Survey of knowledge and perceptions of antibiotic resistance and antibiotic stewardship among doctors and pharmacists in a tertiary hospital: a pilot study

Background: Antibiotic resistance poses a serious global public health threat and results in prolonged illness, increased mortality and cost. The WHO global action plan on antibiotic resistance emphasizes ve strategic objectives, including improved awareness of antibiotic resistance and optimization of antibiotic use. The objectives of this study were to assess doctors’ and pharmacists’ knowledge and perceptions of antibiotic resistance and stewardship, and hospital’s preparedness to implement antibiotic stewardship programs (ASPs). Methods: One hundred and twenty-four doctors and 61 pharmacists were surveyed in University of Uyo Teaching Hospital, Akwa Ibom State, Nigeria. Descriptive and Pearson chi-square analysis were carried out to compare knowledge and perceptions between the two groups. Results: Both doctors and pharmacists perceived antibiotic resistance as a global and national problem (98% vs 97%), respectively. Both groups perceived excessive use of broad-spectrum antibiotics and antibiotics for common cold and cough increase resistance (84% vs 75%, 71% vs 82%, respectively). Only 47% of doctors and 53% of pharmacists correctly dened antibiotic stewardship with 77% and 85%, respectively, agreeing that restriction of certain antibiotics reduces resistance. There was with no signicant difference in knowledge between the two groups in majority of questions/statements; however, there was association between length of practice and knowledge of causes of antibiotic resistance (F = 2.586; p = 0.028). Conclusion: Participants in this study showed good knowledge of the prevalence and causes of antibiotic resistance, as well as antibiotic stewardship strategies. There was however little awareness of the hospital’s plan to implement ASPs. Hospital management needs to emphasize optimizing antibiotic use through stewardship programs. questionnaire pilot test, on hospital plan implement action plan/ASPs additional and causes), and antimicrobial stewardship, and hospital’s preparedness to implement ASPs. Participants in this study had good knowledge of the burden and causes of antibiotic resistance. Both doctors and pharmacists viewed antibiotic resistance as a global and national problem, as well as a problem in their hospital. Similar ndings have been previously reported Although both professional groups perceived practices such as, prescribing antibiotics for common cold and coughs; prescribing broad-spectrum antibiotics when there are suitable narrow-spectrum alternatives and poor hand hygiene contribute to development and/or spread of resistance, less than half of the doctors (45%) were aware excessive use of antibiotics in agriculture and livestock contributes to resistance burden.


Introduction
Infections caused by antibiotic resistant bacteria are di cult to treat and are associated with increased mortality and increased healthcare cost compared to infections caused by sensitive bacteria [1]. Unnecessary or inappropriate use of antibiotics, such as, antibiotics for nonbacterial infections (in uenza, most upper respiratory tract infections (e.g., common cold), yeast infection) or selecting suboptimal type of antibiotic causes the emergence of resistant bacteria [2][3][4][5]. The World Health Organization (WHO) surveillance report of resistance in bacteria (E. coli, K. pneumoniae, S. aureus) associated with hospital and community infections showed increased resistance to rst line agents [1]. Core objectives of the WHO global action plan on antibiotic resistance include improved awareness and understanding of antibiotic resistance through effective communication, education and training of healthcare professionals and the public, as well as optimization of antibiotics use in human and animal health [6]. The WHO urges all member states to develop national action plan on antibiotic resistance that is aligned with the global action plan [6]. In line with WHO recommendations, the Nigerian government developed the Nigerian National Action Plan on antibiotic resistance 2017-2022 [7]. The objectives of this study were to assess doctors' and pharmacists' knowledge and perceptions of antibiotic resistance and antibiotic stewardship, and hospital's preparedness to implement ASPs.

Study setting and population
This was a cross-sectional survey of doctors and pharmacists practicing in the University of Uyo Teaching hospital (UUTH). UUTH is a 500-bed hospital located in Uyo metropolis, Akwa Ibom State, South-South Nigeria. It serves a population of about four million people within the state and neighboring states. It records 6000-7000 patient admission/per year. Doctors and pharmacists at any level of practice were eligible to participate in the survey. The doctors were drawn from the different departments of the hospital: Obstetrics and Gynecology, Pediatrics, Chemical Pathology, Internal Medicine, Surgery, Neuropsychiatry, Medical Microbiology, and Anesthesia. Sampling of participants was purposive.

