Persons who consumed chopped raw fish salad had a 1.9 times greater risk of acquiring the infection than those who did eat this salad after adjusting for sex, age, education level, occupation, and a history of consuming other fish food items.

On the basis of informal interviews with villagers, frequencies of eating chopped raw fish salad have been decreased and consumption generally was confined to special social occasions in this community, such as the fish catching season in summer. During this season, chopped raw fish salad was freshly prepared, and then immediately consumed near the ponds. This information was also reported in other studies.1 In this community, fully preserved fish, i.e., raw fermented fish, was regularly consumed several times a week all year round. This preserved fish was also consumed daily by most people in opisthorchiasis-endemic areas in northeast Thailand. 19 Nevertheless, we found that raw fermented fish were not associated with opisthorchiasis. Preparation of raw fermented fish was unique because it was kept fermented in a highly salted condition for at least 3–6 months. Survival of metacercaria depends on the concentration of salt and duration of fermentation. 20 Sukonthason and others reported that metacercariae in briefly fermented fish were degenerated after the second day. 21 Our interviews showed that raw fermented fish was prepared by local people and kept at least six months. Thus, it is most likely that metacercariae in raw fermented fish were non-pathogenic to humans. The present data showed that raw fermented fish was safe to consume because it was not the potential risk of O. viverrini infection in this community.

In conclusion, the national opisthorchiasis control program in Thailand should clearly address the threat of chopped raw fish salad consumption in acquiring O. viverrini infection. Strategic approaches for the opisthorchiasis control program should include stool examination and treatment of parasite-positive cases with praziquantel to eliminate human host reservoirs. Health education that emphasizes avoiding raw freshwater fish consumption, especially chopped raw fish salad, for preventing O. viverrini infection should be implemented.

Table 1

Incidence of Opisthorchis viverrini-infected persons and characteristics of enrolled subjects, Thailand

Table 1
Table 2

Univariate and multivariate analysis of risk factors for acquiring Opisthorchis viverrini infection, Thailand*

Table 2

*

Address correspondence to Ram Rangsin, Department of Military and Community Medicine, Phramongkutklao College of Medicine, 315 Ratchawithi Road, Ratchathewi, Bangkok 10400 Thailand. E-mail: rrangsin@pmk.ac.th

Authors’ addresses: Ram Rangsin, Somporn Mongklon, and Pote Aimpun, Department of Military and Community Medicine, Phramongkutklao College of Medicine 315 Ratchawithi Road, Ratchathewi, Bangkok 10400 Thailand. Mathirut Mungthin, Paanjit Taamasri, Tawee Naaglor, and Saovanee Leelayoova, Department of Parasitology, Phramongkutklao College of Medicine, 315 Ratchawithi Road, Ratchathewi, Bangkok 10400 Thailand.

Acknowledgments: We thank the authorities of Provincial Health, District Health, head of the village, and all participants for their participation in this study.

Financial support: This study was supported by The Thai Health Promotion Foundation and Phramongkutklao Research Fund.

REFERENCES

  • 1

    Sithithaworn P, Haswell-Elkins M, 2003. Epidemiology of Opisthorchis viverrini.Acta Trop 88 :187–194.

  • 2

    Keiser J, Utzinger J, 2005. Emerging foodborne trematodiasis. Emerg Infect Dis 11 :1507–1514.

  • 3

    Kaewpitoon N, Kaewpitoon SJ, Pengsaa P, 2008. Opisthorchiasis in Thailand: review and current status. World J Gastroenterol 14 :2297–2302.

    • Search Google Scholar
    • Export Citation
  • 4

    Traub RJ, Macaranas J, Mungthin M, Leelayoova S, Cribb T, Murrell KD, Thompson RC, 2009. A new PCR-based approach indicates the range of Clonorchis sinensis now extends to central Thailand. PLoS Negl Trop Dis 3 :e367.

    • Search Google Scholar
    • Export Citation
  • 5

    Sripa B, Kaewkes S, Sithithaworn P, Mairiang E, Laha T, Smout M, Pairojkul C, Bhudhisawasdi V, Tesana S, Thinkamrop B, Bethony JM, Loukas A, Brindley PJ, 2007. Liver fluke induces cholangiocarcinoma. PLoS Med 4 :e201.

    • Search Google Scholar
    • Export Citation
  • 6

    Sriamporn S, Pisani P, Pipitgool V, Suwanrungruang K, Kamsa-ard S, Parkin DM, 2004. Prevalence of Opisthorchis viverrini infection and incidence of cholangiocarcinoma in Khon Kaen, Northeast Thailand. Trop Med Int Health 9 :588–594.

