1. Introduction
Globally, antimicrobial resistance (AMR) is a complex public, animal, and environmental health problem, primarily fueled by inappropriate use of antimicrobials. The trends and problems associated with AMR are observed naturally in pathogenic and commensal or non-pathogenic bacterial organisms [
1,
2]. Currently, AMR is one of the greatest health threats that demands the most urgent attention in global health security. Antimicrobial abuse, misuse, and overuse in animals have devastating effects on humans, animals, and the environment, resulting in serious health and economic consequences [
3,
4]. In Africa, these consequences are often underreported due to inadequate surveillance data [
5,
6,
7]. AMR is projected to be attributed with about 4.15 million human deaths per annum in Africa by the year 2050 if left to continue uncontrolled [
6]. The understanding of barriers and enablers to effective control of AMR is poorly documented in Nigerian veterinary settings. Rational use of antimicrobials remains the main strategy for the prevention of AMR, and this can be achieved by changing the prescribers’ behavior and knowledge, right from the period of formal training. In most developing countries, particularly Nigeria, greater emphasis on AMR control has been placed on incidences in humans, with almost inexistent attention paid to animals (livestock, wildlife, and poultry industry as well as in veterinary clinical practices) until recently [
3]. Discrepancies exist and the level of attention paid to the issue of AMR among the public, animal, and environmental health sectors differ. Hence, resource allocations available to combat AMR in Nigeria have wide discrepancies with consequences of threatened food security in addition to an increased AMR challenge. There is a need to understand the current knowledge and propose means to bridge the existing gap on the trend, status, and situation of AMR arising primarily from food animals and the environment [
8,
9].
Huge antimicrobial consumption and misuse are prevalent in some low- and middle-income countries, such as Nigeria [
10,
11]. Over 20 brands of commercially available antimicrobials are used as growth promoters in the Nigerian livestock industry alone [
12], despite the issued ban by the National Agency for Food and Drug Administration and Control, the institution with the mandate to regulate antimicrobial inclusion in human foods. Antimicrobials are freely available in Nigerian markets, veterinary pharmacies, and agro-allied shops and could often be easily acquired over the counter without prescription by non-veterinarians, including pastoralist and nomadic herders [
13]. Tetracyclines are the most commonly misused antibiotics [
3,
13,
14]. Few studies have documented the irrational use of antimicrobials especially without prescription in the human medical practice in Nigeria [
15,
16]. This misuse was reportedly fueled by over-the-counter sale and access to unprescribed antimicrobials [
17,
18].
Specifically, veterinarians are very important stakeholders and play a vital role in the mitigation of AMR [
8,
19,
20,
21]. The education, awareness, and training of veterinary students is vital to the improvement of antimicrobial use patterns in farms, clinics, and hospitals as well as in many animal species [
8]. Veterinary students are future prescribers and their knowledge could influence progress in combating AMR [
8]. Inadequate exposure of veterinary students to the concept of AMR could affect their practice of drug administration and management after graduation [
22,
23,
24]. Satisfactory knowledge levels of veterinary students on personal antibiotic administration (self-consumption), in addition to their perceptions, attitude, and knowledge of AMR could enhance their practice behaviors [
8,
25].
The scope of AMR in the academic training of undergraduate veterinary students in most Nigerian schools is not clearly defined. A previous survey of final year students in five conveniently selected veterinary schools in Nigeria indicated poor knowledge of AMR [
26]. In this study, we conducted a cross-sectional survey on personal antimicrobial usage among students (year two to year six), studying for the degree of doctor of veterinary medicine (DVM) from 10 veterinary schools in the country. This is the first nationwide multi-institutional survey on the personal use of antimicrobials and knowledge, attitude, and awareness of AMR among veterinary undergraduate students in Nigeria.
