antibiotics
Article2015 versus 2021: Self-Reported Preparedness to Prescribe
Antibiotics Prudently among Final Year Medical Students
in Sweden
Jasmine Al-Nasir 1 , Andrej Belančić 2,3 , Dora Palčevski 4 , Oliver J. Dyar 1, *and on behalf of Student-PREPARE Sweden Working Group †
1

2

3

4

*
†

Citation: Al-Nasir, J.; Belančić, A.;
Palčevski, D.; Dyar, O.J.; on behalf ofStudent-PREPARE Sweden Working
Group. 2015 versus 2021: SelfReported Preparedness to Prescribe
Antibiotics Prudently among Final
Year Medical Students in Sweden.
Antibiotics 2024, 13, 303. https://

Department of Public Health and Caring Sciences, Uppsala University, 75236 Uppsala, Sweden;jasmineeal@outlook.com
Department of Clinical Pharmacology, Clinical Hospital Centre Rijeka, 51000 Rijeka, Croatia;
andrej.belancic@uniri.hr
Department of Basic and Clinical Pharmacology with Toxicology, Faculty of Medicine, University of Rijeka,
51000 Rijeka, Croatia
Department of Internal Medicine, Clinical Hospital Centre Rijeka, 51000 Rijeka, Croatia;
dora.palcevski@gmail.com
Correspondence: oliver.dyar@pubcare.uu.se; Tel.: +46-072-99-99-312
Membership of the Student-PREPARE Sweden Working Group is provided in the Acknowledgments.

Abstract: Cross-sectional surveys have found variations in how prepared medical students feel toprescribe antibiotics responsibly, but insights are lacking on the stability of these outcomes. In a2015 survey, final-year Swedish medical students reported very high preparedness levels across acomprehensive range of relevant curriculum topics. We repeated this survey in 2021 to assess thestability of previous findings and to capture the potential impacts of the COVID-19 pandemic. Finalyear students in 2015 and 2021 at all seven Swedish medical schools were eligible to participate in an
online survey covering curricula topics, teaching methods and COVID-19 impacts (2021). Eligible
students received email invitations and reminders from local coordinators. Students from six ofseven medical schools participated in both surveys, with response rates of 24.1% (309/1281) in 2021
and 21.3% (239/1124) in 2015. The average global preparedness was 77.0% and 83.2%, respectively(p < 0.001), with lower preparedness levels in 24/27 curriculum topics in 2021. Students at certain
universities reported COVID-19 impacts on antibiotic prescribing education (format, duration andperceived quality). Self-reported preparedness levels have fallen slightly but remain high comparedwith 2015 levels in other European countries. Students consistently reported lower preparednessin specific topics; improvement efforts should consider focusing on these areas, particularly in thecontext of the ongoing implementation of programmes leading to a full licence upon graduation.

doi.org/10.3390/antibiotics13040303

Keywords: antimicrobials; antimicrobial stewardship; medical education
Academic Editor: Albert Figueras
Received: 16 February 2024
Revised: 18 March 2024
Accepted: 22 March 2024

1. Introduction

Published: 27 March 2024

Prescribing drugs is a core activity in the daily work of most medical doctors, yet agrowing number of recent studies indicate that many, if not most, medical graduates do
not feel sufficiently prepared for their upcoming prescribing responsibilities [1–6]. Since
junior doctors are responsible for a considerable share of drug prescriptions, this is a serious
concern for medical educators [2,3]. The importance of improving undergraduate educationof medical students in responsible antibiotic prescribing is a key effort in addressing thegrowing mortality burden attributed to antimicrobial resistance (AMR), particularly inthe context of studies indicating persistent antibiotic overuse and misuse in healthcare
settings [7–10]. Education to improve responsible antibiotic use is thus considered a corecomponent of antibiotic stewardship, which has been defined as a coherent set of actions
that promote using antimicrobials responsibly [11]. Such actions include a combination of

Copyright: © 2024 by the authors.
Licensee MDPI, Basel, Switzerland.
This article is an open access article
distributed under the terms andconditions of the Creative Commons
Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).

Antibiotics 2024, 13, 303. https://doi.org/10.3390/antibiotics13040303

https://www.mdpi.com/journal/antibiotics

Antibiotics 2024, 13, 303

2 of 13both restrictive actions (e.g., formulary restrictions and pre-approval requirements) andenablement actions (education, clinical guidelines, audit and feedback) [12].
Strong education in responsible antibiotic use and the broader factors leading to antibiotic misuse and overuse can, at the undergraduate level, lay an important foundation forstudents to contribute to future antibiotic stewardship efforts as well as to understand their
purpose. Medical school is a crucial time during which knowledge, attitudes and behavioursof future prescribers are still being shaped, both by the explicit curriculum and through thehidden curriculum of prescribing practices they are exposed to on clinical placements androtations [13]. It is, therefore, natural that the World Health Organization (in the Global
Action Plan on Antimicrobial Resistance) recommends that educational efforts should target
undergraduates, not just postgraduate education, stating that “making antimicrobial resistance a core component of professional education, training, certification, continuing educationand development in the health and veterinary sectors and agricultural practice will help
to ensure proper understanding and awareness among professionals.” [14]. Developing an
understanding of the current state of undergraduate education in responsible antibiotic use isan essential component of efforts to improve education.
1.1. Antimicrobial Stewardship in Sweden
Sweden has a strong history of raising public awareness of antibiotic resistance andimplementing efforts to reduce the use and misuse of antibiotics. Antibiotic stewardshipinitiatives, coordinated initially by Strama, a nationwide working model to address antibiotic resistance in health care, have existed for many years at national and regional
levels and have placed a strong emphasis on patterns of antibiotic prescribing in primarycare [15]. A Swedish national action plan was first published in 2000 and has been revised
several times, with professional education mentioned in many versions. The 2016 plan [16],following on from the Global Action Plan, stated that the “government expects relevant
staff to have knowledge about antibiotic resistance, the spread of infectious diseases andthe importance of a high degree of compliance with basic hygiene routines and otherinfection prevention measures, as well as knowledge about the seriousness and complexityof the issue from a global perspective” and further that “the government expects antibiotic
resistance, infection prevention and control/hygiene to be included in relevant educationand training programmes”.
A consequence of longstanding efforts to minimise antibiotic misuse and overuse in
Sweden is that surveillance studies have regularly shown relatively low levels of antibiotic
consumption, high proportions of narrow-spectrum antibiotic use and low resistance rates
among key pathogens [9,10,15].
1.2. Aim
Previous cross-sectional surveys suggest that medical students in Europe and beyond
do not feel sufficiently well prepared to prescribe antibiotics responsibly. A key limitationof previous studies is that they have typically captured data at a single time point [4,17–19],
meaning that insights are lacking on the longer-term stability of outcomes from suchstudies; evidence of stable preparedness levels in the absence of widespread changes inteaching would further validate the ability to draw conclusions from studies conducted
at a single time point. In addition, many previous investigations have only assessed anarrow range of curriculum topics relevant to responsible antibiotic use. In 2015, we
conducted a large-scale survey study of final-year medical students at all European medical
schools [4]. Compared with other respondents, Swedish medical students reported very
high preparedness levels across a comprehensive range of curriculum topics in responsible
antibiotic prescribing and low levels of perceived need for further education. The main aimof the present study was to build on the previous literature by assessing the stability of theseprevious findings, both for overall preparedness levels and preparedness in individual
topics, by repeating the same 2015 survey with final-year medical students in Sweden in
2021. In addition, we aimed to capture the potential impacts of the COVID-19 pandemicAntibiotics 2024, 13, 303

