Original Article
Veterinary Medical Students’ Perceptions, Attitude and Knowledge about Antibiotic Resistance and Stewardship: How Prepared Are
Our Future Prescribers?
Madubuike Umunna ANYANWU
1*, Onyinye Josephine OKORIE-KANU
2, Chidiebere Ohazuruike ANYAOHA
2, Oluwatosin Ajoke KOLADE
31University of Nigeria, Microbiology Unit, Department of Veterinary Pathology and Microbiology, Nsukka, Nigeria; [email protected] (*corresponding author)
2University of Nigeria, Department of Public Health and Preventive Medicine, Nsukka, Nigeria; [email protected]; [email protected]
3University of Nigeria, Veterinary Teaching Hospital, Nsukka, Nigeria; [email protected]
Abstract
A cross sectional, multicentre survey utilizing a questionnaire was used to assess 6th- (final-) year veterinary medical students’ perceptions, attitude and knowledge about antibiotic resistance (ABR) and stewardship (ABS) in 5 conveniently- selected veterinary schools in Nigeria. Data obtained were analyzed by Fischer’s exact and χ2 tests at a significance level of P <
0.05. Out of 175 final-year veterinary students, 95 (54.3% i.e., response rate) completed the survey. Of the 95, 17% have heard about ABS and 7% knew the meaning of ABS. Less than 10% knew the core principles and goals of ABS and less than 20% of the respondents knew the ideal members of an ABS team. All the respondents rightly knew that no antibiotic stewardship programme (ASP) exist in veterinary hospitals in Nigeria, nearly all of them (97%) reported that antibiograms are rarely used during antibiotic (AB) prescription in their institutional veterinary teaching hospital (VTH) and about two-third (65%) believed that ABs are overused in most veterinary hospitals in Nigeria. Most of the respondents believed that ABR is of greater concern at national level than in their institutional VTHs and majority of them (92%) believed that ABR is a global problem (P = 0.009). Minority of the respondents knew that inadequate personal hygiene, use of substandard ABs, prescription of ABs by non-veterinarians/professionals, poor infection control practices, treating self-limiting infections with ABs, suboptimal and incomplete AB doses (P = 0.017), are factors that promote ABR. Minority of the respondents knew that education on AB therapy (44%), development of antibiotic usage policies (35%), reduction of AB use (14%), establishment of national AB resistance surveillance (28%) and development of institutional guidelines for AB use (29%), are critical interventions to curb ABR. Only 17% of the respondents felt that their education on ABR is adequate for their veterinary career. Most of the respondents believed that strong knowledge of ABs is important for their future veterinary career and would like more education about ABR and ABS. Overall mean correct score of 29% on clinical knowledge vignettes with similar scores across the schools in all the areas, was recorded. This survey has shown that Nigerian veterinary students’ perception and knowledge about ABR and ABS are poor and therefore creates doubt about their preparedness to practice ABS. There is urgent need for improved ABS education in Nigerian veterinary schools.
Keywords: antibiotic resistance; antibiotic stewardship; education; veterinary medical students Print ISSN 2067-3205; Electronic 2067-3264
Not Sci Biol, 2018, 10(2):156-174. DOI: 10.25835/nsb10210258
Introduction
Antibiotic resistance (ABR) occupies the centre stage in global public health agenda because it is a “tragedy of the commons” affecting both developed and developing nations (O’Neil, 2014; Lanza et al., 2017). The threat posed by ABR has been equated to climatic change and this is of grave
concern globally (Castro-Sanchez et al., 2016; Friedman et al., 2016; Moran, 2017). It is known that ABR could potentially exert catastrophic economic and health impact which on a global scale is enormous and dreadful (Zaidi et al., 2004; Cisneros et al., 2014; O’Neil, 2014; Prestinaci et al., 2015; Fitchet and Antun, 2016).
Received: 12 Mar 2018. Received in revised form: 19 Jun 2018. Accepted: 26 Jun 2018. Published online: 29 Jun 2018.
formed (Weier et al., 2017). Inadequate preparation at undergraduate level in veterinary schools may result in practices that are untoward ABS, particularly inappropriate AB use/prescribing (Wasserman et al., 2017); therefore, there is need to equip veterinary students with adequate ABS knowledge and skills prior to their entry into the veterinary workforce (MacDougal et al., 2017; Wasserman et al., 2017; Weier et al., 2017).
Assessing veterinary students’ perception and level of knowledge about ABR and ABS and their preparedness to practice ABS is crucial for identifying gaps in knowledge;
such information could be useful for policy makers in developing adequate ABS educational programmes for veterinarians, improving curricula in veterinary schools and development of effective ASPs in veterinary hospitals (Cotta et al., 2014; Gharbi et al., 2016; Hoque et al., 2016).
Several studies have assessed medical/allied healthcare profession students’ perceptions and knowledge about AB, ABR and/or ABS and their perceptions about how prepared they are to practice ABS (Minen et al., 2010;
Pulcini et al., 2011; Abbo et al., 2013; Afzal Khan et al., 2013; Justo et al., 2013, Thriemer et al., 2013; Dyar et al., 2014; Harakeh et al., 2015; Tarao et al., 2015; Burger et al., 2016; Ferdoush et al., 2016; Haque et al., 2016; Hoque et al., 2016; Padmanabha et al., 2016; Yang et al., 2016; Weier et al., 2017; Dyar et al., 2018; Wasserman et al., 2017).
