Citation: McLeod M, Ahmad R, Shebl NA, Micallef C, Sim F, Holmes A (2019) A whole-health–economy approach to antimicrobial stewardship: Analysis of current models and future direction. PLoS Med 16(3): e1002774. https://doi.org/10.1371/journal.pmed.1002774
Published: March 29, 2019
Copyright: © 2019 McLeod et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Funding: This article represents independent research that was partially funded by the National Institute for Health Research (NIHR) Health Protection Research Unit in Healthcare Associated Infections and Antimicrobial Resistance at Imperial College London, in partnership with Public Health England (PHE) in collaboration with The Sanger Institute, the University of Cambridge Veterinary School, and Imperial College Health Partners. MM is supported by the NIHR Imperial Patient Safety Translational Research Centre. RA is supported by an NIHR Fellowship in Knowledge Mobilisation. AH is an NIHR Senior Investigator. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
Competing interests: I have read the journal's policy and the authors of this manuscript have the following competing interests: CM has received travel grants to attend scientific conferences from Astellas, Gilead, Pfizer, and Novartis and educational grants from Pfizer and Novartis. CM has attended a Pfizer Advisory Board Meeting and consulted for Astellas. MM has received an educational grant for a medication safety workshop held in November 2017 from Pfizer, unrelated to this study.
Abbreviations: AMR, antimicrobial resistance; AMS, antimicrobial stewardship; ESBL-E, extended-spectrum beta-lactamase producing Enterobacteriaceae; GP, general practitioner; LID, long-term care facility infectious disease; MRSA, methicillin-resistant Staphylococcus aureus; NHS, National Health Service; NIHR, National Institute for Health Research; PHE, Public Health England; TARGET, Treat Antibiotics Responsibly, Guidance, Education, Tools.
Provenance: Not commissioned; externally peer reviewed.
- Antimicrobial stewardship (AMS) strategies are widely implemented in single healthcare sectors and organisations; however, the extent and impact of integrated AMS initiatives across the whole health economy are unknown.
- Assessing degree of integration of AMS across the whole health economy and its impact is essential if we are to achieve a ‘One Health’ approach to addressing antimicrobial resistance (AMR), and therefore we searched systematically for and analysed published examples of integrated AMS initiatives to address this gap.
- Application of a system-level framework to analyse integration of AMS initiatives across and within healthcare sectors shows that integration is emerging but needs strengthening.
- Findings from a small number of evaluations in high-income countries suggest that antimicrobial prescribing and healthcare-associated infections can be reduced using a multisectoral integrated AMS approach.
- More robust research designs to evaluate and understand the impact of multisectoral integrated AMS are needed, particularly with respect to differing health systems in different countries and local organisational contexts.
- Our analysis highlights a number of challenges and ways forward for enhancing the delivery of AMS through an integrated approach.
It is estimated that around 700,000 people die annually from drug-resistant infections, with experts predicting an alarming possible increase to 10 million deaths each year by 2050 and major future challenges to the way we practice medicine and surgery [1,2]. It was welcome news that tackling antimicrobial resistance (AMR) and infectious diseases along with health system strengthening were featured at the G20 summit (November, 2018), under the wider aim of improving sustainability, and progress towards more coordinated international efforts will be reviewed at the 73rd session of the UN General Assembly (September 2018) ; but how are health professionals, managers, and policymakers assuring coordinated efforts within human healthcare? Globally, there has been much emphasis on a ‘One Health’ approach that involves connecting the health of humans, animals, and the environment to tackle AMR . This is driving much-needed antimicrobial stewardship (AMS) activities in animal production sectors . However, we have yet to achieve and establish joined-up approaches within human health. This paper, therefore, focuses on an analysis of multisectoral AMS in human health. AMS remains a cornerstone for addressing AMR with numerous initiatives implemented with varying degrees of success [5,6]. A critical gap we have identified is that approaches have largely focused efforts separately in primary care or secondary care, and have also heavily targeted medical prescribers. In this paper, we propose that policymakers, clinical leaders, and healthcare managers assess and consolidate AMS activities across the whole health economy, and we use a novel, to our knowledge, approach to demonstrate how such an assessment can be made. We present the extent to which existing AMS initiatives are multisectoral or integrated across a whole health economy within individual countries and their impact on antimicrobial-related outcomes. We then highlight some challenges and key considerations for developing and harnessing potential benefits of integrated AMS approaches.
