Journal of Antimicrobial Chemotherapy Advance Access published November 4, 2013
J Antimicrob Chemother doi:10.1093/jac/dkt440
European medical students: a first multicentre study of knowledge, attitudes and perceptions of antibiotic prescribing and antibiotic resistance Oliver J. Dyar1, Ce´line Pulcini2,3*, Philip Howard4 and Dilip Nathwani5 on behalf of ESGAP† (the ESCMID Study Group for Antibiotic Policies) 1
*Corresponding author. Centre Hospitalier Universitaire de Nice, Service d’Infectiologie, Hoˆpital l’Archet 1, Route Saint Antoine de Ginestie`re, BP 3079, 06202 Nice cedex 3, France. Tel: +33-4-92-03-55-15; Fax: +33-4-93-96-54-54; E-mail: [email protected] †Members are listed in the Acknowledgements section.
Received 14 August 2013; returned 9 September 2013; revised 7 October 2013; accepted 9 October 2013 Objectives: To learn about medical students’ knowledge of and perspectives on antibiotic prescribing and resistance, with the aim of helping to develop educational programmes. Methods: Final-year students at seven European medical schools were invited to participate in an online survey in 2012. Results: The response rate was 35% (338/961). Most students (74%) wanted more education on choosing antibiotic treatments. Students at all schools felt most confident in diagnosing an infection and least confident in choosing combination therapies, choosing the correct dose and interval of administration and not prescribing in cases of diagnostic uncertainty. Students felt that too many prescriptions and too much broad-spectrum antibiotic use were the most important contributors to resistance; some (24%) believed poor hand hygiene was not at all important. Most students (92%) believed that resistance is a national problem. Most (66%) felt that the antibiotics they would prescribe would contribute to resistance, and almost all (98%) felt that resistance would be a greater problem in the future. Most students (83%) incorrectly thought that rates of methicillin-resistant Staphylococcus aureus (MRSA) bacteraemia had significantly increased over the past decade in their countries. There was little appreciation of the relative burden of resistance in Europe compared with road traffic accidents (around two to three times greater mortality) and lung cancer (around 10 times greater mortality). Conclusions: Students wanted further education on antibiotic prescribing, and areas of lack of confidence were found. Students overestimated the current burden of resistant bacteria and were unaware of successes in reducing MRSA infections. Educational and stewardship programmes may benefit from including more cases of diagnostic uncertainty, and highlighting successes such as MRSA prevention, as evidence for the importance of current interventions. Keywords: education, antibiotic stewardship, survey, questionnaire, attitudes to health
Introduction The WHO recently highlighted the importance of undergraduate training in prudent prescribing.1 To date, there has been little investigation of students’ attitudes towards antibiotic prescribing, and even less of their knowledge and perceptions of antibiotic resistance, recognized by the WHO as one of the three greatest threats to human health; a few small, mostly single-centre studies have
found gaps in prescribing knowledge and a desire for further education.2 – 6 Our intention was to study the knowledge, attitudes and perceptions of final-year medical students across European medical schools to antibiotic prescribing and bacterial resistance. Our goal was to develop an understanding sufficient to form a foundation for more effective education in antibiotic stewardship for undergraduates.
# The Author 2013. Published by Oxford University Press on behalf of the British Society for Antimicrobial Chemotherapy. All rights reserved. For Permissions, please e-mail: [email protected]
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Downloaded from http://jac.oxfordjournals.org/ at Belgorod State University on November 9, 2013
Medical Sciences Department, Oxford University, Oxford, UK; 2Service d’Infectiologie, CHU de Nice, Nice, France; 3Faculte´ de Me´decine, Universite´ Nice-Sophia Antipolis, Nice, France; 4Pharmacy, Leeds Teaching Hospitals NHS Trust, Leeds, UK; 5Infection Unit, Ninewells Hospital and Medical School, Dundee, UK
Dyar et al.
Methods
Results Out of 961 eligible medical students, 338 (35%) responded to all or part of the survey. The average response rate at each medical school was 29%, ranging from 18% (Nice, 26/148) to 53% (Dundee, 91/172).
