Hospital-based antimicrobial stewardship, India

Bull World Health Organ 2023;101:20–27A | doi: http://dx.doi.org/10.2471/BLT.22.288797 Research 20 Introduction In recent years, several low- and middle-income countries, including India, have reported alarming rates of antimi- crobial resistance. The Global action plan on antimicrobial resistance released by the World Health Organization (WHO) recognized effective implementation of hospital antimicro- bial stewardship programmes as one of the key priorities to protect the efficacy of antimicrobials.1,2Antimicrobial stew- ardship is a coordinated set of cost-effective interventions which support the use of microbiological data to rationalize antimicrobial prescriptions and reduce their adverse effects.3 India’s national action plan for antimicrobial resistance (2017–2021) also recognized antimicrobial stewardship as a key strategy to optimize and reduce the use of antimicrobial drugs.4 However, India does not yet have a national-level antimicrobial stewardship plan. There are several barriers to implementing an effective antimicrobial stewardship programme in low- and middle- income countries.5,6 The foremost barrier is that guidance for establishing such programmes has primarily been developed for hospitals in high-income countries and is often unsuit- able for the health-care systems in low- and middle-income countries. The implementation of antimicrobial stewardship in high-income settings is driven by infectious disease physi- cians and pharmacists, and in some hospitals the entire anti- microbial stewardship programme is pharmacist-led.7 A lack of trained manpower, especially infectious disease physicians and pharmacists, makes it challenging to establish antimicro- bial stewardship in low- and middle-income countries such as India, especially in public sector hospitals.8 The Indian Council of Medical Research undertook a survey in 2015 to understand the capacity available in Indian hospitals for implementing antimicrobial stewardship pro- grammes. The survey highlighted many gaps and challenges. Since then, the council has taken several steps to address these gaps.9 As a preparatory step, in 2017 the council organized capacity-building workshops for hospital teams to sensitize them to the core principles of antimicrobial stewardship.9 Here we report the systematic approach followed by the council to implement antimicrobial stewardship interventions in Indian tertiary hospitals.10 We describe our experience of creating the framework for the interventions – the processes followed, challenges faced and progress made – and suggest mechanisms to sustain antimicrobial stewardship in low- and middle-income settings. Methods Setting In 2017 the Indian Council of Medical Research established a network of tertiary care hospitals to participate in antimicro- bial resistance surveillance.10 We conducted this implementa- tion study in all 20 hospitals of the network, which cover a wide range of geographical regions of India. The selected hospitals included 14 government and six private hospitals. All hospitals provided services to both urban and rural populations. The authorized bed capacity of these 20 hospitals ranged from 373–4500 (intensive care unit 18–360 beds) with an average bed occupancy of 75–100%. The study was approved by the institutional human ethics committees of the participating hospitals. a Division of Epidemiology and Communicable Diseases, Indian Council of Medical Research, New Delhi, Ansarinagar, 110029 India. b Department of Infectious Diseases, Apollo Hospitals, Chennai, India. c Division of Infectious Diseases, Rajiv Gandhi Cancer Institute and Research Centre, New Delhi, India. Correspondence to Kamini Walia (email: waliakamini@ yahoo .co .in). (Submitted: 21 June 2022 – Revised version received: 26 September 2022 – Accepted: 12 October 2022 – Published online: 9 November 2022 ) Hospital-based antimicrobial stewardship, India Sonam Vijay,a V Ramasubramanian,b Nitin Bansal,c VC Ohria & Kamini Waliaa Objective To establish a framework for implementing antimicrobial stewardship in Indian tertiary care hospitals, and identify challenges and enablers for implementation. Methods Over 2018–2021 the Indian Council of Medical Research followed a systematic approach to establish a framework for implementation of antimicrobial stewardship in Indian hospitals. We selected 20 Indian tertiary care hospitals to study the feasibility of implementing a stewardship programme. Based on a questionnaire to lead physicians before and after the intervention, we assessed progress using a set of process and outcome indicators. In a qualitative survey we identified enablers and barriers to implementation of antimicrobial stewardship. Findings We found an improvement in various antimicrobial stewardship implementation indicators in the hospitals after the intervention. All 20 hospitals conducted monthly point prevalence analysis of cultures compared with three hospitals before the intervention. The number of hospitals that initiated formulary restrictions increased from two to 12 hospitals and the number of hospitals that started practising prescription audit and feedback increased from six to 16 hospitals. Respondents in 15 hospitals expressed their willingness to expand the coverage of antimicrobial stewardship implementation to other wards and intensive care units. Six hospitals were willing to recruit the permanent staff needed for antimicrobial stewardship activities. Conclusion Antimicrobial stewardship can be implemented in Indian tertiary hospitals with reasonable success, subject to institutional support, availability of trained manpower and willingness of hospitals to support antimicrobial stewardship-related educational and training activities. 