Uncooked fish consumption among those at risk of Opisthorchis viverrini infection in central Thailand

In contrast to northern and northeastern Thailand, central Thailand was believed not to be endemic for Opisthorchis viverrini (OV). Fieldwork conducted in a rural area of central Thailand revealed that the prevalence and incidence were relatively high compared with regional average data. We hypothesized that the behavioural-psycho-social background of the study population might play an important role in the high burden of the infection. As a result, a qualitative study was conducted to highlight potential social determinants of the infection dynamics to gain greater understanding of the risk behaviours and their contexts. A qualitative study using focus group discussion and in-depth interviews was conducted in Na-ngam Village, Chachoengsao Province from 2012–14. Framework analysis was used to explore associations between infection and thematic content. Social influence showed a strong impact on infection dynamics of OV infection. Our results revealed that Koi pla (chopped raw fish salad) remains a popular dish in the community, as the dish itself represents northeastern culture. The cultural norm had been transferred from ancestors to their descendants. Some elders complained that discontinuing the consumption of Koi pla went against old traditions with respect to cultural norms and socialization. In contrast, modern education teaches about hygiene including OV infection risks, and accordingly teenagers and young adults were reported to modify their lifestyles including their eating habits. Children are a potential key to pass knowledge to their parents and school-based education programs can serve as a practical hub for knowledge dissemination. However, health education alone might not lead to behavioural change in other age groups. Therefore, more efforts are needed to support the transformation.


Supporting information -Study's minimal underlying data set
Health campaign based on the National Control Program was provided to the community including health education, diagnosis and treatment by the collaboration between research team and local health volunteers.
Local health volunteers played an important role to communicate and interact among villagers and local health authorities. They gained respect from the villagers as important key members of the community.
As shown in Table 1, most participants acknowledged that OV infection was still a health burden to the community. They perceived that the infection was strongly associated with consumption behaviours and chronic infection could result in serious outcome. However, misunderstanding and misconception remained in some villagers. The potential of social and cultural influence also impacted on attitudes and perceptions of the infection. High-risk populations and risk factors continued to be identified. Moreover, the prevalence and incidence of OV infection were still relatively high compared with the baseline population.
Most villagers knew that some of their popular fish dishes were uncooked. Some were still confused that all uncooked dished could cause OV infection while some of them knew that only fresh fish material could lead to infection.
Koi pla (chopped raw fish salad) is a popular dish that has been consistently identified as a major risk factor of the infection. Although the community learned that it could lead to infection, the dish was still valued as a Northeastern culture norm. Daily consumption might have decreased; Koi pla consumption was still popular during festive events, friend or family meeting and male social drinking.
Older age showed strong attachment to the traditional value of Northeastern culture; "Most of the elders still eat raw fish; they came from the Northeastern region" said one 48-year-old woman from the newly-infected group mentioning the strong attachment between the elders and their ancestors who originally lived in Northeastern Thailand and later migrated to the current area. Although uncooked fish dishes varied in this community, Koi pla and Pla ra were the most popular dishes villagers frequently consumed in both sexes and all age groups.

Current situation of consumption behaviours
"Everybody eats raw fish; it's very rare to see someone who doesn't" said one member of the re-infected group. However, consumption of Koi pla decreased in females and at younger ages, "As I recognize, it's once a year, twice as a maximum." said one 40-year-old woman describing having Koi pla.
Koi pla was shown to be strongly related to multiple aspects as their way of life. It was considered a food frequently eaten with alcoholic drinks especially in male social drinking. "Koi pla was served in a drinking party among male friends. Koi pla was the best when paired with alcohol", one 70- year-old man from the newly-infected group mentioned about the relationship between alcohol drinking and uncooked fish-eating habit. "It's a socialization process," said one 61-year-old from the newlyinfected group.
"If I have to quit Koi pla, I have to quit alcohol, which is a highly unlikely thing for me to want to do," said one 48-year-old man from the re-infected group.
Some of them stated that eating Koi pla was related to agriculture-related occupations: "Farmers always eat Koi pla, fish is easily caught from the river when they go to a paddy field" said one 40-yearold woman from the never-infected group.
On the contrary, Pla ra consumption was popular at all ages and both sexes. Pla ra was used as a seasoning, food ingredient or even consumed as a main dish. The roles of Pla ra are various. When mentioning uncooked fish dishes, Pla ra would be the very first dish they recognized. "I can't live without Pla ra," said one 48-year-old woman from the previously-infected group.
Some families whose parents still consumed Koi pla kept their children away from it unless cooked. Moreover, if children and teenagers consumed Koi pla, they were always from families with uncooked fish eating habits. "I want to eat it," one 7-year-old boy mentioned about Koi pla, who had parents who regularly consumed Koi pla and he was a newly-infected case.
Some villagers stated that uncooked fish consumption was an old tradition. It might be difficult to avoid or stop eating due to the strong cultural attachment. However, it began to gradually fade out from the younger generation as one 64-year-old women from the never-infected group said, "They don't even recognize Pla ra; they just enjoy hotdogs." The teenage group said that they did not like Koi pla. They thought the preparation method and food appearance looked disgusting and unacceptable. Moreover, the fishy taste did not match their more urbanized lifestyle. Younger generations loved to eat instantly prepared foods such as instant noodles or ready-to-eat meals. Some thought it was fashionable to eat what was advertised on the television.
"Teenagers do not have much uncooked food. They enjoy instant noodles to anything easy to prepare such as fried eggs" "They like cooked food, whatever kind of preparation; fried, grilled or roasted" Health education provided more insights about the threat of uncooked fish consumption. The roles of local health volunteers and health campaigns influenced the behavioural patterns of consumption.
"The newer generation never eats raw fish; they were educated from their school," said one 64- year-old woman from the never-infected group.  vegetables," said one 51-year-old woman from the newly-infected group.

