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Implementation of antibiotic stewardship in different settings - results of an international survey

Implementation of antibiotic stewardship in different settings - results of an international survey Background: Antibiotic stewardship interventions are being implemented across different healthcare settings. We report the findings of a global survey of healthcare professionals on the implementation of antibiotic stewardship programmes. Methods: Learners of a Massive Online Open Course (MOOC) on antibiotic stewardship were invited to complete an online survey on the core available organisational resources for stewardship. The categorical variables were analysed using chi-squared test, and Likert questions were analysed using an ordinal regression model. The p-values were considered as two-tailed. Significance was set at p-value of < 0.05. Results: The response rate was 55% (505/920), from 53 countries. The responders were 36% (182) doctors, 26% (130) pharmacists, 18% (89) nurses and 20% (104) other (researchers, students and members of the public). Post- graduate training in infection management and stewardship was reported by 56% of doctors compared with 43% (OR 0.59, 95%CI 0.35–1.00) nurses and 35% (OR 0.39, 95%CI 0.24–0.62) of pharmacists. Hospitals were significantly (83% in teaching hospitals, 79% in regional hospitals, p = < 0.01) more likely to have antibiotic policies, when compared to primary care. A surveillance mechanism for antibiotic consumption was reported in 58% (104/178) of teaching hospitals and 62% (98/159) of regional hospitals. Antimicrobial resistance, patient needs, policy, peer influence and specialty level culture and practices were deemed important determinants for decision-making. Conclusion: Postgraduate training and support in antibiotic prescribing remains low amongst nurses and pharmacists. Whilst antibiotic policies and committees are established in most institutions, surveillance of antibiotic use is not. The impact of specialty level culture, and peer influence appears to be important factors of antibiotic prescribing. Keywords: Antibiotic stewardship, Education, Culture, Antibiotic prescribing Background secondary care are greater and more significant than in The threat of antimicrobial resistance is driving initiatives primary care. Patients in hospitals represent the frail, eld- across the one health care economy [1, 2]. Whilst it is a erly, very young, and very sick. There is an expectation on well-known fact that 80% of antibiotic prescribing for all healthcare providers, across the globe, to have put in humans occurs in primary care [3] the choice and route of place appropriate measures to tackle antimicrobial resist- antibiotic agents remains largely limited in that setting. ance as part of antibiotic stewardship programmes. This Though antibiotic use in secondary care comprises only expectation however, does not take into consideration the 20% of overall human antibiotic consumption, the risks cultural and contextual drivers at national, local and and unintended consequences of antibiotic use in organizational level. Nor does it consider the available re- sources and active stakeholders in potential stewardship * Correspondence: e.charani@imperial.ac.uk initiatives at the local level. NIHR Health Protection Research Unit in Healthcare Associated Infections To address the global challenges of implementing and Antimicrobial Resistance, Hammersmith Campus, Imperial College antibiotic stewardship, in 2015, an international group of London, W12 ONN London, England Full list of author information is available at the end of the article © The Author(s). 2019 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Charani et al. Antimicrobial Resistance and Infection Control (2019) 8:34 Page 2 of 6 researchers and clinicians developed a six-week Massive online. The survey was placed as an optional activity Open Online Course targeting a global audience [4]. The halfway through the week’s course material. The invitation MOOC was designed and developed by an international to participate included a study information sheet and group of researchers and healthcare professionals with learners were informed that completion of the survey was experience in the design and implementation of antibiotic not mandatory with learners having the option to choose stewardship programmes. The course was first launched to carry on with the week material without completing the in English as an online resource in 2015 (https://www.fu survey (available as supplementary material). All the data turelearn.com/courses/antimicrobial-stewardship). Since from the completed forms were automatically collated then it has been translated to Spanish, Russian and and extracted into an excel sheet. The data entry and Mandarin (2017) with several runs each year. The MOOC collection was anonymous and no learner identifier data has reached a global audience and the feedback so far was collected. suggests it was effective in engaging with participants on the topic of stewardship [4]. There are six modules spread Statistical analysis over 6 weeks of learning. Each week has 3 h of learning The descriptive data were analysed by institution type material which the learners could complete in their own and profession. For the statistical analysis, responses of time. Week five of the course is dedicated to ‘Behaviour ‘not applicable’ were combined with ‘no’ when analysing Change in Antibiotic Prescribing’ and was developed by the response to whether individuals had received post- EC and PD. The content of week five is based on the graduate training. The categorical variables were ana- social science research investigating how contextual lysed using chi-squared test. Cronbach’s alpha test was knowledge can be used to develop bespoke stewardship performed to test the co-efficient alpha for overall interventions in different settings [5]. This is particularly reliability of the Likert questions. The Likert questions important when considering the variation in resources, investigating the perceived determinants of antibiotic both financial and workforce across high, low, and middle prescribing were analysed using an ordinal regression income countries and how this affects stewardship [6]. model. All the determinants (including costs, patient Recognising