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J Antimicrob Chemother 2014; 69: 842 – 846

doi:10.1093/jac/dkt440 Advance Access publication 4 November 2013

European medical students: a first multicentre study of knowledge,


attitudes and perceptions of antibiotic prescribing and antibiotic
resistance
Oliver J. Dyar1, Céline Pulcini2,3*, Philip Howard4 and Dilip Nathwani5 on behalf of ESGAP†
(the ESCMID Study Group for Antibiotic Policies)

1
Medical Sciences Department, Oxford University, Oxford, UK; 2Service d’Infectiologie, CHU de Nice, Nice, France; 3Faculté de Médecine,
Université Nice-Sophia Antipolis, Nice, France; 4Pharmacy, Leeds Teaching Hospitals NHS Trust, Leeds, UK; 5Infection Unit,
Ninewells Hospital and Medical School, Dundee, UK

*Corresponding author. Centre Hospitalier Universitaire de Nice, Service d’Infectiologie, Hôpital l’Archet 1, Route Saint Antoine de Ginestière,
BP 3079, 06202 Nice cedex 3, France. Tel: +33-4-92-03-55-15; Fax: +33-4-93-96-54-54; E-mail: pulcini.c@chu-nice.fr
†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 resist-
ance, 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 antibiot-
ic 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 import-
ant. 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 inter-
ventions.

Keywords: education, antibiotic stewardship, survey, questionnaire, attitudes to health

Introduction found gaps in prescribing knowledge and a desire for further edu-
cation.2 – 6
The WHO recently highlighted the importance of undergraduate Our intention was to study the knowledge, attitudes and per-
training in prudent prescribing.1 To date, there has been little inves- ceptions of final-year medical students across European medical
tigation of students’ attitudes towards antibiotic prescribing, and schools to antibiotic prescribing and bacterial resistance. Our
even less of their knowledge and perceptions of antibiotic resist- goal was to develop an understanding sufficient to form a founda-
ance, recognized by the WHO as one of the three greatest threats tion for more effective education in antibiotic stewardship for
to human health; a few small, mostly single-centre studies have undergraduates.

# The Author 2013. Published by Oxford University Press on behalf of the British Society for Antimicrobial Chemotherapy. All rights reserved.
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842
Antibiotic prescribing and resistance: a student survey JAC
Methods interpreting microbiological results (Figure 1). Students were
least confident in deciding to use combination therapy, choosing
We conducted a cross-sectional survey of all final-year students at seven the correct dose and interval of antibiotics, and deciding not to pre-
European medical schools (Dundee, Scotland; Geneva, Switzerland; Linkop-
scribe an antibiotic if the patient had fever alone or there was un-
ing, Sweden; Ljubljana, Slovenia; Madrid, Spain; Nice, France; Oxford,
certainty in the diagnosis. These areas also showed the greatest
England). These schools were selected due to individual staff connections
with ESGAP (the ESCMID Study Group for Antibiotic Policies).
variation between medical schools.
We developed the questionnaire after a literature review of comparable The majority of students at six out of the seven medical schools
studies,2 – 5,7 – 9 and in consultation with infectious diseases experts. Ten stated that they would like more training on antibiotic selection,
students at two medical schools participated in pilot testing. ranging from 67% (Linkoping, 10/15) to 92% (Ljubljana, 56/61);
The 41-point self-administered survey was Internet based (using www. at Oxford, 43% of students (20/47) did not want further education,
surveymonkey.com). Students received an e-mail from their course admin- and 19% were unsure. Students believed that an average of 30% of
istrator (or infectious diseases educational lead) inviting them to participate antibiotic usage was unnecessary or inappropriate, with means
in the survey. Further e-mail reminders were sent 2 and 4 weeks after the ranging from 22% (Ljubljana) to 38% (Geneva). Most students
initial message. The survey was available from June to August 2012. Partici- [83%, total responses (n)¼ 279] at all medical schools felt prescrib-
pation was voluntary, anonymous and without compensation. Responses ing inappropriate or unnecessary antibiotics to be professionally
were single answer, multiple response and scaled. The survey is available unethical.
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 col-
Knowledge that may shape perceptions of antimicrobial
lapsed into dichotomous variables where appropriate. resistance
Most students (92%, n¼ 265) felt that antibiotic resistance was a
national problem, with 79% feeling it was a problem in their own
Results hospital.
Out of 961 eligible medical students, 338 (35%) responded to all The majority of students (83%, n¼ 265) stated that methicillin-
or part of the survey. The average response rate at each med- resistant Staphylococcus aureus (MRSA) was responsible for a
ical school was 29%, ranging from 18% (Nice, 26/148) to 53% greater proportion of S. aureus bacteraemias in their country
(Dundee, 91/172). 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
Perceptions of antibiotic prescribing ago. The majority of students (65%) thought that over 1% of
Across all medical schools, students were consistently most confi- S. aureus bacteraemias were caused by vancomycin-resistant bac-
dent in making an accurate diagnosis of infection/sepsis and teria 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% 20% 40% 60% 80% 100%

Confident or very confident 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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Dyar et al.