21Bull World Health Organ 2023;101:20–27A| doi: http://dx.doi.org/10.2471/BLT.22.288797 Research Antimicrobial stewardship in Indian hospitalsSonam Vijay et al. Intervention The first step in the series of initiatives in 2017 was to put together a generic protocol and seek local hospital com- mitment and support. We held a meeting with hospital administrators to discuss the skilled manpower and logistic re- quirements needed to implement the protocol. After that, hospitals were invited to participate in an antimicro- bial stewardship study. An introductory workshop was held for participants in 2018. The discussions following the workshop helped participants to un- derstand the feasibility of initiating an antimicrobial stewardship programme in their hospital. Participants identified easily attainable objectives which could be translated into achievable results, while deferring consideration of more challenging objectives.11 In 2018 we conducted a cross- sectional study to collect information on antimicrobial stewardship policies and practices being followed in the participating hospitals. We recruited a clinician or intensive care physician from each hospital to act as lead in- vestigator. Lead physicians answered an email questionnaire on the antimi- crobial stewardship practices in their hospital (available in data repository)12. The questions included whether the institution had a written antimicrobial stewardship document and stewardship committee; whether, and how often, they monitored microbial resistance data and antibiotic prescribing practices; and whether they had a hospital antibiogram and formulary restrictions. Based on the insights from the baseline assess- ment, we devised a stepwise approach for implementation of an antimicrobial stewardship programme in Indian ter- tiary hospitals (Fig. 1). Using information from the base- line assessment and consultations, we determined a key set of activities for the participating hospitals to under- take in the next 3-year period (Box 1). These activities were the foundation of the council’s Antimicrobial Stew- ardship Programme Implementation and Research Initiative (ASPIRE) and formed the basis of a set of process and outcome indicators for monitoring the programme. Implementation The antimicrobial stewardship inter- ventions were implemented in the 20 participating hospitals over 2019–2021; most hospitals were able to initiate ac- tivities in the first quarter of 2019. We provided guidance to all participating hospitals through periodic meetings and workshops conducted by the council. To implement the programme, the council provided funding of 15 000 United States dollars annually to each hospital for up to 3 years to cover expenses for skilled manpower (two new positions, a phar- macist and a nurse, in each hospital), non-recurring expenditure (such as computers), consumables and funding for trainings, meetings, transportation and other costs. Assessment We monitored progress and evaluated the implementation of the steward- ship programme in its initiation and expansion phases using the process and outcome indicators summarized in Box 1.14 In the initiation phase, the study was limited to selected beds in intensive care units. In the expansion phase we had proposed to expand the coverage of antimicrobial stewardship to 10% of total beds. To assess the progress made, lead physicians from the participating hos- pitals repeated the questionnaire from the baseline assessment in 2019. We also performed a comparative analysis of data collected from hospitals before and after the intervention. We drew up a set of process and outcome indicators to evaluate. All the hospitals entered data using the online platform developed by the council.12 Antibiotic consumption was measured using days of therapy and defined daily doses as units. Key activities undertaken in the first year were: (i) point prevalence analysis of antimicrobial resistance of cultures; (ii) initiation of formulary restrictions; (iii) prescription audits; (iv) constitu- tion of antimicrobial stewardship com- mittees; and (v) creation of antibiogram- based guidelines. In the expansion phase, in addition to the activities in the initiation phase, hospitals analysed: Fig. 1. Timeline of the Antimicrobial Stewardship Programme Implementation and Research Initiative of the Indian Council of Medical Research Start of