Perceptions of antibiotic prescribing Across all medical schools, students were consistently most confident in making an accurate diagnosis of infection/sepsis and
Knowledge that may shape perceptions of antimicrobial resistance Most students (92%, n¼ 265) felt that antibiotic resistance was a national problem, with 79% feeling it was a problem in their own hospital. The majority of students (83%, n¼ 265) stated that methicillinresistant Staphylococcus aureus (MRSA) was responsible for a greater proportion of S. aureus bacteraemias in their country today than 10 years ago. Most students at all medical schools (except for Nice) believed that MRSA had accounted for fewer than 5% of all S. aureus bacteraemias in their country 10 years ago. The majority of students (65%) thought that over 1% of S. aureus bacteraemias were caused by vancomycin-resistant bacteria in their country, and most students (59%) believed that over
Making an accurate diagnosis of infection/sepsis Interpreting microbiological results Choosing between intravenous and oral administration Choosing the correct antibiotic Planning to streamline/stop the antibiotic treatment according to clinical evaluation and investigations Planning the duration of the antibiotic treatment Deciding not to prescribe an antibiotic if the patient has fever, but no severity criteria, and if you are not sure about your diagnosis Choosing the correct dose and interval of administration Using a combination therapy if appropriate 0% Confident or very confident
20%
40%
60%
80%
100%
Unconfident or unsure
Figure 1. Confidence in different areas of antibiotic prescribing (n¼286). Whiskers indicate the range between medical schools of ‘confident and very confident’ responses.
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Downloaded from http://jac.oxfordjournals.org/ at Belgorod State University on November 9, 2013
We conducted a cross-sectional survey of all final-year students at seven European medical schools (Dundee, Scotland; Geneva, Switzerland; Linkoping, Sweden; Ljubljana, Slovenia; Madrid, Spain; Nice, France; Oxford, England). These schools were selected due to individual staff connections with ESGAP (the ESCMID Study Group for Antibiotic Policies). We developed the questionnaire after a literature review of comparable studies,2 – 5,7 – 9 and in consultation with infectious diseases experts. Ten students at two medical schools participated in pilot testing. The 41-point self-administered survey was Internet based (using www. surveymonkey.com). Students received an e-mail from their course administrator (or infectious diseases educational lead) inviting them to participate in the survey. Further e-mail reminders were sent 2 and 4 weeks after the initial message. The survey was available from June to August 2012. Participation was voluntary, anonymous and without compensation. Responses were single answer, multiple response and scaled. The survey is available as Supplementary data at JAC Online. The survey results were analysed using Microsoft Excel 2010 (Microsoft Inc., Redmond, WA, USA). Percentages were calculated for the categorical data, with scaled items analysed both as multilevel responses and collapsed into dichotomous variables where appropriate.
interpreting microbiological results (Figure 1). Students were least confident in deciding to use combination therapy, choosing the correct dose and interval of antibiotics, and deciding not to prescribe an antibiotic if the patient had fever alone or there was uncertainty in the diagnosis. These areas also showed the greatest variation between medical schools. The majority of students at six out of the seven medical schools stated that they would like more training on antibiotic selection, ranging from 67% (Linkoping, 10/15) to 92% (Ljubljana, 56/61); at Oxford, 43% of students (20/47) did not want further education, and 19% were unsure. Students believed that an average of 30% of antibiotic usage was unnecessary or inappropriate, with means ranging from 22% (Ljubljana) to 38% (Geneva). Most students [83%, total responses (n)¼ 279] at all medical schools felt prescribing inappropriate or unnecessary antibiotics to be professionally unethical.
JAC
Antibiotic prescribing and resistance: a student survey
Too many antibiotic prescriptions
Too many broad-spectrum antibiotics used
Excessive use of antibiotics in livestock
Dosings of antibiotics are too low Not removing the focus of infection (e.g. medical devices or catheters)
Poor hand hygiene Paying too much attention to pharmaceutical representatives/advertising 0% Not at all important
Slightly important
20%
40%
60%
80%
100%
Moderately or very important
Figure 2. Perceptions of the importance of potential contributors to antibiotic resistance (n¼256). Whiskers indicate the range between medical schools of ‘moderately or very important’ responses.
1% of all bacterial infections in Europe (excluding tuberculosis) were resistant to all known antibiotics. Students consistently believed that the most important contributors to resistance were the use of too many antibiotic prescriptions and broad-spectrum antibiotics, and the least important contributors were poor hand hygiene and paying too much attention to pharmaceutical representatives/advertising (Figure 2). Most students (60%, n¼ 248) believed that more antibiotic classes became available during the period 1980–2011 than will become available during the period 2011 –2020, with 89% of students believing that at least one new class of antibiotic would become available between 2011 and 2020.