the international reach of the MOOC, we de- needs, colleague recommendations, senior opinion, spe- signed a survey to be distributed amongst the learners of cialty level culture and practice and policy and guide- week five this course, during its first run. The survey lines) were fitted into the model to predict their aimed to investigate what stewardship activities existed in perceived influence on prescribing behaviours. The the organisations and countries which were represented p-values were considered as two-tailed and a p-value of by the learners. The survey also explored and what factors < 0.05 was set as significant. Wherever a p value of 0.000 influenced the learners’ own antibiotic prescribing was reported in the software, it was presented as < 0.01 decision-making. in the results. All analyses were conducted in SPSS 24 (IBM Corp., released 2016), and Microsoft Excel 2013 Methods (Microsoft). Data collection To investigate the existing stewardship activities, includ- Results ing education and training, in the participants’ organisa- The first run of the MOOC had 15,570 unique registra- tions and countries and to explore what influenced the tions. Of these 6839 individuals from 164 countries learners’ own antibiotic prescribing decision-making. a completed at least one of the six modules. In total, 920 survey questionnaire (available as supplementary mater- learners continued to, and completed week five. Of the ial) was developed using data from previous studies [7], week five learners, there were 505/920 (55%) survey re- and with input from healthcare professionals in India. In spondents from 53 countries. The top five countries with addition to basic demographic questions, the question- the highest frequency of survey responses comprise 65% naire asked for details of any existing stewardship (327) of the results, summarised in Table 1. The MOOC programmes in place in the home institution of the was, and remains “open source”, meaning any person, participants and any post-graduate training they might including members of the public can complete the have received to support their stewardship activities. course and this was reflected in the survey respondents. Additionally, participants were asked to rank their moti- Since we were primarily interested in the responses of vations for antibiotic prescribing. The key questions healthcare professionals (classified as nurses, doctors asked in the survey together with the results are pre- and pharmacists for the purpose of this study) any sented in the tables and figures in this paper. respondents outside of this classification were grouped The questionnaire was piloted with healthcare staff in together as other (104/505, 21%), Table 1. Students (27/ England. All learners participating in week five of the 104), and biomedical scientists and laboratory staff (20/ MOOC course were invited to complete the questionnaire 104) were the largest group in the other category, there Charani et al. Antimicrobial Resistance and Infection Control (2019) 8:34 Page 3 of 6 Table 1 The survey respondents by profession, the top five countries with most respondents presented in order Countries Respondents Profession n(%) Nurse Pharmacist Other n Doctor UK 208 60 (29) 55 (26) 40 (19) 53 (25) Australia 59 10 (17) 7 (12) 38 (64) 4 (7) India 24 18 (75) 0 (0) 1 (4) 5 (20) Ireland 21 3 (14) 3 (14) 10 (48) 6 (29) United States 15 2 (13) 0 (0) 3 (20) 10 (67) All other countries 178 89 (50) 24 (14) 38 (21) 26 (15) Total n (%) 505 182 (36) 89 (18) 130 (26) 104 (21) were also members of the public, dentists, veterinarians, The pattern of scoring to the Likert questions on and lecturers, as well as members of the public. perceived influences on antibiotic decision making were There were 337/505, (66%) respondents from hospi- similar across the professions. The highest mean scores tals, with 178/505 (35%) from a teaching hospital and on the Likert scale were for antimicrobial resistance, pol- 159/505 (31%) from a regional hospital (Table 2). Ten icy, patient needs and senior colleague recommendations percent (49/505) of the respondents were from primary as respondent perceived determinants on antibiotic pre- care. Doctors were significantly more likely to have re- scribing. When looking at the odds ratios of the mean ceived post-graduate training in infection management rankings for each variable reported to influence decision and antibiotic stewardship (56%, p < 0.01) compared with making, antimicrobial resistance, patient needs, policy, pharmacists (35%, p = 0.44), and nurses (43%, p = 0.06) and specialty level culture and practices were deemed (Table 3). Doctors (141/182, 77%) reported prescribing the most influential factors in this cohort (Fig. 1). Nurse antibiotics as part of their daily job, with 62% (113/182) recommendation, and cost were the least influential fac- reporting reviewing prescriptions of antibiotics. Doctors tors. When compared with the odds ratio for specialty also reported teaching about infection diagnosis and level culture and practices, antibiotic resistance, patient treatment (113/182, 62%), and developing antibiotic pol- needs, and policy were all significantly more influential icy and guidelines (85/182, 47%). A small number (19/ in decision making (p < 0.01). The opinion of colleagues, 130, 15% of pharmacists also reported prescribing antibi- pharmacist recommendation, and senior doctor recom- otics to be part of their daily practice. Amongst the mendation were ranked very closely in influence on spe- nurses 40% (36/89) reported that they review prescribed cialty level and practices (Fig. 1). To assess the internal antibiotic courses, 43% (38/89) reported teaching on the consistency of the Likert questions, a Cronbach’s alpha subject, and 18% (16/89) reported developing steward- test was performed, and a value of 0.744 was reported. ship related policy and guidelines, Table 3. This demonstrates a good co-efficient alpha for overall Hospitals (teaching and regional) were significantly reliability of the Likert questions. more likely to have an institutional antibiotic related policy or guidelines when compared to primary care (p Discussion = < 0.01), Table 4. Hospitals were more likely to have a This survey had a high (55%) response rate from the committee designated to stewardship (p < 0.01) (teach- participants of week five of