Antimicrobial Stewardship in General Practice: A Scoping Review of the Component Parts

There is no published health-system-wide framework to guide antimicrobial stewardship (AMS) in general practice. The aim of this scoping review was to identify the component parts necessary to inform a framework to guide AMS in general practice. Six databases and nine websites were searched. The sixteen papers included were those that reported on AMS in general practice in a country where antibiotics were available by prescription from a registered provider. Six multidimensional components were identified: 1. Governance, including a national action plan with accountability, prescriber accreditation, and practice level policies. 2. Education of general practitioners (GPs) and the public about AMS and antimicrobial resistance (AMR). 3. Consultation support, including decision support with patient information resources and prescribing guidelines. 4. Pharmacist and nurse involvement. 5. Monitoring of antibiotic prescribing and AMR with feedback to GPs. 6. Research into gaps in AMS and AMR evidence with translation into practice. This framework for AMS in general practice identifies health-system-wide components to support GPs to improve the quality of antibiotic prescribing. It may assist in the development and evaluation of AMS interventions in general practice. It also provides a guide to components for inclusion in reports on AMS interventions.

[In 1999 the Department of Health] Set out an action plan for the NHS, aimed at reducing the emergence and spread of antimicrobial resistance and its impact on the treatment of infection. Includes strategies to monitor and optimize antimicrobial prescribing by implementing antibiotic guidelines, supporting professional development on appropriate prescribing, reducing inappropriate prescribing and using clinical governance arrangements to support improved prescribing… [1]. Policy measures to advance appropriate, rational antibiotic use need to be country-specific and tailored to local circumstances including, but not limited to, the prevailing burden of disease, taking into account underlying comorbidities, such as HIV and AIDS, and existing resistance rates [2]. At the national level, operational action plans to combat antimicrobial resistance are needed to support strategic frameworks. All Member States are urged to have in place, within two years of the endorsement of the action plan by the Health Assembly, national action plans on antimicrobial resistance that are aligned with the global action plan and with standards and guidelines established by intergovernmental bodies... These national action plans are needed to provide the basis for an assessment of the resource needs, and should take into account national and regional priorities [3].

Secondary question: Which stakeholders have responsibility for governance of general practice AMS?
Establish clear governance arrangements. The Australian Government Department of Health and Department of Agriculture and Water Resources are responsible for the National Antimicrobial Resistance Strategy…Overall accountability for antimicrobial management lies at the highest level of each health service organisation, and with the clinicians responsible for delivering services efficiently and effectively… [4]. Policymakers are called upon to create an environment where the use of antibiotics is not the norm, by introducing disincentives to antibiotic use and surveillance programs, along with guidance that encourages and promotes self-management with symptomatic medications as the treatment in the first instance [2]. Strama is composed of a national steering group and regional Strama groups in every Swedish county [5]. Implementation of this guidance is the responsibility of local commissioners and/or providers. Commissioners and providers are reminded that it is their responsibility to implement the guidance, in their local context…Ensure that roles, responsibilities and accountabilities are clearly defined within an antimicrobial stewardship programme [6]. The professional bodies supporting this joint statement consider that action must be taken collegiately by the professions, commissioners, service providers, quality assurance bodies and regulators across the UK to reduce the threat of AMR. Leadership and action must be taken at local, regional, national and international level in support of the AMR strategy, and to tackle this issue in a concerted manner [7].

AMR included on national risk register
Recognize antimicrobial resistance as a priority need for action across all government ministries through inclusion in national risk registers or other effective mechanisms for cross government commitment [3].

Regulations around AMS & antibiotic prescribing
National, regional and local governments… responsibilities include legislation, regulation and auditing compliance with legal, policy and professional standards. [8].
Provide leadership to strengthen medicines regulatory systems at national and regional levels, so that appropriate practices for optimizing use of antimicrobial medicines are supported by appropriate and enforceable regulation, and that promotional practices can be adequately regulated [3].

Accreditation of prescribers
In the United Kingdom (UK) it is recommended that defined antimicrobial prescribing and stewardship competencies are incorporated into appraisals for prescribers. [9]. Professional organizations and societies should establish antimicrobial resistance as a core component of education, training, examination, professional registration or certification, and professional development…distribution, prescription, and dispensing of antimicrobials is carried out by accredited health or veterinary professionals under statutory body supervision… [3].

Funding for AMR/AMS activities
Sustainable funding is required to allocate time for clinical experts to work closely with prescribers. A mandate and financial support from the government is needed [10]. Member States should consider assessing investment needs for implementation of their national action plans on antimicrobial resistance, and should develop plans to secure and apply the required financing [3].

