Knowledge, Attitude and Practices of Poultry Farmers on Antimicrobial Use, Resistance and Farm Hygiene Management in Bangladesh

The poultry farming is considered one of the hotspots for the use of antimicrobials. The knowledge, attitude and practices of poultry farmers are closely associated with the prudent use of antimicrobials in poultry farm practices. A cross sectional study was conducted among seventy-four commercial poultry farms using a pretested structured questionnaire survey to assess knowledge, attitude and practices of the poultry farmers regarding antimicrobial use, resistance and farm hygiene management. According to demographics, more farmers were secondary holders (29.72%), followed by higher secondary (22.97%) and illiterate (12.16%) with least number (13.51%) had training on antibiotics but no one had training on AMR. Farmers had sucient knowledge about antibiotics (86.49%) but inadequate knowledge about antimicrobials (14.86%), AMR (51.35%), and animal and sh feed act (20.27%). The majority of farmers strongly agreed that AMR had a negative impact on production (40.54%), human health (36.49%), environment (33.78%) and economy (52.7%). Farm hygiene management revealed that most of them (90.54%) thrown the expired and leftover antibiotics in the open environments. Furthermore, the farm litter was managed diversely with 39.19% kept in open pit; 33.78% used in sh farm and 5.41% used for agricultural land. It was observed that the dead birds were disposed in a variety of ways, buried into ground (58.10%), thrown into eld (9.45%), thrown into bush (6.75%), thrown into garbage (9.45%) and thrown in the water (13.51%). A signicant higher association was found between the level of education and knowledge; level of education with farm practices such as choice of antibiotics, determining doses and duration of antibiotics, disposal of farm wastages, disposal of dead birds, farm biosecurity and vaccination coverage (p<0.05). Continuous education, hands-on training, awareness, and motivation of farmers along with good biosecurity, mass vaccination and proper hygienic measures can minimize the uses of causes using causes AMR; proper doses and antibiotic withdrawal relation between etc.), (iv) attitudes towards (e.g. and for or importance biosecurity, training, vaccination good farm management), (v) practices on AMU and farm operations (e.g. technical support when and how frequency and doses of antibiotics, disposal of leftover antibiotics, farm waste/ litter management footbath farm biosecurity). The interviewee the farm management