Perceptions of bacterial resistance Resistant bacteria are thought to cause 25 000 deaths per year across Europe;10 road traffic accidents (RTAs) and lung cancer are responsible for around 2– 3 and 10 times as many deaths, respectively.11 Few students (9%, n¼ 243) were able to state the correct order of disease burden caused by RTAs, lung cancer and resistant bacteria, with only 1% of students stating the relative magnitude of burden correctly. Many students (51%) believed that resistant bacteria caused a similar or higher number of deaths than lung cancer. Most students [66%, n¼ 250 (ranging from 41% in Ljubljana to 91% in Geneva)] felt that the antibiotics they would prescribe as doctors would contribute to the problem of antibiotic resistance, and almost all students (98%) believed that antibiotic resistance would become a greater clinical problem during their career.
Discussion In all but one medical school, the majority of students wanted further education on antibiotic prescribing. This fits with previous studies of students and doctors.2,6,7 We have identified areas of self-reported confidence and lack of confidence in prescribing, which are broadly consistent across all medical schools and are similar to a recent study of US students.6 Most students (92%) felt confident in making an accurate diagnosis of infection; as misdiagnosis has been found to be a leading cause of unnecessary antibiotic use,12 it may be useful for educational programmes to address possible overconfidence in students and doctors alike. The situations in which antibiotic education is currently addressed may lack some of the complexities of ‘real-world’ clinical decisionmaking. Vignette-based clinical scenario teaching with feedback has been found to be an effective method of promoting learning related to such complexities.13 We must also teach students how to communicate with patients in situations of diagnostic uncertainty, to reduce the number of unnecessary prescriptions.14 Students are aware that a significant proportion of antibiotic prescribing is inappropriate, and the majority believe such use is professionally unethical; a greater proportion (83%) felt this prescribing to be unethical compared with a survey of US doctors (62%).7 As most students believe that their prescribing will contribute to the problem of antibiotic resistance, the link between inappropriate prescribing and ethical responsibility could be a further way to engage students in stewardship efforts. Students consistently over-rated the prevalence of resistant bacteria, with the majority believing that pan-resistant bacteria and vancomycin-resistant S. aureus are responsible for more than 1%
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Downloaded from http://jac.oxfordjournals.org/ at Belgorod State University on November 9, 2013
Too long durations of antibiotic treatment
Dyar et al.
Acknowledgements This work was presented as a poster at the 2013 ECCMID (European Congress of Clinical Microbiology and Infectious Diseases) (Abstract P887) and as an oral presentation at the 2013 ICPIC (International Consortium for Prevention and Infection Control) conference (Abstract O051). We thank all the students who responded to our survey. We are additionally grateful for the support we received in organizing survey distribution at each centre, in particular to Stephan Harbarth (Geneva), Ha˚kan Hanberger (Linkoping), Bojana Beovic´ (Ljubljana) and Jose´ Ramo´n Pan˜o Pardo (Madrid).
ESGAP members The ESGAP executive committee includes Dilip Nathwani, Bojana Beovic, Ce´line Pulcini, Stephan Harbarth, Ha˚kan Hanberger, Leonardo Pagani, Jose´ Ramo´n Pan˜o Pardo, Philip Howard and Agnes Weschesler-Fo¨rdo¨s.
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Funding This study was carried out as part of our routine work.
Transparency declarations None to declare.
Author contributions O. J. D. developed the idea for the study in collaboration with D. N. O. J. D., C. P., P. H. and D. N. participated in the design of the study and in revising the paper critically for substantial intellectual content. O. J. D. was responsible for data collection and analysis, and drafted the manuscript. All authors read and approved the final manuscript.
Supplementary data The questionnaire is available as Supplementary data at JAC Online (http:// jac.oxfordjournals.org/).
