Our study contributes to the existing understanding of antibiotic use by poultry farmers in their farms. It demonstrates that farmers’ use of antibiotics is driven by an interplay of social and economic factors. Injudicious use enhances the risk of AMR in animals, humans and the environment.

Infection control practices

Diseases posed a significant challenge among the interviewed poultry farmers driving antibiotic use. Central to reducing antibiotics use is disease control through measures such as biosecurity procedures and vaccination. This has been demonstrated among pig farms in Belgium, where biosecurity level was associated with the amount of antibiotics used [17]. Biosecurity in poultry production is anchored on three core principles: cleaning, segregation, and disinfection [18]. Combined, these measures reduce the risk of introduction and spread of disease. In our study, there was a low level of adoption of biosecurity measures. Cost–benefit analysis of biosecurity may act as an incentive, encouraging farmers to implement these measures in their poultry farms [18].

In commercial chickens, vaccination coupled with the use of biosecurity measures may significantly reduce antibiotic use without compromising levels of production [19]. In our study, most broiler and layer farmers vaccinated their birds against infectious poultry diseases, although not routinely. A study of beef farmers in Tennessee in the USA found that packing vaccines in large amounts was a key hindrance in the purchase and use of vaccines, as was similarly reported by keepers of indigenous birds in our study [20]. To encourage the utilization of vaccines by indigenous bird keepers, manufacturers should consider packing vaccines in smaller numbers of doses.

Use of antibiotics for disease control and production

Similar to other studies conducted among poultry farmers in LMICs [21, 22], we found that antibiotics were reported to be used in sub-therapeutic doses to enhance production, especially in layers and broilers. The application of antibiotics in sub-therapeutic doses results in selection pressure stimulating the emergence of resistant bacteria [23]. Similarly, studies in Vietnam and Cambodia found that antibiotics were widely used to protect day-old chicks against infections on arrival [24, 25]. The study in Vietnam does not explain the drivers of this practice, but findings of our study strongly point to the influence of sellers of chicks encouraging antibiotic usage for the prevention of omphalitis. Poor sanitary conditions at the hatchery and on the farm are linked to a high prevalence of omphalitis in chicks [26]. The use of antibiotics for prophylaxis may affect the curative use of these antibiotics in human and animal medicine.

In our study, the most commonly used brand for prophylaxis in day-old chicks, product A (refer to Table 2 for reference on active ingredients), gained popularity in the past year. There may have been an economic motivation for the sellers of the chicks to market this product. To effectively reduce the use of antibiotics in poultry, suppliers of chicks form a very important target group.

Use of combined antibiotic brands and critically important antibiotics in poultry production

In our study, a significant proportion of antibiotic brands used (53.3 percent) contained more than two different groups of antibiotics sold as a single product. For instance, product A, the most commonly used antibiotic brand for disease prophylaxis in chicks, had a combination of four different important antibiotics (ref to Table 2). The use of combination antibiotics has been reported as a key driver of the emergence of multiple drug-resistant bacteria due to the exposure of bacteria to different antibiotic classes [27].

The World Health Organization (WHO) lists the majority of antibiotics used for prophylaxis of disease in our study as important and critical medicine in human health. In our study, colistin use was reported in 13 percent of poultry farms. This is consistent with the findings of Muloi et al., who reported that colistin was an antibiotic of choice for poultry farmers: 16 percent of veterinary shops dispensed colistin to poultry farmers in Nairobi, Kenya [12]. The study by Muloi does not explain the drivers of this practice. As previously indicated, our findings point to the promotion of the use of this antibiotic by sellers of day-old chicks with a view to prevent omphalitis. While the use of colistin in poultry production has been banned in countries such as China because of its human medical importance, in most LMICs it is still used in livestock production [4, 21, 28, 29]. The widespread use of colistin in livestock production in China is thought to be a significant driver in the emergence of plasmid-mediated MCR-1 in Enterobacteriales isolated in humans [30].

In our study, the use of poultry droppings as animal feed was very common, and poultry was often housed with other species such as cattle and pigs. This creates potential pathways for the transfer of antibiotic-resistant bacteria including transfer to the environment, to cattle and pigs fed on the droppings, and ultimately to humans at the top of the food chain. Colistin is excreted in its bioactive form. Therefore, the antibiotic is available in sub-therapeutic doses in chicken droppings and may induce selection pressure in the gut of the animals that consume the poultry droppings as animal feeds. This creates an avenue for the spillover of resistant microbes from animals to humans through physical contact or the food chain. Similar strains of resistant genes have been reported in humans and animals, and examples include plasmid-mediated resistance to colistin in Klebsiella spp, suggesting transmission of AMR from animals to humans [31, 32]. This underscores the need for a One Health approach through multiple sectoral and cross-disciplinary cooperation to address the AMR challenge.

Source of veterinary services

Farmers sought veterinary services from AVDs but as noted in a study from Ghana, they did not form part of the farm management [21]. In our study, the high cost of on-farm consultation was reported to be a key hindrance to the involvement of veterinary professionals in the management of poultry farms. In addition, while there were veterinary laboratories near farms, most farmers and AVDs did not utilize them citing the long turnaround time for results. Lack of integration of prescriptions with extension services or laboratory diagnosis results in the use of broad-spectrum antibiotics for perceived improved treatment outcomes. Although in many contexts, drugs are administered without laboratory diagnoses, in the context of our study, very few farmers ever sought such services.

Self-prescription of antibiotics was the second most important route to seeking veterinary services for poultry farmers. This was driven by widespread knowledge of antibiotic brands compounded by factors such as ease of access to antibiotics and financial pressure (the high cost of veterinary consultation). Antibiotic resistance is reported to be higher in settings where self-prescribed antibiotics are used frequently [33, 34]. In LMICs, where the sale of antibiotics is poorly regulated, delinking financial gains from the sale of antibiotics has been suggested as a possible intervention toward reduction of self-prescription use of antibiotics [34].

Recommendations

To increase the efficacy of farmers’ understanding of AMR, research programs should adopt a collaborative effort between social scientists, environmental scientists, animal health and human health practitioners, i.e. a One Health approach. This will give a more complete picture of the risks we are facing from possible overuse of antibiotics, and a better understanding of farmers’ needs. Actions such as surveillance of antimicrobial use and resistance when implemented in synergy across disciplines and sectors increase the potential for the reduction of AMR.

Probably the most salient factor in antibiotic use is financial. If farmers could be shown more effective and either free or inexpensive ways of keeping their poultry healthy, they would be less likely to overuse antibiotics. Day-old chicks are very vulnerable to disease and so farmers are immediately dosing them with antibiotics. One important node for any future intervention would be supplier of these chicks to ensure that they are healthy when they reach the farmer.