Journal of Clinical Pharmacy and Therapeutics, 2014, 39, 516–520

doi: 10.1111/jcpt.12181

A cross-sectional survey of antimicrobial stewardship strategies in UK hospitals A. P. Tonna* BPharm (Hons) MSc PhD MRPharmS, I. M. Gould† MBChB FRCPath FRCP (Edin) and D. Stewart* BSc MSc PhD MRPharmS FFRPS *School of Pharmacy and Life Sciences, Robert Gordon University, Aberdeen, and †Department of Medical Microbiology, Aberdeen Royal Infirmary, Foresterhill, Aberdeen, UK

Received 8 November 2013, Accepted 23 April 2014

Keywords: antimicrobial management team, antimicrobial stewardship, hospital

Despite recent government and regional initiatives, further improvements in antimicrobial stewardship are still required.

SUMMARY What is known and objective: Antimicrobial stewardship programmes describe strategies to optimize antimicrobial prescribing and utilization, minimize resistance and improve patient outcomes. Strategies in hospitals are usually implemented by multidisciplinary antimicrobial teams (AMTs). The objective of this study was to describe the profile and activities of AMTs within hospitals in the United Kingdom (UK). Method: All hospitals within the UK (n = 836) were included, and a prepiloted questionnaire was mailed to the ‘Director of Pharmacy’. Non-respondents were mailed up to two reminder questionnaires at two-weekly intervals. Main outcome measures are as follows: existence and remit of the AMTs; availability of antimicrobial-prescribing policies, aims, scope and methods of dissemination; and monitoring and feedback provided on antimicrobial policy adherence. Results: Response rate was 33% (n = 273). Completed questionnaires analysed were n = 226. Eighty-two (n = 186) of respondents indicated the presence of an AMT within the hospital, with 95% of these (n = 177) reporting an antimicrobial pharmacist as part of the team. All AMTs (n = 186) were involved in development of an antimicrobial policy and almost all (99% n = 184) promoted adherence and restricting use of specific antimicrobials (97% n = 180). Ninety-eight per cent of respondents (n = 222) reported the availability of a local antimicrobialprescribing policy within the hospital with this disseminated mainly through the hospital intranet (98% n = 217). Adherence to policy was measured mainly through audits measuring the appropriateness of antimicrobial use against the local policy (76% n = 169). Hospitals in England (P = 0
010), tertiary care hospitals (P = 0
021) and bed capacity >500 (P < 0
001) were more likely to have an AMT, as were hospitals with an accident and emergency department (P < 0
001), an infectious diseases unit (P = 0
019) and a microbiology department (P < 0
001). Audits to measure policy adherence were more likely (P < 0
001) if an AMT was present. The only variable retained in bivariate logistic regression was the presence of a microbiology unit, with an odds ratio of 14
1 (95% CI 6
02–33
33, P < 0
001). What is new and conclusions: Although most respondents reported an antimicrobial-prescribing policy, less had an AMT.

WHAT IS KNOWN AND OBJECTIVE The detection of antimicrobial resistance and awareness of the magnitude of associated threats have long been recognized. Abraham and Chain identified acquired antimicrobial resistance in 1940 when, during the development of penicillin, they isolated penicillinase.1 There is a complex, well-recognized relationship between the pharmacoepidemiology of antimicrobials and resistance, with an accepted academic view that resistance is accelerated by increased prescribing and consumption.2 Resistance impacts overall treatment costs due to a complex interplay of many factors including the necessity to prescribe higher-cost agents.3 Concern due to increasing antimicrobial resistance and the need for a more coordinated effort to tackle this have resulted in the articulation of initiatives and guidance at global,3 European4 and national levels.5,6 A revised 5-year (2013–2018) United Kingdom (UK) antimicrobial resistance strategy and action plan has recently been published by the Department of Health.7 Antimicrobial stewardship programmes describe strategies to optimize antimicrobial prescribing and utilization, minimize resistance and improve patient outcomes. Interventions largely centre on a multidisciplinary, collaborative approach of: education and training of junior doctors and other health professionals, restricted prescribing of specific antimicrobials, intravenous-to-oral switch policies and clinical audit of drug use and expenditure.8 In a recently published Cochrane systematic review, interventions used either alone or in combination deemed successful at promoting prudent antimicrobial prescribing in hospital inpatients were reported. Eighty-nine reviewed studies (95 interventions) were classified as having a ‘restrictive element’ with prescribers restricted in prescribing selected antimicrobials or a ‘persuasive element’ with interventions (e.g. education, clinical audit) aimed at changing prescribing. Although restrictive interventions were considered more effective in the short-term, persuasive interventions had similar impact on prescribing six months post-intervention. Due largely to differences in study design and reported outcomes, impact of interventions on patient outcomes could not be fully elucidated.9 Although several authors have reported descriptions of strategies to optimize antimicrobial stewardship in single UK centres, there has been no recent pan-UK research of antimicrobial stewardship. A working party for the British Society of Antimicrobial Chemotherapy conducted a UK survey in 1990; this was, however, prior to the devolution within the UK healthcare system

