Open access peer-reviewed chapter
Abstract
Antimicrobials are very important for the treatment of patients. With decades of haphazard prescription and inappropriate use, antimicrobial resistance (AMR) has emerged as a global public health threat. In resource-limited settings, besides AMR, there is also the issue of access to antibiotics and increased healthcare costs. In the past, the discovery of new drugs and the modification of older ones helped to counter antimicrobial resistance. Since the 1970s, only a handful of new agents (a few of which are novel) have been introduced into clinical practice periodically. This makes the existing antibiotics to be a limited resource. Antibiotics must, therefore, be used more responsibly and managed carefully to extend their usefulness while being made available to the patients who truly need them. Antimicrobial stewardship (AMS) refers to systematic actions or interventions that inculcate sustainable, rational, and evidence-based antibiotic prescription and use patterns in healthcare institutions. Implementation of AMS programmes would be an appropriate step towards improving patient outcomes, reducing AMR and its adverse economic impact, and building the best-practices capacity of healthcare professionals, among others. Despite these seemingly beneficial benefits, the implementation of antimicrobial stewardship programmes (ASPs) remains relatively limited and faces complex challenges in resource-poor healthcare settings.
Keywords
- antimicrobial
- stewardship
- resource
- limited
- setting
1. Introduction
Today’s world is a product of continuous change driven by research, industry and innovation to address humanity’s greatest needs. The development of antimicrobials has been an ongoing process dating back to ancient civilisations that utilised plant extracts and mouldy bread to treat infections [1]. Alexander Fleming’s serendipitous discovery of penicillin in 1928 ushered in an era of growing interest in antimicrobial formulation and its ability to save millions of lives [1]. Since then, synthetic chemistry and modern drug discoveries have become the norm. However, the world faces an even more significant threat that may upend the progress made over the years: antimicrobial resistance [1, 2].
Scientists have striven to utilise research and innovation to combat emerging drug resistance and the evolving challenges of infectious diseases [2]. Antimicrobial resistance (AMR) is a primary global public health concern. It occurs when microorganisms develop the ability to evade the effects of antimicrobial medication, resulting in a reduction or loss of the medications’ effectiveness in treating infections [2]. The main drivers of AMR are the inappropriate use and overuse of antimicrobials, which can stem from factors such as poor infection control practices, inadequate surveillance systems, improper prescription practices, inadequate patient education, limited diagnostic facilities, unauthorised sale of antimicrobials, lack of appropriate functioning drug regulatory mechanisms, and non-human use of antimicrobials such as in animal production [2, 3]. The challenges posed by AMR require a comprehensive and coordinated approach to promote responsible antimicrobial use, develop new drugs, strengthen infection prevention and control practices, and enhance surveillance [3]. To this end, antimicrobial stewardship is a crucial strategy that aims to optimise the use of antimicrobial medicines while minimising the development of AMR. It involves a multidisciplinary approach that includes healthcare professionals, policymakers, and patients [4].
Addressing the global threat of resistant infections requires a concerted effort to tackle AMR and promote antimicrobial stewardship. Antimicrobial stewardship is the practice of optimising the use of antimicrobial drugs to combat the growing issue of antimicrobial resistance [4]. It is essential to ensure the responsible use of these drugs. However, resource-poor settings face unique challenges in implementing effective antimicrobial stewardship programmes due to limited resources, infrastructure, and funding [3]. These challenges include limited access to healthcare, inadequate diagnostic capabilities, scarcity of essential medicines, and difficulties in implementing infection prevention and control measures [5]. Innovative solutions and a commitment to ensuring access to essential medicines and healthcare services for all are necessary to address these challenges.
2. The significance of antimicrobial stewardship
Addressing antimicrobial stewardship in resource-poor settings is vital as it directly affects vulnerable populations, decreases the economic burden of inappropriate antimicrobial use, and controls the spread of antimicrobial resistance [5, 6, 7]. In this chapter, we will delve deeper into the topic, exploring the specific challenges faced by resource-poor settings and underscoring the importance of implementing effective antimicrobial stewardship programmes.
Antimicrobial stewardship programmes in resource-poor settings face several unique challenges that hamper their effectiveness. One of the critical challenges is the limited access to healthcare. In many low- and middle-income countries, most people live in rural areas with scarce healthcare facilities. This limited access to healthcare facilities makes it difficult for patients to receive proper diagnosis and treatment for infectious diseases, leading to the inappropriate use of antimicrobials and the development of resistance [5, 6, 7].