Introduction
The poultry subsector plays an important role in promoting agricultural growth and reducing malnutrition in Bangladeshi people (Da Silva and Rankin, 2014; Hamid et al., 2017). Bangladesh's commercial poultry production is growing rapidly to meet the increasing demand for poultry meat and eggs (Imam et al., 2020). It is an integral part of Bangladesh's agricultural system, creating direct and indirect employment opportunities including support services for about 6 million people (Ansari-Lari et al., 2010). Poultry accounts for about 22-27% of the country's total animal protein supply (Hamid et al., 2017). The total investment in the poultry sector is about BDT 35,000 crore and it has created employment opportunities for over 6 million people, majority of them are unemployed youth and women (Saleque and Silvi, 2020). The country has approximately 100 breeder farms & hatcheries, 8 grandparent stock farms, 70,000 commercial layer & broiler farms, more than 200 feed mills and 500 animal health companies (http://wpsa-bb.com/poultry-at-a-glance/). Small scale commercial poultry farm de ned as having less than 5,000 birds in each batch (Begum et al., 2013). It accounts for 81% of the commercial poultry sector, which contributes for about 78% of the total poultry meat supply in Bangladesh (BBS, 2017). Smallholder poultry farms are usually traditional open system houses with natural ventilation, manual feeding and open walls.
In Bangladesh, the level of antibiotic use in animal production is unknown (Khatun et al., 2016) and data on the sale of antibiotics nationwide are unreliable (Ferdous et al., 2019). In addition, frequent sales of antimicrobials by feed and chick traders, and representatives of pharmaceutical companies indicate a lack of governance in the use of antimicrobial agents in Bangladesh (Masud et al., 2020). In addition, there are no regulations on the registration and labeling of veterinary drugs (DGDA, 2016), nor are there speci c guidelines for the use of antimicrobials in livestock (Ferdous et al., 2019). Furthermore, it has been shown that farmers often do not follow the dose and duration recommended by the manufacturer when administering antibiotics to livestock and poultry (Khatun et al., 2016). Antimicrobials are commonly used to treat and prevent poultry diseases, but some farmers use them to promote growth to increase feed conversion ratios (Saiful Islam et al., 2016).
There is increasing concern about the use of antimicrobials in animal feed production and the risk of transmission of antibiotic resistance in the food chain (Laxminarayan et al., 2013). In commercial poultry farms, antimicrobials are more likely to be used for therapeutic purposes without veterinary supervision. Antimicrobials are also used in sub-therapeutic doses by adding them to food and water for prevention, growth promotion, and risk management strategies (Begum et al., 2013). Sub-therapeutic uses of antimicrobials are prevalent in both human medicine and livestock production (Broom et al., 2014). In Bangladesh, the animal and sh feed act, 2010 prohibits the use of antimicrobials in feed (MoFL, 2010).
However, poultry farmers may violate the law by adding antibiotics either in feed and drinking water and provided to chicken. Moreover, governance along with monitoring and surveillance on the poultry farmers are very weak and irregular.
Nonetheless, AMR has been spreading rapidly since last decade and has become a global threat, ultimately causes treatment failure both in humans and animals (Hassan et al., 2020). Lack of legal enforcement of regulation, and selfprescription by farmers, are responsible for the development of AMR, which poses a signi cant threat to public health around the world (WHO, 2021). In Bangladesh most of the poultry farming community are illiterate and they have poor knowledge on rational use of antimicrobials in the production cycle. Most of the poultry farmers are persuaded or motivated by the feed seller or chick seller or pharmaceutical companies to the use of antimicrobials (Masud et al., 2020).
The government of Bangladesh has adopted National Action Plan (NAP) on AMR for the year 2017-2021 but unfortunately the antimicrobial stewardship program in animal health sector was not addressed (MoHFW, 2017).
The rapid growth of poultry farms over time, the accumulation of waste, especially litter and manure, has increased, resulting in environmental impact (Adeoye et al., 2014;Onu et al., 2015). Proper farm hygiene management is a remedy for a long-term productivity, growth and environmental sustainability of the poultry farm. The poultry farm generates abundant amount of solid waste like bedding material (wood shavings, saw dust, straw, rice hulls), feed, feathers, hatchery waste, and waste water with feces, urine, drug and pesticide residues (Moreki and Keaikitse, 2013;Onu et al., 2015). Poultry farm waste contains some essential nutrients which helps in crop cultivation, soil health management and agricultural production (Chan et al., 2008). It also contains microorganisms, hormone, antibiotic and heavy metal residues (Abah et al., 2019). Poultry waste contains high moisture with organic materials, which create environmental problem such as y breeding, odour nuisance and greenhouse gas emission if not disposed of or managed properly (Singh et al., 2018). The dead bird waste is another important driver for the spread of infectious disease as well as environmental pollution (Adeoye et al., 2014).
Poultry farms are considered a hotspot for the use of antimicrobials to treat and prevent diseases. It is also considered the warehouse for spreading of infectious diseases and environmental pollution. It is a demand of time to prevent or reduce the unnecessary and unethical use of antimicrobials in poultry production systems though good farming practices. We can reduce the misuse and overuse of antimicrobials by means of farmer education, motivation, training and awareness building campaigns. There is a scarcity of quality and reliable information about the farmer's knowledge, perception and practices regarding uses of antimicrobials, leading to the development of antimicrobial resistance and farm hygiene management. Considering the backdrop, this study has been undertaken to nd out the knowledge, attitude and practices of the poultry farmers regarding the use of antimicrobials, emergence of antimicrobial resistance and farm hygiene management in Bhaluka, Mymensingh, Bangladesh. The study would reveal knowledge and practice gaps of the farmers and suggests some possible interventions to be needed to minimize the threat of AMR in poultry production system.