Knowledge of the infection
Some villagers perceived that fish from clean water sources was free of metacercariae.
"The water body was clean without aquatic weeds or chemical substances, so the fish was also clean from parasites," said one 70-year-old from the newly-infected group.
They also knew that Koi pla was a risk factor for OV infection. Most of them understood that dressing uncooked fish meat with acidic agents such as lime juice or spirits only changed its colour, it was not completely cooked and metacercariae were still viable.
However, one member from the re-infected group had never heard about OV infection. The villagers acknowledged the transmission process of the parasite. They knew that once stool contaminated with parasite eggs were released in a natural water source, the eggs hatched and continued its life cycle.

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Some of them mentioned that public excretion could be avoided and in fact most of them used toilets on a regular basis, but some factors could not prevent disease transmission.
"I saw the toilet pumping service car dumped stool in the river," one 70-year-old man mentioned about how the authorities managed the public toilet pumping service. • Stigmatization from being infected • School was an information hub The villagers perceived that OV infection was the major problem to the community (Table 4).

Perception of OV infection and its consequences
They showed better attitudes towards OV infection. Although some of them might have misunderstood about the life cycle, they agreed that cooked food was more hygienic and could prevent not only OV infection but other intestinal parasites as well. Their consumption behaviours might be difficult to observe in practice, but parents were trying not to let their children consume Koi pla; "Cooked food was good, vegetables need to be washed as well" After receiving stool examination results, some villagers decreased their uncooked fish consumption as they mentioned, "Though I've never seen the worms, the result makes me stop eating raw fish". Even when the result was negative, some were still concerned about other's results or they were afraid that if they chose to maintain risk behaviours. One day the result might turn to be positive, "I see

doctors collect stool and give medicine; I think it's time to stop eating raw fish. I don't want to be one of the infected"
Some were concerned about possible side effects of taking praziquantel. They were afraid that if they were infected, they would have to take the medication again, "It didn't feel good after taking the medicine," said one 48-year-old from the re-infected group.
The younger generation had better accessibility to information. The school taught them about basic hygiene. Most households could not afford the internet service and IT infrastructure was still under development. However, internet was available at school and internet cafés in community centres. Some of them spent time during break or after class looking for more information about OV infection, "I saw the pictures of worms on the internet," said one school-age participant.
As the villagers perceived that OV infection was a disease, they preferred to focus on treatment rather than prevention. In addition, some of them learned that treatment for the infection was simple and feasible so they were willing to wait for the healthcare worker as they thought it should be the physician's responsibility to take care of them; "Only the doctors know the disease, so it was better to leave it in their hands" said one 70-year-old man. All groups expressed that they were asked for stool examination because the doctors (research team) thought it was important. Practically, nobody ever asked for a stool examination at the local healthcare facility, "I consider what the doctor concerns"

