Barriers to effective antimicrobial resistance management in Nigerian livestock: the role of veterinary practices and client expectations

Abstract

Resistance to antimicrobials is growing faster than the discovery of new drugs. This problem has raised the global concern of a possible pandemic, as the treatment of infections in both humans and animals is becoming more difficult. This study aimed to understand the opinions of practising veterinarians on the factors responsible for increasing antibiotic resistance among animals in Nigeria. A cross-sectional study of veterinarians from 36 states (including the Federal capital territory) was conducted using a paper-based structured questionnaire survey. The questionnaire was made available to the 1,117 veterinarians who attended 2023 Nigerian Veterinary Medical Association (NVMA). A simple random selection was used to select 295 veterinarians as respondents. The data collected were coded and stored electronically in a Microsoft Excel database and anonymised for further analysis. Statistical analyses were conducted using Excel and SPSS Statistics v24.0. Most veterinarians (89.8%) agreed that the antibiogram test (AST) is important before prescription; however, only a few (4.4%) request for an antibiogram before prescriptions to clients due to the unaffordability of the test by clients (x̄=3.21), the desire for rapid results (x̄=3.06), and the lack of diagnostic laboratories nearby (x̄=2.96). As a result, 61.5% reported that clients had complained that antibiotics prescribed did not work (curative). In addition, veterinarians opined that irrational antibiotic use among animal owners (x̄=4.34), an increased number of quackery (x̄=4.10) and ease of access of the public to antibiotics at veterinary pharmacies/shops (x̄=3.86) were the leading causes of increasing antimicrobial resistance in Nigeria. The significant factors responsible for veterinarians’ opinions were education (β = 0.929) and the value of conducting an antibiogram before prescription (β = 1.618) at the p ≤ 0.05 level of significance. This study revealed that irrational antibiotic use among animal owners, an increasing number of quackery and ease of access of the public to antibiotics at veterinary pharmacies/shops were the leading causes of increasing animal antimicrobial resistance in Nigeria. Therefore, this study suggests the development and implementation of policies and frameworks that promote antimicrobial stewardship and the establishment of veterinary laboratories in various communities in the country. Continuous education for veterinarians and livestock workers, especially on AMR, is also critical.

Introduction

The use of antibiotics in animal production is crucial and has been the most popular treatment option for bacterial infections in animals. Antibiotic use is continuing to rise and is projected to increase significantly in developing countries by 2030, with estimated growth rates of 157% in Vietnam, 160% in Peru, 163% in Nigeria, 202% in Indonesia, and 205% in Myanmar [1]. In Nigeria, over 77.0% of livestock farm owners use antibiotics without guidance from veterinarians, mainly to increase animal growth [2]. This situation has led to the misuse of antibiotics, which has contributed to antibiotic resistance (AMR) in animals.

Antimicrobial resistance is a broad concept that involves changes in microbes resulting in the inability of antimicrobial agents (antibiotics, antifungals, antivirals, antiprotozoals, and anthelmintics) to work as expected. This limits the ability to treat infections, making AMR one of the foremost threats to human and animal health. A systematic review of 173 AMR studies conducted in animal populations (poultry and fish) between 1989 and 2021 in Africa indicated the highest AMR percentage of 43.4% in Egypt, followed by 39.2% in Nigeria and then 17.3% in South Africa [3]. The problem of AMR is not limited to Africa but rather a global threat. The World Health Organisation [4] reported that Serbia has the highest rates of resistance in Europe and that AMR is responsible for an estimated 700,000 deaths in Southeast Asia and Western Pacific regions—more than half of the global deaths caused by AMR [5]. In the Americas, more than 35,000 people die annually among at least 2.8 million people who develop antibiotic-resistant infections in the United States [6]. To minimize the AMR risk, research and dissemination of empirical findings have been noted as one of the road maps to propel strategic decisions in reducing AMR [7]. However, in Nigeria, which has a high incidence of AMR, records of veterinarians’ views on increasing antibiotic resistance in animals are scanty.