Another significant challenge is inadequate diagnostic capabilities. Diagnostic tests such as blood cultures, microbiological cultures, and susceptibility testing are essential for identifying the causative agent of an infection and determining the appropriate antimicrobial therapy [5, 6, 7]. However, many resource-poor settings lack the necessary diagnostic capabilities to perform these tests, leading to the widespread use of broad-spectrum antimicrobials and the development of resistance [5, 6, 7].
The scarcity of essential medicines is another challenge faced by resource-poor settings. Essential drugs, including antimicrobials, are often unavailable or in short supply in these settings due to a lack of funding, poor infrastructure, and limited supply chains [5, 6, 7]. This scarcity of essential medicines can lead to inappropriate antimicrobials, contributing to the development of resistance [5, 6, 7]. Implementing infection prevention and control measures significantly challenges antimicrobial stewardship in resource-poor settings [5, 6, 7]. Lack of basic amenities such as clean water, sanitation facilities, and waste management systems can rapidly spread infectious diseases, making it difficult to control outbreaks.
To overcome these challenges, effective antimicrobial stewardship programmes must be implemented in resource-poor settings. These programmes should focus on improving access to healthcare, strengthening diagnostic capabilities, ensuring the availability of essential medicines, and implementing infection prevention and control measures [8]. Improving access to healthcare can be accomplished by deploying community health workers who can provide critical diagnostic and treatment services to patients in rural areas [5]. Rapid diagnostic tests that do not require sophisticated laboratory facilities can also help improve diagnostic capabilities in resource-poor settings [7]. Ensuring the availability of essential medicines requires a coordinated effort between governments, international organisations, and the private sector [6]. This effort should focus on improving supply chain management, increasing funding for research and development of new antimicrobial drugs, and reducing the cost of existing medications [7]. Implementing infection prevention and control measures requires basic amenities such as clean water, sanitation facilities, and waste management systems. These amenities can be provided through public–private partnerships focusing on improving infrastructure in resource-poor settings [5].
To sum up, antimicrobial stewardship is crucial in addressing the global threat of antimicrobial resistance. Nonetheless, implementing effective antimicrobial stewardship programmes in resource-poor settings requires a comprehensive and coordinated effort to address these settings’ unique challenges. Improving access to healthcare, strengthening diagnostic capabilities, ensuring the availability of essential medicines, and implementing infection prevention and control measures are vital steps towards achieving this goal.
3. Understanding antimicrobial resistance in resource-poor settings
The issue of antimicrobial resistance (AMR) is a pressing global public health crisis with far-reaching implications for healthcare systems worldwide [9]. The emergence and spread of antimicrobial resistance significantly threaten our ability to treat infectious diseases effectively, increasing morbidity, mortality, and healthcare costs [10, 11]. The challenges in combating AMR are even more pronounced in resource-poor settings, characterised by poor resources, limited infrastructure, and scarce funding [10, 12, 13]. These settings face unique obstacles in addressing AMR, including limited access to healthcare, inadequate diagnostic capabilities, scarcity of essential medicines, and challenges in implementing infection prevention and control measures [10, 12, 13, 14]. These factors contribute to inappropriate use of antimicrobials, such as overprescribing, inadequate dosing, and misuse, leading to severe consequences, including treatment failures, increased morbidity and mortality, and disproportionate impacts on vulnerable populations [10, 12, 13, 14]. Addressing AMR in resource-poor settings is, therefore, mitigating the effects and preventing the further spread of resistance.
However, the challenges in addressing antimicrobial resistance in resource-poor settings are further compounded by the fragility of health systems. Fragile health systems, characterised by weak characteristics, limited resources, and inadequate governance, pose a significant barrier to effectively combating antimicrobial resistance [15]. The fragility of these health systems undermines efforts to address AMR and poses challenges in addressing other health priorities and achieving global health goals. Many resource-poor settings struggle with fragile health systems, further hampering their ability to address AMR [15, 16]. The World Health Organisation (WHO) has identified six building blocks of health systems: leadership and governance, health workforce, health information systems, access to essential medicines, financing, and service delivery [17]. Addressing these building blocks is critical for improving healthcare infrastructure, human resources, and laboratory capacity, which is necessary for managing antimicrobial resistance in these settings [17].