Planning for release of new antibiotics
Consider using multiple approaches to support the introduction of a new antimicrobial, including: electronic alerts to notify prescribers about the antimicrobial; prescribing guidance about when and where to use the antimicrobial in practice; issuing new or updated formulary guidelines and antimicrobial prescribing guidelines; peer advocacy and advice from other prescribers; providing education or informal teaching on ward rounds; shared risk management strategies for antimicrobials that are potentially useful but may be associated with patient safety incidents [6].

Practice level AMS policy and program
The stewardship programme is established with clear lines of accountability and there is a structure within the organisation/setting that can allow the implementation of a stewardship programme to take place, support the scheme, monitor its performance and hold it to account for performance and outcome measures… [9]. Outpatient clinicians and clinic leaders can implement policies and interventions to promote appropriate antibiotic prescribing practices. A stepwise approach with achievable goals can facilitate policy and practice changes and help clinicians and staff members from feeling overwhelmed. [11].

Monitoring of antibiotic prescriptions
Understanding local, regional and national variation in antimicrobial prescribing is essential for assessing the impact of interventions to change prescribing behaviour. Prescribing data need to be linked to antimicrobial resistance data and patient outcomes to ensure that both positive and negative potential outcomes are evaluated [12]. Consider using the following antimicrobial stewardship interventions: review of prescribing by antimicrobial stewardship teams to explore the reasons for increasing, very high or very low volumes of antimicrobial prescribing, or use of antimicrobials not recommended in local (where available) or national guidelines…Consider developing local systems and processes for peer review of prescribing. Encourage an open and transparent culture that allows health professionals to question antimicrobial prescribing practices of colleagues when these are not in line with local (where available) or national guidelines and no reason is documented [6]. When setting up tracking and reporting systems, decisions need to be made about the level at which to track and report (i.e., at the individual clinician level or at the facility level), which outcomes to track and report, and how to obtain the data for tracking and reporting. … Analysis can occur at the individual clinician level or at the facility level (i.e., aggregate of all clinician antibiotic prescriptions). The preferred approach, when possible, is to track antibiotic prescribing at the individual clinician level…Systems also can track the percentage of visits for which an individual clinician prescribes antibiotics (e.g., number of all antibiotics prescribed for all diagnoses by a clinician divided by the total number of visits for all diagnoses for that clinician). [11].
Secondary question: Which stakeholders have responsibility for monitoring of antibiotic prescribing in the general practice setting? Strama groups in every Swedish county (panel). The national Strama group includes a broad representation of professional organisations and relevant authorities. The main objectives of the national group are to coordinate activities for the containment of antibiotic resistance at the national level. Activities include the analysis of trends in antibiotic resistance and consumption [5]. MedQual …is a network dedicated to monitoring antibiotic use and antibiotic resistance [13].

Monitoring of antimicrobial resistance
We propose that resistance levels in the community could be monitored using sentinel general practices to systematically sample infections or even uninfected attending patients. Routine monitoring resistance in aerobes (collected by nasal swabs) should be straightforward-although anaerobes (collected by faecal swabs) would be more difficult [14]. Particularly important gaps in knowledge that need to be filled include the following: Information on: the incidence, prevalence, range across pathogens and geographical patterns related to antimicrobial resistance is needed to be made accessible in a timely manner in order to guide the treatment of patients; to inform local, national and regional actions; and to monitor the effectiveness of interventions… [3].

Secondary question: Which stakeholders have responsibility for developing and implementing monitoring of general practice antibiotic resistance?
The [clinical microbiology service] should provide annual analyses of cumulative AMR to groups with responsibility for local antimicrobial therapy guidelines to inform recommendations for local empirical therapy and formulary management [4]. Develop a national surveillance system for antimicrobial resistance that: includes a national reference centre with the ability systematically to collect and analyse dataincluding those on a core set of organisms and antimicrobial medicines from both health care facilities and the community -in order to inform national policies and decisionmaking; includes at least one reference laboratory capable of susceptibility testing to fulfil the core data requirements, using standardized tests for identification of resistant microorganisms and operating to agreed quality standards [3].