Study design and location
A cross-sectional study was conducted from July 2020 to January 2021 among the seventy-four poultry farmers (Seventy-three layer and one broiler) at six villages namely Panihadi, Ditpur, Randia, Dholia, Badepurura and Bohuli at Ditpur Union in Bhaluka sub-district of Mymensingh district. The selected villages were characterized by higher concentration of layer farms with integrated aquaculture farming. The layer farms were mostly medium-scale with ock size 2000 to 3000 birds. Most of the poultry farm wastages were used for aquaculture farming. The layer farms were traditionally managed with minimum or no Good Veterinary Practices (GVP), Good Animal Husbandry Practices (GAHP), Good Agricultural Practices (GAP) along with poor biosecurity measures.

Questionnaire
The structured questionnaire was adopted from a previously published study with signi cant modi cations to meet the objectives of this study (Pham-Duc et al., 2019). We conducted the survey using KoBoCollect software on smartphones. Kobo collect is a user-friendly tool for collecting, compiling, and interpreting eld data. The questionnaire was reviewed by a panel of experts consisting of public health professionals, microbiologists and epidemiologists with extensive experience in food safety and antibiotic resistance. In addition, the questionnaire has been translated into Bengali to facilitate communication with farmers. The questionnaire was divided into four different parts, including general and demographic information, knowledge, attitudes and practices. The farmers were interviewed to elicit their knowledge, attitudes and self-reported practices with regards to antimicrobial use (AMU) and resistance.
Major points were captured by the questionnaire included (i) general information of the respondents/ farmers (e.g. gender, age, education, and main occupation) and their households, poultry farming activities (e.g. number of birds, breed type, feeds & feedings, sources of water, shed type, rearing method, sources of feed, day old chick, purchase of farm inputs, formal/ informal negotiations/ agreement with feed/ chick suppliers and farm waste management), (iii) knowledge about antimicrobial use (AMU) and antimicrobial resistance (AMR) (e.g. understanding with antimicrobials, antimicrobials resistance, name of common antimicrobials, causes of using antibiotics, causes of emergence of AMR, participation in training on AMU, AMR; proper doses and duration of antibiotics; antibiotic withdrawal period; relation between antibiotic use and its resistance etc.), (iv) attitudes towards AMU and AMR (e.g. awareness of AMR effects, potential AMU, and attitude towards using antibiotics for disease prevention or growth promotion, importance of biosecurity, training, vaccination for good farm management), (v) practices on AMU and farm operations (e.g. technical support and suggestions for farm management, measures undertaken when poultry became sick, when and how administer antibiotics to chicken, frequency and doses of antibiotics, disposal of leftover antibiotics, farm waste/ litter management system, uses of disinfectant and footbath for farm biosecurity). The interviewee was the farm management decisionmakers who had detailed information related to questionnaire. Map indicating the survey areas in Bhaluka sub-districts

Data Management and analysis
The data was extracted into an MS Excel spreadsheet for cleaning, processing, and further analysis. Each validated question was analyzed individually and the answers were assigned a score of 1 (correct) or 0 (incorrect). The sum of the responses of each participant in that section was calculated to analyze how each farmer behaved overall in each category of knowledge, attitude and practice. Those who are considered to have more than 50% correct answers to any section of the questionnaire (or re ect practices that impede the development of AMR) may have been evaluated as positive knowledge, attitudes, or practices.

Statistical analysis
The data was analyzed using software version 20 of the Social Science Statistics Package (SPSS). We summarized the data using categories and descriptive statistics such as mean frequency (%) and numerical standard deviation (SD). The chi-square test (χ2) was used to clarify the relationship between sociodemographic characteristics and the value of knowledge, attitude, and practice. Statistical signi cance was measured with a p-value less than 0.05 (p <0.05).

