BMJ Open€¦ · Touboul, Pia; Hopital de l'Archet, Département de Santé Publique; Universite de Nice Sophia Antipolis, Department of Teaching and Research in General Practice Aldigs,

For peer review only

Attitudes and behaviours of adolescents towards antibiotics

and self-care for respiratory tract infections: A qualitative

study.

Journal: BMJ Open

Manuscript ID bmjopen-2016-015308

Article Type: Research

Date Submitted by the Author: 24-Nov-2016

Complete List of Authors: Hawking, Meredith; Public Health England, Primary Care Unit; Barts and The London School of Medicine and Dentistry, Centre for Primary Care and Public Health Lecky, Donna; Public Health England, Primary Care Unit Touboul, Pia; Hopital de l'Archet, Département de Santé Publique; Universite de Nice Sophia Antipolis, Department of Teaching and Research in General Practice Aldigs, Eman; King Abdulaziz University, Medical Microbiology and Parasitology Dept., College Of Medicine Abdulmajed, Hind; King Abdulaziz University, Medical Microbiology and Parasitology Dept., College Of Medicine Hadjichambi, Demetra; Government of the Republic of Cyprus Ministry of Education and Culture Ioannidou, Eleni; Cyprus Centre for Environmental Research and Education, CYCERE Khouri, Pauline; Hopital de l'Archet, Département de Santé Publique; Universite de Nice Sophia Antipolis, France and Department of Teaching and Research in General Practice Gal, Micaela; Cardiff University School of Medicine, Department of Population Medicine Hadjichambis, Andreas; Cyprus Center for Environmental Research and Education – CYCERE – KYKPEE Mappouras, Demetrios; Government of the Republic of Cyprus Ministry of Education and Culture McNulty, Cliodna; Public Health England, Primary Care Unit

<b>Primary Subject Heading</b>:

Qualitative research

Secondary Subject Heading: Public health, Infectious diseases, General practice / Family practice

Keywords: interview, focus group, student, perceptions, antimicrobial resistance, international

For peer review only - http://bmjopen.bmj.com/site/about/guidelines.xhtml

BMJ Open on M

arch 25, 2021 by guest. Protected by copyright.

http://bmjopen.bm

j.com/

BM

J Open: first published as 10.1136/bm

jopen-2016-015308 on 6 June 2017. Dow

nloaded from

http://bmjopen.bmj.com/


Page 1 of 31


BMJ Open

123456789101112131415161718192021222324252627282930313233343536373839404142434445464748495051525354555657585960

on March 25, 2021 by guest. P

rotected by copyright.http://bm

jopen.bmj.com

/B

MJ O

pen: first published as 10.1136/bmjopen-2016-015308 on 6 June 2017. D

ownloaded from



1

Attitudes and behaviours of adolescents towards antibiotics and self-care for

respiratory tract infections: A qualitative study.

Meredith K.D. Hawking, MPH. Public Health England Primary Care Unit, Microbiology

Department, Gloucestershire Royal Hospital, Great Western Road, Gloucester GL1 3NN,

UK, [email protected]

Donna M. Lecky, PhD. Public Health England Primary Care Unit, Microbiology Department,

Gloucestershire Royal Hospital, Great Western Road, Gloucester GL1 3NN, UK,

[email protected]

Pia Touboul Lundgren, MD. Département de Santé Publique, Hôpital de l'Archet 1, 151, rte

St Antoine de Ginestière CS 23079, 06202 Nice Cedex 3, France and Department of

Teaching and Research in General Practice, University of Nice Sophia Antipolis, 28 Avenue

de Valombrose, 06107 Nice, France. [email protected]

Eman Aldigs, Medical Microbiology and Parasitology Dept., College Of Medicine, King

Abdulaziz University, Jeddah, Saudi Arabia. [email protected]

Hind Abdulmajed, Medical Microbiology and Parasitology Dept., College Of Medicine, King


Demetra Hadjichambi, Ministry of Education and Culture, Nicosia, Cyprus.

[email protected]

Eleni Ioannidou, 5Cyprus Centre for Environmental Research and Education, CYCERE,

Limassol, Cyprus. [email protected]

Pauline Khouri, MD. Département de Santé Publique, Hôpital de l'Archet 1, 151, rte St

Antoine de Ginestière CS 23079, 06202 Nice Cedex 3, France and Department of Teaching

and Research in General Practice, University of Nice Sophia Antipolis, 28 Avenue de

Valombrose, 06107 Nice, France. [email protected]

Micaela Gal, PHD. Department of Population Medicine, Cardiff University School of

Medicine, Cardiff, CF14 4YS, UK. [email protected]

Page 2 of 31


BMJ Open

123456789101112131415161718192021222324252627282930313233343536373839404142434445464748495051525354555657585960



jopen.bmj.com

/B

MJ O


ownloaded from



2

Andreas Ch. Hadjichambis, Cyprus Center for Environmental Research and Education –

CYCERE – KYKPEE. [email protected]

Demetrios Mappouras, Ministry of Education and Culture, Nicosia, Cyprus.

[email protected]

Cliodna A.M. McNulty, FRC Pathol. Public Health England Primary Care Unit, Microbiology


UK. [email protected]

*Corresponding author: Dr Donna Lecky Tel: +44 7775 113509; Fax: +44-1452-526197;

Email: [email protected]

Word Count: 3,590

Page 3 of 31


BMJ Open

123456789101112131415161718192021222324252627282930313233343536373839404142434445464748495051525354555657585960



jopen.bmj.com

/B

MJ O


ownloaded from



3

Abstract

Background: To understand attitudes and behaviours of adolescents towards antibiotics,

antimicrobial resistance (AMR) and respiratory tract infections (RTIs).

Design: Thematic analysis of semi-structured interviews and focus groups informed by the

Theory of Planned Behaviour. We aimed to inform the development of a behaviour change

intervention in an international setting to improve antibiotic use amongst adolescents,

therefore on completion of analysis, findings were triangulated with qualitative data from

similar studies in France, Saudi Arabia and Cyprus to elucidate differences in the behaviour

change model and adaptation to diverse contexts.

Setting: 7 educational establishments from the South of England.

Participants: 53 adolescents (16-18 years) participated in 7 focus groups, and 21

participated in interviews.

Results: Most participants had taken antibiotics and likened them to other common

medications such as painkillers; they reported that their peers treat antibiotics like a ‘cure-all’

and that they themselves were not interested in antibiotics as a discussion topic. They

demonstrated low knowledge of the difference between viral and bacterial infections.

Participants self-cared for colds and flu but believed antibiotics are required to treat other

RTIs such as tonsillitis, which they perceived as more ‘serious’. Past history of taking

antibiotics for RTIs instilled the belief that antibiotics were required for future RTIs.

Those who characterised themselves as ‘non-science students’ were less informed about

antibiotics and AMR. Most participants felt that AMR was irrelevant to them and their peers.

Some ‘non-science’ students thought resistance was a property of the body, rather than

bacteria.

Conclusions: Addressing adolescents’ misperceptions about antibiotics and the treatment

of RTIs using a behaviour change intervention should help improve antibiotic awareness and

may break the cycle of patient demand for antibiotics to treat RTIs amongst this group.

Page 4 of 31


BMJ Open

123456789101112131415161718192021222324252627282930313233343536373839404142434445464748495051525354555657585960



jopen.bmj.com

/B

MJ O


ownloaded from



4

Schools should consider educating all students in further education about antibiotic usage

and AMR, not only those taking science.

Key words: interview, focus group, student, perceptions, antimicrobial resistance,

international

Funding: This work was supported by an internal grant through the Public Health England

(PHE) Development Bid Fund.

Strengths and Limitations of this Study

• The use of focus groups gave researchers insight into peer group interaction and

shared viewpoints, whereas interviews allowed participants to share personal views

more freely in a private setting.

• Triangulation of the data from this study against similar studies in other countries

confirms the transferability of the findings to other settings.

• Recruitment of participants from non-healthcare settings provides insight into views

and behaviours amongst healthy adolescents.

• Although schools were chosen to maximise diversity, researchers could only

influence the selection of participants within educational establishments by providing

guidelines and a sampling matrix to educators.

• Adolescents not enrolled in education were not included in the study and further

research would be required to explore perceptions amongst this group.

Page 5 of 31


BMJ Open

123456789101112131415161718192021222324252627282930313233343536373839404142434445464748495051525354555657585960



jopen.bmj.com

/B

MJ O


ownloaded from



5

Background

The increase in antimicrobial resistance (AMR) has the potential for devastating impact on

public health and the provision of health care worldwide. There are an estimated 25,000

deaths per year in Europe from antibiotic-resistant bacterial infections.[1] The majority of

antibiotics are prescribed in primary care, and much of this prescribing is for self-limiting

upper respiratory tract infections (URTIs)[2] for which antibiotics are often unnecessary,[3]

with individuals more likely to develop bacterial resistance to that antibiotic after use.[4]

Moreover, patient expectation for antibiotics in primary care is linked to higher prescribing.[5

6] Therefore, the World Health Organisation has stressed the need to raise awareness of the

responsible use of antibiotics and the threat of AMR amongst the general public.[7]

However, in spite of numerous interventions targeting the public and healthcare

professionals, antibiotic use is increasing worldwide.[8]

A large European survey has shown that 15-24 year olds are the highest users of antibiotics

and are more likely than other age groups to take them for URTIs.[9] In addition, research in

the UK found that younger members (15-34 years) of the general public have lower

knowledge around antibiotics, AMR, and how to care for self-limiting infections than older

groups.[10] Qualitative research undertaken in healthcare settings has investigated patient

perceptions of antibiotics of those over 18 years of age,[11-13] and parental perceptions of

RTIs and antibiotics in regards to their children.[14 15] However to date, older adolescents

have attracted less attention from qualitative researchers as a unique group of participants.

These older adolescents (16-18 years) may be a distinct group of antibiotic users for

investigation - unlike younger children, they may be in control of their own medicines,[16]

and responsible for their use. Adolescents are keen to distance themselves from their

parental influence and create their own self-image,[17] so parents may play a limited role in

the day to day management of medications for common infections such as RTIs. However,

as adolescents become more independent, their health related behaviour may be governed

Page 6 of 31


BMJ Open

123456789101112131415161718192021222324252627282930313233343536373839404142434445464748495051525354555657585960



jopen.bmj.com

/B

MJ O


ownloaded from



6

by social norms influenced by their peers, parents and educators. We decided to investigate

this complex behavioural picture amongst 16-18 year olds as they are in education and

therefore school-based, targeted interventions might be an effective strategy to increase

appropriate antibiotic use.

Behavioural interventions have been shown to be effective at improving antibiotic-related

behaviour amongst parents consulting on behalf of their children for RTIs,[18] but there is

little research on interventions targeting adolescents. In order to be successful, any

intervention must be theoretically driven, evidence based and adapted to the local context.

Qualitative inquiry provides a robust methodology for exploring the complex views and

behaviours of this target group. Furthermore, we aimed to triangulate the findings of this

study with country partners of the e-Bug school educational project to inform transferability of

the findings to other settings. e-Bug is a publicly funded international collaborative public

health project which aims to improve school students’ knowledge and behaviours towards

antibiotics and vaccinations.[19]

Page 7 of 31


BMJ Open

123456789101112131415161718192021222324252627282930313233343536373839404142434445464748495051525354555657585960



jopen.bmj.com

/B

MJ O


ownloaded from



7

Methods

Study Design

We conducted in-depth, semi-structured interviews with older adolescents (16-18 years) in

both an individual interview and focus group setting at educational establishments in the

South of England. The Theory of Planned Behaviour (TPB)[20] was used as a theoretical

basis for the topic guide to ensure the topics raised covered multiple factors that influence

behaviour. The TPB aims to predict and explain human behaviour in specific contexts, and

identifies intention as the central factor to performance of a specific behaviour. The TPB

suggests that individuals are more likely to intend to perform a behaviour (use antibiotics

appropriately) if they have a positive attitude towards it, perceive social pressure from others

to perform the behaviour (subjective norms), and perceive that the performance of the

behaviour is within their control (perceived behavioural control). Exploration of these

constructs and the data that results provides a practical basis for the development of an

intervention to change attitudes, norms and behavioural intention.

Setting and Participants

A two-stage purposive sampling technique was used to recruit schools and colleges (Figure

1). All registered educational establishments teaching 16-18 year olds in Gloucestershire

were invited to participate by letter and telephone. Additionally, all education establishments

serving 16-18 year olds on the e-Bug mailing list were invited in order to geographically

widen the sampling area, and include establishments based in areas with differing levels of

deprivation. Participating establishments were also selected to represent different school

and college types, selection policies and governance structures. An educator was identified

as the ‘study coordinator’ in each school, and was given written guidelines to inform their

selection of participants: 16-18 year old adolescents were purposively sampled according to

gender and area with the aid of a sampling matrix, aiming to achieve a diverse population

Page 8 of 31


BMJ Open

123456789101112131415161718192021222324252627282930313233343536373839404142434445464748495051525354555657585960



jopen.bmj.com

/B

MJ O


ownloaded from



8

and range of views. Informed written consent was obtained from all participating schools and

adolescents, and parents could refuse child inclusion via ‘opt-out’ forms.

Data collection

The semi-structured topic guide was piloted with five participants and reviewed by the

research team prior to data collection commencement. It included open questions and follow

up probes to elucidate views on antibiotics, AMR and RTIs (Table 1). Care was taken to

ensure that it did not constrain discussions, and allowed new topics to emerge.

Interviews and focus groups were held between March and July 2013 in a private classroom

or school office. Data collection was undertaken by trained, experienced female qualitative

researchers (MH and DL) who were currently employed by the e-Bug project. Interviewers

introduced themselves as researchers working for Public Health England and e-Bug, with an

interest in participants’ views on antibiotics. Interviews and focus groups began with

confirmation that it was not a test of knowledge and participants were assured anonymity

and confidentiality. Educators oversaw organisation and introductions, but were not present

during data collection sessions. Researchers had no previous contact with the participants

prior to the interview or focus group.

