Document below…
Scanned by CamScanner
Scanned by CamScanner
Scanned by CamScanner
Scanned by CamScanner
Scanned by CamScanner
Scanned by CamScanner
S Y S T E M A T I C R E V I E W
Antibiotic Prescribing in Long-Term Care Facilities:
A Meta-synthesis of Qualitative Researc
h
Aoife Fleming1 • Colin Bradley2 • Shane Cullinan1 • Stephen Byrne
1
Published online: 2 April 2015
� The Author(s) 2015. This article is published with open access at Springerlink.com
Abstrac
t
Objectives The objective of this review was to synthesize
the findings of qualitative studies investigating the factor
s
influencing antibiotic prescribing in long-term care facilities
(LTCFs). These findings will inform the development of fu-
ture antimicrobial stewardship strategies (AMS) in this setting.
Methods We searched Embase, PubMed, PsycInfo, So-
cial Science Citations Index and Google Scholar for all
qualitative studies investigating health care professionals’
views on antibiotic prescribing in LTCFs. The quality o
f
the papers was assessed using the Critical Appraisal Skills
Programme (CASP) assessment tool for qualitative re-
search. Thematic synthesis was used to integrate the
emergent themes into an overall analytical theme.
Results The synthesis of eight qualitative studies ind
i-
cated that health care professionals and administrators have
identified factors that influence antibiotic prescribing in
LTCFs. These factors include variations in knowledge an
d
practice among health care professionals, and the LTCF
context, which is unique given the complex patient
population and restricted access to doctors and diagnosti
c
tests. The social factors underpinning the interaction be-
tween nurses, residents’ families and doctors also influence
decision making around antibiotic prescribing. The study
also found that there is an acknowledged need for col-
laborative, evidence-based AMS specific to LTCFs, as
antibiotic prescribing is heavily influenced by facto
rs
unique to this setting.
Conclusion This review highlighted the key contextual
challenges for AMS in LTCFs. The findings provide an in-
depth insight into the factors—such as the LTCF context
,
social factors, variability in knowledge and prescribing
practices, and antimicrobial resistance—that impact on
antibiotic prescribing and AMS strategies. These factors
must be considered in order to ensure the feasibility and
applicability of future AMS interventions.
Key Poin
ts
The influences of the long-term care facility (LTCF
)
context and social factors have an important impact
on antibiotic prescribing in this setting.
According to the findings of this review, future
antimicrobial stewardship strategies must emphasize
the importance of knowledge of guidelines and
antimicrobial resistance, and the strategies must be
specifically designed for implementation in the
LTCF setting.
1 Introduction
Recent studies evaluating the prescribing of antibiotics in
long-term care facilities (LTCFs) have found that antibiotic
prescribing is common, with reported annual prevalence
rates ranging from 47 to 79 % [1]. As many as 25–75 % of
Electronic supplementary material The online version of this
article (doi:10.1007/s40266-015-0252-2) contains supplementary
material, which is available to authorized users.
& Aoife Fleming
a.fleming@ucc.ie
1
Pharmaceutical Care Research Group, School of Pharmacy,
University College Cork,
Cork, Ireland
2
Department of General Practice, University College Cork,
Cork, Ireland
Drugs Aging (2015) 32:295–303
DOI 10.1007/s40266-015-0252-2
http://dx.doi.org/10.1007/s40266-015-0252-2
antibiotic prescriptions in LTCFs are inappropriate in terms
of their indication, dose or duration of therapy [2]. Through
reductions in antibiotic prescribing and encouragement of
appropriate use of antibiotics, the rates of antimicrobial
resistance (AMR) and adverse drug events can be reduced
[3]. The few antimicrobial stewardship (AMS) intervention
studies that have been conducted in LTCFs have reported
modest effects, which were often not sustained [4, 5]. In
order to establish how best to address AMS strategies in
LTCFs, the factors that influence antibiotic prescribing
behaviours must be determined and understood. There is a
need for detailed awareness and understanding of the be-
haviour of all health care professionals involved in LTCF
antibiotic prescribing.
There have been several qualitative review papers
evaluating influences on antibiotic prescribing in primary
and secondary care settings [6–8]. Qualitative studies in-
vestigating antibiotic prescribing in LTCFs have been
conducted, but, to date, there has not been an overall
synthesis of these studies. Synthesis of knowledge is im-
portant to bring together the findings of individual studies
in order to further the understanding of a given issue [9].
A
qualitative meta-synthesis integrates and compares findings
across different studies, and the accumulated knowledge
may lead to development of a new theory, narrative or
interpretive translation [9, 10]. Synthesis of information
from existing qualitative studies may help to contribute to
AMS strategies in LTCFs.
The objective of this qualitative meta-synthesis was to
synthesize the qualitative research findings that have col-
lected health care professionals’ and administrators’ views
of the factors influencing antibiotic prescribing in LTCFs.
2 Methods
2.1 Search Strategy
The following databases were searched from their incep-
tion until July 2014: Embase, PubMed, PsycInfo, Social
Science Citations Index and Google Scholar. The search
strategy that was adopted included the following search
terms: (antibiotic* OR antibacterial* OR infection*) AND/
OR (attitude of health personnel) AND (nursing home* OR
long term care facilit*) AND (interview* OR ‘qualitative
research’). There were no date or language restrictions
imposed. We searched the reference lists of relevant arti-
cles to screen for any relevant studies.