the MOOC. Most of the ing hospitals 73% 130/178, 77% 123/159, regional survey respondents, however were from the UK and hospitals) when compared to primary care (33% 16/49). Australia, and five countries comprised 65% of the re- A surveillance mechanism for antibiotic consumption spondents. This may have been due to the MOOC being and prescribing was present in 58% (104/178) of teach- in English, and therefore not accessible to non-English ing hospitals and 62% (98/159) of regional hospitals. speakers, although, responses from the USA and Canada Table 2 All respondents by profession and institution Profession n (%) Teaching Hospital Regional Hospital Primary Care Other organisation Doctor 182 (36) 75 (41) 54 (30) 21 (12) 32 (18) Pharmacist 130 (26) 41 (31) 55 (42) 11 (8) 23 (18) Nurse 89 (18) 32 (36) 24 (27) 8 (9) 25 (28) Other 104 (13) 30 (25) 26 (35) 9 (8) 39 (22) Total 505 (100) 178 (35) 159 (31) 49 (10) 119 (24) Charani et al. Antimicrobial Resistance and Infection Control (2019) 8:34 Page 4 of 6 Table 3 Respondent post-graduate education and training and roles in antibiotic management by profession Profession Received Post graduate As part of your job do you do any of the following in relation to antibiotics? n training n (%) N(%) Yes No Odds Ratio (95% CI) Prescribe Administer Review Teach about infection Develop antibiotic diagnosis/treatment policy/guidelines Doctor 182 105 (58) 77 (42) Ref 141 (77) 35 (19) 112 (62) 113 (62) 85 (47) 0.39 (0.24–0.62) Pharmacist 130 45 (35) 85 (65) 19 (15) 10 (8) 117 (90) 58 (45) 74 (57) 0.59 (0.35–1.00) Nurse 89 38 (43) 51 (57) 14 (16) 42 (47) 36 (40) 38 (43) 16 (18) with English speaking populations, and with established of antibiotic prescriptions, and the existence of dedicated stewardship programmes in their healthcare system were committees to stewardship. The availability and report- low. It was encouraging to see participation from nurses ing of antibiotic consumption and surveillance reports and pharmacists, in addition to doctors, in this survey. however, remain low at 58% in teaching hospitals, and Though this course was targeted healthcare professionals 62% in regional hospitals, and 43% in primary care. In in hospitals, it attracted learners from primary care as general, stewardship activities were significantly more well as scientists, students and from other wider likely to be present in hospitals than in primary care. members of the population. This interest from the Since this is a survey with responses from 53 countries, non-healthcare professional workforce in an activity the results will reflect the heterogeneity of the partici- about antibiotic stewardship is a positive step in raising pants’ national healthcare systems. Education and train- awareness about the need to engage with the wider ing in infection management and antibiotic stewardship, population on the necessity to conserve antibiotics. at the postgraduate level, remains a resource primarily The participation of nurses and pharmacists in stew- available to doctors. This may be one of the reasons why ardship activities such as developing policy and guide- it is more difficult for other healthcare professionals to lines, and reviewing antibiotic prescriptions is a positive become involved and participate in stewardship activ- step to a broader inclusion of healthcare professionals, ities. Education and training in this field is not universal globally in stewardship efforts. Although pharmacist par- and requires further resources, particularly in healthcare ticipation in stewardship activities is the norm in some settings where traditionally doctors are still considered healthcare systems such as in USA, UK, Canada and to be the main decision makers and leaders in infection Australia, in many other parts of the world, stewardship management and antibiotic stewardship. remains the responsibility of doctors [8]. The reported When asked to rate the factors that influence anti- nurse involvement and participation is encouraging the biotic decision making, all three professions were con- see, though it has not been reported in other surveys sistent in their rankings of the key factors, namely: and studies. Involving the wider healthcare workforce in antimicrobial resistance, patient need, local policies. stewardship is a key gap that needs to be addressed [9, These determinants were closely followed by the influ- 10]. Whilst culturally, and historically, the expectation is ence of senior doctors, local culture and practices and that doctors lead decision making in the clinical setting, personal experience as key determinants of antibiotic the participants in this survey, representing 53 countries, decision making. This finding of the influence of senior demonstrate that other healthcare professionals can and doctors and specialty level and local culture is similar to do have a role to play in stewardship. findings from in-depth qualitative studies investigating The most common components of stewardship are re- the determinants of antibiotic decision-making [7, 11]. ported to be the use of policy and guidelines, the review To develop sustainable and effective interventions in Table 4 Antibiotic stewardship activities by institution Institution n Do you have antibiotic policy Are there specific committees/ Is there a reporting structure for or guideline in your organistion? groups dedicated to AMS? antibiotic use and prescribing? Yes n(%) No n(%) P Value Yes n(%) No n(%) P Value Yes n(%) No n(%) P Value Teaching Hospital 178 147 (83) 31 (17) < 0.01* 130 (73) 48 (27) < 0.01* 104 (58) 74(42) < 0.01* Regional Hospital 159 126 (79) 33 (21) 123 (77) 36 (23) 98 (62) 61(38) Primary Care 49 32 (65) 17 (35) 16 (33) 33 (67) 21 (43) 28 (57) Other 119 62 (52) 57 (48) 57 (48) 62 (52) 47 (39) 72 (61) Total 505 367 (73) 138 (27) 326 (65) 179 (35) 270 (53) 235 (47) Statistical significance calculated using Pearson Chi Squared test Charani et al. Antimicrobial Resistance and Infection Control (2019) 8:34 Page 5 of 6 Fig. 1 Figure presenting the trend in the odds ratios of respondents self-perceived determinants of antibiotic prescribing, relative to culture and practice at specialty level (set as 1) antibiotic stewardship it is important to recognise and key factors which influence the antibiotic decision-mak- address these cultural determinants to shape the out- ing of key healthcare