Consumer knowledge and practices to pork safety in two Taenia solium cysticercosis endemic districts in Eastern Cape Province of South Africa

Background Globally, Taenia solium can cause cysticercosis in humans (including neurocysticercosis) and in pigs through ingestion of eggs and taeniasis in humans through ingestion of raw/undercooked pork contaminated with mature cysts. It is now recognised globally as one of the most prevalent food-borne parasitic diseases. The majority of cases have been reported in developing countries where consumption of food produced under unhygienic conditions is prevalent, exacerbated by lack of food safety education. The aim of this study was to determine the knowledge and practices of consumers towards pork safety in two districts of the Eastern Cape Province of South Africa, where T. solium cysticercosis is endemic in pigs and humans. Methods Three-hundred-and-sixty-one (361) participants were conveniently interviewed on consumer knowledge (harmfulness of T. solium cysticercosis, ability to identify cysts, trustworthiness of registered butcheries and legal requirements) and practices (storage of pork and method(s) of cooking pork safely) through a structured questionnaire. Chi-square for association of variables was used to compare differences in the districts. Results Overall, 73.1% of the study group from both districts agreed that pork forms an important part of their diet. Consumers (54.2%: 189/349) agreed that pork infected with T. solium cysts could be harmful, and 57.3% (188/328) indicated their inability to identify T. solium cysts in pork when slaughtered at home. Although 69.5% (234/352) trusted pork bought from butcheries, only 52.2% (187/358) were aware that butcheries must present a registration certificate in order to operate. This coincides with the fact that very few (< 10%) were aware of the legal requirements in terms of disease control, slaughter and food preparation. Most consumers (88.7%: 268/302) kept pork in the fridge and only 11.3% (34/302) kept it in a freezer (p = 0.02). Although not significantly different between the districts (p = 0.15), consumers in Alfred Nzo (71.4%: 152/213) and OR Tambo (61.2%: 74/12) mostly cooked pork as a stew, followed by braai/barbeque and frying or baking. This was in line with the fact that consumers in Alfred Nzo (79%: 147/186) and OR Tambo (80.8%: 120) preferred well-cooked pork; the main reason for this was the belief that cooking kills germs (43.6%: 121/277) followed by rendering the meat tasty (26.4%: 73/277). Conclusions Consumers surveyed in the two districts were somewhat aware that T. solium cysticercosis could be harmful, although some were not able to identify T. solium cysts in pork. They also lacked sufficient knowledge regarding butchery certification and other legal requirements related to disease control, slaughter and food preparation. Practices related to cooking have the potential to promote the transmission of human taeniasis and the fact that most respondents preferred stewed pork could be a positive sign, as the cysts are destroyed during the cooking process. Results from this study are useful for the development of a control and prevention strategy targeted towards consumers, and the creation of awareness of food safety, with special emphasis on T, solium cysticercosis.


