Antibiotic use and knowledge of antibiotic resistance among pig farmers in Ejisu and Juaben municipalities of Ashanti region, Ghana

¹School of Veterinary Medicine, Kwame Nkrumah University of Science and Technology (KNUST), Kumasi, Ghana

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

Introduction    

The discovery of antibiotics has greatly improved the treatment and prevention of infectious diseases of bacterial origin that were lethal to humans and animals. This improvement has positively impacted both human and animal health delivery worldwide and played a critical role in the betterment of animal welfare as well as in ensuring food safety and food security [1]. Antibiotics are used in food-producing animals (mainly cattle, poultry, and pigs) for therapeutic, metaphylaxis, prophylaxis and as growth promoters [2]. Amongst the most frequently used antibiotics for human treatments are penicillin, macrolides, and fluoroquinolones, while tetracyclines, penicillin, and sulfonamides are the most commonly used in animal health [3]. It is therefore imperative to safeguard the efficacy of these life-saving and indispensable medications, as well as guarantee their continuous availability for both human and veterinary use, so that the future can be preserved [1].

The surge in the use of antibiotics in animal production is driven by the increase in livestock production to meet the growing demand of citizens for animal protein, particularly in low- and middle-income countries, where the use of antibiotics is poorly regulated and used irrationally to compensate for poor biosecurity measures and other inappropriate animal husbandry practices [4]. The overuse and misuse of antibiotics has led to the development and spread of antimicrobial resistance (AMR) which has now become a threat to public health globally [5]. The emergence of AMR strains is dependent on several factors relating to the antimicrobial itself, including dosage, frequency and duration of use [6]. Antibiotics usage is particularly high in poultry and pig production, compared to other food-producing animals. The intensive conditions under which pigs and chickens are often housed may be associated with greater vulnerability to infectious disease potential and therefore a greater reliance on antibiotics to control sub-clinical infections [6]. In animal husbandry alone, the average yearly consumption of antibiotics has been estimated as 172 mg/kg in pigs, 148 mg/kg in chicken, and 45 mg/kg in cattle worldwide [6].

In Ghana, domestic commercial production of pigs has grown significantly over the past decade, mainly as a result of increasing domestic pork consumption [7]. Commercial pig farming in the Ashanti region, Ghana, is the second most recognized form of commercial food animal production after poultry with Ejisu municipality being the leading producer of pigs in the Ashanti region [8]. About 41% of livestock and poultry farmers in Ghana use antibiotics for infection prevention at least once a month [9] leading to the development of resistant strains of pathogens [10].

Antimicrobial resistance both in human and veterinary medicine has reached alarming levels in most parts of the world and has now been recognized as a significant emerging threat to global public health and food security [11]. The potential threat to human health resulting from inappropriate antibiotic use in food animals is significant, as pathogenic-resistant organisms propagated in the livestock are poised to enter the food supply chain and could be widely disseminated in food products [12]. To tackle the menace posed by antibiotic resistance, proper antibiotic administration practices such as accurate dosing, route of administration, observance of withdrawal periods, and strict adherence to manufacturers´ instructions have been suggested as important solutions [2]. There is, however, a paucity of data and surveillance studies on antibiotic use and farmers´ knowledge of antibiotic resistance in Ghana, especially in pig husbandry.

The World Health Organization´s Global Action Plan on AMR 2016 also addresses the need to strengthen knowledge and evidence-based practices through surveillance and research. This cross-sectional study seeks to provide information crucial for the development of an appropriate intervention to reduce the spread of antibiotic resistance in Ghana using Ejisu and Juaben municipalities as a model to provide evidence on inappropriate antibiotic use and inadequate knowledge of antibiotics by pig farmers. Hence, this study was set out to investigate antibiotic usage among pig farmers as well as to assess pig farmers´ knowledge on antibiotics, and antibiotic resistance in Ejisu and Juaben municipalities in the Ashanti region of Ghana.

