Knowledge and Practices on Consumption of Free-Range Chicken Viscera in Selected Rural Communities of Kwazulu-Natal, South Africa, with Focus on Zoonotic Transmission of Toxoplasma Gondii and Toxocara Spp.

Free-range chickens (FRC) are a host to a variety of pathogens of zoonotic and economic importance which includes Toxoplasma gondii and Toxocara spp among others. Humans acquire infections via the ingestion of infective stages of T. gondii and Toxocara spp with raw or undercooked food. This study aimed to assess knowledge and practices on the household consumption of FRC meat and viscera by rural communities in KwaZulu-Natal (KZN), South Africa as risk factors in the transmission of zoonotic pathogens. A descriptive cross-sectional study was conducted among twenty (20) randomly selected households in each selected community on the northern coast (Gingindlovu and Ozwathini) and southern coast (uMzinto and Shongweni) of KZN province. An adult from each household was interviewed on FRC consumption practices using a semi-structured questionnaire. Data were analyzed using statistical package for social sciences (SPSS) version 25.0. Descriptive, and Chi-square statistics were used to assess knowledge and practices related to FRC consumption and zoonoses transmission. Knowledge of zoonosis transmission was estimated at (31.3%, 25/80) in the four localities and a signicant association was found between the educational level of respondents and study locations (p<0.05). Knowledge was highest among respondents with a high school education (13.75%, 11/80) and lowest (1.3%, 1/80) among respondents with no formal education. Overall, over three-quarters (76.3%, 61/80) of respondents reported chicken viscera consumption although majority (96.7%, 59/80) preferred eating them ‘well-cooked’. This result underscores the need to intensify awareness on health risk associated with the consumption of raw/undercooked viscera from free-range chickens. and occupation of respondents. Information on ownership of free-range chickens (FRC) including the number of FRC owned per household were also collected. Information on ownership of pets, type of pets, and the number owned was also collected. A cross-sectional study was conducted in four rural communities in KwaZulu-Natal province to assess knowledge and practices of consumption of free-range chicken viscera with a focus on T. gondii and Toxocara spp transmission from March to July 2019. Localities where the study was conducted, and their population sizes are as follows; Gingindlovu (GI) (1,109) and Ozwathini (OZ) (1,979) in the northern coast and uMzinto (MZ) (16,205) and Shongweni (SH) (427,613) in the southern coast of KZN (Fig. These localities have sugar cane as their main followed by livestock farming which include rearing of free-range chickens. The study population comprised 80 randomly selected participants and each participant represented a household. Twenty participants were randomly selected from each of the localities. The sample size was calculated using the following equation with 95% condence level and 11% error margin.


Introduction
Free-range chickens are major agents in parasite transmission due to their exposure to infective stages of parasites existing in contaminated environment (De Vries et al. 2018). Commonly reported parasites from chickens include but not limited to; Toxoplasma gondii and Toxocara spp (Zibaei et al. 2017; dos Santos Silva et al. 2020). Toxoplasma gondii is an apicomplexan parasite that causes toxoplasmosis in animals and humans globally (Dubey 2020). The main de nitive hosts are felids while birds and a wide range of animals serve as the intermediate hosts (Gaulin et al. 2020). Although Toxocara canis and T. cati are helminth parasites of canids and felids, they also are responsible for human toxocariasis worldwide (Yoshida et al. 2016).
Although free-range chickens (FRC) contribute signi cantly to animal protein, reports on their role in transmitting zoonotic pathogens is scanty (Rodrigues et al. 2019). Free-range chickens are infected during scavenging when they ingest the infective stage of parasites from the contaminated environment (Sasse et al. 2020). Humans acquire infection indirectly via the consumption of raw or undercooked infected chicken viscera or meat containing tissue cysts (T. gondii) or larvae (T. canis and T. cati) (Fan et al. 2015; Gaulin et al. 2020). Once ingested by humans, the parasites migrate through the viscera and are deposited in various organs where they cause varying degrees of diseases ranging from fever, headache, sore throat, arthralgia, myalgia, and blindness depending on the affected organs, infection intensity and duration, host age and immunity status of the infected host ( Consumption of poultry meat viscera is a dietary habit that is common in different communities worldwide and dependent on socio-cultural practices and culinary habits where it can either be eaten raw or undercooked (Broglia and Kapel 2011). The practice of eating raw or undercooked meat or viscera is In South Africa, the greater population lives in rural areas and rear chickens following a free-range system (Mwale and Masika 2009; Mukaratirwa and Khumalo 2010a; Malatji et al. 2016). In KwaZulu-Natal (KZN) province of South Africa, the majority of the population are rural farmers and rear FRC for consumption, marketing and socio-cultural purposes (Naidoo 2005). The farming practice, allows the chickens to scavenge freely in the environment during daytime and use trees for shelter at night or con ned to rustic chicken runs (Naidoo 2005).
The tendency of FRC to pick up T. gondii and Toxocara spp infective oocysts and eggs respectively in the environment increases with the abundance and availability of stray dogs and cats' which are de nitive hosts of the parasites, particularly in KwaZulu-Natal (KZN) province where stray dogs and feral cats have been reported to be abundant (Tannent et al. 2010; Mukaratirwa and Singh 2010b) thereby leading to persistent environmental contamination with these parasites.
Moreover, change in globalization has led to the adoption of a variety of culinary and consumption patterns regarding raw or undercooked food as delicacies (Broglia and Kapel 2011). Besides, due to the high poverty level in rural areas of KZN there is a high level of household food insecurity thereby leading to alternative foods and various ways of food preparation (Tarwireyi and Fanadzo 2013). Understanding the consumption pattern of the much available freerange chicken meat or viscera is imperative in these communities as a basis for guaranteeing food security as well as identifying risks related to food-borne diseases such as toxoplasmosis and toxocariasis.
Considering the poor socio-economic status and food insecurity of the rural communities in KZN province of South Africa, it is imperative to determine household consumption patterns of free-range chicken viscera and preparation practices that may be favouring zoonotic transmission in the study area.
Hence, this study was designed to address this aim with the hope of using the information to create awareness on the health risks associated with the consumption of raw or undercooked FRC meat or viscera.
Methodology A cross-sectional study was conducted in four rural communities in KwaZulu-Natal province to assess knowledge and practices of consumption of free-range chicken viscera with a focus on T. gondii and Toxocara spp transmission from March to July 2019. Localities where the study was conducted, and their population sizes are as follows; Gingindlovu (GI) (1,109) and Ozwathini (OZ) (1,979) in the northern coast and uMzinto (MZ) (16,205) and Shongweni (SH) (427,613) in the southern coast of KZN ( Fig. 1) (http://www.durban.gov.za/). These localities have sugar cane farming as their main livelihood followed by livestock farming which include rearing of free-range chickens. The study population comprised 80 randomly selected participants and each participant represented a household. Twenty participants were randomly selected from each of the localities. The sample size was calculated using the following equation with 95% con dence level and 11% error margin. L=limits of error on the prevalence and the expected prevalence was set at 11%.