Need for a whole-health–economy approach
Health systems are required to deliver best outcomes efficiently, facing the challenges of macroeconomic constraints, technology costs, and increasing public need and demand. Consolidating the sometimes disparate programs and initiatives within the health sector is necessary, and integrated models of care across primary, secondary, tertiary, and long-term care can help with coordinated implementation of AMS . Assessment of the degree of integration of AMS across the whole health economy is essential if we are to understand how a ‘One Health’ approach to addressing AMR may be achieved. Much AMS activity has been concentrated in hospital settings, creating a practical but somewhat artificial boundary that neglects bidirectional influences between hospital and community care services. Antimicrobial use in the community is associated with the development of AMR in and outside hospitals . Furthermore, use of accident and emergency departments by ambulatory patients contributes to fragmented care and overuse of antimicrobials . The way people access healthcare has evolved: the availability of blended care and complex patient-care pathways in some countries allows for patient-centred approaches as well as more rational use of services. The availability of antimicrobials without a prescription in some countries and increasing availability of online pharmacies provides an additional challenge for AMS. Fundamentally, AMS is lagging behind the advances made in health service delivery and patient behaviours by remaining sector-based.
What does integration mean and how can we assess it?
The One Health perspective on integration involves multiple sectors communicating and working together to design and implement programs, policies, legislation, and research to achieve better public health outcomes . In practice, in England, new integrated care models are being developed through 50 selected collaborative organisations that will inform potential redesign of the whole health system, and 25 integrated care pioneer sites to test new and different ways of joining up health and social care services . Elsewhere in Europe, the Dutch Ministry of Health, Welfare, and Sport established nine pioneer sites to integrate clinical and community services with the aim of achieving ‘better healthcare at lower cost’ . In the United States, accountable care organisations—which typically involve multiple physician practices and at least one hospital—have been established to improve the quality of care while lowering costs . However, AMS is not explicit in any of these wider health-system–integration models.
To further complicate matters, there is no standard definition of integration, and a number of integrated care models have been proposed in the literature [13–17] (S1 Table). In this analysis, we define and summarise the extent of integration based on the six facets of critical health system function described by Atun and colleagues [16,18] because it provides a practical level of granularity on the concept of intervention integration and is specific to healthcare (Table 1). We appreciate that there may be unpublished initiatives. However, as a novel, to our knowledge, analysis of this issue, the focus was on examining evidence of integrated AMS initiatives from the literature so that some measures of impact and associated context can be synthesised. Our aim was to identify practical considerations to support policymakers seeking to develop integrated AMS across the whole health economy. We carried out a systematic search of the literature published between January, 2006 and December, 2018, selected relevant articles using prespecified inclusion criteria, and reviewed evaluative studies (S1 Appendix). This paper describes an analysis based on 16 AMS initiatives from nine high-income countries and one low-middle–income country (Tables 2 and 3).
Extent of AMS integration across the whole health economy
Integration mapping of the 16 initiatives based on Table 1 suggests that a range of approaches have been used to achieve multisectoral AMS (Fig 1). Full integration in Planning was often considered a key factor for establishing many initiatives coupled with an integrated Stewardship and Governance approach. Integration in these two facets was mainly achieved through expansion of the AMS program, by which the primary governance responsibilities remained with the host institution [19,20,30,32,33], rather than through establishment of new structures . AMS initiatives that had a shared governance structure across healthcare organisations (i.e., partially integrated) were either national programs  or state-wide programs [26,31]. While these provide examples of an integrated AMS governance approach, effective governance is likely to require much more than a multistakeholder approach to plan and deliver services; a mixed regulatory and persuasive strategy including effective public engagement is needed . In our analysis, nine initiatives were partially integrated for Demand Generation, showing a potential missed opportunity for this critical facet that includes raising awareness and increasing engagement with the public, practitioners, health service managers, and policymakers. Monitoring and Evaluation relate to the functions around data collection, analysis, reporting, and performance-management systems. Full integration was identified in one initiative in which the health system oversaw these functions regionally or was responsible for these functions directly . More often, data collection and analyses were managed by the wider health system; however, performance management roles were not [19,20,22,25,26,32]. Financing relates to the pooling of funds/funding source, cross-program use of funds, and provider payment methods involved in the AMS initiative. The majority of initiatives did not report on how they were or should be financed or how the funds were or should be used [19,20,22,23,26,30,32]. While fund pooling was partially integrated in three initiatives [25,32,33], decisions for provider payment methods were not. Overall, 11 studies evaluated the AMS initiative using mainly quasiexperimental study designs [19–23,25,27,30,31,39] (S2 Table). These reported on a range of positive impacts including reductions in antibiotic prescribing, reductions in the proportion of broad-spectrum antibiotic prescribed, reduction in C. difficile infection rates, and perceived improvement in citizens’ knowledge and attitudes about self-management of minor infections. However, potential for bias should be borne in mind because of study limitations associated with uncontrolled research designs, insufficient data time points, and risk of self-selection by participants who are interested in AMS.