References 1 WHO. The Evolving Threat of Antimicrobial Resistance: Options for Action. 2012. http://whqlibdoc.who.int/publications/2012/9789241503181_eng. pdf (14 August 2013, date last accessed). 2 Minen MT, Duquaine D, Marx MA et al. A survey of knowledge, attitudes, and beliefs of medical students concerning antimicrobial use and resistance. Microb Drug Resist 2010; 16: 285– 9. 3 Ibia E, Sheridan M, Schwartz R et al. Knowledge of the principles of judicious antibiotic use for upper respiratory infections: a survey of senior medical students. South Med J 2005; 98: 889–95. 4 Wright EP, Jain P. Survey of antibiotic knowledge amongst final year medical students. J Antimicrob Chemother 2004; 53: 550– 1. 5 Humphreys H, Dillane T, O’Connell B et al. Survey of recent medical graduates’ knowledge and understanding of the treatment and prevention of infection. Ir Med J 2006; 99: 58– 9. 6 Abbo L, Cosgrove S, Pottinger P et al. Medical students’ perceptions and knowledge about antimicrobial stewardship: how are we educating our future prescribers? Clin Infect Dis 2013; 57: 631–8. 7 Abbo L, Sinkowitz-Cochran R, Smith L et al. Faculty and resident physicians’ attitudes, perceptions, and knowledge about antimicrobial use and resistance. Infect Control Hosp Epidemiol 2011; 32: 714–8. 8 Ziglam HM, Morales D, Webb K et al. Knowledge about sepsis among training-grade doctors. J Antimicrob Chemother 2006; 57: 963–5. 9 Pulcini C, Williams F, Molinari N et al. Junior doctors’ knowledge and perceptions of antibiotic resistance and prescribing: a survey in France and Scotland. Clin Microbiol Infect 2011; 17: 80– 7. 10 ECDC/EMEA Joint Technical Report. The Bacterial Challenge: Time to React. 2009. http://www.ecdc.europa.eu/en/publications/Publications/0909_TER_ The_Bacterial_Challenge_Time_to_React.pdf (14 August 2013, date last accessed). 11 WHO. Global Burden of Disease: Cause Specific Mortality Regional Estimates for 2000–2011. http://www.who.int/healthinfo/global_burden_ disease/estimates_regional/en/index.html (14 August 2013, date last accessed).
Downloaded from http://jac.oxfordjournals.org/ at Belgorod State University on November 9, 2013
of infections in Europe. Furthermore, students grossly overestimated the relative burden of disease caused by resistant bacteria, with most suggesting it was similar to or higher than that of lung cancer (which is, in reality, responsible for 10 times as many deaths). These findings suggest that students currently lack a context for antibiotic resistance; moreover, gradual increases in the burden of resistance may go unnoticed as these students progress in their careers, since their initial expectations have been set too high. Over 80% of students felt that MRSAwas responsible for a greater proportion of S. aureus bacteraemias in their country today than 10 years ago. This perception is likely to have been influenced by exaggerated popular media coverage and the political focus placed on MRSA, but may also reflect a lack of understanding of the success of efforts to reduce MRSA infections, which have actually decreased or remained stable in the countries of the students surveyed here. Students were broadly aware of contributors to resistance, but a quarter of students felt that handwashing was not at all important. Highlighting the successes of antibiotic stewardship programmes may be an important way to help future doctors recognize that actions they take individually can collectively lead to important results. This study has several limitations: (i) the response rate of 35% is low, but comparable to the study by Minen et al.2 (30%); (ii) the participating medical schools had leads with an interest in antimicrobial stewardship, who may affect the culture of antibiotic prescribing present in their hospitals, and interested students were more likely to respond; and (iii) we are not sure of the diversity of the structure, content and learning pedagogy of the medical schools included, all of which may influence the responses. However, the responses were consistent across medical schools for most questions, indicating a degree of external validity. In conclusion, we have found that most students want further education on antibiotics at medical school, and that such courses may be of most benefit if they can address feelings of unconfidence, particularly in relation to combination therapy and dose selection. Articulating more clearly when not to prescribe and how long to prescribe for with pragmatic examples is likely to be useful and address potential overconfidence. These and other factors will help to develop more targeted educational material to address currently unmet needs. Larger studies with more robust methodology are required to further understand key educational interventions to support learning about antibiotic stewardship.
Antibiotic prescribing and resistance: a student survey
JAC
12 Pulcini C, Cua E, Lieutier Fet al. Antibiotic misuse: a prospective clinical audit in a French university hospital. Eur J Clin Microbiol Infect Dis 2007; 26: 277–80.
http://www.pause-online.org.uk/?q=taxonomy/term/29 (14 August 2013, date last accessed).
13 Prudent Antibiotic User. Standardized Teaching Materials for Prudent Antimicrobial Prescribing for Use in the Undergraduate Medical Curriculum.
14 Pulcini C, Gyssens IC. How to educate prescribers in antimicrobial stewardship practices. Virulence 2013; 4: 192– 202.