Demographic and general information
The interview has been conducted in seventy-four farms consisting of 33 (44.59%) in PaniHadi, 13 (17.56%) in Randia, 5 (6.7%) in Ditpur, 19 (25.67%) in Dholia, 2 (2.7%) in Badepurara and 2 (2.7%) in Bohuli villages respectively. Almost all of the farmers were male (98.65%) with a single was female (1.35%). Majority farmers (43.24%) had been aged below 30 years old whilst, second highest number of farmers (39.18%) had been aged between 30 to 45 years old and only a single had upper 60 years old. The foremost of the interviewee (86.48%) himself was farm owner followed by manager (9.45%) and remaining was part time workers (4.05%). Maximum farmers had secondary education (29.72%) followed by bachelor degree (22.97%), higher secondary (18.91%), primary education (16.21%) and some had no formal education (12.16%). Poultry farming used to be the secondary occupation of the most of the farmers (51.35%) whereas, almost half (48.64%) of the farmers it had principal occupation. Of all farmers, 49% had 4-6 years, 31% had less than 3 years and 9% had more than 10 years farming experiences. Most of the farm (66.21%) had single shed and 31.08% farms had been running between 3 to 5 batches of poultry. A total of 91.9% farm owners had no formal contract with the feed/chick traders, and 41.89% purchased feed and chicks by cash. It was found that 32.44% farms faced antibiotic treatment failure in the last six months (Table 1). attended the training on the use of antibiotics in the poultry production cycle, but no one received training on antimicrobial resistance. Nearly 60.81% believed that all antibiotics can be used for both humans and animals. About 71.62% believed that higher doses of antibiotics could provide better results in treatments. Nearly 86.49% felt that improper use of antibiotics had an economic impact on farm management. Almost 71.62% had conception that antibiotics can be used as growth promoters and 54.05% said antibiotics can be used for disease prevention. About 66.22% of respondents believed that the withdrawal period should be maintained before selling/slaughtering of chicken. Nearly 62.16% thought that there was no relationship between antibiotic use and antibiotic resistance. The detail of farmer knowledge has given in Table 2A, 2B and 2C.      It was observed that the dead birds were disposed by different means, buried in the ground (58.10%), thrown in the eld (9.45%), thrown in the bush near the farm (6.75%), thrown in the garbage (9.45%) and thrown in the water (13.51%). A number of 91.89% respondent's sprayed disinfectant with regular interval to clean the farm premises. Almost none of the farmers had no footbath (95.95%) and 63.51% had no vaccination schedule so far. The practices of poultry farmers has shown in Table 4.

Association between knowledge and practice
The level of knowledge was not satisfactory, and practices were poor for all farmers. A signi cant higher association was found between the level of education and knowledge; level of education with farm practices such as choice of antibiotics, determining doses and duration of antibiotics, dispose of farm wastages, dispose of dead birds, farm biosecurity and vaccination coverage (p<0.05). Similarly, signi cant association was also found between experiences and farm practices such as choice of antibiotics, determining doses and duration of antibiotics, dispose of farm wastages, dispose of dead birds, farm biosecurity and vaccination coverage (p<0.05). Furthermore, higher statistical association was observed between age and farm practices such as biosecurity, vaccination coverage, dispose of dead birds and dispose of farm wastages (p< 0.05).