Correspondence: A. P. Tonna, School of Pharmacy and Life Sciences, Robert Gordon University, Riverside East, Garthdee Road, Aberdeen AB10 7GJ, UK. Tel.: (0044) 01224 262578; fax: (0044) 01224 262555; e-mail: [email protected]

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and the establishment of widespread hospital multidisciplinary antimicrobial teams (AMTs).10 The aim of this study was to describe UK antimicrobial stewardship strategies, specifically the profile and activities of antimicrobial management teams, antimicrobial prescribing policies, and methods of monitoring and feedback provided to prescribers on antimicrobial policy adherence.

pharmacist was present on the site. A number of questionnaires were completed on behalf of more than one hospital. A total of 226 completed questionnaires were analysed. Details of the role of respondents within the pharmacy department are at Table 1. Demographics from the respondent hospitals are at Table 2. Responses were mainly from English hospitals (70%) and district general hospitals (57%).

METHOD

Profile and activities of antimicrobial management team Eighty-two per cent (n = 186) of respondents reported the presence of an AMT within the hospital. Consultant medical microbiologists (97%; n = 180), antimicrobial pharmacists (95%; n = 177) and infection control managers (60%; n = 112) were most commonly reported to be team members. Only 2
7% (n = 5) reported having a specialist public health pharmacist and 5
9% (n = 11) having a patient representative as part of the team. Further detail of membership profile of AMTs is provided in Table 3. Associations between hospital demographics and AMT presence are given in Table 4. Univariate analysis identified hospitals in England (P = 0
010), tertiary care hospitals (P = 0
021), hospitals with a bed capacity of >500 (P < 0
001), hospitals with an accident and emergency (A&E) department (P < 0
001), an infectious diseases unit (P = 0
019) and a microbiology department (P < 0
001) as more likely to have an AMT. The only variable retained in bivariate logistic regression was the presence of a microbiology department, with an odds ratio of 14
1 (95% CI 6
02–33
33, P < 0
001). All of the AMTs (n = 186) had input in formulating an antimicrobial policy. Almost all were involved in promoting adherence (n = 184) and restricting use of specific antimicrobials (n = 180). Details of other activities are reported at Table 5.

Subjects and setting All UK NHS hospitals (n = 856), identified through NHS England, NHS Wales, Scottish Government and Health and Social Care Northern Ireland Gateway websites, were included in the study. Questionnaire development, validation and piloting A pilot questionnaire was devised based on the literature on antimicrobial stewardship programmes.8,11 The questionnaire was reviewed for face and content validity by one consultant physician specializing in infectious diseases and seven specialist antimicrobial pharmacists. The pilot questionnaire was sent to 30 hospitals which were selected randomly by generation of random numbers. Minor modifications were made to the questionnaire post-piloting. The final questionnaire (which is available online) contained five sections of mainly closed questions and Likert-type statements on: the hospital demographics (five items), the antimicrobial management team within the hospital (four items), the antimicrobialprescribing policy within the hospital (six items), measurement of adherence to the policy (two items) and non-medical prescribing of antimicrobials in the hospital (four items). The questionnaires were mailed (n = 856), along with an information leaflet and reply-paid envelope, to the ‘pharmacist in charge’ at each hospital. Up to two reminders were sent to nonrespondents at two-weekly intervals. Data collection took place during November 2011–January 2012.

Hospital antimicrobial-prescribing policy Ninety-eight per cent (n = 222) of respondents reported having an antimicrobial-prescribing policy within the hospital with 47% (n = 105) of these also highlighting a joint hospital/community policy. Joint policies were less likely to be reported in England (P < 0
001); there were no other associations between hospital demographics and presence of a joint hospital/community policy. Policies were aimed to encourage appropriate use of antimicrobials so that they are prescribed only if clinically needed (95%; n = 211). Reducing the incidence of Clostridium difficile infection (92%; n = 204) and encouraging prescribing of antimicrobials for the correct route, dose, frequency and duration were other common aims (90
5%; n = 201). Almost all antimicrobial-prescribing policies included empirical treatment guidelines for common

Analysis Data were coded and entered into an SPSS database (version 17.0; SPSS Inc., Cary, NC, USA) and analysed using descriptive statistics to profile demographics. Chi-squared was used as a test of association between variables (e.g. hospital country, bed capacity) and the outcome measures of interest (e.g. presence of an antimicrobial team). Variables identified as significant were then entered into bivariate logistic regression. P values ≤0
05 were considered statistically significant. Governance

Table 1. Role of respondents within pharmacy department (N = 226; some reported multiple roles)

This research was approved by the Ethical Review Panel of the School of Pharmacy and Life Sciences, Robert Gordon University, Aberdeen, UK. NHS ethical review was not required.