These studies reported significant differences among the students in terms of perceptions and knowledge about ABS and ABR. Studies evaluating veterinary medical students’
perceptions and knowledge about ABR and ABS and their preparedness to practice ABS, are rare in the literature. The only study which assessed veterinary students’ perception and knowledge about ABR and ABS is that of Dyar et al. (2018) in the United Kingdom (UK). There have been calls (Wesse et al., 2015; Brink et al., 2017; Dyar et al., 2018) for studies evaluating veterinary students’ perceptions and knowledge about ABR and ABS.
In Nigerian veterinary medical schools, courses on ABR are taught in the 3rd and 4th years in Microbiology and Pharmacology, and students are further exposed to AB sensitivity testing and prescription in the 6th (final) year during clinical postings/rotations in their respective institutional veterinary teaching hospitals (VTHs) (Anyanwu and Kolade, 2017). No study has evaluated Nigerian veterinary medical students’ perceptions, attitude and knowledge about ABR and ABS. Likewise there are no data on the perception of Nigerian veterinary students about their preparedness to practice ABS. This study was, therefore, undertaken to assess final-year veterinary medical students’ perceptions and knowledge about ABR and ABS.
Materials and Methods Study design, site and population
This cross-sectional, multicentre descriptive survey was carried out between June and August, 2017 in 5 (out of 10 registered) Universities in Nigeria offering Veterinary Medicine (VM): the University of Nigeria, Nsukka in Enugu State southeastern region, the Michael Okpara Federal University of Agriculture, Umudike in Abia State southeastern region, the Ahmadu Bello University, Zaria in Amongst the numerous contributions to ABR,
inappropriate use of antibiotics (ABs), especially wrong prescribing behavior by healthcare professionals, including veterinarians, have been identified as a major factor that promote ABR (Cotta et al., 2014; Wasserman et al., 2017).
Lack of knowledge required for appropriate use of AB and scarce training offered to healthcare professionals, have been identified as the major cause of wrong use of AB by healthcare/veterinary practitioners (Cisneros et al., 2014). It is known that AB is prescribed by virtually all clinicians/veterinarians, including allied healthcare professionals, regardless of training or knowledge (Abbo et al., 2013; Wasserman et al., 2017).
Veterinary settings are reservoirs of zoonotic multidrug- resistant organisms, particularly in developing countries, including Nigeria, owing to inappropriate use of ABs (Van Boeckel et al., 2015; Moran, 2017). Therefore, veterinarians are expected to be in the frontline of the fight against ABR (Castro-Sanchez et al., 2016; Brink, et al., 2017; Moran, 2017; Dyar et al., 2018). Optimization of AM prescribing is the best way to checkmate escalating ABR worldwide and to preserve AB for future generations (Broom et al., 2016;
Moran, 2017). Interventions that strengthen the concept of
‘One-Health’ at the human-animal interface such as antibiotic stewardship (ABS), have been established the best strategy to contain ABR (Cisneros et al., 2014; Bowater, 2015; O’Donnel and Guarrascio, 2016; Wasserman et al., 2017). Education (especially of the healthcare workers and the public) on AB therapy and ABR is considered one of the most important interventions/strategy of ABS (Wasserman et al., 2017; O’Donnel and Guarrascio, 2017; MacDougall et al., 2017). The World Health Organization (WHO) identified education of healthcare workers and health profession students on rational AB prescribing and ABS as an integral part of all ABR containment activities (Vickers, 2011; WHO, 2012; Abbo et al., 201; Hoque et al., 2016). It has been observed that ABS efforts in most parts of the world focused more on understanding the perceptions of practicing physicians/veterinarians and modifying their behaviors, with far less attention being paid to the education of medical and veterinary medical students (Abbo et al., 2013; Luther et al., 2013; MacDougall et al., 2017) . It is a well-established fact that for ABR to be contained, the next generation of healthcare professionals, particularly the physicians and veterinarians who are the major prescribers and/or dispensers of ABs, must be better prepared to use AB more judiciously (Abbo et al., 2013; Fairles, 2013;
Schwartz, 2016; O’Donnel and Guarascio, 2017) . Thus, education of veterinary medical undergraduate students on ABS is critical for the control of ABR because these future veterinarians are to be in the frontline (as professionals and educators of other allied healthcare professionals, the public and their clients/patients) in infection control, development, establishment and implementation of ASPs (Delit et al., 2007; Wasserman et al., 2017; O’Donnel and Guarascio, 2017). A veterinarian with insufficient knowledge about ABs, ABR and ABS would neither be able to practice ABS nor lead others in stewardship programmes (Brink et al., 2017). Moreover, it is difficult for veterinarians to change habits that are untoward ABS once they are
157
Kaduna State northwest region, the Federal University of Agriculture, Markurdi in northcentral region and the University of Abuja in the Federal Capital Territory. The University of Nigeria, Nsukka served as the coordinating site. The participating schools were selected by convenience sampling. The total number of registered final-year veterinary medical students (VMS) in these five participating schools as at the period of the study was 175 (Table 1). The target population comprised of all registered final-year VMS in the various schools. Only those who were willing to participate in the survey and provided written informed consent were included in the study. The 6th-year was selected purposefully for this survey because it is the last (final) year of undergraduate studies in VM schools in Nigeria and a good estimation of the knowledge of veterinary students about ABR and ABS could be obtained at this level since these students have completed their pre- clinical and clinical years, including rotations in their respective institutional VTHs.
Ethical approval
Ethical approval was not necessary for this study;
however, permission to conduct the study was obtained from the University of Nigeria Research Ethics Committee.
Permission to conduct the study in each of the participating sites was obtained from the lecturer who served as the Head/Coordinator of the final-year class. Informed consent of all participants involved in the study was obtained and confidentiality and anonymity of the data obtained was ensured.
