Antibiotic usage and prevalence of antibiotic residue in broiler chicken in the Kumasi metropolitan area

¹Department of Pathobiology, School of Veterinary Medicine, Kwame Nkrumah University of Science and Technology, Kumasi, Ghana, ²Department of Veterinary Pathology, Faculty of Veterinary Medicine, University of Ibadan, Ibadan Nigeria, ³Department of Veterinary Services, Ministry of Agriculture, Ogun State, Nigeria

^&Corresponding author
Benjamin Obukowho Emikpe, Department of Pathobiology, School of Veterinary Medicine, Kwame Nkrumah University of Science and Technology, Kumasi, Ghana

Introduction    

Antibiotic residues are chemical remnants or pharmacologically active compounds that either represent the parent antibiotic or its broken-down by-products and are released, gathered, or stored in the animal's edible tissues [1]. These antibiotics play pivotal roles in modern poultry farming, contributing significantly to the prevention and treatment of bacterial infections [1]. This has become a common practice to prevent and treat bacterial infections in livestock, however, the overuse and misuse of antibiotics in the meat industry has led to the presence of antibiotic residues in meat products [2]. Despite the inappropriate usage of antibiotics in food animals' production in recent times, regulations and monitoring programs are in place to ensure that food animal meat and meat products are safe from excessive levels of antibiotic residues [3]. These include Maximum residue limits (MRLs) for antibiotics in animal products, and guidelines for the responsible use of antibiotics in farming and veterinary medicine [3]. Regardless of these regulations, antibiotic residue has become a significant public health concern, as the consumption of antibiotic-contaminated meat can lead to the development of antibiotic-resistant bacteria in humans, rendering antibiotics ineffective in treating infections [4,5].

As antibiotic resistance continues to escalate globally, understanding the dynamics of antibiotic usage in local poultry farming is crucial for developing sustainable practices that ensure both food safety and public health [6,7]. The Kumasi metropolitan area, located in the Ashanti Region of Ghana, serves as a pertinent case study for examining antibiotic usage and residue prevalence in chicken production. The region's poultry industry has witnessed significant growth in recent years, driven by increasing demand for poultry products [8]. This growth, however, has been accompanied by a surge in antibiotic usage, raising questions about the potential consequences for both animal and human health [9-11]. Poultry farmers in Kumasi, Ghana, face challenges in acquiring veterinary drugs and antibiotics, often relying on non-veterinary personnel for administration [12]. About 98% of antibiotics are given without proper veterinary oversight, leading to risks of misuse and antimicrobial resistance [12]. Farmers typically purchase antibiotics over the counter, lacking prescriptions and guidance. Although they recognize the importance of veterinary advice, limited access to veterinary services forces reliance on personal experience [12]. In the Kumasi metropolitan area, chicken produced from farms are sold to live bird markets in Kumasi and are bought by consumers all over the region and beyond. Nevertheless, there is a knowledge deficit on antibiotic usage, the adherence of withdrawal periods by farmers and the occurrence of antibiotic residue in broiler chicken. This study therefore sought to investigate the antibiotic usage pattern, farmers' adherence to withdrawal periods of antibiotics and the occurrence of antibiotic residue in broiler chicken produced in the Kumasi metropolitan area in the Ashanti Region of Ghana.

Methods     

Study area and study design

This study was carried out in the Kumasi metropolitan area and utilized the cross-sectional study design. This study site was chosen because of the increase in poultry production activities as well as the consumption of poultry and poultry products. The administrative map of the study location is displayed in Figure 1 below.

Sampling technique and sample size

In this study, the sampling frame consisted of all the commercial poultry farmers and breeders within the Kumasi metropolitan area. Within the metropolitan area, a total of fifty-five (55) poultry farmers and breeders were identified and constituted the sample frame for this study. A simple random sampling technique was used to sample the poultry farmers and breeders from various locations within the metropolitan area including Kwadaso, Nhyiaeso, Suame, Tafo, Subin and Asawase. This sampling technique was used to ensure that each farmer had an equal chance of being selected in the study as well as to avoid selection bias.