Opportunities and implications for policy
Especially when planning new initiatives, a health system function framework as employed here can be critical to minimise duplication of effort and achieve efficiencies from the viewpoint of healthcare professionals and service users. Our assessment has highlighted strengths of initiatives associated with beneficial outcomes, and we present these as three interconnected practical recommendations for policymakers to consider.
A successful integrated AMS approach can be developed through expansion of an existing AMS program
When compared to hospital-based AMS, strategies within primary care and long-term care have generally been slow to develop. Outside of hospitals, structural constraints sometimes include undefined AMS leadership at the organisational level and therefore unclear responsibilities around local AMS objectives and lack of timely pathways to specialist support. An integrated AMS model, particularly one involving secondary care, can overcome some of the community-based issues by either extending existing secondary-care AMS programs [19,26,32,33], adapting from established frameworks for secondary-care AMS , or creating a joint platform for multisectoral AMS strategies to be presented, developed, monitored, and/or shared [25,27]. It therefore follows that an integrated AMS program may also be able to address process issues such as fragmented and timely follow-up of patients, their symptom progression, and medical management. However, further research is required to investigate this. Critically, there is a need for establishing sustainable funding for AMS teams working beyond hospital settings that is not solely derived from cost savings through reduced drug expenditure. Instead, funding for developing and supporting AMS teams should be considered within the patient safety and healthcare-quality–related spending . Irrespective of these issues, adoption and uptake of AMS strategies are likely to be influenced by the underlying health system and culture in a country.
Opportunities for success establishing consistent communication channels with responsibilities and common goals clearly defined
Few health systems appear to have effective mechanisms for sharing and disseminating learning about AMS, leading to small-scale local initiatives. Strengthening communication between commissioners, providers, and consumers by having more structured and clear communication pathways, such as in the Strama model developed in Sweden and the similarly structured Scottish Antimicrobial Prescribing Group, can be an effective way to develop, disseminate, and monitor ways to improve AMS [25,27].
Capitalise on existing resources and processes
Patients and the public have a pivotal role in infection prevention and management, yet failure to involve and engage with them in decision-making or achieve sustained behaviour change remains a problem in all health sector settings [41,42]. We found few examples of patient or public involvement in the design and delivery of integrated AMS initiatives (Table 3). However, we know from other studies that patient misconceptions about AMR and what constitutes appropriate antibiotic use is a major driver for inappropriate behaviours around antibiotic use . Furthermore, our stakeholder analysis suggests that there are potentially more opportunities for integration, particularly involving primary care service providers. For instance, in the United Kingdom, it is well recognised that nurses and pharmacists in the community are generally more accessible to the public than general practitioners (GPs). The continuing expansion of their roles in the community, which not only provides support to patients but also reduces the burden on primary care physicians, is testament to this [44,45]. However, there are few AMS initiatives that capitalise on these valuable resources to deliver integrated AMS—by this, we mean appropriate antibiotic access and preservation and knowledge mobilisation for promoting AMS that is aligned with primary, secondary, tertiary, and long-term institutional care sectors. We found little involvement of dental practitioners in most multisectoral AMS initiatives, which is another missed opportunity. Further work is required to investigate such AMS roles in the community and embed these more widely as applicable in the respective country. A more robust evidence base is needed to establish the effectiveness of integrated AMS initiatives and specifically consider contextual antecedents to better inform future sustained improvements.
