READ-ing antimicrobial stewardship in the Caribbean: a tri-nation document review

El método READ y la administración de antimicrobianos en el Caribe: una revisión trinacional de documentos

Uso racional de antibióticos no Caribe com base na abordagem READ: revisão de documentos de três países

Tamarie Rocke Aniebiot-abasi Udofia Nathalie El Omeiri Pilar Ramon-Pardo About the authors

ABSTRACT

Objective.

To explore the antimicrobial stewardship policy landscape in three English-speaking Caribbean countries (Barbados, Guyana, and Saint Lucia) and examine the key enablers and challenges to the design and implementation of formal antimicrobial stewardship programs.

Methods.

A document analysis that searched for existing policy, communications, and contributions on antimicrobial stewardship from these three countries, adapting the READ (Ready materials; Extract data; Analyze data; Distill findings) approach, a systematic procedure for health policy document review.

Results.

The search strategy identified 726 initial records. Of those, 15 (2%) met the inclusion criteria. The analysis included official policy documents (n = 3), scholarly works/reviews (n = 3), advocacy documents (n = 2), news articles (n = 4), and confidential reports (n = 3) from the three countries.

Conclusions.

Critical matters such as cross-programmatic coordination, the significance of individual action, and the need for bidirectional knowledge discourse are prominent in optimizing antimicrobial stewardship adaptation in these countries. CARICOM regional coordination has positively impacted the integration of infection prevention and control with antimicrobial stewardship across this knowledge network.

Keywords
Review; antimicrobial stewardship; drug resistance, microbial; Caribbean region

RESUMEN

Objetivo.

Explorar el panorama de las políticas de optimización del uso de antimicrobianos en tres países caribeños de habla inglesa (Barbados, Guyana y Santa Lucía) y examinar los principales facilitadores y desafíos para elaborar y aplicar programas formales de optimización del uso de antimicrobianos.

Métodos.

Se adaptó el método READ (acrónimo en inglés de "materiales listos; extraer los datos; analizar los datos; destilar los resultados"), un procedimiento sistemático para la revisión de documentos sobre políticas de salud, a fin de realizar un análisis de documentos que buscó las políticas, comunicaciones y contribuciones existentes sobre la optimización del uso de antimicrobianos en esos tres países.

Resultados.

La estrategia de búsqueda permitió localizar 726 documentos iniciales. De ellos, 15 (el 2%) cumplían los criterios de inclusión. El análisis abarcó documentos oficiales de políticas (n = 3), trabajos académicos o revisiones (n = 3), documentos de promoción de la causa (n = 2), artículos de noticias (n = 4) e informes confidenciales (n = 3) de los tres países.

Conclusiones.

Varios aspectos críticos, como la coordinación interprogramática, la importancia de la acción individual y la necesidad de una comunicación bidireccional del conocimiento, son preponderantes para adaptar de la mejor manera la optimización del uso de antimicrobianos en estos países. La coordinación regional de la CARICOM ha influido positivamente para integrar la prevención y el control de infecciones con la optimización del uso de antimicrobianos en toda esta red de conocimientos.

Palabras clave
Revisión; programas de optimización del uso de los antimicrobianos; farmacorresistencia microbiana; región del Caribe

RESUMO

Objetivo.

Explorar o cenário da política para uso racional de antibióticos em três países anglófonos do Caribe (Barbados, Guiana e Santa Lúcia) e examinar os principais fatores facilitadores e desafios para a elaboração e implementação de programas formais de uso racional de antibióticos.

Métodos.

Análise de documentos em busca de políticas, comunicações e contribuições existentes sobre o uso racional de antibióticos nesses três países, adaptando a abordagem READ (sigla em inglês para preparar materiais, extrair e analisar dados e destacar os principais achados), um procedimento sistemático para a revisão de documentos de políticas de saúde.

Resultados.

A estratégia de busca identificou 726 registros iniciais. Desses, 15 (2%) atenderam aos critérios de inclusão. A análise incluiu documentos oficiais de políticas (n = 3), trabalhos acadêmicos/revisões (n = 3), documentos em defesa da causa (n = 2), reportagens (n = 4) e relatórios confidenciais (n = 3) dos três países.