Health concern of risk factors and the infection
However, some thought to look after the health was the doctor's responsibility.
"I'll do whatever they say. They said I have the parasite, so they gave me a drug." said one 70- year-old man.
Most villagers were not sure about the relationship between OV infection and cholangiocarcinoma. It was noticeable that the villagers also expressed various opinions toward the parasite and infection with respect to their age; teenage, adult or elderly.
Teenagers and adults knew that chronic infection could lead to cancer, but they did not know exactly what kind of cancer resulted from OV infection. Moreover, the name "liver fluke" (also called in Thai) confused the villagers and that the pathology occurred in liver tissue. Some believed that consuming Koi pla with alcohol could accelerate the process of liver cirrhosis. Elderly members thought OV infection was not related to cholangiocarcinoma. They observed that many were still healthy even though they regularly consumed uncooked fish.
Although all age groups realized the medical importance of OV infection, younger aged members were concerned about live worms living in their body while they were less aware of being sick from the infection. Male youths started to consume uncooked fish in adolescence to imitate their friends. Small children might be fed uncooked fish by their parents.
Adults and the elderly paid more attention to infection from the parasite. Lastly, the elderly members were concerned about both parasite and the infection. However, some admitted that they could not avoid eating uncooked fish despite knowing the unhealthy consequences.
The villagers stated that uncooked fish consumption needed to be slowly reduced. Abruptly discontinuing consumption seemed impractical. For Koi pla consumption, quantity and frequency were decreased over time except in the elder group that stated it was difficult to give up their way of life.
Moreover, some of them mentioned that contributing to a major change was not worthwhile because they only had a few years left in their life. "I've been living so far and I all have to die anyway, why not just enjoy life while it lasts," said one 83-year-old woman from the re-infected group.  Table 6, standard treatment with praziquantel was provided by the research team under the project after the stool was examined. OV infection cases received their diagnosis with praziquantel and other parasitic infections also received corresponding medication.

Diagnosis and treatment
When they were aware of being infected, two approaches allowed them to receive medication.
Firstly, they waited for the stool examination result from the research team who regularly visited them.
They would definitely receive praziquantel with this method, "Doctors come very often. If I got infected, then they'll give me drugs," said one 47-year-old woman in the local volunteer group.
Secondly, they also perceived that anthelminthic medication was available at the community healthcare centre or they could directly purchase over-the-counter medicine from the pharmacy for their convenience. Unfortunately, those anthelminthic drugs were for intestinal helminths such as albendazole or mebendazole. Praziquantel was not available in the community pharmacies unless villagers went to the district hospital which was 1 hour away.
Additionally, some thought that a single drug could cure all parasitic infections including OV infection. Especially for those who currently consumed uncooked fish, some purchased medicine from a drugstore and misunderstood that it could cure liver flukes so they returned to resume their eating behaviours, "It's simple, just go to the drug store," Said one 61-year-old from the newly-infected group.
After receiving praziquantel, some felt that the infection was truly eradicated from their body, "After I took your drug, all worms were killed. So I feel I'm stronger," said one 60-year-old woman from the previously-infected group.
However, some who used to take medicine still recognized praziquantel from its side effects,  Table 7, the participants stated that they had better knowledge after they received health education. Consumption of Koi pla decreased, even some could not definitely quit but could reduce in terms of frequency and amount of consumption.
"The doctors come and talk about it every year. I see the health campaign posters every day, it keeps reminding me not to eat Koi pla," said one 54-year-old from the previously-infected group.
Because the development of cholangiocarcinoma is a long process and mainly asymptomatic, so the cancer was not a major concern to the villagers after being infected with OV infection. In fact, the prevention was simple. Avoidance of uncooked fish did not require sophisticated medical intervention.
Moreover, the treatment was also effective and affordable. At this point, some of them admitted that they did not pay much attention to cholangiocarcinoma, "I can seek healthcare whenever I think I'm getting the infection," said one member of the adult group.
The National Control Program has focused on the control of uncooked fish consumption, which would interrupt the infection process; therefore, it could potentially prevent the occurrence of cholangiocarcinoma from OV infection. However, the consumption behaviours were strongly attached to 11 the local culture, "There were many raw fish dishes, I can't avoid all of them," some mentioned about uncooked fish dishes. The control program suggested that all uncooked fish dishes should be avoided.
The group discussion agreed that when a particular dish was identified as a risk factor, it would be easier and more promising for behavioural modification.
Children had a better understanding about the knowledge of infection. Some adults and elderly felt more comfortable and hesitated less to be educated from their offspring. Children served as an effective medium for transferring knowledge. Additionally, they did not want their children to practice the same habit.
"It was a good strategy. They're ashamed if they do not behave as role models," said one 38- year-old female from the adult group.
Most villagers had toilets in their house. Some of them installed toilets on their farm. Otherwise they would excrete in the field and cover with soil. Just a few people excreted directly in the natural water resource.
"Toilets are everywhere, nowadays. Those who can't find one use a spade to cover it with soil," one 55-year-old local health volunteer mentioned about how to excrete in the paddy field without toilet. "I would hold it until I get home," said one 18-year-old from the never-infected group.