of these previous findings, both for overall preparedness levels and preparedness inindividual topics, by repeating the same 2015 survey with final-year medical students in
3 of 13
Sweden in 2021. In addition, we aimed to capture the potential impacts of the COVID-19
pandemic on education and preparedness within responsible antibiotic use. Our primaryresearch questions were: Are the previously observed high overall preparedness levels
on education and preparedness within responsible antibiotic use. Our primary researchamong final-year Swedish students stable (i.e., similar in 2021 to 2015)? Have there beenquestions were: Are the previously observed high overall preparedness levels among finalwidespread improvements or declines in preparedness levels for individual curriculum
year Swedish students stable (i.e., similar in 2021 to 2015)? Have there been widespread
topics? Do final-year students believe that the COVID-19 pandemic has aﬀected the form,
improvements or declines in preparedness levels for individual curriculum topics? Do
quality and duration of education on antibiotic prescribing at medical school?
final-year students believe that the COVID-19 pandemic has affected the form, quality andduration of education on antibiotic prescribing at medical school?
2. Results
2.1.
Participation
2. Results
2.1. Participation
A total of 239 and 309 eligible responses were received in 2015 and 2021, respectively,
representingof 21.3%(239/1124)
and24.1% (309/1281).
rates per
A total ofresponse
239 and rates
309 eligible
responses
werereceived
in 2015 andResponse
2021, respectively,
individual
medicalschoolpresented
in Supplementary
Figure S1. Response
No significant
representing
response
ratesareof 21.3%(239/1124)
and 24.1% (309/1281).
rates
diﬀerence
was
found
in
genderdistribution
between
the
two
years
(57.3%
vs.
63.7%
per individual medical school are presented in Supplementary Figure S1. No significant
female;p =was0.128),
butintheaverageage of participating
was
lower
2021 thanindifference
foundgenderdistribution
between thestudents
two years(57.3%
vs.in63.7%
female;p = 0.128),
averageage of2015(52.4%but
vs.the37.0%≤25 years
oldparticipating, p < 0.001). students was lower in 2021 than in 2015
(52.4% vs. 37.0% ≤25 years old, p < 0.001).
2.2. Global Preparedness Scores2.2. Global Preparedness Scores
The country-level global preparedness score (GPS), representing the average
The country-levelglobalpreparedness
score(GPS),
representing
the average
percentage
of topics forwhich
students felt
at least
suﬃciently
prepared,
was percentslightly
age of topics
for(83.2%
whichvs.
students
least sufficiently
wasranged
slightlyfrom
higherinhigherin 2015
77.0%, felt
p < at0.001).
The medicalprepared,
school GPS
80.5–
2015
(83.2%
vs.
77.0%,
p<0.001).
The
medicalschoolGPS
rangedfrom
80.5–85.9%
in2015
85.9% in 2015 and 69.3–82.5% in 2021, as presented in Figure 1, with lower GPS scores atand 69.3–82.5%
in 2021,
as presented
in Figure
1, withlower GPSscores at everyTable
medicalevery
medical schoolin 2021.
Statisticallysignificant
diﬀerences(Supplementary
S1)schoolin
2021.
Statisticallysignificant
differences(Supplementary
Table
S1)
were
observed
were observed for Örebro (11.5% diﬀerence), Umeå (13% diﬀerence) and Karolinska (3.5%for Örebro (11.5% difference), Umeå (13% difference) and Karolinska (3.5% difference).
diﬀerence).

Figurefor eacheach medical
medical school
school inin 20152015 andand 2021.
2021.
Figure 1.
1. Global
Global preparedness
preparedness scoresscores for2.3. Topic Preparedness Scores
Students reported lower preparedness levels in 2021 than in 2015 for 24 of the
27 curriculum topics included in the study instrument, with 10 of these differences being statistically significant (Table 1). The only questions for which students reported being

Antibiotics 2024, 13, 303

4 of 13more prepared in 2021 (although non-significant) were: ‘To recognise the clinical signs ofinfection’ (+0.2% difference), ‘To interpret biochemical markers of inflammation’ (+0.9%
difference) and ‘To work within the multi-disciplinary team in managing antibiotic use in
hospitals’ (+2.2% difference). The absolute percentage changes in topic preparedness scores
between studied years per medical school are shown in Supplementary Table S2. The curriculum topic for which students felt the least prepared was ‘To prescribe using principles
of surgical antibiotic prophylaxis’ both in 2015 and 2021 (53.8% vs. 44.0%, p = 0.020), whilst
they felt the best prepared ‘To recognise the clinical signs of infection’ (99.2% vs. 99.4%,
p = 0.700). The topics with the highest and lowest preparedness and greatest variations
between medical schools for 2021 are shown in Table 2. Table 3 shows the two topics withthe lowest preparedness scores at each medical school in 2021.
Table 1. Average preparedness score in 2021 compared to 2015 for each topic. The difference is shownin the table and the range in difference between medical schools.