Conclusões.

Questões críticas, como a coordenação interprogramática, a importância da ação individual e a necessidade de um discurso bidirecional de conhecimento, se destacam na adaptação otimizada das diretrizes de uso racional de antibióticos nesses países. A coordenação regional da Comunidade do Caribe (CARICOM) contribuiu para integrar a prevenção e o controle de infecções ao uso racional de antibióticos em toda essa rede de conhecimento.

Palavras-chave
Revisão; gestão de antimicrobianos; resistência microbiana a medicamentos; região do Caribe

Antimicrobial resistance (AMR) is the ability of microorganisms to resist the effects of antibiotics adaptively. It is a leading cause of death globally, especially in low- and middle-income countries and the most vulnerable populations (11. Antimicrobial Resistance Collaborators. Global burden of bacterial antimicrobial resistance in 2019: a systematic analysis. Lancet. 2022;399(10325):629–55. https://doi.org/10.1016/s0140-6736(21)02724-0.
https://doi.org/10.1016/s0140-6736(21)02...
, 22. World Health Organization. The evolving threat of antimicrobial resistance: options for action. Geneva: WHO; 2012 [cited 2022 Nov 11]. Available from: https://apps.who.int/iris/handle/10665/44812.
https://apps.who.int/iris/handle/10665/4...
). The rapidly growing mortality rate associated with AMR is considered one of the top ten threats to humanity. Researchers estimated bacterial AMR-associated mortality in 2019 to be 4.95 million worldwide, with direct mortality reported as 1.27 million (11. Antimicrobial Resistance Collaborators. Global burden of bacterial antimicrobial resistance in 2019: a systematic analysis. Lancet. 2022;399(10325):629–55. https://doi.org/10.1016/s0140-6736(21)02724-0.
https://doi.org/10.1016/s0140-6736(21)02...
). These numbers far exceed estimates by O’Neill et al. in 2014, who projected 700 000 deaths per year (33. Review on Antimicrobial Resistance. Antimicrobial Resistance: Tackling a crisis for the health and wealth of nations. London: [Review on AMR]; 2014. Available from: https://amr-review.org/Publications.html.
https://amr-review.org/Publications.html...
). Alarmingly, their predicted estimate of 10 million deaths attributable to AMR per year in 2050 steadily approaches reality despite interventions (33. Review on Antimicrobial Resistance. Antimicrobial Resistance: Tackling a crisis for the health and wealth of nations. London: [Review on AMR]; 2014. Available from: https://amr-review.org/Publications.html.
https://amr-review.org/Publications.html...
). In the Caribbean, expanding AMR surveillance has confirmed that there is regional spread of diverse and highly virulent pathogens resistant to commonly used antibiotics (44. Dozois A, Thomsen I, Jimenez-Truque N, Soper N, Pearson A, Mohamed-Rambaran P, et al. Prevalence and molecular characteristics of methicillin-resistant Staphylococcus aureus among skin and soft tissue infections in an emergency department in Guyana. Emerg Med J. 2015 Oct;32(10):800–3. https://doi.org/10.1136/emermed-2013-203373.
https://doi.org/10.1136/emermed-2013-203...
). Meanwhile, the rate of development of new medications to tackle this upsurge is insufficient (55. World Health Organization [Internet]. Geneva: WHO; 2021 Nov 17. Antimicrobial resistance. Available from: https://www.who.int/news-room/fact-sheets/detail/antimicrobial-resistance.
https://www.who.int/news-room/fact-sheet...
).

AMR burden is not just reflected in the number of deaths; its pernicious impact on patient morbidity and the overall socioeconomic landscape is expanding (11. Antimicrobial Resistance Collaborators. Global burden of bacterial antimicrobial resistance in 2019: a systematic analysis. Lancet. 2022;399(10325):629–55. https://doi.org/10.1016/s0140-6736(21)02724-0.
https://doi.org/10.1016/s0140-6736(21)02...
, 22. World Health Organization. The evolving threat of antimicrobial resistance: options for action. Geneva: WHO; 2012 [cited 2022 Nov 11]. Available from: https://apps.who.int/iris/handle/10665/44812.
https://apps.who.int/iris/handle/10665/4...
). Therefore, without deliberate, coordinated, and targeted interventions, poorer outcomes are expected in not only human but also animal and environmental health sectors (66. World Health Organization. Global Action Plan on Antimicrobial Resistance. Geneva: WHO; 2015. Available from: https://apps.who.int/iris/handle/10665/193736.
https://apps.who.int/iris/handle/10665/1...
).