Table 1: Topic Guide

Topic Probes

History of taking antibiotics General experience

Perceptions of antibiotics Usage, positives, negatives

Management of colds/flu Self-care, use of medications

Consulting for RTIs Decision to consult, advice, expectations

Others’ views on antibiotics Friends, parents, teachers, media

Antibiotic resistance (AMR) Knowledge, importance, responsibility

Others’ views on AMR Friends, parents, teachers, media

Page 9 of 31


BMJ Open

123456789101112131415161718192021222324252627282930313233343536373839404142434445464748495051525354555657585960



jopen.bmj.com

/B

MJ O


ownloaded from



9

Sources of information Friends, family, media, school, others

Individual interviews lasted 20 - 40 minutes. Focus groups ran for one hour and usually

consisted of between of 5 and 10 participants. Care was taken to allow and encourage all

participants to express their views. Field notes made after each session included

impressions and additional topics that had emerged during data collection. Sessions were

audio recorded, pseudo-anonymised, and transcribed verbatim. Interviews progressed until

theoretical data saturation had occurred and no new themes were arising, after discussion

and agreement within the research team. All data was encrypted, stored and handled

according data protection regulations. There was no financial reward for establishments or

participants; students who took part received a certificate. Repeat interviews were not

undertaken and transcripts were not returned to participants for comment.

Data Analysis and Interpretation

Inductive thematic analysis of the data was undertaken in six stages, as outlined below.[21]

Due to the unbalance of gender in our sample, data was analysed according to gender and

then combined when the themes were found to be common to both female and male

participants. First the transcripts were read by researchers for accuracy, familiarisation and

immersion, then a subset (10%) was annotated with codes by MH and DL. Initial codes were

then discussed with all researchers to resolve any discrepancies. All codes were derived

from the data and a coding schedule was developed for common coding between

researchers. Care was taken not to lose the context of a code by coding too narrowly. Codes

were then grouped into related categories and sorted into a draft framework of six main

themes, which was discussed and agreed between all researchers. Themes were revised

iteratively as the fieldwork and analysis progressed.[21] Use of NVivo software (version 10)

facilitated data organisation. Once coding was complete, the one sheet of paper (OSOP)

method was used to clarify findings within, and between, themes.[22] Finally the results were

Page 10 of 31


BMJ Open

123456789101112131415161718192021222324252627282930313233343536373839404142434445464748495051525354555657585960



jopen.bmj.com

/B

MJ O


ownloaded from



10

collated and summarised, where links between the themes were reviewed and finalised, and

characteristic quotes identified to illuminate the data.

Triangulation

On analysis completion, we triangulated the study findings with qualitative data derived using

the same topic guide (translated and adapted) from similar adolescent (15-18 years)

samples, in e-Bug partner countries (France, Saudi Arabia and Cyprus). The aim was to

shed light on our findings and to assess their transferability across differing contexts. These

countries represent the most diverse range of healthcare systems, antibiotic provision and

usage across the e-Bug partner countries, and we used this approach to inform and assess

the need for country specific adaptations to any potential behavioural intervention. For more

detailed information about the samples and methods these countries used, please see

supplementary file 1.

Results

Final Sample

74 adolescents took part in the study at seven educational establishments in three counties

(Berkshire, Gloucestershire and Essex) in the South of England; 53 participated in seven

focus groups, and 21 were interviewed (Table 2). 24% of participants were male, and 76%

were female. Three of the educational establishments were in rural locales, and four in urban

settings, with average district deprivation index levels ranging from 10.9 to 22.9.[23]

Participants were recruited from three further education colleges and four sixth form schools,

including one Local Education Authority-controlled comprehensive, two comprehensive

academies, and one selective academy. After giving consent, 3 students dropped out due to

illness absence on the day of the interviews, meaning that one focus group only had 3

members.

Page 11 of 31


BMJ Open

123456789101112131415161718192021222324252627282930313233343536373839404142434445464748495051525354555657585960



jopen.bmj.com

/B

MJ O


ownloaded from



11

Table 2: Sample characteristics

Interviews Focus

Groups

Total

n % n % n %

Gender

Female 14 66 42 79 56 76

Male 7 33 11 21 18 24

Subject under study

Biology/ Science 7 33 12 22 19 26

Health and Social Care 8 38 21 40 29 39

All other subjects 6 29 20 38 26 35

School Type

Further Education College 8 38 21 40 29 39

Sixth Form 13 62 32 60 45 61

Location

Rural 6 29 25 47 31 41

Urban 15 71 28 53 43 58

Main findings

Understanding and perceptions of antibiotics

The majority of adolescents had previously taken antibiotics and believed them to be

effective for treating infections. Some expressed positive views on antibiotics.

“C1FG1, F1: It just feels like you’re doing something to make yourself better. So if you’re put

on antibiotics it’s like you’re near the end of whatever’s wrong with you”.

Page 12 of 31


BMJ Open

123456789101112131415161718192021222324252627282930313233343536373839404142434445464748495051525354555657585960



jopen.bmj.com

/B

MJ O


ownloaded from



12

Most participants did not perceive antibiotics to be specifically for bacterial infections and

some of the sample felt they were no different from other medications such as painkillers,

and talked in general terms about medications when they had been asked about antibiotics.

Some participants described avoiding antibiotics, and painkillers, because they were

concerned that they would become reliant on them, or felt that they were harmful.

“C7IS3M: It's like a subconscious thing that you always think it's going to be slightly harmful

if you take it [antibiotic].”

"C5IS2F: I try not to rely on painkillers and tablets because I feel like my body is going to get

used them and then it just won’t be able to get better on its own."

A small minority of participants directly confused painkillers and antibiotics, or weren’t quite

sure of the difference between these two groups of medicines.

“C3IS1F: Is that when you go to the doctors they give you antibiotics? It’s paracetamol. Is

paracetamol an antibiotic?”

“C3FG3, F2: Like what are antibiotics? [laugh] ‘cause I know I've taken like paracetamol and

things, I know that’s not antibiotics is it?”

There was some misunderstanding about the difference between viral and bacterial

infections, and those who were aware of the distinction were mostly science students.

“C5IS3F (non-science student): Because you go to doctors and you feel like, oh you have

got a sore throat, earache, whatever and they’re like oh it’s a virus, so you get nothing and

you go out and it’s just like ‘oh it’s a virus again’ but I didn’t know the difference between a

virus and an infection.”

Page 13 of 31


BMJ Open

123456789101112131415161718192021222324252627282930313233343536373839404142434445464748495051525354555657585960



jopen.bmj.com

/B

MJ O


ownloaded from



13

“C7IS2M (science student): I recently spent my work experience, a week at a GPs, and the

amount of people who came in asking for antibiotics, it's remarkable! And a lot of the time, it

was a viral infection, so they didn’t need them”.

Perceptions and treatment of respiratory tract infections (RTIs)

Adolescents grouped different types of uncomplicated RTIs according to their perceived

severity. Colds and flu were seen as simple infections that could be treated at home with

‘natural’ remedies such as honey, taking comfort measures such as drinking hot drinks and

resting, or over the counter medications such as painkillers. GP consultations would only be

considered if symptoms persisted or were more serious than their normal cold symptoms. A

few adolescents indicated that they would expect antibiotics in this case, especially if they

had taken them for the same kind of illness before.

“C2IS3F: I know I had the illness, I know what it feels like and I know taking antibiotics is

important because I won’t get it again, well hopefully”.

Other expectations were to receive a clear diagnosis, reassurance and advice from their

doctor. RTIs such as tonsillitis and sinusitis were seen as more serious infections that

required clinical intervention and would require antibiotics. A few adolescents attributed

feeling better during past RTI illnesses to the antibiotic treatment they took, and therefore

believed that antibiotics are an effective treatment for RTIs, as exemplified by the following

participant:

“C5IS1F: This was a sinus infection. The doctor didn’t, he said that it might help, because it

was like viral or bacterial and stuff like that, which I do not really know about. I think if it is

viral you are not supposed to have antibiotics and he wasn’t sure whether it was viral or

Page 14 of 31


BMJ Open

123456789101112131415161718192021222324252627282930313233343536373839404142434445464748495051525354555657585960



jopen.bmj.com

/B

MJ O


ownloaded from



14

bacterial so he gave me antibiotics. After the first week I was still not better, but then after

the second week I was better, so taking them must work.”

Perceptions on parents and peers

Most participants thought that their peers take a lot of antibiotics and treat them as a quick

fix, a ‘cure-all’, like painkillers.

“C2IS1M: They just think it’s just like any other medicine that they are taking”.

Most adolescents felt that their peers do not think about, discuss or worry about AMR, or feel

it is relevant to their age group. Antibiotics were not a popular or priority topic of discussion

in their peer group.

“C4IS4F: It’s [antibiotics] not something that you talk about, if that makes sense, [laughter]

don’t just strike up a conversation about it, we just don’t.”

Parents were described as having an advisory role, either by ensuring they were used ‘only

when necessary’, or were occasionally reported as encouraging use.

“C3IS2F: My parents just think they’re a means to an end really I suppose, they’re to be

used when necessary”.

Some participants reported feeling that their parents were less knowledgeable about

antibiotics than themselves.

Page 15 of 31


BMJ Open

123456789101112131415161718192021222324252627282930313233343536373839404142434445464748495051525354555657585960



jopen.bmj.com

/B

MJ O


ownloaded from



15

“C7IS1M: They're not the smartest people [slight laugh] so they just think ‘if you just take

them [antibiotics] you’ll feel fine’, I mean, ‘I've taken them I feel fine’. So it's just trying to

explain that to them”.

Antimicrobial resistance (AMR)

In general, the majority of adolescents had poor understanding of AMR. A small minority of

students in the individual interviews did not know what the term ‘antibiotic resistance’ meant

- one interviewee thought that antibiotic resistance referred to “people against antibiotics”.

With the exception of those who characterised themselves as ‘science students’, many

thought that the ‘body or person becomes resistant’ to antibiotics, as exemplified by the

following excerpts.

“C1IS3F: I suppose if you really had, a really serious illness and then you couldn’t treat it,

because you’re immune to one of the tablets, then it could have an effect.”

“C2IS2M: Isn’t that where your body gets, what’s it called? um, too used to antibiotics so that

they no longer work."

However, despite this lack of knowledge, after prompting, some of those who had incorrect

understanding or had not heard of AMR went on to display basic knowledge of resistance in

non-scientific terms, such as: ‘antibiotics might not work for you next time you take them if

you haven’t taken them properly’, or ‘overuse of antibiotics means that they may not work in

the future’. In contrast, students who demonstrated more knowledge of AMR, mostly science

students, felt that it was an important issue and awareness should be increased amongst the

general public, as these quotes demonstrate:

Page 16 of 31


BMJ Open

123456789101112131415161718192021222324252627282930313233343536373839404142434445464748495051525354555657585960



jopen.bmj.com

/B

MJ O


ownloaded from



16

“C3IS2F: I think that’s [antibiotic resistance] going to be increasingly important. If we’re

creating more resistant bacteria we’re going to have to try and make new antibiotics, and

what do we do when we can’t really do anything else?”

“C7IS2M: Sooner or later we’re going to run out of antibiotics that work, and it's going to

take a lot of time and a lot of money to find new ones. And it's probably inevitable, but it

could be slowed, that8 if people aren’t aware of antibiotic resistance then that situation may

come faster.”

Some participants expressed the view that it is the GP’s responsibility to prescribe

appropriately and monitor antibiotic usage, and it is not their concern.

“C1FG1, F2: I don’t really worry about it, because I think the doctor knows if they’re going to

give it to you whether it’s going to slightly become resistant. [8] I think they’ll monitor how

much you have. I don’t think we have to worry about it ourselves, the patients.”

Results - comparison between countries

Our findings aligned with the main findings from the Cypriot, French and Saudi Arabian

samples, with a few exceptions. Interviewed adolescents in the UK, Saudi Arabia and

France confused painkillers and antibiotics, however this was not the case with participants

in Cyprus. Adolescents from Saudi Arabia and Cyprus reported obtaining antibiotics over the

counter without a prescription, and this was seen as a very common behaviour amongst

peers, however this is not possible in the UK or France. As with English participants,

previous use of antibiotics in Cyprus and Saudi Arabia lead to an increased expectation for

antibiotics for RTIs. The easy accessibility of antibiotics over the counter in these countries

seemed to increase this effect – antibiotics were described as ‘candies’ and used for a

variety of reported symptoms. Finally, like in the UK, parents had an influence over antibiotic

taking behaviour. This was particularly prominent in Saudi Arabia, where parents more

commonly encouraged the use of antibiotics in contrast to the UK findings where parents

Page 17 of 31


BMJ Open

123456789101112131415161718192021222324252627282930313233343536373839404142434445464748495051525354555657585960



jopen.bmj.com

/B

MJ O


ownloaded from



17

were mainly described as discouraging use, unless they felt that antibiotics were really

necessary.

Discussion

Statement of principle findings

This study found that, with the exception of some science students, adolescents in

educational establishments in England have low knowledge about antibiotics and AMR, and

do not feel that these topics are important or relevant to themselves or their peer group.

Adolescents are confident to self-care for colds and flu, but think other types of RTIs such as

tonsillitis and sinusitis need antibiotics, a perception that is reinforced by previous

experience of receiving antibiotics for infections. Amongst their peers, they perceive overuse

of antibiotics and a lack of concern about AMR. Parents have an advisory role, acting to limit

or encourage use. Comparison with data from other countries confirms very similar findings,

but greater overuse of antibiotics in countries where they are available ‘over the counter’

without prescription; other countries also had differing levels of parental influence.

Strengths and Limitations of this study

Our final sample was large, with participants from a diverse selection of schools and areas,

however our sampling strategy did result in an unequal gender balance, with more females

taking part. It may be that males were less likely to volunteer, or the study format was more

attractive to females. Selection of participants was governed by the study coordinator

(usually an educator) in the school, which we were not able to control, however

establishments were selected carefully to represent different educational types, deprivation

levels and geographical areas, and study coordinators were provided with guidelines and a

sampling matrix to follow. To assess the impact of gender in the sample, we initially

analysed according to gender and found there were no thematic differences between males

Page 18 of 31


BMJ Open

123456789101112131415161718192021222324252627282930313233343536373839404142434445464748495051525354555657585960



jopen.bmj.com

/B

MJ O


ownloaded from



18

and females, and therefore combined the findings, so this may not be an important

drawback. Triangulation of the data against findings from other countries within the e-Bug

project who undertook similar studies allows us to be more confident in the

comprehensiveness and transferability of our findings to other 16-18 year olds in education

in the UK and abroad. Further research is required to understand the views of older

adolescents who are not enrolled in education.