In livestock production, essential stakeholders include livestock farmers, livestock superintendents and veterinarians. The role of veterinarians is critical for the availability, prescription and administration of antimicrobial compounds in veterinary medicine [8]. They have a role in advocating for measures to control the development of antibiotic resistance in livestock and in educating their clients on the proper use of antibiotics. Therefore, understanding how veterinarians perceive clients’ and colleagues’ antibiotic use and their beliefs about the development of antibiotic resistance is pivotal for identifying areas in which AMR education and training efforts are needed to improve antimicrobial stewardship in Nigeria.

This study sought to understand the opinions of veterinarians on the factors responsible for increasing antibiotic resistance among animals in Nigeria. Specifically, this study assessed the sociodemographic characteristics of veterinarians, the perceptions of veterinarians regarding the causes of antibiotic resistance in animals and antibiotic susceptibility testing in veterinary practices. The present study further hypothesised that the veterinarians’ sociodemographic characteristics and the AMR perceived drivers are not significant factors influencing the causes of antimicrobial resistance in animals.

Materials and methods

Study population

The target population of this study comprises all members of the Nigerian Veterinary Medical Association (NVMA) practising in 36 states, including the Federal Capital Territory in Nigeria (Fig. 1). In Nigeria, veterinarians are responsible for prescribing antibiotics to companion, food and wild animals [9]. A veterinarian in Nigeria was defined as any individual with a Doctor of Veterinary Medicine (DVM) from any of the accredited veterinary faculties within and outside Nigeria, certified by the Veterinary Council of Nigeria (VCN) to practice veterinary medicine in Nigeria [9]. The VCN is the body authorised by law to issue practice licences and to regulate all practising veterinarians in Nigeria [10]. All members of the Nigerian Veterinary Medical Association (NVMA) are registered veterinarians with the VCN.

Fig. 1

Map of Nigeria showing the 36 states with the Federal Capital Territory (FCT). The base layer of the map was created using DIVA-GIS Version 7.5 (https://www.diva-gis.org/) software

Survey design, recruitment and instrument

A cross-sectional study among veterinarians in Nigeria was conducted using a paper-based structured questionnaire. The instrument was developed, in English language, based on reviews of the relevant literature [11, 12] and was designed in collaboration with experienced veterinarians and researchers who are well knowledgeable about antibiotic use, resistance and stewardship. Content and face validity were conducted on the instrument by experts in the fields of veterinary, agricultural and sociology. Modifications suggested by the experts were effected on the instrument. Furthermore, an internal consistency reliability test was conducted by a pre-test on fourteen (14) veterinarians in Kwara State who did not attend the conference. After the responses, the Cronbach’s alpha test was applied to check the reliability of the scale. The value of the Cronbach’s alpha test was 0.81. Thus, the instrument was considered fit and reliable for data collection.

The questionnaire consisted of three sections in line with the specific objectives of the study. Section A gathered information on the sociodemographic characteristics of the respondents, while section B obtained information on the factors influencing the conduct of antibiograms all the time before prescription or administration. Section C obtained information on respondents’ perceived drivers of growing antibiotic resistant in animal care in Nigeria. The details of the variables under each section can be found in supplementary file 1.

The questionnaire was administered in a paper-based format to veterinarians during the 59th National Congress and Annual General Conference of the Nigerian Veterinary Medical Association (NVMA) held at Landmark Center, Victoria Island Oniru, Lagos State, Nigeria, between 30th October and 3rd November 2023. A total of 1,117 veterinarians who participated in the NVMA conference were considered the population for the study. The sample size for the study was determined by the Yamane [13] formula to obtain 295 participants. The formula is expressed mathematically as follows:

$$\:n=\frac{\text{N}}{1+\text{N}{\left(e\right)}^{2}}$$

(1)

where n= sample size; N = target population = 1,117; and e = margin of error = 0.05.

A simple random method was used to select 295 veterinarians who gave consent to participate as respondents during the conference. Three research assistants were recruited and trained on the contents of the questionnaire for speedy dissemination. The questionnaire completed by each participant were tagged by the number of participants; thus, re-administration of the questionnaire to a participant was avoided..