2.2 Study Inclusion Criteria
The studies were included in the review if they met the
following criteria: (1) used qualitative data collection and
analysis methods; (2) were focussed on LTCF antibiotic
use; (3) included health care professionals (doctors, nurses
or pharmacists, or a combination of these groups) or LTCF
administrators in the sample; and (4) used qualitative
methods to evaluate an AMS intervention. In the case of
studies where qualitative and quantitative methods were
employed, only the qualitative data were collected. The
abstracts were evaluated by the primary author according
to the inclusion criteria, and the full-text articles were
obtained and evaluated where appropriate. Where there
was uncertainty about whether to include a study in the
review, another author was consulted.
2.3 Quality Appraisal
The quality of the papers was assessed using the Critical
Appraisal Skills Programme (CASP) assessment tool for
qualitative research, as outlined in Electronic Supplemen-
tary Material (ESM) Online Resource 1 [11]. Each author
individually assessed the quality of each study, and a de-
cision on the exclusion and inclusion of studies was made
collectively and with consensus between all authors.
2.4 Analysis
Thematic synthesis was used to analyse the results of the
studies included in this review. This method identifies the
prominent or recurring themes in the literature and collates
these findings under thematic headings [9, 12]. The initial
stages conducted by two authors were line-by-line coding
of the text and development of descriptive sub-themes as
free codes without a hierarchy. The final stage was gen-
eration of main themes based on discussion between all
authors. In order to present the synthesis of the findings, a
conceptual model was developed by the primary author and
reviewed by all authors. This qualitative synthesis is re-
ported in accordance with the Enhancing Transparency in
Reporting the Synthesis of Qualitative Research
(ENTREQ) guidelines (see ESM Online Resource 2) [13].
3 Results
3.1 Study Selection Process
A total of 1308 papers were retrieved and reviewed ac-
cording to the title. An abstract review of 139 studies was
conducted, and 34 studies were selected for full-text revie
w
(Fig. 1). At this stage, 25 papers were excluded, leaving
nine relevant studies, which were appraised for quality,
using the CASP tool (see ESM Online Resources 1 and 3).
One study was excluded on the basis of this assessment
;
therefore, eight studies were included in the analysis.
296 A. Fleming et al.
3.2 Study Characteristics
The details of the included studies are displayed in Table 1.
All studies were conducted in LTCFs. Most studies in-
cluded a mixed health care professional sample of nurses
and doctors. One study included medical directors and
administrators in the sample [14]. The most recently pub-
lished study included nurses, doctors and pharmacists [15].
The focus of the studies was respiratory tract infection
[RTI] (n = 3), urinary tract infection [UTI] (n = 2),
asymptomatic bacteriuria (n = 1) or pneumonia (n = 1),
and another study investigated antibiotic prescribing in
LTCFs in general.
The studies that were included collected their data by
interviews (n = 3) or focus group discussions (n = 2), and
three studies used interviews and focus group discussions.
Three studies were conducted to review the implementa-
tion of an infection management intervention: two re-
viewed an RTI care pathway and one reviewed a UTI care
pathway, implemented during randomized controlled trials
[14, 16, 17].
The quality appraisal of the studies found that all studies
clearly stated their research aims and used qualitative
methods appropriately (see ESM Online Resource 1). The
research design was discussed in detail, and in all studies,
the recruitment of participants was explained and justified.
The method of data collection was presented in sufficient
detail in all studies. One area where nearly all studies were
lacking was that of researcher reflexivity. Two studies did
not state whether they had obtained ethical approval or not
Fig. 1 Flow diagram outlining
the identification of papers from
searches. LTCF Long-term care
facility
Antibiotic Prescribing in Long-Term Care Facilities 297
T
a
b
le
1
C
h
a
ra
c
te
ri
st
ic
s
o
f
th
e
e
ig
h
t
st
u
d
ie
s
in
c
lu
d
e
d
i
n
th
e
sy
n
th
e
si
s
R
e
fe
r
e
n
c
e
s
G
e
o
g
ra
p
h
ic
a
l
lo
c
a
ti
o
n
P
a
rt
ic
ip
a
n
ts
D
a
ta
c
o
ll
e
c
ti
o
n
A
n
a
ly
si
s
A
im
C
a
ru
so
n
e
e
t
a
l.
,
p
a
rt
I
[1
6
]
O
n
ta
ri
o
,
C
a
n
a
d
a
2
4
N
u
rs
e
s
7
F
o
c
u
s
g
r
o
u
p
s,
1
in
te
r
v
ie
w
T
h
e
m
a
ti
c
a
n
a
ly
si
s
(t
e
m
p
la
te
5
p
h
a
se
)
a
T
o
d
e
te
r
m
in
e
n
u
rs
e
s’
p
e
rs
p
e
c
ti
v
e
s
o
n
th
e
u
ti
li
ty
a
n
d
su
st
a
in
a
b
il
it
y
o
f
a
n
R
T
I
p
a
th
w
a
y
C
a
ru
so
n
e
e
t
a
l.
,
p
a
rt
I
I
[1
4
]
O
n
ta
ri
o
,
C
a
n
a
d
a
6
A
d
m
in
is
tr
a
to
rs
,
2
m
e
d
i
c
a
l
d
ir
e
c
to
rs
In
te
rv
ie
w
s
T
h
e
m
a
ti
c
a
n
a
ly
si
s
(t
e
m
p
la
te
5
p
h
a
se
)
T
o
d
e
te
rm
in
e
a
d
m
in
is
tr
a
to
rs
’
v
ie
w
s
o
f
a
n
R
T
I
p
a
th
w
a
y
a
n
d
c
o
m
p
a
re
t
h
e
m
w
it
h
n
u
rs
e
s’
v
ie
w
s
(f
ro
m
C
a
ru
so
n
e
e
t
a
l.