Data collection
Information about students’ demographics, knowledge/perceptions of principles, goals and development strategies of ABS, ABR and AB use/prescribing, resources used for AB education and clinical knowledge vignettes, was collected using a self- administered structured questionnaire. The questionnaire was developed after thorough review and modification (to adapt for veterinary students) of comparable studies (Abbo et al., 2013; Burger et al., 2016; Yang et al., 2016;
Wasserman et al., 2017) and validated by a pilot study on 15 fresh VM graduates from the 5 veterinary schools.
Knowledge was assessed using 11 validated clinical vignettes (Abbo et al., 2013; Yang et al., 2016). The surveys were administered to final-year VM students during whole class lectures at the participating veterinary schools. The students were instructed to abstain from using resources or consulting peers in filling the survey (Thriemer et al., 2013;
Justo et al., 2014; Wasserman et al., 2017). They were also
asked to fill the questionnaires on-site within 4 hours to ensure that consultation of resources and peers are precluded (Thriemer et al., 2013). No incentives were given to the participants. Participation was voluntary and responses were anonymous.
Data analysis
The participating veterinary medical schools were de- identified as “A”, “B”, “C”, “D” and “E” in order to conduct blinded data analysis. Answers to questions that used a 5- point Likert scale were merged into two dichotonomous categories (strongly agree/agree and strongly disagree/disagree/neutral, often/occasionally/sometimes and rarely/never, very good/good and poor/very poor/neutral) (Abbo et al., 2013; Justo et al., 2014; Yang et al. 2016). Data were entered into Microsoft Excel sheet version 15.0 and exported to SPSS version 15.0 for analysis.
Frequencies and percentages of all variables were calculated.
Non parametric tests were used to assess for the presence of any significant difference among the students’ response from the 5 survey sites. The Fischer’s exact and χ2 tests were used to compare the parameters as appropriate and statistical significance was set at P < 0.05. An overall knowledge score was evaluated by calculating the total percentages (each counts one point) of correct answers for the vignette-based questions (Aboo et al., 2013; Yang et al., 2016).
Results
Response rate
Ninety five final-year VMS out of a total of 175 registered students in the 5 veterinary schools completed the survey for an overall response rate of 54.3% (range across schools, 31.7%-100%). Response rate by schools are shown in Table 1.
Student demographics
Overall, 65.3% (62/95) of the respondents were males while 34.7% (33/95) were females. More than two-third (70.5%, 67/95) of the respondents were between the ages of 20 and 25 years, 26.3% (25/95) were between 26 and 30 years while 3.2% (3/95) were 30 years and above.
Background knowledge and perceptions of antibiotic stewardship
Respondents’ background knowledge and perceptions about ABS are summarized in Table 2. Overall, a low proportion (17%) of the respondents agreed that they have heard of ABS, with 8%, 2%, 3%, 7% and 1% of these having heard or learnt about ABS from lecturer(s), peers, senior
Table 1. Response rate by school
University Number of final-year Veterinary Medicine students
Response rate
Number (n) Percentage
A 45 25 55.6
B 63 20 31.7
C 32 19 59.4
D 22 18 81.8
E 13 13 100
All 175 95 54.3
colleagues, mass media and scientific journals, respectively.
Only 7% of the respondents agreed that they know the meaning of ABS. Regarding perceptions and knowledge about the principles of ABS, 4% of the respondents agreed that ABS involves therapeutic monitoring of AB use and timely collection of appropriate specimens for microscopy, culture and sensitivity while 7% knew that ABS involves choosing the proper AB, timely administration of AB at the appropriate dose and route, and administering AB for appropriate duration in every case. Five percent of the respondents perceived that using AB only when needed is among the principles of ABS while 3% of the respondents knew that ABS involves improving hygiene and infection control, and the study of AB.
Perceptions and attitudes about antibiotic use/prescribing and resistance
Respondents’ perceptions and attitude about AB use/prescribing and resistance is summarized in Table 3.
The majority of the respondents (72%) (range across institutions, 44%-100%; P = 0.009) agreed that ABR is a global problem while far less minority of the respondents (9%) (range across institutions, 0%-4%; P = 0.030) agreed that ABR is not a significant problem in Nigeria.