professionals. Whilst antibiotic come of stewardship interventions. The general MOOC policies and committees are established in most institu- course participants were invited to respond to a tions, surveillance of antibiotic use is not universal. Post- post-course survey, to which 219/6839 participants graduate training and support in antibiotic prescribing responded. The findings of this survey have been pub- remains low amongst nurses and pharmacists. The im- lished, and report 95% (208/219) of learners rating the pact of specialty level culture, and peer influence appears course as good or excellent, with week five of the course to be significant factors of antibiotic decision-making. scoring most favourably with learners [4]. Furthermore, These data identify existing gaps in adequate training the discussion forum for week five of the MOOC pro- and education for staff involved in stewardship, and the vided ample feedback on the relevance and importance need for greater participation of nurses and pharmacists to of understanding the social and behavioural aspects of ensure effective and sustainable stewardship programmes. antibiotic prescribing. This feedback is available in the Abbreviations week five course content (https://www.futurelearn.com/ MOOC: Massive Open Online Course courses/antimicrobial-stewardship). Acknowledgements Limitations EC, ECS and AH acknowledge funding by Economic and Social Science Research Council (ESRC) as part of the Antimicrobial Cross Council initiative This survey was conducted across a group of individuals [ES/P008313/1] supported by the seven UK research councils, and the Global who had registered to participate in a course on anti- Challenges Research Fund and the National Institute for Health Research, UK biotic stewardship. There will have been inherent selec- Department of Health [HPRU-2012-10047] in partnership with Public Health England. tion bias in this group of respondents. The data is from 2015, and since then there has been further progress in Funding supporting antibiotic stewardship programmes both The MOOC was hosted on the FutureLearnVC platform and was supported internationally and nationally. by the British Society for Antimicrobial Chemotherapy (BSAC) through donated time and unrestricted educational grants secured by the BSAC under a consortia funding arrangement contributed to by five commercial Conclusions stakeholder partners (Alere, Bayer, Pfizer, MSD and Pharma AG). This study with participants representing 53 countries provides insights into the main components of antibiotic Availability of data and materials stewardship programmes in different countries and the All data analysed during this study are included in this published article. Charani et al. Antimicrobial Resistance and Infection Control (2019) 8:34 Page 6 of 6 Authors’ contributions EC, PD, DN and SB were course organisers for the MOOC. EC, PD, and ECS, AH, and SB contributed to the questionnaire development. EC and PD analysed the results of the survey. All authors contributed to the writing of the manuscript. All authors read and approved the final manuscript. Ethics approval and consent to participate Permission to complete this study was obtained from the joint research office of Imperial College London and University of Dundee. The opinion of both institutions was that this study did not require full ethical approval. The study information leaflet was presented to all participants. Electronic consent to participate in the study was provided by participants. Consent for publication Not applicable. Competing interests The authors declare that they have no competing interests. Publisher’sNote Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations. Author details NIHR Health Protection Research Unit in Healthcare Associated Infections and Antimicrobial Resistance, Hammersmith Campus, Imperial College London, W12 ONN London, England. British Society for Antimicrobial Chemotherapy, 53 Regent Place, Birmingham, England. University of Dundee, Medical School, Dundee, Scotland. Received: 19 October 2018 Accepted: 4 February 2019 References 1. O ‘neill J. Tackling drug-resistant infections globally: an overview of our work. London; 2016. 2. World Health Organization. The evolving threat of antimicrobial resistance: options for action. WHO Publ. 2014:1–119. 3. Health Protection Scotland and Information Services Division. Scottish antimicrobial use and resistance in humans in 2015; 2016. p. 1–33. 4. Sneddon J, Barlow G, Bradley S, Brink A, Chandy SJ, Nathwani D. Development and impact of a massive open online course (MOOC) for antimicrobial stewardship. J Antimicrob Chemother. 2018;73(4):1091–7. 5. Lorencatto F, Charani E, Sevdalis N, Tarrant C, Davey P. Driving sustainable change in antimicrobial prescribing practice: how can social and behavioural sciences help? J Antimicrob Chemother. 2018;(July):2613–24. 6. Pulcini C, Binda F, Lamkang AS, Trett A, Charani E, Goff DA, et al. Developing core elements and checklist items for global hospital antimicrobial stewardship programmes: a consensus approach. Clin Microbiol Infect. 2019;25(1):20–5. 7. Charani E, Castro-Sanchez E, Sevdalis N, Kyratsis Y, Drumright L, Shah N, et al. Understanding the determinants of antimicrobial prescribing within hospitals: the role of prescribing etiquette. Clin Infect Dis. 2013;57(2):188–96. 8. Charani E, Smith I, Skodvin B, Perozziello A, Lescure F-X, Lucet J-C, et al. Investigating the cultural and contextual determinants of antimicrobial stewardship programmes across low-, middle- and high-income countries – a qualitative study. PLoS One. 2019;14(1):e0209847. 9. Charani E, Holmes AH. Antimicrobial stewardship programmes: the need for wider engagement. BMJ Qual Saf. 2013 Nov;22(11):885–7. 10. Edwards R, Drumright LN, Kiernan M, Holmes A. Covering more territory to fight resistance: considering nurses’ role in antimicrobial stewardship. J Infect Prev. 2011;12(1):6–10. 11. Charani E, Ahmad R, Rawson T, Castro-Sanchez E, Tarrant C, Holmes A. The differences in antibiotic decision-making between acute surgical and acute medical teams – an ethnographic study of culture and team dynamics. Clin Infect Dis. 2018. https://doi.org/10.1093/cid/ciy844. Epub ahead of print. http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Antimicrobial Resistance & Infection Control Springer Journals