Data management and analysis

The data collected were coded and stored electronically in a Microsoft Excel database and anonymised for further analysis. Statistical analyses were conducted using Excel and SPSS Statistics v24.0 (IBMSPSS Statistics for Windows Version 24.0; New York: IBM Corp.). Both the factors influencing the conduct of antibiogram all the time before prescription or administration and the perceived drivers of growing antibiotic resistance in animal healthcare were measured on a 5-point Likert scale as follows: strongly agree = 5, agree = 4, undecided = 3, disagree = 2, strongly disagree = 1. Descriptive statistics were calculated for all variables and are presented in tables as frequencies and percentages. Mean and standard deviation values were generated to understand the central tendencies of the questions to which the respondents agreed or disagreed [14, 15]. To further understand respondents’ order of preference or priorities of factors under consideration, the mean values of the responses were ranked such that the highest mean values were assigned first (1st), indicating the most prioritized variable. Additionally, inferential statistics were calculated. A correlation matrix of variables was generated to check and identify high correlations between independent variables. The highly correlated variables identified were transformed to reduce nonlinearity, after which an ordinary least squares (OLS) regression model was employed to determine the factors responsible for respondents’ perceptions of the causes of increasing antibiotic resistance. The choice of this model is based on its proven adequacy in situations where there is the need to predict the value of a variable (the dependent variable) on the basis of the value of two or more other variables called the independent, regressor or predictor variables. The model is specified as follows:

$$\:Y={\beta\:}_{0}+{\beta\:}_{1}{X}_{1}+{\beta\:}_{2}{X}_{2}\:+{\beta\:}_{3}{X}_{3}+{\beta\:}_{4}{X}_{4}+{\beta\:}_{5}+\:.\:.\:.\:.+{e}_{i}$$

(2)

Where Y = Respondents’ perceived drivers of increasing antibiotic resistance; (X) = Independent variables; X₁ = Age (in years); X₂ = sex (dummy male = 1; otherwise, 0); X₃ = Educational status (in years of schooling); X₄ = Nature of the job (dummy clinical practice = 1; otherwise, 0); X₅ = Duration of practice (in years); X₆ = Place of residence (dummy urban = 1; otherwise, 0); X₇ = Number of times (in the last 6 months) that the clients complained that the antibiotics prescribed were not working (in number); X₈ = Frequency of checking the antibiogram (antibiotic susceptibility testing) before prescription (in number); e_i = Error term.

Results

Sociodemographic characteristics of prescribers

In terms of age group, veterinarian aged 28–37 years were the most common (41.4%), followed by those aged 38–47 years (29.8%), whereas the least common age group was veterinarians older than 47 years (10.5%) (Table 1). A report on the gender of the respondents revealed that 54.9% (162/295) were males, whereas the remaining 45.1% (133/295) were females. The highest level of education showed that slightly more than half of the respondents (150/295; 50.8%) still held a DVM degree, whereas 36.3% (107/295) of the respondents had obtained master’s and doctorate degrees. Clinical practice was the main nature of the job of the majority (64.1%; 189/295), while most respondents had been in practice for over 5 years (135/295; 45.8%). Residence of practice was mostly carried out in urban areas (169/295; 57.3%), with the lowest percentage of the respondents practising in rural communities (53/295; 18.0%).

Table 1 Sociodemographic characteristics of antibiotic prescribers

Client complaints that the antibiotics prescribed are not working and the frequency of checking antibiograms

With respect to clients’ complaints on the effectiveness of antibiotic prescriptions by veterinarians, 34.9% (103/295) of the veterinarians had never received a complaint of every five prescriptions, 30.2% (89/295) had one complaint, 20.7% (61/295) had two complaints, 8.8% (26/295) had three complaints, and 2.0% (6/295) had five complaints (Fig. 2). Additionally, the results indicated that the majority of the respondents (265/295; 89.8%) claimed that checking an antibiogram profile before prescription is important, whereas the rest (30/295;10.2%) did not see a need for it.