    • Search Google Scholar
    • Export Citation
  • 7

    Jongsuksuntigul P, Imsomboon T, 2003. Opisthorchiasis control in Thailand. Acta Trop 88 :229–232.

  • 8

    Upatham ES, Viyanant V, Kurathong S, Rojborwonwitaya J, Brockelman WY, Ardsungnoen S, Lee P, Vajrasthira S, 1984. Relationship between prevalence and intensity of Opisthorchis viverrini infection, and clinical symptoms and signs in a rural community in north-east Thailand. Bull World Health Organ 62 :451–461.

    • Search Google Scholar
    • Export Citation
  • 9

    Kurathong S, Lerdverasirikul P, Wongpaitoon V, Pramoolsinsap C, Upatham ES, 1987. Opisthorchis viverrini infection in rural and urban communities in northeast Thailand. Trans R Soc Trop Med Hyg 81 :411–414.

    • Search Google Scholar
    • Export Citation
  • 10

    Kato K, Miura M, 1954. Comparative examinations. Jap J Parasitol 3 :35.

  • 11

    Truant AL, Elliott SH, Kelly MT, Smith JH, 1981. Comparison of formalin-ethyl ether sedimentation, formalin-ethyl acetate sedimentation, and zinc sulfate flotation techniques for detection of intestinal parasites. J Clin Microbiol 13 :882–884.

    • Search Google Scholar
    • Export Citation
  • 12

    Jongsuksuntigul P, Imsomboon T, 1997. The impact of a decade long opisthorchiasis control program in northeastern Thailand. Southeast Asian J Trop Med Public Health 28 :551–557.

    • Search Google Scholar
    • Export Citation
  • 13

    Sithithaworn P, Yongvanit P, Tesana S, Pairojkul C, 2007. Liver flukes. Murrell KD, Fried B, eds. Food Borne Parasitic Zoonoses: Fish and Plant-Borne Parasites. New York: Springer, 3–52.

  • 14

    Lengeler C, Utzinger J, Tanner M, 2002. Questionnaires for rapid screening of schistosomiasis in sub-Saharan Africa. Bull World Health Organ 80 :235–242.

    • Search Google Scholar
    • Export Citation
  • 15

    Steinmann P, Zhou XN, Li YL, Li HJ, Chen SR, Yang Z, Fan W, Jia TW, Li LH, Vounatsou P, Utzinger J, 2007. Helminth infections and risk factor analysis among residents in Eryuan county, Yunnan province, China. Acta Trop 104 :38–51.

    • Search Google Scholar
    • Export Citation
  • 16

    Sayasone S, Odermatt P, Phoumindr N, Vongsaravane X, Sensombath V, Phetsouvanh R, Choulamany X, Strobel M, 2007. Epidemiology of Opisthorchis viverrini in a rural district of Southern Lao PDR. Trans R Soc Trop Med Hyg 101 :40–47.

    • Search Google Scholar
    • Export Citation
  • 17

    Vichasri S, Viyanant V, Upatham ES, 1982. Opisthorchis viverrini intensity and rates of infection in cyprinoid fish from an endemic focus in northeast Thailand. Southeast Asian J Trop Med Public Health 13 :138–141.

    • Search Google Scholar
    • Export Citation
  • 18

    World Health Organization, 1995. Control of foodborne trematode infections. Report of a WHO Study Group. World Health Organ Tech Rep Ser 849 :1–157.

    • Search Google Scholar
    • Export Citation
  • 19

    Migasena P, 1982. Liver flukes relationship to dietary habits and development programs in Thailand. Patrice Jellife EF, Jellife DB, eds. Adverse Effects of Foods. New York: Plenum Press, 307–311.

  • 20

    Kruatrachue M, Chitramvong YP, Upatham ES, Vichasri S, Viyanant V, 1982. Effects of physico-chemical factors on the infection of hamsters by metacercariae of Opisthorchis viverrini.Southeast Asian J Trop Med Public Health 13 :614–617.

    • Search Google Scholar
    • Export Citation
  • 21

    Sukontason K, Methanitikorn R, Piangjai S, Choochote W, 1998. Viability of metacercariae in northern Thai traditional foods. Southeast Asian J Trop Med Public Health 29 :714–716.

    • Search Google Scholar
    • Export Citation
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