Topic

To recognise the clinical signs of infection
To assess the clinical severity of infection (e.g.,using criteria such as the septic shock criteria)
To use point-of-care tests (e.g., urine dipstick,rapid diagnostic tests for streptococcal
pharyngitis)
To interpret biochemical markers of inflammation(e.g., CRP)To decide when it is important to takemicrobiological samples before starting antibiotic
therapy
To interpret basic microbiological investigations(e.g., blood cultures, antibiotic susceptibility
reporting)To identify clinical situations when not toprescribe an antibiotic
To differentiate between bacterial colonisation andinfection (e.g., asymptomatic bacteriuria)
To differentiate between bacterial and viral upper
respiratory tract infections
To select initial empirical therapy based on themost likely pathogen(s) and antibiotic resistancepatterns without using guidelines
To decide the urgency of antibiotic administrationin different situations (e.g., <1 h for severe sepsis,
non-urgent for chronic bone infections)
To prescribe antibiotic therapy according tonational/local guidelines
To assess antibiotic allergies (e.g., differentiating
between anaphylaxis and hypersensitivity)
To identify indications for combination antibiotic
therapy
To decide the shortest possible adequate durationof antibiotic therapy for a specific infection
To prescribe using principles of surgical antibiotic
prophylaxis
To review the need to continue or change
antibiotic therapy after 48–72 h, based on clinicalevolution and laboratory results2015 (n = 239)

2021 (n = 309)

Sufficiently
PreparedSufficiently
Prepared

Difference 1

%

Range

%

Range

(Range)99.2

97–10099.4

97–100

95.0

92–100

92.2

89–98

0.2 (−0.3–0.8)−2.8(−7.5–5.9)

89.9

80–94

87.3

72–98

97.1

92–100

98.0

95.4

92–97

93.7

p

Trend

0.7

↗

0.2

↘

−2.6
(−14.8–4.4)

0.3↘

94–1000.9 (−1.7–4.3)

0.5

↗

94.1

85–98

−1.3
(−6.9–1.0)

0.5

↘

86–97

92.8

85–100−0.9(−6.8–6.0)

0.7

↘

93.7

92–97

84.4

64–90

<0.001

↘

91.2

89–97

87.3

75–95

0.1

↘

93.3

86–100

81.9

75–88

<0.001

↘

71.4

64–82

61.8

49–78

−9.6
(−26.6–2.6)

0.02

↘

87.9

76–94

82.8

77–90

−5.1
(−17.7–9.4)

0.1

↘

92.4

82–97

87.3

75–94

0.05

↘

76.1

66–94

72.3

60–91

0.3

↘

61.4

48–70

48.3

32–62

0.002

↘

62.2

46–76

48.2

36–57

0.001

↘

53.8

35–62

44.0

32–51

0.02

↘

81.2

71–94

75.4

62–89

0.1

↘

−9.3
(−30.2–−2.6)−3.9(−19.1–2.1)−11.4(−25.0–−2.6)−5.1(−11.6–3.6)−3.8(−18.5–25.5)−13.1(−25.8–−5.4)−14.0(−31.7–0.4)−9.8(−25.8–−5.4)−5.8(−25.6–11.9)

Antibiotics 2024, 13, 303

5 of 13

Table 1. Cont.

Topic

To assess clinical outcomes and possible reasonsfor the failure of antibiotic treatment
To decide when to switch from intravenous (IV) to
oral antibiotic therapy
To measure/audit antibiotic use in a clinicalsetting and to interpret the results of such studies
To work within the multi-disciplinary team inmanaging antibiotic use in hospitals
To discuss antibiotic use with patients who areasking for antibiotics when I feel they are notnecessary
To communicate with senior doctors in situations
where I feel antibiotics are not necessary, but I feelI am being inappropriately pressured into
prescribing antibiotics by senior doctors
To use knowledge of the common mechanisms ofantibiotic resistance in pathogens
To use knowledge of the epidemiology of bacterial
resistance, including local/regional variations
To practise effective Infection control and hygiene(to prevent the spread of bacteria)
To use knowledge of the negative consequences ofantibiotic use (bacterial resistance, toxic/adverse
effects, cost, Clostridium difficile infections)2015 (n = 239)

2021 (n = 309)

Sufficiently
PreparedSufficiently
Prepared

Difference 1

%

Range

%

Range

83.1

76–88

77.5

66–87

75.1

68–82

65.2

51–75

64.4

44–57

50.2

21–43

69.3

54–70

71.5

42–71

(Range)−5.6(−12.3–−1.2)−9.9(−22.0–−4.2)−14.2(−30.6–−7.8)
2.2(−17.2–5.4)

95.3

88–97

93.4

81–98

60.9

46–71

47.3

22–47

84.0

78–100

78.8

62–90

75.5

69–82

62.1

38–78

97.9

95–100

95.5

89–98

97.9

94–100

95.8

89–98

p

Trend

0.1

↘

0.01

↘

<0.001

↘

0.6

↗

−1.9
(−7.7–3.9)

0.3

↘

−13.6
(−48.4–−0.4)

0.002

↘

−5.2
(−30.9–5.9)−13.4(−40.6–−3.5)−2.4(−6.6–−0.3)

0.1↘

<0.001

↘

0.1

↘

−2.1
(−8.6–3.1)

0.2↘

1 A negative result indicates a lower score in 2021 than in 2015.

Table 2. Curriculum topics with the highest and lowest preparedness scores and greatest variation
between medical schools in 2021.
Lowest Preparedness

Greatest Variation between Medical
Schools

To recognize the clinical signs of infection(99.4%)

To prescribe using principles of surgicalantibiotic prophylaxis (44.0%)

To use knowledge of the negative
consequences of antibiotic use (bacterial
resistance, toxic/adverse effects, cost,
Clostridium difficile infections)(37.7–78.3%)

To interpret biochemical markers ofinflammation (e.g., CRP) (98.0%)

To communicate with senior doctors insituations where I feel antibiotics are notnecessary but I feel I am being
inappropriately pressured into
prescribing antibiotics by senior doctors(47.3%)To use knowledge of the common
mechanisms of antibiotic resistance inpathogens (60.4–91.5%)

To use knowledge of the negative
consequences of antibiotic use (bacterial
resistance, toxic/adverse effects, cost,
Clostridium difficile infections) (95.8%)