Concerning factors that promote ABR, slightly above half (55%) of the respondents agreed that widespread/overuse of
AB in humans/animals promotes ABR. Very little proportion of the respondents (8%) knew that poor hand washing practice and poor infection control practices are also contributors to ABR. Minority of the respondents agreed that substandard quality of ABs (15%), administration of inappropriate quantity of AB for inadequate duration (23%), use of broad-spectrum AB for treating animals when narrow-spectrum is available (26%) and use/prescription of ABs by non- veterinarians/professionals (29%), respectively, are also factors and practices that promote ABR. Two-third of the respondents (65%) agreed that prescribing and use of ABs in veterinary hospitals are not appropriate in Nigeria. About one-third of the respondents (35%) agreed that they have prescribed/have been allowed to prescribe AB in their institutional VTH where they have rotated while nearly all the respondents (97%) indicated that antibiograms are rarely used during prescription in their institutional VTH where they have rotated. Less than one-third (28%) of the respondents reported that ABs are overused in their institutional VTH where they have rotated but a majority of the respondents (73%) reported that ABR is not a significant problem in their institutional VTH where they have rotated. A high proportion of the respondents (78%) agreed that better use of ABs will reduce problems with ABR and majority of the respondents (73%) also indicated
Table 2. Veterinary medical students’ background knowledge and perceptions of antibiotic stewardship Background knowledge
Percentage (rounded) of students per university who strongly agree/agree
P value School
All (n = 95)
A (n = 25)
B (n = 20)
C (n = 19)
D (n = 18)
E (n =13) I am familiar with the term or have heard
about antibiotic stewardship 17% 24% 20% 16% 6% 15% 0.621a
I know the meaning of antibiotic
stewardship 7% 8% 15% 5% 0% 8% 0.567a
Source/Means from which antibiotic stewardship was heard/learnt
Lecturer 8% 20% 0% 5% 0% 15% 0.050a
Peers (other students) 2% 0% 5% 0% 6% 0% 0.596a
Senior colleague 3% 0% 10% 0% 0% 8% 0.134a
Mass media (newspaper, magazine, radio,
television, internet) 7% 8% 10% 16% 0% 0% 0.362a
Scientific journals 1% 0% 5% 0% 0% 0% 0.737a
Seminar/conference/symposium 0% 0% 0% 0% 0% 0% Nc
Principles of antibiotic stewardship Timely collection of appropriate
specimens for microscopy, culture and sensitivity
4% 8% 0% 5% 0% 8% 0.551a
Using antibiotic only when needed 5% 8% 5% 0% 6% 8% 0.821a
Choosing the proper antibiotic for specific
infection 7% 16% 0% 11% 0% 8% 0.173a
Timely administration of antibiotics at the
appropriate dose and route 7% 8% 5% 16% 0% 8% 0.515a
Administering antibiotic for appropriate
duration in every case 7% 20% 5% 0% 0% 8% 0.065a
Therapeutic monitoring of antibiotic use 4% 8% 0% 5% 0 0% 8% 0.551a
Improved hygiene and infection control 3% 8% 0% 0% 0% 8% 0.331a
The study of antibiotics 3% 12% 0% 0% 0% 0% 0.116a
aFischer’s exact test Nc: Not calculable
160 Table 3. Veterinary medical students’ perceptions and attitude about antibiotic use and resistance
Perceptions and attitude
Percentage (rounded) of students per university who strongly agree/agree
P Value School
All (n = 95) A (n = 25) B (n = 20) C (n = 19) D (n = 18) E (n = 13) Antibiotic resistance is a global
problem 72% 68% 70% 84% 44% 100% 0.009b
Inappropriate use of antibiotics can directly
harm patients 84% 96% 70% 95% 72% 85% 0.047a
Antibiotic resistance is not a significant problem in my institutional Veterinary Teaching Hospital where I have rotated
73% 56% 70% 79% 83% 85% 0.210b
Antibiotic resistance is not a significant
problem in Nigeria 9% 4% 20% 0% 22% 0% 0.030a
Contributors/promoters of antibiotic resistance Widespread/overuse of antibiotics in
humans and animals 55% 48% 55% 74% 61% 31% 0.168b
Unnecessary use of broad-spectrum antibiotic for treating animals when narrow-
spectrum antibiotic is available
26% 36% 30% 26% 6% 31% 0.250b
Poor hand washing practice by
healthcare/veterinary workers 8% 8% 5% 5% 6% 23% 0.467a
Inadequate farm biosecurity and animal
vaccination 8% 12% 10% 0% 11% 8% 0.624a
Using/prescribing antibiotics by non-
veterinarians/non-professionals 29% 32% 40% 21% 28% 23% 0.741b
Administering inadequate antibiotic doses
for inappropriate frequency 23% 48% 20% 16% 6% 15% 0.017a
Prescribing and using substandard quality of
antibiotics to treat animals 15% 16% 20% 21% 11% 0% 0.465a
Antibiotic use attitudes in veterinary settings Prescribing and use of antibiotics in
veterinary hospitals in Nigeria are not appropriate
65% 64% 60% 89% 50% 62% 0.133b
I have prescribed or have been allowed to prescribe antibiotic in my institutional Veterinary Teaching Hospital where I have
rotated
35% 32% 20% 47% 28% 54% 0.219b
Antibiograms are rarely used during prescription in my institutional Veterinary
Teaching Hospital where I have rotated
97% 96% 100% 89% 100% 100% 0.362a
Antibiotics are overused in my institutional Veterinary Teaching Hospital where I have
rotated
28% 40% 35% 37% 11% 8% 0.087b
Better use of antibiotic will reduce problems
with antibiotic resistance 78% 76% 80% 74% 67% 100% 0.206a
I would like more education on antibiotic
resistance 73% 84% 70% 89% 61% 77% 0.258a
Factors that could influence my decision to prescribe antibiotic
Client pressure/push 18% 8% 45% 11% 17% 8% 0.020a
Health status/condition of the patient 37% 20% 50% 21% 56% 46% 0.043b
Peers (other students) 8% 8% 5% 11% 11% 8% 0.964a
Senior colleague 11% 8% 20% 5% 6% 15% 0.541a
Antibiogram of isolates 52% 68% 10% 68% 50% 62% <0.001
Cost of antibiotic 37% 52% 10% 63% 28% 23% 0.002b
Profit to be made 15% 16% 25% 5% 17% 8% 0.487a
Ensure therapeutic success 40% 32% 50% 42% 44% 31% 0.716b
Troublesome resistant zoonotic bacteria of public health concern
Staphylococcus aureus 39% 44% 65% 11% 33% 38% 0.013b
Pseudomonas aeruginosa 17% 24% 35% 0% 11% 8% 0.024a
Klebsiella pneumoniae 6% 16% 5% 5% 0% 0% 0.278a
Enterococcus faecium 4% 4% 5% 5% 6% 0% 1.000a
Clostridium difficile 13% 16% 10% 0% 33% 0% 0.017a
aFischer’s exact test
bχ2 test
161
that they would like more education on ABR.