Feedback to prescribers and reporting
The how and why of measurement in antimicrobial stewardship is important but more important is that once you have gone to the effort to collect and analyse the data that you use it, that you share it with front-line clinicians to enable them to reflect on their practice and change their prescribing behaviour to improve patient outcomes and minimise resistance and other harm. It is important to share data in as near real time as possible…Comparison with peers and identification of prescribers who are outliers are useful techniques to change behaviour… [9]. Consider developing systems and processes for providing regular updates (at least every year) to individual prescribers and prescribing leads on: local and national antimicrobial resistance rates and trends; individual prescribing benchmarked against local and national antimicrobial prescribing rates and trends; patient safety incidents related to antimicrobial use, including hospital admissions for potentially avoidable life-threatening infections, infections with C. difficile or adverse drug reactions such as anaphylaxis [6].

Community & patient education about AMR and AMS
Consumers should be provided with information about the risks and benefits of the most effective and appropriate treatment options for them. This includes information about specific antimicrobials (if appropriate) and the risks associated with AMR. When discussing the use of antimicrobials and AMR with consumers, it is important that the messages are clear, simple and consistent. Information may need to be provided in different formats and styles, tailored to the needs and preferences of the consumer [4]. Objective 1: Improve awareness and understanding of antimicrobial resistance through effective communication, education and training. Steps need to be taken immediately in order to raise awareness of antimicrobial resistance and promote behavioural change, through public communication programmes that target different audiences in human health, animal health and agricultural practice as well as consumers. Inclusion of the use of antimicrobial agents and resistance in school curricula will promote better understanding and awareness from an early age [3].

Secondary question: Which stakeholders have responsibility for implementing community and patient education about AMR and AMS?
All staff members in outpatient facilities, including administrative staff members, medical assistants, nurses, allied health professionals, and medical directors, can improve antibiotic prescribing by using consistent messages when communicating with patients about the indications for antibiotics [11]. Other stakeholders -including civil society organizations, trade and industry bodies, employee organizations, foundations with an interest in science education, and the media -should help to promote public awareness and understanding of infection prevention and use of antimicrobial medicines across all sectors [3].

GP continuing education in AMS & AMR
For clinicians, AMS education should start during undergraduate training and continue throughout their careers. Local education programs should include local AMS recommendations. Programs that are multifaceted and include one or more active educational activities are more likely to be successful in changing clinicians' behaviour [4]. Support multiprofessional local groups in the implementation of infection treatment recommendations, e.g. by producing locally adapted materials and local educational meetings and events [10].

GP education about nonantibiotic management of self-limiting infection
If antimicrobial treatment is not considered necessary, give the patient advice about the expected natural history of the illness, the limited or absent benefit of antimicrobial treatment, and the potential unwanted side effects of antimicrobials such as diarrhoea and rash, recommendations for symptom management, as well as advice about actions in case of worsening clinical condition (safety netting) [8].
If immediate antimicrobial prescribing is not the most appropriate option, discuss with the patient and/or their family members or carers (as appropriate) other options such as self-care with over-the-counter preparations, back-up (delayed) prescribing, other non-pharmacological interventions, for example, draining the site of infection [6]. GP education about delayed prescribing or watchful waiting Senior leaders, including medical directors, Clinical Commissioning Group (CCG) chairs and directors of public health, need to support and empower prescribers, and other health and public health professionals who advise on prescribing decisions, to make the decision not to prescribe where other appropriate strategies exist such as 'watchful waiting' or delayed prescribing [7].

General practice team member education
Communicate with all clinic staff members to set patient expectations. Patient visits for acute illnesses might or might not result in an antibiotic prescription. All staff members in outpatient facilities, including administrative staff members, medical assistants, nurses, allied health professionals, and medical directors, can improve antibiotic prescribing by using consistent messages when communicating with patients about the indications for antibiotics. Education for clinicians and clinic staff members can reinforce appropriate antibiotic prescribing and improve the quality of care [11].

Independent education (restrict pharma marketing)
Drug advertising and academic detailing by pharmaceutical companies influences physicians prescribing behaviours. Further regulation of the material supplied to clinicians by the pharmaceutical industry may be needed if overuse of broad-spectrum antimicrobials is to be reduced. [15]. In some cases, industry spending on promoting products is greater than governmental investment in promoting rational use of antimicrobial medicines or providing objective information…Professional bodies and associations, including industry associations, health insurance providers and other payers, should develop a code of conduct for appropriate training in, education about, and marketing, purchasing, reimbursement and use of antimicrobial agents. This code should include commitment to comply with national and international regulations and standards, and to eliminate dependence on the pharmaceutical industry for information and education on medicines and, in some cases, income [3].