Indian Council of Medical Research antimicrobial stewardship initiative Building capacities for antimicrobial stewardship in tertiary care hospitals Implementation stages of initiative Initiation phase Expansion phase 2017 2018 2018 2018-2019 2019 2019- • Generic protocol of antimicrobial stewardship drawn up • Meetings with hospital administrators • Introductory workshop with hospital lead investigators • Engagement with lead investigators through site visits and interactive meetings • Guidance documents published: - Treatment guidelines for antimicrobial use in common syndromes, 1st edition - Hospital infection control guidelines - Antimicrobial stewardship programme guidelines • Engagement with lead investigators through site visits and interactive meetings and workshops • Monitoring progress on indicators and data collection during intervening periods • Guidance document revised: - Treatment guidelines for antimicrobial use in common syndromes, 2nd edition • Capturing data on indicators • Monthly data submitted to Indian Council of Medical Research online database • Education and awareness activities 22 Bull World Health Organ 2023;101:20–27A| doi: http://dx.doi.org/10.2471/BLT.22.288797 Research Antimicrobial stewardship in Indian hospitals Sonam Vijay et al. (i) antibiotic prescriptions; (ii) adher- ence to hospital policies; and (iii) clini- cal outcomes. Antibiotics prescribed to patients were analysed according to the World Health Organization’s Access, Watch, Reserve (AWaRe) classifica- tion. Clinical outcomes from intensive care units and ward patients’ data were recorded as cured and discharged; left against medical advice; or death. Each hospital conducted the point prevalence survey of cultures every month of the study period and recorded rates of de- escalation of antibiotic use. We also did a qualitative survey to obtain feedback on the hospitals’ experience of the programme via an email questionnaire (available in the data repository).12 Lead physicians were asked about their views on antimicrobial stewardship for health-care institutions; their motivation for working on the programme; challenges faced during the implementation of antimicrobial stew- ardship in their hospital and their sug- gested solutions; and positive changes after implementation of antimicrobial stewardship. Individual hospitals did their own data analysis and uploaded antimicro- bial consumption data to the online data system. The data was received and analysed at the Indian Council of Medi- cal Research coordination unit from all the participating hospitals in the form of annual reports. Results Assessment of progress Multidisciplinary team The improvements in the various antimi- crobial stewardship parameters before and after the intervention in hospitals are summarized in Fig. 2. The data show that after the intervention, 19 of the 20 hospitals (95%) had established antimi- crobial stewardship teams as compared with only seven hospitals (35%) before the intervention. After the intervention, a physician, clinical microbiologist and hospital administrator were part of the antimicrobial stewardship committee in 19 hospitals (95%), a clinical pharmacist in 17 hospitals (85%), a nurse in 12 hospitals (60%) and an infectious dis- ease specialist in seven hospitals (35%). Nineteen hospitals (95%) conducted regular antimicrobial stewardship team meetings after the intervention, of which nine hospitals (45%) organized quarterly meetings and five hospitals (25%) half-yearly meetings. These data demonstrate substantial improvements as only five hospitals (25%) had these meetings before the intervention. Full details of the progress in antimicrobial stewardship after the intervention are shown in the data repository.12 Guidelines and policies After the intervention, all 20 hospitals were able to create the hospital anti- biogram and 18 hospitals were able to develop an antibiotic policy based on the antibiogram. Capacity-building work- shops on antimicrobial stewardship were organized by all hospitals, compared with only one hospital before imple- mentation of the intervention. Overall, the 20 hospitals conducted training for 2377 medical and paramedical staff over the study period, thus expanding the provision of antimicrobial stewardship education after the intervention. Improvement strategies Analyses of antimicrobial resistance and monitoring of antimicrobial use were performed by 19 hospitals (95%) compared with only 15 hospitals (75%) before the intervention period. The practice of formulary restriction was in- troduced by 12 hospitals (60%), of which six hospitals reported restrictions on the use of colistin, four hospitals restricted polymyxin B, four hospitals restricted ceftazidime–avibactam and tigecycline, three hospitals restricted carbapenems and two hospitals restricted linezolid and fosfomycin. Only two hospitals (10%) reported having formulary re- strictions before the intervention period. After the intervention 16 hospitals (80%) introduced prescription audit and feedback, compared with only six (30%) hospitals that