Antimicrobial stewardship programs (ASP) are an effective organizational tool integral to healthcare systems that monitor and improve antibiotic use, thereby prolonging the effectiveness and relevance of these medicines (77. World Health Organization. Antimicrobial stewardship programmes in health-care facilities in low- and middle-income countries: a WHO practical toolkit. 1st edition. Geneva: WHO; 2019. Available from: https://apps.who.int/iris/handle/10665/329404.
https://apps.who.int/iris/handle/10665/3...
). The core principle of antimicrobial stewardship (AMS) is to demonstrate a solid commitment to the judicious use of antimicrobials by creating policies and evidence-based guidelines that control antibiotic prescribing and improve antibiotic selection (88. Majumder MAA, Rahman S, Cohall D, Bharatha A, Singh K, Haque M, et al. Antimicrobial Stewardship: Fighting Antimicrobial Resistance and Protecting Global Public Health. Infect Drug Resist. 2020;13:4713–38. https://doi.org/10.2147/IDR.S290835.
https://doi.org/10.2147/IDR.S290835...
). In human health, by educating both clinical staff and patients on the proper use of antimicrobials and collaborating with other sectors to analogously promote AMS, health systems may impact the overprescription of antibiotics and minimize the emergence and spread of AMR (99. Septimus EJ, Owens RC Jr. Need and Potential of Antimicrobial Stewardship in Community Hospitals. Clin Infect Dis. 2011;53(Suppl 1):S8–S14. https://doi.org/10.1093/cid/cir363.
https://doi.org/10.1093/cid/cir363...
).

There is, however, a need to demonstrate a causal relationship between public health programs such as ASPs and health outcomes in health systems research to identify pathways to successful program implementation and progression (1010. Dalglish SL, Khalid H, McMahon SA. Document analysis in health policy research: the READ approach. Health Policy Plan. 2020;35(10):1424–31. https://doi.org/10.1093/heapol/czaa064.
https://doi.org/10.1093/heapol/czaa064...
). The World Health Organization (WHO) Practical Toolkit recommends that, before developing an action plan for AMS, a situation analysis should be carried out to ensure facilities build on existing infrastructure in ASP design (77. World Health Organization. Antimicrobial stewardship programmes in health-care facilities in low- and middle-income countries: a WHO practical toolkit. 1st edition. Geneva: WHO; 2019. Available from: https://apps.who.int/iris/handle/10665/329404.
https://apps.who.int/iris/handle/10665/3...
). Situation analysis marries a range of research methods, including using standardized tools to obtain a baseline policy assessment and underline existing opportunities (1111. Martin W, Pauly B, MacDonald M. Situational Analysis for Complex Systems: Methodological Development in Public Health Research. AIMS Public Health. 2016;3(1):94–109. https://doi.org/10.3934/publichealth.2016.1.94.
https://doi.org/10.3934/publichealth.201...
).

Document analysis is a well-defined qualitative research method that involves the systematic review of documents on the subject of interest. The process requires the selection of relevant documents, assessment and evaluation of the documents, and extraction of the relevant data needed to promote an idea or hypothesis (1010. Dalglish SL, Khalid H, McMahon SA. Document analysis in health policy research: the READ approach. Health Policy Plan. 2020;35(10):1424–31. https://doi.org/10.1093/heapol/czaa064.
https://doi.org/10.1093/heapol/czaa064...
). It is an effective tool in health care policymaking and research (1010. Dalglish SL, Khalid H, McMahon SA. Document analysis in health policy research: the READ approach. Health Policy Plan. 2020;35(10):1424–31. https://doi.org/10.1093/heapol/czaa064.
https://doi.org/10.1093/heapol/czaa064...
). The information that is gathered could then be used to add justification or give meaning to an idea (1010. Dalglish SL, Khalid H, McMahon SA. Document analysis in health policy research: the READ approach. Health Policy Plan. 2020;35(10):1424–31. https://doi.org/10.1093/heapol/czaa064.
https://doi.org/10.1093/heapol/czaa064...
, 1212. Bowen GA. Document analysis as a qualitative research method. Qual Res J. 2009;9(2):27–40. https://doi.org/10.3316/QRJ0902027.
https://doi.org/10.3316/QRJ0902027...
).