Regarding factors that could influence the respondent’s prescription of AB, 18% (range across institutions, 8%-45%;
P = 0.020) agreed that their client could influence them, 37% reported that the health status/condition of the animal (range across institutions, 20%-56%; P = 0.043) and cost of AB (range across institution, 10%-63%; P = 0.002) could influence their prescription, slightly above half of the respondents (52%) (range across institutions, 10%-68%; P
< 0.001) reported that antibiogram of the isolate could influence them, while 8%, 10%, 14% and 40% agreed that peers, senior colleague(s), profit to be made, and ensuring therapeutic success, are factors that could influence their prescription of AB (Table 3).
With regards to perceptions/knowledge about zoonotic resistant bacteria of public health concern, 39% (range across institutions, 11%-44%; P = 0.013) of the respondents recognized Staphylococcus aureus, Pseudomonas aeruginosa 17% (range across institutions, 0%-35%; P = 0.024), and Clostridium difficile 13% (range across institutions, 0%- 33%; P = 0.017) (Table 3). Far less minority of the respondents agreed that Klebsiella pneumoniae (6%) and Enterococcus faecium (4%) are also problematic zoonotic resistant bacteria.
Perceptions and knowledge about goals and development strategies of antibiotic stewardship
The respondents’ perceptions about goals and development strategies of ABS are summarized in Table 4.
Concerning the goals of ABS, minority of the respondents knew that ABS seek to reduce hospital stay (2%), reduce ABR (17%), and minimize toxicity and other adverse effects (6%). Very minimal proportion of the respondents agreed that ABS seek to increase the use of broad-spectrum AB (1%) and increase duration of therapy to ensure therapeutic success (2%) whereas none of the respondent agreed that increasing the use of AB is among the goals of ABS.
Regarding the development strategies of ABS, minority of the respondents (19%) agreed that assembling and leading of the core ABS team is one of the responsibilities of the veterinarians in ASPs. None of the respondent agreed that ASP exist for veterinary hospitals in Nigeria. For the formation of ABS team, low proportion of the respondents agreed that veterinarians (19%), veterinary assistants (5%), physicians (9%), veterinary hospital pharmacists (13%) and infection control staffs (8%), are members of ABS team.
There was also agreement by a minority of the respondents (13%) that hospital cleaning staffs are members of ABS team but with significant variation (P < 0.001; range across institutions, 0%-50%) in responses of the respondents.
Pertaining to the role of veterinarians in ABS, prescribing AB over-the-counter was thought to be the major role of veterinarians (69%) whereas promoting optimal use of antibiotic (15%), educating veterinary allied healthcare professionals (13%) and working with therapeutic committees to develop policies (7%), were regarded as the minor roles of veterinarians in ASPs.
Regarding interventions that could help in curbing ABR, majority of the respondents (92%) agreed that the establishment and implementation of ASPs in veterinary hospitals are essential in Nigeria while less than half of the respondents agreed that education on AB therapy (44%)
and development of AB usage policies (35%) are useful interventions to contain ABR (Table 4). Less than one- third of the respondents agreed that reduction of AB use (14%), establishment of national AB resistance surveillance (28%) and development of institutional guidelines for AB use (29%), are interventions to curb ABR. Majority of the respondents (84%) agreed that inappropriate use of AB can harm patients although with significant difference in responses between the schools (range across institutions, 70%-96%; P = 0.047). Only half of the respondents (51%) agreed that avoidance of treating self-limiting infections reduces ABR. High proportion of the respondents (88%) agreed that strong knowledge of AB is important for their future veterinary career and teaching about ABR and ABS at all levels of veterinary education will enhance appropriate use of AB by veterinarians. Majority of the respondents (71%) agreed that new AB will be developed in the future that will keep up with the problem of ABR.
Perceptions about education on appropriate antibiotic use and stewardship preparedness
Respondents’ perception about the quality and quantity of their ABS education and ABS preparedness is summarized in Table 5. Overall, minority of the respondents (12%) agreed they have had formal lecture on ABS for 1-4 hours whereas most of them (88%) reported that they have never had any formal training on ABS. None of the respondents agreed to have ever had ABS training for 5 hours. A low proportion of the respondents (17%) were confident that what they were taught on ABR resistance is enough for their veterinary career while most of them (84%) indicated that they would like more training on ABS.
Regarding topics on AB and AB therapy, 68 out of 95 (72%) of the students recalled that spectrum of therapy for different AB have been taught very well with significant variation in responses between the schools (range across institutions, 56%-96%; P = 0.020). Most of the respondents agreed that their education about the basic mechanisms of ABR (74%) and how to select the best AB for specific infection was good/very good. Less than two-third (59%) of the respondents also believed that their education about how to find reliable information to treat patients, when to start AB therapy (57%), and how to interpret antibiograms (60%) was good/very good while less than one-third lacked confidence about their education on transitioning from intravenous to oral ABs (27%), streamlining/de-escalating AB therapy (19%) and handling clients demanding unnecessary AB for their animals (41%).
Educational resources used for learning about antibiotic use and resistance
Sources of information about AB use and resistance used by the respondents are summarized in Table 6. The sources of information used by the respondents were, in rank of decreasing frequency: iPhone/Smart phone applications (36%), lecturers/resident doctors (25%) (range across schools, 0%-40%; P=0.014), textbooks /Merck’s/Black’s veterinary manual (17%), class lecture notes (16%) (range across schools, 0%-35%; P = 0.010), Nigerian veterinary formulary (14%), medical/veterinary journals (12%) (range across schools, 0%-24%; P = 0.023), Wikipedia (8%), peers (other students) (5%), veterinary hospital pharmacists (3%) and veterinary assistants (2%).