4. Discussion
This multi-institutional national survey investigated the knowledge and attitude of undergraduate veterinary students on antibiotic use and antimicrobial resistance with key findings. It provides an insight into the importance of possible points of intervention. Whereas veterinary students demonstrated good personal use of antibiotics, the majority had an unsatisfactory level of knowledge of AMR. Veterinary students’ academic level of study and age groupings are important factors associated with a satisfactory knowledge of AMR. It should be understood that the higher-level classes roughly correlated with higher ages and specific training in pharmacology, microbiology, and medicine, and these may have influenced the observations above. Although the respondents demonstrated positive attitudes toward tackling AMR, their awareness of key terms and concepts of AMR is low. These findings are key to understanding the situation of antibiotic use in humans and animals as well as important to evaluate knowledge of AMR among veterinary students in Nigeria. Since these students are the future prescribers for the nation’s veterinary (production and health) and food industries, they remain important stakeholders who will be playing pertinent roles in combating AMR in food animals and the environment in the future.
While over half of the respondents (64.6%) reported that the last time they used antibiotics was over six months back, based on these self-reports, the awareness of compliance with proper antibiotic usage in humans is heightened. Previously, undergraduate pharmacy students in Sri Lanka have similarly demonstrated a high degree of compliance with antibiotic use [
30]. In the UK, over a third of human and animal health students were reported to have used oral antibiotics in the previous year [
21]. Whether this heightened compliance is associated with training received in the field of medicine, veterinary medicine, and pharmacy has not been explored, but anecdotal evidence suggests that such knowledge will influence disposition to antibiotic usage. Besides, non-medical students in Nigeria were found to have low knowledge of antibiotic use and resistance based on previous studies [
33,
34]. Similar to our finding, some students in the UK were reported to obtain antibiotics from friends or family or started treatment from leftover antibiotics from a previous supply [
21].
The gender distribution of respondents to the questionnaire in this survey corresponds to the gender aggregation of students of veterinary medicine in Nigerian universities. Overall, the surveyed students demonstrated an unsatisfactory level of knowledge of AMR, particularly in areas of knowledge of the use of antibiotics, AMR in humans and animals, and on the contributory factors to incidences of AMR. These findings signify a deficiency in aspects of the clinical training curricula, especially microbiology, pharmacology, and medicine, or lack of integration of knowledge as well as poor exposure of Nigerian veterinary students to associated outcomes of AMR. Comparably, in another survey, low knowledge about AMR was documented among final year veterinary students [
26]
It was not surprising that the senior-level students possess higher knowledge levels on AMR compared to others. In this study, satisfactory knowledge of AMR increased with an increasing academic year of the veterinary studentship. Clinical-level students (particularly those in year six) were generally better than the other students. However, more year 5 students (34.5%) had satisfactory knowledge scores of AMR in animals than year 6 students (22.4%). A possible reason could be that year 5 students have a better memory of pharmacology since in most veterinary schools in Nigeria, pharmacology lessons are concluded in year 5 with clinical or applied pharmacology. Previous evaluation, even among the senior-level non-medical students, showed that they have appreciable knowledge on AMR than those in lower levels [
33]. Sakeena et al. [
30] reported that senior pharmacy students demonstrated a significantly better understanding of antibiotics and AMR when compared to junior pharmacy students in Sri Lanka. This is also similar to the findings of Hardefeldt et al. [
25] in a national survey of Australian veterinary students. It can be inferred that greater exposure to the prudent use of antimicrobials during clinical teaching in the final year of veterinary school may lead to greater awareness and perceptions of AMR [
25]. Efforts should also be intensified to expose veterinary students in Nigeria to AMR concepts in the preliminary years of their training. Undergraduate education is likely to be the main source of improving knowledge of antibiotics, AMR, and related terminology among health professionals as previously demonstrated in Sri Lanka [
30]. Students between the ages of 22 and 26 years were four times more likely to have satisfactory knowledge on AMR in this survey, and this should translate to influence on rational use and application of antimicrobials. Students in this age category are most likely to have done preliminary years of study and maybe in the para-clinical (year four) or clinical (year five and six) years of study wherein they are exposed to pharmacology, microbiology, and related fields that may influence AMR awareness. Younger students are more informed about AMR. Expectedly, veterinary students, who are future prescribers will play an important role in the control of AMR. The observation that only a few students from three universities had satisfactory knowledge of AMR calls for serious concern. We do not have adequate information as regards the differences in curricula used to teach veterinary students across Nigerian veterinary schools, but it is expected that curricular harmonization and standardization should exist among veterinary schools in Nigeria. What is certain is that the Veterinary Council of Nigeria—the body that regulates veterinary training and practice in the country—sets a benchmark for curriculum development and use in veterinary training. We also could not confirm if AMR was adequately emphasized for teaching in the benchmark. However, our study suggests that the benchmark should be honed up, monitored, and periodically evaluated, to emphasize the teaching of AMR across years of study in veterinary schools in Nigeria. AMR education in all Nigerian veterinary schools should be reworked, reoriented, and focused to meet these identified gaps.