Implementation of antibiotic stewardship in different settings - results of an international survey

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Abstract

Background: Antibiotic stewardship interventions are being implemented across different healthcare settings. We report the findings of a global survey of healthcare professionals on the implementation of antibiotic stewardship programmes. Methods: Learners of a Massive Online Open Course (MOOC) on antibiotic stewardship were invited to complete an online survey on the core available organisational resources for stewardship. The categorical variables were analysed using chi-squared test, and Likert questions were analysed using an ordinal regression model. The p-values were considered as two-tailed. Significance was set at p-value of < 0.05. Results: The response rate was 55% (505/920), from 53 countries. The responders were 36% (182) doctors, 26% (130) pharmacists, 18% (89) nurses and 20% (104) other (researchers, students and members of the public). Post- graduate training in infection management and stewardship was reported by 56% of doctors compared with 43% (OR 0.59, 95%CI 0.35–1.00) nurses and 35% (OR 0.39, 95%CI 0.24–0.62) of pharmacists. Hospitals were significantly (83% in teaching hospitals, 79% in regional hospitals, p = < 0.01) more likely to have antibiotic policies, when compared to primary care. A surveillance mechanism for antibiotic consumption was reported in 58% (104/178) of teaching hospitals and 62% (98/159) of regional hospitals. Antimicrobial resistance, patient needs, policy, peer influence and specialty level culture and practices were deemed important determinants for decision-making. Conclusion: Postgraduate training and support in antibiotic prescribing remains low amongst nurses and pharmacists. Whilst antibiotic policies and committees are established in most institutions, surveillance of antibiotic use is not. The impact of specialty level culture, and peer influence appears to be important factors of antibiotic prescribing. Keywords: Antibiotic stewardship, Education, Culture, Antibiotic prescribing Background secondary care are greater and more significant than in The threat of antimicrobial resistance is driving initiatives primary care. Patients in hospitals represent the frail, eld- across the one health care economy [1, 2]. Whilst it is a erly, very young, and very sick. There is an expectation on well-known fact that 80% of antibiotic prescribing for all healthcare providers, across the globe, to have put in humans occurs in primary care [3] the choice and route of place appropriate measures to tackle antimicrobial resist- antibiotic agents remains largely limited in that setting. ance as part of antibiotic stewardship programmes. This Though antibiotic use in secondary care comprises only expectation however, does not take into consideration the 20% of overall human antibiotic consumption, the risks cultural and contextual drivers at national, local and and unintended consequences of antibiotic use in organizational level. Nor does it consider the available re- sources and active stakeholders in potential stewardship * Correspondence: e.charani@imperial.ac.uk initiatives at the local level. NIHR Health Protection Research Unit in Healthcare Associated Infections To address the global challenges of implementing and Antimicrobial Resistance, Hammersmith Campus, Imperial College antibiotic stewardship, in 2015, an international group of London, W12 ONN London, England Full list of author information is available at the end of the article © The Author(s). 2019 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Charani et al. Antimicrobial Resistance and Infection Control (2019) 8:34 Page 2 of 6 researchers and clinicians developed a six-week Massive online. The survey was placed as an optional activity Open Online Course targeting a global audience [4]. The halfway through the week’s course material. The invitation MOOC was designed and developed by an international to participate included a study information sheet and group of researchers and healthcare professionals with learners were informed that completion of the survey was experience in the design and implementation of antibiotic not mandatory with learners having the option to choose stewardship programmes. The course was first launched to carry on with the week material without completing the in English as an online resource in 2015 (https://www.fu survey (available as supplementary material). All the data turelearn.com/courses/antimicrobial-stewardship). Since from the completed forms were automatically collated then it has been translated to Spanish, Russian and and extracted into an excel sheet. The data entry and Mandarin (2017) with several runs each year. The MOOC collection was anonymous and no learner identifier data has reached a global audience and the feedback so far was collected. suggests it was effective in engaging with participants on the topic of stewardship [4]. There are six modules spread Statistical analysis over 6 weeks of learning. Each week has 3 h of learning The descriptive data were analysed by institution type material which the learners could complete in their own and profession. For the statistical analysis, responses of time. Week five of the course is dedicated to ‘Behaviour ‘not applicable’ were combined with ‘no’ when analysing Change in Antibiotic Prescribing’ and was developed by the response to whether individuals had received post- EC and PD. The content of week five is based on the graduate training. The categorical variables were ana- social science research investigating how contextual lysed using chi-squared test. Cronbach’s alpha test was knowledge can be used to develop bespoke stewardship performed to test the co-efficient alpha for overall interventions in different settings [5]. This is particularly reliability of the Likert questions. The Likert questions important when considering the variation in resources, investigating the perceived determinants of antibiotic both financial and workforce across high, low, and middle prescribing were analysed using an ordinal regression income countries and how this affects stewardship [6]. model. All the determinants (including costs, patient Recognising the international reach of the MOOC, we de- needs, colleague recommendations, senior