# Resident-, prescriber-, and facility-level factors associated with antibiotic use in long-term care facilities: a systematic review of quantitative studies

Aurélie Bocquier, Berkehan Erkilic, Martin Babinet, Céline Pulcini, Nelly Agrinier

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Aurélie Bocquier, Berkehan Erkilic, Martin Babinet, Céline Pulcini, Nelly Agrinier. Resident-, prescriber-, and facility-level factors associated with antibiotic use in long-term care facilities: a systematic review of quantitative studies. Antimicrobial Resistance and Infection Control, 2024, 13 (1), pp.29. 10.1186/s13756-024-01385-6. hal-04505771

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# Resident-, prescriber-, and facility-level factors associated with antibiotic use in long-term care facilities: a systematic review of quantitative studies

Aurélie Bocquier¹*, Berkehan Erkilic¹, Martin Babinet², Céline Pulcini¹,³, Nelly Agrinier¹,² and
on behalf of the ORANEAT Study Group

## Abstract

**Background** Antimicrobial stewardship programmes are needed in long-term care facilities (LTCFs) to tackle antimicrobial resistance. We aimed to identify factors associated with antibiotic use in LTCFs. Such information would be useful to guide antimicrobial stewardship programmes.

**Method** We conducted a systematic review of studies retrieved from PubMed, Cochrane Library, Embase, APA PsycArticles, APA PsycINFO, APA PsycTherapy, ScienceDirect and Web of Science. We included quantitative studies that investigated factors associated with antibiotic use (i.e., antibiotic prescribing by health professionals, administration by LTCF staff, or use by residents). Participants were LTCF residents, their family, and/or carers. We performed a qualitative narrative synthesis of the findings.

**Results** Of the 7,591 screened records, we included 57 articles. Most studies used a longitudinal design (n = 34/57), investigated resident-level (n = 29/57) and/or facility-level factors (n = 32/57), and fewer prescriber-level ones (n = 8/57). Studies included two types of outcome: overall volume of antibiotic prescriptions (n = 45/57), inappropriate antibiotic prescription (n = 10/57); two included both types. Resident-level factors associated with a higher volume of antibiotic prescriptions included comorbidities (5 out of 8 studies which investigated this factor found a statistically significant association), history of infection (n = 5/6), potential signs of infection (e.g., fever, n = 4/6), positive urine culture/dipstick results (n = 3/4), indwelling urinary catheter (n = 12/14), and resident/family request for antibiotics (n = 1/1). At the facility-level, the volume of antibiotic prescriptions was positively associated with staff turnover (n = 1/1) and prevalence of after-hours medical practitioner visits (n = 1/1), and negatively associated with LTCF hiring an on-site coordinating physician (n = 1/1). At the prescriber-level, higher antibiotic prescribing was associated with high prescription rate for antibiotics in the previous year (n = 1/1).

**Conclusions** Improving infection prevention and control, and diagnostic practices as part of antimicrobial stewardship programmes remain critical steps to reduce antibiotic prescribing in LTCFs. Once results confirmed

Full list of author information is available at the end of the article

<footnote>*Correspondence:
Aurélie Bocquier
aurelie.bocquier@univ-lorraine.fr</footnote>
by further studies, implementing institutional changes to limit staff turnover, ensure the presence of a professional accountable for the antimicrobial stewardship activities, and improve collaboration between LTCFs and external prescribers may contribute to reduce antibiotic prescribing.

**Keywords** Anti-bacterial agents, Nursing homes, Long-term care, Epidemiologic factors, Systematic review

**Introduction**

Antimicrobial resistance (AMR) is one of the top 10 global health threats according to the World Health Organisation (WHO) [1, 2]. AMR, notably bacterial resistance to antibiotics, is of particular concern in long-term care facilities (LTCFs) where antibiotic use is frequent and often unnecessary or inappropriate [3] and antibiotic-resistant bacteria more prevalent than in the community [4].

Antimicrobial stewardship (AMS) (i.e., a coherent set of actions which promote using antimicrobials responsi-bly [5]) has proven effective in reducing antimicrobial use (in particular broad-spectrum antibiotics), prevalence of multidrug resistant organisms (MDRO), and total costs of care in different healthcare settings [6–8]. Evidence suggests greater effectiveness in intensive care units [8] and in paediatric care settings [6] than in LTCFs for which evidence is scarce, inconsistent, and of low quality [9–11]. The AMS interventions in LTCFs mainly involved multiple components, most often educational strategies and promotion of clinical guidelines targeting both phy-sicians and nurses; few interventions used tailored strate-gies adapted to the local LTCF context [9, 10]. Besides, studies that have conducted a process evaluation showed that adoption of interventions by facilities and staff was low [10].