Methods     

Study area: this study was carried out in the Ejisu and Juaben municipalities of the Ashanti region, Ghana. Data available at the Ejisu-Juaben Municipal Agricultural office indicates that chicken (70.3%) is the most-reared animal by households in the municipality. Other types of animals reared by households are sheep (10.2%) and goats (8.3%). There are about 104 pig farmers in the municipality representing (2.4%) of the livestock keepers.

Study design: a cross-sectional study using a close-ended questionnaire was designed and applied to collect data on antibiotic usage and pig farmers´ knowledge of antibiotic resistance. The study was conducted from May 2022 to September 2022.

Questionnaire development: questionnaires from previous studies were adopted and modified [13,14]. The questionnaire was piloted with 5 pig farmers and reviewed for clarity before implementation. The final version had three sections: demographics of pig herd and farmer; knowledge of antibiotics and antibiotics resistance; and pattern of antibiotic use. The word ‘pattern´ explains the use of antibiotics in terms of the active ingredients; the route of administration such as injection or via feed and water; and the purpose of the use, including treatment, prophylaxis, and growth promotion. The questionnaire contained mostly closed-ended questions with few open-ended questions. Pictures of different types of antibiotics were obtained from veterinary pharmacies and were added to the questionnaire to help farmers with easy identification of the antibiotics they used on their farms.

Study population: pig farmers who were involved in the day-to-day activities on their farms and in active production were the target group for this study.

Sample technique: the snowball technique was adopted for this study since there were no established documents containing the phone number and locations of the farmers. In addition, contacts provided by agriculture extension officers, district veterinary officers as well as local Pig Farmers´ Association were used in identifying some of the farmers.

Sample size: fifty (50) pig farmers were sampled for this study. The sample size was determined using standardized sample size estimates for the prevalence of antimicrobial resistance in a large population developed by the World Organization for Animal Health (WOAH) (OIE Standards, Guidelines and Resolution on antimicrobial resistance and the use of antimicrobial agents, 2015). The parameters were: level of confidence = 90%, desired precision =10%, and expected prevalence of farmers´ antibiotic usage = 20%.

Validity and reliability of the instrument: the content validity of the questionnaire was ensured by facts identified from the literature review. The responses to the structured questionnaire were subjected to the Cronbach Alpha test to verify the reliability of the questions asked in the questionnaires; thus, the reliability coefficient (Cronbach alpha) was compiled. A Cronbach alpha which had a reliability coefficient of 0.72 was deemed acceptable.

Data collection: permission was obtained from the respondents before questionnaires were administered and they were informed that their identification was not required. The questionnaire was developed and administered in English language but translated into Twi (the local Ghanaian language), when needed, in a face-to-face interview. Telephone calls were made with farmers who were not available for a face-to-face interview. The first section collected demographic information such as farmer´s age, gender, education level, number of pigs owned, type of pig husbandry methods, and their main source of income. The second section assessed farmer´s knowledge of antibiotics and antibiotic resistance. Two questions in this section were asked as open-ended questions but immediately categorized by the interviewer (how do you think an antibiotic works and what is the impact of antibiotic resistance?). Immediately after the questions that assessed if farmers had an accurate understanding of antibiotics and antibiotic resistance or not, the definition of antibiotics was clearly explained before proceeding to the third section of the questionnaire which assessed antibiotic use in pigs. Eight questions were selected to assess the knowledge of farmers on antibiotics and antibiotic resistance. A correctly answered question scored one (1) whereas a wrongly answered question scored zero (0). Farmers were grouped into having adequate or inadequate knowledge based on their assessment score of ≥ 4/8 and < 4/8 respectively and similarly into appropriate or inappropriate practices on antibiotic use assessment score of ≥ 5/9 and < 5/9 respectively.

Each interview took an average of 13 minutes (telephone) and 25 minutes (face-to-face) to complete. All responses were recorded on paper and subsequently entered and managed in Google Forms and Microsoft Excel Spreadsheets respectively. The research maintained absolute confidentiality throughout the study.