Fig. 2

The number of times (in the last 6 months) clients complained that the antibiotics prescribed is not working

The frequency of veterinarians requesting antibiogram testing on samples (from the veterinary laboratory) before prescription in the last six months revealed that out of five prescriptions, 38.0% (112/295) never did antibiogram, 24.4% (72/295) did antibiogram once, 12.5% (37/295) did antibiogram twice, 15.6% (46/295) did antibiogram three times, 5.1% (15/295) did antibiogram four times, and only 4.4% (13/295) did antibiogram in all prescriptions (Fig. 3).

Fig. 3

Frequency of checking antibiogram (antibiotic susceptibility testing) before prescription

Factors influencing the request of antibiograms all the time before prescription or administration

Regarding the factors influencing the need for antibiogram tests, the results revealed that “the client does not have the money” (x̄=3.21 ± 1.66) was the first-ranked factor, followed by “the client wants a quick result/immediate change in abnormal sign” (x̄=3.06 ± 1.68) as the second-ranked factor; “there is no diagnostic laboratory nearby” (x̄=2.96 ± 1.59) as the third-ranked factor; “the antibiogram test result usually comes out late” (x̄=2.77 ± 1.59) as the fourth-ranked factor; and “I don’t consider it necessary most of the time” (x̄=1.75 ± 1.19) was ranked seventh (Table 2).

Table 2 Factors influencing the request of antibiograms all the time before prescription or administration

Perceived drivers of growing antibiotic resistance in animal healthcare

With respect to the perceived causes of increasing antibiotic resistance in animal health care, the results revealed that “irrational use of antibiotics among animal owners (livestock owners, breeders)” (x̄=4.34 ± 1.41) was the leading cause, followed by, in descending order, “increasing number of quackery” (x̄=4.10 ± 1.56), “ease of access of the public to antibiotics at veterinary pharmacies/shops” (x̄=3.86 ± 1.60) and “poor policy on antibiotic access and its use” (x̄=3.66 ± 1.67), whereas poor knowledge of antibiotic use among veterinarians (x̄=2.70 ± 1.57) was ranked the lowest (Table 3). Since veterinarians could also contribute to indiscriminate antimicrobial use and increasing antibiotic resistance, their willingness to refresh their knowledge of antimicrobials showed that 80.0% (236/295) were willing to participate in any available antimicrobial workshop.

Table 3 Perceived drivers of antibiotic resistance in animal care

Determinants of prescribers’ perceived causes of increasing antibiotic resistance

The results of multiple regression (least squares model) revealed that the positive significant determinants of veterinarians’ perceptions of the drivers of increasing antibiotic resistance (p < 0.05) were the education of the veterinarian (β = 0.929; p = 0.007; 95%CI = 0.029–1.887) and the nature of the job (β = 1.882; p = 0.004; 95%CI = 0.158–0.605) (Table 4).

Table 4 Determinants of prescribers’ perceived causes of increasing antibiotic resistance

Discussion

The sociodemographic features of the respondents in this study revealed that > 59% of the veterinarians in Nigeria were young adults (18–37 years). This finding corroborates the report by Ogwuche et al. [9], who reported that veterinarians in Nigeria are mainly young adults aged less than 50 years. This study revealed that more than 40% of veterinarians had further education post-DVM, suggesting a desire to know more about their career path. It is believed that continuous education after professional qualification reminds a veterinarian of the duties and responsibilities of their practices.

In the last 6 months, several veterinarians reported that their clients had complained of antibiotics prescribed not working (> 61.7%), confirming the accelerating rate of antibiotic resistance in Nigeria. This situation is expected to possibly cause an increase in AMR in humans because studies have linked AMR in humans with AMR in animals [16, 17], making AMR an important health challenge that is emerging on a global scale [9, 18]. Nigeria was listed among the top 50 consumers of antibiotics in food animals in 2010 and is projected to increase food animal antibiotic use up to 167% by 2030 [1, 19].