opinion, spe- signed a survey to be distributed amongst the learners of cialty level culture and practice and policy and guide- week five this course, during its first run. The survey lines) were fitted into the model to predict their aimed to investigate what stewardship activities existed in perceived influence on prescribing behaviours. The the organisations and countries which were represented p-values were considered as two-tailed and a p-value of by the learners. The survey also explored and what factors < 0.05 was set as significant. Wherever a p value of 0.000 influenced the learners’ own antibiotic prescribing was reported in the software, it was presented as < 0.01 decision-making. in the results. All analyses were conducted in SPSS 24 (IBM Corp., released 2016), and Microsoft Excel 2013 Methods (Microsoft). Data collection To investigate the existing stewardship activities, includ- Results ing education and training, in the participants’ organisa- The first run of the MOOC had 15,570 unique registra- tions and countries and to explore what influenced the tions. Of these 6839 individuals from 164 countries learners’ own antibiotic prescribing decision-making. a completed at least one of the six modules. In total, 920 survey questionnaire (available as supplementary mater- learners continued to, and completed week five. Of the ial) was developed using data from previous studies [7], week five learners, there were 505/920 (55%) survey re- and with input from healthcare professionals in India. In spondents from 53 countries. The top five countries with addition to basic demographic questions, the question- the highest frequency of survey responses comprise 65% naire asked for details of any existing stewardship (327) of the results, summarised in Table 1. The MOOC programmes in place in the home institution of the was, and remains “open source”, meaning any person, participants and any post-graduate training they might including members of the public can complete the have received to support their stewardship activities. course and this was reflected in the survey respondents. Additionally, participants were asked to rank their moti- Since we were primarily interested in the responses of vations for antibiotic prescribing. The key questions healthcare professionals (classified as nurses, doctors asked in the survey together with the results are pre- and pharmacists for the purpose of this study) any sented in the tables and figures in this paper. respondents outside of this classification were grouped The questionnaire was piloted with healthcare staff in together as other (104/505, 21%), Table 1. Students (27/ England. All learners participating in week five of the 104), and biomedical scientists and laboratory staff (20/ MOOC course were invited to complete the questionnaire 104) were the largest group in the other category, there Charani et al. Antimicrobial Resistance and Infection Control (2019) 8:34 Page 3 of 6 Table 1 The survey respondents by profession, the top five countries with most respondents presented in order Countries Respondents Profession n(%) Nurse Pharmacist Other n Doctor UK 208 60 (29) 55 (26) 40 (19) 53 (25) Australia 59 10 (17) 7 (12) 38 (64) 4 (7) India 24 18 (75) 0 (0) 1 (4) 5 (20) Ireland 21 3 (14) 3 (14) 10 (48) 6 (29) United States 15 2 (13) 0 (0) 3 (20) 10 (67) All other countries 178 89 (50) 24 (14) 38 (21) 26 (15) Total n (%) 505 182 (36) 89 (18) 130 (26) 104 (21) were also members of the public, dentists, veterinarians, The pattern of scoring to the Likert questions on and lecturers, as well as members of the public. perceived influences on antibiotic decision making were There were 337/505, (66%) respondents from hospi- similar across the professions. The highest mean scores tals, with 178/505 (35%) from a teaching hospital and on the Likert scale were for antimicrobial resistance, pol- 159/505 (31%) from a regional hospital (Table 2). Ten icy, patient needs and senior colleague recommendations percent (49/505) of the respondents were from primary as respondent perceived determinants on antibiotic pre- care. Doctors were significantly more likely to have re- scribing. When looking at the odds ratios of the mean ceived post-graduate training in infection management rankings for each variable reported to influence decision and antibiotic stewardship (56%, p < 0.01) compared with making, antimicrobial resistance, patient needs, policy, pharmacists (35%, p = 0.44), and nurses (43%, p = 0.06) and specialty level culture and practices were deemed (Table 3). Doctors (141/182, 77%) reported prescribing the most influential factors in this cohort (Fig. 1). Nurse antibiotics as part of their daily job, with 62% (113/182) recommendation, and cost were the least influential fac- reporting reviewing prescriptions of antibiotics. Doctors tors. When compared with the odds ratio for specialty also reported teaching about infection diagnosis and level culture and practices, antibiotic resistance, patient treatment (113/182, 62%), and developing antibiotic pol- needs, and policy were all significantly more influential icy and guidelines (85/182, 47%). A small number (19/ in decision making (p < 0.01). The opinion of colleagues, 130, 15% of pharmacists also reported prescribing antibi- pharmacist recommendation, and senior doctor recom- otics to be part of their daily practice. Amongst the mendation were ranked very closely in influence on spe- nurses 40% (36/89) reported that they review prescribed cialty level and practices (Fig. 1). To assess the internal antibiotic courses, 43% (38/89) reported teaching on the consistency of the Likert questions, a Cronbach’s alpha subject, and 18% (16/89) reported developing steward- test was performed, and a value of 0.744 was reported. ship related policy and guidelines, Table 3. This demonstrates a good co-efficient alpha for overall Hospitals (teaching and regional) were significantly reliability of the Likert questions. more likely to have an institutional antibiotic related policy or guidelines when compared to primary care (p Discussion = < 0.01), Table 4. Hospitals were more likely to have a This survey had a high (55%) response rate from the committee designated to stewardship (p < 0.01) (teach- participants of week five of the MOOC. Most of the ing hospitals 73% 130/178, 77% 123/159, regional survey respondents, however