Role

% (n)

Director of pharmacy Director of acute division Specialist antimicrobial pharmacist Consultant antimicrobial pharmacist Other pharmacy role

13
8 0
9 59
2 2
2 37
2

RESULTS Response rate and demographics Of the 856 questionnaires mailed, 273 were returned complete (response rate 32
7%), with a further 20 returned undelivered. Of the 273 returned, 47 were incomplete mainly due to the fact that no

© 2014 John Wiley & Sons Ltd

(31) (2) (132) (5) (67)

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Antimicrobial stewardship strategies in UK hospitals

Table 2. Hospital hospitals

demographics

(N = 226)

of

respondent

Table 4. Association between hospital demographics and AMT presence (N = 226; do not always total to n = 226 due to missing data)

% (n)

England Scotland Wales Northern Ireland No response District general Tertiary Community Others No response Bed capacity 1500 No response

Accident and emergency department Infectious diseases unit Microbiology department

70
4 19
9 5
3 3
5 0
9 57
1 23
9 8
4 8 2
6

(159) (45) (12) (8) (2) (129) (54) (19) (18) (6)

47
3 31
4 13
7 4
4 3
2

(107) (71) (31) (10) (7)

Yes % (n)

No % (n)

No response % (n)

80
5 (182)

18
6 (42)

0
9 (2)

22
1 (50) 75
2 (170)

73
9 (167) 23
5 (53)

4 (9) 1
3 (3)

AMT present % (n)

England Scotland Wales Northern Ireland Hospital type Tertiary District general Community Others Bed capacity 1500

No AMT % (n)

60
6 13
3 5
3 4
4

(137) (30) (12) (6)

8
4 (19) 6
6 (15) 0 0
9 (2)

22
1 51
3 2
2 5
3

(50) (116) (5) (12)

1
3 5
3 5
7 2
6

33
2 28
7 13
7 4
4

(75) (65) (31) (10)

(3) (12) (13) (6)

12
8 (29) 2
6 (6) 0 0

AMT, multidisciplinary antimicrobial team.

Adherence to policy Adherence to the hospital antimicrobial policy was monitored most commonly through audits measuring the appropriateness of antimicrobial use against the local policy (76%; n = 169). 73% (n = 162) reviewed the volume of prescribing within the hospital, for example using defined daily doses. There was a significant association between the presence of an AMT and audits (P < 0
001). Feedback on adherence to the antimicrobial policy was mainly provided on the basis of ward team prescribing (62%; n = 138) rather than to the individual prescribers (33%; n = 74). Only 29% (n = 66) reported providing feedback to prescribers about local antimicrobial resistance patterns. No association was found between the way feedback on adherence was provided and the presence of an AMT within the hospital.

Table 3. Membership profile of AMTs (N = 186)

Consultant medical microbiologist Specialist antimicrobial pharmacist Infection control manager Consultant in infectious diseases Nurse Consultant surgeon Non-medical prescriber Consultant paediatrician General practitioner Consultant obstetrician Patient representative Consultant in public health Specialist public health pharmacist

Yes % (n)

No % (n)

No response % (n)

96
8 95
2 60
2 52
2 48
9 31
7 25
3 19
9 12
9 10
2 5
9 4
8 2
7

1
1 3
8 16
1 25
8 28 38
2 40
9 44
6 53
2 51
1 59
1 54
3 59
1

2
2 1
1 23
7 22
0 23
1 30
1 33
9 35
4 33
9 38
8 34
9 40
9 38
2

(180) (177) (112) (97) (91) (59) (47) (37) (24) (19) (11) (9) (5)

(2) (7) (30) (48) (52) (71) (76) (83) (99) (95) (110) (101) (110)

(4) (2) (44) (41) (43) (56) (63) (66) (63) (72) (65) (76) (71)