The majority of veterinarians (89.8%; 265/295) indicated that checking an antibiogram (antibiotic susceptibility test) before prescription is important, suggesting a good understanding of the necessity of conducting AST in the selection of an appropriate antibiotic compound [20]. However, only 4.4% (13/295) of the respondents requested for AST of all five prescriptions in the last 6 months for guidance and informed their clinical decision on antibiotic prescription. Other participants were inconsistent and/or did not see a need for AST in all the five antibiotic prescriptions. This implied that veterinarians’ sound knowledge does not translate into good practice, however factors impeding this translation were revealed to include clients’ inability to pay for AST (first-ranked factor), desire for quick results (second-ranked factor), and lack of a nearby diagnostic laboratory (third-ranked factor). This finding corroborates previous reports that the unavailability of veterinary laboratory services and clients’ inability to pay for services are key barriers to conducting AST by veterinarians [9, 21]. In middle-income countries such as Nigeria, the average cost of conducting AST in veterinary laboratories ranges from ₦4,500– ₦10,000 ($2.78–$6.17), depending on the location of practice, and may not be affordable to clients [22]. The challenges as a whole call for government and private institutions to establish veterinary laboratories equipped to render fast, robust, and affordable services in urban, semiurban and rural areas of Nigeria. Additionally, livestock farmers should cooperate with their veterinarians to ensure the use of existing diagnostic laboratories and to conduct AST for more effective therapy options.

Furthermore, “increase rate of irrational use among livestock owners” (1st ranked factor), “increasing number of quackeries” (2nd ranked factor) and “ease of access of the public to antibiotics at veterinary pharmacies/shops” (3rd ranked factor) were veterinarians’ perceived additional causes of unceasing AMR in livestock production in Nigeria. Several reports globally claimed that the increase in antibiotic resistance in animal production is largely caused by excessive use of antibiotics due to farmers’ concerns for the welfare of their cattle and desire to treat ailments swiftly [2, 3, 9, 11, 20, 21, 23]. Additionally, overprescription of antibiotics by veterinarians and poor attitudes of veterinarians with more years of practice were perceived to be contributors to the increase in antibiotic-resistant strains by an international group of veterinarians from different countries [11].

Multiple regression analysis revealed that veterinarians’ understanding of the importance of performing an antibiotic susceptibility test before prescription was a positive and significant determinant of veterinarians’ perception of the cause of antibiotic resistance. This finding is a clear indication that educational programmes such as the “Antimicrobial Stewardship Programme”, which are capable of updating and refreshing prescribers’ knowledge of their roles as antibiotic stewards, are undoubtedly among the best strategies for sustainably reducing antibiotic resistance in animal and human populations. The willingness of veterinarians to participate in the AMR programme is clearly a favourable attitude towards continual learning through educational programmes as one of the strategies to reduce the growing trend of AMR in any part of the globe. This factor is expected to result in a large number of veterinarians when they are invited to the AMR stewardship workshop. This finding corroborates the findings of Aworh et al. [24], who reported that veterinarians in Nigeria understood the importance of antimicrobial stewardship (AMS) programmes as a way to reduce antibiotic overuse. Hence, the veterinary profession needs an in-depth understanding of the AMS intervention concept, the coordination, and frameworks for the development and implementation of an efficient antimicrobial stewardship programme.

This study revealed that irrational antibiotic use among livestock owners, an increasing number of quackeries and public access to antibiotics at veterinary pharmacies/shops are the leading causes of increasing antimicrobial resistance in livestock production in Nigeria. Therefore, this study suggests a policy process that promotes the establishment of veterinary laboratories in rural, semiurban and urban communities where livestock farmers are located across the country and minimizes AST-associated costs. Such a policy should also consider limiting access to antibiotics as well as ending quackeries in animal production. Additionally, relevant government and nongovernmental bodies can organise antimicrobial stewardship workshops for veterinarians and all relevant stakeholders in livestock production. As revealed in this study, the organizer of such an AMR workshop should specifically focus on educating stakeholders on possible indigenous solutions to the leading causes of increasing antimicrobial resistance in Nigeria.