To decide the shortest possible adequate
duration of antibiotic therapy for a
specific infection (48.2%)

To interpret basic microbiologicalinvestigations (e.g., blood cultures,
antibiotic susceptibility reporting)(41.7–71.4%)

To practise effective Infection control andhygiene (to prevent the spread ofbacteria) (95.5%)

To identify indications for combination
antibiotic therapy (48.3%)

To differentiate between bacterial andviral upper respiratory tract infections(32.1–61.7%)

Highest Preparedness

Antibiotics 2024, 13, 303

6 of 13

Table 2. Cont.
Highest Preparedness

Lowest Preparedness

Greatest Variation between Medical
Schools

To decide when it is important to takemicrobiological samples before starting
antibiotic therapy (94.1%)

To measure/audit antibiotic use in aclinical setting and to interpret the resultsof such studies (50.2%)

To assess antibiotic allergies (e.g.,differentiating between anaphylaxis andhypersensitivity) (49.1–78.3%)

Table 3. Curriculum topics with the lowest preparedness score per medical school in 2021.
Gothenburg

Karolinska

To prescribe using
principles ofsurgical antibiotic
prophylaxis(36.2%)

To communicate
with senior doctors
in situations where
I feel antibiotics are
not necessary but I
feel I am being
inappropriatelypressured into
prescribing
antibiotics bysenior doctors(34.7%)To measure/audit
antibiotic use in aclinical setting and
to interpret theresults of suchstudies (40.6%)

To measure/audit
antibiotic use in aclinical setting and
to interpret theresults of suchstudies (38.8%)

To communicate
with senior doctors
in situations where
I feel antibiotics are
not necessary but I
feel I am being
inappropriatelypressured into
prescribing
antibiotics bysenior doctors(45.3%)To measure/audit
antibiotic use in aclinical setting and
to interpret theresults of suchstudies (36.2%)

Lund

Umeå

UppsalaÖrebroTo measure/audit
antibiotic use in aclinical setting and
to interpret theresults of suchstudies (20.8%)

To prescribe using
principles ofsurgical antibiotic
prophylaxis(40.0%)

To communicate
with senior doctors
in situations where
I feel antibiotics are
not necessary but I
feel I am being
inappropriatelypressured into
prescribing
antibiotics bysenior doctors(22.2%)

To prescribe using
principles ofsurgical antibiotic
prophylaxis(32.1%)To measure/audit
antibiotic use in aclinical setting and
to interpret theresults of suchstudies (43.3%)

To measure/audit
antibiotic use in aclinical setting and
to interpret theresults of suchstudies (27.8%)

2.4. Expressed Need for Further Education
The percentages of students at each medical school who felt they needed more education on prudent antibiotic use are presented in Table 4. Students expressed greater needs
for more education in 2021 than in 2015 on average (36% vs. 21%, p = 0.003), with the same
trend observed at every medical school. The greatest between-survey difference was atÖrebro (34% difference, p = 0.023), and the least was for Uppsala (3% difference, p = 0.706).
Table 4. Students’ expressed needs for more education on responsible antibiotic use in 2015 and 2021.
Percentage of Students Who Feel They Need More Education

2015

2021

p

Gothenburg University
Karolinska Institutet
Lund UniversityUmeå University
Uppsala UniversityÖrebro University
Average

18%
25%
19%
32%
13%
18%
21%

36%
40%
32%
37%
16%
52%
36%

0.05
0.09
0.18
0.63
0.7
0.02
0.003

2.5. Impacts of COVID-19 on Education
Respondents in the 2021 survey expressed that COVID-19 had negatively affected
their teaching of prudent antibiotic use in terms of format (32.4%, 94/290), duration (12.0%,

Antibiotics 2024, 13, 303

7 of 13

35/291) and quality (16.5%, 47/284). Sixteen per cent of respondents (45/286) felt that the
impacts of the COVID-19 pandemic on their education at medical school had worsened
how prepared they felt to prescribe antibiotics prudently. Widespread variations were seen
between medical schools.
Fourteen per cent (39/273) of students reported having received teaching on prescribing antibiotics for patients with COVID-19, either primarily by clinical supervisors (51%,
20/39) or at lectures, seminars or case-based discussions (49%, 19/39).
2.6. Perceived Usefulness of Teaching Methods
Table 5 presents the perceived usefulness of different teaching methods among 2015
and 2021 respondents, including variations between medical schools. The most usefulteaching method was considered to be ‘small group teaching’ both in 2015 and 2021, andthe least useful teaching methods were considered to be ‘microbiology clinical placement’and ‘active learning assignments’. In addition, the teaching methods considered to be least
available/used were ‘microbiology clinical placement’ and ‘pear or near-peer teaching’.
Table 5. Students’ perceived usefulness of different teaching methods for responsible antibiotic use.
Teaching
MethodWas Not
Used 1

2021

2015

2021

Useful or Very Useful

Not Useful

Neutral

2015

2015

2021

2015

2021

2015

2021

2015

Teaching Method

Lectures (with >15 people)
Small group teaching (with<15 people)
Discussions of clinicalcases and vignettes
Active learningassignments
Infectious diseases clinicalplacement
Microbiology clinicalplacement
Peer or near-peer teaching

I Do Not
Understandthe
Question

I Am
Unsure

2021

%

Range

%

Range

%

%

%

%

%

%

%

%

%

%

88.1

77.1–97.0

77.7

57.8–86.7

0.4

0.0

10.2

19.1

1.3

3.2

0.0

0.0

0.4

2.1

95.0

70.6–93.9

91.0

55.6–90.6

0.9

0.7

2.7

3.7

1.4

4.5

0.0

0.0

5.5

7.9

92.2

82.4–92.5

90.9

66.7–92.2

0.4

0.3

4.8

5.9

2.2

2.1

0.4

0.7

1.3

1.0

51.9

35.1–52.0

54.1

25.0–47.2

7.4

6.4

35.4

32.7

5.3

6.8

0.0

0.0

18.9

23.9

93.6

88.6–95.5

82.6

58.3–85.9

0.4

3.2

5.1

12.4

0.8

1.1

0.0

0.7

0.0

2.8

47.1

8.6–52.9

38.8

8.3–29.8

10.1

6.2

30.4

39.5

11.6

14.7

0.7

0.8

41.5

55.2

68.5

27.3–48.6

67.5

22.2–42.2

1.5

1.3

17.7

20.5

10.8

9.9

1.5

0.7

44.7

47.8

1 Participants who responded that a teaching method was not used were not included in denominators forassessing the usefulness of a teaching method (i.e., all the other results in the table).