used it before the intervention. A point prevalence survey of cultures from patients before initia- tion or change in antibiotics was carried out by all 20 hospitals (100%) after the intervention, compared with only three hospitals before the intervention (15%). Fifteen hospitals were able to obtain clinical outcome data from a total of 20 691 patients in the expansion phase of the initiative. The full data are shown in the data repository.12 Fig. 3 (available at: https:// www .who .int/ publications/ journals/ bulletin/ ) shows the AWaRe groups of 14 168 antibiotic prescriptions in 13 of these hospitals. The proportion of antibiotics prescribed from the Access group ranged from 4% to 52% across the hospitals. We found that across all Box 1. Key activities and indicators for assessing the implementation of an antimicrobial stewardship programme in Indian hospitals Initiation phase (2019): process indicators • Set up a hospital antimicrobial stewardship committee. • Create an antibiotic policy based on the hospital antibiogram. • Undertake point prevalence surveys of antimicrobial resistance from cultures. • Record antibiotic consumption in intensive care units (days of therapy and defined daily doses). • Initiate prescription audits for carbapenems and polymyxin prescriptions in intensive care units. • Initiate formulary restrictions. • Implement initial or minimal level of de-escalation of antibiotic use.a • Organize awareness and education workshops for staff on antimicrobial stewardship. Expansion phase (2020): process and outcome indicators • Expand the implementation of antimicrobial stewardship within hospital to increase the coverage to10% of total beds (10% of intensive care beds and 10% of non-intensive care beds). • Monitor adherence to hospital antibiotic policies. • Continue capturing antibiotic consumption and prescription audits. • Classify antibiotic consumption data as per the AWaRe classification of the WHO: Access, Watch or Reserve.13 • Record patients’ clinical outcomes: cured and discharged; left hospital against medical advice; or died. WHO: World Health Organization. a De-escalation criteria were: stopping antibiotics within 5 days; changing from combination to monotherapy; and changing narrower spectrum intravenous drugs to oral formulations. 23Bull World Health Organ 2023;101:20–27A| doi: http://dx.doi.org/10.2471/BLT.22.288797 Research Antimicrobial stewardship in Indian hospitalsSonam Vijay et al. hospitals, 2752 (19%) antibiotics were prescribed from the Access group, 8732 (62%) antibiotics were prescribed from the Watch group and 2684 (19%) antibiotics were prescribed from the Reserve group. Participants’ experiences According to the qualitative survey, 12 hospitals (60%) had a positive experi- ence of the antimicrobial stewardship implementation project according to the lead physician. Respondents reported that activities undertaken in the study were helpful in creating awareness about the appropriate choice of antimicrobials and the correct dosage and duration of use among the medical staff of their hos- pital. Antimicrobial stewardship com- mittees in 19 hospitals (95%) conducted regular meetings and undertook annual updates of the antibiotic policy. Nine hospitals (45%) reported improvement in obtaining cultures before the use of antimicrobial drugs or any change in an- timicrobials. This approach was helpful in restricting unnecessary antibacterial and antifungal use as reported by eight hospitals (40%). Respondents in all hospitals expressed their desire and will- ingness to continue antimicrobial stew- ardship as a permanent activity, while six hospitals (30%) have also assigned permanent hospital staff for manage- ment of antimicrobial stewardship after completion of the project. Overall, phy- sicians in 16 hospitals (80%) saw value in expanding the coverage of antimicrobial stewardship to more intensive care units than those included in the current study. Antimicrobial stewardship committees in 14 hospitals (70%) have decided to continue the stewardship activities after the completion of the project, including measuring antimicrobial consumption by prescription audit in intensive care units, carrying out monthly point preva- lence studies, implementing formulary restrictions and conducting educational and awareness activities for staff on antimicrobial stewardship. Discussion The core elements for setting up effective antimicrobial stewardship in hospitals requires a structure and resources that are usually not available in hospitals in low- and middle-income countries.11 The Indian Council of Medical Research supported 20 Indian tertiary care hos- pitals to set up a framework for imple-F ig . 