Therefore, comprehensive strategies should be implemented to improve access to healthcare, enhance diagnostic capabilities, ensure the availability of essential medicines, and strengthen infection prevention and control measures. Additionally, capacity building and education initiatives are vital to promote responsible antimicrobial use and raise awareness about the significance of AMR [9]. By addressing both the challenges in resource-poor settings and the fragility of health systems, we can contribute to safeguarding the effectiveness of antimicrobials, protecting vulnerable populations, and preserving the efficacy of these life-saving drugs for future generations.
4. Challenges and barriers to antimicrobial stewardship in resource-poor settings
The global healthcare context in resource-poor settings is often characterised by limited resources, infrastructure, and funding to adequately meet the population’s healthcare needs [15, 17]. This scenario poses unique challenges when it comes to addressing antimicrobial stewardship. Limited access to healthcare facilities and professionals, inadequate diagnostic capabilities, scarcity of essential medicines, and difficulties implementing infection prevention and control measures are some of the challenges faced in these settings [18].
The lack of reliable and timely diagnostic tools hampers accurate determination of the cause of infection and appropriate antimicrobial therapy selection [19]. Addressing antimicrobial stewardship in resource-poor settings is essential due to its impact on vulnerable populations, the economic burden of inappropriate antimicrobial use, and the potential for spreading antimicrobial resistance [16, 19]. Inadequate stewardship can result in treatment failures, increased morbidity and mortality, and disproportionately affect vulnerable populations. The emergence and spread of antimicrobial resistance are particularly concerning in resource-poor settings, where limited access to healthcare, inadequate diagnostics, and infection prevention and control challenges can contribute to its development [5, 19].
The limitations to antimicrobial stewardship in resource-poor settings can be attributed to several factors, including the lack of trained healthcare professionals and awareness, financial constraints, limited resources, and cultural and behavioural factors affecting antimicrobial use [16, 19]. The need for more trained healthcare professionals in resource-poor settings poses a significant challenge to implementing effective antimicrobial stewardship programmes. Financial constraints and limited resources also play a crucial role in inhibiting antimicrobial stewardship efforts.
Cultural beliefs, practices, and patient expectations may influence the demand for antimicrobials, leading to their inappropriate use [20]. For instance, in some cultures, antibiotics are considered a miracle cure, and their use is expected for any illness, regardless of whether bacteria or viruses cause it [20]. Additionally, limited health literacy and understanding of the risks of antimicrobial misuse among community members can perpetuate the problem. Therefore, addressing these factors is crucial in implementing effective antimicrobial stewardship programmes in resource-poor settings.
Several interventions can be implemented to ensure effective antimicrobial stewardship in resource-poor settings. Firstly, there is a need for increased investment in healthcare infrastructure, particularly in diagnostic capabilities and infection prevention and control measures [19]. This investment should be accompanied by appropriate training of healthcare workers on antimicrobial stewardship and infection control practices. Secondly, there is a need for increased awareness campaigns to educate the public on the proper use of antimicrobials and the risks associated with their misuse [14].
Thirdly, there is a need to develop guidelines and protocols for the appropriate use of antimicrobials in resource-poor settings. Such policies should be context-specific, considering the unique challenges faced in resource-poor settings [5, 19]. Fourthly, there is a need for increased surveillance of antimicrobial use and resistance patterns to guide the development and implementation of effective stewardship programmes [18, 21].
In conclusion, antimicrobial stewardship in resource-poor settings is crucial to prevent the emergence and spread of antimicrobial resistance and ensure the appropriate use of antimicrobials. Addressing the challenges these settings face requires a multi-pronged approach that involves increased investment in healthcare infrastructure, proper training of healthcare workers, increased public awareness campaigns, and developing context-specific guidelines and protocols. These interventions will go a long way in ensuring effective antimicrobial stewardship in resource-poor settings.
5. Strategies for implementing antimicrobial stewardship in resource-poor settings
Antimicrobial stewardship programmes (ASPs) are crucial in promoting responsible antimicrobial use and combating AMR. However, implementing effective ASPs in resource-poor settings is challenging due to the need for more resources and infrastructure. To address these challenges, multiple aspects of healthcare delivery must be addressed. Building local capacity and training healthcare professionals is crucial [22, 23, 24]. This means providing education and training on antimicrobial stewardship principles, appropriate use, and infection prevention and control measures [25]. It is also essential to strengthen healthcare infrastructure, including improving access to diagnostics such as laboratory facilities and point-of-care tests [5, 26, 27]. This enables accurate diagnosis of infections and facilitates appropriate antimicrobial prescribing. Developing guidelines and protocols for antimicrobial use tailored to the specific context of resource-poor settings helps standardise practices and promote responsible prescribing [4, 25, 26].