DISCUSSION Our study is the first recent UK-wide report of antimicrobial stewardship strategies and provides insight into any differences in national practices post-devolution. Furthermore, our findings are timely given the recent announcement that the revised 5-year (2013–2018) United Kingdom (UK) antimicrobial resistance strategy and action plan has been published by the Department of Health.7 The majority of our respondents reported the existence of an AMT. Hospitals in England, tertiary care hospitals and bed capacity >500 were more likely to have an AMT, as were hospitals with an accident and emergency department, an infectious diseases unit and a microbiology department. Audits to measure policy adherence were more likely if an AMT was present. AMTs were reported to have a wide ranging remit around antimicrobial policy development, review, dissemination; promoting policy adherence; undertaking clinical audit; and restricting prescribing of targeted antimicrobials. Most reported use of electronic methods of communication with the wider healthcare team. Although we received responses from all four home nations, we acknowledge limitations of the reliance of self-reported data and

AMTs, multidisciplinary antimicrobial teams.

infections (99%; n = 220), and many included a gentamicin protocol (89
2%; n = 198) and a surgical prophylaxis policy (87
8%; n = 195). Policy was largely disseminated electronically via the hospital intranet (97
7%; n = 217) with only 7% (n = 16) reporting dissemination via portable devices such as mobile phones. Healthcare professionals were informed of updates in the policy most commonly through the hospital intranet (92
3%; n = 205) or through contact with other healthcare professionals such as pharmacists (71
2%; n = 158).

© 2014 John Wiley & Sons Ltd

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Antimicrobial stewardship strategies in UK hospitals Table 5. Activities reported to be within the remit of the AMT (N = 186; many reported multiple activities)

Formulating an antimicrobial policy Promoting adherence to the antimicrobial policy Reviewing and tailoring national policy for local use Reviewing newly marketed antimicrobials for use within the hospitals Reviewing new indications for antimicrobials available within the hospital Restricting prescribing of specific/named antimicrobials Ensuring a strategy in place for education and training of healthcare professionals Overseeing antimicrobial-related education for general public

Yes % (n)

No % (n)

No response % (n)

100 98
9 93
5 73
1 81
2 96
8 82
3 36

0 0
5 3
2 18
3 10
7 1
6 11
8 48
9

0 0
5 3
2 8
6 8
1 1
6 5
9 15

(186) (184) (174) (136) (151) (180) (153) (67)

(1) (6) (34) (20) (3) (22) (91)

(1) (6) (16) (15) (3) (11) (28)

AMT, multidisciplinary antimicrobial team.

competence, hence there may be merit in reviewing AMT composition to ensure that these professions are represented. The reported antimicrobial policy aims were to reduce antimicrobial resistance and to reduce the incidence of healthcareassociated infections including MRSA, ESBLs and C. difficile, which are in accord with the international literature of ‘antimicrobial stewardship’ programmes.4,19 Empirical treatment guidelines were an integral part of most prescribing policies. The majority of respondents reported that rotation of antimicrobials and automatic stop orders were interventions least employed as part of the policies. Interestingly, there is a lack of evidence as to the efficacy of both these interventions in reducing antimicrobial resistance.19 As expected, dissemination of both the policies and updates occurred through hospital electronic systems. It was surprising that very few reported dissemination via portable devices such as mobile phones. A new smartphone app developed by doctors and pharmacists to support healthcare professionals in antimicrobial-prescribing has been launched in an English hospital.20 It is likely that this form of dissemination will flourish in the near future. Although the specific details of AMT stewardship strategies varied, all reported antimicrobial policy development and almost all were involved in promoting policy adherence to this policy. Clinical audits were only reported by three quarters of respondents, with these appearing to be more likely if an AMT was present. The reasons for one-quarter of respondents not undertaking clinical audits require further research and elucidation as this is a missed opportunity to provide prescribers with key feedback data to optimize antimicrobial prescribing as per Infectious Diseases Society of American and the Society of Healthcare Epidemiology of America guidelines.19 Most AMTs implemented restricted use of policies, which are highly recommended to generate immediate reductions in both antimicrobial use and cost, although the long-term benefits of such policies on antimicrobial resistance have not yet been clearly demonstrated.19 A Cochrane review of interventions to improve hospital antimicrobial prescribing concludes that restrictive interventions may be more effective than prospective interventions on improving antimicrobial prescribing in the short term, with no differences in the long term. No conclusions on effects of either intervention on patient outcomes could be made.9 Interestingly, the majority of our respondents did not report overseeing antimicrobial education of the general public to be within their remit and very few included patient/public representatives within their members. This requires further consideration