,
p
a
rt
I
[1
6
])
H
e
lt
o
n
e
t
a
l.
[2
1
]
N
e
th
e
rl
a
n
d
s;
N
o
rt
h
C
a
ro
li
n
a
,
U
S
A
P
h
y
si
c
ia
n
s
(N
e
th
e
rl
a
n
d
s:
1
2
;
N
o
rt
h
C
a
ro
li
n
a
:
1
2
)
S
e
m
i-
st
ru
c
tu
re
d
in
te
rv
ie
w
s
E
d
it
in
g
a
n
a
ly
si
sb
T
o
e
x
p
lo
re
th
e
fa
c
to
rs
in
fl
u
e
n
c
in
g
tr
e
a
tm
e
n
t
d
e
c
is
io
n
s
w
h
e
n
n
u
rs
in
g
h
o
m
e
p
a
ti
e
n
ts
w
it
h
d
e
m
e
n
ti
a
b
e
c
o
m
e
a
c
u
te
ly
il
l
w
it
h
p
n
e
u
m
o
n
ia
L
im
e
t
a
l.
[
1
5
]
V
ic
to
ri
a
,
A
u
st
ra
li
a
4
0
N
u
rs
e
s,
1
5
G
P
s,
6
p
h
a
rm
a
c
is
ts
F
o
c
u
s
g
ro
u
p
s,
se
m
i-
st
ru
c
tu
re
d
in
te
rv
ie
w
s
F
ra
m
e
w
o
rk
a
n
a
ly
si
s
T
o
e
x
p
lo
re
p
e
rc
e
p
ti
o
n
s
a
n
d
a
tt
it
u
d
e
s
o
f
k
e
y
h
e
a
lt
h
c
a
re
p
ro
v
id
e
rs
to
w
a
rd
s
a
n
ti
b
io
ti
c
p
re
sc
ri
b
i
n
g
L
o
h
fi
e
ld
e
t
a
l.
[1
7
]
O
n
ta
ri
o
,
C
a
n
a
d
a
;
Io
w
a
,
U
S
A
5
2
N
u
rs
e
s,
1
9
a
d
m
in
is
tr
a
to
rs
1
9
In
te
rv
ie
w
s,
1
0
fo
c
u
s
g
ro
u
p
s
E
d
it
in
g
st
y
le
o
f
a
n
a
ly
si
s
T
o
e
x
a
m
in
e
th
e
v
ie
w
s
o
f
n
u
rs
e
s
a
n
d
a
d
m
in
is
tr
a
to
rs
re
g
a
rd
in
g
a
c
li
n
ic
a
l
p
a
th
w
a
y
f
o
r
m
a
n
a
g
in
g
U
T
Is
R
u
ss
e
ll
a
n
d
G
a
ll
e
n
[2
2
]
E
n
g
la
n
d
8
N
u
rs
e
s,
5
d
o
c
to
rs
2
F
o
c
u
s
g
ro
u
p
s
T
h
e
m
a
ti
c
a
n
a
ly
si
s
T
o
d
e
te
rm
in
e
th
e
fa
c
to
rs
in
fl
u
e
n
c
in
g
a
n
ti
b
io
ti
c
p
re
sc
ri
b
in
g
in
n
u
rs
in
g
h
o
m
e
s
S
c
h
w
e
iz
e
r
e
t
a
l.
[1
8
]
B
e
lf
a
st
,
N
o
rt
h
e
rn
Ir
e
la
n
d
1
0
G
P
s,
1
0
n
u
rs
e
s
S
e
m
i-
st
ru
c
tu
re
d
in
te
rv
ie
w
s
T
h
e
m
a
ti
c
a
n
a
ly
si
s
T
o
e
st
a
b
li
sh
th
e
d
e
c
is
io
n
m
a
k
in
g
p
ro
c
e
ss
fo
r
U
T
Is
b
y
q
u
a
li
ta
ti
v
e
m
e
a
n
s
to
id
e
n
ti
fy
st
e
p
s
in
th
e
p
ro
c
e
ss
W
a
lk
e
r
e
t
a
l.
[2
0
]
O
n
ta
ri
o
,
C
a
n
a
d
a
8
N
u
rs
e
s,
8
d
o
c
to
rs
F
o
c
u
s
g
ro
u
p
T
h
e
m
a
ti
c
a
n
a
ly
si
s
T
o
e
x
p
lo
re
p
e
rc
e
p
ti
o
n
s,
a
tt
it
u
d
e
s
a
n
d
o
p
in
io
n
s
o
f
d
o
c
to
rs
a
n
d
n
u
rs
e
s
a
b
o
u
t
a
sy
m
p
to
m
a
ti
c
b
a
c
te
ri
u
ri
a
G
P
g
e
n
e
ra
l
p
ra
c
ti
ti
o
n
e
r,
R
T
I
re
sp
ir
a
to
ry
tr
a
c
t
in
fe
c
ti
o
n
,
U
T
I
u
ri
n
a
ry
tr
a
c
t
in
fe
c
ti
o
n
a
T
e
m
p
la
te
a
n
a
ly
si
s:
th
e
te
x
t
is
o
rg
a
n
iz
e
d
a
c
c
o
rd
in
g
to
p
re
-e
x
is
ti
n
g
th
e
o
re
ti
c
a
l
o
r
lo
g
ic
a
l
c
a
te
g
o
ri
e
s,
to
p
ro
v
id
e
n
e
w
d
e
sc
ri
p
ti
o
n
s
o
f
p
re
v
io
u
sl
y
k
n
o
w
n
p
h
e
n
o
m
e
n
a
[3
0
]
b
E
d
it
in
g
a
n
a
ly
si
s:
u
n
it
s
in
th
e
te
x
t
a
re
id
e
n
ti
fi
e
d
th
a
t
fo
rm
th
e
b
a
si
s
fo
r
d
a
ta
-d
e
v
e
lo
p
e
d
c
a
te
g
o
ri
e
s;
th
e
se
a
re
u
se
d
to
re
o
rg
a
n
iz
e
th
e
te
x
t
so
th
a
t
th
e
m
e
a
n
in
g
c
a
n
b
e
c
le
a
rl
y
se
e
n
[3
0
]
