Raw Pig Blood Consumption and Potential Risk for Streptococcus suis Infection, Vietnam

We assessed consumption of raw pig blood, which is a risk factor for Streptococcus suis infection in Vietnam, by using a mix-method design. Factors associated with consumption included rural residency, age, sex, occupation, income, and marital status. We identified risk groups and practices and perceptions that should be targeted by communication programs.

C onsumption of undercooked animal products is a wellestablished risk factor for acquiring many infectious diseases (1-5). In Vietnam, raw blood of pigs or other animals is consumed in a dish known as tiet canh. The main ingredients of porcine tiet canh include coagulated, fresh, uncooked blood mixed with chopped cooked pork tissues ( Figure). A recipe is shown in online Technical Appendix Table 1 (http://wwwnc.cdc.gov/EID/article/20/11/14-0915-Techapp1.pdf). Consumption of raw pig products is associated with trichinellosis and Streptococcus suis meningitis in humans in Vietnam (6-8).
S. suis is a common gram-positive bacterium found in pigs, which can cause severe infections in humans; ≈90% of human cases are reported from Asia (9,10). Case-fatality rates range from 3% to 7% but may reach ≈60% among patients with severe sepsis, as observed in a large outbreak in Sichuan, China, in 2005 (11). Studies have identified occupational exposure to pigs and consumption of specific traditional pork dishes as key risk factors for contracting S. suis infection (10). Effective control of diseases transmitted through consumption of undercooked pig products requires a thorough understanding of this food practice. Therefore, we investigated consumption of porcine tiet canh in northern Vietnam and explored community perceptions regarding associated disease risks.

The Study
The study was conducted in 2 health care and demographic surveillance sites in Hanoi Province, Vietnam: Ba Vi District (rural) and Dong Da District (urban). Each site contained ≈11,000 households that were selected by cluster sampling to represent the district population (12). This study was approved by ethical committees at the University of Oxford and Hanoi Medical University.
A quantitative survey on tiet canh consumption was administered to household members at health care and demographic surveillance sites (Ba Vi: May-June 2012; Dong Da: December 2012-January 2013). Field surveyors visited households as part of their routine survey schedules and interviewed 1 member per household individually. A total of 6,993 participants in Ba Vi and 3,991 participants in Dong Da were interviewed (no households refused). After persons for whom no data were available regarding age and sex were excluded, 6,943 (99.3%) persons in Ba Vi and 3,921 (98.2%) in Dong Da were included in the analysis (mean age [range]: 47.0  years in Ba  years in Dong Da).
Rural and urban respondents differed significantly by sex (24.6% vs. 34.5% male participants, respectively), education (21.9% vs. 74.3% with ≥10 years of education), and occupation (2.4% vs. 29.6% office workers). Subsequently, 10 focus groups that involved 81 participants in the 2 districts were formed (April-June 2013). Participants in focus groups were selected on the basis of reported consumption of tiet canh in the previous survey and were stratified by district, sex, and consumption status. For each district, 1 focus group was also conducted for local government workers. Details on data collection, characteristics of participants, and data analysis are described in the online Technical Appendix.
A total of 35% (95% CI 33.8%-36.1%) of persons in the rural area vs. 8.6% (95% CI 7.7%-9.5%) in the urban area reported eating porcine tiet canh in the past year. Duck blood was the second most common source of tiet canh (online Technical Appendix Table 3). Subsequent analyses were restricted to porcine tiet canh. Sex, age, level of education, occupation, economic status, and marital status were associated with consumption patterns by univariate analysis (Table 1). However, level of education was not associated by multivariable regression (Table 2).
More men than women reported consumption, and this difference was greater in the urban setting than the rural setting. Given that more women than men participated in the survey, the estimated frequency of persons consuming tiet canh will likely be higher than reported in this study.
The practice was more common in persons 40-49 years of age than in other groups. Persons who reported highest consumption included farmers, manual laborers, persons working in service and sales. In the urban district, household economic status was negatively associated with consumption levels (odds ratio >2.0 for 2 lowest quintiles compared with the highest quintile). This finding was further confirmed in focus groups because tiet canh is relatively inexpensive and available in most markets. Therefore lowincome workers are more likely to eat this dish (online Technical Appendix Table 5).