Discussion
Poultry farming, particularly broiler and layer, is considered the hotspot in using antimicrobials for therapeutic and nontherapeutic purposes. Conversely, it is thought to be that antimicrobial misuse, abuse and overuse are common practices in poultry rearing communities. Poultry growers believed that without antimicrobials, poultry farms would not be viable and the prevalence of the disease would be higher. Most poultry farmers are illiterate and are not familiar with modern poultry farming practices such as vaccination, biosecurity, waste management and the proper uses of antimicrobials. In our study, we evaluated the knowledge, attitude, and practices (KAP) of poultry farmers regarding AMU, AMR and farm hygiene management. The study described demographic information of farmers, including livelihoods, farm size, and income, retroactive linkages with feed and chick vendors. The study revealed information on farm waste management, in particular the disposal of dead birds, farm litter and fecal waste throwing into environment, aquaculture and agricultural system. The ndings of the study would suggest to improve the practice of the famers about the adoption of good farming practices as well as policy interventions for commercial poultry operations. However, the modalities of our study was more likely to be aligned with other previous studies on antibiotic use and resistance (Chapot et  One study demonstrated that farmers regularly use antibiotics, including those that are not allowed to be used in poultry. Multiple antibiotics have been administered since the rst day of the production cycle to the point of sale. It was found in a study that farmers were used antibiotics ubiquitously for growth promotion and prophylaxis as a risk-management measure (Begum et al., 2013). A study shown that most commercial poultry producers procured antibiotics directly from feed dealers or even directly from pharmaceutical company (GARP, 2018). Other studies shown that most farmers (>60%) used antibiotics without the prescription of the veterinarians (Saiful Islam et al., 2016). Dealers create functional links between input producers and smallholder farmers by sourcing from large companies through their networks and self-credit. Dealers purchase production inputs with credit from the manufacturers and supply it to farms with credits and purchase harvested products from the small farmers, thus keeping the production cycle moving (Mandal et al., 2017). Pharmaceutical representatives are always focused on achieving the sales target and maintaining ongoing liaison with dealerships. Sometimes, to promote the sale of antibiotics pharmaceutical companies provide their own veterinary assistance through dealers to small farmers. There is a substantial penetration and promotion of animal drug usage by pharmaceutical companies and their agents (Roess et al., 2013).
Most farmers have used antimicrobials for therapeutic and prophylaxis purposes. Prophylactic use of antimicrobials can occur due to a lack of knowledge and frequent advice from the drug vendor. The farmers believed that preventive usage of antimicrobials might reduce the disease burden and to stop frequently occurring poultry diseases (Roess et al., 2013) or because vaccination against poultry diseases has not been carried out. In addition, farmers believed that prophylactic use of antibiotics could save veterinary costs and treatment costs by reducing the prevalence of illness. (Okeke et al., 2005). Farmers were not interested in going to a local veterinary hospital because of communication problems and sometimes lack of self-con dence and reluctant attitude. Laboratory con rmation of poultry diseases and antimicrobial susceptibility testing facilities were not available in rural Bangladesh. Thus, farmers might be unable to use the facility of laboratories to diagnose diseases, which could result in a widespread prophylactic administration of antimicrobials based on farmers' perceptions of disease risk or their own experience. Farmers did not report the use of antimicrobials as growth promoters. It must inform the farmers about the unnecessary uses of antimicrobials for growth promotion and preemptive purposes and might abstain from using antimicrobials for this purpose (Saiful . Preventive use of antibiotics in commercial poultry production is also common in other Asian countries, including Cambodia, Indonesia, Vietnam and Thailand (Coyne et al., 2019).
There few antimicrobials were common and frequently administered in the poultry farming in our study area such as were penicillin, ampicillin, cloxacillin, gentamicin, streptomycin, oxytetracycline, ceftriaxone, cipro oxacin, amoxicillin, sulfamethoxazole-trimethoprim and tylosin. Among these, cipro oxacin and tylosin are considered 'Highest Priority Critically Important Antimicrobials' for public health (WHO, 2019). Indeed, cipro oxacin and tylosin are used as the last resort for the treatment of infectious diseases. Among these, tylosin is used for the treatment of MDR Salmonella spp., and Shigella infections, Campylobacter spp. and Legionella whilst cipro oxacin is used for the treatment of MDR Salmonella spp., and Campylobacter spp. (WHO, 2020). It was recommended that cipro oxacin and tylosin should not to be used as rst choice of therapy in poultry and only can be administered after culture and sensitivity testing of the pathogens. In fact, cipro oxacin and colistin should never be administered to feed-producing animals, including chickens, in the absence of clinical signs (OIE, 2020). Surprisingly, many farmers have used antimicrobials (including cipro oxacin, tylosin and colistin) without noticing clinical signs.