298 A. Fleming et al.
[17, 18]. One study was excluded on the basis of the quality
assessment, as it was reported as a preliminary qualitative
study, which had a small sample size and did not reach data
saturation [19]. There was no loss of relevant findings on
exclusion of that study. Themes and sub-themes that were
derived from the thematic analysis, with supportive quo-
tations from the studies, are presented in ESM Online
Resource 4. A summary of the presence of the main themes
within each included study is provided in ESM Online
Resource 5.
3.3 Themes
3.3.1 The Long-Term Care Facility Context
The influence of the context of health care delivery in
LTCFs was reported by nurses and doctors in most of
the included studies. In two studies, it was noted that
care of patients in the LTCF setting, rather than in the
acute hospital setting, is better [14, 16]. This is linked to
the relationship between the patient and the nurses and
doctors. When the doctor, nurse or care assistant in the
LTCF knows the patient for many years, it is likely that
they will detect subtle changes in clinical signs and
symptoms that could suggest infection [16, 20, 21].
Doctors providing on-call duty reported difficulty when
managing patients that they did not know well, and they
often prescribed an antibiotic to ‘‘cover themselves’’
[20]. There were many challenges reported by nurses and
doctors in diagnosing patients with infection in LTCFs.
The delay in obtaining microbiology results for urine
samples was perceived as leading to increased empirical
prescribing of antibiotics [15, 17, 18, 22]. Participants
often depend on dipstick test results, interpreting a pa-
tient’s change in behaviour or changes in the urine as a
UTI [18, 20]. The difficulty in collecting urine samples
from these patients was highlighted, as residents are
often bed bound and incontinent [18]. Co-morbidities,
such as cognitive impairment and incontinence, chal-
lenged the nurses’ and doctors’ ability to diagnose in-
fection and conduct the necessary investigations. Not
having a doctor on-site to assess patients as quickly as
possible was also identified as a challenge to fast diag-
nosis and care [16–18, 22]. Prescribing of antibiotics
without assessment by the doctor was referred to in
several studies [17, 18]. The reasons that may have
contributed to this included lack of time on the doctors’
part to visit the LTCF and poor reimbursement for LTCF
patient care, which resulted in reduced visits. Russell and
Gallen [22] reported that many prescriptions were
ordered over the telephone and that nurses were worried
that antibiotic prescribing was conducted as a substitute
for coming to see the patient.
3.3.2 Social Factors Influencing Prescribing
The central role of the LTCF nurse emerged as a very
strong influence on antibiotic prescribing and infection
management, as reported by nurses, doctors, administrators
or pharmacists. It was evident that patient care in the LTCF
is led by nurses, who are primarily responsible for detect-
ing infection, assessing patients, taking microbiology
samples where possible and communicating this informa-
tion to the doctors [15, 20, 22]. Doctors reported that they
depend on and trust the nurses’ judgment in many cases
[15, 20, 22]. In most studies, the doctors reported that nurse
pressure can sometimes lead to increased use of antibiotics
[15]. In general, however, they trust the nurses’ judgment
and recommendations. In two studies, doctors were
sometimes critical of nurses in terms of the quality of
communication and the accuracy of clinical information
conveyed to them [20, 22]. The nurses in the study by
Russell and Gallen [22] expressed frustration when doctors
did not trust their knowledge or judgment. Poor commu-
nication between nurses and doctors was discussed by
Carusone et al. [16] as having an impact on managing
infection; distrust between doctors and nurses may lead to
poor communication, which may compromise the quality
of patient care.
Family pressure on nurses and doctors was a theme that
emerged in seven studies [14, 15, 17, 18, 20–22]. The in-
fluence of residents’ families can result in increased pres-
sure to hospitalize a resident, to have a doctor assess a
resident or to prescribe an antibiotic [15, 20]. The fear of ill
consequences for residents or litigation from the family
was reported as impacting on decision making by doctors
[18, 22]. Some cultural differences within this theme were
found, as participants reported that family wishes had more
influence on doctors’ treatment decisions in the USA than
in the Netherlands [21].
3.3.3 Antimicrobial Resistance
The influence of AMR on antibiotic prescribing was raised
in only three studies [15, 20, 22]. Walker et al. [20] re-
ported that many nurses and doctors appreciate the need for
information to reduce AMR, but there was no further
elaboration around this in relation to antibiotic prescribing.