ASPs also require a cultural shift in the healthcare system. Promoting rational prescribing practices and patient education is crucial in shifting cultural and behavioural factors contributing to antimicrobial misuse [20]. Public awareness campaigns and educating patients about the risks of inappropriate antimicrobial use and the importance of completing prescribed treatments are vital strategies [23]. Engaging stakeholders, including healthcare professionals, policymakers, and community leaders, fosters collaboration and creates a supportive environment for implementing ASPs [28, 29, 30]. Experts in the field have identified nine key strategies to enhance antimicrobial stewardship (AMS) [28]. These include implementing quality improvement measures, promoting peer learning across different disciplines, assigning AMS leads, carrying out individual-level prescribing audits, creating practical tools for prescribing audits, improving induction processes for new prescribers, standardising local approaches to antibiotic prescribing, providing online AMS training to all patient-facing staff, and increasing staff time devoted to AMS work through the standardisation of AMS-related roles [28].
Implementing ASPs in resource-poor settings is challenging and requires a comprehensive and coordinated approach. Developing national action plans and policies can provide a framework for implementing ASPs and ensuring sustainability [31, 32]. Additionally, funding and technical support from international organisations and donor agencies can provide critical resources to support ASP implementation [25, 33, 34].
In conclusion, addressing AMR in resource-poor settings requires a comprehensive approach that includes strengthening healthcare infrastructure, improving access to essential medicines, enhancing diagnostic capabilities, and implementing effective infection prevention and control measures. Capacity building and education for healthcare professionals and the community are vital in promoting responsible antimicrobial use. Promoting rational prescribing practices and patient education is crucial in shifting cultural and behavioural factors contributing to antimicrobial misuse. Engaging stakeholders and developing national action plans and policies can provide a framework for implementing ASPs and ensuring sustainability [31, 32]. Like the National Action Plan for AMR developed in India [35]. In 2019, a framework for addressing AMR was designed to be an ongoing and adaptable process that responds to contextual factors, allowing for continuous improvement and refinement of national action plans [36]. This was to address the need for a systematic approach to the governance of national plans [36]. By systematically addressing these strategies, resource-poor settings can enhance their ability to combat antimicrobial resistance and improve patient outcomes.
6. Lessons from case studies
The successful implementation of antimicrobial stewardship programmes in resource-poor settings has been the subject of various studies. These studies have demonstrated the potential for positive outcomes, such as significantly reducing inappropriate antimicrobial prescribing and improving guideline adherence [26, 35]. The key to success lies in tailored training and education programmes considering resource-poor settings’ specific contexts and challenges [26]. Additionally, developing and implementing evidence-based local guidelines and protocols can considerably reduce the prevalence of antimicrobial resistance and improve patient outcomes. Continuous monitoring and feedback to healthcare professionals also play a vital role in ensuring responsible antimicrobial use [18, 21]. These successful initiatives challenge the notion that limited resources are insurmountable barriers to implementing effective antimicrobial stewardship programmes in resource-poor settings.
Numerous studies have explored the implementation of antimicrobial stewardship programmes in resource-poor settings, revealing their potential to reduce inappropriate antimicrobial prescribing and improve adherence to guidelines. The key to success lies in tailored training and education programmes that address the unique challenges of such settings [15, 22, 23, 31]. Evidence-based local procedures and protocols are crucial in tackling antimicrobial resistance and enhancing patient outcomes.
Despite limited resources, establishing active antimicrobial stewardship programmes in resource-poor settings is achievable through a collaborative approach involving healthcare professionals, policymakers, and the community [30]. It is essential to provide tailored training and education programmes that cater to the specific challenges faced by healthcare professionals [30]. Developing and implementing context-specific guidelines and protocols based on evidence can considerably reduce antimicrobial resistance and improve patient outcomes [20]. Regular monitoring and feedback to healthcare professionals are critical for responsible antimicrobial use.
The successful implementation of antimicrobial stewardship programmes in resource-poor settings challenges the notion that limited resources are insurmountable barriers. By adopting an evidence-based, context-specific approach, healthcare professionals and policymakers can effectively address the issue of antimicrobial resistance in such settings.