LTCFs are indeed challenging settings for AMS imple-
mentation [12]. Due to less specific symptoms, comor-
bidities, and impaired ability to report symptoms, the
diagnostic process is often complex in LCTF residents.
Moreover, LCTFs often face staff turnover and absentee-
ism, and a lack of resources dedicated to quality moni-
toring and improvement [12]. All of these specificities
combined hinder implementation of AMS programmes.
In addition, specific determinants of antibiotic use in
LCTFs might have been overlooked in the development
of AMS programmes so far. This might explain part of
the inconsistent evidence about AMS programme effec-
tiveness in LCTFs [9–11].

One meta-synthesis of qualitative studies highlighted
that specific contextual factors (e.g., restricted access to
on-site resources) and social factors (e.g., nurses' central
role) critically impact antibiotic prescribing in LCTFs
[13]. However, to date, to the best of our knowledge, no
study has reviewed the empirical evidence derived from
quantitative studies identifying factors significantly asso-
ciated with antibiotic use in LCTFs.

Therefore, we conducted a systematic review of quanti-
tative studies to identify and summarise the factors asso-
ciated with antibiotic use among residents in LTCFs.

Methods

Search strategy

We followed the Preferred Reporting Items for System-
atic reviews and Meta-Analyses (PRISMA) 2020 state-
ment guidelines (see checklist in Table S1) [14], and
registered the protocol with the International Prospec-
tive Register of Systematic Reviews (PROSPERO) data-
base (registration number CRD42022345784).

We identified peer-reviewed journal articles published
from inception until the 24th of May, 2022 on the follow-
ing databases: MEDLINE (PubMed), Cochrane Library,
Embase, APA PsycArticles, APA PsycINFO, APA Psyc-
Therapy, ScienceDirect, and Web of Science. We also
crosschecked reference lists of all included articles.

We used keywords and MeSH terms at the intersec-
tion of three topics: “antibiotic use”, “LTCF”, and “factors/
determinants” (see search strategies in Table S2). For the
purpose of this review, LTCFs were defined as structures
accommodating dependent yet medically stable older
adults and providing adapted medical and paramedi-
cal care in a permanent or temporary arrangement [15].
They typically provided 24-hour supervision and a high
level of nursing care, but did not provide specialised
medical care or invasive medical procedures.

Eligibility criteria

Studies were eligible for inclusion if they met the fol-
lowing criteria. First, study population of eligible studies
included either LTCF residents, their family (i.e., people
who are related to the residents, such as their children,
nephews/nieces, brothers/sisters), and/or carers, espe-
cially all health professionals who may play a role in
antibiotic use among LTCF residents. Second, eligible
studies focused on exposure to factors of any kind, as for
example factors related to patients, health professionals,
or LTCFs' characteristics. Third, eligible studies included
any outcome related to antibiotic use: e.g., antibiotic
prescribing by health professionals (volume or inappro-
priateness, e.g. prolonged treatment duration), adminis-
tration by LTCF staff, use (including self-medication) by
residents. Fourth, eligible studies relied on the following
design: ecological, cross-sectional, case-control, or lon-
gitudinal studies quantitatively assessing associations
between exposure and outcome. We excluded literature
reviews and studies that addressed effectiveness of a formal AMS programmes as their primary objective.

After the removal of duplicates, two reviewers (among B.E. M.B., and A.B.) independently screened articles based on titles and abstracts. Then two reviewers (among B.E., M.B., A.B., and N.A.) independently screened retrieved full texts against the eligibility criteria. The screening process used the free web application Rayyan [16]. Differences between authors were resolved through consensus and the opinion of a third reviewer when needed.

## Data extraction

Two reviewers (A.B. and B.E.) independently performed data extraction for ten articles, and solved discrepancies by consensus. The remaining articles were divided in two batches, and each reviewer extracted data for all articles in one of the two batches.

The following information was extracted: study characteristics (first author, year of publication, journal, study country, year/period of data collection, study objective, design and sample size), participants' characteristics, type of statistical analysis, outcome measures (nature, definition, unit, data collection method), and the list of the factors investigated (nature, definition, and unit). For each factor that was statistically significantly (i.e., $p \le 0.05$) associated with at least one outcome, we extracted the main findings (direction and magnitude of the association, and p-value).