The sample size for this study was determined using the Yamane's formula as shown below.

Where: n = required sample size, N = population size (55), e = error margin (standard value 0.05), n = 58 / (1+ 55 (0.05²); n= 48; sample size = 48.

A total of 48 poultry farmer respondents were to be used as the sample size used in this study. Nevertheless, due to farmer accessibility and availability a total of forty-five (45) farmer respondents were available for this study.

Data collection instrument and procedure

A structured questionnaire was designed by the authors used to collect data in this study. The questionnaire included the sociodemographic characteristics of the farmers, the farm management system, the type of birds kept and the farm size. This was to give the researchers an overview of the type of farmers involved in chicken production and the dynamics of commercial poultry production in the Kumasi metropolitan area. The questionnaire also comprised questions on farmers' knowledge of antibiotics, antibiotics residue, practices associated with the usage of antibiotics and observance of the withdrawal period regarding antibiotics. Some questions on farmer practices on antibiotic usage were on a 5-point Likert scale to determine their level of agreement with some of the practices. These questions were vital in assessing the overall antibiotic usage and how farmers adhere to withdrawal periods in antibiotics which could help in relating to the outcome of the antibiotic residues test in this study. Questionnaires were administered using Google Forms and shared with poultry farmers who were contacted in person. Questionnaires were created in English language but questions were translated into the Twi language for farmers who could not read the English language. The validity of the research questionnaire was performed through the review of the study questionnaire while the reliability of the study questionnaire was ascertained through the use of the Cronbach alpha test of which the alpha value was recorded to be 0.71 indicating the reliability of the study instrument used.

Chicken sample collection

One kilogramme (1kg) of liver and gizzard samples were obtained from 5 markets and distributors of broiler chicken meat products from the farms investigated. A total of 184 samples were collected consisting of 29 livers and 155 gizzards. Collected samples were stored in frozen labeled zipped-locked plastic bags and transported on ice to the Pesticides Residues Laboratory at the Ghana Standards Authority for antibiotic residue test.

Antibiotic residue test

In this study antibiotic residue test was carried out on the liver and gizzard samples. Liver and gizzard samples were subjected to the Multiresidue Method Protocol by LC-MS/ MS 5991-0013 EN (2012) to test for antibiotic residues at the Pesticides Residues Laboratory at the Ghana Standards Authority (GSA).

Data analysis

Data obtained was cleaned and coded with Microsoft Excel and subjected to descriptive statistical analysis using the Statistical Package for Social Sciences (SPSS) Version 27. Results were presented in tables and figures.

Ethical consideration

In this study, informed consent from the participants were obtained after the objectives and the benefits of the study was explained to the poultry farmers and individuals who sell broiler meat at the markets. In addition, farmers' response to participate in the study was voluntary and not under compulsion. The researcher ensured that the confidentiality and anonymity of poultry farmers' response was maintained.

Results     

Demography of farmers and farm characteristics

The demographic analysis of the 45 poultry farmers surveyed revealed that the majority were male (89.2%), with a smaller proportion being female (10.8%). Age distribution indicated that 29.7% of the farmers were aged 20-29 years, 37.8% were 30-39 years, 18.9% were 40-49 years and 10.8% were 50 years or older. Educationally, 10.8% had completed junior high school, 51.4% had secondary education and 35.1% had tertiary education. Regarding farming experience, 24.3% had 1-3 years, 27% had 4-6 years, 10.8% had 7-9 years and 13.5% had 10 or more years of experience (Table 1).

The analysis of farm characteristics revealed that the majority of farmers (81.1%) utilized a deep litter farming system, with smaller percentages using battery cages (10.8%) or a combination of both systems (5.4%). Bird types varied, with commercial layers being the most common (48.6%), followed by commercial broilers (18.9%), layer breeders (18.9%), mixed types (10.8%) and broiler breeders (2.7%). Bird populations were primarily within the range of 1,000-5,000 birds (54.1%), with fewer farms housing 5,000-10,000 birds (10.8%), over 10,000 birds (8.1%), or less than 1,000 birds (27%) (Table 2).