Consultation support Prescribing guidelines
Evidence-based prescribing guidelines for antimicrobials are a fundamental component of AMS programs because they guide appropriate antimicrobial use. They can also be used to educate prescribers and students on accepted practice for antimicrobial prescribing in the organisation…This includes the importance of documenting in the patient's healthcare record the indication for the prescribing decision and, where the prescriber varies from guideline-concordant practice, the rationale for the decision [4]. Organizational structures could pose barriers to [AMS]. Clinic visits were often too brief to discuss guidelines with patients…External guidelines were not always used because they were sometimes difficult to locate, too long, or not seen as relevant…external guidelines needed to be accessible to clinicians and trusted by clinicians [16]. …national treatment guidelines must include: diagnostic criteria for each condition; an analysis of the antibiotic risks and benefits both for the patient and for society; and recommendations for when to reevaluate a patient's treatment. Second, to ease the implementation of national guidelines in primary health care, they need to be transformed into simple treatment algorithms, e.g. clear advice to health professionals on when and when not to prescribe an antibiotic…easily accessible summaries of guidelines for common infections have been well received and used [10].

Secondary question: Which stakeholders have responsibility for implementing prescribing guidelines?
In 2010 the UK Health Protection Agency developed and updated antibiotic guidance for GPs, which was locally adaptable by primary care trusts and distributed to practices [1]. Require explicit written justification in the medical record for nonrecommended antibiotic prescribing. This technique has reduced inappropriate prescribing by holding clinicians accountable in the medical record for their decisions [11].

Point of care tests
In POC testing interventions, participants found that it was unclear which staff members to train in POC testing, as various organizational roles performed the test in different clinics [16]. A disadvantage of near patient testing is that it may increase patients' expectations and increase re-consultation by medicalising self limiting illnesses such as sore throat [15]. Decisions to prescribe antibiotics are rarely based on definitive diagnoses. Effective, rapid, low-cost diagnostic tools are needed for guiding optimal use of antibiotics in human and animal medicine, and such tools should be easily integrated into clinical, pharmacy and veterinary practices [3].

Microbiology testing and reporting
Microbiology testing is a key component of antimicrobial stewardship (AMS). The clinical microbiology service (CMS) performs the combined role of patient-specific diagnostic testing to guide direct patient care, and system-wide diagnostic stewardship, surveillance of resistant organisms and outbreak investigation. a positive microbiology diagnostic test is used to confirm a provisional clinical diagnosis, and the antimicrobial susceptibility results guide targeted antimicrobial management. Optimal specimen collection and transport are critical elements of the testing process. [4]. Restrictive reporting of the results of antimicrobial susceptibility testing is one stewardship activity that varies from laboratory to laboratory and, perhaps, may be underused… [9].
Considering that most bacterial infections are also self-limiting (5), antibiotic prescription on the basis of a positive result in an otherwise healthy individual should be carefully considered [2].
Allergy testing Promote allergy testing for patients with a history of allergic reaction to beta-lactams, as a measure to promote use of first-line antimicrobials in non-allergic patients [8].

Electronic decision support for prescribers
eCDSSs [Electronic clinical decision support systems] can organise and present appropriate information to the user in a way that supports them to make clinical decisions with increased accuracy and reduced error… may include online access to documents such as formulary restrictions, local antimicrobial prescribing guidelines and Therapeutic Guidelines: Antibiotic [4]. Advanced decision support systems use complex logic, mathematical modelling or case-based probabilities to provide patient-specific recommendations. They can provide decision support by helping identify potential infections, pathogens and treatment options based on inputs about patient symptoms… CDSSs are simply assistive tools and cannot replace expert decision-making. They may support the prescriber or the AMS program, or both [9].

Expert advice
Clinicians may also want to discuss antimicrobial prescriptions with nominated experts based on clinical concerns. Pathways for prescribers in community settings to access such specialist advice should be clearly identified. This may occur through links with ID or pharmacy services at local hospitals, or with clinical microbiologists at laboratory service providers…Telehealth can support improved access to clinical services, specialist advice, diagnostic information and education, over distance, as part of formalised service networks [4]. Strategies to encourage appropriate prescribing in primary care include the development of evidence-based policies, in collaboration with local experts, who provide practical guidance on how to rule out serious infections and how to handle patient demand for an antibiotic, complemented by information on various symptomatic treatment options [2]. Clinical microbiologists should be available to clinicians for counselling on diagnostics of infectious diseases, including correct sampling and interpretation of test results, difficult-to-treat pathogens and complicated infections. Pharmacists in community and hospital settings have expertise in medicines and are the gatekeepers to the use of antimicrobials. As such, pharmacists can act as an important source of advice and information for patients and prescribers on the safe, rational and effective use of antimicrobials [8]. Telephone advice lines are provided in a few regions of France. These are provided by hospitals or health networks and may be staffed by an infectious disease specialist or a trained GP [13].

