Community-directed intervention against liver fluke and soil-transmitted helminths in endemic areas of southern Laos

Background: Food-borne trematodiasis (FBT) and soil-transmitted helminth (STH) are neglected tropical diseases (NTDs) and threat human health in Southeast Asia. An estimate 67.3 million people are at risk of FBT caused by Opisthorchis viverrini (O. viverrini). Human infected with this parasite by consumption raw or insufficiently cooked fish dishes. Poor sanitation spreads the infection in environment. High burden of infection cause hepatobiliary diseases and with a longstanding of infection leads to develop cholangiocarcinoma (CCA). Liver fluke, O. viverrini, and STH are major public health problems in Laos. Over two million people are infected with O. viverrini mostly in central and southern Laos. An estimate 1,646,000 people are at risk for the STH. Hookworm is the most predominant species among the STH. Mass treatment alongside with health education is prioritized by Lao Ministry of Health for helminth control. However it is mainly implemented via vertical program that means leaving affected community having passive role for the helminth control. In addition this implementation requires substantial amount of human resource and fund to run the intervention which is challenging for Lao government to support for long-term intervention particularly intervention against liver fluke. In the work of this PhD thesis we developed, implemented and evaluated a community-directed intervention against the liver fluke and STH in southern Lao PDR. It has inspired by the CDTi of onchocerciasis in Western Africa.
Objectives:The main goal of this thesis is to develop an innovative approach, CDI, for the control of liver fluke and STHin southern Laos. Specific objectives were: 1.) to update the knowledge on helminth infection in the last four decades in Laos and the current helminth infection in liver fluke endemic areas in southern Laos; 2.) to understand helminth infections in relation to local community’s knowledge, attitudes and practices regarding worm infections; 3.) to deepen our understanding on consumption of raw fish dishes in relation to liver fluke infection in liver fluke endemic areas of southern Laos; 4.) to assess the community’s perception regarding the deworming intervention in endemic areas of S. mekongi and high prevalence of multiparasitism; 5.) to evaluate the effectiveness of the community-directed intervention against liver fluke and STHin southern Laos; and 6.) to identify factors associated with compliance to the intervention (CDI).
Methods: Five studies in this PhD thesis were community-based investigations and one was a literature review. A cross-sectional study designs was applied and using both quantitative and qualitative research techniques. Quantitative technique included stool examination to assess the prevalence and intensity of helminth infection, and structured interview with heads of households and household members. Qualitative methods comprised of semi-structured interviews, in-depth interviews, focus group discussions (FGD), and observations. Quantitative data were entered twice in Epidata software version 3.1 and analyzed in Stata software version 10.1. Conversations were transcribed from notes and tape-recorders and MAXQDA software version 10 was used for qualitative content analysis. For the literature review, data were obtained from international publications between 1970 and 2013 mainly searching through PubMed database via the website of University of Basel.
Results: Review on helminth infection in the last four decades of Lao PDR showed that currently ascariasis, trichuriasis, and hookworm infection rates are relatively low compared to the 1990s. But this not true for the mountainous and highland areas; hookworm is still a highly prevalent STH. O. viverrini infection rate remains high and even currently higher than before. The advance diagnosis using multiple stool sampling and multiple Kato Katz slides per a stool explains some of the increase. Multiparasitism together with liver flukes infections was observed. The habit of consumption of raw or insufficiently cooked fish dishes and open defecation is common practice in Laos thus it might keep infection and re-infection with O. viverrini in community. However possibilities to intervene on this habit are limited. Nowadays, in endemic area of S. mekongi the infection re-emerged, and children at 5 years of age were found already infected.
A baseline survey conducted in 10 villages of liver fluke endemic areas of Saravane district southern Laos pointed at very high infection prevalence of helminth infection but low level of awareness regarding worm infection. For instance, of 574 subjects the prevalence of O. viverrini, hookworm, Trichuris trichiura, Ascaris lumbricoides and Taenia sp. was 88.7%, 86.6%, 32.9%, 9.8%, and 11.5%, respectively. Most individuals were co-infected with O. viverrini and hookworm (77.3%). More men had multiple helminth infections than women. Of 130 heads of household, one third heard about liver fluke before, of which 59.2% associated it with eating raw fish dishes. Among the STH, roundworm was the most well-known (70.8%) but most people linked it with consumption of raw food (91.3%). Consumption of raw fish dishes was most commonly practiced (75.4%); few households possessed a latrine (16.1%); less than half mentioned health benefits from latrine use and personal hygiene. FGD participants had poor awareness on worm infections; more men liked eating raw fish than women; some disliked using latrine because they did not get used to it and due to its bad smell. Poor personal hygiene practices and village hygiene were observed.