16 – 18 year olds were recruited from schools regardless of their past exposure to antibiotics

or health status making the results of this study more applicable to healthy adolescents in

everyday contexts compared to previous studies that have recruited adult participants from

healthcare settings alone.[11-13] The perceptions and reported behaviours of healthy

adolescents may differ, however, from those who are recruited when they are currently

experiencing an infection, or taking antibiotics. Our use of multiple data collection methods

allowed a comprehensive approach: undertaking individual interviews allowed for more

candid sharing of information and discussion of more personal beliefs and feelings, and gave

quieter students a better chance to voice their views, helping to eliminate difficulties

adolescents can have discussing their health,[24] and concerns about confidentiality.[25 26]

On the other hand, the dynamic interaction of focus groups provided insight into shared

viewpoints and social norms.[27] Care was taken to encourage discussion, by introducing

focus group ‘rules’, distancing the sessions from examination type connotations, and

exclusion of educators from the room.

Comparison to other research

A lack of understanding around the type of infection that antibiotics should be used for has

been shown amongst this age group and others in other countries.[6 9 28-31] In one such

study, 38% believed that antibiotics work against viral infections.[6] We found that young

people believe antibiotics are required to treat what they perceive as ‘serious’ URTI

infections, such as sinus infections and tonsillitis. However, antibiotics have little clinical

Page 19 of 31


BMJ Open

123456789101112131415161718192021222324252627282930313233343536373839404142434445464748495051525354555657585960



jopen.bmj.com

/B

MJ O


ownloaded from



19

benefit in these conditions.[3] Patient expectations for antibiotics within a primary care

consultation have been shown to affect whether or not antibiotics are prescribed [5 6] and

this can have a medicalising effect, leading to greater expectation for antibiotics for future

episodes of similar infections,[5] which was expressed by many of our adolescents.

Research has shown that painkillers are seen as an essentially harmless ‘ordinary, everyday

medicine’ by young teenage women.[32] Young adolescents are often responsible for taking

their own medication, for example in a survey of school students, 22% of 11-13 year olds

reported that they were allowed to use pain medications without asking for permission, and

this increased significantly with age.[16] A lack of understanding between these pain

medications and antibiotics, as demonstrated in our study, may have negative impacts on

antibiotic use of and prescription expectation.

In a recent qualitative study with Swedish teenagers aged 16-19 years, students argued that

the effect of paracetamol declined if it was used too often.[17] This belief is similar to basic

understandings of AMR seen in our study. The perception that resistance is a property of the

body echoes similar qualitative research undertaken with adults recruited from health care

settings.[11-13 33 34]

Adolescents in the study said that they would not discuss antibiotics with their friends, and

did not think the topic of antibiotics or AMR was relevant or interesting to them. Holmström

and colleagues [17] found that Swedish adolescents held similar views about pain

medication: it was considered a ‘non-issue’ and was not discussed. However in other health

related areas peers have been shown to have an influential role.[35]

Implications for clinical practice and policymakers

The perceived need and expectation for antibiotics for the treatment of RTIs by young

people should be taken into account by clinicians when adolescents consult, remembering

that adolescence is a key time for the development of life long health behaviours and

decision making. Provision of reassurance and information about self-care for RTIs [36] has

been shown to be highly satisfactory to patients in this scenario and should therefore be

Page 20 of 31


BMJ Open

123456789101112131415161718192021222324252627282930313233343536373839404142434445464748495051525354555657585960



jopen.bmj.com

/B

MJ O


ownloaded from



20

promoted for this age group. It may be useful to address the differences between painkillers

and antibiotics with adolescent patients to ensure antibiotics are treated appropriately, and to

address any concerns about the body becoming reliant on or resistant to antibiotics.

The lack of concern shown by young people for AMR, unless addressed, could contribute to

irresponsible use of antibiotics and demand for antibiotics when this age group consult. As

the more knowledgeable ‘science’ students in the study believe it is their personal

responsibility to help control AMR, peer to peer interventions that promote interaction

between science students and those not studying science subjects could raise the profile of

antibiotic resistance and situate it as an important and relevant topic for young adults to be

concerned with. According to our study, studying science post 16 years may provide

adolescents with more rounded knowledge about antibiotics and AMR that could influence

their future health related behaviour.

Implications for future research

Our findings demonstrate that there are misperceptions about antibiotics and how to treat

RTIs amongst older adolescents currently enrolled in education in England, which goes

some way to explaining the high reported use of antibiotics amongst this age group seen in

previous research. Further research is required to assess perceptions amongst adolescents

who are not in education to assess transferability of the findings to these groups. As our

study suggests that young adults in educational environments are a good target group for

behavioural interventions, peer to peer education and interaction between those studying

different subject types could be a key target for intervention development and evaluation.

Triangulation with contrasting international contexts demonstrated that a common

intervention model would be relevant. Whilst many perceptions are shared amongst

adolescents in different countries, some country-specific adaptation of any intervention

would be necessary. The e-Bug team have used the findings to develop a behaviour change

intervention for schools and young people. For more information on the development of the

intervention, visit the e-Bug website.[19]

Page 21 of 31


BMJ Open

123456789101112131415161718192021222324252627282930313233343536373839404142434445464748495051525354555657585960



jopen.bmj.com

/B

MJ O


ownloaded from



21

Acknowledgements

A warm thanks to all of the participants and to their educators for their help in facilitating the

study in each school, and to the youth health centre Carrefour Santé Jeunes and General

Council in Nice, France.

Competing Interests

CM leads the e-Bug project development and writes evidence-based antibiotic guidance for

primary care and leads the Royal College of General Practitioners (RCGP) TARGET (Treat

Antibiotics Responsibly, Guidance and Education Tools) antibiotic toolkit development

including a patient leaflet encouraging delayed/back-up prescribing. She is a past member

(2008-16) of the Advisory Committee on Antimicrobial Resistance and Healthcare

Associated Infection (ARHAI). All other authors were involved in the e-Bug project in their

respective countries at the time of the research. The funding body had no role in the design,

execution, analysis or reporting of the research.

Governance

Internal Public Health England review only was required as participants were not recruited

through the National Health Service (NHS) and all UK participants were over 16 years of

age. The Department of Education was consulted and the study was referred to the

Governmental Disclosure and Barring Service (DBS). The study was undertaken in full

accordance with the DBS regulations.

Authors’ contributions

MH was the main researcher, wrote the protocol, recruited schools, interviewed participants

in the UK, coded the data from the UK, Cyprus and Saudi Arabia and led analysis of the data

and writing the manuscript. DL discussed the protocol, supervised the project, interviewed

participants in the UK, double coded the data and edited the manuscript. PTL facilitated the

Page 22 of 31


BMJ Open

123456789101112131415161718192021222324252627282930313233343536373839404142434445464748495051525354555657585960



jopen.bmj.com

/B

MJ O


ownloaded from



22

project in France and coded and analysed the French data with PK who also carried out the

interviews in France. EA and HA facilitated the project in Saudi Arabia, collecting the data

and translated the interviews. DH, AChH and DM facilitated the project in Cyprus, EI

interviewed the participants and organised transcript translation. MG was involved in

protocol development and commented on methodology throughout data collection. CMcN

led the overall project, advising on protocol, methodology, analysis and interpretation. All

authors reviewed and commented on the protocol and the manuscript.

Funding

In the UK this work was supported by an internal grant through the Public Health England

(PHE) Development Bid Fund. There was no specific funding for this study in France,

Cyprus and Saudi Arabia. In France PTL was supported by the Ministry of Health and Nice

University Hospital for coordination of the e-Bug project and PK undertook the research as

part of her medical student thesis. In Cyprus DH and EI were supported by the Ministry of

Education and Culture and the Cyprus Centre for Environmental Research and Education. In

Saudi Arabia EA and HA were supported by King Abdulaziz University.

Data sharing

Please contact Dr Donna Lecky to discuss access to unpublished data from the study.

References

1. European Centre for Disease Control. The bacterial challenge: time to react. . Secondary The bacterial challenge: time to react. 2009. http://www.ecdc.europa.eu/en/publications/Publications/0909_TER_The_Bacterial_Challenge_Time_to_React.pdf.

2. Public Health England. The English Surveillance Programme for Antimicrobial Utilisation and Resistance Report 2014. Secondary The English Surveillance Programme for Antimicrobial Utilisation and Resistance Report 2014 2014. https://www.gov.uk/government/uploads/system/uploads/attachment_data/file/362374/ESPAUR_Report_2014__3_.pdf

3. National Institute for Health and Clinical Excellence. Respiratory tract infections – antibiotic prescribing: Prescribing of antibiotics for self-limiting respiratory tract infections in adults and children in primary care. Secondary Respiratory tract

Page 23 of 31


BMJ Open

123456789101112131415161718192021222324252627282930313233343536373839404142434445464748495051525354555657585960



jopen.bmj.com

/B

MJ O


ownloaded from



23

infections – antibiotic prescribing: Prescribing of antibiotics for self-limiting respiratory tract infections in adults and children in primary care. 2008. http://www.nice.org.uk/nicemedia/live/12015/41323/41323.pdf

4. Costelloe C, Metcalfe C, Lovering A, Mant D, Hay AD. Effect of antibiotic prescribing in primary care on antimicrobial resistance in individual patients: systematic review and meta-analysis. BMJ 2010;340

5. Butler CC, Rollnick S, Pill R, Maggs-Rapport F, Stott N. Understanding the culture of prescribing: qualitative study of general practitioners' and patients' perceptions of antibiotics for sore throats. Bmj 1998;317(7159):637-42

6. McNulty CA, Nichols T, French DP, Joshi P, Butler CC. Expectations for consultations and antibiotics for respiratory tract infection in primary care: the RTI clinical iceberg. Br J Gen Pract 2013;63(612):e429-36 doi: 10.3399/bjgp13X669149[published Online First: Epub Date]|.

7. World Health Organisation. Combating antimicrobial resistance, including antibiotic resistance. Secondary Combating antimicrobial resistance, including antibiotic resistance. 2014. http://apps.who.int/gb/ebwha/pdf_files/EB134/B134_R13-en.pdf.

8. Laxminarayan R, Duse A, Wattal C, et al. Antibiotic resistance—the need for global solutions. The Lancet Infectious Diseases 2013;13(12):1057-98 doi: http://dx.doi.org/10.1016/S1473-3099(13)70318-9[published Online First: Epub Date]|.

9. European Commission. Special Eurobarometer 407: Antimicrobial Resistance. Secondary Special Eurobarometer 407: Antimicrobial Resistance. 2013. http://ec.europa.eu/public_opinion/archives/ebs/ebs_407_en.pdf.

10. McNulty CAM, Lecky DM, Hawking MKD, Roberts C, Quigley A, Butler CC. How much information about antibiotics do people recall after consulting in primary care? Family Practice 2016 doi: 10.1093/fampra/cmw022[published Online First: Epub Date]|.

11. Hawkings NJ, Wood F, Butler CC. Public attitudes towards bacterial resistance: a qualitative study. Journal of Antimicrobial Chemotherapy 2007;59(6):1155-60 doi: 10.1093/jac/dkm103[published Online First: Epub Date]|.

12. Brooks L, Shaw A, Sharp D, Hay AD. Towards a better understanding of patients' perspectives of antibiotic resistance and MRSA: a qualitative study. Family Practice 2008;25(5):341-48 doi: 10.1093/fampra/cmn037[published Online First: Epub Date]|.

13. Brookes-Howell L, Elwyn G, Hood K, et al. 'The body gets used to them': patients' interpretations of antibiotic resistance and the implications for containment strategies. J Gen Intern Med 2012;27(7):766-72 doi: 10.1007/s11606-011-1916-1[published Online First: Epub Date]|.

14. Barden LS, Dowell SF, Schwartz B, Lackey C. Current Attitudes Regarding Use of Antimicrobial Agents: Results from Physicians' and Parents' Focus Group Discussions. Clinical Pediatrics 1998;37(11):665-71 doi: 10.1177/000992289803701104[published Online First: Epub Date]|.

15. Ingram J, Cabral C, Hay AD, Lucas PJ, Horwood J. Parents’ information needs, self-efficacy and influences on consulting for childhood respiratory tract infections: a qualitative study. BMC Family Practice 2013;14(1):1-9 doi: 10.1186/1471-2296-14-106[published Online First: Epub Date]|.

16. Holstein BE, Andersen A, Krølner R, Due P, Hansen EH. Young adolescents' use of medicine for headache: sources of supply, availability and accessibility at home. Pharmacoepidemiology and drug safety 2008;17(4):406-10 doi: 10.1002/pds.1563[published Online First: Epub Date]|.

17. Holmström IK, Bastholm-Rahmner P, Bernsten C, Röing M, Björkman I. Swedish teenagers and over-the-counter analgesics - responsible, casual or careless use. Res Social Adm Pharm 2014;10(2):408-18 doi: 10.1016/j.sapharm.2013.06.004[published Online First: Epub Date]|.

18. Vodicka TA, Thompson M, Lucas P, et al. Reducing antibiotic prescribing for children with respiratory tract infections in primary care: a systematic review. British Journal of General Practice 2013;63(612):e445

Page 24 of 31


BMJ Open

123456789101112131415161718192021222324252627282930313233343536373839404142434445464748495051525354555657585960



jopen.bmj.com

/B

MJ O


ownloaded from



24

19. e-Bug. e-Bug: a place to play games and learn about microbes. Secondary e-Bug: a place to play games and learn about microbes. 2014. www.e-bug.eu.

20. Ajzen I. The Theory of Planned Behavior. Organizational Behavior and Human Decision Processes 1991;50:179-211

21. Braun V, Clarke V. Using thematic analysis in psychology. Qualitative Research in Psychology 2006;3(2):77-101 doi: 10.1191/1478088706qp063oa[published Online First: Epub Date]|.

22. Ziebland S, McPherson A. Making sense of qualitative data analysis: an introduction with illustrations from DIPEx (personal experiences of health and illness). Medical Education 2006;40(5):405-14 doi: 10.1111/j.1365-2929.2006.02467.x[published Online First: Epub Date]|.

23. Department for Communities and Local Government. English indices of deprivation 2015. Secondary English indices of deprivation 2015 2015. https://www.gov.uk/government/statistics/english-indices-of-deprivation-2015.