The Caribbean Community (CARICOM) represents a complex regional health systems partnership, in which overlapping political, sociocultural, and economic elements may underscore fundamental interactions influencing health outcomes (1313. Caribbean Community Secretariat [Internet]. Georgetown: CARICOM Secretariat; c2021 Who we are. [cited 2021 Aug 8]. Available from: https://caricom.org/our-community/who-we-are/.
https://caricom.org/our-community/who-we...
). The three English-speaking Caribbean countries we assess in this document analysis (Barbados, Guyana, and Saint Lucia) emerged as early adopters of the WHO Global Action Plan (GAP) on AMR, drafting national action plans (NAPs) between 2017 and 2019. As of 2022, the majority of the CARICOM country NAPs remain in draft with limited progression toward implementation of stewardship activities. This document review, therefore, aims to explore the antimicrobial stewardship policy landscape in three English-speaking Caribbean countries (Barbados, Guyana, and Saint Lucia) and examine the key enablers and challenges to the design and implementation of formal antimicrobial stewardship programs.

MATERIALS AND METHODS

Search strategy

We first conducted a systematic search of a range of documents produced by policymakers, providing context to AMS policy strategies or aiming to generate discourse on AMS among users in these settings. Using the READ Approach to health policy review (1010. Dalglish SL, Khalid H, McMahon SA. Document analysis in health policy research: the READ approach. Health Policy Plan. 2020;35(10):1424–31. https://doi.org/10.1093/heapol/czaa064.
https://doi.org/10.1093/heapol/czaa064...
), one author (TR) searched for formal documents, informal or working policy documents, gray literature, and media communications from key international and regional sources, and from the hospital, district, and national levels, as described in the following section. While the READ Approach lists a range of types of documents that can be consulted in studies of health policy (1010. Dalglish SL, Khalid H, McMahon SA. Document analysis in health policy research: the READ approach. Health Policy Plan. 2020;35(10):1424–31. https://doi.org/10.1093/heapol/czaa064.
https://doi.org/10.1093/heapol/czaa064...
), we were particularly interested in accessing working and implementation documents and guidelines.

To improve the discovery of relevant documents for inclusion, we used the online international and regional databases that specifically access government archives and regional health sciences information: MEDLINE®/PubMedCentral – U.S. National Library of Medicine, Bethesda, MD, United States of America; SciELO – Scientific Electronic Library Online, Latin American and Caribbean Center on Health Sciences Information, São Paulo, Brazil; MedCarib – University of the West Indies, Mona Library, MED Carib Regional Coordinating Centre, this database contains information on all aspects of health and medicine relating to the English-speaking Caribbean and Suriname; Virtual Health Library (VHL) Regional Portal – VHL accesses national databases of scientific publications in Argentina, Cuba, and Jamaica; PAHO IRIS – the Pan American Health Organization’s (PAHO) Institutional Repository for Information Sharing (IRIS); LILACS – Latin American and Caribbean Center on Health Sciences Information, PAHO/WHO, São Paulo, Brazil.

Author TR supplemented the database search with a search for titles from the Oxford University Library online resource (Search Oxford Libraries Online; SOLO) and Google Scholar. The search strategy used a combination of first- and second-string terms summarized in Table 1. In addition, we directly contacted regional stakeholders from relevant institutional and government sectors (infection prevention and control [IPC]; water, sanitation, and hygiene [WASH]; national public health institutes; and clinical faculties) via email, as publicly available or referred by PAHO, The University of the West Indies, or government sources in this process – a “snowballing technique” (1414. Oxford Reference [Internet]. Oxford: Oxford University Press; c2023. Snowballing technique. [cited 2021 Jul 18]. Available from: https://www.oxfordreference.com/view/10.1093/oi/authority.20110803100514607.
https://www.oxfordreference.com/view/10....
).

