Understanding attitude, practices and knowledge of zoonotic infectious disease risks among poultry farmers in Ghana

Abstract Zoonotic infectious diseases (ZIDs) are increasing globally, and livestock farmers in low‐ and middle‐income countries are at particularly high risk. An evaluation of farmer's behaviour on farms can be used to identify the risk factors and to develop tailored control strategies. This study documents the knowledge of zoonotic poultry diseases (ZPD) among 152 poultry farm workers (respondents) from 76 farms in the Ashanti region of Ghana and assessed their on‐farm attitude and practices that increase their risk to exposure of ZPD. The median age of respondents was 29 years, 91.4% (n = 139) had a formal education, and 80.9% (n = 123) had worked on the farm for more than 1 year. The majority of farms (n = 69, 90.8%) had multiple flocks and 27.6% (n = 21) kept other animals, of which 57.1% (n = 12) were pigs. The majority of respondents had good knowledge about poultry diseases but not about ZPD. A higher level of education and longer work experience improved respondents’ knowledge of poultry and ZPD. Although respondents identified the wearing of personal protective equipment (PPE) as a major ZPD preventive measure, the majority did not put that knowledge into practice. Most farms (71.1%, n = 54) had no footbath and 55.3% (n = 42) deposited farm‐waste on the farm. While 97.4% (n = 148) of respondents washed their hands after working, only 48.7% (n = 74) wore protective footwear, 2.7% (n = 4) wore overalls, 2% (n = 3) wore nose masks and none (n = 0) wore gloves. The husbandry practices and attitude of farmers expose them to pathogens on the farm and increase their risk of becoming infected with ZPD in the sub‐region. The results from this study could be used to promote human health among farm workers in Ghana.

revenue loss from the imposition of trade restrictions, low patronage by consumers and increased marketing costs to regain consumer confidence may impede economic growth of countries, where ZIDs are common in farmed livestock (Halliday et al., 2015;McDermott & Arimi, 2002;WHO, 2006). There has been a growing demand for animal products in many urban and peri-urban communities in low-and middle-income countries (LMIC) due to increasing rural-urban migration, and changes in socio-cultural and socio-economic status. This has contributed to intensification of livestock production in densely populated areas, thus increasing the risk of human infections with zoonotic pathogens (Thornton, 2010;Zinsstag et al., 2007). Livestock farmers remain at high risk of acquiring ZIDs due to their proximity and frequent contact with the animals and their environment.
Thirty percent of livestock farmers from developing countries live in sub-Saharan Africa (Thornton et al., 2002). Their husbandry practices are often based on traditional knowledge and skills inherited from their ancestors, which may be fused with modern methods of livestock keeping. Such practices may differ between and within countries even for the same species and therefore the potential risk of becoming infected with ZIDs may differ (FAO, 2009;Mangesho et al., 2017). Poultry production is a major component of the livestock sector in Ghana and contributes substantially to the animal protein source and food security.
Several poultry diseases with both zoonotic and non-zoonotic potential characterise the industry (Andoh et al., 2016;Ayim-Akonor, Obiri-Danso, Toah-Akonor, & Sellers, 2018;FAO, 2014). Three outbreaks of highly pathogenic avian influenza virus (HPAIV) H5 have affected the Ghanaian poultry industry in the last 12 years (Asante et al., 2016;OIE, 2019). Although no human infections occurred, the risk to poultry farmers remains high; 16 countries worldwide have recorded human infections with a 53% fatality rate and contact with infected poultry or the environment was identified as transmission pathways (WHO, 2019).
In this study, we aimed to assess the knowledge level of poultry farmers regarding zoonotic poultry disease (ZPD) and further evaluate their on-farm attitude and practices that increase their risk of becoming infected with ZPD. The information will provide baseline data to develop practical control methods to reduce zoonotic transmission among poultry farmers in sub-Saharan Africa.

| Study area
The study was performed in the Ashanti region of Ghana from April 2016 to February 2017. The Ashanti region is located in the forest belt of the country. It is the third largest region covering 10.2% of the total country land size. The region has the highest human population (19.4% of national population). The Ashanti region is the second largest poultry-producing region, holding 28% of the total poultry population in Ghana. Breeders, layers (egg-type) and broilers (meat-type) form the

| Ethical consideration
Ethical approval for the study was obtained from the ethics committees of the Council for Scientific and Industrial Research, Ghana (RPN 001/CSIR-IACUC/2016) and the Ethik-Kommission der Ärztekammer Hamburg (PV5296) in Germany.

| Farm selection
Members of the regional poultry farmer association were contacted personally or through a mobile phone call. The study was explained to the farmers and, where informed consent was provided, farms were visited to conduct interviews. Famers were asked whether they knew colleagues who were not members of the poultry farmer association, and these were considered as potential study participants (snow-ball sampling). Questionnaires were administered only on farms if birds were present and at least one farm worker worked at the time of visit.

| Questionnaire administration
A questionnaire with open-ended and close-ended questions was used. Questionnaires were administered in English and in the local language 'Twi' (responses were translated into English for analysis).
The questionnaire included sections on farm characteristics, farm husbandry practices, demographics, biosecurity practices, knowledge of poultry diseases, awareness of zoonotic diseases and selfprotection from zoonotic diseases.