24. Harvey K, Churchill D, Crawford P, et al. Health communication and adolescents: what do their emails tell us? Family Practice 2008;25(4):304-11 doi: 10.1093/fampra/cmn029[published Online First: Epub Date]|.

25. Churchill R, Allen J, Denman S, Williams D, Fielding K, von Fragstein M. Do the attitudes and beliefs of young teenagers towards general practice influence actual consultation behaviour? The British Journal of General Practice 2000;50(461):953-57

26. Carlisle J, Shickle D, Cork M, McDonagh A. Concerns over confidentiality may deter adolescents from consulting their doctors. A qualitative exploration. Journal of Medical Ethics 2006;32(3):133-37 doi: 10.1136/jme.2004.011262[published Online First: Epub Date]|.

27. Kitzinger J. The methodology of Focus Groups: the importance of interaction between research participants. Sociology of health & illness 1994;16(1):103-21 doi: 10.1111/1467-9566.ep11347023[published Online First: Epub Date]|.

28. McNulty CAM, Boyle P, Nichols T, Clappison P, Davey P. Don't wear me out—the public's knowledge of and attitudes to antibiotic use. Journal of Antimicrobial Chemotherapy 2007;59(4):727-38 doi: 10.1093/jac/dkl558[published Online First: Epub Date]|.

29. Azevedo MM, Pinheiro C, Yaphe J, Baltazar F. Portuguese students' knowledge of antibiotics: a cross-sectional study of secondary school and university students in Braga. BMC Public Health 2009;9:359 doi: 10.1186/1471-2458-9-359[published Online First: Epub Date]|.

30. Huang Y, Gu J, Zhang M, et al. Knowledge, attitude and practice of antibiotics: a questionnaire study among 2500 Chinese students. BMC Med Educ 2013;13:163 doi: 10.1186/1472-6920-13-163[published Online First: Epub Date]|.

31. Cebotarenco N, Bush PJ. Reducing antibiotics for colds and flu: a student-taught program. Health Education Research 2008;23(1):146-57 doi: 10.1093/her/cym008[published Online First: Epub Date]|.

32. Hansen DL, Holstein BE, Hansen EH. “I'd Rather Not Take it, But . . .”: Young Women's Perceptions of Medicines. Qualitative Health Research 2009;19(6):829-39 doi: 10.1177/1049732309335447[published Online First: Epub Date]|.

33. Norris P, Chamberlain K, Dew K, Gabe J, Hodgetts D, Madden H. Public Beliefs about Antibiotics, Infection and Resistance: A Qualitative Study. Antibiotics 2013;2(4):465-76 doi: 10.3390/antibiotics2040465[published Online First: Epub Date]|.

34. Reynolds L, McKee M. Factors influencing antibiotic prescribing in China: an exploratory analysis. Health Policy 2009;90(1):32-6 doi: 10.1016/j.healthpol.2008.09.002[published Online First: Epub Date]|.

35. Maxwell KA. Friends: The Role of Peer Influence Across Adolescent Risk Behaviors. Journal of Youth and Adolescence 2002;31(4):267-77 doi: 10.1023/A:1015493316865[published Online First: Epub Date]|.

Page 25 of 31


BMJ Open

123456789101112131415161718192021222324252627282930313233343536373839404142434445464748495051525354555657585960



jopen.bmj.com

/B

MJ O


ownloaded from



25

36. Welschen I, Kuyvenhoven M, Hoes A, Verheij T. Antibiotics for acute respiratory tract symptoms: patients' expectations, GPs' management and patient satisfaction. Fam Pract 2004;21(3):234-7

Page 26 of 31


BMJ Open

123456789101112131415161718192021222324252627282930313233343536373839404142434445464748495051525354555657585960



jopen.bmj.com

/B

MJ O


ownloaded from



26

Figure 1: Recruitment Flowchart

Invite sent to schools (n=37)

Characteristics of 1st

stage schools

assessed

Unrepresented schools approached

(n=6)

Students invited to take part by teachers

74 Adolescents give consent and are

recruited to the study

Characteristics of adolescents assessed

2nd

stage schools consent to take part

(n=4)

1st

stage schools consent to take part

(n=3)

Page 27 of 31


BMJ Open

123456789101112131415161718192021222324252627282930313233343536373839404142434445464748495051525354555657585960



jopen.bmj.com

/B

MJ O


ownloaded from



Supplementary File 1

Qualitative Data from interviews and focus groups with adolescents in France, Saudi Arabia

and Cyprus collected using similar methods were used to triangulate the findings from the

UK dataset. This file outlines the methodology used in these countries to allow consideration

of any differences between the samples and findings. Country specific details are denoted

by the following abbreviations: France (FR), Saudi Arabia (SA), Cyprus (CY).

Participants and Setting

FR: Adolescents were recruited in Nice via a youth healthcare centre, a facility providing

medical attention and advice for a range of health related issues for young people. 15-18

year old adolescents were approached by and purposively sampled by the research team

according to age, gender, geographic area, socio-economic area and academic pathway.

SA: All registered educational establishments in Jeddah were invited to participate by letter

followed by a telephone call if necessary. A study coordinator was appointed in each school

to identify participating students and provide study information. 15-18 year old adolescents

were purposively sampled according to age, gender, geographic area, socio-economic area

and academic pathway. The female research team were unable to enter male schools.

Therefore, male adolescents were recruited via personal networks through friends and

relatives, ensuring these were from a mix of science and non-science backgrounds.

CY: All registered educational establishments in Limassol, Nicosia, Larnaca and Paphos

were invited to participate by letter followed by a telephone call if necessary. A study

coordinator was appointed in each school to identify participating students and provide study

information. 15-18 year old adolescents were purposively sampled according to age, gender,

geographic area, socio-economic area and academic pathway.

Data collection

All countries used the same topic guide as the one developed for the UK sample, but

adapted it for the local context and to incorporate emerging topics as data collection

commenced. Interviews and focus groups were held between March and July 2013.

Individual face to face interviews typically lasted between 20 and 40 minutes, whilst focus

groups usually ran for one hour. Focus groups consisted of between 4 and 11 participants.

Interviews progressed in each country until theoretical data saturation had occurred, and no

Page 28 of 31


BMJ Open

123456789101112131415161718192021222324252627282930313233343536373839404142434445464748495051525354555657585960



jopen.bmj.com

/B

MJ O


ownloaded from



new themes were emerging from the data, which was judged by discussions within the

research team.

FR: In France the interviews were held in youth health care centres. Focus groups were not

undertaken in France. Interviews were undertaken by a trained interviewer (PK).

SA: School based interviews and focus groups were overseen by educators although the

responsible educator was not present in the school room during the sessions. Interviews and

focus groups were undertaken by trained interviewers (EA, HA).

CY: Interviews in Cyprus were overseen by educators although the responsible educator

was not present in the school room during the sessions. Focus groups were not undertaken

in Cyprus. Interviews were undertaken by a trained interviewer (EI).

Ethical considerations

All participants provided written, informed consent to take part. In schools, parents were

provided with opt out forms. All data was encrypted, anonymised, stored and handled

according data protection regulations in each country. There was no financial reward for

establishments or participants.

CY: Official research approval for the study was obtained from the Pedagogical Institute of

Cyprus (reference number 153909). Written approval for the study was provided by the

schools. Participants received a certificate.

FR: No formal ethical approval was required. Written approval was obtained from the

general council responsible for the youth health centre. There was no reward for taking part.

SA: No formal ethical approval was required. Written approval for the study was provided by

the schools. Participants received a certificate.

Analysis

All sessions were audio recorded, pseudo-anonymised, and transcribed in the local

language. Transcripts from Cyprus and Saudi Arabia were translated into English for

analysis (performed by MKDH and DL) and double checked with the interviewer(s) if there

were any queries. Analysis in France was undertaken by PTL and PK. The analysis

methodology was the same in all four countries, following the structure for thematic analysis

as outlined in the main paper. Once country specific analyses were complete, the summary

reports were circulated and discussed in detail by all researchers, highlighting comparisons

Page 29 of 31


BMJ Open

123456789101112131415161718192021222324252627282930313233343536373839404142434445464748495051525354555657585960



jopen.bmj.com

/B

MJ O


ownloaded from



between the findings. Finally the results for all countries were collated and summarised at a

face to face meeting, where links between the themes were reviewed and finalised.

Final Sample

Interviews Focus

Groups Total

n n n

France

Female 13 0 13

Male 8 0 8

Total 21 0 21

Cyprus

Female 5 0 5

Male 4 0 4

Total 9 0 9

Saudi Arabia

Female 9 30 39

Male 3 4 7

Total 12 34 46

Page 30 of 31


BMJ Open

123456789101112131415161718192021222324252627282930313233343536373839404142434445464748495051525354555657585960



jopen.bmj.com

/B

MJ O


ownloaded from



COREQ 32-point Checklist for Reporting Qualitative Research

Item Guide questions/description Reported? Page, Section

Domain 1: Research team and reflexivity

Personal Characteristics

1 Interviewer/facilitator Which author/s conducted the interview or focus group? Yes Page 8, paragraph 2

2 Credentials What were the researcher's credentials? E.g. PhD, MD Yes Title page

3 Occupation What was their occupation at the time of the study? Yes Page 8, paragraph 2

4 Gender Was the researcher male or female? Yes Page 8, paragraph 2

5 Experience and training What experience or training did the researcher have? Yes Page 8, paragraph 2

Relationship with participants

6 Relationship established Was a relationship established prior to study commencement?

Yes Page 8, paragraph 2

7 Participant knowledge of the interviewer

What did the participants know about the researcher? e.g. personal goals, reasons for doing the research


8 Interviewer characteristics What characteristics were reported about the interviewer/facilitator? e.g. Bias, assumptions, reasons and interests in the research topic

Yes Page 6, paragraph 2, page 8, paragraph 2

Domain 2: study design

Theoretical framework

9 Methodological orientation and Theory

What methodological orientation was stated to underpin the study? e.g. grounded theory, discourse analysis, ethnography, phenomenology, content analysis


Participant selection

10 Sampling How were participants selected? e.g. purposive, convenience, consecutive, snowball


11 Method of approach How were participants approached? e.g. face-to-face, telephone, mail, email


12 Sample size How many participants were in the study? Yes Page 10, paragraph 2

13 Non-participation How many people refused to participate or dropped out? Reasons?


Setting

14 Setting of data collection Where was the data collected? e.g. home, clinic, workplace


15 Presence of non-participants Was anyone else present besides the participants and researchers?


16 Description of sample What are the important characteristics of the sample? e.g. demographic data, date

Yes Page 10, paragraph 2, table 2

Page 31 of 31


BMJ Open

123456789101112131415161718192021222324252627282930313233343536373839404142434445464748495051525354555657585960

on March 25, 2021 by guest. Protected by copyright. http://bmjopen.bmj.com/ BMJ Open: first published as 10.1136/bmjopen-2016-015308 on 6 June 2017. Downloaded from



Data collection

17 Interview guide Were questions, prompts, guides provided by the authors? Was it pilot tested?


18 Repeat interviews Were repeat interviews carried out? If yes, how many? Yes Page 9, paragraph 1

19 Audio/visual recording Did the research use audio or visual recording to collect the data?


20 Field notes Were field notes made during and/or after the interview or focus group?


21 Duration What was the duration of the interviews or focus group? Yes Page 9, paragraph 1

22 Data saturation Was data saturation discussed? Yes Page 9, paragraph 1

23 Transcripts returned Were transcripts returned to participants for comment and/or correction?


Domain 3: analysis and findings

Data analysis

24 Number of data coders How many data coders coded the data? Yes Page 9, paragraph 2

25 Description of the coding tree Did authors provide a description of the coding tree? Yes Page 9, paragraph 2

26 Derivation of themes Were themes identified in advance or derived from the data?


27 Software What software, if applicable, was used to manage the data?


28 Participant checking Did participants provide feedback on the findings? No Participants did not provide feedback on the findings

Reporting

29 Quotations presented Were participant quotations presented to illustrate the themes / findings? Was each quotation identified? e.g. participant number

Yes Page 11 - 16

30 Data and findings consistent Was there consistency between the data presented and the findings?

Yes Page 11 - 16

31 Clarity of major themes Were major themes clearly presented in the findings? Yes Page 11 - 16

32 Clarity of minor themes Is there a description of diverse cases or discussion of minor themes?

Yes Page 11 - 16

Allison Tong, Peter Sainsbury, Jonathan Craig. Consolidated criteria for reporting qualitative research (COREQ): a 32-item checklist for interviews and focus groups. International Journal for Quality

in Health Care. Dec 2007, 19 (6) 349-357; DOI: 10.1093/intqhc/mzm042

Page 32 of 31


BMJ Open

123456789101112131415161718192021222324252627282930313233343536373839404142434445464748495051525354555657585960




Attitudes and behaviours of adolescents towards antibiotics

and self-care for respiratory tract infections: A qualitative

study.