## Quality assessment

We assessed studies for quality of reporting using a purpose-built standardised tool adapted from the Strengthening the Reporting of Observational Studies in Epidemiology (STROBE) statement checklist [17]. We included 16 items assessing the quality of reporting of the study design, setting, eligibility criteria for participants, sample size, variables, data source, method of measurement, and statistical methods (Table S3). For each study, based on the extracted data, the reviewer coded each item 0 (poor quality of reporting) or 1 (good quality of reporting) and then calculated the study score by summing the 16 items' code (theoretical range: 0 for minimal quality of reporting to 16 for maximal quality of reporting).

## Data synthesis

First, we conducted a descriptive synthesis of studies' characteristics (e.g., design, type of outcomes, and factors investigated).

Second, due to heterogeneity pertaining to selected outcomes, metrics of the factors investigated, and the methods used across studies, we could not perform a meta-analysis, and thus provided a qualitative narrative

synthesis of the findings. To make interpretation easier, relying on thematic content analysis, we grouped the factors investigated in the included studies into categories and sub-categories, defined by consensus between researchers involved in the review and derived from classifications of determinants of antibiotic use applied in other settings (e.g., in primary care settings) [18–20]. We identified five categories of factors: resident-level, prescriber-level, prescription-level, facility-level and other contextual factors (e.g., year, season).

For each category of outcome and factor identified, we relied on the number of studies that found a statistically significant positive association (i.e., $p \le 0.05$), a statistically significant negative association (or both types of association depending on the outcome for example), and the number of studies that found no statistically significant association. For each factor, if >50% of the studies which investigated the factor showed a statistically significant association in the same direction, we used the term “trend toward” to summarise the results in the Results section; in other cases, we used the term “mixed results”. For each factor with a trend, we described five of the Hill's criteria for causation [21]. We assessed temporality using the number of longitudinal studies over the number of studies that found a statistically significant association consistent with the trend. We also assessed strength (e.g., RR, OR), and dose-response relationship (coded as ‘yes’ if a dose-response relationship was observed in at least one study; ‘no’ if there was no dose-response relationship in any study or ‘not applicable’ if the factor metrics did not allow to measure a dose-response relationship). Then we assessed internal consistency (i.e., number of studies that used adjusted analyses over the number of studies that found a statistically significant association consistent with the trend) and reproducibility (i.e., the number of studies that found a statistically significant association consistent with the trend over the total number of studies that investigated the concerned factor).

## Results

### Study selection and characteristics

We identified 11,326 records. After removing duplicates, we selected 300 articles based on title and abstract, of which 57 [19, 22–77] met the inclusion criteria after full-text reading (see the flow diagram in Fig. 1, the list of full-text reports that could not be retrieved or excluded in Table S4, and the list of the included articles in Table S5).

Characteristics of the included studies are described in Fig. 2 and Table S6. Most studies used data collected in North America (30/57), and a longitudinal (34/57) or cross-sectional (20/57) design. Adjusted statistical analyses were performed in 35/57 studies (Table S6).
<figure><img src="image_3.png" /><figcaption>**Fig. 1** PRISMA 2020 flow diagram for the systematic review of quantitative studies on the factors associated with antibiotic use in LTCFs
LTCF, long-term care falicity</figcaption></figure>

The quality of reporting score ranged from 7 to 15 (median=12). Only 8/57 studies reported any efforts to address potential sources of bias and 7/57 how missing data were handled (Table S3).

Studies included two main types of outcome. First, overall volume of antibiotic prescriptions (n=45/57), at the resident-level (e.g., being prescribed an antibiotic on the index assessment date, antibiotic days of therapy per 1,000 resident days) or aggregated at the facility-level (number of antibiotic courses started per 1,000 resident care days per month, total antibiotic prescriptions in defined daily doses per 100 bed-days). Second, inappropriate antibiotic prescription (n=10/57) (e.g., in terms of antibiotic drug indication, choice, dose, and/or treatment duration). Two studies included both types of outcomes.

Factors investigated in the included studies related either to the resident, the prescriber, the LCTF's characteristics, or to other contextual factors (e.g., year, season). Only three studies investigated simultaneously resident, prescriber, and facility-level factors (Fig. 2).