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Conclusions: Consumers surveyed in the two districts were somewhat aware that T. solium cysticercosis could be harmful, although some were not able to identify T. solium cysts in pork. They also lacked sufficient knowledge regarding butchery certification and other legal requirements related to disease control, slaughter and food preparation. Practices related to cooking have the potential to promote the transmission of human taeniasis and the fact that most respondents preferred stewed pork could be a positive sign, as the cysts are destroyed during the cooking process. Results from this study are useful for the development of a control and prevention strategy targeted towards consumers, and the creation of awareness of food safety, with special emphasis on T, solium cysticercosis.
Keywords: Taenia solium cysticercosis, Food/meat safety, Consumer knowledge and practices Background Food-borne diseases have become widespread and are a serious public health problem, especially in industrialised countries where the percentage of people infected by food-borne diseases each year has been increasing [1]. This has been attributed to industrialisation of animal production, mass food processing and distribution, globalisation of the food trade and increased mobility of people and goods around the world [1,2]. Food-borne parasitic diseases result in considerable morbidity and mortality [3], and T. solium is among the list of foodborne zoonotic parasites known to cause epilepsy and other neurological sequelae in populations across sub-Saharan Africa [3]. When pig (intermediate host) ingests faeces contaminated with T. solium eggs, larvae invade the body of the animal, mostly in the subcutaneous fat, muscles or brain, resulting in porcine cysticercosis. When human (definitive host) ingests infected (metacestode) in under-cooked or raw pork this develops to mature form of the tapeworm, causing taeniasis. Humans occasionally become intermediate hosts by drinking water or eating food contaminated with T. solium eggs or by transferring eggs to mouth with contaminated hands or through autoinfection. This may result in human cysticercosis and/or neurocysticercosis. Taenia solium cysticercosis is an underreported and neglected zoonotic disease in man and pigs in many developing countries [4] and has been classified as one of the most important global foodborne parasites [5]. The public health and economic impacts are difficult to determine because of the complexities of the disease in resource-poor livestock farming and the economic loss due to meat condemnation (lack of affordable diagnostic tools in humans, ineffectiveness of meat inspection in detecting cysts, home slaughter of pigs and stigma related to NCC in endemic areas) [6][7][8]. In South Africa, the diseases' cost was estimated to be USD 5 million for the agricultural sector alone, with an overall cost of between USD 18.6 million and USD 34.2 million [6].
Despite strong evidence indicating that T. solium is an important pathogen of resource-poor, pig farming communities in South Africa, there has been only one report on the prevalence of porcine cysticercosis of 64.6% in the villages of Alfred Nzo and OR Tambo Districts of the Eastern Cape Province, South Africa [9]. However in the past 30 years, several hospital surveys utilising serological and/or radiological diagnostic techniques have indicated that 28-50% of epileptic cases including children were positive for cysticercosis [10]. Inactive and active NCC detected through computed tomography CT scans were found in 61.1% of patients with epilepsy in Lusikisiki, in the Alfred Nzo District of South Africa [11].
South Africa has the largest number of pigs in sub-Saharan Africa, of which approximately 25% are free ranging and owned by emerging pig producers in resource-poor areas of the country [9,12]. As part of this study, Sithole et al. [13] reported on pig husbandry practices, pig health management, feeding, marketing and slaughter of pigs by farmers in two districts of Eastern Cape Province, South Africa. Results showed that pigs were managed under traditional free range, resulting in them roaming freely with other domestic animals such as cattle, sheep, goats, chickens, dogs and game.
Although meat inspection has traditionally been the main means of control to detect cysts at slaughter, the effectiveness of the method is poor and has some limitations in terms of sensitivity [14,15]. Sithole et al. [16] also confirmed that meat inspection alone was insufficient to detect porcine cysticercosis and therefore suggested additional multiple incisions on the heart, tongue, shank and masticatory muscles to improve cyst detection.
Although studies on T. solium cysticercosis have been conducted in Alfred Nzo and OR Tambo Districts [12,17] no study has been carried out on consumer knowledge and practices on pork safety. The objective of this study therefore was to assess consumer knowledge and practices of pork safety in two T. solium cysticercosis endemic districts in Eastern Cape Province, South Africa.

Study areas
The study was conducted in villages located in two district municipalities of Eastern Cape Province, namely Alfred Nzo and O.R. Tambo Districts and the demographic characteristics and prevalence of T. solium taeniasis/cysticerosis in the two locations have been previously described [17].

Study design
This study forms part of a larger study related to the occurrence and detection of T. solium in Eastern Cape Province of South Africa. A cross-sectional communitybased study was conducted between August and October 2016. Prior to commencement of the survey, an inception meeting was held with the representatives of the local House of Traditional Leaders to explain the purpose of the study. Convenience sampling, which is a non-probability sampling technique, was used to select respondents based on their accessibility and willingness to participate in the study.
Three-hundred-and-sixty-one (361) household heads, originating from 30 villages of Alfred Nzo (n = 236) and OR Tambo (n = 125) districts were included. A structured questionnaire collected information from consumers on demographics (age, gender, level of education), consumer knowledge (knowledge of T. solium cysticercosis, ability to identify cysts, trustworthiness of butcheries and legal requirements) and practices (storage, methods of cooking) towards pork safety. The questionnaire was translated into IsiXhosa, which is the native language of both the study districts and was pre-tested with five consumers per district and improvements were made prior to the administration to study participants. The pre-tested questionnaires were not included in the results. Due to the high level of illiteracy among villagers, interviews, with the aid of the translated structured questionnaire, were conducted by the researcher and a research assistant both of whom were conversant with IsiXhosa. In South Africa, persons under 18 years of age are regarded as minors therefore, no such person was interviewed during the study.

Data analysis
Due to the nature of the questions, not all were answered by respondents and therefore the sample size (n) of the variables differed. Frequencies observed within the categories of each question and between districts were tested by constructing row x column frequency tables of meaningful associations and a Chi-square (χ 2 ) test for independence (association) of variables (p ≤ 0.05 at 95% CL were regarded as significantly different) [18]. All data analyses were done using SAS Statistical Software [19].