Knowledge of antibiotics, antibiotics residue, resistance and withdrawal periods

The study revealed that while a high proportion of poultry farmers (88.9%) were knowledgeable about antibiotics, their understanding of antibiotic residues, antibiotic resistance and withdrawal periods was significantly lower. Only 31.1% of farmers were aware of antibiotic residues and 35.6% were knowledgeable about antibiotic resistance and withdrawal periods (Table 3).

Practices towards antibiotic usage

The study revealed that 62% of the 45 poultry farmers surveyed had not received any training on antibiotics, while 38% had undergone training. The majority (84%) used a single type of antibiotic, with 16% using a combination of antibiotics. Regarding the purpose of antibiotic use, 62% used them therapeutically, 32% both therapeutically and prophylactically and only 2.7% used them solely prophylactically. Additionally, only 4.4% of farmers added antibiotics to feed, whereas 95.6% did not, however, all farmers (100%) added antibiotics to water (Table 4).

The results also indicated that when it came to administering antibiotics according to instructions, only 6.7% of the farmers strongly disagreed, while 33.3% agreed and 8.9% strongly agreed. A notable 33.3% of farmers were neutral on this matter. Regarding the observance of withdrawal periods, 60% of the farmers remained neutral, 26.7% agreed and 4.4% strongly agreed. Conversely, only 4.4% of the farmers both strongly disagreed and disagreed with observing withdrawal periods (Table 4).

Source of recommendation for antibiotic usage

The results revealed that 80% of the farmers purchased antibiotics based on recommendations from veterinarians. Additionally, 64.4% of the farmers made antibiotic purchases based on recommendations from other farmers, whereas 35.6% did not. Recommendations from shopkeepers influenced only 22.2% of the farmers, while 77.8% did not consider such advice. Only 13.3% of the farmers purchased antibiotics based on self-recommendation, with the majority (86.7%) not doing so (Figure 2).

Antibiotic residues in chicken

The findings showed that the residue levels of all antibiotics in both broiler chicken liver and gizzard samples were below the test threshold in all markets (markets A, B, C, D and E). All antibiotics had residue levels less than 0.01mg/kg in both liver and gizzard (Table 5).

Discussion     

This current study investigated antibiotic usage, withdrawal period adherence and occurrence of antibiotic residue in broiler chicken in the Kumasi metropolitan area in the Ashanti Region of Ghana. The study findings showed that 11.1% of the farmers did not know about what antibiotics are while 88.9% of the poultry farmers had much knowledge of antibiotics which is different from the findings of Galaa et al. [13] who also reported that a relatively lower percentage (25%) of poultry farmers knew much about antibiotics in Sunyani. The poultry farmers in this study had attained secondary and tertiary education which could have exposed them to knowing antibiotics. In this research, only a small percentage had knowledge of antibiotic resistance (31.1%), antimicrobial residue (35.6%) and withdrawal periods for antibiotics (35.6%). This study's findings corroborate an earlier study by Chilawa et al. who also reported 29.2% awareness of antimicrobial resistance among farmers in Zambia [14]. These findings are also consistent with a study conducted by Dione et al. [15] in Senegal, which found that the majority of farmers had knowledge of antibiotics but lacked knowledge of antibiotic resistance and withdrawal periods. The limited knowledge about Antimicrobial Resistance (AMR), antimicrobial residue and withdrawal periods within the poultry farming communities could lead to indiscriminate use of antibiotics which might end up in the poultry products.