Our result on consumption of raw fish dishes in relation to liver fluke infection in liver fluke endemic areas southern Laos was heterogeneous. The majority of FGD participants considered fish flesh that had been prepared with weaver ant extract (giving sour juice) and that then turned to white colour to be safe for consumption. Visual appearance, taste, smell and personal preference were given as reasons for consumption of raw fish dishes. Moreover, participants considered it a traditional way of food preparation, and practiced for generations in Laos. Ten different fish dishes that use raw or fermented fish were identified. All FGD participants reported to consume raw fish dishes.
In endemic areas of S. mekongiin southern Laos where also multiparasitism prevails, we found that opinion leaders and villagers were well aware of taking deworming during MDA in village. Leaders perceived the effectof MDA against severe schistosomiasis (big belly and patient ended up with vomit a lot of blood) and appreciated that it was provided free of charge in their village. They encouraged villagers to attend and take the drug. Anticipated adverse effect of praziquantel was a barrier for participation. Most leaders purchased deworming (except praziquantel) in a local pharmacy for deworming when MDA was absent in their villages (19/21). Most leaders (20/21) had a good knowledge on severe schistosomiasisthough only a few of them (5/21) described its cause correctly. They knew little about the disease consequences of liver fluke (3/21) and STH (4/21) infections but more about their causes. A high risk for worm infection was observed in community: consumption of raw or insufficiently cooked fish dishes (100%), frequent physical contacts with MekongRiver water (76.0%) and few latrines in village (14.5%).
In Saravane province, after implementing two rounds of CDI against liver fluke and STH we found that the prevalence of O. viverrini, hookworm, roundworm, and whipworm infection was reduced by 26.4%, 38.1%, 45.9%, and 30.3%, respectively. The frequency of multiparasitism was also reduced. Household heads had better knowledge on liver fluke, hookworm, and whipworm infection, means for prevention of liver fluke, and correct association between risk factors with hookworm and whipworm infection. Misconception on acquiring roundworm infection through eating any raw food was frequent. Few heads of households consumed raw fish dishes which was consistent with FGD participants discussed that after taking treatment they felt not eating raw fish dishes anymore and some were afraid of getting liver fluke again. Participants viewed that intervention was effective against liver fluke and other worm infection and prevented diseases. Community leaders had ownership in conducting the intervention.
The factor associated with the compliance to intervention (CDI)was assessed. We found that of 600 interviewees, 46.5% reported to have taken treatment during the mass treatment in village. Those who took treatment were mostly from poor households (p=0.013), aware of intervention (p<0.001), knew that intervention provided treatment for liver fluke (p<0.001) and abdominal pain (p=0.028) and saw the tapeworm in their stool (p=0.016). The majority of respondents heard about liver fluke and roundworm. The compliance with MDA was associated with poverty: very poor (OR=2.13, p=0.018) and poor (OR=2.07, p=0.022), knowing the effectiveness of intervention against liver fluke (OR=1.57, p=0.035) and recognizing about tapeworm infection (OR=2.95, p=0.037). CDDs performed their task quite well though supervision was rarely made by trained health center staff.
In conclusion: We conclude that beside the high prevalence of O. viverrini and STH, community leaders and community members have poor knowledge regarding worm infection and the role of MDA. Risk behaviour for worm infection is observed: eating raw or insufficiently cooked fish does exist due to people loved its taste, smell and look; perceived preparation technique is safe to eat and it is a traditional way, and practiced since generations; poor practice of hand-washing; barefoot walking; poor sanitation and less use latrine due to bad smell and they did not used to it. We also conclude that a new approach CDI is effective against worm infections and corrects community’s knowledge, attitudes and practicesregarding worm infections and mass treatment. Community leaders have ownership and capacity in conducting the CDI. Hence, it is possible to scale up this CDIto other liver fluke endemic areas of Saravane province and later to all southern Laos for the control of liver fluke and co-infected worms.