were from the UK and hospitals) when compared to primary care (33% 16/49). Australia, and five countries comprised 65% of the re- A surveillance mechanism for antibiotic consumption spondents. This may have been due to the MOOC being and prescribing was present in 58% (104/178) of teach- in English, and therefore not accessible to non-English ing hospitals and 62% (98/159) of regional hospitals. speakers, although, responses from the USA and Canada Table 2 All respondents by profession and institution Profession n (%) Teaching Hospital Regional Hospital Primary Care Other organisation Doctor 182 (36) 75 (41) 54 (30) 21 (12) 32 (18) Pharmacist 130 (26) 41 (31) 55 (42) 11 (8) 23 (18) Nurse 89 (18) 32 (36) 24 (27) 8 (9) 25 (28) Other 104 (13) 30 (25) 26 (35) 9 (8) 39 (22) Total 505 (100) 178 (35) 159 (31) 49 (10) 119 (24) Charani et al. Antimicrobial Resistance and Infection Control (2019) 8:34 Page 4 of 6 Table 3 Respondent post-graduate education and training and roles in antibiotic management by profession Profession Received Post graduate As part of your job do you do any of the following in relation to antibiotics? n training n (%) N(%) Yes No Odds Ratio (95% CI) Prescribe Administer Review Teach about infection Develop antibiotic diagnosis/treatment policy/guidelines Doctor 182 105 (58) 77 (42) Ref 141 (77) 35 (19) 112 (62) 113 (62) 85 (47) 0.39 (0.24–0.62) Pharmacist 130 45 (35) 85 (65) 19 (15) 10 (8) 117 (90) 58 (45) 74 (57) 0.59 (0.35–1.00) Nurse 89 38 (43) 51 (57) 14 (16) 42 (47) 36 (40) 38 (43) 16 (18) with English speaking populations, and with established of antibiotic prescriptions, and the existence of dedicated stewardship programmes in their healthcare system were committees to stewardship. The availability and report- low. It was encouraging to see participation from nurses ing of antibiotic consumption and surveillance reports and pharmacists, in addition to doctors, in this survey. however, remain low at 58% in teaching hospitals, and Though this course was targeted healthcare professionals 62% in regional hospitals, and 43% in primary care. In in hospitals, it attracted learners from primary care as general, stewardship activities were significantly more well as scientists, students and from other wider likely to be present in hospitals than in primary care. members of the population. This interest from the Since this is a survey with responses from 53 countries, non-healthcare professional workforce in an activity the results will reflect the heterogeneity of the partici- about antibiotic stewardship is a positive step in raising pants’ national healthcare systems. Education and train- awareness about the need to engage with the wider ing in infection management and antibiotic stewardship, population on the necessity to conserve antibiotics. at the postgraduate level, remains a resource primarily The participation of nurses and pharmacists in stew- available to doctors. This may be one of the reasons why ardship activities such as developing policy and guide- it is more difficult for other healthcare professionals to lines, and reviewing antibiotic prescriptions is a positive become involved and participate in stewardship activ- step to a broader inclusion of healthcare professionals, ities. Education and training in this field is not universal globally in stewardship efforts. Although pharmacist par- and requires further resources, particularly in healthcare ticipation in stewardship activities is the norm in some settings where traditionally doctors are still considered healthcare systems such as in USA, UK, Canada and to be the main decision makers and leaders in infection Australia, in many other parts of the world, stewardship management and antibiotic stewardship. remains the responsibility of doctors [8]. The reported When asked to rate the factors that influence anti- nurse involvement and participation is encouraging the biotic decision making, all three professions were con- see, though it has not been reported in other surveys sistent in their rankings of the key factors, namely: and studies. Involving the wider healthcare workforce in antimicrobial resistance, patient need, local policies. stewardship is a key gap that needs to be addressed [9, These determinants were closely followed by the influ- 10]. Whilst culturally, and historically, the expectation is ence of senior doctors, local culture and practices and that doctors lead decision making in the clinical setting, personal experience as key determinants of antibiotic the participants in this survey, representing 53 countries, decision making. This finding of the influence of senior demonstrate that other healthcare professionals can and doctors and specialty level and local culture is similar to do have a role to play in stewardship. findings from in-depth qualitative studies investigating The most common components of stewardship are re- the determinants of antibiotic decision-making [7, 11]. ported to be the use of policy and guidelines, the review To develop sustainable and effective interventions in Table 4 Antibiotic stewardship activities by institution Institution n Do you have antibiotic policy Are there specific committees/ Is there a reporting structure for or guideline in your organistion? groups dedicated to AMS? antibiotic use and prescribing? Yes n(%) No n(%) P Value Yes n(%) No n(%) P Value Yes n(%) No n(%) P Value Teaching Hospital 178 147 (83) 31 (17) < 0.01* 130 (73) 48 (27) < 0.01* 104 (58) 74(42) < 0.01* Regional Hospital 159 126 (79) 33 (21) 123 (77) 36 (23) 98 (62) 61(38) Primary Care 49 32 (65) 17 (35) 16 (33) 33 (67) 21 (43) 28 (57) Other 119 62 (52) 57 (48) 57 (48) 62 (52) 47 (39) 72 (61) Total 505 367 (73) 138 (27) 326 (65) 179 (35) 270 (53) 235 (47) Statistical significance calculated using Pearson Chi Squared test Charani et al. Antimicrobial Resistance and Infection Control (2019) 8:34 Page 5 of 6 Fig. 1 Figure presenting the trend in the odds ratios of respondents self-perceived determinants of antibiotic prescribing, relative to culture and practice at specialty level (set as 1) antibiotic stewardship it is important to recognise and key factors which influence the antibiotic decision-mak- address these cultural determinants to shape the out- ing of key healthcare professionals. Whilst antibiotic come of stewardship interventions. The general MOOC policies and