Results
In total, 361 questionnaires were completed, of which 65.4% (236) were from Alfred Nzo and 34.6% (125) from OR Tambo district (p = 0.03). Overall, 73.1% of the respondents from the two districts confirmed that pork formed an important part of their diet. Table 1 shows the socio-demographic characteristics of respondents from the two study districts. Gender distribution between the two districts differed significantly (p = 0.03), with most respondents being males (56.2%: 203/361). Of the 296 (n = 358) from both districts who indicated that they purchase meat themselves, 56% were males. The age distribution of respondents from the two districts was significantly different (χ 2 (df = 5) 50.0; p = 0.01), with a mean age of 45 years (range = 18-88 years) for Alfred Nzo, and 34 years (range = 18-80 years) for OR Tambo. The number of family members per household for both districts ranged from one to five, with a mean of three (χ 2 (df = 4) 7.3; p = 0.11

Consumer practices
A summary of the respondents' practices on pork preparations and consumptions is shown in

Discussion
There is a strong relationship between consumer perception of risks, trust in food safety and purchasing behaviour [20]. This study revealed that there were more men responsible for meat purchasing compared to women, which was an interesting phenomenon. In most African cultural practices, it is the responsibility of women to buy and cook food for the family [21], as women tend to be more aware of food safety than men [22]. In this case, a possible intervention would be to establish educational food safety programmes specifically for food handlers. The high level of unemployment was comparable to that of previous studies (approximately 55%) in the area [9,23] and this compels people to buy pork and other meat from cheap informal/illegal food vendors, or to slaughter animals themselves for own consumption and commercial purposes to enhance income [24]. Of concern was that a high percentage of   Note: p < 0.05 denote significant difference in association between the Alfred Nzo and OR Tambo Districts consumers had an education level below grade 9, which is the minimum school education level in South Africa [25]. This result is similar to that of other reports in Alfred Nzo, where 58% of respondents were without formal education [26] and OR Tambo had 26% with no schooling at all [27]. It has been reported that a low level of education exacerbates a high unemployment rate [25,28,29], and this may impact negatively on public health initiatives targeted to improve consumers knowledge and practices on consumption of safe pork [30]. Due to the low level of education, the general lack of knowledge on food legislation was expected. Improving the knowledge levels of consumers could advance food safety legislation awareness [31,32]. In the South African context, awareness regarding hygiene practices and legal requirements may be enhanced by structures such as National and Provincial Departments of Health and of Agriculture, Food and Fisheries and the National Consumer Commission of South Africa who are mandated to ensure the welfare of consumers, which includes the implementation of relevant policies and strategies to ensure safe pork production in rural settings, such as the areas from this study.
Even though participants referred to cysts as "Amaqhakuva, Amaqhanqa or Intshulube" in IsiXhosa, it was of particular concern that almost half of the participants (45.9%) believed that pork with cysticercosis may not be harmful. This could be ascribed to the complexity of the life cycle of T. solium involving humans, pigs and environment; lack of knowledge and awareness of the public health importance of the parasite. Furthermore, since pork was bought from local butcheries there might be an element of trust that the pork was safe, without realising the possible consequences of consuming uninspected pork infected with T. solium cysts. This was similar to studies in Tanzania and Zimbabwe [33,34], where it was reported that infected pork was purchased from unregistered fresh meat markets. A study conducted by Soji et al. [35], in South Africa, reported that consumers do not mind purchasing meat from formal or informal suppliers as long as it is affordable. This constitutes the need for consumer awareness campaigns by relevant authorities and other stakeholders. The development of schemes that would allow for gradual development of compliance would allow for interim registration and monitoring of butcheries on a regular basis to ensure safe meat products for human consumption (Powell et al., 2013).
The low percentage of consumers using freezers may be ascribed to the unaffordability thereof and the unavailability of electricity in most villages. This is an unfortunate situation as freezing of meat with T. solium  [36]. The South African red meat regulations prescribe temperatures of − 10°C for 10 days or − 18°C for 3 days to inactivate the T. solium in pork meat [37]. It was proven that domestic freezers were capable of maintaining temperatures of − 20.3°C, [38], which fell within the aforementioned temperature ranges and thus should have the capacity to deactivate T. solium cysts. However, the fact that most consumers preferred stewed pork was fortunate as this normally requires slow cooking for longer periods [39] wherein T. solium cysts can be inactivated when the pork reach an internal temperature of 65°C [40]. The other preparation methods, such as braai/barbeque, especially medium to rare are risky, as T. solium cysts may not be killed and consumers are exposed to infection [41].

Conclusion
This study confirmed that the majority of consumers from the study areas believed pork formed part of their diet as a source of protein, thus emphasising that rural pig farming would remain a source of livelihood for resource-poor farmers. Ensuring food safety, requires effective food safety systems that are vital to maintain consumer confidence and provide a sound regulatory foundation for domestic and international trade in food, which supports economic development [42]. This study revealed that pork consumers in the study areas have the likelihood of being exposed to pork infected with T. solium cysts, mainly due to eating uninspected pork derived from home-slaughtered pigs or buying of pork from unregistered sources and following unsafe cooking practices. Given the importance of this parasite, awareness programmes for consumers should be initiated on the importance of consuming safe pork, and the zoonotic importance of T. solium since the parasite is endemic in these areas.