Conclusions
Consumption of tiet canh is closely linked with traditional family celebrations, particularly weddings. These traditions are a source of pride and social bonding among community members. Pigs are frequently slaughtered at homes of families hosting celebrations. Several male participants expressed pride and fond memories of their experience in participating in slaughtering events. Tiet canh is sometimes served at family celebrations expressly to demonstrate that slaughtered pigs are healthy. Cultural contributions of tiet canh must be understood to develop effective communication messages to reduce health risks associated with this practice.
Participants articulated strong confidence in the safety of raw pig products when the source of the pig was known to the consumer and the pig appeared healthy. Sources of pigs considered relatively safe were homeraised pigs, wild boars, or pig breeds locally known as 'lợn mán and lợn mường (typically free-range, scavenging  pigs raised by ethnic minorities). These perceptions contrast with findings of prevalence studies that showed high carriage rates of S. suis, even in apparently healthy pigs and pig products (13), and with reports of transmission of neurocystercercosis (14) and trichinellosis (6,15), which suggested increased transmission risks associated with scavenging pigs. Beliefs about potential health benefits of eating tiet canh, such as preventing anemia or a general cooling effect, were widespread. However, participants did not fully understand the health risks posed by infectious agents or contaminants, and risks were dismissed or overlooked. Although concerns regarding the risk for diseases associated with tiet canh were raised in all focus groups, few participants knew what specific diseases are transmissible to humans through tiet canh consumption. In contrast, risk underestimation through optimistic bias was common, and fatalistic attitudes were shared in the group setting (online Technical Appendix).
The Agriculture Ministry of Vietnam had issued an official letter (no. 18 BNN/CĐ, May 21, 2009) that requested coordinated actions in controlling transportation, slaughtering, selling, and consumption of animals and animal products in response to recent disease reemergence. This letter also recommended a ban on selling of tiet canh. However, this proposed ban was considered to be unenforceable and ineffective among participants in all focus groups. The profit from selling tiet canh and consumer demand were considered key features that will perpetuate this traditional dish. Furthermore, trade in raw pig products is too widespread and decentralized, and the food chain from pig producers to pork consumers is too complex to enable regulation or enforcement of trade bans.
This study showed that consumption of tiet canh was more common among adult working-age men, outdoor workers, low-income urban inhabitants, and married persons in rural areas. Children rarely eat tiet canh, which may partly explain why S. suis meningitis is mainly a disease of adults and more common in men. Disease surveillance and reporting should be improved to better estimate the incidence of S. suis infections and clarify the relative role of the foodborne transmission route.
Given the traditions of consumption of tiet canh during family celebrations, interventions such bans on consumption or simple education messages on health risks without accounting for associated cultural values are unlikely to be effective. However, changes in education, urbanization, and increasing income levels will affect social and behavioral attitudes toward consumption of tiet canh in the future. Food safety research could benefit consumers by exploring methods of preparation of tiet canh designed to reduce infectivity of any pathogens in raw blood and preserve desired texture or taste characteristics of this traditional cuisine. Ms Huong is a doctoral student at the Nuffield Department of Medicine, University of Oxford, Oxford, UK, and the Oxford University Clinical Research Unit, Hanoi, Vietnam. Her primary research interests include epidemiologic and behavioral aspects of emerging infectious diseases in Asia; the interface between animals and humans and how these interfaces contribute to spread of diseases in the context of rapidly changing agricultural, husbandry and food supply practices; and how interventions can be culturally tailored to prevent infections.

Data Collection
We conducted a community survey about consumption of raw pig blood during May- Respondents were asked the following closed ended question for the food practice: "How many times have you eaten raw animal blood in the past year?" and answered by choosing one of the options offered: none, 1-3 times, 4-8 times, 9-12 times, >12 times, and unsure.
Participants were required to specify the type of animal blood that they consumed, which include pig blood, duck blood, and other types of blood. All complete data forms were checked by field supervisors and a data clerk before data entry. Sociodemographic data, including sex, age, highest education level, marital status, occupation, and household economic status, of the respondents were extracted from the latest household update survey in both sites.
The follow-up qualitative study used a grounded-theory embedded design to uncover the experiences of participants related to raw pig blood eating and build the concepts from the data to explain the behavior. This study was conducted during April-June 2013 with 5 focus groups (FGs) in Bavi, including FG1-4 at participants' house and FG5 at the meeting room of the FilaBavi office located in the district hospital, and 5 (FG5-10) in Dong Da, which were organized at the community health centers in the participants' vicinity. All FGs were moderated by one of the authors (VTLH) in Vietnamese by using a question guide. The question guide was designed to include 5 categories of questions to maintain the flow of the discussion: opening, introductory, transition, key, and ending (1).
The main aspects discussed are contexts in which the dish is consumed, attributes of Eighty-one persons were purposefully selected from the 2 surveillance sites to participate in 10 FGs. These participants were met and invited individually by the field interviewers. In each site, we held 2 FGs for men and 2 FGs for women who were the general community residents, and 1 FG for local staff (health workers, women's union staff, and culture and information staff). Each FG had 6-9 participants. All FGs included persons who never consumed, who used to consume, and who were consuming raw pig blood dishes at the time of the study.