| Data entry and analysis
Medians and interquartile ranges were computed for continuous variables, and the frequency and percentages were computed for categorical variables. Data on age, education and length of employment on the farm were dichotomised to calculate association measures. A dichotomised knowledge level score of poultry diseases (good or poor) was developed based on the respondents' ability to name at least one correct visible clinical sign indicating animal disease and being able to name at least one poultry disease and its corresponding clinical signs. A dichotomised knowledge level score of ZPDs (good or poor) was developed based on the respondents' awareness of becoming infected with certain diseases of poultry, correctly naming at least one zoonotic poultry disease, and mentioning at least one method to protect against zoonotic poultry disease. Risk ratios (RR), with their corresponding 95% confidence intervals (CI), were calculated to estimate associations between the dichotomised scores and individual characteristics. A binomial regression model, with a log-link function, was fitted to calculate multivariate models. Backward elimination was applied to select the final models. All analyses were conducted using the statistical program Stata (Version 14, StataCorp).

| Farm characteristics
In all, 76 poultry farms in the study region were visited during the sampling period. Seven farms were reported to have one flock (9.2%), 38 (50%) to have two or three flocks and 31 (40.8%) to have more than three flocks. The total number of birds on the farms varied from 50 to more than 10,000. In all, 55 farms had less than 5,000 birds (72.4%), 13 (17.1%) had 5,000-10,000 birds and eight (10.5%) had more than 10,000 birds. Most farms (n = 55, 72.4%) kept only chickens. Some farms (n = 21, 27.6%) additionally kept other animals, predominantly pigs (n = 12, 57.1%), ruminants (n = 7, 33.3%) and others such as freerange chicken, ducks, guinea fowl and turkeys. The majority of farms

| Safety and hygiene practices of respondents on the farm
Respondents reported on various safety and hygiene practices that they perform routinely on their farms. Most respondents (n = 148, 97.4%) changed their clothes before starting work on the farm. Few respondents (n = 4, 2.7%) wore 'overalls' and nearly half (n = 74, 48.7%) wore footwear that covers the entire foot. Most respondents (n = 151, 99.3%) changed their footwear before leaving the farm.
The majority of respondents (n = 149, 98%) did not wear nose masks and none (n = 152, 100%) wore gloves when working on the farm.

| Knowledge of poultry diseases
Most respondents (n = 132, 86.8%) could identify when their birds were sick. Respondents used clinical signs exhibited by their chickens to determine their health status. Common clinical signs reported comprised the following: greenish diarrhoea, weakness, loss of appetite, trachea rales, cough, sneeze, drop in egg production, bloody spots in faeces, pox on comb and ruffled feathers. Of the respondents who could identify sick animals by clinical signs, very few (n = 29, 22%) could not name any poultry disease. The majority of respondents (n = 101, 76.5%) correctly named at least one poultry disease with one or more associated clinical sign(s). In total, respondents named 12 different poultry diseases ( Figure 1). NDV, Gumboro disease and Coccidiosis were most frequently named while infectious bronchitis and salmonellosis were the least frequently mentioned (Figure 1).

| Awareness and self-protection from zoonotic poultry diseases
In all, 87 (57.2%) respondents were aware that they could become infected with certain poultry diseases. Of those, nearly half (n = 39, 44.8%) could name at least one zoonotic poultry disease. Respondents named avian influenza (AI), NDV and salmonellosis as diseases they could contract from their poultry. AI was the most frequently named  or less on the farm (RR = 1.5, 95% CI = 1.2-1.9). In binomial regression, estimates comparable to the crude results were calculated (Table 3).
The knowledge level of respondents on ZPD varied considerably from their knowledge of poultry diseases. A quarter (n = 38, 25%) of respondents had good knowledge about ZPD. Respondents with a higher education level were 10 times more likely to have good knowledge of ZPD than respondents with a lower education level (RR = 9.7, 95% CI = 3.6-26.0). Respondents, who worked on the farm for >5 years, were about twice as likely to have good knowledge of ZPD than respondents with up to 5 years of employment experience (RR = 2.0, 95% CI = 1.1-3.3). The binary regression yields comparable results as the crude estimates, highlighting that the chosen variables were unconfounded (Table 4).  TA B L E 4 Factors influencing respondents' knowledge of zoonotic poultry diseases soap in hand washing that is effective in reducing risk of infection significantly. We did not explore the use of detergents by respondents and can therefore not determine the reduced risk level of hand washing. Respondents did not wear nose masks and remain at high risk of airborne transmitted ZIDs such as AI if circulating in the farms (Harder, Buda, Hengel, Beer, & Mettenleiter, 2016).

| D ISCUSS I ON
Gloves were not worn and farm clothing was predominantly a separate set of clothes (often a T-shirt and a pair of shorts or trousers) that the farmer kept on the farm. The use of these separate clothing does not provide the same level of protection as would be provided by overalls (Odo et al., 2015). Interestingly, the majority of respondents had formal education and largely recognised that wearing of PPE is an important preventive measure for ZIDs yet did not implement their use. According to the FAO (2014), poultry farmers in Ghana received extensive training on biosecurity and biosafety practices after the original AI outbreak. However, this study reveals poor adoption and implementation among respondents, implying that education and awareness alone may not be enough to bring about behavioural change among farmers.
Behavioural change among respondents may require a multidisciplinary approach including communication and economic analysis. The poor adoption of PPE we observe here is similar to that reported in Bangladesh and Thailand (Odo et al., 2015;Sarker, Sumon, Khan, & Islam, 2016).
Infectious diseases are of major concern to the global poultry industry as frequent outbreaks reduce net profit margins. Our respondents had good knowledge about poultry diseases, particularly those that are endemic and have major economic importance in the country (FAO, 2014

ACK N OWLED G EM ENTS
The authors are grateful to the poultry farmers who participated in the study. This study forms part of a larger study of 'Influenza at the human-animal interface in Ghana' and financially supported by the West Africa Agricultural Productivity Programme (WAAPP II) and International Foundation for Science (IFS, Sweden).

CO N FLI C T O F I NTE R E S T
Authors and funders declare no conflict of interest.