From the study findings, majority of farmers did not add antibiotics to feed but added antibiotics to water. A large percentage of farmers were neutral on administering antibiotics according to instructions and observance of withdrawal periods. These findings are consistent with astudy conducted in Nigeria, which found that farmers lacked knowledge on proper antibiotic usage and did not observe withdrawal periods [16]. This is concerning because the withdrawal period is critical in ensuring that no antibiotic residues remain in animal products. Failure to observe the withdrawal period can lead to antibiotic residues in animal products, which can have negative health implications for consumers who consume these products. In view of this, education and awareness creation initiatives are imperative to address this issue as highlighted by several researchers [17-19]. Farmers need to be informed about the proper usage of antibiotics, emphasizing the significance of following recommended guidelines and withdrawal periods. Training programs should be designed to disseminate knowledge on the potential consequences of antibiotic misuse, not only for animal health but also for the broader implications on human health. Moreover, collaboration between agricultural extension services, veterinary professionals and public health authorities is crucial for developing comprehensive strategies to promote responsible antibiotic use in livestock farming. This could include the creation of accessible and culturally relevant educational materials, workshops, and outreach programs to reach a wide audience of farmers. Most farmers in this study purchased antibiotics from veterinarians and other farmers, while only a small percentage purchased antibiotics from shopkeepers or for themselves. These findings are consistent with a study conducted in Nigeria, which found that the majority of farmers purchased antibiotics from veterinary shops based on veterinarian recommendation [16].

Antibiotic residues existed in the broiler liver and the gizzards from the poultry farms in this study. However, these were traces that were below the 0.01mg/kg allowable limit of the Ghana Standards Authority. This is a positive finding as it suggests that the antibiotics used by the farmers did not leave any residue in the poultry products. These findings are consistent with a study conducted in Nigeria, which found that the residue levels of antibiotics in poultry products were below the maximum residue limits set by the European Union [16]. The low antibiotic residues in broiler liver and gizzard in this study could be attributed to antibiotics not administered through the chicken feed but rather through water. This assertion is in agreement with previous report that found the use of antibiotics in water being associated with lower levels of antibiotic residues in chicken meat [20], while on the other hand, the use of antibiotics in chicken feed is found to be associated with higher levels of antibiotic residues in chicken meat [21]. It is worthy of mention that the absence of direct exposure of the gastrointestinal tract to antibiotics through feed, antibiotics administered via water may have limited systemic absorption and reduced bioavailability [22]. The differential metabolism of antibiotics, faster clearance and a potential dilution effect in body fluids contribute to lower residual concentrations in the meat [22]. While these results are reassuring, it is important for farmers to observe the withdrawal period to ensure that no antibiotic residues remain in poultry products. In addition, farmers should follow good poultry farming practices such as good biosecurity measures, and use antibiotics judiciously to minimize the development of antibiotic resistance.

The smaller sample size of farmers and broiler chicken samples posed a limitation to generalizing the results. In addition, the cost involved in obtaining the full chicken sample as well as conducting the antibiotic residue test on all antibiotics identified was also a limitation. The unwillingness of market women to sell the liver and gizzard separately from the whole broiler was also a limitation of this study farmers before slaughtering birds for sale in this study.

Conclusion     

The study concludes that while broiler poultry farmers are aware of antibiotics, their knowledge of antibiotic resistance, antibiotic residues and withdrawal periods is limited. The practice of adhering to withdrawal periods is also low. Despite this, antibiotic residues were found in broiler chicken liver and gizzard in the markets, but they remain within acceptable limits. It is recommended that antimicrobial resistance advocacy coupled with antimicrobial stewardship should be directed at poultry farmers in the study area. Poultry farmers need to be enlightened more on the consequences of excessive antibiotic usage to prevent excess antibiotic residues in chicken products. Further studies are needed on a national scale to quantify the antibiotic residues in poultry meat itself as this study considered only the liver and the gizzard.

Competing interests     

The authors declare no competing interests.

Authors' contributions     

All authors have contributed to this study. All have read and agreed to the final manuscript.

Tables and figures     

Table 1: demographic characteristics of poultry farmers

Table 2: management system, type and population of birds

Table 3: farmers' knowledge of antibiotics, antibiotics residue, antibiotics resistance and withdrawal periods

Table 4: farmer's practices towards antibiotic usage

Table 5: antibiotic residues in broiler chicken liver and gizzard

Figure 1: map of study area

Figure 2: source of recommendation for antibiotics purchase for poultry farmers

References