3. Discussion
We conducted a repeated cross-sectional questionnaire survey of final-year medical
students in Sweden to assess changes in preparedness to prescribe antibiotics responsibly
between 2015 and 2021. Our aim was to assess whether the previously high levels of
preparedness were stable in the context of factors that may have influenced preparedness
levels, such as rising global awareness of AMR with the Global Action Plan [14], a new
Swedish National Action Plan in 2016 [16] and the impacts of the COVID-19 pandemic [20].
3.1. Overall Preparedness Levels and Needs for Further Education
Our overall results show that medical students in Sweden had significantly lower
overall self-reported preparedness levels in 2021 compared to 2015, with trends towards
lower preparedness levels seen in all medical schools and across almost all curriculum
topics. In keeping with lower reported preparedness levels, we also found increased
proportions of students reporting a need for more education on prudent antibiotic use at
all medical schools in 2021.
It is thus clear that there has not been any large-scale improvement in preparedness
despite the growing awareness of antimicrobial resistance and the development and implementation of both the Global Action Plan [14] and the National Action Plan [16]. Althoughboth of these plans stressed the importance of undergraduate professional education, toAntibiotics 2024, 13, 303

8 of 13

our knowledge, there have been no systematic or top-down efforts to improve educationin responsible antibiotic use in medical education since 2015. One potential explanation
for this lack of effort is that data on antibiotic prescribing suggest that doctors in Sweden
already have very low levels of antibiotic misuse and overuse, in international terms, andcurrent approaches in undergraduate education may have been considered sufficient. Our
study methodology does not allow us to explain the observed lowering of preparedness
levels and raising of perceived needs for more education from 2015 to 2021. One possibility
is that more widespread awareness of the perceived threat of AMR, in part in response to
global and national action plans, may have negatively influenced students’ perceptions of
their own preparedness to prescribe antibiotics responsibly.
Many students reported impacts on the form, quality and duration of education on
antibiotic prescribing caused by the COVID-19 pandemic. Medical schools in Sweden, as
in the rest of the world, had to shift from clinical placements to predominantly virtual
education during the pandemic, with potential consequences on the quality of teaching
and learning [20–22]. Even if the majority of students in this study had already had theirclinical rotations in infectious diseases before the pandemic, a reduction in exposure to daily
antibiotic prescribing practices on other clinical placements could be a contributing factor
to the observed lower perceived preparedness levels. This hypothesis is supported by aprevious study in which medical students from Gothenburg reported that clinical rotations
were the element considered to be most valuable for learning, as well as the chance topractice prescribing medications under supervision in clinical wards [18]. Interestingly, oneof the curriculum topics with the greatest reduction in preparedness levels between 2021
and 2015 was differentiating between bacterial and viral respiratory tract infections. This result
could be a result of a greater awareness of the complexity of the task of distinguishing
between viral and bacterial infections gained during the pandemic. It is possible that theprevious very high levels of preparedness on this topic (93%) actually represented a degreeof over-confidence among students, so a lowering in perceived preparedness levels inthis topic is not necessarily negative. This is in line with studies showing that during theearly stages of the COVID-19 pandemic, patients often received empirical antibiotics eventhough they did not have a bacterial infection, mainly because the symptoms of bacterial
infections are similar to viral infections [23].
3.2. Consistency in Relative Topic Preparedness Scores and Teaching Methods
The ranking of topic preparedness levels, i.e., from high to low preparedness levels,
was quite consistent between medical schools in both 2015 and 2021 and is largely inkeeping with the overall ranking of curriculum topics observed across all European medical
schools in 2015 [4]. A similar study using an almost identical questionnaire was recently
conducted with medical students in Croatia and found that results on preparedness oncertain topics were largely consistent between 2015 and 2019 [5]. This consistency, despite
variations in medical school curricula, socioeconomic features and cultures, suggests thatcertain topics are either inherently more difficult to feel prepared for or are consistently lesswell taught than others.
Similarly, we identified no large changes between 2015 and 2021 in terms of theteaching methods used or their perceived usefulness in the context of learning about
responsible antibiotic use. Small group teaching, discussion of clinical cases and infectious
diseases clinical placements were considered to be most useful, a pattern seen across all
European medical schools in 2015 [4] and also in the repeated cross-sectional study among
students in Croatia in 2019 [5]. A number of medical programmes outside Sweden arestarting to use externally produced virtual courses, such as the WHO-online antibiotic
stewardship course, and it will be interesting to assess the longer-term impact of theseteaching methods both in terms of resource-saving potential and student preparedness [24].