In the study conducted by Russell and Gallen [22], the
issue of AMR centred on methicillin-resistant Staphylo-
coccus aureus (MRSA), primarily in relation to the
knowledge of testing and treating MRSA. The doctors in
this study felt that their prescribing patterns had changed in
recent years but not as a result of MRSA or public health
concerns. The most recent study, by Lim et al. [15], pre-
sented mixed views in relation to AMR. Some doctors
reported little experience with multidrug resistance (MDR)
Antibiotic Prescribing in Long-Term Care Facilities 299
in their practice [15]. Other doctors reported increased
incidence rates of recurrent UTIs, catheter usage, antibiotic
prophylaxis and chronic wound colonization [15]. Only a
small proportion of nurses in this study were concerned
with AMR, with the main concern being ‘‘infection control
efforts in preventing MDR organism transmission’’ [15].
This study found that only a minority of doctors were
concerned that AMR would impact on their choice of
empirical antibiotics [15]. The views of pharmacists in-
cluded in the study regarding AMR were not presented.
3.3.4 Knowledge and Prescribing Practices
In all studies, the level of knowledge about infections and
antibiotics was reported as varying between health care
professionals [14–18, 20–22]. Walker et al. [20]
specifically investigated why antibiotics are prescribed for
asymptomatic bacteriuria. They noted that many miscon-
ceptions exist in practice about the symptoms of UTI and
that doctors’ and nurses’ views regarding positive dipstick
test results vary [20]. The ambiguity around interpretation
of urine sample results was reiterated in other studies [14,
17, 18, 20, 22]. In many cases, it was suggested that a UTI
was presumed to be present if a patient’s behaviour had
changed or if the urine had a strong smell or concentration
[17, 18, 20, 22]. Walker et al. [20] found that some doctors
would prescribe an antibiotic for an asymptomatic patient
if the urine culture was positive. Nurses in one study re-
ported different prescribing practices between doctors, with
some doctors being more reluctant to prescribe than others,
regardless of the patients’ clinical presentation [20].
The studies by Carusone et al. and Lohfield et al. [14,
16, 17] evaluated the implementation of pathways for
pneumonia and UTI, respectively. The aims of the trials
included reducing antibiotic prescribing. This suggested
existing knowledge on the part of the researchers that an-
tibiotic prescribing was not performed optimally in the
LTCF setting. The lack of implementation of guidelines for
treating UTI or MRSA was explained by a lack of
awareness of the guidelines by doctors [22]. Across all
health care professional groups, the main focus of decision
making was on accurately diagnosing an infection and then
deciding whether or not to prescribe an antibiotic. The
detail of the prescribing process, in terms of the antibiotic
choice, dose and duration of treatment, was not a focal
point across the studies. The issue of prescribing broad-
spectrum antibiotics for the elderly in LTCFs was justified
by doctors in the most recent study [15]. Pharmacists in this
study also raised their concern regarding prolonged dura-
tions of prescriptions [15]. In general, this review found
that many study participants were of the opinion that an-
tibiotic prescribing in their LTCF is ‘‘probably about
right’’. Any negative opinions about antibiotic prescribing
were often made in criticism of other health care profes-
sionals rather than self-criticism [15].
One study reported the views of doctors who felt that the
standards of care in some LTCFs were insufficient. In this
particular study, there seemed to be a ‘‘strain in the rela-
tionship between nursing home staff and GPs [general
practitioners]’’, even though all participants were from
different LTCFs [22]. Such a finding was not reported in
any other study.
Cultural differences in the care of residents with de-
mentia who had pneumonia were noted between par-
ticipants of a study conducted in the USA and the
Netherlands [21]. The USA physicians were reportedly
more inclined to hospitalize residents and to defer to the
families’ decisions. In the Netherlands, physicians were
more likely not to hospitalize and reported giving instruc-
tion to the family regarding the best decision for the resi-
dent. While this sub-theme was linked to the social factors
theme, it was more appropriately assigned as a variation in
knowledge and prescribing practices between these two
cultures. The importance of including that study in the
review was to highlight that there may be cultural differ-
ences between countries in the processes of infection
management and antibiotic prescribing for residents at the
end of life in LTCFs.
3.3.5 Antimicrobial Stewardship and Changing Practices
Two studies did not investigate the influence of AMS on
antibiotic prescribing [18, 21]. Walker et al. [20] recom-
mended improving inter-professional communication and
education, and this recommendation was based on the au-
thors’ own conclusions rather than the opinions of the
participants. Russell and Gallen [22] made several rec-
ommendations, including a review of doctors’ reimburse-
ment for LTCF services, improvement in inter-professional
relations, improvement in arrangements for sample testing
and collection of data regarding antibiotic sensitivities. It
was not evident that these suggestions were made by the
participants.
Of the studies that addressed this issue in detail with
participants, the facilitators and barriers to introducing
AMS strategies in LTCFs were investigated [14–17]. The
main facilitator to implementing changes in practice was
the motivation and ‘‘buy-in’’ of health care
professionals
[14, 17]. Participants noted that the presence of a study
leader or ‘champion’ would improve the implementation of
a new pathway or process by providing extra support and
reassurance for nursing staff [14]. In order to support the
implementation of AMS interventions, it was identified that
skills training and education for doctors and nurses was
needed [15, 17]. The overall positive experiences of using a
pathway, as reported by the participants in the trials
300 A. Fleming et al.
conducted by Carusone et al. and Lohfield et al. [14, 16,
17], provided useful information for future strategies. The
nurses, medical directors and administrators could see the
benefit for patients when implementing the pathways, as a
faster diagnosis was made and patient care was reportedly
improved [14, 16, 17]. Participants recommended that
guidelines or education specifically regarding infection
diagnosis and treatment in LTCFs would be beneficial [15].