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J Antimicrob Chemother doi:10.1093/jac/dkt440
European medical students: a first multicentre study of knowledge, attitudes and perceptions of antibiotic prescribing and antibiotic resistance Oliver J. Dyar1, Ce´line Pulcini2,3*, Philip Howard4 and Dilip Nathwani5 on behalf of ESGAP† (the ESCMID Study Group for Antibiotic Policies) 1
*Corresponding author. Centre Hospitalier Universitaire de Nice, Service d’Infectiologie, Hoˆpital l’Archet 1, Route Saint Antoine de Ginestie`re, BP 3079, 06202 Nice cedex 3, France. Tel: +33-4-92-03-55-15; Fax: +33-4-93-96-54-54; E-mail: [email protected] †Members are listed in the Acknowledgements section.
Received 14 August 2013; returned 9 September 2013; revised 7 October 2013; accepted 9 October 2013 Objectives: To learn about medical students’ knowledge of and perspectives on antibiotic prescribing and resistance, with the aim of helping to develop educational programmes. Methods: Final-year students at seven European medical schools were invited to participate in an online survey in 2012. Results: The response rate was 35% (338/961). Most students (74%) wanted more education on choosing antibiotic treatments. Students at all schools felt most confident in diagnosing an infection and least confident in choosing combination therapies, choosing the correct dose and interval of administration and not prescribing in cases of diagnostic uncertainty. Students felt that too many prescriptions and too much broad-spectrum antibiotic use were the most important contributors to resistance; some (24%) believed poor hand hygiene was not at all important. Most students (92%) believed that resistance is a national problem. Most (66%) felt that the antibiotics they would prescribe would contribute to resistance, and almost all (98%) felt that resistance would be a greater problem in the future. Most students (83%) incorrectly thought that rates of methicillin-resistant Staphylococcus aureus (MRSA) bacteraemia had significantly increased over the past decade in their countries. There was little appreciation of the relative burden of resistance in Europe compared with road traffic accidents (around two to three times greater mortality) and lung cancer (around 10 times greater mortality). Conclusions: Students wanted further education on antibiotic prescribing, and areas of lack of confidence were found. Students overestimated the current burden of resistant bacteria and were unaware of successes in reducing MRSA infections. Educational and stewardship programmes may benefit from including more cases of diagnostic uncertainty, and highlighting successes such as MRSA prevention, as evidence for the importance of current interventions. Keywords: education, antibiotic stewardship, survey, questionnaire, attitudes to health
Introduction The WHO recently highlighted the importance of undergraduate training in prudent prescribing.1 To date, there has been little investigation of students’ attitudes towards antibiotic prescribing, and even less of their knowledge and perceptions of antibiotic resistance, recognized by the WHO as one of the three greatest threats to human health; a few small, mostly single-centre studies have
found gaps in prescribing knowledge and a desire for further education.2 – 6 Our intention was to study the knowledge, attitudes and perceptions of final-year medical students across European medical schools to antibiotic prescribing and bacterial resistance. Our goal was to develop an understanding sufficient to form a foundation for more effective education in antibiotic stewardship for undergraduates.
# The Author 2013. Published by Oxford University Press on behalf of the British Society for Antimicrobial Chemotherapy. All rights reserved. For Permissions, please e-mail: [email protected]
1 of 5
Downloaded from http://jac.oxfordjournals.org/ at Belgorod State University on November 9, 2013
Medical Sciences Department, Oxford University, Oxford, UK; 2Service d’Infectiologie, CHU de Nice, Nice, France; 3Faculte´ de Me´decine, Universite´ Nice-Sophia Antipolis, Nice, France; 4Pharmacy, Leeds Teaching Hospitals NHS Trust, Leeds, UK; 5Infection Unit, Ninewells Hospital and Medical School, Dundee, UK
Dyar et al.
Methods
Results Out of 961 eligible medical students, 338 (35%) responded to all or part of the survey. The average response rate at each medical school was 29%, ranging from 18% (Nice, 26/148) to 53% (Dundee, 91/172).