162 Table 4. Veterinary medical students’ perceptions and knowledge about goals and development strategies of antibiotic stewardship
Goals and development strategies of antibiotic stewardship
Percentage (rounded) of students per university who strongly agree/agree
P Value School
All (n = 95) A (n = 25) B(n=20) C (n = 19) D (n = 18) E (n = 13) Goals of antibiotic stewardship
Increasing the use of antibiotics 0% 0% 0% 0% 0% 0% Nc
Reducing hospital stay 2% 0% 10% 0% 0% 0% 0.133a
Increasing duration of therapy to ensure
therapeutic success 2% 0% 5% 0% 0% 8% 0.299a
Increasing use of broad-spectrum
antibiotics 1% 4% 0% 0% 0% 0% 1.000a
Reducing antibiotic resistance 17% 20% 15% 21% 6% 23% 0.630a
Minimizing toxicity and other adverse
effects 6% 4% 5% 11% 6% 8% 0.945a
Members of the antibiotic stewardship team
Physicians 9% 20% 5% 11% 6% 0% 0.351a
Veterinary assistants 5% 12% 5% 0% 6% 0% 0.534a
Veterinary hospital pharmacists 13% 24% 5% 16% 11% 0% 0.221a
Infection control staff 8% 12% 5% 11% 11% 0% 0.775 a
Veterinary clinical microbiologist 5% 12% 5% 0% 6% 0% 0.534 a
Veterinary hospital cleaning staff 13% 12% 0% 0% 50% 0% <0.001
Veterinarians 19% 24% 5% 16% 28% 23% 0.340a
Roles of veterinarians in antibiotic stewardship Assembling and leading of the core
antibiotic stewardship team 19% 16% 5% 21% 33% 23% 0.234a
Promoting optimal use of antimicrobials 15% 12% 10% 21% 17% 15% 0.871a
Educating veterinary allied healthcare
professionals/public 13% 12% 5% 21% 11% 15% 0.650a
Working with therapeutic committees to
develop policies 7% 8% 10% 5% 11% 0% 0.852a
Prescribing antibiotics over-the-counter 69% 48% 85% 79% 67% 77% 0.062b
Interventions that can help in combating antibiotic resistance
Development of antibiotic usage policies 35% 40% 50% 26% 33% 15% 0.283b
Reduction of antibiotic use 14% 16% 25% 11% 11% 0% 0.373a
Establishment of national antibiotic
resistance surveillance 28% 36% 40% 11% 28% 23% 0.274b
Development of institutional guidelines for
antibiotic use 29% 32% 40% 16% 17% 46% 0.201b
Education on antibiotic therapy 44% 56% 40% 37% 44% 38% 0.723b
Antibiotic stewardship programme exist for
veterinary clinics/hospitals in Nigeria 0% 0% 0% 0% 0% 0% Nc
Establishment and implementation of antibiotic stewardship programmes in veterinary hospitals are essential in Nigeria
92% 92% 90% 89% 89% 100% 0.863a
Avoidance of treating self-limiting infections in animals reduces antibiotic
resistance
51% 40% 50% 74% 56% 23% 0.055b
Teaching about antibiotic resistance and stewardship at all levels of veterinary education will enhance appropriate use of
antibiotics by veterinarians
88% 96% 75% 84% 78% 92% 0.242a
Strong knowledge of antibiotics is
important for my future veterinary career 88% 92% 80% 84% 78% 92% 0.645a
New antibiotics will be developed in the future that will keep up with the problem of
antibiotic resistance
71% 68% 70% 68% 72% 77% 0.984b
aFischer’s exact test
bχ2 test; Nc: Not calculable
Table 5. Veterinary medical students’ perceptions of their antibiotic stewardship education and preparedness 163
Perceptions
Percentage (rounded) of students per university who strongly agree/agree
P Value School
All (n = 95) A (n = 25) B (n = 20) C (n = 19) D (n = 18) E (n = 13) I have attended a formal lecture on antibiotic
stewardship 12% 16% 20% 5% 6% 8% 0.573 a
I have attended a 1-4 hour antibiotic
stewardship lecture or training 12% 16% 20% 5% 6% 8% 0.573 a
I have attended antimicrobial stewardship lecture/training that lasted more than 5
hours
0% 0% 0% 0% 0% 0% Nc
I have had no formal antibiotic stewardship
lecture/training 88% 84% 80% 95% 94% 92% 0.573 a
What I have been taught on antibiotic resistance in the veterinary school is enough
for my future veterinary career
17% 16% 20% 5% 28% 15% 0.481 a
I would like to be trained/more training on
antibiotic stewardship 87% 96% 75% 89% 78% 100% 0.093 a
Antibiotic stewardship activity understood very well and considered useful for my career Finding reliable information to treat my
patients 59% 64% 55% 79% 56% 31% 0.097 b
Basic mechanisms of antibiotic resistance 74% 88% 70% 68% 61% 77% 0.337 a
Handling clients demanding unnecessary
antibiotics for their animals 41% 36% 55% 47% 39% 23% 0.424 a
When to start antibiotic therapy in sick
animals 57% 60% 70% 42% 61% 46% 0.423 b
Selecting appropriate antibiotic for specific
infection 79% 92% 70% 84% 78% 62% 0.166 a
Identifying spectrum of therapy for different
antibiotics 72% 96% 70% 58% 56% 69% 0.020 b
Interpreting antibiograms 60% 76% 60% 47% 50% 62% 0.330 b
Transitioning from intravenous to oral
antibiotics 27% 28% 45% 21% 28% 8% 0.209 b
Streamlining/de-escalating antibiotic
therapy 19% 20% 35% 21% 11% 0% 0.126 a
aFischer’s exact test
bχ2 test; Nc: Not calculable
Table 6. Resources used for learning about antibiotic use/prescribing and resistance Resource
Percentage (rounded) of students per university who agree to have often/sometimes/occasionally used the resource
P Value School
All (n = 95) A (n = 25) B (n = 20) C (n = 19) D (n = 18) E (n = 13) iPhone/Smartphone