2 . Ac tiv iti es co m pl et ed b ef or e a nd af te r i m pl em en ta tio n of th e a nt im icr ob ia l s te w ar ds hi p in te rv en tio n in 20 In di an te rt ia ry ca re h os pi ta ls, 20 19 –2 02 1 Ho sp ita ls An tim icr ob ia l st ew ar ds hi p do cu m en t An tim icr ob ia l st ew ar ds hi p co m m itt ee An tim icr ob ia l st ew ar ds hi p te am m ee tin gs An tim icr ob ia l re sis ta nc e d at a an al ys is An tib io gr am de ve lo pe d An tib io tic p ol icy de ve lo pe d An tib io tic p ol icy im pl em en ta tio n Po in t p re va le nc e An tim icr ob ia l a ge nt us ag e d at a an al ys ed W rit te n gu id el in es fo r a nt im icr ob ia l ag en t p re sc rip tio ns Fo rm ul ar y re st ric tio n im pl em en te d Au di t o f pr es cr ip tio n an d fe ed ba ck Be for e Af ter Be for e Af ter Be for e Af ter Be for e Af ter Be for e Af ter Be for e Af ter Be for e Af ter Be for e Af ter Be for e Af ter Be for e Af ter Be for e Af ter Be for e Af ter 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 To tal no . o f h os pit als co m ple tin g a cti vit y 5 16 7 19 5 19 15 19 17 20 14 18 9 15 3 20 9 19 9 15 2 12 6 16 N o Ye s Ac tiv ity co m pl et ed N ot e: W e an al ys ed d at a fro m b ef or e th e in te rv en tio n in F eb ru ar y 20 18 a nd a fte r t he in te rv en tio n in Ju ne 2 01 9. 24 Bull World Health Organ 2023;101:20–27A| doi: http://dx.doi.org/10.2471/BLT.22.288797 Research Antimicrobial stewardship in Indian hospitals Sonam Vijay et al. menting antimicrobial stewardship by providing funding and the necessary training and guidance. Our findings document that nearly all hospitals that participated in the study appreciated the importance of implementation of antimicrobial stewardship strategies and welcomed the initiative. The available guidelines on antimi- crobial stewardship from high-income countries clearly specify that infectious disease specialists and clinical pharma- cists are the pillars of hospital antimi- crobial stewardship.15,16 Indian hospitals have a shortage of both professions, as highlighted in our previous survey.8 In the current study, we addressed this challenge by choosing intensive care physicians and clinicians (paediatricians and surgeons) to lead this initiative in their respective hospitals. These profes- sions are likely to be the most committed to antimicrobial stewardship and all the participants led the projects with good success at all hospitals, irrespective of their specialization. Our study showed that 19 out of 20 hospitals were able to formulate a multidisciplinary team and undertake capacity-building activities that led to successful implementation of the proposed activities. Capacity-building is one of the key components for in- stituting antimicrobial stewardship programmes in low- and middle-income countries.17 Furthermore, providing clinical pharmacists to hospitals led to recognition of the value a clinical pharmacist brings to the quality of antimicrobial prescribing. In our study, antimicrobial stewardship driven by clinical pharmacists led to 80% of hos- pitals practising audit and feedback and 60% of hospitals applying formulary restrictions on the use of many broad- spectrum antimicrobials compared with 30% and 10% of hospitals, respectively, before the intervention. All 20 hospitals were able to mea- sure the process indicators during the first year of the study but, due to the coronavirus disease 2019 (COVID-19) pandemic, data on the outcome indica- tors were available in only 15 hospitals. All hospitals conducted point preva- lence surveys of antimicrobial resis- tance in cultures after the antimicrobial stewardship intervention. All hospitals performed appropriate antimicrobial sensitivity tests from bacterial or fun- gal cultures for all patients who were prescribed parenteral antimicrobials. In our study, prescriptions of antibiot- ics from the Access group were in the range of 4–52%, contrary to the WHO AWaRe policy-based indicator which recommended that more than 60% of antibiotics prescribed should be from the Access group.18 A 2019 study of antibiotic sales data from India also documented minimum consumption of antibiotics from the Access group.19 Antimicrobial stewardship activities suffered a setback in all hospitals due to the COVID-19 pandemic response. Reluctance to accept formulary restric- tions and de-escalation of therapy in some hospitals was also among the key challenges that we identified. Through this study we wanted to evaluate whether hospitals were re- ceptive to changes after antimicrobial stewardship interventions. Overall, the hospital administrators and clinicians were supportive of introducing antimi- crobial stewardship and the clinicians reported having positive experiences in their institutions. This finding could be attributed to the sensitization meetings with hospital administrators, which the council organized before launching the project. Antimicrobial stewardship implementation in these hospitals dem- onstrated small but effective changes. It is encouraging to note that most of the hospitals were able to initiate the activities to measure the process and outcome indicators, although no trend could be documented. However, the data on outcome indicators continue to be monitored and further findings will reveal trends over time. As a next step, to further enhance the hospital’s antimicrobial stewardship plan for ac- curate and consistent data collection of antimicrobial utilization, the