Perceptions of antibiotic prescribing Across all medical schools, students were consistently most confident in making an accurate diagnosis of infection/sepsis and
Knowledge that may shape perceptions of antimicrobial resistance Most students (92%, n¼ 265) felt that antibiotic resistance was a national problem, with 79% feeling it was a problem in their own hospital. The majority of students (83%, n¼ 265) stated that methicillinresistant Staphylococcus aureus (MRSA) was responsible for a greater proportion of S. aureus bacteraemias in their country today than 10 years ago. Most students at all medical schools (except for Nice) believed that MRSA had accounted for fewer than 5% of all S. aureus bacteraemias in their country 10 years ago. The majority of students (65%) thought that over 1% of S. aureus bacteraemias were caused by vancomycin-resistant bacteria in their country, and most students (59%) believed that over
Making an accurate diagnosis of infection/sepsis Interpreting microbiological results Choosing between intravenous and oral administration Choosing the correct antibiotic Planning to streamline/stop the antibiotic treatment according to clinical evaluation and investigations Planning the duration of the antibiotic treatment Deciding not to prescribe an antibiotic if the patient has fever, but no severity criteria, and if you are not sure about your diagnosis Choosing the correct dose and interval of administration Using a combination therapy if appropriate 0% Confident or very confident
20%
40%
60%
80%
100%
Unconfident or unsure
Figure 1. Confidence in different areas of antibiotic prescribing (n¼286). Whiskers indicate the range between medical schools of ‘confident and very confident’ responses.
2 of 5
Downloaded from http://jac.oxfordjournals.org/ at Belgorod State University on November 9, 2013
We conducted a cross-sectional survey of all final-year students at seven European medical schools (Dundee, Scotland; Geneva, Switzerland; Linkoping, Sweden; Ljubljana, Slovenia; Madrid, Spain; Nice, France; Oxford, England). These schools were selected due to individual staff connections with ESGAP (the ESCMID Study Group for Antibiotic Policies). We developed the questionnaire after a literature review of comparable studies,2 – 5,7 – 9 and in consultation with infectious diseases experts. Ten students at two medical schools participated in pilot testing. The 41-point self-administered survey was Internet based (using www. surveymonkey.com). Students received an e-mail from their course administrator (or infectious diseases educational lead) inviting them to participate in the survey. Further e-mail reminders were sent 2 and 4 weeks after the initial message. The survey was available from June to August 2012. Participation was voluntary, anonymous and without compensation. Responses were single answer, multiple response and scaled. The survey is available as Supplementary data at JAC Online. The survey results were analysed using Microsoft Excel 2010 (Microsoft Inc., Redmond, WA, USA). Percentages were calculated for the categorical data, with scaled items analysed both as multilevel responses and collapsed into dichotomous variables where appropriate.
interpreting microbiological results (Figure 1). Students were least confident in deciding to use combination therapy, choosing the correct dose and interval of antibiotics, and deciding not to prescribe an antibiotic if the patient had fever alone or there was uncertainty in the diagnosis. These areas also showed the greatest variation between medical schools. The majority of students at six out of the seven medical schools stated that they would like more training on antibiotic selection, ranging from 67% (Linkoping, 10/15) to 92% (Ljubljana, 56/61); at Oxford, 43% of students (20/47) did not want further education, and 19% were unsure. Students believed that an average of 30% of antibiotic usage was unnecessary or inappropriate, with means ranging from 22% (Ljubljana) to 38% (Geneva). Most students [83%, total responses (n)¼ 279] at all medical schools felt prescribing inappropriate or unnecessary antibiotics to be professionally unethical.
JAC
Antibiotic prescribing and resistance: a student survey
Too many antibiotic prescriptions
Too many broad-spectrum antibiotics used
Excessive use of antibiotics in livestock
Dosings of antibiotics are too low Not removing the focus of infection (e.g. medical devices or catheters)
Poor hand hygiene Paying too much attention to pharmaceutical representatives/advertising 0% Not at all important
Slightly important
20%
40%
60%
80%
100%
Moderately or very important
Figure 2. Perceptions of the importance of potential contributors to antibiotic resistance (n¼256). Whiskers indicate the range between medical schools of ‘moderately or very important’ responses.
1% of all bacterial infections in Europe (excluding tuberculosis) were resistant to all known antibiotics. Students consistently believed that the most important contributors to resistance were the use of too many antibiotic prescriptions and broad-spectrum antibiotics, and the least important contributors were poor hand hygiene and paying too much attention to pharmaceutical representatives/advertising (Figure 2). Most students (60%, n¼ 248) believed that more antibiotic classes became available during the period 1980–2011 than will become available during the period 2011 –2020, with 89% of students believing that at least one new class of antibiotic would become available between 2011 and 2020.