Study procedure
After brie ng the community leaders regarding the objectives of the study, 20 household representatives were randomly selected from each locality and consent was obtained regarding their willingness to participate in the study. Questionnaires were translated into isiZulu, which is the local language of all the localities, and were administered to selected participants following an interview-guided approach. Prior to administration, a pilot study was done to validate the tool. The questionnaire administration process took approximately 20 minutes for each participant. Upon completion of questionnaires, participants were enlightened on the dangers associated with zoonosis transmission and prevention methods.
Data collected from the interview included socio-demographic information, knowledge, and practice of participants related to zoonosis transmission.
Questions were asked speci cally on habits on consumption of chicken viscera, type of the viscera eaten, and the preferred method of preparation and designated members of the family who eat each type of viscera. The demographic information collected included age, gender, household size, educational quali cations, and occupation of respondents. Information on ownership of free-range chickens (FRC) including the number of FRC owned per household were also collected. Information on ownership of pets, type of pets, and the number owned was also collected.

Study design and sample
A cross-sectional study was conducted in four rural communities in KwaZulu-Natal province to assess knowledge and practices of consumption of free-range chicken viscera with a focus on T. gondii and Toxocara spp transmission from March to July 2019. Localities where the study was conducted, and their population sizes are as follows; Gingindlovu (GI) (1,109) and Ozwathini (OZ) (1,979) in the northern coast and uMzinto (MZ) (16,205) and Shongweni (SH) (427,613) in the southern coast of KZN ( Fig. 1) (http://www.durban.gov.za/). These localities have sugar cane farming as their main livelihood followed by livestock farming which include rearing of free-range chickens. The study population comprised 80 randomly selected participants and each participant represented a household. Twenty participants were randomly selected from each of the localities. The sample size was calculated using the following equation with 95% con dence level and 11% error margin. L=limits of error on the prevalence and the expected prevalence was set at 11%.

Study procedure
After brie ng the community leaders regarding the objectives of the study, 20 household representatives were randomly selected from each locality and consent was obtained regarding their willingness to participate in the study. Questionnaires were translated into isiZulu, which is the local language of all the localities, and were administered to selected participants following an interview-guided approach. Prior to administration, a pilot study was done to validate the tool. The questionnaire administration process took approximately 20 minutes for each participant. Upon completion of questionnaires, participants were enlightened on the dangers associated with zoonosis transmission and prevention methods.
Data collected from the interview included socio-demographic information, knowledge, and practice of participants related to zoonosis transmission.
Questions were asked speci cally on habits on consumption of chicken viscera, type of the viscera eaten, and the preferred method of preparation and designated members of the family who eat each type of viscera. The demographic information collected included age, gender, household size, educational quali cations, and occupation of respondents. Information on ownership of free-range chickens (FRC) including the number of FRC owned per household were also collected. Information on ownership of pets, type of pets, and the number owned was also collected.