Journal: BMJ Open

Manuscript ID bmjopen-2016-015308.R1

Article Type: Research

Date Submitted by the Author: 27-Feb-2017

Complete List of Authors: Hawking, Meredith; Public Health England, Primary Care Unit; Barts and The London School of Medicine and Dentistry, Centre for Primary Care and Public Health Lecky, Donna; Public Health England, Primary Care Unit Touboul, Pia; Hopital de l'Archet, Département de Santé Publique; Universite de Nice Sophia Antipolis, Department of Teaching and Research in General Practice Aldigs, Eman; King Abdulaziz University, Medical Microbiology and Parasitology Dept., College Of Medicine Abdulmajed, Hind; King Abdulaziz University, Medical Microbiology and Parasitology Dept., College Of Medicine Ioannidou, Eleni; Cyprus Centre for Environmental Research and Education, CYCERE Hadjichambi, Demetra; Government of the Republic of Cyprus Ministry of Education and Culture Khouri, Pauline; Hopital de l'Archet, Département de Santé Publique; Universite de Nice Sophia Antipolis, France and Department of Teaching and Research in General Practice Gal, Micaela; Cardiff University School of Medicine, Department of Population Medicine Hadjichambis, Andreas; Cyprus Center for Environmental Research and Education – CYCERE – KYKPEE; Government of the Republic of Cyprus Ministry of Education and Culture Mappouras, Demetrios; Government of the Republic of Cyprus Ministry of Education and Culture McNulty, Cliodna; Public Health England, Primary Care Unit

<b>Primary Subject Heading</b>:

Qualitative research

Secondary Subject Heading: Public health, Infectious diseases, General practice / Family practice

Keywords: interview, focus group, student, perceptions, antimicrobial resistance, international


BMJ Open on M

arch 25, 2021 by guest. Protected by copyright.

http://bmjopen.bm

j.com/

BM

J Open: first published as 10.1136/bm

jopen-2016-015308 on 6 June 2017. Dow

nloaded from



Page 1 of 33


BMJ Open

123456789101112131415161718192021222324252627282930313233343536373839404142434445464748495051525354555657585960



jopen.bmj.com

/B

MJ O


ownloaded from



1



Meredith K.D. Hawking, MPH. Public Health England Primary Care Unit, Microbiology


UK, Centre for Primary Care and Public Health, Bart’s and the London School of Medicine

and Dentistry, London, UK. [email protected]

Donna M. Lecky, PhD. Public Health England Primary Care Unit, Microbiology Department,

Gloucestershire Royal Hospital, Great Western Road, Gloucester GL1 3NN, UK,

[email protected]

Pia Touboul Lundgren, MD. Département de Santé Publique, Hôpital de l'Archet 1, 151, rte

St Antoine de Ginestière CS 23079, 06202 Nice Cedex 3, France and Department of

Teaching and Research in General Practice, University of Nice Sophia Antipolis, 28 Avenue

de Valombrose, 06107 Nice, France. [email protected]

Eman Aldigs, Medical Microbiology and Parasitology Dept., College Of Medicine, King


Hind Abdulmajed, Medical Microbiology and Parasitology Dept., College Of Medicine, King


Eleni Ioannidou, Cyprus Centre for Environmental Research and Education, CYCERE,

Limassol, Cyprus. [email protected]

Demetra Paraskeva-Hadjichambi, Ministry of Education and Culture, Nicosia, Cyprus.

[email protected]

Pauline Khouri, MD. Département de Santé Publique, Hôpital de l'Archet 1, 151, rte St

Antoine de Ginestière CS 23079, 06202 Nice Cedex 3, France and Department of Teaching

and Research in General Practice, University of Nice Sophia Antipolis, 28 Avenue de

Valombrose, 06107 Nice, France. [email protected]

Page 2 of 33


BMJ Open

123456789101112131415161718192021222324252627282930313233343536373839404142434445464748495051525354555657585960



jopen.bmj.com

/B

MJ O


ownloaded from



2

Micaela Gal, PHD. Department of Population Medicine, Cardiff University School of

Medicine, Cardiff, CF14 4YS, UK. [email protected]

Andreas Ch. Hadjichambis, Cyprus Centre for Environmental Research and Education –

CYCERE – KYKPEE, Ministry of Education and Culture Nicosia, Cyprus.

[email protected]

Demetrios Mappouras, Ministry of Education and Culture, Nicosia, Cyprus.

[email protected]

Cliodna A.M. McNulty, FRC Pathol. Public Health England Primary Care Unit, Microbiology


UK. [email protected]

*Corresponding author: Dr Donna Lecky Tel: +44 7775 113509; Fax: +44-1452-526197;

Email: [email protected]

Word Count: 3,590

Page 3 of 33


BMJ Open

123456789101112131415161718192021222324252627282930313233343536373839404142434445464748495051525354555657585960



jopen.bmj.com

/B

MJ O


ownloaded from



3

Abstract

Background: To understand attitudes and behaviours of adolescents towards antibiotics,

antimicrobial resistance (AMR) and respiratory tract infections (RTIs).

Design: Qualitative approach informed by the Theory of Planned Behaviour. Semi-

structured interviews and focus groups were undertaken. We aimed to inform the

development of an intervention in an international setting to improve antibiotic use amongst

adolescents, therefore on completion of thematic analysis, findings were triangulated with

qualitative data from similar studies in France, Saudi Arabia and Cyprus to elucidate

differences in the behaviour change model and adaptation to diverse contexts.

Setting: 7 educational establishments from the South of England.

Participants: 53 adolescents (16-18 years) participated in 7 focus groups, and 21

participated in interviews.

Results: Most participants had taken antibiotics and likened them to other common

medications such as painkillers; they reported that their peers treat antibiotics like a ‘cure-all’

and that they themselves were not interested in antibiotics as a discussion topic. They

demonstrated low knowledge of the difference between viral and bacterial infections.

Participants self-cared for colds and flu but believed antibiotics are required to treat other

RTIs such as tonsillitis, which they perceived as more ‘serious’. Past history of taking

antibiotics for RTIs instilled the belief that antibiotics were required for future RTIs.

Those who characterised themselves as ‘non-science students’ were less informed about

antibiotics and AMR. Most participants felt that AMR was irrelevant to them and their peers.

Some ‘non-science’ students thought resistance was a property of the body, rather than

bacteria.

Conclusions: Addressing adolescents’ misperceptions about antibiotics and the treatment

of RTIs using a behaviour change intervention should help improve antibiotic awareness and

may break the cycle of patient demand for antibiotics to treat RTIs amongst this group.

Page 4 of 33


BMJ Open

123456789101112131415161718192021222324252627282930313233343536373839404142434445464748495051525354555657585960



jopen.bmj.com

/B

MJ O


ownloaded from



4

Schools should consider educating all students in further education about antibiotic usage

and AMR, not only those taking science.

Key words: interview, focus group, student, perceptions, antimicrobial resistance,

international

Funding: This work was supported by an internal grant through the Public Health England

(PHE) Development Bid Fund.

Strengths and Limitations of this Study

• The use of focus groups gave researchers insight into peer group interaction and

shared viewpoints, whereas interviews allowed participants to share personal views

more freely in a private setting.

• Triangulation of the data from this study against similar studies in other countries

confirms the transferability of the findings to other settings.

• Recruitment of participants from non-healthcare settings provides insight into views

and behaviours amongst healthy adolescents.

• Although schools were chosen to maximise diversity, researchers could only

influence the selection of participants within educational establishments by providing

guidelines and a sampling matrix to educators.

• Adolescents not enrolled in education were not included in the study and further

research would be required to explore perceptions amongst this group.

Page 5 of 33


BMJ Open

123456789101112131415161718192021222324252627282930313233343536373839404142434445464748495051525354555657585960



jopen.bmj.com

/B

MJ O


ownloaded from



5

Background

The increase in antimicrobial resistance (AMR) has the potential for devastating impact on

public health and the provision of health care worldwide. There are an estimated 25,000

deaths per year in Europe from antibiotic-resistant bacterial infections.[1] The majority of

antibiotics are prescribed in primary care, and much of this prescribing is for self-limiting

upper respiratory tract infections (URTIs)[2] for which antibiotics are often unnecessary,[3]

with individuals more likely to develop bacterial resistance to that antibiotic after use.[4]

Moreover, patient expectation for antibiotics in primary care is linked to higher prescribing.[5

6] Therefore, the World Health Organisation has stressed the need to raise awareness of the

responsible use of antibiotics and the threat of AMR amongst the general public.[7]

However, in spite of numerous interventions targeting the public and healthcare

professionals, antibiotic use is increasing worldwide.[8]

A large European survey has shown that 15-24 year olds are the highest users of antibiotics

and are more likely than other age groups to take them for URTIs.[9] In addition, research in

the UK found that younger members (15-34 years) of the general public have lower

knowledge around antibiotics, AMR, and how to care for self-limiting infections than older

groups.[10] Qualitative research undertaken in healthcare settings has investigated patient

perceptions of antibiotics and AMR of those over 18 years of age,[11-13] They found that

adult patients see antibiotic resistance as a societal or hospital problem due to the

widespread overuse of antibiotics, but not as something that could affect them personally,

and they do not believe that their individual antibiotic use could contribute to or help resolve

the issue.[11-13] Parental perceptions of RTIs and antibiotics in regards to their children has

also been undertaken,[14 15] however to date, older adolescents have attracted less

attention from qualitative researchers as a unique group of participants. These older

adolescents (16-18 years) may be a distinct group of antibiotic users for investigation - unlike

younger children, they may be in control of their own medicines,[16] and responsible for their

Page 6 of 33


BMJ Open

123456789101112131415161718192021222324252627282930313233343536373839404142434445464748495051525354555657585960



jopen.bmj.com

/B

MJ O


ownloaded from



6

use. Adolescents are keen to distance themselves from their parental influence and create

their own self-image,[17] so parents may play a limited role in the day to day management of

medications for common infections such as RTIs. However, as adolescents become more

independent, their health related behaviour may be governed by social norms influenced by

their peers, parents and educators. We decided to investigate this complex behavioural

picture amongst 16-18 year olds as they are in education and therefore school-based,

targeted interventions might be an effective strategy to increase appropriate antibiotic use.

Behavioural interventions have been shown to be effective at improving antibiotic-related

behaviour amongst parents consulting on behalf of their children for RTIs,[18] but there is

little research on interventions targeting adolescents. In order to be successful, any

intervention must be theoretically driven, evidence based and adapted to the local context.

Qualitative inquiry provides a robust methodology for exploring the complex views and

behaviours of this target group. Furthermore, we aimed to triangulate the findings of this

study with country partners of the e-Bug school educational project to inform transferability of

the findings to other settings. e-Bug is a publicly funded international collaborative public

health project which aims to improve school students’ knowledge and behaviours towards

antibiotics and vaccinations.[19]

Page 7 of 33


BMJ Open

123456789101112131415161718192021222324252627282930313233343536373839404142434445464748495051525354555657585960



jopen.bmj.com

/B

MJ O


ownloaded from



7

Methods

Study Design

We conducted in-depth, semi-structured interviews with older adolescents (16-18 years) in

both an individual interview and focus group setting at educational establishments in the

South of England. The Theory of Planned Behaviour (TPB)[20] was used as a theoretical

basis to inform the development of the topic guide to ensure the topics raised covered

multiple factors that influence behaviour. The TPB was used to shape the questions asked in

the interview, and therefore influenced the topics that emerged. However, the TPB was not

used to directly structure the thematic analysis. This was to allow for an inductive approach,

where the themes and thematic framework are shaped by the data, and to allow for any new

constructs that had arisen directly from the interviews. The TPB aims to predict and explain

human behaviour in specific contexts, and identifies intention as the central factor to

performance of a specific behaviour. The TPB suggests that individuals are more likely to

intend to perform a behaviour (take antibiotics) if they have a positive attitude towards it,

perceive social pressure from others to perform the behaviour (subjective norms), and

perceive that the performance of the behaviour is within their control (perceived behavioural

control). Exploration of these constructs and the data that results provides a practical basis

for the development of an intervention to change attitudes, norms and behavioural intention.

Setting and Participants

A two-stage purposive sampling technique was used to recruit schools and colleges (Figure

1). All registered educational establishments teaching 16-18 year olds in Gloucestershire

were invited to participate by letter and telephone. Additionally, all education establishments

serving 16-18 year olds on the e-Bug mailing list were invited in order to geographically

widen the sampling area, and include establishments based in areas with differing levels of

deprivation. Participating establishments were also selected to represent different school

and college types, selection policies and governance structures. An educator was identified

Page 8 of 33


BMJ Open

123456789101112131415161718192021222324252627282930313233343536373839404142434445464748495051525354555657585960



jopen.bmj.com

/B

MJ O


ownloaded from



8

as the ‘study coordinator’ in each school, and was given written guidelines to inform their

selection of participants: 16-18 year old adolescents were purposively sampled according to

gender and area with the aid of a sampling matrix, aiming to achieve a diverse population

and range of views. Informed written consent was obtained from all participating schools and

adolescents, and parents could refuse child inclusion via ‘opt-out’ forms. Participation was

voluntary, therefore we do not have information on those students who did not wish to take

part.

Data collection

The semi-structured topic guide was piloted with five participants and reviewed by the

research team prior to data collection commencement. It included open questions and follow

up probes to elucidate views on antibiotics, AMR and RTIs (Table 1). Care was taken to

ensure that it did not constrain discussions, and allowed new topics to emerge.

Interviews and focus groups were held between March and July 2013 in a private classroom

or school office. Data collection was undertaken by trained, experienced female qualitative

researchers (MH and DL) who were currently employed by the e-Bug project. Interviewers

introduced themselves as researchers working for Public Health England and e-Bug, with an

interest in participants’ views on antibiotics. Interviews and focus groups began with

confirmation that it was not a test of knowledge and participants were assured anonymity

and confidentiality. Educators oversaw organisation and introductions, but were not present

during data collection sessions. Researchers had no previous contact with the participants

prior to the interview or focus group.

Table 1: Topic Guide

Topic Probes

History of taking antibiotics General experience

Perceptions of antibiotics Usage, positives, negatives

Page 9 of 33


BMJ Open

123456789101112131415161718192021222324252627282930313233343536373839404142434445464748495051525354555657585960



jopen.bmj.com

/B

MJ O


ownloaded from



9

Management of colds/flu Self-care, use of medications

Consulting for RTIs Decision to consult, advice, expectations

Others’ views on antibiotics Friends, parents, teachers, media

Antibiotic resistance (AMR) Knowledge, importance, responsibility

Others’ views on AMR Friends, parents, teachers, media

Sources of information Friends, family, media, school, others

Individual interviews lasted 20 - 40 minutes. Focus groups ran for one hour and usually

consisted of between of 5 and 10 participants. Care was taken to allow and encourage all

participants to express their views. Field notes made after each session included

impressions and additional topics that had emerged during data collection. Sessions were

audio recorded, pseudo-anonymised, and transcribed verbatim. Interviews progressed until

theoretical data saturation had occurred and no new themes were arising, after discussion

and agreement within the research team. All data was encrypted, stored and handled

according data protection regulations. There was no financial reward for establishments or

participants; students who took part received a certificate. Repeat interviews were not

undertaken and transcripts were not returned to participants for comment.