Perceptions of bacterial resistance Resistant bacteria are thought to cause 25 000 deaths per year across Europe;10 road traffic accidents (RTAs) and lung cancer are responsible for around 2– 3 and 10 times as many deaths, respectively.11 Few students (9%, n¼ 243) were able to state the correct order of disease burden caused by RTAs, lung cancer and resistant bacteria, with only 1% of students stating the relative magnitude of burden correctly. Many students (51%) believed that resistant bacteria caused a similar or higher number of deaths than lung cancer. Most students [66%, n¼ 250 (ranging from 41% in Ljubljana to 91% in Geneva)] felt that the antibiotics they would prescribe as doctors would contribute to the problem of antibiotic resistance, and almost all students (98%) believed that antibiotic resistance would become a greater clinical problem during their career.
Discussion In all but one medical school, the majority of students wanted further education on antibiotic prescribing. This fits with previous studies of students and doctors.2,6,7 We have identified areas of self-reported confidence and lack of confidence in prescribing, which are broadly consistent across all medical schools and are similar to a recent study of US students.6 Most students (92%) felt confident in making an accurate diagnosis of infection; as misdiagnosis has been found to be a leading cause of unnecessary antibiotic use,12 it may be useful for educational programmes to address possible overconfidence in students and doctors alike. The situations in which antibiotic education is currently addressed may lack some of the complexities of ‘real-world’ clinical decisionmaking. Vignette-based clinical scenario teaching with feedback has been found to be an effective method of promoting learning related to such complexities.13 We must also teach students how to communicate with patients in situations of diagnostic uncertainty, to reduce the number of unnecessary prescriptions.14 Students are aware that a significant proportion of antibiotic prescribing is inappropriate, and the majority believe such use is professionally unethical; a greater proportion (83%) felt this prescribing to be unethical compared with a survey of US doctors (62%).7 As most students believe that their prescribing will contribute to the problem of antibiotic resistance, the link between inappropriate prescribing and ethical responsibility could be a further way to engage students in stewardship efforts. Students consistently over-rated the prevalence of resistant bacteria, with the majority believing that pan-resistant bacteria and vancomycin-resistant S. aureus are responsible for more than 1%
3 of 5
Downloaded from http://jac.oxfordjournals.org/ at Belgorod State University on November 9, 2013
Too long durations of antibiotic treatment
Dyar et al.
Acknowledgements This work was presented as a poster at the 2013 ECCMID (European Congress of Clinical Microbiology and Infectious Diseases) (Abstract P887) and as an oral presentation at the 2013 ICPIC (International Consortium for Prevention and Infection Control) conference (Abstract O051). We thank all the students who responded to our survey. We are additionally grateful for the support we received in organizing survey distribution at each centre, in particular to Stephan Harbarth (Geneva), Ha˚kan Hanberger (Linkoping), Bojana Beovic´ (Ljubljana) and Jose´ Ramo´n Pan˜o Pardo (Madrid).
ESGAP members The ESGAP executive committee includes Dilip Nathwani, Bojana Beovic, Ce´line Pulcini, Stephan Harbarth, Ha˚kan Hanberger, Leonardo Pagani, Jose´ Ramo´n Pan˜o Pardo, Philip Howard and Agnes Weschesler-Fo¨rdo¨s.
4 of 5
Funding This study was carried out as part of our routine work.
Transparency declarations None to declare.
Author contributions O. J. D. developed the idea for the study in collaboration with D. N. O. J. D., C. P., P. H. and D. N. participated in the design of the study and in revising the paper critically for substantial intellectual content. O. J. D. was responsible for data collection and analysis, and drafted the manuscript. All authors read and approved the final manuscript.
Supplementary data The questionnaire is available as Supplementary data at JAC Online (http:// jac.oxfordjournals.org/).