7. Overcoming challenges and sustainability of antimicrobial stewardship programmes
Antimicrobial resistance (AMR) is a pressing global health issue that threatens the effective prevention and treatment of infections caused by bacteria, viruses, fungi, and parasites [9]. The misuse and overuse of antimicrobial agents, poor infection prevention and control practices, and inadequate access to clean water, sanitation, and hygiene are major drivers of AMR. Resource-poor settings, where access to healthcare and essential medicines is limited, are particularly vulnerable to the negative impact of AMR. Antimicrobial stewardship programmes (ASPs) are crucial interventions to address AMR and promote the rational use of antimicrobial agents [31]. However, the implementation and sustainability of ASPs in resource-poor settings face several challenges that must be addressed [31]. Financial constraints and limited resources are significant obstacles to implementing and sustaining ASPs in resource-poor settings. External funding from international organisations, donor organisations, and philanthropic foundations can help overcome these constraints [33, 34]. Advocating for increased healthcare budgets and prioritising allocating ASPs can also contribute to addressing and identifying innovative approaches for funding, resource mobilisation and partnerships, which can provide additional resources and expertise [37].
Partnerships with organisations, institutions, and pharmaceutical companies can also provide access to expertise, resources, and funding. Collaborating with local communities and engaging community leaders can promote sustainability by fostering ownership and support for ASPs [30]. Engaging patients and their families in antimicrobial stewardship efforts can also increase awareness and guideline adherence [23]. Integrating ASPs into existing healthcare systems is crucial for long-term sustainability [17, 24, 38]. This can be achieved by incorporating antimicrobial stewardship principles and training into medical and nursing curricula and establishing dedicated antimicrobial stewardship teams or committees within healthcare facilities [24]. Collaboration between healthcare professionals, policymakers, and regulators is essential to develop and enforce antimicrobial prescribing guidelines and policies that align with national and international recommendations [38]. Furthermore, leveraging existing healthcare infrastructure and systems, such as electronic medical records and surveillance systems, can facilitate monitoring and evaluating antimicrobial use and resistance patterns [21].
Ensuring the long-term sustainability and scalability of ASPs is a critical consideration. This can be achieved by establishing monitoring and evaluation mechanisms to assess the programmes’ impact and identify areas for improvement [38]. Continuous education and training of healthcare professionals on antimicrobial stewardship principles and practices is essential to maintain awareness and adherence to guidelines [24]. Fostering a culture of accountability and responsibility among healthcare professionals and the community is crucial for sustaining the momentum of ASPs. Engaging stakeholders, including policymakers, healthcare professionals, patients, and community members, in discussions and decision-making processes can contribute to the sustainability and scalability of ASPs [27].
Finally, implementing and sustaining ASPs in resource-poor settings requires addressing frequent constraints, forming partnerships, integrating stewardship into existing healthcare systems, and focusing on long-term scalability. When implemented in a coordinated and comprehensive manner, these strategies can contribute to the successful implementation and long-term impact of antimicrobial stewardship initiatives in resource-poor settings.
8. Future directions and recommendations
The field of antimicrobial stewardship in resource-poor settings presents several areas for further exploration. To ensure the sustained effectiveness and sustainability of antimicrobial stewardship programmes, research should investigate the long-term impact of such programmes on antimicrobial resistance patterns, patient outcomes, and healthcare costs [39]. Additionally, evaluating the effectiveness of different strategies and interventions used in antimicrobial stewardship programmes, including education and training programmes, guidelines and protocols, and electronic decision support systems, is essential [39, 40]. Understanding the social and behavioural factors influencing antimicrobial use in these settings is also crucial. Policymakers should prioritise developing and implementing national antimicrobial stewardship policies and guidelines and advocate for increased funding and resources to support programme implementation and sustainability [31, 32, 35, 36]. Global collaboration and knowledge sharing can also advance antimicrobial stewardship efforts in resource-poor settings. By addressing these areas, resource-poor locations can strengthen their antimicrobial stewardship programmes and contribute to the global fight against antimicrobial resistance.
Antimicrobial resistance (AMR) is a growing concern globally, and it is especially significant in resource-poor settings. In these locations, the prevalence of infectious diseases is high, and antibiotics are often the primary treatment option. Unfortunately, the misuse and overuse of antibiotics have led to the emergence of resistant strains of bacteria, making infections difficult to treat [6]. The World Health Organisation (WHO) has recognised the importance of antimicrobial stewardship programmes, which aim to reduce the inappropriate use of antibiotics, improve prescribing practices, and optimise patient outcomes.