council has approved funds to these hospitals for collecting data on outcome measures related to antimicrobial stewardship for another 3 years. The next phase will be to understand the impact of the inter- vention on optimizing antimicrobial selection (drug, dose and duration) and on reducing adverse drug events (mor- bidity and mortality, length of hospital stay and health-care expenditure). For this phase, hospitals will measure the impact of stewardship on performance indicators such as adherence to guide- lines, multidrug resistance rates, clinical outcomes and antimicrobial consump- tion.20 Capturing these outcomes is important not only for evaluating the success of the antimicrobial steward- ship at an individual hospital level but also for identifying areas for further improvement.21,22 Although the council is providing funds to these hospitals for a finite period, the hospitals have been asked to identify resources to sustain the antimicrobial stewardship activities beyond completion of the project. There were many administrative challenges in running this project. One challenge was that senior clinicians and surgeons have little time to spare for the stewardship activities owing to busy clinics and hospital administration responsibilities. Another issue was that principal investigators of the projects, who were mostly clinicians, were not ac- customed to managing research grants, and had difficulty finding time from their clinical work. Many sites reported staff leaving in the middle of the project, which also led to interruptions in data collection. Unfortunately, the ongoing antimicrobial stewardship activities were de-prioritized in five hospitals out of 20 (three government and two private hospitals) at the time of the COVID-19 pandemic. During the pandemic, these hospitals faced challenges in accessing intensive care units and gathering infor- mation, as most of their intensive care units were converted to COVID care, and because fewer non-COVID patients were admitted during that period. Nevertheless, our experience shows that – in the absence of infectious disease specialists – intensive care physicians or other clinicians can lead effective antimicrobial stewardship activities in hospitals. Administrative support for antimicrobial stewardship within the hospital and the availability of clinical pharmacists exclusively for antimicrobial stewardship, supported through hospital funds, would be crucial for sustaining this activity in Indian hospitals. With the increasing levels of micro- bial resistance to all the broad-spectrum antimicrobials in India,23 there is an urgent need to prioritize antimicrobial stewardship. Optimizing and reduc- ing the use of antimicrobials (strategic priority No. 4 of India’s national action plan) needs to be achieved through implementation of mandatory national antimicrobial stewardship at least in all tertiary and secondary level hospitals. The tertiary care hospitals included in this study offer the advantage of having multidisciplinary teams, which are cru- cial for implementation of antimicrobial 25Bull World Health Organ 2023;101:20–27A| doi: http://dx.doi.org/10.2471/BLT.22.288797 Research Antimicrobial stewardship in Indian hospitalsSonam Vijay et al. stewardship. From our experience, we envision that implementing an effective antimicrobial stewardship programme in secondary hospitals is going to be even more challenging, in terms of infrastructure constraints, financial constraints, lack of trained manpower and lack of higher-level support. Be- sides that, microbiology laboratories in low-resource settings do not have qual- ity control systems, infrastructure and trained manpower.24 Factors which are key for the successful implementation of antimicrobial stewardship programmes in low- and middle-income countries include fostering the political willpower, involvement of clinical leadership, or- ganizational commitment and creation of mandatory national guidelines for implementation of antimicrobial stew- ardship. Recently, the Indian National Medical Commission has made it man- datory for all medical colleges to have a functional antimicrobial stewardship committee.25 These developments are encouraging and, if implemented effec- tively, would be valuable for establishing antimicrobial stewardship as a perma- nent activity in medical colleges. The challenge will be to hold the attention of policy-makers and health administra- tors to prioritize antimicrobial steward- ship so that the resources necessary for its implementation are made available across the health-care systems. Our study has some limitations. First, we were not able to study the clini- cal and microbiological impact of the antimicrobial stewardship programme in any of these hospitals due to the short duration of the study and to the COVID-19 pandemic disrupting the implementation. Second, this study was focused on creating a basic framework for antimicrobial stewardship in hospi- tals and piloting a set of interventions that can be applied to Indian hospitals; we did not assess the quality