Antibiotics 2024, 13, 303

9 of 133.3. Variations between and within Medical Schools
Our primary aim was to assess the stability of results at a national level in Sweden
by repeating our survey with the same instrument and at the same time point in the medical programs. Although we did detect a number of statistically significant differences atindividual medical schools between the two survey years, our study was likely underpowered to detect many potential variations (for instance, at the level of preparedness inindividual topics). We also purposely avoided comparing preparedness results between
medical schools, as our study was not designed to facilitate such comparisons. The level ofperceived preparedness may be affected by recency in exposure to core teaching in infectiondiseases and antibiotics. The placement of this course varied from Term 5 (Gothenburg) toTerm 9 (Uppsala), which may have influenced the feeling of preparedness and our results.
This is challenging to assess, however, given the variations in exposure that individual
students will have both through the hidden curriculum (i.e., exposure to daily clinicalpractices on other clinical rotations) as well as through case-based discussions as part ofother clinical rotations, which may involve consideration of antibiotic therapy. It is also
important to note that one medical school, Örebro, is a relatively new medical school.
The first students graduated soon after the 2015 survey, so particular caution needs to betaken when comparing variations between survey years at Örebro with changes observed
between survey years at other medical schools.
Finally, it is important to note that a comprehensive review of changes at individual
medical schools in curricula, teaching sessions and examinations between 2015 and 2021
was beyond the scope of the present study. Such a review is to be encouraged at participating medical schools to allow a context-specific interpretation of the results presented here,
particularly regarding changes in preparedness in individual curricula topics.
3.4. Methodological Considerations
Key strengths of our study include the use of an identical study design and comprehensive questionnaire, in order to allow comparison between two cohorts whilst minimizing
the introduction of additional sources of bias. Since our primary aim was to assess thestability of self-reported preparedness levels between 2015 and 2021, we did not choose toinclude additional questions covering topic areas that may now appear in medical school
curricula within antimicrobial stewardship (e.g., the concept of One Health and the WHO
AWaRe classification of antibiotics). Our response rates were consistent between years
but, as with many other studies in the same subject area [4,6,25], somewhat low. We haveno data available on reasons for non-participation. We consider that even if the response
rates were low, our results are likely representative of all medical schools, as no correlation
was found between response rate and preparedness levels. Furthermore, the similarityof response rates between survey years provides some indication that any effects of selection biases (e.g., risks of over-representation of students with strongest opinions) weresimilar during both survey periods. We have previously noted [4,18] that an importantconsideration when interpreting our findings is that the questionnaire was designed toelicit students’ self-reported preparedness levels within each curriculum topic, as opposed
to objectively assessing individual students’ actual preparedness levels. This, therefore,
limits the interpretations that can be directly made from our results; additional studies
are required to understand how more objective assessments (e.g., with case vignettes) andself-reported preparedness levels are related and whether the strength of the relationshipvaries between different topics. Nonetheless, we contend that gaining student perspectives
on teaching is a vital component of quality improvement efforts and is fully in keepingwith recommended student-centered practices in higher education [26]. Finally, it is also
important to note that observational questionnaire studies such as ours, even if conducted
anonymously, may be influenced by a social-desirability bias among respondents; however,
we have no reason to suspect that this potential bias would disproportionately affect datacollection from a particular study period, so it should not influence our ability to assess
stability in self-reported preparedness levels between survey years.

Antibiotics 2024, 13, 303

10 of 134. Materials and Methods
4.1. Study Design
To assess medical students’ self-reported preparedness for responsible use of antibiotics, the European Society of Clinical Microbiology and Infectious Diseases (ESCMID)
Study Group for Antimicrobial Stewardship (ESGAP) conducted a cross-sectional, multicentre, web-based survey for final year medical students at medical schools in 29 European
countries in 2015 [4]. The same study design was repeated in 2021 in Sweden at all sevenmedical schools with a modified questionnaire tool.
4.2. Medical Schools in Sweden
There are seven medical schools in Sweden, located in Stockholm, Gothenburg, Uppsala, Lund, Linköping, Umeå and Örebro. A set of seventeen national “examination goals”
exist and every medical school is legally required to ensure that their own curriculum ensures that graduating students reach these learning outcomes. Importantly, these learning
outcomes consist of high-level descriptions of the Knowledge and understanding, Skills andabilities, and Judgment and approach that students should develop. This means that withina specific subject area, such as responsible antibiotic use, there can be variations between
medical schools in terms of the curricula content, teaching methods used and examinations.
For instance, in Linköping and Örebro, problem-based learning is the main teaching method
throughout the medical programme, whereas flipped classroom case-based learning is the mostused teaching activity at Lund. At the time of the survey, all medical programmes wererequired to be 5.5 years (11 terms) in duration. The structure, however, varies between
universities, including the time points at which specific subjects and clinical placements
are included. For instance, the infectious diseases course takes place during different terms:
Gothenburg (during the 5th term), Karolinska Institute (5th and 6th terms), Lund (7th term),Umeå (8th term), Uppsala (9th term) and Örebro (7th and 8th terms).
4.3. Survey Development
The survey instrument was developed in 2015 by a group of six international experts
on antimicrobial stewardship through an informal consensus process based both on aprevious study of undergraduate curricula coverage of principles of prudent antibiotic use
in European medical schools [13] and a review of relevant previous studies among medical
students. Its complete design, development and piloting (with students from two countries)
have been extensively described elsewhere [4]. The 47-item study instrument included
questions on demographics, self-reported preparedness in 27 curricular topics on prudent
antibiotic use (based on a 7-point Likert-type scale principle), opinions of the usefulnessof a selection of commonly used teaching methods in undergraduate medical education,and perceived need for further education on this topic. The survey instrument was revised
before use in 2021 through the development and addition of nine questions concerning theimpact of the COVID-19 pandemic on education in responsible antibiotic use, included
at the end of the 2015 version of the questionnaire. These questions were developed by
the first and last author through a literature review in 2021 to identify other studies that
had investigated the impacts of COVID-19 on medical student teaching and learning, andthe questions were constructed to follow a similar format to the other questions in theoriginal questionnaire. The additional questions were tested for face validity but were nototherwise subjected to pilot testing, given the low complexity level of the questions.
4.4. Survey Distribution and Participants
We followed the same steps for recruitment of participants and survey distribution forthe 2021 survey as in the study protocol from 2015 [4]: the “program committee” at each
medical school was contacted during early autumn 2021 to identify a local coordinator withresponsibility for sending invitations to all eligible medical students, i.e., students in their
final term or second last term of medical school at a Swedish university during autumn
2021. Template invitations were drafted by the central study coordinator and forwarded