One area that requires further exploration is the long-term impact of antimicrobial stewardship programmes on antimicrobial resistance patterns, patient outcomes, and healthcare costs [40, 41]. While it is clear that such programmes can reduce the development of antimicrobial resistance, the long-term effects still need to be better understood. Research should investigate the impact of stewardship programmes over extended periods to determine their sustained effectiveness and sustainability. This information can help policymakers and healthcare providers make informed decisions about resource allocation and programme implementation.
Another critical area for exploration is the evaluation of the effectiveness of different strategies and interventions used in antimicrobial stewardship programmes [42]. These may include education and training programmes, guidelines and protocols, and electronic decision support systems [42, 43]. By evaluating these strategies, healthcare providers can identify the most effective ways to reduce inappropriate antibiotic use and improve patient outcomes. This information can help providers tailor their programmes to the unique needs of their patients and communities.
Understanding the social and behavioural factors influencing antimicrobial use in resource-poor settings is also crucial [44]. While healthcare providers can significantly reduce inappropriate antibiotic use, patients and their families also have a role to play. Cultural beliefs, practices, and limited access to healthcare facilities and diagnostics can contribute to inappropriate antibiotic use [43]. By understanding these factors, healthcare providers can develop targeted interventions to address them.
In conclusion, the importance of antimicrobial stewardship in addressing the global challenge of AMR cannot be overstated. In resource-poor settings, the challenges of implementing effective stewardship programmes are significant but manageable. By addressing research, evaluation, social and behavioural factors, policymaking, and collaboration, resource-poor locations can strengthen their antimicrobial stewardship programmes and contribute to the global fight against AMR. The health of populations in resource-poor settings, as well as future generations, depends on collective action by policymakers, healthcare providers, and researchers to develop and implement effective antimicrobial stewardship programmes.
References
- 1.
Rahman M, Sarker SD. Antimicrobial natural products. In: Annual Reports in Medicinal Chemistry. United States: Elsevier; 2020. pp. 77-113 - 2.
Dyary HO, Faraj GJ, Saeed NM. History, Current Situation, and Future Perspectives on Antibiotics and Antibiotic Resistance. One Heal Triad. Vol. 2. Faisalabad, Pakistan: Unique Scientific Publisher; 2023. pp. 109-118 - 3.
Ayukekbong JA, Ntemgwa M, Atabe AN. The threat of antimicrobial resistance in developing countries: Causes and control strategies. Antimicrobial Resistance and Infection Control. 2017; 6 (1):1-8 - 4.
Fishman N. Antimicrobial stewardship. American Journal of Infection Control. 2006; 34 (5):S55-S63 - 5.
Kakkar AK, Shafiq N, Singh G, Ray P, Gautam V, Agarwal R, et al. Antimicrobial stewardship programs in resource-constrained environments: Understanding and addressing the need of the systems. Frontiers in Public Health. 2020; 8 :140 - 6.
Cox JA, Vlieghe E, Mendelson M, Wertheim H, Ndegwa L, Villegas MV, et al. Antibiotic stewardship in low-and middle-income countries: The same but different? Clinical Microbiology and Infection. 2017; 23 (11):812-818 - 7.
Hijazi K, Joshi C, Gould IM. Challenges and opportunities for antimicrobial stewardship in resource-rich and resource-limited countries. Expert Review of Anti-Infective Therapy. 2019; 17 (8):621-634 - 8.
Caron WP, Mousa SA. Prevention strategies for antimicrobial resistance: A systematic review of the literature. Infection and Drug Resistance. 2010; 3 :25-33 - 9.
Ferri M, Ranucci E, Romagnoli P, Giaccone V. Antimicrobial resistance: A global emerging threat to public health systems. Critical Reviews in Food Science and Nutrition. 2017; 57 (13):2857-2876 - 10.
Roope LSJ, Smith RD, Pouwels KB, Buchanan J, Abel L, Eibich P, et al. The challenge of antimicrobial resistance: What economics can contribute. Science (80-). 2019; 364 (6435):eaau4679 - 11.
Cars O, Nordberg P. Antibiotic resistance–the faceless threat. The International Journal of Risk & Safety in Medicine. 2005; 17 (3-4):103-110 - 12.
Tenover FC. Mechanisms of antimicrobial resistance in bacteria. The American Journal of Medicine. 2006; 119 (6):S3-S10 - 13.