Schweizer et al. [18] made specific recommendations to
introduce protocols to guide the management of UTIs, in-
cluding how and when to take a urine sample. It was also
noted that flexibility in terms of deviating from a guideline
or protocol must be allowed, as not every case is likely to
fit a treatment pathway [17].
The concept and principles of AMS were welcomed by
participants in most studies. The facilitators of AMS in-
cluded acceptance by nurses of implementation of quality
improvement initiatives and clinical pathways [15]. The
pharmacists reported willingness to expand their clinical
role in this area but acknowledged that funding would be
required to support this [15]. The promotion of evidence-
based practice was accepted by all health care professionals
as being a key benefit of AMS.
Barriers to implementing AMS and raising awareness of
growing AMR were identified in several studies [14–17].
The strategies involved in AMS and securing the willing-
ness of doctors to accept policies or guidelines can affect
how the interventions are adopted into daily practice [15].
Concern was expressed that non-acceptance of a strategy
by doctors would be problematic for nurses who are willing
to implement new strategies in the LTCF [15]. Some nurses
were concerned about the extra workload and level of re-
sponsibility demanded by these strategies [16]. This related
to lack of confidence and fear of change, which were
highlighted by participants in one study [17]. On the other
hand, it was also reported that nurses’ confidence increased
on implementation of the pathway, as they felt more em-
powered [16]. Another barrier to implementing AMS
pathways was the influence of families, who could pres-
surize nurses and doctors to act against the pathway [17].
4 Discussion
This review is the first to systematically incorporate the
findings of all qualitative investigations of antibiotic pre-
scribing in LTCFs. This study outlines the many factors
that influence antibiotic prescribing in LTCFs and also the
challenges facing AMS strategies in LTCFs. The key issues
are the contextual features of LTCF care, coupled with
variable knowledge and practices in managing infection,
which are all subject to heavy social factors. The inter-
dependent relationship between nurses and doctors in
LTCFs is a unique one, as most doctors are not on-site. It
was encouraging to find that many participants in these
studies welcomed the opportunity for further training or
education, suggesting that there is an acceptance of change
and AMS in LTCFs. One challenge in changing antibiotic
prescribing behaviours in LTCFs is that many participants,
as identified in this study, were not self-critical regarding
antibiotic prescribing at their LTCF. This synthesis study
has contributed a greater understanding of the factors in-
fluencing antibiotic prescribing in LTCFs. There was a
noteworthy similarity in themes emerging from all of the
included studies, which reinforces the validity of the
findings of this review.
LTCF context:
– Lack of LTCF resources
(doctors, diagnos�c
equipment).
– Care in LTCF priority over
hospitalisa�on.
Social Factors:
– Central role of nurse
– Influence of family
Knowledge & prac�ce:
– Variable knowledge of
diagnosis & prescribing
guidelines
– Variable prescribing prac�ce
between doctors
LTCF An�microbial resistance
informa�on
LTCF An�microbial
Stewardship:
Customised to the
LTCF se�ng.
Consider all relevant
informa�on.
Address local barriers
& facilitators.
Con�nuous An�microbial
prescrip�on surveillance.
Outcomes:
– An�bio�c prescribing rates
– Adherence to prescribing
guidelines
– Feedback from healthcare
professionals
Current influencing factors Strategies to be incorporated
Fig. 2 Conceptual model of the
factors influencing antibiotic
prescribing in long-term care
facilities (LTCFs) and
recommendations for
interventions
Antibiotic Prescribing in Long-Term Care Facilities 301
4.1 Analytical Theme
Through synthesis of the individual themes and descriptive
themes, the overall analytical theme was generated, and a
conceptual model is proposed in Fig. 2. Antibiotic pre-
scribing in LTCFs is a process that begins before the point
of actual prescribing, as it is heavily influenced by the
LTCF context of care. The challenges of shared decision
making between nurses and doctors, the variability in
knowledge of up-to-date evidence and the social relation-
ships underlining all of this activity have an impact on the
decision about whether or not to prescribe an antibiotic.
There was a notable absence of discussion about antibiotic
surveillance by the participants and authors of the included
studies. It is possible that continuous monitoring of an-
tibiotic prescribing trends and practices may influence
doctors and nurses by encouraging reflection and providing
evidence to support AMS strategies. Evidence exists to
support the effect of audits and feedback on improving
prescribing practices [23]. The implementation of AMS
initiatives in LTCFs will need to take into account the
complexity of the context of care in this setting. It has
already been established that there are numerous social,
cultural and contextual factors influencing prescribing
processes in LTCFs that are not present in other health care
settings [24]. The factors faced by health care professionals
on a daily basis, such as lack of on-site resources, will
impact on the implementation of any quality improvement
strategy. This has been reported in a recent AMS inter-
vention study in North Carolina, USA [5]. The existing
variability in knowledge and practices within and between
LTCFs will challenge the content of AMS. It has been
identified that the use of theory to inform behavioural
change interventions can contribute to the success of the
intervention [25]. A gap in the research identified by this
review was the lack of qualitative research underpinned by
a behavioural change theory or theoretical framework to
explain the antibiotic prescribing behaviours in more de-
tail. Efforts to work towards evidence-based practice must
allow for local consensus and AMS strategies that are
customized for the LTCF setting on the local and national
levels. This will improve the likelihood of participant
support for, and acceptance of, AMS in LTCFs.