committees are established in most institu- course participants were invited to respond to a tions, surveillance of antibiotic use is not universal. Post- post-course survey, to which 219/6839 participants graduate training and support in antibiotic prescribing responded. The findings of this survey have been pub- remains low amongst nurses and pharmacists. The im- lished, and report 95% (208/219) of learners rating the pact of specialty level culture, and peer influence appears course as good or excellent, with week five of the course to be significant factors of antibiotic decision-making. scoring most favourably with learners [4]. Furthermore, These data identify existing gaps in adequate training the discussion forum for week five of the MOOC pro- and education for staff involved in stewardship, and the vided ample feedback on the relevance and importance need for greater participation of nurses and pharmacists to of understanding the social and behavioural aspects of ensure effective and sustainable stewardship programmes. antibiotic prescribing. This feedback is available in the Abbreviations week five course content (https://www.futurelearn.com/ MOOC: Massive Open Online Course courses/antimicrobial-stewardship). Acknowledgements Limitations EC, ECS and AH acknowledge funding by Economic and Social Science Research Council (ESRC) as part of the Antimicrobial Cross Council initiative This survey was conducted across a group of individuals [ES/P008313/1] supported by the seven UK research councils, and the Global who had registered to participate in a course on anti- Challenges Research Fund and the National Institute for Health Research, UK biotic stewardship. There will have been inherent selec- Department of Health [HPRU-2012-10047] in partnership with Public Health England. tion bias in this group of respondents. The data is from 2015, and since then there has been further progress in Funding supporting antibiotic stewardship programmes both The MOOC was hosted on the FutureLearnVC platform and was supported internationally and nationally. by the British Society for Antimicrobial Chemotherapy (BSAC) through donated time and unrestricted educational grants secured by the BSAC under a consortia funding arrangement contributed to by five commercial Conclusions stakeholder partners (Alere, Bayer, Pfizer, MSD and Pharma AG). This study with participants representing 53 countries provides insights into the main components of antibiotic Availability of data and materials stewardship programmes in different countries and the All data analysed during this study are included in this published article. Charani et al. Antimicrobial Resistance and Infection Control (2019) 8:34 Page 6 of 6 Authors’ contributions EC, PD, DN and SB were course organisers for the MOOC. EC, PD, and ECS, AH, and SB contributed to the questionnaire development. EC and PD analysed the results of the survey. All authors contributed to the writing of the manuscript. All authors read and approved the final manuscript. Ethics approval and consent to participate Permission to complete this study was obtained from the joint research office of Imperial College London and University of Dundee. The opinion of both institutions was that this study did not require full ethical approval. The study information leaflet was presented to all participants. Electronic consent to participate in the study was provided by participants. Consent for publication Not applicable. Competing interests The authors declare that they have no competing interests. Publisher’sNote Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations. Author details NIHR Health Protection Research Unit in Healthcare Associated Infections and Antimicrobial Resistance, Hammersmith Campus, Imperial College London, W12 ONN London, England. British Society for Antimicrobial Chemotherapy, 53 Regent Place, Birmingham, England. University of Dundee, Medical School, Dundee, Scotland. Received: 19 October 2018 Accepted: 4 February 2019 References 1. O ‘neill J. Tackling drug-resistant infections globally: an overview of our work. London; 2016. 2. World Health Organization. The evolving threat of antimicrobial resistance: options for action. WHO Publ. 2014:1–119. 3. Health Protection Scotland and Information Services Division. Scottish antimicrobial use and resistance in humans in 2015; 2016. p. 1–33. 4. Sneddon J, Barlow G, Bradley S, Brink A, Chandy SJ, Nathwani D. Development and impact of a massive open online course (MOOC) for antimicrobial stewardship. J Antimicrob Chemother. 2018;73(4):1091–7. 5. Lorencatto F, Charani E, Sevdalis N, Tarrant C, Davey P. Driving sustainable change in antimicrobial prescribing practice: how can social and behavioural sciences help? J Antimicrob Chemother. 2018;(July):2613–24. 6. Pulcini C, Binda F, Lamkang AS, Trett A, Charani E, Goff DA, et al. Developing core elements and checklist items for global hospital antimicrobial stewardship programmes: a consensus approach. Clin Microbiol Infect. 2019;25(1):20–5. 7. Charani E, Castro-Sanchez E, Sevdalis N, Kyratsis Y, Drumright L, Shah N, et al. Understanding the determinants of antimicrobial prescribing within hospitals: the role of prescribing etiquette. Clin Infect Dis. 2013;57(2):188–96. 8. Charani E, Smith I, Skodvin B, Perozziello A, Lescure F-X, Lucet J-C, et al. Investigating the cultural and contextual determinants of antimicrobial stewardship programmes across low-, middle- and high-income countries – a qualitative study. PLoS One. 2019;14(1):e0209847. 9. Charani E, Holmes AH. Antimicrobial stewardship programmes: the need for wider engagement. BMJ Qual Saf. 2013 Nov;22(11):885–7. 10. Edwards R, Drumright LN, Kiernan M, Holmes A. Covering more territory to fight resistance: considering nurses’ role in antimicrobial stewardship. J Infect Prev. 2011;12(1):6–10. 11. Charani E, Ahmad R, Rawson T, Castro-Sanchez E, Tarrant C, Holmes A. The differences in antibiotic decision-making between acute surgical and acute medical teams – an ethnographic study of culture and team dynamics. Clin Infect Dis. 2018. https://doi.org/10.1093/cid/ciy844. Epub ahead of print.

Journal

Antimicrobial Resistance & Infection Control – Springer Journals

Published: Dec 1, 2019

Keywords: medical microbiology; drug resistance; infectious diseases

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