Data analysis: data was entered into Microsoft Excel version 2019 for cleaning and for the generation of graphs. The responses were then coded into figures and exported to the Statistical Package for Social Sciences (SPSS) for further analysis. Descriptive statistical analysis was performed using Statistical Package for Social Sciences (SPSS) version 20.0. Pearson´s Chi-square test was used to determine the association between demographic characteristics and farmers´ knowledge of antibiotics and antibiotic resistance. The same approach was used for farmer practices on antibiotic usage. Statistical significance was tested at a 5% significant level or a 95% confidence interval. Significance values that were less than or equal to 0.05 were considered statistically significant.

Results     

Socio-demographic characteristics of the respondent: a total of 50 pig farmers were sampled for this cross-sectional survey. Out of the 50 farmers interviewed (Table 1), most of the respondents were male (88%, n = 44) and most of them belonged to the 41-50-year age group (48%, n = 24) with only (4%, n = 2) belonging to the 18-30-year group. There was no significant difference in a number of farmers who had primary and secondary education (36%, n = 18 and 34%, n = 17 respectively). The majority of the farmers (60%, n = 30) had less than 10 years of experience in pig rearing. In terms of source of income, nearly half (48%, n = 24) had pig rearing as their main source of income.

Commonly used antibiotics in the study area: several antibiotic types were used by farmers in the study area. Nearly all (96%, n = 48) the farmers used at least two antibiotic types. Only one farmer did not use any antibiotics on pigs. Of the antibiotics used, penicillin-streptomycin was the most commonly used antibiotic type (98%, n = 49), sulfadimidine (72%, n = 36), tetracyclines (70%, n = 35) with trimethoprim (2%, n = 1) being the least commonly used antibiotic (Figure 1).

Knowledge of farmers on antibiotics and antibiotic resistance and their practices: to assess farmers´ knowledge on antibiotics and antibiotic resistance, farmers were asked 8 questions as indicated in Table 2. Most (88%, n = 44) of the respondents said they knew what antibiotics are and of this percentage, 66% (n = 29) heard about antibiotics from colleague farmers. When specifically asked how antibiotics work, a larger proportion of the respondents (79.5%) did not know how antibiotics work.

Only 30% of the respondents have heard about antibiotic resistance and of this percentage, 42.8% (n = 6) heard about antibiotic resistance from seminars. A majority of the respondents who heard about antibiotic resistance (73.3%, n = 11) are likely to say antibiotic resistance make antibiotics less effective. A sizeable proportion (72%) of the respondents disagreed with the fact that overdose/low dose may lead to antibiotic resistance. Surprisingly, 82% (n = 41) further gave a negative response when asked whether the misuse and overuse of antibiotics could result in antibiotic resistance and affect the health of both humans and animals. Only 26% answered yes when they were asked whether they are aware of drug residue, preceding whether drugs taken by pigs can pass to meat which received 42% yes responses. Knowledge of farmers on antibiotics and antibiotic resistance was categorized as adequate (26%) and inadequate (74%) as shown in Table 2.

Practices on antibiotic use among pig farmers are detailed in Table 3 and Figure 2. Almost all the farmers had ever given antibiotics to their pigs (98%, n = 49). When asked the frequency of antibiotic use, 79.6% said they give antibiotics to their pigs anytime they look sick and about half of them (51%) gave antibiotics to their pigs just after weaning. Other farmers gave antibiotics to their pigs routinely; every three months (40%), monthly (16.3%), and weekly (8.2%). Of farmers who give antibiotics to their pigs (98%, n = 49), 40.8% used them as growth promoters while 82% used them to prevent diseases. Diarrhea was the most common clinical sign that prompted antibiotic use with a (100%, n = 49) response among farmers who used antibiotics. Inappetence was a factor that prompted 75.5% of the farmers to use antibiotics in pig production. With regards route of administration, 36% added antibiotics to feed mostly just after weaning, 14% by water medication, and 50% used injectable antibiotics (Table 3).