4.2 Comparison with Other Research
Previous systematic reviews of qualitative research inves-
tigating opinions on and experiences of antibiotic pre-
scribing have been conducted in the primary care and
hospital care settings [8]. There are some similarities and
differences in the findings between these settings and the
LTCF setting. Tonkin-Crine et al. [6] found that there was
often uncertainty around RTI diagnosis and management in
primary care, which was also identified in LTCFs. In pri-
mary care, however, GPs have to manage pressure from
patients, rather than their families, which is the case in
LTCF studies. In secondary care settings, it has been re-
ported that AMR is perceived as a national problem rather
than a local one [26]. A multi-country qualitative investi-
gation of doctors’ perceptions of AMR in primary care
found that most participants stated that AMR was not a
problem in their practice [27]. This is mirrored to some
degree in the findings of this review, as very little asso-
ciation between AMR and antibiotic prescribing in LTCFs
was noted by the participants. An analysis of LTCF pre-
scribing databases in Ontario, Canada, found that the du-
ration of antibiotic prescriptions in LTCFs was largely
driven by prescriber preference rather than by patient fac-
tors [28]. The variability in doctors’ antibiotic prescribing
practices that was identified as a theme in this review
concurs with this.
4.3 Strengths and Limitations
This is the first study to synthesize the qualitative evidence
on the opinions and experiences of health care profes-
sionals regarding antibiotic prescribing in LTCFs. This
review complements the quantitative studies that have
analysed antibiotic prescribing in LTCFs, such as the point
prevalence studies conducted across Europe in recent years
[29]. There were some limitations in this review. Certain
included studies did not focus solely on antibiotic pre-
scribing in LTCFs, for example. The aim of the study by
Russell and Gallen [22] was to investigate factors influ-
encing antibiotic prescribing, but a large focus of the
findings related to MRSA only. The included studies were
of variable quality following the application of the CASP
appraisal tool. No study explicitly addressed researcher
reflexivity, but we overlooked this. In the case of this re-
view, the emergence of similar themes across all of the
studies overcame this limitation. Through inclusion only of
studies that related to LTCFs, the importance of the context
and health care organization was protected. The synthesis
of the findings in terms of discussing factors influencing
AMS in LTCFs attempted to increase the clinical relevance
of the review results. The findings were credible, and
sufficient supportive data existed for synthesis of the
findings for the purposes of this review.
5 Conclusion
This meta-synthesis review highlighted some key influ-
ences on antibiotic prescribing in LTCFs. The specific
LTCF context factors, such as the relationship between the
GP or nurse and the patient, restricted access to resources
302 A. Fleming et al.
and social factors (for example, the central role of the
nurse) have an important impact on antibiotic prescribing
in LTCFs. The need for multidisciplinary collaborative
AMS strategies to address the variability in practice and
knowledge, and to increase the awareness of AMR, is
evident. This synthesis of existing studies may contribute
important information to the development of future high-
quality studies addressing antibiotic prescribing in LTCFs.
Acknowledgments This research was supported by the Health
Research Board in Ireland under Grant Number PHD/2007/16.
Open Access This article is distributed under the terms of the
Creative Commons Attribution Noncommercial License which per-
mits any noncommercial use, distribution, and reproduction in any
medium, provided the original author(s) and the source are credited.
References
1. van Buul LW, van der Steen JT, Veenhuizen RB, Achterberg WP,
Schellevis FG, Essink RT, et al. Antibiotic use and resistance in
long term care facilities. J Am Med Dir Assoc. 2012;13(6):568
e1–13.
2. Nicolle L, Bentley D, Garibaldi R, Neuhaus E, Smith P. An-
timicrobial use in long term care facilities. Infect Control Hosp
Epidemiol. 2000;21(8):537–45.
3. Kuehn BM. ‘‘Nightmare’’ bacteria on the rise in US hospitals,
long-term care facilities. JAMA. 2013;309(15):1573–4.
4. Fleming A, Browne J, Byrne S. The effect of interventions to
reduce potentially inappropriate antibiotic prescribing in long-
term care facilities: a systematic review of randomised controlled
trials. Drugs Aging. 2013;30(6):401–8.
5. Zimmerman S, Sloane PD, Bertrand R, Olsho LE, Beeber A,
Kistler C, et al. Successfully reducing antibiotic prescribing in
nursing homes. J Am Geriatr Soc. 2014;62(5):907–12.
6. Tonkin-Crine S, Yardley L, Little P. Antibiotic prescribing for
acute respiratory tract infections in primary care: a systematic
review and meta-ethnography. J Antimicrob Chemother.
2011;66(10):2215–23.
7. Charani E, Edwards R, Sevdalis N, Alexandrou B, Sibley E,
Mullett D, et al. Behavior change strategies to influence antimi-
crobial prescribing in acute care: a systematic review. Clin Infect
Dis. 2011;53(7):651–62.
8. TeixeiraRodrigues A, Roque F, Falcao A, Figueiras A, Herdeiro
MT. Understanding physician antibiotic prescribing behaviour: a
systematic review of qualitative studies. Int J Antimicrob Agents.
2013;41(3):203–12.
9. Kastner M, Tricco AC, Soobiah C, Lillie E, Perrier L, Horsley T,
et al. What is the most appropriate knowledge synthesis method
to conduct a review? Protocol for a scoping review. BMC Med
Res Methodol. 2012;12(1):114.
10. Grant M, Booth A. A typology of reviews: an analysis of 14
review types and associated methodologies. Health Inform Libr J.
2009;26(2):91–108.
11. Critical Appraisal Skills Programme (CASP). Qualitative re-
search checklist. Collaboration for Qualitative Methodologies.