Data Analysis and Interpretation

Inductive thematic analysis of the data was undertaken in six stages, as outlined below.[21]

Due to the unbalance of gender in our sample, data was analysed according to gender and

then combined when the themes were found to be common to both female and male

participants. First the transcripts were read by researchers for accuracy, familiarisation and

immersion, then a subset (10%) was annotated with codes by MH and DL. Initial codes were

then discussed with all researchers to resolve any discrepancies. All codes were derived

from the data and a coding schedule was developed for common coding between

researchers. Care was taken not to lose the context of a code by coding too narrowly. Codes

were then grouped into related categories and sorted into a draft framework of six main

Page 10 of 33


BMJ Open

123456789101112131415161718192021222324252627282930313233343536373839404142434445464748495051525354555657585960



jopen.bmj.com

/B

MJ O


ownloaded from



10

themes, which was discussed and agreed between all researchers. Themes were revised

iteratively as the fieldwork and analysis progressed.[21] Use of NVivo software (version 10)

facilitated data organisation. Once coding was complete, the one sheet of paper (OSOP)

method was used to clarify findings within, and between, themes.[22] Finally the results were

collated and summarised, where links between the themes were reviewed and finalised, and

characteristic quotes identified to illuminate the data. Codes provided with each quote

highlight participant characteristics (IS = individual student interview, FG = focus group

participant, F= female, M= male, Ur = urban, Ru = rural, Sc = science student, NSc = non-

science student).

Triangulation

On analysis completion, we triangulated the study findings with qualitative data derived using

the same topic guide, translated and adapted for local use, from similar samples of 15-18

year olds from schools and an adolescent health care centre, in e-Bug partner countries

(France n=21, Saudi Arabia n=48, and Cyprus n=9). The analysis methodology was the

same in all four countries, following the structure for thematic analysis as outlined above,

using a shared coding manual and thematic framework. Findings were translated to English

by researchers in each country alongside discussions to ensure culturally specific meanings

were retained. Once country specific analyses were complete, the summary reports were

circulated and discussed in detail by all researchers, highlighting comparisons between the

findings. Finally the results for all countries were collated and summarised at a face to face

meeting, where links between the themes were reviewed and finalised. The aim was to shed

light on our findings and to assess their transferability across differing contexts. These

countries represent the most diverse range of healthcare systems, antibiotic provision and

usage across the e-Bug partner countries, and we used this approach to inform and assess

the need for country specific adaptations to any potential behavioural intervention. For more

detailed information about the samples and methods these countries used, please see

supplementary file 1.

Page 11 of 33


BMJ Open

123456789101112131415161718192021222324252627282930313233343536373839404142434445464748495051525354555657585960



jopen.bmj.com

/B

MJ O


ownloaded from



11

Results

Final Sample

74 adolescents took part in the study at seven educational establishments in three counties

(Berkshire, Gloucestershire and Essex) in the South of England; 53 participated in seven

focus groups, and 21 were interviewed (Table 2). 24% of participants were male, and 76%

were female. Three of the educational establishments were in rural locales, and four in urban

settings, with average district deprivation index levels ranging from 10.9 to 22.9.[23]

Participants were recruited from three further education colleges and four sixth form schools,

including one Local Education Authority-controlled comprehensive, two comprehensive

academies, and one selective academy. After giving consent, 3 students dropped out due to

illness absence on the day of the interviews, meaning that one focus group only had 3

members.

Table 2: UK Sample characteristics

Interviews Focus

Groups

Total

n % n % n %

Gender

Female 14 66 42 79 56 76

Male 7 33 11 21 18 24

Subject under study

Biology/ Science 7 33 12 22 19 26

Health and Social Care 8 38 21 40 29 39

All other subjects 6 29 20 38 26 35

School Type

Page 12 of 33


BMJ Open

123456789101112131415161718192021222324252627282930313233343536373839404142434445464748495051525354555657585960



jopen.bmj.com

/B

MJ O


ownloaded from



12

Further Education College 8 38 21 40 29 39

Sixth Form 13 62 32 60 45 61

Location

Rural 6 29 25 47 31 41

Urban 15 71 28 53 43 58

Main findings

Understanding and perceptions of antibiotics

The majority of adolescents had previously taken antibiotics and believed them to be

effective for treating infections. Some expressed positive views on antibiotics.

“It just feels like you’re doing something to make yourself better. So if you’re put on

antibiotics it’s like you’re near the end of whatever’s wrong with you”. C1FG1,F1,Ru,NSc

Most participants did not perceive antibiotics to be specifically for bacterial infections and

some of the sample felt they were no different from other medications such as painkillers,

and talked in general terms about medications when they had been asked about antibiotics.

Some participants described avoiding antibiotics, and painkillers, because they were

concerned that they would become reliant on them, or felt that they were harmful.

“It's like a subconscious thing that you always think it's going to be slightly harmful if you

take it [antibiotic].” C7IS3,M,Ur,Sc

" I try not to rely on painkillers and tablets because I feel like my body is going to get used

them and then it just won’t be able to get better on its own." C5IS2,F,Ur,NSc

Page 13 of 33


BMJ Open

123456789101112131415161718192021222324252627282930313233343536373839404142434445464748495051525354555657585960



jopen.bmj.com

/B

MJ O


ownloaded from



13

A small minority of participants directly confused painkillers and antibiotics, or weren’t quite

sure of the difference between these two groups of medicines.

“Is that when you go to the doctors they give you antibiotics? It’s paracetamol. Is

paracetamol an antibiotic?” C3IS1,F,Ru,NSc

“Like what are antibiotics? [laugh] ‘cause I know I've taken like paracetamol and things, I

know that’s not antibiotics is it?” C3FG3,F2,Ru,NSc

There was some misunderstanding about the difference between viral and bacterial

infections, and those who were aware of the distinction were mostly science students.

“Because you go to doctors and you feel like, oh you have got a sore throat, earache,

whatever and they’re like oh it’s a virus, so you get nothing and you go out and it’s just like

‘oh it’s a virus again’ but I didn’t know the difference between a virus and an infection.”

C5IS3,F,Ur,NSc

“I recently spent my work experience, a week at a GPs, and the amount of people who came

in asking for antibiotics, it's remarkable! And a lot of the time, it was a viral infection, so they

didn’t need them”. C7IS2,M,Ur,Sc

Perceptions and treatment of respiratory tract infections (RTIs)

Adolescents grouped different types of uncomplicated RTIs according to their perceived

severity, and this categorisation affected their intentions to take antibiotics. Colds and flu

were seen as simple infections that could be treated at home with ‘natural’ remedies such as

honey, taking comfort measures such as drinking hot drinks and resting, or over the counter

medications such as painkillers. GP consultations would only be considered if symptoms

persisted or were more serious than their normal cold symptoms. A few adolescents

Page 14 of 33


BMJ Open

123456789101112131415161718192021222324252627282930313233343536373839404142434445464748495051525354555657585960



jopen.bmj.com

/B

MJ O


ownloaded from



14

indicated that they would expect antibiotics in this case, especially if they had taken them for

the same kind of illness before.

“I know I had the illness, I know what it feels like and I know taking antibiotics is important

because I won’t get it again, well hopefully”. C2IS3,F,Ru,Sc

Other expectations were to receive a clear diagnosis, reassurance and advice from their

doctor. RTIs such as tonsillitis and sinusitis were seen as more serious infections that

required clinical intervention and would require antibiotics. A few adolescents attributed

feeling better during past RTI illnesses to the antibiotic treatment they took, and therefore

believed that antibiotics are an effective treatment for RTIs, as exemplified by the following

participant:

“This was a sinus infection. The doctor didn’t, he said that it might help, because it was like

viral or bacterial and stuff like that, which I do not really know about. I think if it is viral you

are not supposed to have antibiotics and he wasn’t sure whether it was viral or bacterial so

he gave me antibiotics. After the first week I was still not better, but then after the second

week I was better, so taking them must work.” C5IS1,F,Ur,NSc

Perceptions on parents and peers

Most participants thought that their peers take a lot of antibiotics and treat them as a quick

fix, a ‘cure-all’, like painkillers.

“They just think it’s just like any other medicine that they are taking”. C2IS1,M,Ru,NSc

Page 15 of 33


BMJ Open

123456789101112131415161718192021222324252627282930313233343536373839404142434445464748495051525354555657585960



jopen.bmj.com

/B

MJ O


ownloaded from



15

Most adolescents felt that their peers do not think about, discuss or worry about AMR, or feel

it is relevant to their age group. Antibiotics were not a popular or priority topic of discussion

in their peer group.

“It’s [antibiotics] not something that you talk about, if that makes sense, [laughter] don’t just

strike up a conversation about it, we just don’t.” C4IS4,F,Ur,NSc

Parents were described as having an advisory role whereby they could influence intentions

to take antibiotics, either by ensuring they were used ‘only when necessary’, or were

occasionally reported as encouraging use.

“My parents just think they’re a means to an end really I suppose, they’re to be used when

necessary”. C3IS2,F,Ru,Sc

Some participants reported feeling that their parents were less knowledgeable about

antibiotics than themselves.

“They're not the smartest people [slight laugh] so they just think ‘if you just take them

[antibiotics] you’ll feel fine’, I mean, ‘I've taken them I feel fine’. So it's just trying to explain

that to them”. C7IS1,M,Ur,Sc

Antimicrobial resistance (AMR)

In general, the majority of adolescents had poor understanding of AMR. A small minority of

students in the individual interviews did not know what the term ‘antibiotic resistance’ meant

- one interviewee thought that antibiotic resistance referred to “people against antibiotics”.

With the exception of those who characterised themselves as ‘science students’, many

Page 16 of 33


BMJ Open

123456789101112131415161718192021222324252627282930313233343536373839404142434445464748495051525354555657585960



jopen.bmj.com

/B

MJ O


ownloaded from



16

thought that the ‘body or person becomes resistant’ to antibiotics, as exemplified by the

following excerpts.

“I suppose if you really had, a really serious illness and then you couldn’t treat it, because

you’re immune to one of the tablets, then it could have an effect.” C1IS3,F,Ru,NSc

“Isn’t that where your body gets, what’s it called? Um, too used to antibiotics so that they no

longer work." C2IS2,M,Ru,NSc

However, despite this lack of knowledge, after prompting, some of those who had incorrect

understanding or had not heard of AMR went on to display basic knowledge of resistance in

non-scientific terms, such as: ‘antibiotics might not work for you next time you take them if

you haven’t taken them properly’, or ‘overuse of antibiotics means that they may not work in

the future’, which could act to make them less likely to want to take antibiotics too often. In

contrast, students who demonstrated more knowledge of AMR, mostly science students, felt

that it was an important issue and awareness should be increased amongst the general

public, as these quotes demonstrate:

“I think that’s [antibiotic resistance] going to be increasingly important. If we’re creating more

resistant bacteria we’re going to have to try and make new antibiotics, and what do we do

when we can’t really do anything else?” C3IS2,F,Ru,Sc

“Sooner or later we’re going to run out of antibiotics that work, and it's going to take a lot of

time and a lot of money to find new ones. And it's probably inevitable, but it could be slowed,

that< if people aren’t aware of antibiotic resistance then that situation may come faster.”

C7IS2,M,Ur,Sc

Some participants expressed the view that it is the GP’s responsibility to prescribe

appropriately and monitor antibiotic usage, and it is not their concern.

Page 17 of 33


BMJ Open

123456789101112131415161718192021222324252627282930313233343536373839404142434445464748495051525354555657585960



jopen.bmj.com

/B

MJ O


ownloaded from



17

“I don’t really worry about it, because I think the doctor knows if they’re going to give it to you

whether it’s going to slightly become resistant. [<] I think they’ll monitor how much you

have. I don’t think we have to worry about it ourselves, the patients.” C1FG1,F2,Ru,NSc

Results - comparison between countries

Our findings aligned with the main findings from the Cypriot, French and Saudi Arabian

samples, with a few exceptions. Interviewed adolescents in the UK, Saudi Arabia and

France confused painkillers and antibiotics, however this was not the case with participants

in Cyprus. Adolescents from Saudi Arabia and Cyprus reported obtaining antibiotics over the

counter without a prescription, and this was seen as a very common behaviour amongst

peers, however this is not possible in the UK or France. As with English participants,

previous use of antibiotics in Cyprus and Saudi Arabia lead to an increased expectation for

antibiotics for RTIs. The easy accessibility of antibiotics over the counter in these countries

seemed to increase this effect – antibiotics were described as ‘candies’ and used for a

variety of reported symptoms. Finally, like in the UK, parents had an influence over antibiotic

taking behaviour. This was particularly prominent in Saudi Arabia, where parents more

commonly encouraged the use of antibiotics in contrast to the UK findings where parents

were mainly described as discouraging use, unless they felt that antibiotics were really

necessary.

Discussion

Statement of principle findings

This study found that, with the exception of some science students, adolescents in

educational establishments in England have low knowledge about antibiotics and AMR, and

do not feel that these topics are important or relevant to themselves or their peer group.

Adolescents are confident to self-care for colds and flu, but think other types of RTIs such as

tonsillitis and sinusitis need antibiotics, a perception that is reinforced by previous

Page 18 of 33


BMJ Open

123456789101112131415161718192021222324252627282930313233343536373839404142434445464748495051525354555657585960



jopen.bmj.com

/B

MJ O


ownloaded from



18

experience of receiving antibiotics for infections. Amongst their peers, they perceive overuse

of antibiotics and a lack of concern about AMR. Parents have an advisory role, acting to limit

or encourage use. Comparison with data from other countries confirms very similar findings,

but greater overuse of antibiotics in countries where they are available ‘over the counter’

without prescription; other countries also had differing levels of parental influence.

Strengths and Limitations of this study

Our final sample was large, with participants from a diverse selection of schools and areas,

however our sampling strategy did result in an unequal gender balance, with more females

taking part. It may be that males were less likely to volunteer, or the study format was more

attractive to females. Selection of participants was governed by the study coordinator

(usually an educator) in the school, which we were not able to control, however

establishments were selected carefully to represent different educational types, deprivation

levels and geographical areas, and study coordinators were provided with guidelines and a

sampling matrix to follow. To assess the impact of gender in the sample, we initially

analysed according to gender and found there were no thematic differences between males

and females, and therefore combined the findings, so this may not be an important

drawback. Triangulation of the data against findings from other countries within the e-Bug

project who undertook similar studies allows us to be more confident in the

comprehensiveness and transferability of our findings to other 16-18 year olds in education

in the UK and abroad. Further research is required to understand the views of older

adolescents who are not enrolled in education.