Antibiotics 2024, 13, 303

11 of 13

to medical school coordinators for distribution via email to students. The medical school
coordinators were also asked to provide the exact number of eligible students per term,in order to be able to calculate response rates. The initial invitation with a survey link
was sent by each medical school coordinator by email to all eligible medical students, andthis was followed by two email reminders after 2–3 and 4–6 weeks. The self-administeredsurvey was accessible via SurveyMonkey® (SurveyMonkey Inc., San Mateo, CA, USA)during spring 2015 (for approximately five months) and autumn 2021 (for approximately
three months). Informed consent was obtained from all subjects involved in the study.
Participation was voluntary and anonymous.
4.5. Statistical Analyses
Data was exported from the SurveyMonkey® service, and the analyses were performed
using Microsoft Excel 2019® (Microsoft Office). Responses were excluded from subsequent
analyses if (i) the response rate at the medical school was lower than the pre-specified
cut-off of 10% in 2015 and 2021 (leading to the removal of Linköping medical school) or(ii) a respondent did not answer all of the preparedness questions. Responses to questions
about preparedness for each of the 27 topics covered in the curriculum were divided into
two categories: (4–7) “at least sufficiently prepared” and (1–3) “insufficiently prepared”.
“Topic preparedness scores” and “global preparedness scores” (GPS) were calculated.
The topic preparedness score represents the percentage of medical school students at anindividual medical school who felt at least sufficiently prepared for an individual topic.
The global preparedness score represents the average of the 27 topic preparedness scoresat each medical school. National-level topic preparedness scores and global preparedness
scores were also calculated, with each medical school being weighted equally.
Data were presented as measures of central tendency and measures of spread as well
as absolute and relative frequencies. The Kolmogorov–Smirnov (KS) test was used toassess the normality of distribution. Comparisons between the availability of teaching
methods according to the year of graduation (2015 vs. 2021), the perceived needs for further
education and topic/global preparedness scores were conducted using a chi-square test.
The COVID-19 and teaching methods questions were presented via descriptive statisticalanalyses. Statistical significance was set at p < 0.05.
5. Conclusions
Self-reported preparedness levels in rational antibiotic prescribing fell slightly between
2015 and 2021, but students in Sweden still feel well-prepared compared with students inother European countries, at least according to 2015 levels. Students consistently reported
low levels of preparedness in specific curricula topics, and future improvement efforts
should consider focusing on these areas. COVID-19 likely had at least some negative impacts on teaching about responsible antibiotic prescribing, and the long-term consequencesof these effects deserve follow-up.
More broadly, as all medical schools in Sweden now continue efforts to introduce a
six-year (twelve-term) medical programme, we hope that our results can help stimulate
and facilitate reflection on the content and form of teaching about responsible antibiotic
use. From spring 2027, students will graduate with a full medical licence and, thus, greater
expectations for competence and independence.
Supplementary Materials: The following supporting information can be downloaded at: https://www.
mdpi.com/article/10.3390/antibiotics13040303/s1, Figure S1: Response rate at each medical school,2015 and 2021; Table S1: Differences in global preparedness scores between medical schools, 2015 and2021; Table S2. Absolute percentage change in curriculum preparedness score in 2021 versus 2015 per
medical school. Survey instrument (2021 version).
Author Contributions: Conceptualization, J.A.-N. and O.J.D.; Methodology, J.A.-N. and O.J.D.;
Validation, J.A.-N., D.P., A.B. and O.J.D.; Formal Analysis, J.A.-N. and D.P.; Data Curation, J.A.-N.
and O.J.D.; Writing—Original Draft Preparation, A.B. and O.J.D.; Writing—Review & Editing, J.A.-N.,

Antibiotics 2024, 13, 303

12 of 13

D.P., A.B., O.J.D. and Student-PREPARE Sweden Working Group; Project Administration, O.J.D.
and Student-PREPARE Sweden Working Group. All authors have read and agreed to the publishedversion of the manuscript.
Funding: This research received no external funding.
Institutional Review Board Statement: According to the Swedish Ethical Review Act (SFS 2003:460),
ethical approval was not required for this type of study using anonymous data without patient
involvement.
Informed Consent Statement: Informed consent was obtained from all subjects involved in the
study.
Data Availability Statement: The data presented in this study are available on request from thecorresponding author.
Acknowledgments: The Student-PREPARE Sweden Working Group consisted of Estelle Naumburg(Department of Clinical Sciences, Pediatrics, Umeå University, Umeå, Sweden), Mikael Hasselgren(School of Medical Sciences, Faculty of Medicine and Health, Örebro University, Örebro, Sweden;
Centre for Clinical Research and Education, Region Värmland, Karlstad, Sweden) and Veronica Milos
Nymberg (Department of Clinical Sciences, Malmö, Lund University Sweden; Center for Primary
Health Care Research, Malmö, Sweden). We thank all students who participated in the study and all
medical school coordinators for their efforts in conducting the study.
Conflicts of Interest: The authors declare no conflicts of interest.

References
1.
2.

3.
4.

5.

6.
7.
8.

9.

10.

11.
12.
13.
14.