Questionnaire Development
The questionnaire for this study was developed following review of previous studies [8][9][10][11][12] and national and international reports [7,8]. The 16-item questionnaire collected information on demographic characteristics of participants, knowledge and perceptions of the prevalence and causes of antibiotic resistance as well as factors that in uence prescribing in the hospital. We assessed doctors' and pharmacists' knowledge of antibiotic stewardship by asking them to de ne antibiotic stewardship and rate their agreement on antibiotic stewardship strategies. To gauge the hospital's preparedness to implement ASPs, we asked questions on the awareness of the national action plan on antibiotic resistance. Statements on prevalence and causes of antibiotic resistance, and antibiotic stewardship strategies were on ve-point Likert scale (strongly agree, agree, not sure, strongly disagree, disagree). Questions on the action plan/programs to minimize antibiotic resistance were a combination of 'yes'/'no'/'I don't know' and multiple choice.
We assessed content validity of the instrument by asking antibiotic stewardship expert/antimicrobial resistance strategist from Public Health England to review the questions; feedback was used to improve the instrument. The questionnaire was piloted to ten doctors and pharmacists, respectively to ensure there were no ambiguities. Following the pilot test, questions on hospital plan to implement national action plan/ASPs (Question 16) was modi ed from ve-point scale to 'yes'/'no'/'I don't know' response. The survey instrument is provided as additional le (Additional le 1).

Data Collection
We employed paper-based questionnaire which was administered over a six-week period (July 22 to August 26, 2019). Doctors and pharmacists were approached during their clinical or review meetings to complete the questionnaire; completed questionnaires were collected at the close of work on each day. Personal reminders (telephone calls, SMS and o ce visit) were given after one week for questionnaires that were not completed at close of work on the days meetings were held. Approval for the study was obtained from the University of Uyo Teaching Hospital Institutional Health Research Ethical Committee (UUTH/AD/S/96/VOL.XXI/278). Consent to participate in the survey was sought in the questionnaire.

Data analysis
Data analysis was done using SSPS software version 25 [IBM SPSS, New York, USA]. Descriptive statistics: frequency and mean were determined. For ease of analysis, knowledge and perception questions on ve-point Likert scale were modi ed to three-point scale. Strongly agree and agree were merged to 'agree' while strongly disagree and disagree were merged to 'disagree'; not sure option was unaltered. For statements on causes of antibiotic resistance and antibiotic stewardship strategies, we assigned scores to participants' responses. 'Agree' response was the correct response and was assigned one point. 'Not sure' and 'disagree' were grouped to be incorrect responses, and were together assigned zero point.
We used Pearson chi-square test to compare knowledge/perceptions of prevalence and causes of antibiotic resistance and strategies to contain antibiotic resistance between the two professional groups (doctors and pharmacists). Furthermore, we sought to determine whether length of practice had any in uence on knowledge of causes of antibiotic resistance and antibiotic stewardship strategies between the two groups. We determined sum scores for causes of antibiotic resistance and antibiotic stewardship strategies and used one-way ANOVA to assess in uence of length of practice on knowledge. Signi cant level, p-value was set at < 0.05

Results
Of 350 and 79 eligible doctors and pharmacists, respectively, 124 doctors (35%) and 61 pharmacists (77%) participated in the survey. Majority of the respondents were males (110/185, 60%), within the age bracket (25-34 years). The demographic characteristics of participants are summarized in Table 1. Both doctors and pharmacists perceived antibiotic resistance as a global and national problem (98% vs 97%), respectively. There were no signi cant differences in perception of burden of resistance and/or awareness of the national or hospital rates of antibiotic resistance between doctors and pharmacists, Fig. 1.

Knowledge/perceptions Of The Causes Of Antibiotic Resistance
Six statements assessed respondents' knowledge of the causes and/or factors that contribute to spread of antibiotic resistance ( Table 2). Majority of the doctors and pharmacists provided the correct response; there was no signi cant difference in knowledge between the two groups for ve of the statements. However, more pharmacists knew that excessive use of antibiotics in agriculture increases antibiotic resistance.

Factors That In uence Antibiotic Prescribing
We sought to identify factors that in uence doctors' antibiotic prescribing in the study hospital. The main factors that in uence antibiotic prescribing were knowledge of antibiotics and infections, microbiology results, evidenced-based guidelines and previous experience (Fig. 2).

Knowledge Of Programs To Minimize Antibiotic Resistance
Sixty-four of 124 doctors (52%) and 38/61 of pharmacists (63%) were aware of the term 'antimicrobial or antibiotic stewardship'. Only 47% of doctors and 53% of pharmacists correctly de ned antibiotic stewardship. Majority of doctors and pharmacists provided the correct response to statements on antibiotic stewardship strategies (Table 3). There was no signi cant difference in knowledge of antibiotic stewardship strategies between doctors and pharmacists, however, more pharmacists (p = 0.013) knew that prompt deescalation of empiric antibiotic based on culture minimizes development of antibiotic resistance.  (Fig. 3).
Insert Fig. 3 here: Association of length of practice with knowledge of causes of antibiotic resistance and stewardship strategies We assessed the in uence of length of practice on knowledge of causes of antibiotic resistance and antibioitic stewardship strategies and found that the longer the years of practice, the more knowledgeable participants were of the causes of antibiotic resistance (F = 2.586; p = 0.028). There was no association between length of practice and knowlegdge of antibiotic stewardship strategies (F = 1.185; p = 0.319).

