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A whole-health–economy approach to antimicrobial stewardship: Analysis of current models and future direction

  • Monsey McLeod ,

    ‡ These authors share first authorship on this work.

    Affiliations Centre for Medication Safety and Service Quality, Pharmacy Department, Imperial College Healthcare National Health Service (NHS) Trust, London, United Kingdom, National Institute for Health Research Health Protection Research Unit, Healthcare Associated Infections and Antimicrobial Resistance, Imperial College, London in partnership with Public Health England, Hammersmith Hospital, London, United Kingdom

  • Raheelah Ahmad ,

    ‡ These authors share first authorship on this work.

    Affiliation National Institute for Health Research Health Protection Research Unit, Healthcare Associated Infections and Antimicrobial Resistance, Imperial College, London in partnership with Public Health England, Hammersmith Hospital, London, United Kingdom

  • Nada Atef Shebl,

    Affiliation Department of Clinical and Pharmaceutical Sciences, University of Hertfordshire, Hatfield, United Kingdom

  • Christianne Micallef,

    Affiliation Pharmacy Department, Cambridge University Hospitals NHS Foundation Trust, Addenbrooke's Hospital, Cambridge, United Kingdom

  • Fiona Sim,

    Affiliations Institute for Health Research, University of Bedfordshire, Luton, United Kingdom, NHS England (Midlands & East), United Kingdom

  • Alison Holmes

    alison.holmes@imperial.ac.uk

    Affiliation National Institute for Health Research Health Protection Research Unit, Healthcare Associated Infections and Antimicrobial Resistance, Imperial College, London in partnership with Public Health England, Hammersmith Hospital, London, United Kingdom

A whole-health–economy approach to antimicrobial stewardship: Analysis of current models and future direction

  • Monsey McLeod, 
  • Raheelah Ahmad, 
  • Nada Atef Shebl, 
  • Christianne Micallef, 
  • Fiona Sim, 
  • Alison Holmes
PLOS
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Summary points

  • 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.

Background

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) [3]; 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 [2]. This is driving much-needed antimicrobial stewardship (AMS) activities in animal production sectors [4]. 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 [7]. 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 [8]. Furthermore, use of accident and emergency departments by ambulatory patients contributes to fragmented care and overuse of antimicrobials [9]. 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 [2]. 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 [10]. 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’ [11]. 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 [12]. 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 [1317] (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).

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Table 1. Critical health system functions and elements of integration adapted from Atun and colleagues [16,18] for AMS initiatives.

https://doi.org/10.1371/journal.pmed.1002774.t001

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 [25]. AMS initiatives that had a shared governance structure across healthcare organisations (i.e., partially integrated) were either national programs [27] 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 [38]. 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 [33]. 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 [1923,25,27,30,31,39] (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.

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Fig 1. An overview of the extent of multisectoral AMS integration for each of the 16 AMS initiatives identified.

The integration framework is based on all six facets of critical health system function defined by Atun and colleagues [16,18] (Table 1). AMS, antimicrobial stewardship.

https://doi.org/10.1371/journal.pmed.1002774.g001

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 [30], 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 [40]. 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 [43]. 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.

Supporting information

S1 Appendix. Search strategy and article selection.

https://doi.org/10.1371/journal.pmed.1002774.s001

(PDF)

S1 Table. Frameworks for assessing extent of integration considered.

https://doi.org/10.1371/journal.pmed.1002774.s002

(PDF)

S2 Table. Overview of 15 integrated AMS initiatives.

AMS, antimicrobial stewardship.

https://doi.org/10.1371/journal.pmed.1002774.s003

(PDF)

Acknowledgments

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.

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