Table 2 shows the inclusion and exclusion criteria employed. Author TR assessed the records for duplicates, which were removed. Then, each document’s title and abstract were screened and those ineligible were omitted. Authors TR, PR-P, and NEO reviewed the selected documents in full for a final decision on eligibility (Figure 1). The complete search result lists from MEDLINE and VHL are available upon request.

Data extraction

The data were collated in a Microsoft Excel spreadsheet outlining the following variables from all documents meeting the inclusion criteria: title; type of document; country/region of origin; date of publication; authors; intended audience; brief summary, including motivation and impact.

Using NVivo, we developed a coding guide for the thematic content analysis drawing on deductive (linked to a priori themes) and inductive (generated from the data) approaches, through line-by-line reading to identify codes arising from AMS content. We characterized codes under themes including key structure, process, and outcome measures in the WHO Practical Toolkit for AMS programs in low- and middle-income countries (LMICs) (77. World Health Organization. Antimicrobial stewardship programmes in health-care facilities in low- and middle-income countries: a WHO practical toolkit. 1st edition. Geneva: WHO; 2019. Available from: https://apps.who.int/iris/handle/10665/329404.
https://apps.who.int/iris/handle/10665/3...
) and the Donabedian Framework (1515. National Health Service, England. Quality, Service and Redesign Tools: A model for measuring quality care. [no place]: NHS England; 2018. Available from: https://www.england.nhs.uk/wp-content/uploads/2022/02/qsir-measuring-quality-care.pdf.
https://www.england.nhs.uk/wp-content/up...
), as applicable. Although presented as a linear, step-by-step procedure, the research analysis was an iterative and reflexive process (1616. Watt D. On Becoming a Qualitative Researcher: The Value of Reflexivity. Qual Rep. 2007;12(1):82–101. https://doi.org/10.46743/2160-3715/2007.1645.
https://doi.org/10.46743/2160-3715/2007....
).

We then sorted the segments of text, and through data retrieval, organized the codes or clustered codes for each project document across the three country data sets (1616. Watt D. On Becoming a Qualitative Researcher: The Value of Reflexivity. Qual Rep. 2007;12(1):82–101. https://doi.org/10.46743/2160-3715/2007.1645.
https://doi.org/10.46743/2160-3715/2007....
). The analysis served to frame the current composition of AMS activities in these three countries, provide a general description of implementation status, and highlight imperatives such as enablers and challenges in AMS policy.

RESULTS

The search strategy identified 719 relevant records, and 7 were added manually for a total of 726 initial records. After duplicates were removed and irrelevant title/abstracts were excluded, the remaining 34 documents were screened in full for AMS content eligibility. Of those, 15 (2% of the total records) met the inclusion criteria. Official policy documents accounted for 20% (n = 3) of the records, scholarly works/reviews accounted for 20% (n = 3), advocacy documents 13% (n = 2), news articles 27% (n = 4), and confidential reports 20% (n = 3).

TABLE 1.
Search strategy used for each database
TABLE 2.
Study inclusion and exclusion criteria

Documents supporting public communication play an important role in underlining political priorities as the language of AMS evolves in this region. The independent media, reporting to the public, facilitated the introduction of the WHO-GAP-aligned NAPs for two countries by high-ranking officials in the Ministry of Health and Wellness (Barbados), Ministry of Public Health (Guyana), and the livestock and agricultural industry, signaling early high-level political buy-in, multisectoral involvement in AMR strategies, and country compliance with international standards (Table 3). Similarly, newsletters and articles published through international organizations (PAHO/WHO) reinforced international commitment to the region and encouraged regional cooperation to increase competency in AMS (Table 4). This message is contextualized using local stewardship success stories, highlighting regional “AMS champions,” and providing direct country feedback for the NAP, identifying priority actions for AMS.