Maxwell, S.R.; Cascorbi, I.; Orme, M.; Webb, D.J. Educating European (junior) doctors for safe prescribing. Basic Clin. Pharmacol.
Toxicol. 2007, 101, 395–400. [CrossRef] [PubMed]
Brinkman, D.J.; Tichelaar, J.; Schutte, T.; Benemei, S.; Böttiger, Y.; Chamontin, B.; Christiaens, T.; Likic, R.; Maˇiulaitis, R.; Marandi,T.; et al. Essential competencies in prescribing: A first European cross-sectional study among 895 final-year medical students.
Clin. Pharmacol. Ther. 2017, 101, 281–289. [CrossRef] [PubMed]
Brinkman, D.J.; Tichelaar, J.; Graaf, S.; Otten, R.H.J.; Richir, M.C.; van Agtmael, M.A. Do final-year medical students havesufficient prescribing competencies? A systematic literature review. Br. J. Clin. Pharmacol. 2018, 84, 615–635. [CrossRef]
Dyar, O.J.; Nathwani, D.; Monnet, D.L.; Gyssens, I.C.; Stålsby Lundborg, C.; Pulcini, C.; Wechsler-Fördös, A.; Kostyanev, T.;
Vlahović-Palčevski, V.; Kolar, M.; et al. Do medical students feel prepared to prescribe antibiotics responsibly? Results from across-sectional survey in 29 European countries. J. Antimicrob. Chemother. 2018, 73, 2236–2242. [CrossRef] [PubMed]
Vázquez-Lago, J.M.; Montes-Villalba, R.A.; Vázquez-Cancela, O.; Otero-Santiago, M.; López-Durán, A.; Figueiras, A. Knowledge,
Perceptions, and Perspectives of Medical Students Regarding the Use of Antibiotics and Antibiotic Resistance: A Qualitative
Research in Galicia, Spain. Antibiotics 2023, 12, 558. [CrossRef] [PubMed]
Palčevski, D.; Belančić, A.; Mikuličić, I.; Oštarijaš, E.; Likić, R.; Dyar, O.; Vlahović-Palčevski, V. Antimicrobial Prescribing
Preparedness of Croatian Medical Students—Did It Change between 2015 and 2019? Medicines 2023, 10, 39. [CrossRef]
Ferri, M.; Ranucci, E.; Romagnoli, P.; Giaccone, V. Antimicrobial resistance: A global emerging threat to public health systems.
Crit. Rev. Food Sci. Nutr. 2017, 57, 2857–2876. [CrossRef]
Cassini, A.; Högberg, L.D.; Plachouras, D.; Quattrocchi, A.; Hoxha, A.; Simonsen, G.S.; Colomb-Cotinat, M.; Kretzschmar,
M.E.; Devleesschauwer, B.; Cecchini, C.; et al. Attributable deaths and disability-adjusted life-years caused by infections with
antibiotic-resistant bacteria in the EU and the European Economic Area in 2015: A population-level modelling analysis. Lancet
Infect. Dis. 2019, 19, 56–66. [CrossRef]
European Centre for Disease Prevention and Control. Antimicrobial Consumption in the EU/EEA (ESAC-Net)—Annual
Epidemiological Report for 2021. Available online: https://www.ecdc.europa.eu/en/publications-data/surveillanceantimicrobialconsumption-europe-2021 (accessed on 12 February 2024).
2022 WHO Regional Office for Europe/European Centre for Disease Prevention and Control. Antimicrobial Resistance
Surveillance in Europe 2022–2020 Data. Available online: https://www.ecdc.europa.eu/en/publications-data/antimicrobialresistancesurveillance-europe-2022-2020-data (accessed on 12 February 2024).
Dyar, O.J.; Huttner, B.; Schouten, J.; Pulcini, C.; ESGAP (ESCMID Study Group for Antimicrobial stewardshiP). What is
antimicrobial stewardship? Clin. Microbiol. Infect. 2017, 23, 793–798. [CrossRef]
Davey, P.; Marwick, C.A.; Scott, C.L.; Charani, E.; McNeil, K.; Brown, E.; Gould, I.M.; Ramsay, C.R.; Michie, S. Interventions toimprove antibiotic prescribing practices for hospital inpatients. Cochrane Database Syst. Rev. 2017, 2, CD003543. [CrossRef]
Pulcini, C.; Gyssens, I.C. How to educate prescribers in antimicrobial stewardship practices. Virulence 2013, 4, 192–202. [CrossRef][PubMed]WHO. Global Action Plan on Antimicrobial Resistance. 2015. Available online: https://www.who.int/publications/i/item/9789
241509763 (accessed on 12 February 2024).

Antibiotics 2024, 13, 303

15.

16.

17.

18.

19.

20.
21.
22.
23.

24.
25.
26.

13 of 13

Mölstad, S.; Erntell, M.; Hanberger, H.; Melander, E.; Norman, C.; Skoog, G.; Lundborg, C.S.; Söderström, A.; Torell, E.; Cars, O.
Sustained reduction of antibiotic use and low bacterial resistance: 10-year follow-up of the Swedish Strama programme. Lancet
Infect. Dis. 2008, 8, 125–132. [CrossRef]
Government Offices of Sweden. Swedish Strategy to Combat Antibiotic Resistance. 2016. Available online: https://www.vr.se/
download/18.19df7fb916622e206d81e5/1538575613387/Swedish-strategy-to-combat-antibiotic-resistance.pdf (accessed on 5
March 2024).
Pulcini, C.; Wencker, F.; Frimodt-Møller, N.; Kern, W.V.; Nathwani, D.; Rodríguez-Baño, J.; Simonsen, G.S.; Vlahović-Palčevski,
V.; Gyssens, I.C.; Gyssens, I.; et al. European survey on principles of prudent antibiotic prescribing teaching in undergraduate
students. Clin. Microbiol. Infect. 2015, 21, 354–361. [CrossRef]
Dyar, O.J.; Lund, M.; Lindsjö, C.; Stålsby Lundborg, C.; Pulcini, C. Preparedness to prescribe antibiotics responsibly: A comparison
between final year medical students in France and Sweden. Eur. J. Clin. Microbiol. Infect. Dis. 2019, 38, 711–717. [CrossRef][PubMed]Abbo, L.M.; Cosgrove, S.E.; Pottinger, P.S.; Pereyra, M.; Sinkowitz-Cochran, R.; Srinivasan, A.; Webb, D.J.; Hooton, T.M. Medical
students’ perceptions and knowledge about antimicrobial stewardship: How are we educating our future prescribers. Clin. Infect.
Dis. 2013, 57, 631–638. [CrossRef]
Rose, S. Medical Student Education in the Time of COVID-19. JAMA 2020, 323, 2131–2132. [CrossRef] [PubMed]
Singh, K.; Srivastav, S.; Bhardwaj, A.; Dixit, A.; Misra, S. Medical Education During the COVID-19 Pandemic: A Single Institution
Experience. Indian Pediatr. 2020, 57, 678–679. [CrossRef]
Theoret, C.; Ming, X. Our education, our concerns: The impact on medical student education of COVID-19. Med. Educ. 2020, 54,
591–592. [CrossRef]
Schouten, J.; De Waele, J.; Lanckohr, C.; Koulenti, D.; Haddad, N.; Rizk, N.; Sjövall, F.; Kanj, S.S.; Alliance for the Prudent Use of
Antibiotics. Antimicrobial stewardship in the ICU in COVID-19 times: The known unknowns. Int. J. Antimicrob. Agents 2021, 58,
106409. [CrossRef]
Malli, I.A.; Mohamud, M.S.; Al-Nasser, S. Enhancing Medical Students’ Confidence and Knowledge in Antibiotic Prescription
and Administration through Virtual Education: A Quasi-Experimental Study. Antibiotics 2023, 12, 1546. [CrossRef]
Shahrvini, B.; Baxter, S.L.; Coffey, C.S.; MacDonald, B.V.; Lander, L. Pre-clinical remote undergraduate medical education during
the COVID-19 pandemic: A survey study. BMC Med. Educ. 2021, 21, 13. [CrossRef] [PubMed]
Biggs, J.; Tang, C. Teaching for Quality Learning at University, 4th ed.; Open University Press: Maidenhead, UK, 2011.

Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual
author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury topeople or property resulting from any ideas, methods, instructions or products referred to in the content.