References 1 WHO. The Evolving Threat of Antimicrobial Resistance: Options for Action. 2012. http://whqlibdoc.who.int/publications/2012/9789241503181_eng. pdf (14 August 2013, date last accessed). 2 Minen MT, Duquaine D, Marx MA et al. A survey of knowledge, attitudes, and beliefs of medical students concerning antimicrobial use and resistance. Microb Drug Resist 2010; 16: 285– 9. 3 Ibia E, Sheridan M, Schwartz R et al. Knowledge of the principles of judicious antibiotic use for upper respiratory infections: a survey of senior medical students. South Med J 2005; 98: 889–95. 4 Wright EP, Jain P. Survey of antibiotic knowledge amongst final year medical students. J Antimicrob Chemother 2004; 53: 550– 1. 5 Humphreys H, Dillane T, O’Connell B et al. Survey of recent medical graduates’ knowledge and understanding of the treatment and prevention of infection. Ir Med J 2006; 99: 58– 9. 6 Abbo L, Cosgrove S, Pottinger P et al. Medical students’ perceptions and knowledge about antimicrobial stewardship: how are we educating our future prescribers? Clin Infect Dis 2013; 57: 631–8. 7 Abbo L, Sinkowitz-Cochran R, Smith L et al. Faculty and resident physicians’ attitudes, perceptions, and knowledge about antimicrobial use and resistance. Infect Control Hosp Epidemiol 2011; 32: 714–8. 8 Ziglam HM, Morales D, Webb K et al. Knowledge about sepsis among training-grade doctors. J Antimicrob Chemother 2006; 57: 963–5. 9 Pulcini C, Williams F, Molinari N et al. Junior doctors’ knowledge and perceptions of antibiotic resistance and prescribing: a survey in France and Scotland. Clin Microbiol Infect 2011; 17: 80– 7. 10 ECDC/EMEA Joint Technical Report. The Bacterial Challenge: Time to React. 2009. http://www.ecdc.europa.eu/en/publications/Publications/0909_TER_ The_Bacterial_Challenge_Time_to_React.pdf (14 August 2013, date last accessed). 11 WHO. Global Burden of Disease: Cause Specific Mortality Regional Estimates for 2000–2011. http://www.who.int/healthinfo/global_burden_ disease/estimates_regional/en/index.html (14 August 2013, date last accessed).
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of infections in Europe. Furthermore, students grossly overestimated the relative burden of disease caused by resistant bacteria, with most suggesting it was similar to or higher than that of lung cancer (which is, in reality, responsible for 10 times as many deaths). These findings suggest that students currently lack a context for antibiotic resistance; moreover, gradual increases in the burden of resistance may go unnoticed as these students progress in their careers, since their initial expectations have been set too high. Over 80% of students felt that MRSAwas responsible for a greater proportion of S. aureus bacteraemias in their country today than 10 years ago. This perception is likely to have been influenced by exaggerated popular media coverage and the political focus placed on MRSA, but may also reflect a lack of understanding of the success of efforts to reduce MRSA infections, which have actually decreased or remained stable in the countries of the students surveyed here. Students were broadly aware of contributors to resistance, but a quarter of students felt that handwashing was not at all important. Highlighting the successes of antibiotic stewardship programmes may be an important way to help future doctors recognize that actions they take individually can collectively lead to important results. This study has several limitations: (i) the response rate of 35% is low, but comparable to the study by Minen et al.2 (30%); (ii) the participating medical schools had leads with an interest in antimicrobial stewardship, who may affect the culture of antibiotic prescribing present in their hospitals, and interested students were more likely to respond; and (iii) we are not sure of the diversity of the structure, content and learning pedagogy of the medical schools included, all of which may influence the responses. However, the responses were consistent across medical schools for most questions, indicating a degree of external validity. In conclusion, we have found that most students want further education on antibiotics at medical school, and that such courses may be of most benefit if they can address feelings of unconfidence, particularly in relation to combination therapy and dose selection. Articulating more clearly when not to prescribe and how long to prescribe for with pragmatic examples is likely to be useful and address potential overconfidence. These and other factors will help to develop more targeted educational material to address currently unmet needs. Larger studies with more robust methodology are required to further understand key educational interventions to support learning about antibiotic stewardship.
Antibiotic prescribing and resistance: a student survey
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12 Pulcini C, Cua E, Lieutier Fet al. Antibiotic misuse: a prospective clinical audit in a French university hospital. Eur J Clin Microbiol Infect Dis 2007; 26: 277–80.
http://www.pause-online.org.uk/?q=taxonomy/term/29 (14 August 2013, date last accessed).
13 Prudent Antibiotic User. Standardized Teaching Materials for Prudent Antimicrobial Prescribing for Use in the Undergraduate Medical Curriculum.
14 Pulcini C, Gyssens IC. How to educate prescribers in antimicrobial stewardship practices. Virulence 2013; 4: 192– 202.
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