Within the formal policy documents (Table 5), all of which are NAPs, each country attempts to align policy with the WHO-GAP. In some cases, the NAPs remain in the draft phase pending situation analysis, integration of WHO recommendations following institutional point-prevalence surveys (PPS), multistakeholder contribution, and clear sustainable funding streams. The One Health approach to policy development outlines a multistakeholder consensus, encouraging collaboration between the animal, human, and environmental health sectors in AMR strategy design. Nevertheless, AMS as a priority area for human health and ASP implementation strategies are not explicitly outlined. For instance, there was no specific programmatic AMS content except to state that ASPs will be established by specific dates, for which no further updates have been accessed. At the same time, confidential reports from conduct of WHO hospital antibiotic use point prevalence surveys (PPS) and Tripartite AMR Country Self-Assessment Survey (TrACSS) (Guyana) highlight the lack of formal stewardship programs at an institutional and national level, challenging policymakers to design and implement ASPs through national coordination.

Finally, local research and publication of scholarly work (Table 6) contribute to stewardship discourse, shaping targeted AMS policy, and achieving major quality improvement milestones. In this way, a WHO PPS and one-year prevalence study in Barbados predated and informed the establishment of an institutional ASP and the national adaptation of the WHO action plan. Scholarly work from contributors at The University of the West Indies, Cave Hill, published in late 2020, underlined a critical need to focus on AMR priorities during the COVID-19 pandemic (88. Majumder MAA, Rahman S, Cohall D, Bharatha A, Singh K, Haque M, et al. Antimicrobial Stewardship: Fighting Antimicrobial Resistance and Protecting Global Public Health. Infect Drug Resist. 2020;13:4713–38. https://doi.org/10.2147/IDR.S290835.
https://doi.org/10.2147/IDR.S290835...
, 3030. Majumder MAA, Singh K, Gittens-St Hilaire M, Rahman S, Sa B, Haque M. Tackling Antimicrobial Resistance by promoting Antimicrobial stewardship in Medical and Allied Health Professional Curricula. Expert Rev Anti Infect Ther. 2020;18(12):1245–58. https://doi.org/10.1080/14787210.2020.1796638.
https://doi.org/10.1080/14787210.2020.17...
, 3131. Courtenay M, Burnett E, Castro-Sánchez E, Du Toit B, Figueiredo RM, Gallagher R, et al. Preparing nurses for COVID-19 response efforts through involvement in antimicrobial stewardship programmes. J Hosp Infect. 2020;106(1):176–8. https://doi.org/10.1016/j.jhin.2020.06.011.
https://doi.org/10.1016/j.jhin.2020.06.0...
).

These works (Table 6) amplify the message of AMS, advocating for stronger clinical AMS teams, providing a description of stewardship as a concept in clinical practice requiring core competency development. Local advocacy for enhanced pre-service training (preclinical) and involvement of university/health professional training programs in national stewardship activities also emerges within scholarly sources.

DISCUSSION

AMS policy process

Taken together, the document content creates a narrative of salient events and actors within and between these three countries, highlighting influences and barriers to policy strategy development and implementation. Starting with the carbapenemase-resistant Klebsiella pneumoniae (CRKP) outbreak investigation in Barbados, referenced in 4 of the 15 documents found (1 official policy, 1 newsletter, 1 scholarly work, 1 news report), we now outline what has emerged as a snapshot of the policy landscape between these three CARICOM states.