Discussion
The objectives of this study were to assess doctors' and pharmacists' knowledge and perceptions of antibiotic resistance (prevalence and causes), and antimicrobial stewardship, and hospital's preparedness to implement ASPs. Participants in this study had good knowledge of the burden and causes of antibiotic resistance. Both doctors and pharmacists viewed antibiotic resistance as a global and national problem, as well as a problem in their hospital. Similar ndings have been previously reported [8][9][10][11]. Although both professional groups perceived practices such as, prescribing antibiotics for common cold and coughs; prescribing broad-spectrum antibiotics when there are suitable narrow-spectrum alternatives and poor hand hygiene contribute to development and/or spread of resistance, less than half of the doctors (45%) were aware excessive use of antibiotics in agriculture and livestock contributes to resistance burden.
Our ndings show that four main factors, namely knowledge of antibiotics and infections, microbiology results, evidenced-based guidelines and previous experience in uenced doctors' antibiotic prescribing in the study hospital. These ndings are however inconsistent with a previous study to determine the pattern of use of antibiotics in the same facility. In a prospective review of case notes of patients seen at the general outpatient department of the hospital, antibiotics, especially uoroquinolones were frequently prescribed without microbiology investigations [13]. The authors reported microbiology investigations were requested in only 96/511(19%) of the cases reviewed, with 80/96 (83%) of the investigations documented in the case notes and used as a guide for antibiotic prescribing. Findings of a point prevalence survey of antibiotic use in the same facility showed that 97% of inpatient antibiotic prescribing were empirical; only 3% were targeted treatment. Futhermore, evidence-based guidelines were not available and/or inaccessble in 95% of antibiotic indications (Unpublished data). Evidence has shown that doctors' antibiotic prescribing are largely guided by clinical knowledge and experience/expertise rather than guidelines/policies. Even where guidelines are available, they have little in uence on antibiotic prescribing, and are somewhat considered obstructive to autonomy and/or subordinate to clinical knowledge and experience [14,15]. education/training and restriction of certain antibiotics are important in reducing development of resistance. However, less than half of the doctors (47%) and just above average of pharmacists (53%) correctly de ned antibiotic stewardship. This suggests there is little emphasis or awareness on the role of antibiotic stewardship in combating growing antibiotic resistance. In line with WHO recommendations [6], the Nigerian National Action Plan on antibiotic resistance 2017-2022 was published [7]. Interestingly, majority of participants in this study (70% and 72%, doctors and pharmacists, respectively) were unaware of the existence of such action plan, nor were they aware of their hospital's plan to implement recommendations contained in the action plan. This nding further suggests that while government took the laudable step of developing a national action plan on antibiotic resistance, it exists in the achives of federal ministries. Little or no awareness has been created on its existence or efforts directed at ensuring its implementation. There is therefore a need for government at the national level to give priority to and lead in the ght against antibiotic resistance. This can be achieved through promotion of the national action plan at all levels of healthcare, participation in the World Antibiotic Awareness Week held November each year to create awareness of antibiotic resistance and to encourage best practices among the general public and health workers. The national government can learn from other governments [16][17][18] and develop and launch antibiotic stwardardship toolkit/guide taking into consideration available resources across all tiers of healthcare in the country.
This study had some limitations. This was a pilot/single-centre study involving only doctors and pharmacists, ndings may not be generalized to other settings. A national survey is planned; ndings will be compared with those of this pilot study. Secondly, ndings presented are self-report of doctors and pharmacists, we could not verify the honesty of participants response.
In conclusion, doctors and pharmacists in this study showed good knowledge of the prevalence and causes of antibiotic resistance, as well as antibiotic stewardship strategies, with no signi cant difference in knowledge between the two groups in majority of questions/statements. There was however little awareness of the national action plan on antibiotic resistance and hospital's plan to implement recommendations of the national action plan, including institutional antibiotic stewardship programs. Government at all levels and hospital management need to emphasize optimizing antibiotic use through stewardship programs.

Declarations
Ethics approval and consent to participate Ethics approval for this study was sought and obtained from University of Uyo Teaching Hospital Institutional Health Research Ethical Committee (UUTH/AD/S/96/VOL.XXI/278). Consent to participate in the study was sought in the questionnaire; participants were required to check box and consent to participate before proceeding to complete survey.

Consent for publication
Not applicable Availability of data and materials The datasets used and/or analysed in this study are available from the corresponding author on reasonable request. Factors that in uence doctors prescribing. ID -Infectious diseases; BNF-British National Formulary