### Factors associated with overall volume of antibiotic prescriptions

Figure 3 displays a summary of the evidence on the factors associated with overall volume of antibiotic prescriptions (see Table S7 for detailed results by study). Out of 47 studies including at least one "overall volume of antibiotic prescriptions" outcome, 43 found at least one statistically significant association with at least one of the factors investigated (see Table S8 for
<figure><img src="image_4.png" /><figcaption>**Fig. 2** Main characteristics of selected studies about factors associated with antibiotic use (n=57)</figcaption></figure>

DCE, Discrete Choice Experiment; UK, United Kingdom; USA, United States of America.

detailed results on these associations and Table S9 for
details on the Hill's criteria for causation).

Example at the facility-level, two studies assessed the association between the LTCF country (USA or Canada) and the overall volume of antibiotic prescriptions; one found no significant association; one found higher anti-biotic prescriptions in the USA as compared to Canada.

Factor written (i) in grey: factor investigated in at least one study but which has not been statistically significantly associated with the outcome in any of them; (ii) in black: factor investigated in at least one study and which was statistically significantly associated with the outcome in at least one of them.

Resident-level factors

Resident-level factors investigated related to residents'
demographic characteristics (n=18/47), health status,
either general status or history/potential signs of infec-
tion (n=20/47), lab test results (n=5/47), devices or
treatments (n=15/47), or other factors (n=7/47).

Regarding residents' demographic characteristics, we
found mixed results on the association between age,
gender, or ethnicity, and overall volume of antibiotic
prescriptions.

Regarding the general health status, there was a trend toward higher antibiotic prescriptions among residents having comorbidities (n=5/8) and lower antibiotic prescriptions among residents with dementia (n=6/9). Evidence for both characteristics came from longitudinal studies, adjusted analyses, and showed a dose-response relationship (Table S9). Results also showed a trend toward higher antibiotic prescriptions among residents with a history of infection (n=5/6) and those with potential signs of infection (e.g., confusion/agitation, fever, specific symptoms of urinary tract infection [UTI]).

We also found a trend toward higher antibiotic pre-
scriptions among residents with positive urine culture/
dipstick results (n=3/4) and those with an indwelling
urinary catheter (n=12/14), who were two to three times
more likely to be prescribed an antibiotic (Table S9).

One study found higher antibiotic use in case of anti-
biotic request by the resident or his/her family (n=1/1).

<footnote>* One study included data from the USA and from Canada and one study included data from the USA and the Netherlands.</footnote>

<footnote>† Last year of data collection.</footnote>

<footnote>‡ All in all, 32 studies investigated resident-level factors, 32 facility-level factors, and 8 prescriber-level factors.</footnote>
<figure><img src="image_5.png" /><figcaption>**Fig. 3** Factors associated with the overall volume of antibiotic prescriptions in LTCFs: summary of the evidence from quantitative studies included in the systematic review (n = 47)</figcaption></figure>

AMS, antimicrobial stewardship; GP, general practitioner; LTCF, long-term care facility; NH, nursing home; SSTI, skin and soft tissue infection; USA, United States of America; UTI, urinary tract infection; WHO, World Health Organisation.

n in brackets: number of studies that investigated this factor.

For each study:

Ø Non significant association between the factor investigated and the outcome.

+ Significant (p≤0.05) positive association (i.e., associated with higher overall volume of antibiotic prescriptions).

- Significant (p≤0.05) negative association (i.e., associated with lower overall volume of antibiotic prescriptions).

± Significant positive or negative association, depending on the outcome/factor variable.
### Prescriber-level and prescription-level factors

Prescriber-level factors investigated related to prescribers' demographic (n=5/47), professional characteristics (n=4/47), prescribing habits (n=2/47), and attitudes (n=1/47).

Few studies (n=1/1 each time) found characteristics associated with lower antibiotic prescriptions (e.g., graduated in Canada, having a training in bioethics) or higher antibiotic prescriptions (e.g., having a high prescription rate for antibiotics or for other medications in the previous year).

### Facility-level factors

Facility-level factors investigated related to facility's general characteristics (n=17/47), residents' characteristics aggregated at the facility-level (n=13/47), organisational factors (n=16/47), routine AMS activities (n=6/47), diagnostic and prescribing practices (n=6/47), and other factors (n=4/47).

Results regarding the association between overall volume of antibiotic prescriptions and LTCF's general characteristics (e.g., location) were mixed.