In Barbados, 2012, the infectious disease specialist at the national referral hospital was alerted by laboratory services of a CRKP outbreak (2929. Forde C, Stierman B, Ramon-Pardo P, Dos Santos T, Singh N. Carbapenem-resistant Klebsiella pneumoniae in Barbados: Driving change in practice at the national level. PLoS One [Internet]. 2017;12(5):e0176779. [cited 2020 Dec 29]. Available from: https://doi.org/10.1371/journal.pone.0176779.
https://doi.org/10.1371/journal.pone.017...
, 3232. Mulani MS, Kamble EE, Kumkar SN, Tawre MS, Pardesi KR. Emerging strategies to combat ESKAPE pathogens in the era of antimicrobial resistance: a review. Front Microbiol. 2019 Apr 1;10:539. https://doi.org/10.3389/fmicb.2019.00539.
https://doi.org/10.3389/fmicb.2019.00539...
). The infectious disease specialist contacted the PAHO AMR team, who coinvestigated the outbreak using the WHO PPS, adapted as an IPC evaluative tool. The investigation was followed by a one-year CRKP prevalence surveillance study in 2014, which identified significant CRKP risk factors associated with infection/colonization, such as using specific antimicrobials, including fluoroquinolones and piperacillin/tazobactam (2929. Forde C, Stierman B, Ramon-Pardo P, Dos Santos T, Singh N. Carbapenem-resistant Klebsiella pneumoniae in Barbados: Driving change in practice at the national level. PLoS One [Internet]. 2017;12(5):e0176779. [cited 2020 Dec 29]. Available from: https://doi.org/10.1371/journal.pone.0176779.
https://doi.org/10.1371/journal.pone.017...
). The investigation informed targeted institutional ASP development and implementation in this institution by 2015 (comprising an AMS committee, antibiotic use guidelines, and regular antibiogram publication) (3333. World Health Organization. WHO policy guidance on integrated antimicrobial stewardship activities. Geneva: WHO; 2021. Available from: https://apps.who.int/iris/handle/10665/341432.
https://apps.who.int/iris/handle/10665/3...
). IPC leadership in Barbados furthermore committed to establishing a regional IPC network to combat AMR in 2014 (1818. Nation News [Internet]. St. Michael, Barbados: Nation News; 2018 Jun 26. Antimicrobial resistance a growing public health threat. [cited 2023 May 11]. Available from: https://www.nationnews.com/2018/06/26/antimicrobial-resistance-a-growing-public-health-threat/.
https://www.nationnews.com/2018/06/26/an...
).

FIGURE 1.
Search strategy flowchart

By 2015, the WHO-GAP was introduced globally, urging that “all Member States would have, by 2017, a national action plan (NAP) aligned with the GAP objectives” (2020. World Health Organization. Driving change in antimicrobial stewardship in a low-resource setting. WHO Glob Action Plan AMR Newsl. 2017;(20).). The Barbados “success story” was shared at a regional conference for IPC leaders in 2016, and the country’s NAP was drafted in May 2017. The results of the Barbados WHO PPS and one-year point prevalence survey were published, coauthored by the Head of Infectious Diseases and PAHO AMR Director the same month. By January 2018, Guyana and Saint Lucia had drafted their NAPs, and the WHO PPS protocol was published, streamlining its conduct globally. By July 2018, both countries also carried out WHO PPS on antibiotic use in hospitals.

In summary, in Barbados, the WHO PPS adapted as an IPC investigative tool led to the implementation of an institutional ASP that informed the NAP, influencing the PAHO AMR team’s advocacy activities on AMS in the subregion. Of note, although conducted in 2012, the results of the CRKP outbreak were published in 2017; therefore, no documents specifically on AMS were discovered using the search strategy between 2010 and 2017.

Bidirectional pathway – actions of an individual

The actions of an individual appear to have driven targeted AMS strategies “from the bottom up,” positioning actors in Barbados as early innovators in the region for PPS and stewardship policy design and implementation. The 2019 WHO Practical Toolkit (77. World Health Organization. Antimicrobial stewardship programmes in health-care facilities in low- and middle-income countries: a WHO practical toolkit. 1st edition. Geneva: WHO; 2019. Available from: https://apps.who.int/iris/handle/10665/329404.
https://apps.who.int/iris/handle/10665/3...
) later noted that “it is often the same people involved in issues related to IPC and AMS both at the facility level and the national (state/regional) level,” using the case study of the CRKP outbreak investigation in this country as an example of the uses of PPS, and the overlapping responsibilities in LMICs. Using this case study, the “AMS champion” concept as an enabler of stewardship appears to comprise three fundamental attitudes or behaviors: competence, influence, and persistence, demonstrating AMS “software” elements influencing action at the prescriber level (77. World Health Organization. Antimicrobial stewardship programmes in health-care facilities in low- and middle-income countries: a WHO practical toolkit. 1st edition. Geneva: WHO; 2019. Available from: https://apps.who.int/iris/handle/10665/329404.
https://apps.who.int/iris/handle/10665/3...
).