of its imple- mentation. Finally, we were not able to document any change in prescription patterns (such as de-escalation rates) as per the AWaRe classification. We be- lieve that establishing an antimicrobial stewardship framework in any hospital is the first step towards the larger goal of rational antimicrobial prescribing. Despite these limitations, we believe that our study highlights the key steps which are needed to implement antimicrobial stewardship in low- and middle-income countries. In conclusion, most hospitals im- plemented antimicrobial stewardship programmes in their hospitals with the help of funding and capacity-building activities from the Indian Council of Medical Research. Administrative support and the availability of clinical pharmacists supported through hospital funds would be crucial for sustaining antimicrobial stewardship activity. Our study highlights the importance of developing the capacity of multi- disciplinary teams, identifying local problems and finding innovative local solutions. ■ Competing interests: None declared 摘要 印度医院抗菌药物管理 目的 旨在建立印度三级保健医院实施抗菌药物管理的 框架，并确定实施管理所面临的挑战和推动因素。 方法 在 2018 至 2021 年期间，印度医学研究理事会 采用系统方法建立了印度医院实施抗菌药物管理的框 架。我们选择了 20 家印度三级护理医院，对实施管 理计划的可行性进行研究。根据一项就干预前后情况 对指导医师开展的问卷调查，我们使用一组过程和结 果指标对进展进行了评估。在一项定性调查中，我们 确定了实施抗菌药物管理的推动因素和障碍。 结果 我们发现，在实施干预后医院各项抗菌药物管理 实施指标均有改善。所有 20 家医院均进行了月度文 化流行率分析，而仅有三家医院在实施干预之前开展 了该项分析。实施处方限制的医院数量从 2 家增加到 12 家，开始实施处方审核和反馈的医院数量从 6 家增 加到 16 家。15 家医院的受访者表示，他们愿意将抗 菌药物管理实施的覆盖面扩大到其他病房和重症监护 病房。6 家医院愿意招聘长期工作人员，负责抗菌药 物管理工作。 صخلم دنلها ،تايفشتسلما في تابوركيلما تاداضم لىع فاشرلإا تابوركيلما تاداضم لىع فاشرلإا ذيفنتل لمع راطإ عضو ضرغلا تايدحتلا ديدتحو ،ةيدنلها ةثلاثلا ةجردلا نم ةياعرلا تايفشتسم في .ذيفنتلا لىع ةدعاسلما لماوعلاو يدنلها سلجلما عبتا ،2021 لىإ 2018 نم ةترفلا للاخ ةقيرطلا فاشرلإا ذيفنتل لمع راطإ ءاشنلإ اًيجهنم اًبولسأ ةيبطلا ثاحبلأل 20 رايتخاب انمق .ةيدنلها تايفشتسلما في تابوركيلما تاداضم لىع جمانرب ذيفنت ىودج ةساردل ةثلاثلا ةجردلا نم ةياعر ىفشتسم لخدتلا لبق ينيسيئرلا ءابطلأل يأر علاطتسا لىع ًءانب .فاشرلإا ةيلمعلا تاشرؤم نم ةعوممج مادختساب مدقتلا مييقتب انمق ،هدعبو ذيفنت لىع ةدعاسلما لماوعلا ديدحتب انمق ،يعون حسم في .جئاتنلاو نود لوتح يتلا تاقوعلماو ،تابوركيلما تاداضم لىع فاشرلإا .فاشرلإا اذه ذيفنت فاشرلإا ذيفنتل ةفلتخلما تاشرؤـلما في اًنستح انظحلا جئاتنلا ترجأ .لخدتلا دعب تايفشتسلما في تابوركيلما تاداضم لىع تافاقثلل طاقنلا راشتنلا اًيرهش ًلايلتح 20 ـلا تايفشتسلما عيجم يتلا تايفشتسلما ددع داز .لخدتلا لبق تايفشتسم ةثلاثب ةنراقم ددع أدبو ،ىفشتسم 12 لىإ ينيفشتسم نم تابيكترلا دويق تأدب ةعجارلماو ةيبطلا تافصولا في قيقدتلا سراتم يتلا تايفشتسلما نع ىفشتسم 15 في نوكراشلما برعأ .ىفشتسم 16 لىإ ةتس نم ،تابوركيلما تاداضم لىع فاشرلإا ذيفنت ةيطغت عيسوت في مهتبغر ةتس تناك .ىرخلأا ةزكرلما ةيانعلا تادحوو ةحنجلأا لمشتل ةطشنلأ ينمزلالا ينمئادلا ينفظولما ينيعت في بغرت تايفشتسم .تابوركيلما تاداضم لىع فاشرلإا في تابوركيلما تاداضم لىع فاشرلإا ذيفنت نكمي جاتنتسلاا ،لوقعم حاجن زارحإ عم ةثلاثلا ةجردلا نم ةيدنلها تايفشتسلما ،ةبردلما ةلماعلا ىوقلا رفاوتو ،سيسؤلما معدلا دوجو لظ في ةقلعتلما ةيبيردتلاو ةيميلعتلا ةطشنلأا معد في تايفشتسلما ةبغرو .تابوركيلما تاداضم لىع فاشرلإاب 26 Bull World Health Organ 2023;101:20–27A| doi: http://dx.doi.org/10.2471/BLT.22.288797 Research Antimicrobial stewardship in Indian hospitals Sonam Vijay et al. 结论 在印度三级医院实施抗菌药物管理工作可取得一 定的成功，这取决于机构支持、可用的接受过培训的 人力资源以及医院支持与抗菌药物管理相关的教育和 培训活动的意愿。 Résumé Gestion des antimicrobiens en milieu hospitalier, Inde Objectif Établir un cadre pour la mise en œuvre d'une gestion des antimicrobiens dans les hôpitaux de soins tertiaires en Inde, et identifier les défis et les moteurs de cette mise en œuvre. Méthodes Durant la période comprise entre 2018 et 2021, le Conseil indien de la recherche médicale a adopté une approche systématique visant à instaurer un cadre pour assurer la gestion des antimicrobiens dans les hôpitaux indiens. Nous avons sélectionné 20 hôpitaux de soins tertiaires en Inde afin d'étudier la faisabilité du déploiement d'un tel programme. En nous fondant sur un questionnaire soumis aux médecins-chefs avant et après l'intervention, nous avons évalué les progrès au moyen d'une série d'indicateurs relatifs aux processus et aux résultats. Par le biais d'une enquête qualitative, nous avons déterminé quels étaient les obstacles et facteurs favorables à la mise en œuvre d'une gestion des antimicrobiens. Résultats Nous avons constaté une amélioration au niveau de plusieurs indicateurs de mise en œuvre dans les hôpitaux à l'issue de l'intervention. Les 20 établissements ont tous mené chaque mois une analyse de prévalence ponctuelle des cultures, alors qu'ils n'étaient que trois à le faire avant l'intervention. Le nombre d'hôpitaux ayant introduit une dispensation contrôlée est passé de deux à 12, et ils sont désormais 16 à vérifier et réguler les prescriptions, contre six auparavant. Dans 15 établissements, les participants ont exprimé leur volonté d'étendre ces pratiques à d'autres services et unités de soins intensifs. Enfin, six hôpitaux étaient prêts à recruter le personnel requis pour accomplir des tâches liées à la gestion des antimicrobiens. Conclusion La mise en œuvre de ce type de gestion