16 – 18 year olds were recruited from schools regardless of their past exposure to antibiotics

or health status making the results of this study more applicable to healthy adolescents in

everyday contexts compared to previous studies that have recruited adult participants from

healthcare settings alone.[11-13] The perceptions and reported behaviours of healthy

adolescents may differ, however, from those who are recruited when they are currently

Page 19 of 33


BMJ Open

123456789101112131415161718192021222324252627282930313233343536373839404142434445464748495051525354555657585960



jopen.bmj.com

/B

MJ O


ownloaded from



19

experiencing an infection, or taking antibiotics. Our use of multiple data collection methods

allowed a comprehensive approach: undertaking individual interviews allowed for more

candid sharing of information and discussion of more personal beliefs and feelings, and gave

quieter students a better chance to voice their views, helping to eliminate difficulties

adolescents can have discussing their health,[24] and concerns about confidentiality.[25 26]

On the other hand, the dynamic interaction of focus groups provided insight into shared

viewpoints and social norms.[27] Care was taken to encourage discussion, by introducing

focus group ‘rules’, distancing the sessions from examination type connotations, and

exclusion of educators from the room.

Comparison to other research

Misperceptions about antibiotics and AMR have been found in previous qualitative research

with adults. [11-13 28 29] The development and the resolution of AMR are seen as the

responsibility of other people, hospitals and doctors who overuse antibiotics, which is

mirrored in our study. Additionally, lack of understanding around the type of infection that

antibiotics should be used for has been shown amongst this age group and others in other

countries.[6 9 30-33] In one such study, 38% believed that antibiotics work against viral

infections.[6] We found that young people believe antibiotics are required to treat what they

perceive as ‘serious’ URTI infections, such as sinus infections and tonsillitis. However,

antibiotics have little clinical benefit in these conditions.[3] Patient expectations for antibiotics

within a primary care consultation have been shown to affect whether or not antibiotics are

prescribed [5 6] and this can have a medicalising effect, leading to greater expectation for

antibiotics for future episodes of similar infections,[5] which was expressed by many of our

adolescents. Receiving a prescription is a positive and valued action that signals that the

consultation has reached a conclusion.[34] Patient expectations for antibiotic prescriptions

and their positive views towards them, as seen in our study, may be linked to the perceived

need for action, to ensure ‘something is being done’ which may be especially important for

Page 20 of 33


BMJ Open

123456789101112131415161718192021222324252627282930313233343536373839404142434445464748495051525354555657585960



jopen.bmj.com

/B

MJ O


ownloaded from



20

infections perceived as ‘severe’. In connection with a perceived lack of responsibility for the

preservation of antibiotics, this desire to ‘do something’ about the infection could drive

antibiotic use amongst this age group.

Research has shown that painkillers are seen as an essentially harmless ‘ordinary, everyday

medicine’ by young teenage women.[35] Young adolescents are often responsible for taking

their own medication, for example in a survey of school students, 22% of 11-13 year olds

reported that they were allowed to use pain medications without asking for permission, and

this increased significantly with age.[16] A lack of understanding between these pain

medications and antibiotics, as demonstrated in our study, may have negative impacts on

antibiotic use of and prescription expectation.

In a recent qualitative study with Swedish teenagers aged 16-19 years, students argued that

the effect of paracetamol declined if it was used too often.[17] This belief is similar to basic

understandings of AMR seen in our study. The perception that resistance is a property of the

body echoes similar qualitative research undertaken with adults recruited from health care

settings.[11-13 28 29]

Adolescents in the study said that they would not discuss antibiotics with their friends, and

did not think the topic of antibiotics or AMR was relevant or interesting to them. Holmström

and colleagues [17] found that Swedish adolescents held similar views about pain

medication: it was considered a ‘non-issue’ and was not discussed. However in other health

related areas peers have been shown to have an influential role.[36]

Low knowledge of antibiotics has been linked to low educational attainment in studies of

adults,[30] however the findings in our study suggest that engaging in post-16 science

education provides students with a well-rounded knowledge in relation to antibiotics and

AMR. This suggests the impact of education may be more nuanced – it would be possible to

achieve a high level of educational attainment following a non-scientific pathway in further

education and therefore have a poor understanding of antibiotics and AMR. On the other

hand, our findings suggest that increasing education adapted to different pathways around

antibiotics in further education may help young adults to engage with the topic and act to

Page 21 of 33


BMJ Open

123456789101112131415161718192021222324252627282930313233343536373839404142434445464748495051525354555657585960



jopen.bmj.com

/B

MJ O


ownloaded from



21

protect antibiotics for future generations, by increasing their intentions to take antibiotics less

and only when necessary.

Implications for clinical practice and policymakers

The perceived need and expectation for antibiotics for the treatment of RTIs by young

people should be taken into account by clinicians when adolescents consult, remembering

that adolescence is a key time for the development of life long health behaviours and

decision making. Provision of reassurance and information about self-care for RTIs [37] has

been shown to be highly satisfactory to patients in this scenario and should therefore be

promoted for this age group. It may be useful to address the differences between painkillers

and antibiotics with adolescent patients to ensure antibiotics are treated appropriately, and to

address any concerns about the body becoming reliant on or resistant to antibiotics.

The lack of concern shown by young people for AMR, unless addressed, could contribute to

irresponsible use of antibiotics and demand for antibiotics when this age group consult. As

the more knowledgeable ‘science’ students in the study believe it is their personal

responsibility to help control AMR, peer to peer interventions that promote interaction

between science students and those not studying science subjects could raise the profile of

antibiotic resistance and situate it as an important and relevant topic for young adults to be

concerned with. According to our study, studying science post 16 years may provide

adolescents with more rounded knowledge about antibiotics and AMR that could influence

their future health related behaviour.

Implications for future research

Our findings demonstrate that there are misperceptions about antibiotics and how to treat

RTIs amongst older adolescents currently enrolled in education in England, which goes

some way to explaining the high reported use of antibiotics amongst this age group seen in

previous research. Further research is required to assess perceptions amongst adolescents

who are not in education to assess transferability of the findings to these groups. As our

Page 22 of 33


BMJ Open

123456789101112131415161718192021222324252627282930313233343536373839404142434445464748495051525354555657585960



jopen.bmj.com

/B

MJ O


ownloaded from



22

study suggests that young adults in educational environments are a good target group for

behavioural interventions, peer to peer education and interaction between those studying

different subject types could be a key target for intervention development and evaluation.

Triangulation with contrasting international contexts demonstrated that a common

intervention model would be relevant. Whilst many perceptions are shared amongst

adolescents in different countries, some country-specific adaptation of any intervention

would be necessary. The e-Bug team have used the findings to develop a behaviour change

intervention for schools and young people. For more information on the development of the

intervention, visit the e-Bug website.[19]

Page 23 of 33


BMJ Open

123456789101112131415161718192021222324252627282930313233343536373839404142434445464748495051525354555657585960



jopen.bmj.com

/B

MJ O


ownloaded from



23

Acknowledgements

A warm thanks to all of the participants and to their educators for their help in facilitating the

study in each school, and to the youth health centre Carrefour Santé Jeunes and General

Council in Nice, France.

Competing Interests

CM leads the e-Bug project development and writes evidence-based antibiotic guidance for

primary care and leads the Royal College of General Practitioners (RCGP) TARGET (Treat

Antibiotics Responsibly, Guidance and Education Tools) antibiotic toolkit development

including a patient leaflet encouraging delayed/back-up prescribing. She is a past member

(2008-16) of the Advisory Committee on Antimicrobial Resistance and Healthcare

Associated Infection (ARHAI). All other authors were involved in the e-Bug project in their

respective countries at the time of the research. The funding body had no role in the design,

execution, analysis or reporting of the research.

Governance

Internal Public Health England review only was required as participants were not recruited

through the National Health Service (NHS) and all UK participants were over 16 years of

age. The Department of Education was consulted and the study was referred to the

Governmental Disclosure and Barring Service (DBS). The study was undertaken in full

accordance with the DBS regulations.

Authors’ contributions

MH was the main researcher, wrote the protocol, recruited schools, interviewed participants

in the UK, coded the data from the UK, Cyprus and Saudi Arabia and led analysis of the data

and writing the manuscript. DL discussed the protocol, supervised the project, interviewed

participants in the UK, double coded the data and edited the manuscript. PTL facilitated the

Page 24 of 33


BMJ Open

123456789101112131415161718192021222324252627282930313233343536373839404142434445464748495051525354555657585960



jopen.bmj.com

/B

MJ O


ownloaded from



24

project in France and coded and analysed the French data with PK who also carried out the

interviews in France. EA and HA facilitated the project in Saudi Arabia, collecting the data

and translated the interviews. DH, AChH and DM facilitated the project in Cyprus, EI

interviewed the participants and organised transcript translation. MG was involved in

protocol development and commented on methodology throughout data collection. CMcN

led the overall project, advising on protocol, methodology, analysis and interpretation. All

authors reviewed and commented on the protocol and the manuscript.

Funding

In the UK this work was supported by an internal grant through the Public Health England

(PHE) Development Bid Fund. There was no specific funding for this study in France,

Cyprus and Saudi Arabia. In France PTL was supported by the Ministry of Health and Nice

University Hospital for coordination of the e-Bug project and PK undertook the research as

part of her medical student thesis. In Cyprus DH and EI were supported by the Ministry of

Education and Culture and the Cyprus Centre for Environmental Research and Education. In

Saudi Arabia EA and HA were supported by King Abdulaziz University.

Data sharing: Please contact Dr Donna Lecky to discuss access to unpublished data

from the study.

References

1. European Centre for Disease Control. The bacterial challenge: time to react. . Secondary The bacterial challenge: time to react. 2009. http://www.ecdc.europa.eu/en/publications/Publications/0909_TER_The_Bacterial_Challenge_Time_to_React.pdf.

2. Public Health England. The English Surveillance Programme for Antimicrobial Utilisation and Resistance Report 2014. Secondary The English Surveillance Programme for Antimicrobial Utilisation and Resistance Report 2014 2014. https://www.gov.uk/government/uploads/system/uploads/attachment_data/file/362374/ESPAUR_Report_2014__3_.pdf

3. National Institute for Health and Clinical Excellence. Respiratory tract infections – antibiotic prescribing: Prescribing of antibiotics for self-limiting respiratory tract infections in adults and children in primary care. Secondary Respiratory tract infections – antibiotic prescribing: Prescribing of antibiotics for self-limiting respiratory tract infections in adults and children in primary care. 2008. http://www.nice.org.uk/nicemedia/live/12015/41323/41323.pdf

Page 25 of 33


BMJ Open

123456789101112131415161718192021222324252627282930313233343536373839404142434445464748495051525354555657585960



jopen.bmj.com

/B

MJ O


ownloaded from



25

4. Costelloe C, Metcalfe C, Lovering A, Mant D, Hay AD. Effect of antibiotic prescribing in primary care on antimicrobial resistance in individual patients: systematic review and meta-analysis. BMJ 2010;340

5. Butler CC, Rollnick S, Pill R, Maggs-Rapport F, Stott N. Understanding the culture of prescribing: qualitative study of general practitioners' and patients' perceptions of antibiotics for sore throats. Bmj 1998;317(7159):637-42

6. McNulty CA, Nichols T, French DP, Joshi P, Butler CC. Expectations for consultations and antibiotics for respiratory tract infection in primary care: the RTI clinical iceberg. Br J Gen Pract 2013;63(612):e429-36 doi: 10.3399/bjgp13X669149[published Online First: Epub Date]|.

7. World Health Organisation. Combating antimicrobial resistance, including antibiotic resistance. Secondary Combating antimicrobial resistance, including antibiotic resistance. 2014. http://apps.who.int/gb/ebwha/pdf_files/EB134/B134_R13-en.pdf.

8. Laxminarayan R, Duse A, Wattal C, et al. Antibiotic resistance—the need for global solutions. The Lancet Infectious Diseases 2013;13(12):1057-98 doi: http://dx.doi.org/10.1016/S1473-3099(13)70318-9[published Online First: Epub Date]|.

9. European Commission. Special Eurobarometer 407: Antimicrobial Resistance. Secondary Special Eurobarometer 407: Antimicrobial Resistance. 2013. http://ec.europa.eu/public_opinion/archives/ebs/ebs_407_en.pdf.

10. McNulty CAM, Lecky DM, Hawking MKD, Roberts C, Quigley A, Butler CC. How much information about antibiotics do people recall after consulting in primary care? Family Practice 2016 doi: 10.1093/fampra/cmw022[published Online First: Epub Date]|.

11. Hawkings NJ, Wood F, Butler CC. Public attitudes towards bacterial resistance: a qualitative study. Journal of Antimicrobial Chemotherapy 2007;59(6):1155-60 doi: 10.1093/jac/dkm103[published Online First: Epub Date]|.

12. Brooks L, Shaw A, Sharp D, Hay AD. Towards a better understanding of patients' perspectives of antibiotic resistance and MRSA: a qualitative study. Family Practice 2008;25(5):341-48 doi: 10.1093/fampra/cmn037[published Online First: Epub Date]|.

13. Brookes-Howell L, Elwyn G, Hood K, et al. 'The body gets used to them': patients' interpretations of antibiotic resistance and the implications for containment strategies. J Gen Intern Med 2012;27(7):766-72 doi: 10.1007/s11606-011-1916-1[published Online First: Epub Date]|.

14. Barden LS, Dowell SF, Schwartz B, Lackey C. Current Attitudes Regarding Use of Antimicrobial Agents: Results from Physicians' and Parents' Focus Group Discussions. Clinical Pediatrics 1998;37(11):665-71 doi: 10.1177/000992289803701104[published Online First: Epub Date]|.

15. Ingram J, Cabral C, Hay AD, Lucas PJ, Horwood J. Parents’ information needs, self-efficacy and influences on consulting for childhood respiratory tract infections: a qualitative study. BMC Family Practice 2013;14(1):1-9 doi: 10.1186/1471-2296-14-106[published Online First: Epub Date]|.

16. Holstein BE, Andersen A, Krølner R, Due P, Hansen EH. Young adolescents' use of medicine for headache: sources of supply, availability and accessibility at home. Pharmacoepidemiology and drug safety 2008;17(4):406-10 doi: 10.1002/pds.1563[published Online First: Epub Date]|.

17. Holmström IK, Bastholm-Rahmner P, Bernsten C, Röing M, Björkman I. Swedish teenagers and over-the-counter analgesics - responsible, casual or careless use. Res Social Adm Pharm 2014;10(2):408-18 doi: 10.1016/j.sapharm.2013.06.004[published Online First: Epub Date]|.