Statistical analysis
Data were processed and analyzed using statistical package for social sciences (SPSS) version 25.0. Descriptive and Chi-square statistics were used to assess knowledge and practices related to the consumption of FRC viscera and risks of transmission of T. gondii and Toxocara spp in KwaZulu-Natal. A pvalue < 0.05 was considered as statistically signi cant.

Statistical analysis
Data were processed and analyzed using statistical package for social sciences (SPSS) version 25.0. Descriptive and Chi-square statistics were used to assess knowledge and practices related to the consumption of FRC viscera and risks of transmission of T. gondii and Toxocara spp in KwaZulu-Natal. A pvalue < 0.05 was considered as statistically signi cant.

Results
Socio-demographic pro le of participants Table 1 shows the demographic characteristics of participants in all four study localities. Participants interviewed in the four localities ranged from the category of father, mother, and household member greater than 18 years (GI-5%, 55%, and 40%; OZ-5%, 80%, and 15%; MZ-10% 50%, and 40%; SH-25%, 60%, and 15%). Overall, the mean age of the respondents was 47.11±18.02) ( The percentage of respondents that were unemployed was highest (90%, 18/20) in OZ, (85%, 17/20) in GI and SH, followed by (70%, 14/20) in MZ. Overall, household size ranged from 1-16 with a mean of (6.40±3.26). Household size ranged from 2-11 with a mean of 7.05±2.65, 2-14 (6.65±3.79), 2-13 (5.70±2.89) and 1-16 (6.20±3.67) in GI, MZ, OZ, and SH respectively ( Table 1). Availability of playground for children was also observed to be signi cantly different among study locations (p<0.05), with only (5%, 1/20) in GI and MZ and (15%, 3/20) in SH having reported to have reserved playground for children in the household respectively while none was reported in OZ (Table 1). Overall, three-quarters (75%, 60/80) of the households utilized household vicinity as playgrounds while only (2.5%, 2/80) had reserved playgrounds for children (Table 1).   (Table 3). A three-way Cross-Tabulation and Chi-square statistic for respondents' categories (father, mother, or household members ≥ 18 years), the types of chicken viscera that were being consumed, and consumption preference showed a signi cant association in all the study locations (p<0.05) with the majority of the respondents (96.7%, 59/80) reporting their consumption preference as 'well-cooked' ( Table 4). The proportion of respondents consuming the combination of all chicken viscera i.e., gizzard, heart, liver, lungs, kidney, and intestines was higher than the other chicken viscera combinations, however, the difference was not signi cant (p>0.05) ( Table 5). Table 4 Responses from participants on type and consumption preference of viscera from free range in four localities in KwaZulu-Natal province of South Africa.

Respondents
Category Viscera type consumed and preferred manner of consumption in Gingindlovu (n = 12)  Father  -------1  1  -0.001   Mother  -----1  2  4  7  -Family members ≥ 18  years   ------2  2  3  1   Total  -----1  4  7  11  1 Respondents Category Viscera type consumed and preferred manner of consumption in Ozwathini (n = 16)  Moreover, the co-existence of dogs, cats, and free-range chickens observed in this study may provide insight into the roles of these animals in transmitting Furthermore, this study showed that 20%) (16/80) of the household owning pets allow them to roam. This may be attributed to low education level of owners thus, negatively in uencing veterinary seeking practice for their pets. This is consistent with other studies who reported the positive in uence of postsecondary education in seeking veterinary services (Pereira et al. 2016). This study underscores the need to intensify awareness on standard pet care practice and risk of disease transmission among animals and from animals to humans.
Regarding consumption patterns, the majority (76.3%, 61/80) of respondents reported the practice of consumption of FRC viscera in the households. The reason for the high demand for chicken viscera in the study area is however unknown. Additionally, viscera of chicken and other avian animals have been reported to be rich in essential nutrients that are highly valuable to humans (Schönfeldt and Gibson 2008).
Despite a high trend in the consumption of chicken viscera, this study does not nd any signi cant association between the consumption of free-range chicken viscera and symptoms of zoonosis (p>0.05). This may be attributed to the respondents' preference for 'well-cooked' viscera. Also, a study reported the important role of mothers in the provision and preparation of healthy meals for their households (Reid et al., 2015) which might be the case in our study.
Although the association between household size and consumption pattern was not signi cant in this study, a previous study showed the inverse relationship between household size and certain food consumption patterns (Abdulai et al. 1999). Considering the high rate of chicken viscera consumption practiced by communities in this study, although most preferred "well-cooked", it is important to intensify awareness on health associated with the consumption of raw/undercooked viscera from free-range chickens.
Declarations Figure 1 Map showing the study location sites in KwaZulu-Natal South Africa