A larger proportion of the farmers (66%) consulted veterinary services only when their animals did not respond to treatment; 22.4% consulted veterinary technicians before the administration of antibiotics. On following manufacturer´s instructions, 74% of the farmers followed label instructions which they relied on for treatment as an alternative to veterinary services to save time and to reduce cost of production. When asked about observing withdrawal periods, 53% said they observed withdrawal periods after antibiotic administration (Table 3). About 91% of the farmers purchased antibiotics from the markets in Ejisu and Juaben. A total of 69.4% of farmers stored antibiotics on their farms (mostly in polytene bags and containers in which the drugs were bought) which they kept in feed stores. Only one farmer had a designated box for the storage of drugs. Most of the farmers (83.7%) did not keep records of antibiotics used on their farms (Table 3).

Influence of demographic characteristics on farmers´ knowledge of antibiotics and antibiotic resistance and their practices: an association test was performed to show the significant factors between the demographic variables and knowledge. The results demonstrated in Table 4, show that farmer´s level of education (p = 0.001) and experience in pig rearing (p = 0.006) were the significant factors influencing the knowledge of farmers on antibiotics and antibiotic resistance.

Factors such as famer´s level of education (p = 0.017) and farm type (p = 0.020) were significant demographic factors influencing the practices involved in antibiotic use. A greater proportion of farmers who had tertiary education (69.2%, n = 9) and more than half of the large-scale farmers (58.8%, n = 10) practices were appropriate. Detailed results are indicated in Table 4.

Influence of veterinary services involvement on knowledge of farmers on antibiotics and antibiotic resistance and their practices: an association test was performed to assess how the involvement of veterinary services in pig rearing influenced the farmer´s knowledge on antibiotics and antibiotic resistance (Table 5). Farmers that accessed veterinary services only when they are unable to treat (84.8%) had inadequate knowledge which was significant (p = 0.037). Source of information by the farmers was a significant factor that influenced their knowledge (p = 0.001). This study revealed that 86.2% of the farmers who heard about antibiotics and resistance from colleagues had inadequate knowledge while 60% of farmers who heard about antibiotics and resistance from veterinarians had adequate knowledge. All those farmers who heard about antibiotics from seminars had adequate knowledge on antibiotics and antibiotic resistance.

The test analysis revealed veterinary consultation (p = 0.003) before antibiotic use was a significant factor influencing practices (Table 5). Veterinary consultation before antibiotic use resulted in appropriate practices. The practices of majority of the farmers who accessed veterinary services only when they were unable to treat (75.8%) were inappropriate.

Discussion     

Extensive use of antibiotics in food-producing animals contributes significantly to the development and emergence of antimicrobial resistance which has become a threat to public health globally. Recognizing this threat, the World Health Organization´s Global Action Plan on AMR 2016, addresses the need to strengthen knowledge and evidence-based practices on antibiotic use through surveillance and research.

This cross-sectional study examined antibiotic use and pig farmers´ knowledge of antibiotic resistance in Ghana's Ejisu and Juaben municipalities. Results obtained indicate that 98% of pig farmers surveyed use antibiotics in pig production. The common classes of antibiotics used include penicillin, sulfonamides, tetracyclines, aminoglycosides, macrolides, and fluoroquinolones which is consistent with results of previous studies by Hossain et al. [14], Osei-Sekyere [8], Phares et al. [15] and Wangmo et al. [16].

In our study, penicillin-streptomycin was the most commonly (98%, n = 50) used antibiotic type amongst the pig farmers. This finding is contrary to previous work done in the study area by Osei-Sekyere [8] and in Ethiopia [17] which found tetracyclines as the most commonly used antibiotic type. The study revealed that 69.4% of the respondents do not consult veterinarians before administering antibiotics to their pigs. They give antibiotics to their pigs without any specific indication warranting their use; thus, giving antibiotics to pigs anytime they appeared sick or not feeding well. Most of the respondents who called on veterinarians did that only when their animals did not respond to treatment. Our finding is consistent with those of previous studies done in Bangladesh [14], Shandong province, China [18] Ashanti region, Ghana [8], and Southern Ghana [15].