It has been observed that poultry farmers of the study areas administered antimicrobials through drinking water which is similar with preceding ndings (Masud et al., 2020). Bangladesh has enacted the "animal and sh feed act 2010" that prohibits the mixing of antimicrobials with animal feed and provides for a penalty if anybody violate the act (MoFL, 2010). However, some farmers may have broken the law regarding antimicrobials in feed, even though they did not admit it. Farmers had no clear conception about antimicrobial residue and withdrawal period and were selling eggs while administering antimicrobials (Ferdous et al., 2019). A lack of monitoring from governmental agencies had been previously identi ed as a reason why withdrawal periods were not followed by farmers (Imam et al., 2020). It is suggested to have surveillance of farm management practices, as well as surveillance of antimicrobial residues in accordance with Codex standards (FAO, 2020).
Vaccines are promising alternatives to antibiotics (WHO, 2014). Numerous studies have shown that the use of various bacterial and viral vaccines in animal populations can lead to signi cant reductions in antibiotic consumption (Murphy et al., 2017). Vaccines can be used to prevent or control infections in animal populations, or to minimize clinical symptoms and minimize post-infection (Holt and Gast, 2004). Conceptually, vaccines reduce the risk of developing antimicrobial resistance by preventing infection and reducing the need for antibiotics to treat primary or secondary bacterial infections after viral or parasitic infections. In addition, vaccines help to eliminate speci c pathogens as the cause of the disease and allow the use of narrower spectrum antibiotics by reducing the pressure of the disease in the population by boosting herd immunity (Lipsitch and Siber, 2016). Vaccine has potential effects on the reduction of bacterial population density and consequent resistance gene (Lipsitch and Siber, 2016). Biosafety is a powerful tool for reducing antibiotic consumption in animals. Improving biosecurity practices means that bacteria have less chance of developing resistance and that antibiotics remain effective when they are needed to treat the disease.
Our research revealed that poultry farm hygiene was not up to the mark and farm waste was not well managed or decomposed. Direct poultry farm waste is drained to the nearest pond for aquaculture and, to a certain extent, to agricultural land. In addition, farmers thrown the dead or diseased bird directly into nearby land or water sources.
Consequently, poultry farm waste has polluted the environment and may exaggerate the occurrence of AMR pathogens in the environment. Poultry production generates signi cant amounts of excretion including solid waste and wastewater.  (Thanner et al., 2016). Fecal contamination is considered to be important drivers to the spread of pathogenic and AMR bacteria across the poultry production cycle (Imam et al., 2020). Fecal contamination can also contribute to spread of resistant determinants into soil, surface water, ground water, and agricultural crops (Su et al., 2015). Poultry production operations utilize untreated water that could subsequently expose poultry to resistant bacteria (Talukdar et al., 2013). This study contained a number of limitations. Firstly, geographical representation with a small number of farmers was taken into consideration. The study was conducted in a small cluster of commercial poultry farming community which may have some different practices due to geographic location, culture and access to inputs and farming practices compared with other parts of the country. Second, the quality of some of the interview data could have been in uenced by recall and self-reported practices in participants. Although this study evaluated the knowledge, attitude, and practices associated with AMU, AMR and farm hygiene measures, but more robust countrywide survey is needed to understand the cultural, social, and agro-ecological factors to identify the differences of KAP in different region of the country.

Conclusion
Antimicrobials are commonly used for therapeutic, preventive and growth promotion in the poultry farms. Farmers had inadequate knowledge and poor practices regarding use of antimicrobials and farm hygiene precautions in the production cycle. Farmer's education, experiences and age played signi cant role towards the rational use of antibiotics and good farm management interventions. In addition, a rigorous regulatory holistic approach on antibiotic use, marketing and prescribing helps to improve antibiotic misuse and reduce antibiotic resistance. It is suggested to improve farmers' knowledge, attitude and practices through good governance, motivation, training and outreach. Farmers should be made aware of good farm hygienic practices, on-farm biosecurity and the vaccination campaign. All farms must be registered with the livestock departments for continuous monitoring and surveillance of farm biosecurity, waste management and antimicrobial uses regime.

Declarations
Declaration of competing interest The authors declare no actual or potential con ict of interest with other people or organizations that might in uence the associated research.