18. Vodicka TA, Thompson M, Lucas P, et al. Reducing antibiotic prescribing for children with respiratory tract infections in primary care: a systematic review. British Journal of General Practice 2013;63(612):e445

19. e-Bug. e-Bug: a place to play games and learn about microbes. Secondary e-Bug: a place to play games and learn about microbes. 2014. www.e-bug.eu.

Page 26 of 33


BMJ Open

123456789101112131415161718192021222324252627282930313233343536373839404142434445464748495051525354555657585960



jopen.bmj.com

/B

MJ O


ownloaded from



26

20. Ajzen I. The Theory of Planned Behavior. Organizational Behavior and Human Decision Processes 1991;50:179-211

21. Braun V, Clarke V. Using thematic analysis in psychology. Qualitative Research in Psychology 2006;3(2):77-101 doi: 10.1191/1478088706qp063oa[published Online First: Epub Date]|.

22. Ziebland S, McPherson A. Making sense of qualitative data analysis: an introduction with illustrations from DIPEx (personal experiences of health and illness). Medical Education 2006;40(5):405-14 doi: 10.1111/j.1365-2929.2006.02467.x[published Online First: Epub Date]|.

23. Department for Communities and Local Government. English indices of deprivation 2015. Secondary English indices of deprivation 2015 2015. https://www.gov.uk/government/statistics/english-indices-of-deprivation-2015.

24. Harvey K, Churchill D, Crawford P, et al. Health communication and adolescents: what do their emails tell us? Family Practice 2008;25(4):304-11 doi: 10.1093/fampra/cmn029[published Online First: Epub Date]|.

25. Churchill R, Allen J, Denman S, Williams D, Fielding K, von Fragstein M. Do the attitudes and beliefs of young teenagers towards general practice influence actual consultation behaviour? The British Journal of General Practice 2000;50(461):953-57

26. Carlisle J, Shickle D, Cork M, McDonagh A. Concerns over confidentiality may deter adolescents from consulting their doctors. A qualitative exploration. Journal of Medical Ethics 2006;32(3):133-37 doi: 10.1136/jme.2004.011262[published Online First: Epub Date]|.

27. Kitzinger J. The methodology of Focus Groups: the importance of interaction between research participants. Sociology of health & illness 1994;16(1):103-21 doi: 10.1111/1467-9566.ep11347023[published Online First: Epub Date]|.

28. Norris P, Chamberlain K, Dew K, Gabe J, Hodgetts D, Madden H. Public Beliefs about Antibiotics, Infection and Resistance: A Qualitative Study. Antibiotics 2013;2(4):465-76 doi: 10.3390/antibiotics2040465[published Online First: Epub Date]|.

29. Reynolds L, McKee M. Factors influencing antibiotic prescribing in China: an exploratory analysis. Health Policy 2009;90(1):32-6 doi: 10.1016/j.healthpol.2008.09.002[published Online First: Epub Date]|.

30. McNulty CAM, Boyle P, Nichols T, Clappison P, Davey P. Don't wear me out—the public's knowledge of and attitudes to antibiotic use. Journal of Antimicrobial Chemotherapy 2007;59(4):727-38 doi: 10.1093/jac/dkl558[published Online First: Epub Date]|.

31. Azevedo MM, Pinheiro C, Yaphe J, Baltazar F. Portuguese students' knowledge of antibiotics: a cross-sectional study of secondary school and university students in Braga. BMC Public Health 2009;9:359 doi: 10.1186/1471-2458-9-359[published Online First: Epub Date]|.

32. Huang Y, Gu J, Zhang M, et al. Knowledge, attitude and practice of antibiotics: a questionnaire study among 2500 Chinese students. BMC Med Educ 2013;13:163 doi: 10.1186/1472-6920-13-163[published Online First: Epub Date]|.

33. Cebotarenco N, Bush PJ. Reducing antibiotics for colds and flu: a student-taught program. Health Education Research 2008;23(1):146-57 doi: 10.1093/her/cym008[published Online First: Epub Date]|.

34. Pinder R, Sallis A, Berry D, Chadborn T. Behaviour change and antibiotic prescribing in healthcare settings: Literature review and behavioural analysis. Secondary Behaviour change and antibiotic prescribing in healthcare settings: Literature review and behavioural analysis 2015. https://www.gov.uk/government/uploads/system/uploads/attachment_data/file/405031/Behaviour_Change_for_Antibiotic_Prescribing_-_FINAL.pdf.

35. Hansen DL, Holstein BE, Hansen EH. “I'd Rather Not Take it, But . . .”: Young Women's Perceptions of Medicines. Qualitative Health Research 2009;19(6):829-39 doi: 10.1177/1049732309335447[published Online First: Epub Date]|.

Page 27 of 33


BMJ Open

123456789101112131415161718192021222324252627282930313233343536373839404142434445464748495051525354555657585960



jopen.bmj.com

/B

MJ O


ownloaded from



27

36. Maxwell KA. Friends: The Role of Peer Influence Across Adolescent Risk Behaviors. Journal of Youth and Adolescence 2002;31(4):267-77 doi: 10.1023/A:1015493316865[published Online First: Epub Date]|.

37. Welschen I, Kuyvenhoven M, Hoes A, Verheij T. Antibiotics for acute respiratory tract symptoms: patients' expectations, GPs' management and patient satisfaction. Fam Pract 2004;21(3):234-7

Page 28 of 33


BMJ Open

123456789101112131415161718192021222324252627282930313233343536373839404142434445464748495051525354555657585960



jopen.bmj.com

/B

MJ O


ownloaded from



Figure 1: Recruitment Flowchart

60x85mm (300 x 300 DPI)

Page 29 of 33


BMJ Open

123456789101112131415161718192021222324252627282930313233343536373839404142434445464748495051525354555657585960



jopen.bmj.com

/B

MJ O


ownloaded from





Supplementary File 1

Authors: Hawking M.K.D., Lecky D.M., Touboul Lundgren P., Aldigs E., Abdulmajed H.,

Ioannidou E., Paraskeva-Hadjichambi D., Khouri P., Gal M., Hadjichambis A.Ch.,

Mappouras D. & McNulty C.A.M.

Qualitative Data from interviews and focus groups with adolescents in France, Saudi Arabia

and Cyprus collected using similar methods were used to triangulate the findings from the

UK dataset. This file outlines the methodology used in these countries to allow consideration

of any differences between the samples and findings. Country specific details are denoted

by the following abbreviations: France (FR), Saudi Arabia (SA), Cyprus (CY).

Participants and Setting

FR: Adolescents were recruited in Nice via a youth healthcare centre, a facility providing

medical attention and advice for a range of health related issues for young people. 15-18

year old adolescents were approached by and purposively sampled by the research team

according to age, gender, geographic area, socio-economic area and academic pathway.

SA: All registered educational establishments in Jeddah were invited to participate by letter

followed by a telephone call if necessary. A study coordinator was appointed in each school

to identify participating students and provide study information. 15-18 year old adolescents

were purposively sampled according to age, gender, geographic area, socio-economic area

and academic pathway. The female research team were unable to enter male schools.

Therefore, male adolescents were recruited via personal networks through friends and

relatives, ensuring these were from a mix of science and non-science backgrounds.

CY: All registered educational establishments in Limassol, Nicosia, Larnaca and Paphos

were invited to participate by letter followed by a telephone call if necessary. A study

coordinator was appointed in each school to identify participating students and provide study

information. 15-18 year old adolescents were purposively sampled according to age, gender,

geographic area, socio-economic area and academic pathway.

Page 30 of 33


BMJ Open

123456789101112131415161718192021222324252627282930313233343536373839404142434445464748495051525354555657585960



jopen.bmj.com

/B

MJ O


ownloaded from



Data collection

All countries used the same topic guide as the one developed for the UK sample, but

adapted it for the local context and to incorporate emerging topics as data collection

commenced. Interviews and focus groups were held between March and July 2013.

Individual face to face interviews typically lasted between 20 and 40 minutes, whilst focus

groups usually ran for one hour. Focus groups consisted of between 4 and 11 participants.

Interviews progressed in each country until theoretical data saturation had occurred, and no

new themes were emerging from the data, which was judged by discussions within the

research team.

FR: In France the interviews were held in youth health care centres. Focus groups were not

undertaken in France. Interviews were undertaken by a trained interviewer (PK).

SA: School based interviews and focus groups were overseen by educators although the

responsible educator was not present in the school room during the sessions. Interviews and

focus groups were undertaken by trained interviewers (EA, HA).

CY: Interviews in Cyprus were overseen by educators although the responsible educator

was not present in the school room during the sessions. Focus groups were not undertaken

in Cyprus. Interviews were undertaken by a trained interviewer (EI).

Ethical considerations

All participants provided written, informed consent to take part. In schools, parents were

provided with opt out forms. All data was encrypted, anonymised, stored and handled

according data protection regulations in each country. There was no financial reward for

establishments or participants.

CY: Official research approval for the study was obtained from the Pedagogical Institute of

Cyprus (reference number 153909). Written approval for the study was provided by the

schools. Participants received a certificate.

FR: No formal ethical approval was required. Written approval was obtained from the

general council responsible for the youth health centre. There was no reward for taking part.

SA: No formal ethical approval was required. Written approval for the study was provided by

the schools. Participants received a certificate.

Page 31 of 33


BMJ Open

123456789101112131415161718192021222324252627282930313233343536373839404142434445464748495051525354555657585960



jopen.bmj.com

/B

MJ O


ownloaded from



Analysis

All sessions were audio recorded, pseudo-anonymised, and transcribed in the local

language. Transcripts from Cyprus and Saudi Arabia were translated into English for

analysis (performed by MKDH and DL) and double checked with the interviewer(s) if there

were any queries. Analysis in France was undertaken by PTL and PK. The analysis

methodology was the same in all four countries, following the structure for thematic analysis

as outlined in the main paper. Once country specific analyses were complete, the summary

reports were circulated and discussed in detail by all researchers, highlighting comparisons

between the findings. Finally the results for all countries were collated and summarised at a

face to face meeting, where links between the themes were reviewed and finalised.

Final Sample

Interviews

Focus

Groups Total

n n n

France

Female 13 0 13

Male 8 0 8

Total 21 0 21

Cyprus

Female 5 0 5

Male 4 0 4

Total 9 0 9

Saudi Arabia

Female 9 30 39

Male 3 4 7

Total 12 34 46

Page 32 of 33


BMJ Open

123456789101112131415161718192021222324252627282930313233343536373839404142434445464748495051525354555657585960



jopen.bmj.com

/B

MJ O


ownloaded from



COREQ 32-point Checklist for Reporting Qualitative Research

Item Guide questions/description Reported? Page, Section

Domain 1: Research team and reflexivity

Personal Characteristics

1 Interviewer/facilitator Which author/s conducted the interview or focus group? Yes Page 8, paragraph 2

2 Credentials What were the researcher's credentials? E.g. PhD, MD Yes Title page

3 Occupation What was their occupation at the time of the study? Yes Page 8, paragraph 2

4 Gender Was the researcher male or female? Yes Page 8, paragraph 2

5 Experience and training What experience or training did the researcher have? Yes Page 8, paragraph 2

Relationship with participants

6 Relationship established Was a relationship established prior to study commencement?


7 Participant knowledge of the interviewer

What did the participants know about the researcher? e.g. personal goals, reasons for doing the research


8 Interviewer characteristics What characteristics were reported about the interviewer/facilitator? e.g. Bias, assumptions, reasons and interests in the research topic

Yes Page 6, paragraph 2, page 8, paragraph 2

Domain 2: study design

Theoretical framework

9 Methodological orientation and Theory

What methodological orientation was stated to underpin the study? e.g. grounded theory, discourse analysis, ethnography, phenomenology, content analysis


Participant selection

10 Sampling How were participants selected? e.g. purposive, convenience, consecutive, snowball


11 Method of approach How were participants approached? e.g. face-to-face, telephone, mail, email


12 Sample size How many participants were in the study? Yes Page 10, paragraph 2

13 Non-participation How many people refused to participate or dropped out? Reasons?


Setting

14 Setting of data collection Where was the data collected? e.g. home, clinic, workplace


15 Presence of non-participants Was anyone else present besides the participants and researchers?


16 Description of sample What are the important characteristics of the sample? e.g. demographic data, date


Page 33 of 33


BMJ Open

123456789101112131415161718192021222324252627282930313233343536373839404142434445464748495051525354555657585960




Data collection

17 Interview guide Were questions, prompts, guides provided by the authors? Was it pilot tested?


18 Repeat interviews Were repeat interviews carried out? If yes, how many? Yes Page 9, paragraph 1

19 Audio/visual recording Did the research use audio or visual recording to collect the data?


20 Field notes Were field notes made during and/or after the interview or focus group?


21 Duration What was the duration of the interviews or focus group? Yes Page 9, paragraph 1

22 Data saturation Was data saturation discussed? Yes Page 9, paragraph 1

23 Transcripts returned Were transcripts returned to participants for comment and/or correction?


Domain 3: analysis and findings

Data analysis

24 Number of data coders How many data coders coded the data? Yes Page 9, paragraph 2

25 Description of the coding tree Did authors provide a description of the coding tree? Yes Page 9, paragraph 2

26 Derivation of themes Were themes identified in advance or derived from the data?


27 Software What software, if applicable, was used to manage the data?


28 Participant checking Did participants provide feedback on the findings? No Participants did not provide feedback on the findings

Reporting

29 Quotations presented Were participant quotations presented to illustrate the themes / findings? Was each quotation identified? e.g. participant number

Yes Page 11 - 16

30 Data and findings consistent Was there consistency between the data presented and the findings?

Yes Page 11 - 16

31 Clarity of major themes Were major themes clearly presented in the findings? Yes Page 11 - 16

32 Clarity of minor themes Is there a description of diverse cases or discussion of minor themes?

Yes Page 11 - 16

Allison Tong, Peter Sainsbury, Jonathan Craig. Consolidated criteria for reporting qualitative research (COREQ): a 32-item checklist for interviews and focus groups. International Journal for Quality

in Health Care. Dec 2007, 19 (6) 349-357; DOI: 10.1093/intqhc/mzm042

Page 34 of 33


BMJ Open

123456789101112131415161718192021222324252627282930313233343536373839404142434445464748495051525354555657585960



Documents

BMJ Open€¦ · Touboul, Pia; Hopital de l'Archet, Département de Santé Publique; Universite de Nice Sophia Antipolis, Department of Teaching and Research in General Practice Aldigs,