peut rencontrer un certain succès dans les hôpitaux tertiaires en Inde. Ce succès dépend notamment de l'aide qu'apportent les institutions, de l'accès à une main-d'œuvre qualifiée et de la volonté des hôpitaux à soutenir les activités de formation et d'éducation à la gestion des antimicrobiens. Резюме Стратегия использования противомикробных средств на базе больниц, Индия Цель Создать основу для реализации стратегии использования противомикробных средств в больницах третьего звена в Индии, а также определить комплексы задач и факторы, способствующие ее реализации. Методы В течение 2018–2021 гг. Индийский совет по медицинским исследованиям придерживался системного подхода к созданию основы для реализации стратегии использования противомикробных средств в больницах Индии. Для изучения возможности реализации программы управления лекарственными средствами было выбрано 20 больниц Индии, относящихся к третьему звену. На основе опросника для ведущих врачей до вмешательства и после него была проведена оценка прогресса с помощью набора показателей процесса и результатов. В ходе качественного исследования авторы определили факторы, способствующие и препятствующие реализации стратегии использования противомикробных средств. Результаты Авторы отметили улучшение различных показателей реализации стратегии использования противомикробных средств в больницах после вмешательства. Во всех 20 больницах ежемесячно проводился точечный анализ распространенности культур по сравнению с показателями трех больниц до вмешательства. При этом количество больниц, которые начали вводить ограничения доступа к отдельным антибиотикам, увеличилось с двух до двенадцати, а количество больниц, которые начали практиковать аудит рецептов и обратную связь, увеличилось с шести до шестнадцати. Респонденты из 15 больниц выразили готовность расширить охват стратегии использования противомикробных средств на другие отделения и блоки интенсивной терапии. В шести больницах выразили готовность нанять постоянный персонал, необходимый для проведения мероприятий по использованию противомикробных средств. Вывод Стратегия использования противомикробных средств может быть достаточно успешно реализована в больницах третьего звена в Индии при условии оказания организационной поддержки, наличия подготовленных кадров и готовности больниц поддерживать образовательные и учебные мероприятия, связанные с применением противомикробных средств. Resumen Optimización del uso de antimicrobianos en los hospitales, India Objetivo Establecer un marco para la aplicación del programa de optimización del uso de antimicrobianos en los hospitales de atención especializada de la India, e identificar los desafíos y los factores que facilitan la aplicación. Métodos Entre 2018 y 2021, el Consejo Indio de Investigación Médica siguió un enfoque sistemático para establecer un marco que permitiera la aplicación de la optimización del uso de antimicrobianos en los hospitales de la India. Se seleccionaron 20 hospitales de atención especializada de la India para estudiar la viabilidad de implementar un programa de optimización de uso. A partir de un cuestionario dirigido a los médicos principales antes y después de la intervención, se evaluaron los avances mediante un conjunto de indicadores de procesos y desenlaces. En una encuesta cualitativa, se identificaron los factores que facilitan la optimización del uso de antimicrobianos y los obstáculos que la dificultan. Resultados Se encontró una mejora en varios indicadores de optimización del uso de antimicrobianos en los hospitales después de la intervención. Los 20 hospitales realizaron análisis mensuales de prevalencia puntual de cultivos, en comparación con tres hospitales antes de la intervención. La cantidad de hospitales que iniciaron restricciones en el formulario aumentó de dos a 12 hospitales y la cantidad de hospitales que comenzaron a practicar la auditoría de 27Bull World Health Organ 2023;101:20–27A| doi: http://dx.doi.org/10.2471/BLT.22.288797 Research Antimicrobial stewardship in Indian hospitalsSonam Vijay et al. prescripción y la retroalimentación aumentó de seis a 16 hospitales. Los encuestados de 15 hospitales expresaron su voluntad de ampliar la cobertura del programa de optimización del uso de antimicrobianos a otras salas y unidades de cuidados intensivos. Seis hospitales estaban dispuestos a contratar el personal permanente necesario para las actividades de optimización del uso de antimicrobianos. 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Bull World Health Organ 2023;101:20–27A| doi: http://dx.doi.org/10.2471/BLT.22.288797 27A Research Antimicrobial stewardship in Indian hospitalsSonam Vijay et al. Fig. 3. AWaRe classification of 14 168 antibiotic prescriptions in 13 Indian tertiary care hospitals, 2019–2021 Ho sp ita l 0 10 20 30 40 50 60 70 80 90 100 1 2 4 5 6 7 8 10 11 12 13 14 15 Access Watch Reserve % of antimicrobial prescriptions Note: The bars show the percentage of total antibiotics prescribed in each hospital, classified according to the World Health Organization Access, Watch, Reserve (AWaRe) groups.13