Most farmers (91%) purchased antibiotics from market-based pharmacies, often without a veterinarian's prescription. The farmers mostly relied on prior experience and advice from fellow farmers for the choice of antibiotics used. Easy access to antibiotics is possible because the use of antibiotics in animals is poorly regulated in many countries [6], which supports our finding.

Participants in this survey had a 26% total knowledge score on antibiotics, their proper application, and antibiotic resistance. This result emphasizes the need for user education to prevent antibiotic misuse and overuse, which can harm humans and animals. These levels of knowledge are comparable to those observed in earlier studies, including Nigeria [19], Timor-Leste [13], Sudan [20], China [18], and Bangladesh [14].

According to studies by Osei-Sekyere [8], Phares et al. [15] and Addah et al. [21], the observance of withdrawal period among farmers is nearly absent in Ghana. In our study, however, 53% of the respondents stated that they observed a withdrawal period according to manufacturer´s instruction. This finding even though low, is better than what was previously reported and can be improved upon through seminars and training for these farmers on the proper utilization of antibiotics.

A study done in Sudan found a significant association between farmers´ low education level and poor knowledge on antibiotic use and AMR awareness [20]. Our study found that farmers' understanding of antibiotics and antibiotic resistance is influenced by education level, animal husbandry knowledge, information source, and veterinary services advice as opined by Phares et al. [15]. Long-time pig farmers knew much more than those with less than five years experience. This may come from extensive practice. University-educated animal farmers employed antibiotics more successfully than those with only a primary education. This agrees with Geta and Kibret [17] and Osei-Sekyere [8].

This study again revealed that farmers who heard about antibiotics and AMR in seminars and those who consulted veterinarians prior to antibiotic use had higher knowledge levels and used antibiotics more appropriately. Due to a low number of veterinarians in Ghana, few farmers access veterinary services for farm inspections and antibiotic prescription [22].

Prior to the time of the study, there was an outbreak of African swine fever in the study area which led to the loss of a large number of pigs, completely wiping out the flock of some farmers. This unfortunate occurrence drove some farmers out of production, hence affecting the sample size of this study. This limitation did not, however, have any significant impact on the quality of the data collected. Accordingly, the results of the study are a true reflection of the situation in the study area.

Conclusion     

This study has identified penicillin-streptomycin as the most frequently used antibiotic in the study area, exposed the inadequate knowledge of farmers on antibiotics and antibiotic resistance, and also the poor practices regarding antibiotic use amongst farmers in the Ejisu and Juaben municipalities of Ashanti region, Ghana. This suggests a critical need for effective policy development and implementation to increase awareness of antibiotics and antibiotic resistance and the need to ensure the enforcement of already existing policies to mitigate the indiscriminate use of antibiotics because it can negatively impact humans, animals, the environment, and food security.

Competing interests     

The authors declare no competing interests.

Authors' contributions     

Conceptualization of the study: Raphael Folitse and Rejoice Esenam Nyarku; data gathering: Richard Dogbatse; statistical analysis: Vitus Burimuah, and Esther Amemor; manuscript drafting and editing: Richard Dogbatse, Raphael Folitse, and Benjamin Obukowho Emikpe. All the authors read and approved the final version of this manuscript.

Acknowledgments     

We thank the farmers in the Ejisu and Juaben municipalities of Ashanti region, Ghana for their contribution.

Tables and figures     

Table 1: demographic and socio-economic characteristics of the respondent

Table 2: knowledge of pig farmers regarding antibiotics and antibiotic resistance

Table 3: pig farmers´ practices with regards to antibiotics usage

Table 4: effect of demographic characteristics on farmer knowledge on antibiotics and farmer antibiotic usage (practices)

Table 5: effect of veterinary involvement on knowledge of farmers and their practices regarding antibiotic usage

Figure 1: antibiotics commonly used by pig farmers

Figure 2: frequency of antibiotic usage among pig farmers

References