Cosgrove SE. The relationship between antimicrobial resistance and patient outcomes: Mortality, length of hospital stay, and health care costs. Clinical Infectious Diseases. 2006; 42 (Supplement_2):S82-S89 - 14.
DiazGranados CA, Cardo DM, McGowan JE Jr. Antimicrobial resistance: International control strategies, with a focus on limited-resource settings. International Journal of Antimicrobial Agents. 2008; 32 (1):1-9 - 15.
Akilimali A, Awuah WA, Cakwira H, Mirindi MK, Masimango G, Amani T, et al. Antimicrobial resistance in Democratic Republic of Congo: The way forward. In: IJS Global Health. Vol. 6. Netherlands: Wolters Kluwer; 2023. p. e0150 - 16.
MacPherson EE, Reynolds J, Sanudi E, Nkaombe A, Phiri C, Mankhomwa J, et al. Understanding antimicrobial resistance through the lens of antibiotic vulnerabilities in primary health care in rural Malawi. Global Public Health. 2022; 17 (11):2630-2646 - 17.
World Health Organization (WHO). Monitoring the Building Blocks of Health Systems: A Handbook of Indicators and their Measurement Strategies [Internet]. Geneva, Switzerland: World Health Organization; 2010. Available from: https://www.google.com/url?sa=t&rct=j&q=&esrc=s&source=web&cd=&cad=rja&uact=8&ved=2ahUKEwij6Ifn59SAAxXgV0EAHRi8AcEQFnoECCUQAQ&url=https%3A%2F%2Fapps.who.int%2Firis%2Fbitstream%2Fhandle%2F10665%2F258734%2F9789241564052-eng.pdf&usg=AOvVaw1VUvLpCAGxolA87_WiE - 18.
Iskandar K, Molinier L, Hallit S, Sartelli M, Hardcastle TC, Haque M, et al. Surveillance of antimicrobial resistance in low and middle-income countries: A scattered picture. Antimicrobial Resistance and Infection Control. 2021; 10 (1):1-19 - 19.
Gebretekle GB, Haile Mariam D, Abebe W, Amogne W, Tenna A, Fenta TG, et al. Opportunities and barriers to implementing antibiotic stewardship in low and middle-income countries: Lessons from a mixed-methods study in a tertiary care hospital in Ethiopia. PLoS One. 2018; 13 (12):e0208447 - 20.
Charani E, Smith I, Skodvin B, Perozziello A, Lucet JC, Lescure FX, et al. Investigating the cultural and contextual determinants of antimicrobial stewardship programmes across low-, middle-and high-income countries—A qualitative study. PLoS One. 2019; 14 (1):e0209847 - 21.
Simonsen GS, Tapsall JW, Allegranzi B, Talbot EA, Lazzari S. The antimicrobial resistance containment and surveillance approach-a public health tool. Bulletin of the World Health Organization. 2004; 82 (12):928-934 - 22.
Prentiss T, Weisberg K, Zervos J. Building capacity in infection prevention and antimicrobial stewardship in low-and middle-income countries: The role of partnerships inter-countries. Current Treatment Options in Infectious Diseases. 2018; 10 :7-16 - 23.
Virhia J, Gilmour M, Russell C, Mutua E, Nasuwa F, Mmbaga BT, et al. If you do not take the medicine and complete the dose… it could cause you more trouble: Bringing awareness, local knowledge and experience into antimicrobial stewardship in Tanzania. Antibiotics. 2023; 12 (2):243 - 24.
World Health Organization. Health Workers’ Education and Training on Antimicrobial Resistance: Curricula Guide. Geneva, Switzerland: WHO; 2019 - 25.
Majumder MAA, Rahman S, Cohall D, Bharatha A, Singh K, Haque M, et al. Antimicrobial stewardship: Fighting antimicrobial resistance and protecting global public health. Infection and Drug Resistance. 2020; 13 :4713-4738 - 26.
Rolfe R, Kwobah C, Muro F, Ruwanpathirana A, Lyamuya F, Bodinayake C, et al. Barriers to implementing antimicrobial stewardship programs in three low-and middle-income country tertiary care settings: Findings from a multi-site qualitative study. Antimicrobial Resistance and Infection Control. 2021; 10 :1-11 - 27.
World Health Organization. Diagnostic Stewardship: A Guide to Implementation in Antimicrobial Resistance Surveillance Sites. Geneva, Switzerland: World Health Organization; 2016 - 28.