Moderator list all suggestions from participants on the flipchart.
Following is a list of possible programs that might be carried out to prevent S.suis infection through eating pig tiết canh and other undercooked pig products, please choose the most effective intervention that you think can work for your community. Provide reasons for your choice.

Moderator shows the following list of interventions on a flipchart to the participants, and add any new interventions mentioned by the participants in the previous question:
Public education campaign (via TV, radio, newspaper, loudspeakers…) to advice the public not to prepare or eat raw/ undercooked pig derived dishes Public education programs to provide information for communities of how to prepare safer pig dishes from the high-risk pig products. Public ban on selling tiết canh products and implementation of this ban Vaccination of pigs against S.suis Education at school on the health risks of eating raw/ undercooked pig products Prohibition of selling, processing and consumption of sick/ dead pigs Ending (10 min) Moderator summarizes the main content of the focus group. Is there anything else you would like to add or mention before we wrap-up?
Technical Appendix Table 2. Recipe commonly used for making tiet canh in northern Vietnam Preparing blood: Pig is bled and blood is collected into a large container which already contains a small amount of saline solution to initially prevent the blood from coagulating. The saline solution is usually made from salt and water (or diluted fish sauce). If too much salt, the blood will not coagulate when mixing with the solid mix at the later stage. Preparing the solid mix: varies depending on type of pig and geographic regions. Common pig portions used for making the solid mix are: spareribs meat, rib cartilage, neck meat, lung, tongue, throat, intestines. These are boiled/ roasted and chopped and maybe fried until crunchy. Roasted onion and ginger also can be added .Put the mix into bowls/ plates that will be used for preparing the final dish. Add the prepared blood together with some water (suggested amount 1 spoon of blood and 2 spoons of water) to the bowl/ plate containing the solid mix above. Let it set until it coagulates. When it coagulates, sprinkle some peppers and roasted peanuts on top. Served with lemon, some aroma leaves such as mint leaves, basil, thorny coriander, and rice wine. Boiled intestines, stomach, and uterus can also be served with tiet canh.
(summarized from the transcripts of focus group discussions) Technical Appendix Technical Appendix Table 6. Factors influencing participants' choice of eating tiet canh explored from focus groups discussions, Vietnam* Category Descriptions Food characteristics Taste, appealing appearance, easy-to-eat Social contexts Weddings (in rural area), parties, slaughtering events: Tiet canh eating was most commonly learned in social occasions such as rural weddings, New Year celebrations and other special gatherings. Pigs are often slaughtered in the early morning, tiet canh is made and consumed as soon as possible within the morning when it is still fresh. Weddings were the most frequently reported occasion for tiet canh consumption in the rural area. Indeed, among young rural women, their first reported instance of tiet canh Drinking encounters (best matched food for alcohol drinking) at home or in shops: Many shops sell fresh tiet canh in the morning, however it is also sold for lunch and dinner. Family contexts: children copy adults within the family to eat tiet canh, parents made it as a special treat for children, encouraged children to eat due to belief that it provides improved immunity Availability and accessibility Available in social parties; Available in shops at affordable price: Tiet canh can also be found in most markets in both urban and rural settings, and is relatively cheap (≈10-20,000Vietnam Dong, equivalent to <$US 0.5-1). High profit made from selling the dish; Perceived benefits Mentioned by 44% (n = 36) of respondents The most commonly mentioned benefit was the notion that tiet canh is a 'cold' food that serves to ease internal body heat or could be helpful in treating mouth ulcers (n = 24, mainly in urban FGs). Other perceived benefits included preventing anemia, treating headache, cough and dysentery, detoxification, clean the body internal system, or clearing minute dust in the lungs (e.g., hair clippings). Myth: Tiet canh was considered a 'red' food associated with good luck if eating tiet canh on the 1st day of the lunar month (n = 13, mainly in urban FGs). Perceived safety Safe food source: Home grown pig/ self-made dish, free-range pig, rural pig, wild boar, trustworthy/ known source; Perceived tiet canh was safe when the source of the pig or the person preparing the dish was known to the consumer (mentioned by 61% and 50% of rural and urban participants, respectively). Even when the blood was bought at the wet market, people considered tiet canh to be more safe when prepared by someone they knew and trusted, versus an unknown commercial source. The word 'clean' was used by a substantial number of consumers (31%, n = 16) to describe deliberate choices on whether to eat tiet canh in a given context, and it conveyed two different meanings: the source was known or was perceived as prepared under trusted hygienic conditions Drinking alcohol: Several men expressed the belief that rice wine can help mitigate possible health risks by "disinfecting" tiet canh. This type of drink is regularly served to pair with tiet canh. In addition, alcohol helps reduce the bloody smell of the dish, and neutralize the dish (hot and cold food).