Respondents to our survey exhibited positive attitudes toward AMR control. A similar observation has been observed among undergraduate paramedical students [
29]. The respondents agreed that it is necessary to give more education to clinical-level students on AMR, and on the prescription of antimicrobials before graduation; dispensing of antimicrobials and control of over-the-counter access to medication; and on the conduct of research on AMR with the involvement of students. However, less than half (47.4%) of the participants agreed that they have sufficient knowledge on antibiotic use for future clinical practice. Some Australian veterinary students similarly opined that more education is needed in veterinary pharmacology [
25]. Surveyed medical students in the United Kingdom, France, and the United States of America have also demonstrated the need for more education on AMR [
29,
35,
36,
37,
38,
39]. Preliminary-level introduction and exposure to training on AMR in Nigerian veterinary schools at lower levels of training will improve students’ appreciation and understanding of antibiotic use and AMR. Also, having a one health perspective on AMR is important since it is a trans-national and global issue linking humans, animals, and the environment.
On key terms in AMR, only 42.3% of respondents were aware of the term “AMR”. This is confirmed by the previous observation of Anyanwu et al. [
26]. Similar low scores (approximately 25%) were observed for “superbugs”, “antimicrobial stewardship”, “Global Antimicrobial Resistance Surveillance System”, “Global Antibiotic Research and Development Partnership”, and the “Global Action Plan on Antimicrobial Resistance”. For the “National Action Plan for Antimicrobial Resistance, Nigeria”, three-fourths of respondents were unaware. This low level of awareness on AMR could be attributable to the lack of in-depth AMR education in Nigerian veterinary schools [
26] and deficiencies in veterinary curricula [
38,
39]. Furthermore, the unexpectedly low national attention accorded to AMR in food animals and the environment could contribute to the low awareness observed. Comparably, fewer than half of all students (44%) had heard of either “antimicrobial stewardship” or “antibiotic stewardship” in a survey of human and animal health students in the UK [
21].
A major limitation of this study was the use of an online questionnaire tool for data collection, which may be associated with enrolment bias. However, the overall response rate is sufficient to eliminate or reduce this bias. Because of the peculiar situation of some institutions, some students could have had limited access to the online questionnaire due to poor availability and limited access to the internet, and this possibly affected the uneven distribution of respondents from various schools. Also, it is harder to draw probability samples based on e-mail addresses or website visitations as well as a lack of trained interviewers to clarify and probe responses. Nevertheless, it was believed that the pre-testing before actual data collection should improve the accuracy and internal quality control of the tool. The logistic regression model was run with year two students serving as the reference against other years of study. Only one year two student had satisfactory knowledge of AMR in animals, resulting in a small sample size of year two students with satisfactory knowledge. Thus, this affected the outcome resulting in a wide confidence interval for students in higher years of study (4–6) with more satisfactory knowledge scores of AMR in animals. Also, wording options, such as “inadequacy of drug regulation agencies”, sounds extremely bias, possibly influencing students to click on them. However, only about 58% of respondents picked these options. Thus, the bias was unpronounced as envisaged.