Overall, we urge policymakers, clinical leaders, and healthcare managers to assess and consider consolidating AMS activities across the whole health economy. Each of these stakeholders have an important role to drive and support clinicians, researchers, and research-active patients to carry out quality research that will inform the development of more robust evidence-based policies and guidelines. The analytic framework presented here can be used to assess the extent of integration of existing or planned multisectoral AMS initiatives, and we have outlined three areas with practical considerations towards how future integration of AMS initiatives across the whole health economy may be achieved. Ultimately, integrated AMS must prove itself as an essential element of efficient redesign if it is to deliver sustained patient benefits.
S1 Appendix. Search strategy and article selection.
S1 Table. Frameworks for assessing extent of integration considered.
We thank the following for their support in this work and for giving up their time to assist in article collation: Michiyo Iwami and Elle Clegg. We would also like to acknowledge the National Institute for Health Research Imperial Biomedical Research Centre.
The views expressed in this publication are those of the authors and not necessarily those of the National Health Service (NHS), the National Institute for Health Research (NIHR), Public Health England (PHE), or the UK Department of Health and Social Care.
- 1. O’Neill J. Antimicrobial Resistance: Tackling a crisis for the health and wealth of nations. The review on antimicrobial resistance. [Internet]. London; 2014. Available at: https://amr-review.org/sites/default/files/AMRReview Paper—Tackling a crisis for the health and wealth of nations_1.pdf [cited 31 Aug 2017].
- 2. World Health Organization. One Health. In: WHO [Internet]. World Health Organization; 2017. Available at: http://www.who.int/features/qa/one-health/en/. [cited 1 Nov 2017].
- 3. United Nations. Annotated preliminary list of items to be included in the provisional agenda of the seventy-third regular session of the General Assembly [Internet]. 2018. Available at: https://undocs.org/A/73/100 [cited 9 Aug 2018].
- 4. Schar D, Sommanustweechai A, Laxminarayan R, Tangcharoensathien V. Surveillance of antimicrobial consumption in animal production sectors of low- and middle-income countries: Optimizing use and addressing antimicrobial resistance. PLoS Med. 2018;15: 1–9. pmid:29494582
- 5. Charani E, Edwards R, Sevdalis N, Alexandrou B, Sibley E, Mullett D, et al. Behavior change strategies to influence antimicrobial prescribing in acute care: a systematic review. Clin Infect Dis. 2011;53: 651–662. pmid:21890770
- 6. Davey P, Marwick CA, Scott CL, Charani E, McNeil K, Brown E, et al. Interventions to improve antibiotic prescribing practices for hospital inpatients (Review). Cochrane Database Syst Rev. 2017;2: CD003543. pmid:28178770
- 7. The Health Foundation. Infection prevention and control: lessons from acute care in England. Towards a whole health economy approach. London; 2015.
- 8. Aldeyab M, Harbarth S, Vernaz N, Kearney MP, Scott MG, Darwish Elhajji FW, et al. The impact of antibiotic use on the incidence and resistance pattern of extended-spectrum beta-lactamase-producing bacteria in primary and secondary healthcare settings. Br J Clin Pharmacol. 2011;74: 171–179. pmid:22150975
- 9. May L, Cosgrove S, L’Archeveque M, Talan A, Payne P, Jordan J, et al. A call to action for antimicrobial stewardship in the emergency department: approaches and strategies. Ann Emerg Med. 2013;62: 69–77. pmid:23122955
- 10. NHS England; New care models [Internet]. Available at: https://www.england.nhs.uk/new-care-models/. [cited 21 Mar 2018].
- 11. Drewes HW, Struijs JN, Baan CA. How the Netherlands is Integrating Health and Community Services. In: N Engl J Med Catalyst [Internet]. 2017. Available at: http://catalyst.nejm.org/netherlands-integrating-health-community-services/. [cited 1 Jun 2017].
- 12. Ham C, Alderwick H. Place-based systems of care. A way forward for the NHS in England. London: The King's Fund; 2015.
- 13. Curry N, Ham C. Clinical and service integration: the route to improved outcomes [Internet]. London; 2010. Available at: www.kingsfund.org.uk/publications [cited 14 May 2017].
- 14. The NHS Confederation. Building integrated care. Lessons from the UK and elsewhere. London: The NHS Confederation; 2005.
- 15. Contandriopoulos A-P, Denis J-L, Touati N, Rodríguez C. The integration of health care: dimensions and implementation. Montreal: Groupe de recherche interdisciplinaire en sante; 2003.