2006. http://media.wix.com/ugd/dded87_29c5b002d99342f788c6
ac670e49f274 . Accessed 8 July
2014.
12. Thomas J, Harden A. Methods for the thematic synthesis of
qualitative research in systematic reviews. BMC Med Res
Methodol. 2008;8:45.
13. Tong A, Flemming K, McInnes E, Oliver S, Craig J. Enhancing
transparency in reporting the synthesis of qualitative research:
ENTREQ. BMC Med Res Methodol. 2012;12:181.
14. Carusone SC, Loeb M, Lohfeld L. A clinical pathway for treating
pneumonia in the nursing home: part II. The administrators’
perspective and how it differs from nurses’ views. J Am Med Dir
Assoc. 2006;7(5):279–86.
15. Lim CJ, Kwong M, Stuart RL, Buising KL, Friedman ND,
Bennett N, et al. Antimicrobial stewardship in residential aged
care facilities: need and readiness assessment. BMC Infect Dis.
2014;14:410.
16. Carusone SC, Loeb M, Lohfeld L. A clinical pathway for treating
pneumonia in the nursing home: part I. The nursing perspective.
J Am Med Dir Assoc. 2006;7(5):271–8.
17. Lohfeld L, Loeb M, Brazil K. Evidence-based clinical pathways
to manage urinary tract infections in long-term care facilities: a
qualitative case study describing administrator and nursing staff
views. J Am Med Dir Assoc. 2007;8(7):477–84.
18. Schweizer AK, Hughes CM, Macauley DC, O’Neill C. Managing
urinary tract infections in nursing homes: a qualitative assess-
ment. Pharm World Sci. 2005;27(3):159–65.
19. Longo DR, Young J, Mehr D, Lindbloom E, Salerno LD. Barriers
to timely care of acute infections in nursing homes: a preliminary
qualitative study. J Am Med Dir Assoc. 2004;5(2 Suppl):S4–10.
20. Walker S, McGeer A, Simor AE, Armstrong-Evans M, Loeb M.
Why are antibiotics prescribed for asymptomatic bacteriuria in
institutionalized elderly people? A qualitative study of physi-
cians’ and nurses’ perceptions. CMAJ. 2000;163(3):273–7.
21. Helton MR, van der Steen JT, Daaleman TP, Gamble GR, Ribbe
MW. A cross-cultural study of physician treatment decisions for
demented nursing home patients who develop pneumonia. Ann
Fam Med. 2006;4(3):221–7.
22. Russell JG, Gallen D. Influencing factors on antimicrobial pre-
scribing in nursing homes. Primary Health Care Res Develop.
2003;4(1):69–75.
23. Ivers N, Jamtvedt G, Flottorp S, Young JM, Odgaard-Jensen J,
French SD, O’Brien MA, Johansen M, Grimshaw J, Oxman AD.
Audit and feedback: effects on professional practice and health-
care outcomes. Cochrane Database Syst Rev. 2012;(6):CD000
259. doi:10.1002/14651858.CD000259.pub3.
24. Hughes CM, Lapane K, Watson MC, Davies HT. Does organisa-
tional culture influence prescribing in care homes for older people?
A new direction for research. Drugs Aging. 2007;24(2):81–93.
25. Michie S, Atkins L, West R. The behaviour change wheel: a
guide to designing interventions. London: Silverback Publishing;
2014.
26. Giblin T, Sinkowitz-Cochran R, Harris P. Clinician’s perceptions
of the problem of antimicrobial resistance in health care facilities.
Arch Intern Med. 2004;164:1662–8.
27. Wood F, Phillips C, Brookes-Howell L, Hood K, Verheij T,
Coenen S, et al. Primary care clinicians’ percriptions of antibiotic
resistance: a multi-country qualitative interview study. J Antimi-
crob Chemother. 2013;68:237–43.
28. Daneman N, Gruneir A, Bronskill SE. Prolonged antibiotic
treatment in long-term care: role of the prescriber. JAMA Internal
Med. 2013;173(8):673–82.
29. Cotter M, Donlon S, Roche F, Byrne H, Fitzpatrick F. Health-
care-associated infection in Irish long-term care facilities: results
from the First National Prevalence Study. J Hosp Infect.
2012;80(3):212–6.
30. Malterud K. Qualitative research: standards, challenges and
guidelines. Lancet. 2001;358:483–8.
Antibiotic Prescribing in Long-Term Care Facilities 303
http://media.wix.com/ugd/dded87_29c5b002d99342f788c6ac670e49f274
http://media.wix.com/ugd/dded87_29c5b002d99342f788c6ac670e49f274
http://dx.doi.org/10.1002/14651858.CD000259.pub3
Copyright of Drugs & Aging is the property of Springer Science & Business Media B.V. and
its content may not be copied or emailed to multiple sites or posted to a listserv without the
copyright holder’s express written permission. However, users may print, download, or email
articles for individual use.
- Antibiotic Prescribing in Long-Term Care Facilities: A Meta-synthesis of Qualitative Research
Abstract
Objectives
Methods
Results
Conclusion
Introduction
Methods
Search Strategy
Study Inclusion Criteria
Quality Appraisal
Analysis
Results
Study Selection Process
Study Characteristics
Themes
The Long-Term Care Facility Context
Social Factors Influencing Prescribing
Antimicrobial Resistance
Knowledge and Prescribing Practices
Antimicrobial Stewardship and Changing Practices
Discussion
Analytical Theme
Comparison with Other Research
Strengths and Limitations
Conclusion
Acknowledgments
References