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)

Too long durations of antibiotic treatment

Poor hand hygiene

Paying too much attention to pharmaceutical


representatives/advertising

0% 20% 40% 60% 80% 100%

Not at all important Slightly important 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) Discussion


were resistant to all known antibiotics.
Students consistently believed that the most important contri- In all but one medical school, the majority of students wanted
butors to resistance were the use of too many antibiotic prescrip- further education on antibiotic prescribing. This fits with previous
tions and broad-spectrum antibiotics, and the least important studies of students and doctors.2,6,7 We have identified areas of
contributors were poor hand hygiene and paying too much atten- self-reported confidence and lack of confidence in prescribing,
tion to pharmaceutical representatives/advertising (Figure 2). which are broadly consistent across all medical schools and are
Most students (60%, n¼ 248) believed that more antibiotic similar to a recent study of US students.6 Most students (92%)
classes became available during the period 1980–2011 than will felt confident in making an accurate diagnosis of infection; as mis-
become available during the period 2011 –2020, with 89% of stu- diagnosis has been found to be a leading cause of unnecessary
dents believing that at least one new class of antibiotic would antibiotic use,12 it may be useful for educational programmes to
become available between 2011 and 2020. 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 decision-
making. Vignette-based clinical scenario teaching with feedback
Perceptions of bacterial resistance has been found to be an effective method of promoting learning
Resistant bacteria are thought to cause 25 000 deaths per year related to such complexities.13 We must also teach students how
across Europe;10 road traffic accidents (RTAs) and lung cancer to communicate with patients in situations of diagnostic uncer-
are responsible for around 2– 3 and 10 times as many deaths, tainty, to reduce the number of unnecessary prescriptions.14
respectively.11 Few students (9%, n¼ 243) were able to state the Students are aware that a significant proportion of antibiotic
correct order of disease burden caused by RTAs, lung cancer and prescribing is inappropriate, and the majority believe such use is
resistant bacteria, with only 1% of students stating the relative professionally unethical; a greater proportion (83%) felt this pre-
magnitude of burden correctly. Many students (51%) believed scribing to be unethical compared with a survey of US doctors
that resistant bacteria caused a similar or higher number of (62%).7 As most students believe that their prescribing will contrib-
deaths than lung cancer. ute to the problem of antibiotic resistance, the link between in-
Most students [66%, n¼ 250 (ranging from 41% in Ljubljana to appropriate prescribing and ethical responsibility could be a
91% in Geneva)] felt that the antibiotics they would prescribe as further way to engage students in stewardship efforts.
doctors would contribute to the problem of antibiotic resistance, Students consistently over-rated the prevalence of resistant bac-
and almost all students (98%) believed that antibiotic resistance teria, with the majority believing that pan-resistant bacteria and
would become a greater clinical problem during their career. vancomycin-resistant S. aureus are responsible for more than 1%

844
Antibiotic prescribing and resistance: a student survey JAC
of infections in Europe. Furthermore, students grossly overestimated
the relative burden of disease caused by resistant bacteria, with most Funding
suggesting it was similar to or higher than that of lung cancer (which This study was carried out as part of our routine work.
is, in reality, responsible for 10 times as many deaths). These findings
suggest that students currently lack a context for antibiotic resist-
ance; moreover, gradual increases in the burden of resistance may
go unnoticed as these students progress in their careers, since Transparency declarations
their initial expectations have been set too high. None to declare.
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 Author contributions
exaggerated popular media coverage and the political focus
O. J. D. developed the idea for the study in collaboration with D. N. O. J. D.,
placed on MRSA, but may also reflect a lack of understanding of
C. P., P. H. and D. N. participated in the design of the study and in revising
the success of efforts to reduce MRSA infections, which have actually
the paper critically for substantial intellectual content. O. J. D. was respon-
decreased or remained stable in the countries of the students sur- sible for data collection and analysis, and drafted the manuscript. All
veyed here. Students were broadly aware of contributors to resist- authors read and approved the final manuscript.
ance, 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 recog-
nize that actions they take individually can collectively lead to im- Supplementary data
portant results. The questionnaire is available as Supplementary data at JAC Online (http://
This study has several limitations: (i) the response rate of 35% is jac.oxfordjournals.org/).
low, but comparable to the study by Minen et al.2 (30%); (ii) the par-
ticipating 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
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