Decision support for use with patients
Providing easy-to-understand information to consumers about the expected duration of symptoms, and how to identify signs and symptoms of more serious illness, may help to manage their expectations about antimicrobials. Consumers should be provided with information about the risks and benefits of the most effective and appropriate treatment options for them... When discussing the use of antimicrobials and AMR with consumers, it is important that the messages are clear, simple and consistent. Information may need to be provided in different formats and styles, tailored to the needs and preferences of the consumer [4]. Patient information leaflets on common infections are produced in six languages to target a large proportion of the immigrant population [10].

Unit dispensing
Explore per unit dispensing of antimicrobials taking into consideration all relevant guidelines and regulations [8].

Supply of and timely access to antibiotics
Ensure the adequate supply of, and timely access to, antimicrobials…Certain interventions, such as removing broad-spectrum antimicrobials from clinical areas to limit their inappropriate use, may delay antimicrobial delivery if appropriate pathways for antimicrobial supply do not accompany the restrictions [4]. Ensure access to the antimicrobials recommended in clinical guidance, by conducting a review of national market availability, implementing measures to support sustained market availability for both innovative and generic products and tackling shortages. At the same time, limit the use of last-resort antimicrobials to safeguard their effectiveness, by establishing restrictive measures for use… [8].

Pharmacy review & advice
In addition to clinically reviewing and dispensing antimicrobial prescriptions, community pharmacists can educate patients and carers about using antimicrobials appropriately…Pharmacists should consider whether there is still a clinical need to fill all prescriptions presented -for example, original and repeat prescriptions that are presented for dispensing several months after they were written (when it would be expected that the original infection would have resolved), or prescriptions for long-term use (for example, for several months). Such prescriptions should only be dispensed if the pharmacist is satisfied that the use is appropriate. If not, there should be discussion with the prescriber. Community pharmacy is an important site of community education and activities for AMS in primary care because of the ease and frequency of the public's access to community pharmacists compared with other clinicians…At the system level, the pharmacist's role may include planning and implementing AMS programs and other initiatives that encourage appropriate antimicrobial use [4]. It is important that any advice on medications and formulations is tailored to the patient's specific symptoms and preferences. In addition, pharmacy staff need to be able to identify red-flag symptoms and other risk factors for a serious infection and refer patients to physicians where necessary… [2].

Appropriate disposal of left-over antibiotics
It should be routine practice that consumers who have been dispensed antimicrobials, or their carers, are…Advised not to keep any unused antimicrobials, but to return them to a pharmacy for disposal [4].

Nurse triage, patient assessment & education
…professional associations and experts, internationally and in Australia, highlight that nurses, midwives and infection control practitioners (ICPs) play key roles in preventing and controlling AMR. They can help to safeguard the effectiveness of antimicrobials through infection prevention and control, education, and involvement in AMS activities. [4]. Materials are created for nurses providing education about common infections to parents of newborns at child health-centres and for schoolchildren… [10]. Use call centers, nurse hotlines, or pharmacist consultations as triage systems to prevent unnecessary visits [11].

Research into AMR/AMS gaps, translation into practice
Agree a national research agenda and promote investment in innovative approaches to containing antimicrobial resistance…Priority areas for action are to: Identify current gaps, and agree to national research and development priorities… More research is needed to understand any unintended consequences of the use of restrictive interventions [4]. Few studies focused on the organization component of the work system model or the structures and roles that organize a clinic… [16]. There is a paucity of studies on the potential harm of withholding or overuse of antibiotics and how to identify which patients may benefit, and by how much [15]. …implementation research is needed to determine which outpatient stewardship interventions work best in different outpatient settings, effective strategies to implement interventions, and sustainable approaches to outpatient stewardship [11].

Research into context, culture of general practice and behaviour change strategies
In general, prescribing has been shown to be influenced by several factors, including the cultural beliefs of the patient and the prescriber, patient demand, socio-economic factors and clinical autonomy. [12]. Understanding the organisational context, culture and workplace norms, including local prescribing rules and behaviours, is critical to successfully establishing an AMS program. A 'one size fits all' approach is not appropriate and does not sufficiently recognise that each setting has unique elements to be considered, such as enablers and barriers for appropriate antimicrobial prescribing and use… Education strategies that incorporate behaviour change principles such as audit and feedback, along with more active strategies including academic detailing, consensus-building sessions and educational workshops, are more effective in changing behaviour than the passive dissemination of information alone [4].