Borek AJ, Wanat M, Sallis A, Ashiru-Oredope D, Atkins L, Beech E, et al. How can national antimicrobial stewardship interventions in primary care be improved? A stakeholder consultation. Antibiotics. 2019; 8 (4):207 - 29.
Wathne JS, Kleppe LKS, Harthug S, Blix HS, Nilsen RM, Charani E, et al. The effect of antibiotic stewardship interventions with stakeholder involvement in hospital settings: A multicentre, cluster randomized controlled intervention study. Antimicrobial Resistance and Infection Control. 2018; 7 :1-12 - 30.
Logan AY, Williamson JE, Reinke EK, Jarrett SW, Boger MS, Davidson LE. Establishing an antimicrobial stewardship collaborative across a large, diverse health care system. Joint Commission Journal on Quality and Patient Safety. 2019; 45 (9):591-599 - 31.
Frumence G, Mboera LEG, Sindato C, Katale BZ, Kimera S, Metta E, et al. The governance and implementation of the National Action Plan on antimicrobial resistance in Tanzania: A qualitative study. Antibiotics. 2021; 10 (3):273 - 32.
Charani E, Mendelson M, Pallett SJC, Ahmad R, Mpundu M, Mbamalu O, et al. An analysis of existing national action plans for antimicrobial resistance—Gaps and opportunities in strategies optimising antibiotic use in human populations. The Lancet Global Health. 2023; 11 (3):e466-e474 - 33.
Wernli D, Harbarth S, Levrat N, Pittet D. A ‘whole of United Nations approach’ to tackle antimicrobial resistance? A mapping of the mandate and activities of international organisations. BMJ Global Health. 2022; 7 (5):e008181 - 34.
Tattevin P, Levy Hara G, Toumi A, Enani M, Coombs G, Voss A, et al. Advocacy for increased international efforts for antimicrobial stewardship actions in low-and middle-income countries on behalf of alliance for the prudent use of antimicrobials (APUA), under the auspices of the International Society of Antimicrobial Chemotherapy (ISAC). Frontiers in Medicine. 2020; 7 :503 - 35.
Ranjalkar J, Chandy SJ. India’s National Action Plan for antimicrobial resistance–an overview of the context, status, and way ahead. Journal of Family Medicine and Primary Care. 2019; 8 (6):1828 - 36.
Anderson M, Schulze K, Cassini A, Plachouras D, Mossialos E. A governance framework for development and assessment of national action plans on antimicrobial resistance. The Lancet Infectious Diseases. 2019; 19 (11):e371-e384 - 37.
Uzochukwu BSC, Ughasoro MD, Etiaba E, Okwuosa C, Envuladu E, Onwujekwe OE. Health care financing in Nigeria: Implications for achieving universal health coverage. Nigerian Journal of Clinical Practice. 2015; 18 (4):437-444 - 38.
World Health Organization. Antimicrobial Stewardship Interventions: A Practical Guide. Geneva, Switzerland: World Health Organization; 2021 - 39.
Saubolle MA. Antimicrobial resistance: Current status and future direction. American Journal of Rhinology. 2006; 20 (6):667-671 - 40.
Engler D, Meyer JC, Schellack N, Kurdi A, Godman B. Antimicrobial stewardship activities in public healthcare facilities in South Africa: A baseline for future direction. Antibiotics. 2021; 10 (8):996 - 41.
Newland JG, Banerjee R, Gerber JS, Hersh AL, Steinke L, Weissman SJ. Antimicrobial stewardship in pediatric care: Strategies and future directions. Pharmacotherapy: The Journal of Human Pharmacology and Drug Therapy. 2012; 32 (8):735-743 - 42.
Same RG. The current state and future directions of inpatient pediatric antimicrobial stewardship. Infectious Disease Clinics. 2022; 36 (1):173-186 - 43.
Briggs DC, Oboro IL, Bob-Manuel M, Amadi SC, Enyinnaya SO, Lawson SD, et al. Antibiotic prescription patterns in paediatric wards of Rivers state university teaching hospital, southern Nigeria: A point prevalence survey. The Nigerian Health Journal. 2023; 23 (3):837-843 - 44.
Bassetti M, Giacobbe DR, Vena A, Brink A. Challenges and research priorities to progress the impact of antimicrobial stewardship. Drugs Context. 2019; 8 :212600