Regarding residents' characteristics aggregated at the facility-level, we found a trend toward higher antibiotic prescriptions in LTCFs with a high infection rate (n=4/6).

As part of the LTCF's organisational factors, studies showed mixed results regarding the association between the overall volume of antibiotic prescriptions and both healthcare assistant staff and nurse staff. One cross-sectional study found a positive association between staff turnover and volume of antibiotic prescriptions for respiratory tract infections (RTIs) (n=1/1). In terms of management, one cross-sectional study found lower antibiotic prescriptions in LTCFs having an internal coordinating physician (n=1/1). Longitudinal studies also found higher antibiotic prescriptions among LTCFs with a high prevalence of after-hours medical practitioner visits (n=1/1) and a high number of prescribers (n=1/1).

Few studies (n=1/1 each time) found a higher volume of antibiotic prescriptions in case of antibiotic request by nurses or use of some routine diagnostic procedures (e.g., microbiological sample taken before any antibiotic prescription).

### Other contextual factors

Few studies reported temporal variation in the volume of antibiotic prescriptions. Higher antibiotic prescriptions in 2017 vs. 2014 (n=1/1), lower antibiotic prescriptions in 2020 vs. 2019 (n=1/1) and in summer season (n=2/2) were noted.

### Factors associated with inappropriate antibiotic prescription

Figure 4 displays a summary of the evidence on the factors associated with inappropriate antibiotic prescription (see Table S10 for detailed results by study). Out of 12 studies including at least one “inappropriate antibiotic prescription” outcome, 11 found at least one statistically significant association with at least one of the factors investigated (see Table S11 for detailed results on these associations and Table S12 for details on the Hill's criteria for causation).

*Example* at the resident-level, three studies assessed the association between ethnicity and inappropriateness of antibiotic prescription; one found that being African American was associated with a lower risk of inappropriate antibiotic prescription; two others found no significant association.

Factor written (i) in grey: factor investigated in at least one study but which has not been statistically significantly associated with the outcome in any of them; (ii) in black: factor investigated in at least one study and which was statistically significantly associated with the outcome in at least one of them.

### Resident-level factors

Resident-level factors investigated related to residents' demographic characteristics (n=5/12), health status (n=6/12), lab test results (n=1/12), devices or treatments (n=2/12), or other factors (n=2/12).

We found a trend toward a lower risk of inappropriate antibiotic prescription among residents with a diagnosis of chronic obstructive pulmonary disease (n=2/3) and a higher risk among those with UTI or lower RTI (vs. skin and soft tissue infection) (n=1/1).

### Prescriber-level and prescription-level factors

One longitudinal study using adjusted analyses found that older male prescribers were more prone to inappropriate antibiotic prescription than others (n=1/1), as those used to prescribe longer antibiotic treatment duration during the previous year (n=1/1), with a dose-response relationship (Table S12).

Inappropriate antibiotic prescription was more frequent when antibiotic was initiated in an outpatient clinic (vs. in nursing home) (n=1/1), administered as prophylaxis (n=1/1), or topically (n=1/1). On the contrary, documentation of a treatment review or a stop date reduced the risk of inappropriate antibiotic prescription (n=1/1).

### Facility-level factors

One study found significant variation in inappropriate antibiotic prescription between LTCFs (n=1/1) and a
<figure><img src="image_6.png" /><figcaption>**Fig. 4** Factors associated with inappropriate antibiotic prescription in LTCFs: summary of the evidence from quantitative studies included in the systematic review (n = 12) LTCF, long-term care facility; UTI, urinary tract infection. n in brackets: number of studies that investigated this factor.</figcaption></figure>

For each study:

Ø Non significant association between the factor and the outcome.

+ Significant (p≤0.05) positive association (i.e., associated with a higher risk of inappropriateness of antibiotic prescription).

- Significant (p≤0.05) negative association (i.e., associated with a lower risk of inappropriateness of antibiotic prescription).

± Significant positive or negative association, depending on the outcome/factor variable.

higher risk of inappropriate antibiotic prescription in urban proprietary facilities (n = 1/1).