- 16. Atun R, De Jongh T, Secci F, Ohiri K, Adeyi O. Integration of targeted health interventions into health systems: A conceptual framework for analysis. Health Policy Plan. 2010;25: 104–111. pmid:19917651
- 17. Leutz WN. Five laws for integrating medical and social services: lessons from the United States and the United Kingdom. Milbank Q. 1999;77: 77–110. pmid:10197028
- 18. Atun R, De Jongh T, Secci F, Ohiri K, Adeyi O. A systematic review of the evidence on integration of targeted health interventions into health systems. Health Policy Plan. 2010;25: 1–14. pmid:19959485
- 19. Stuart RL, Orr E, Kotsanas D, Gillespie EE. A nurse-led antimicrobial stewardship intervention in two residential aged care facilities. Healthc Infect. 2015;20: 4–6. http://dx.doi.org/10.1071/HI14016
- 20. Wutzke SE, Artist MA, Kehoe LA, Fletcher M, Mackson JM, Weekes LM. Evaluation of a national programme to reduce inappropriate use of antibiotics for upper respiratory tract infections: effects on consumer awareness, beliefs, attitudes and behaviour in Australia. Health Promot Int. 2007;22: 53–64. pmid:17046966
- 21. Golding GR, Quinn B, Bergstrom K, Stockdale D, Woods S, Nsungu M, et al. Community-based educational intervention to limit the dissemination of community-associated methicillin-resistant Staphylococcus aureus in Northern Saskatchewan, Canada. BMC Public Health. 2012;12: 15. pmid:22225643
- 22. McKay RM, Vrbova L, Fuertes E, Chong M, David S, Dreher K, et al. Evaluation of the do bugs need drugs? Program in British Columbia: Can we curb antibiotic prescribing? Can J Infect Dis Med Microbiol. 2011;22: 19–24. pmid:22379484
- 23. Plachouras D, Antoniadou A, Giannitsioti E, Galani L, Katsarolis I, Kavatha D, et al. Promoting prudent use of antibiotics: the experience from a multifaceted regional campaign in Greece. BMC Public Health. 2014;14: 866. pmid:25149626
- 24. Mondain V, Secondo G, Guttmann R, Ferrea G, Dusi A, Giacomini M, et al. A toolkit for the management of infection or colonization by extended-spectrum beta-lactamase producing Enterobacteriaceae in Italy: implementation and outcome of a European project. Eur J Clin Microbiol Infect Dis. Springer Berlin Heidelberg; 2018;37: 987–992. pmid:29600324
- 25. Mölstad S, Erntell M, Hanberger H, Melander E, Norman C, Skoog G, et al. Sustained reduction of antibiotic use and low bacterial resistance: 10-year follow-up of the Swedish Strama programme. Lancet Infect Dis. 2008;8: 125–132. pmid:18222163
- 26. Aldeyab MA, Scott MG, Kearney MP, Alahmadi YM, Magee FA, Conlon G, et al. Impact of an enhanced antibiotic stewardship on reducing methicillin-resistant Staphylococcus aureus in primary and secondary healthcare settings. Epidemiol Infect. 2014;142: 494–500. pmid:23735079
- 27. Nathwani D, Sneddon J, Malcolm W, Wiuff C, Patton A, Hurding S, et al. Scottish Antimicrobial Prescribing Group (SAPG): Development and impact of the Scottish National Antimicrobial Stewardship Programme. Int J Antimicrob Agents. 2011;38: 16–26. pmid:21515030
- 28. Powell N, Davidson I, Yelling P, Collinson A, Pollard A, Johnson L, et al. Developing a local antimicrobial resistance action plan: the Cornwall One Health Antimicrobial Resistance Group. J Antimicrob Chemother. 2017;72: 2661–2665. pmid:28595316
- 29. Lawes T, Lopez-Lozano J-M, Nebot CA, Macartney G, Subbarao-Sharma R, Wares KD, et al. Effect of a national 4C antibiotic stewardship intervention on the clinical and molecular epidemiology of Clostridium difficile infections in a region of Scotland: a non-linear time-series analysis. Lancet Infect Dis. 2017;17: 194–206. pmid:27825595
- 30. Centers for Disease Control and Prevention. The Core Elements of Antibiotic Stewardship for Nursing Homes [Internet]. Atlanta: US Department of Health and Human Services; 2015. Available at: http://www.cdc.gov/longtermcare/prevention/antibiotic-stewardship.html [cited 22 May 2017].