Disease risk awareness
Awareness that the dish can transmit diseases to humans; Pig outbreaks (such as porcine respiratory and reproductive syndrome [PRRS] and foot and mouth diseases): The presence of ongoing disease outbreaks in pigs negatively influenced consumption patterns, and discouraged some people from eating. This effect was noted more frequently among rural participants, and in communities with a history of pig outbreaks (FG1,2,4) Risk underestimation through optimistic bias: attitudes such as diseases can't happen because I am resistant (FG3,6,7,8), diseases happen somewhere else but not here (FG6). Confidence in the relative safety of tiet canh was expressed by many participants based on repeated personal experience: I've never had any bad experience after eating tiet canh (FG1,4,7,8). Fatalistic attitude: death is our fate. Some participants, despite being aware of health risks and having stopped consumption for some time, resumed eating tiet canh again in situations where they believed the risk was low (e.g., a woman in FG10 ate when she was given tiet canh prepared from a lợn Mán).
Technical Appendix Table 7. Key perceptions about public health interventions, Vietnam* Type of intervention Key perceptions Information, Education, Communication activities Mass media was not perceived as an effective method to reach certain populations such as mobile manual workers, men, heavy drinkers and older generations (FG1,9,10). Communication messages should be repeated frequently and sustained over time to be most effective (FG8, 10).

Type of intervention Key perceptions Pig vaccination against S. suis
Pig vaccination overall was perceived as an effective measure, but most farmers were not aware of S. suis bacteria in pigs, probably due to the unavailability of an effective vaccine for this disease in the local market and thus lack of information on this specific pathogen. Some concerns were expressed about current government programs for animal vaccination, including possible disease spread due poor biosecurity practices of field teams responsible for vaccination, insufficient vaccine supply and limited coverage (FG1, 4). Ban on selling tiet canh Considered to be infeasible and ineffective among participants in all FGs. Monetary profit from selling tiet canh and the consumer demand were considered as key features that will perpetuate this traditional dish. Trade in raw pig products is too widespread and decentralized, and the food chain from pig producers to pork consumers too complex to enable regulation or enforcement of trade bans.

Food inspection
Not confident in the standards of food inspection programs Complained that sellers of unsafe or contaminated products are able to bypass inspections and they do not trust certified food *FG, focus group.
Technical Appendix . "I think bacteria will die when there is rice wine." (M, village health worker, age 41, rural, FG5). Availability/ accessibility "Wake up in the morning, they already sit there at tables on the roads, in the market in B20." (F,age 69,urban,FG7). "Not only it is men's favorite, but selling it make a lot of money, high profit so in any circumstances they will sell it." (F,age 47,rural,FG1). "If eating out, tiet canh is the most suitable food for our pocket money." (M, age 45, rural, FG4). "...laborers often eat tiet canh more. In my opinion, it's simply because it is low-price." (M, age 48, urban, FG8). Information, education, communication "Communication campaigns can only reach more perceptive people, especially the mass media... The remaining groups including mobile manual laborers, low awareness, don't care anything... they still eat." (F,age 48,urban,FG10). "A while ago TV mentioned about eating tiet canh and Streptococcus suis infection, at that time I stopped eating. Then when it no longer talked about it, I thought the outbreak was over... so TV, radio and newspapers should continue talking about this, eating tiet canh will decrease." (F,age 33,rural,FG3). "I think communication campaigns should be longer. Not one period with one or two days, need to repeat, one week, ten days or more, if someone could not hear it today they can hear it at another time." (M, age 48, urban, FG8). Food inspection "To prevent (infections), first, the commune units for animal products inspection need to continue to inspect the hygiene and safety of food products regularly." (M, age 63, urban, FG6). "First inspection, have you done it right? ...We don't know if there is an outbreak, we sell, the pig blood looks still clean, so we still eat. Who will check if this pig has enough qualities for sale or it is diseased and therefore not allowed for selling?" (M, age 45, rural, FG4) "In the early mornings the inspector goes to check (the meat products in the market), (the seller) gives him money then he will give a stamp (on the product), he doesn't care what is what (the quality)..." (F,age 29,urban,FG10). "About inspection, in reality they (the sellers/ transporters) still transport many, one truck with hundreds of pigs, then to the market, clearly there are stamps on the pork but do they really know what the quality is, stamp then collect money... we still need to go to the market, don't know which pig is good, which one is sick." (F, age 48, urban, FG9). Ban on selling raw animal blood "The trade is everywhere at small scales in this rural area, can't control. Even when they come, they did not have strong actions on the people they know." (F, age 38, rural, FG1). "Ban it (tiet canh) but they (the sellers) still sell it illegally... They keep it in the fridge inside, anyone who wants to eat can ask and they will bring it out." (F,age 50,urban,FG10). "There is still a demand, then no one able to control, can you control it both day and night? So you can prohibit them now, they continue it another time, you punish them with big money they still keep the practice." (M, age 63, urban, FG6).