## Discussion

### Key results: an interplay of individual, organisational and other contextual factors associated with antibiotic use in LTCFs

In this systematic review of 57 quantitative studies, resident-level factors associated with a higher volume of antibiotic prescriptions included comorbidities, history of infection, potential signs of infection, positive urine culture/dipstick results and indwelling urinary catheter. At the facility-level, the volume of antibiotic prescriptions was positively associated with infection rate. A few studies also showed higher antibiotic prescribing in LTCFs with high staff turnover, prevalence of after-hours medical practitioner visits, and number of prescribers; it was lower in LTCFs having an internal coordinating physician. At the prescriber-level, a few studies found higher antibiotic prescribing among prescribers with a high prescription rate for antibiotics or for other medications in the previous year. A few studies showed that

inappropriate antibiotic prescription was more frequent when antibiotic was administered as prophylaxis, or topically; and less frequent when a treatment review or a stop date was documented. Considered as a whole, all these factors might result in a complex conceptual framework underpinning antibiotic use in LCTFs. This framework includes not only individual, but also organisational and other contextual factors associated with antibiotic use.

### Improving infection prevention, and diagnosis process: critical steps to curb antibiotic use in LTCFs

We found that residents with a history of infection were about twice as likely to receive an antibiotic vs. residents with no such history and that this risk was about three times higher among residents with a urinary catheter, a major risk factor for UTI [78]. Evidence derived from our review points at improving infection prevention and control (IPC) as a critical step to reduce antibiotic prescribing in LTCFs. Evidence from the literature suggests that IPC programmes including a multi-modal strategy with four or more WHO core elements were effective in
reducing respiratory or MDRO infections, and improving
adherence to handwashing practices in LTCF [79].

Results of our systematic review also suggest a key
role of the diagnostic process in reducing antibiotic pre-
scribing [30]. Improving the diagnostic process is indeed
an essential component of AMS [80]. Potential signs of
infection, and positive urine culture/dipstick results were
associated with higher antibiotic prescribing. Diagnosis
of infections and decision-making about their manage-
ment in LTCFs are complex and involve several profes-
sionals (notably nurses) whose attitudes and practices
vary according to the context (e.g., pharmacy accessibil-
ity) [81, 82]. A recent review of decision tools used in
LTCFs to improve UTI diagnosis showed no consensus
as to the clinical criteria on which these tools rely [83].
Besides, living in a high urine-culturing LTCF was inde-
pendently associated with in an increased likelihood of
receiving an antibiotic [30]. Given the high prevalence of
asymptomatic bacteriuria in LTCFs, a high proportion of
suspected UTIs in LTCFs are indeed not UTIs (estimated
at 88% in Latour et al. [84]) and this greatly contributes
to unnecessary antibiotic use. Despite some AMS inter-
ventions improved UTI diagnosis in LCTFs, their feasi-
bility and sustainability beyond experimental conditions
remain unknown, and might be influenced by nursing
staff commitment and motivation [83].

Organisational changes in LTCFs to enhance effective
antibiotic stewardship and prescribing practices

Regarding LTCFs' characteristics, we did not find any
effect of facility size or nurse/nursing assistant staff. How-
ever, the few studies that investigated other aspects of
human resources (e.g., staff turnover), management (e.g.,
presence of an internal coordinating physician) or organ-
isational features (e.g., prevalence of after-hours medical
practitioner visits) showed significant associations with
antibiotic prescribing. Staff turnover may impair adop-
tion of AMS strategies and reduce their effect on anti-
biotic use [10, 85]. On the contrary, the presence of an
on-site coordinating physician may facilitate the imple-
mentation of AMS strategies by providing extra support
and reassurance for the nursing staff [13], in line with the
accountability CDC core element of antibiotic steward-
ship for nursing homes [86]. After-hours medical prac-
titioner visits in LTCFs may enhance antibiotic initiation
for reasons including limited knowledge of the resident
medical history, limited access to medical records, poor
resident current health status, and family or LTCF staff
pressure [87]. The majority of current AMS programmes
in LTCFs include education strategies and promotion
of clinical practice guidelines; a smaller number include
audit and feedback interventions and the provision of
advice by an infectious disease team [9, 10]. Results from
our review suggest that organisational changes requiring

more structural adjustments and resource investments
may contribute to further reduce antibiotic prescribing
in LTCFs. These challenging adjustments may need to
limit staff turnover rates, ensure the presence of a pro-
fessional accountable for the AMS activities, and enhance
collaboration between LTCFs and external prescribers,
especially physicians engaged in after-hours medical vis-
its (e.g., facilitate access to resident medical records).