- 31. Gonzales R, Corbett KK, Leeman-Castillo BA, Glazner J, Erbacher K, Darr CA, et al. The “Minimizing Antibiotic Resistance in Colorado” Project: Impact of Patient Education in Improving Antibiotic Use in Private Office Practices. Health Serv Res. 2005;40: 101–116. pmid:15663704
- 32. Gugkaeva Z, Franson M. Pharmacist-led model of antibiotic stewardship in a long-term care facility. Ann Long-Term Care. 2012;20: 22–26.
- 33. Jump RLP, Olds DM, Seifi N, Kypriotakis G, Jury LA, Peron EP, et al. Effective antimicrobial stewardship in a long-term care facility through an infectious disease consultation service: keeping a LID on antibiotic use. Infect Control Hosp Epidemiol. 2012;33: 1185–1192. pmid:23143354
- 34. Long A, Lungu JC, Machila E, Schwaninger S, Spector J, Tadmor B, et al. A programme to increase appropriate usage of benzathine penicillin for management of streptococcal pharyngitis and rheumatic heart disease in Zambia. Cardiovasc J Afr. 2017;28: 242–247. pmid:28906539
- 35. Dellit TH, Owens RC, McGowan JE, Gerding DN, Weinstein RA, Burke JP, et al. Infectious Diseases Society of America and the Society for Healthcare Epidemiology of America guidelines for developing an institutional program to enhance antimicrobial stewardship. Clin Infect Dis. 2007;44: 159–77. pmid:17173212
- 36. Barlam TF, Cosgrove SE, Abbo LM, Macdougall C, Schuetz AN, Septimus EJ, et al. Implementing an Antibiotic Stewardship Program: Guidelines by the Infectious Diseases Society of America and the Society for Healthcare Epidemiology of America. Clin Infect Dis. 2016;62: e51–e77. pmid:27080992
- 37. British Society for Antimicrobial Chemotherapy. Practical guide to antimicrobial stewardship in hospitals [Internet]. Available at: http://bsac.org.uk/wp-content/uploads/2013/07/Stewardship-Booklet-Practical-Guide-to-Antimicrobial-Stewardship-in-Hospitals.pdf [cited 22 May 2016].
- 38. Birgand G, Castro-Sanchez E, Hansen S, Gastmeier P, Lucet J-C, Ferlie E, et al. Comparison of governance approaches for the control of antimicrobial resistance: Analysis of three European countries. Antimicrob Resist Infect Control. 2018;7: 28. pmid:29468055
- 39. Aldeyab MA, Kearney MP, Scott MG, Aldiab MA, Alahmadi YM, Darwish Elhajji FW, et al. An evaluation of the impact of antibiotic stewardship on reducing the use of high-risk antibiotics and its effect on the incidence of Clostridium difficile infection in hospital settings. J Antimicrob Chemother. 2012;67: 2988–2996. pmid:22899806
- 40. Pulcini C, Morel CM, Tacconelli E, Beovic B, De With K, Goossens H, et al. Human resources estimates and funding for antibiotic stewardship teams are urgently needed. Clin Microbiol Infect. 2017;23: 785–787. pmid:28778544
- 41. Rawson TM, Moore LSP, Gilchrist MJ, Holmes AH. Antimicrobial stewardship: Are we failing in cross-specialty clinical engagement? J Antimicrob Chemother. 2016;71: 554–559. pmid:26498747
- 42. World Health Organization. Patient Engagement. In: Technical Series on Safer Primary Care [Internet]. 2016. Available at: http://apps.who.int/iris/bitstream/10665/252269/1/9789241511629-eng.pdf [cited 20 Jun 2017].
- 43. McCullough AR, Parekh S, Rathbone J, Del Mar CB, Hoffmann TC. A systematic review of the public’s knowledge and beliefs about antibiotic resistance. J Antimicrob Chemother. 2016;71: 27–33. pmid:26459555
- 44. England NHS. General Practice. Forward View. London: NHS England; 2016.
- 45. Klepser ME, Adams AJ, Klepser DG. Antimicrobial stewardship in outpatient settings: leveraging innovative physician-pharmacist collaborations to reduce antibiotic resistance. Health Secur. 2015;13: 166–173. pmid:26042860