applications 36% 28% 35% 42% 50% 23% 0.490b
Nigerian veterinary formulary 14% 8% 15% 32% 6% 8% 0.177a
Veterinary hospital pharmacists 3% 4% 5% 0% 0% 8% 0.755a
Veterinary assistants 2% 0% 5% 5% 0% 0% 0.681 a
Lecturers/Resident doctors 25% 36% 40% 0% 22% 23% 0.014a
Medical/Veterinary journals 12% 24% 5% 0% 22% 0% 0.023a
Textbook/Merck’s Veterinary Manual/Black’s Veterinary
Manual
17% 16% 30% 11% 17% 8% 0.507a
Peers (other students) 5% 4% 10% 0% 11% 0% 0.439a
Class lecture notes 16% 16% 35% 0% 22% 0% 0.010a
Wikipedia 8% 4% 20% 0% 11% 8% 0.191a
aFischer’s exact test
bχ2 test
Students’ mean correct knowledge score for the clinical vignettes was 29% with no statistical significance in responses between the study sites. The concepts assessed and scores are shown in Table 7. Respondents scored fairly highly on questions dealing with identification of scenarios with potential for unnecessary use of AB in animals (68%), recognizing the possible risks associated with unnecessary use of AB in animals (62%) and recognition of spectrum of activity of selected AB (56%), but poorly on questions regarding recognition of critically-important AB for human
use (9%), treating ESBL-resistant infections in companion animals (11%), recognition of Clostridium difficile infection (25%), determination of antibiogram of colistin-resistant enterobacterial isolates (2%), treating complicated urinary tract infection in companion animals (19%), and mechanisms of resistance of bacteria of zoonotic public health importance (13-23%). Suboptimal scores were recorded for Escherichia coli/β-lactam resistance (23%), Staphylococcus aureus/methicillin resistance (28%) and Enterococcus/cephalosporin (13%).
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Table 7. Summary of knowledge vignettes with corresponding proportion of correct responses by veterinary schools Clinical vignettes
Percentage (rounded) of students per university who showed correct competency
P Value School
All (n = 95) A (n=25) B (n =20) C (n = 19) D (n = 18) E (n = 13) Identify scenarios with potential for unnecessary
use of antibiotics in animals 68% 72% 80% 74% 44% 69% 0.173b
Recognize the possible risks associated with
unnecessary use of antibiotics in animals 62% 64% 50% 58% 67% 77% 0.603b
Recognize Clostridium difficile infection in humans/animals secondary to the use of
antibiotics
25% 20% 25% 37% 17% 31% 0.637b
Recognize the spectrum of activity of selected
antibiotic 56% 40% 55% 58% 67% 77% 0.222b
Colistin-resistant enterobacterial diarrhoea:
appropriate antibiotic susceptibility test 2% 4% 0% 0% 6% 0% 0.782a
Recognize critically-important antibiotics for
human use 9% 8% 10% 5% 17% 8% 0.845a
Extended-spectrum β-lactamases-producing Escherichia coli bacteraemia in companion
animals: antibiotic selection
11% 8% 15% 11% 11% 8% 0.985a
Complicated urinary tract infection in companion animals: appropriate antibiotic
selection and duration of treatment
19% 20% 25% 21% 11% 15% 0.878a
Match the antibiotic/organism with the most likely mechanism of resistance
E. coli/β-lactam resistance 23% 24% 20% 21% 22% 23% 1.000 a
Staphylococcus aureus/methicillin resistance 28% 32% 40% 32% 17% 15% 0.436b
Enterococcus/cephalosporin 13% 12% 15% 16% 11% 8% 0.722a
Overall for all questions 29% 28% 30% 30% 26% 30% 0.232a
aFischer’s exact test
bχ2 test
Discussion
This is the first assessment of Nigerian veterinary medical students’ perception about ABR and ABS and their preparedness for appropriate use of ABs, and to our knowledge it is the first of such report in Africa. In Nigeria, a fresh VM graduate is expected to start prescribing drugs from inception of a compulsory one year national youth service, thus every Nigerian veterinarian is a potential prescriber and dispenser of AB (Fairles, 2013; Anyanwu and Kolade, 2017), and there are limited opportunities (if there is any) for postgraduate training in ABS, particularly outside the academic setting (Wasserman et al., 2017). Further, there is no residency (house job/internship) programme for fresh VM graduates, and veterinarians (most of which have no experience/skill on graduation) are allowed to start
prescribing (with or without supervision by senior veterinarians) and dispensing AB immediately on graduation from veterinary schools (Anyanwu and Kolade, 2017). Given the importance of veterinarians as key partners in ABS efforts, VMS should therefore be knowledgeable about ABR and ABS (Brink et al., 2017). In this study, 3 major findings which are similar with those of multicentre studies (Minen et al., 2010; Abbo et al., 2013;
Dyar et al., 2014; Justo et al., 2014; Burger et al., 2016;
Ferdoush et al., 2016; Yang et al., 2016; Wasserman et al., 2017) conducted among medical/pharmacy students in developed and developing countries were made: (i) low level of knowledge about ABR and ABS, (ii) perceived lack of preparedness to practice ABS and lead in ASPs, and (iii) desire for more education about ABR and ABS.