Finally, one study included in our review suggested that
antibiotic request from resident/family increased the
odds of being prescribed an antibiotic by more than 60%.
Yet, current LTCF AMS programmes usually target both
nurses and physicians but fewer also target residents and/
or their family [9, 10]. Inspiration may be drawn from
AMS strategies in primary care, where the importance of
patients' expectations is well recognised [88, 89].

Strengths and limitations

This review has several strengths. As far as we know, this
is the first systematic review summarising quantitative
evidence about the factors associated with antibiotic use
in LTCFs, and highlighting the complexity of the con-
ceptual framework (i.e., including individual, contextual
and organisational factors) underpinning antibiotic use
in LTCFs. In addition to previous synthesis of qualitative
studies [13], our review identified original characteris-
tics that were significantly associated with antibiotic use
(both quantity and quality metrics), and provided insight
into strengths of associations. Besides, we attempted to
provide an assessment of causality based on Hill criteria.
It resulted in a conceptual framework underpinning anti-
biotic use in LTCFs that might help for the development
of specific AMS programmes fit to LTCFs settings and
suggests the urgent need of institutional changes (e.g.,
limiting LTCF staff turn-over or hiring on-site physi-
cians) to foster their implementation.

The main limitation is the heterogeneity pertaining to
selected outcomes, metrics of the factors investigated,
and the methods used across studies that prevented us
from performing a meta-analysis. Studies also came
from several countries with different LTCF organisation
and methods of care delivery that may influence the type
of factors associated with antibiotic prescriptions. For
instance, request from family may have a lower impact in
countries having permanent on-site physicians in LTCFs,
and thus many more opportunities for families and phy-
sicians to discuss [48]. Another limitation is the small
number of studies we could analyses for some factors
associated with antibiotic prescribing. For more than half
of them, results relied on only one study, hampering any
attempt to assess reproducibility (Tables S9 and S12), and
highlighting the need for further validation of our con-
ceptual framework.
## Conclusion

Improving infection prevention and control, and diagnostic practices as part of AMS programmes remain critical steps to reduce antibiotic prescribing in LTCFs. Institutional changes to limit staff turnover, ensure the presence of a professional accountable for the AMS activities, and enhance collaboration between LTCFs and external prescribers may also contribute to reduce antibiotic prescribing. The results of this review suggest that reducing antibiotic prescribing in LTCFs requires actions at various levels and the involvement of different stakeholders. Some actions could be implemented at the facility-level, with support from the director, as for example providing staff with tools and training to help them improve infectious diseases diagnosis practices. To improve their collaboration with the external structures that are critical to AMS (e.g., general practitioner private practices, community pharmacies, hospital departments involved in elderly care), LTCFs could also specify in their agreements setting the collaboration with such structures, which stakeholder is in charge of what concerning AMS. Other actions could pertain to other organisational levels external to the LTCF setting, with support from regional and/or national decision makers. These actions could include setting up and funding specialised structures dedicated to AMS to support LTCF in improving their practices. This could also include more general actions targeting the organisation and the resources allocated to LTCFs (e.g., revising salary policies and working conditions to limit staff turnover).

## Supplementary Information

The online version contains supplementary material available at https://doi.org/10.1186/s13756-024-01385-6.

Supplementary Material 1

Supplementary Material 2

Supplementary Material 3

## Acknowledgements

The ORANEAT Study Group: Gabriel Birgand, Patrick Castel, Frédérique Claudot, Catherine Dumartin, Jonathan Epstein, Laëtitia Ricci.

## Author contributions

AB: Methodology, Investigation, Formal analysis, Data Curation, Visualisation, Writing - Original Draft. BE: Methodology, Investigation, Formal analysis.

MB: Methodology, Investigation. CP: Writing - Review & Editing. NA: Conceptualisation, Methodology, Investigation, Writing - Review & Editing, Supervision. All authors have approved the final version of the paper.

## Funding

The ORANEAT research project is funded by a government grant managed by the Agence Nationale de la Recherche (ANR) under the Programme d'Investissements d'Avenir (Grant #ANR-20-PAMR-0008; date of award: 2021).

## Data availability

All data generated or analysed during this study are included in this published article and its supplementary information files.

## Declarations

### Ethics approval and consent to participate

Not applicable.

### Consent for publication

Not applicable.

### Competing interests

The authors declare no competing interests.

### Author details

Received: 26 October 2023 / Accepted: 29 February 2024

Published online: 06 March 2024

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