the low response rate, with potential for response bias thus limiting generalizability of findings. UK guidance in all four nations highlights the importance of the AMT in UK hospitals. The ‘Start Smart – then Focus’ (England and Wales) guidance recommends setting up a multidisciplinary management team ‘. . . to develop and implement the organization’s antimicrobial stewardship programme for all adults and children admitted to hospital’.12,13 The ScotMARAP plan goes on to further define the role of the AMT and includes supporting staff education and involvement in dissemination, audit and feedback of antimicrobial policies.14 The Northern Ireland strategy for tackling antimicrobial resistance, 2012–2017, reiterates the importance of an AMT within each trust as a main action relating specifically to tackling antimicrobial resistance.15 Our study findings are very encouraging, demonstrating effective implementation of this guidance. The situation in the UK contrasts with recent data from the United States, with just over half of hospitals (n = 206 of 406 responding hospitals) reporting the existence of an AMT.16 Similarly, just over half of hospitals reported an AMT in south-western French hospitals (56% of 74 responding hospitals).17 In our study, the presence of an AMT was significantly associated with presence of infectious disease, microbiology and emergency departments. Furthermore, hospitals in England and those with higher bed capacity were also more likely to have an AMT. One study in Belgium also identified bed capacity to be a key variable.18 However, our findings highlight the presence of a microbiology department within the hospital as a significant, independent predictor in the presence of an AMT. These findings are important and serve as a focus for further research and also targeting of activities and support to encourage rational use of antimicrobials. It is evident that AMTs have sought to ensure wide representation of key stakeholders, with consultant microbiologists, infectious diseases specialists and antimicrobial pharmacists having prominent roles. This reflects the need to ensure appropriate specialist expertise but also to encourage acceptance of AMT support, recommendations and general guidance from all those involved in the use of antimicrobials. However, notable findings were the relatively low proportions of respondents reporting surgeons or nurses within their teams, which is in stark contrast to national guidance for core membership of AMTs in hospitals in the UK.12–15 This is a particular issue with the implementation of independent and supplementary prescribing by non-medical health professionals (e.g. nurses, pharmacists, physiotherapists, optometrists, etc.) who may prescribe antimicrobials within their

© 2014 John Wiley & Sons Ltd

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UK hospitals. However, areas for further development are evident including wider membership of AMTs and more effective audit and dissemination of prescribing and antimicrobial resistance patterns.

given the focus on lay involvement in healthcare developments generally, although the role of the patient in antimicrobial prescribing within the secondary care environment may be less obvious than in primary care where patient pressure may be a factor in the decision whether or not to prescribe. Only around half of the respondents reported a joint secondary care, primary care antimicrobial-prescribing policy, which is disappointing given UK guidances, the ScotMARAP in particular, promoting ‘single-system working’ by including all sectors within remit of the AMT, as a means of ensuring a collaborative and streamlined approach to antimicrobial use.14 Further research should focus on determining the most effective strategy for dissemination of prescribing data and resistance patterns to be employed by an AMT. Further evidence is also required to determine the long-term effect of prospective and restrictive interventions on patient outcomes.

ACKNOWLEDGEMENTS We would like to thank all respondents who completed the questionnaire. We would also like to thank the 4th year MPharm students involved in data gathering: Elaine Campbell, Cherith Chamberlain, Brian Clancy and Rebecca Connor. FUNDING None. CONFLICT OF INTEREST

WHAT IS NEW AND CONCLUSION

No conflict of interests have been declared.

This study demonstrates the effective implementation of UK national guidance regarding the setting up of AMTs in responding

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15. Department of Health, Social Services and Public Safety. Strategy for Tackling Antimicrobial Resistance (STAR) 2012–2017. 2012. Available at: http://www.dhsspsni.gov. uk/star-doc.pdf (accessed 5 September 2013). 16. Doron S, Nadkarni L, Price LL, Lawrence K, Davidson LE, Evans J, Garber C , Syndman DR. A nationwide survey of antimicrobial stewardship practices. Clin Ther, 2013;35: 758–765. 17. Dumartin C, Rogues A, Amadeo B, Pefau M, Venier A, Parneix P, Maurain C. Antibiotic usage in south-western French hospitals: trends and association with antibiotic stewardship measures. J Antimicrob Chemother, 2011;66:1631–1637. 18. Van Gastel E, Costers M, Peetermans WE, Struelens MJ, on behalf of the Hospital Medicine Working Group of the Belgian Antibiotic Policy Coordination Committee. Nationwide implementation of antibiotic management teams in Belgian hospitals: a self-reporting survey. J Antimicrob Chemother, 2010;65:576–580. 19. Dellit TH, Owens RC, McGowen JE et al. Infectious Diseases Society of America and the Society for the Healthcare Epidemiology of America guidelines for developing an institutional programme to enhance antimicrobial stewardship. Clin Infect Dis, 2007; 44:159–177. 20. Anonymous. Brief update. Clinical Pharmacist, 2011;3:231.

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