The result of this study revealed that a very minimal proportion (7%) of Nigerian veterinary students may know the meaning of ABS. Burger et al. (2015) reported that 83.5% among 260 final-year pharmacy students in 3 South African Universities knew the meaning of antimicrobial stewardship (AMS). The low level of knowledge about ABS in this study is attributed to the fact that very few (17%) of the respondents in this study have heard of ABS. Ferdoush et al. (2016) reported that 6% among 171 4th-year students in 3 Bangladeshi medical schools were familiar with the term AMS while less than two-third of 289 final-year students in 3 South African medical schools reported familiarity with the term ABS (Wasserman et al., 2017).
Anyanwu and Kolade (2017) reported that 17.1% among 280 practicing/teaching veterinarians in Enugu State Nigeria have heard of ABS. The disparities in these studies may be due to differences in ABS awareness education that has been conducted in the various health profession institutions, degree of integration in the curricula and teaching of AMS education in the institutions, and/or the degree of AMS education awareness that has been conducted via sources such as mass media, journals, peers, etc in the study area (Lee et al., 2015; Anyanwu and Kolade, 2017). Among the NVS that reported familiarity with the term ABS, highest number reported that they heard about ABS from their lecturer while a very minority of them heard/learnt of ABS from their peers, senior colleagues, mass media and/or scientific journals (Lee et al., 2015). The low awareness about ABS observed in this study, suggested that there is little or no effort in Nigeria to educate veterinary students about ABS and there is also little or no ABS education awareness in form of seminars, symposium, radio jingles, etc in Nigeria (Lee et al., 2015). It also suggested that the curricula of Nigerian veterinary medical schools might be deficient on issues of ABS (Anyanwu and Kolade, 2017).
Regarding background knowledge and perceptions of ABS, it is very worrisome that very minimal proportion of NVS (7%) knew that ABS involves therapeutic monitoring of AB use, timely collection of appropriate specimens for microscopy, culture and sensitivity, choosing the proper AB, timely administration of AB at the appropriate dose and route, administering AB for appropriate duration in every case, using AB only when needed, improving hygiene and infection control, and the study of AB (O’Donnell and Guarascio, 2017). This finding contrasts Burger et al. (2016) that 50.4%-95% (range for the principles) among pharmacy students in South Africa, knew that ABS involved the above principles. Variation in the perceptions of students in these studies may be attributed to differences in exposure to ABS in the various institutions and/or study area (Thriemer et al., 2016; Anyanwu and Kolade, 2017).
The low level of knowledge about ABS principles in the present study, further suggested that veterinary students in Nigeria may not be well exposed to the basic principles of ABS.
In this study, respondents shared common perceptions and attitudes about AB use/prescribing and resistance across the veterinary schools. Inappropriate AB use may result from inadequate preparation at undergraduate level and an under-appreciation of the extent and implications of ABR (O’Donnell and Guarascio; 2017; Wasserman et al.,
2017). About two-third (65%) of the respondents in this study perceived that AB prescribing and use in most Nigerian veterinary hospitals are inappropriate. This finding is higher than 53.9% reported by Anyanwu and Kolade (2017) among practicing/teaching veterinarians in Enugu State Nigeria, who also agreed that AB prescribing and use in most Nigerian veterinary hospitals are inappropriate. But it is lower than 94% among 311 final-year students in 3 American medical schools (Abbo et al., 2013), 84.8%
among 611 4th-year students in 3 Chinese medical schools (Yang et al., 2016) and 87.5% among medical doctors/students in the Democratic Republic (DR) of Congo (Thriemer et al., 2013), respectively, who agreed that antimicrobials (AMs) are overused nationally in healthcare.
It has been severally reported that > 50% of AB prescription in hospitals could be adjudged inappropriate (Cotta et al., 2014; Cisneros et al., 2014); the case of veterinary hospitals in Nigeria may not be different as almost all the students in this study reported that antibiograms are rarely used during empiric treatment in their institutional VTH where they have rotated and about half of the students do not know that treating self-limiting infections with ABs promotes ABR. It is disconcerting that despite the fact that all the participants in this study agreed that ASP does not exist in any veterinary clinic/hospital in Nigeria, less than one-third (28%) perceived that ABs are overused in their institutional VTH where they have rotated. Sixty nine percent among 579 graduating students in 12 American pharmacy schools (Justo et al., 2014) and 63% among medical students in South Africa (Wasserman et al., 2017), respectively, perceived that AMs are overused in hospitals where they have rotated/are working.
The lower perception on AB overuse in local settings observed in this study, further suggested that NVS may not be well grounded on the issues of ABR and ABS, this is because arbitrary AB prescription not based on culture and sensitivity as observed in the hereby study, is a major cause of ABR (Coyne et al., 2016; O’Donnell and Guarascio, 2017). It equally suggested that these students may also not be well grounded on how to detect cases associated with resistance in animals (Afzal Khan et al., 2013; O’Donnell and Guarascio, 2017). Many drivers are associated with overuse of drugs in Nigerian veterinary settings, including the use of AB to counterbalance poor hygiene, lack of knowledge/awareness about appropriate AB for specific infections, etc (Thriemer et al., 2013; Anyanwu and Kolade, 2017; O’Donnell and Guarascio, 2017). However, AB overuse could result from the intention to fulfill the responsibility of offering optimal therapy to the individual patient under a veterinary clinician’s care while neglecting/overlooking the responsibility of preserving the efficacy of AB and minimizing the development of resistance in the same patient and other patients in the future and to public health (Scaioli et al., 2015; Gharbi et al., 2016; Anyanwu and Kolade, 2017).
Concerning the impact and scope of ABR, majority of the respondents (74%) in this study believed that ABR is a global problem, but there was significant variation (P = 0.009) in responses between the schools. The global problem of ABR was perceived stronger (85.4%-97.7%) among medical/pharmacy students in other countries (Afzal Khan et al., 2013; Thriemer et al., 2013; Burger et al.,
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