TABLE 3.
Communication for public consumption: independent news media

The 2018 WHO Competency Framework for Health Workers’ Education and Training on Antimicrobial Resistance (3434. World Health Organization. WHO competency framework for health workers’ education and training on antimicrobial resistance. Geneva: WHO; 2018. Available from: https://apps.who.int/iris/handle/10665/272766.
https://apps.who.int/iris/handle/10665/2...
) maintains that the foundation of AMR awareness-building is ensuring healthcare workers’ competency to “promote awareness of AMR and appropriate antimicrobial use amongst all health care workers, patient communities and the general public,” and “act to protect the effectiveness of antimicrobials as an ethical imperative”; that is, act on resistance (3434. World Health Organization. WHO competency framework for health workers’ education and training on antimicrobial resistance. Geneva: WHO; 2018. Available from: https://apps.who.int/iris/handle/10665/272766.
https://apps.who.int/iris/handle/10665/2...
). The AMS champion in Barbados was an infectious disease specialist trained in outbreak investigation, research, and AMS, which placed this individual in an influential leadership position. In LMIC settings, limitations in human resources may increase the likelihood of overlapping roles in AMR objectives such as IPC/AMS/AMR surveillance and, as seen in this case, highlight this as a crucial area for capacity-building, as these individuals could potentially influence and shape implementation of policy and intervention strategies.

Horizontal (cross-programmatic) integration

Ensuring patient safety is an overarching principle of AMR strategies toward health system strengthening; therefore, successful integration of targeted AMS may require cross-programmatic integration. WHO cross-programmatic efficiency analysis (3535. Sparkes S, Durán A, Kutzin J. A system-wide approach to analysing efficiency across health programmes. Health Finance Diagnostics and Guidance No. 2. Geneva: World Health Organization; 2017. Available from: https://apps.who.int/iris/handle/10665/254644.
https://apps.who.int/iris/handle/10665/2...
) stresses the importance of interconnectedness between programmatic activities and enables countries to detect and analyze duplications, overlaps, and misalignments within and across programmatic activities. It is evident from this review that policy structures and processes exist for IPC and tertiary education clinical research institutions, which either have overlapping agendas or human resources to contribute to activities involving AMS. Therefore, identifying areas for integrating AMS in IPC and the health education sector could improve efficiency in achieving programmatic objectives in the broader health system.

TABLE 4.
Communication for public consumption: international organizations

Firstly, actors in IPC appear to lead AMS policy activities from the local to the regional level in the Caribbean; therefore, IPC may have a strong network of regional influence for AMS policy development and implementation (2929. Forde C, Stierman B, Ramon-Pardo P, Dos Santos T, Singh N. Carbapenem-resistant Klebsiella pneumoniae in Barbados: Driving change in practice at the national level. PLoS One [Internet]. 2017;12(5):e0176779. [cited 2020 Dec 29]. Available from: https://doi.org/10.1371/journal.pone.0176779.
https://doi.org/10.1371/journal.pone.017...
). For instance, IPC networks conduct regional conferences (initiated by Barbados following the CRKP study in 2014) in relevant skills training, sharing success stories on IPC and AMS (2929. Forde C, Stierman B, Ramon-Pardo P, Dos Santos T, Singh N. Carbapenem-resistant Klebsiella pneumoniae in Barbados: Driving change in practice at the national level. PLoS One [Internet]. 2017;12(5):e0176779. [cited 2020 Dec 29]. Available from: https://doi.org/10.1371/journal.pone.0176779.
https://doi.org/10.1371/journal.pone.017...
). They also promote the identification of “regional stewards” for AMS in the Caribbean (2222. Pan American Health Organization [Internet]. Washington, DC: PAHO; 2018 Oct 26. Sub-Regional Meeting on Infection Prevention and Control (IPC) and Health-Care Associated Infection Surveillance in Castries, St. Lucia on 15 to 17 October 2018. [cited 2023 May 11]. Available from: https://www3.paho.org/hq/index.php?option=com_content&view=article&id=14756:sub-regional-meeting-on-infection-prevention-and-control-ipc-and-health-care-associated-infection-surveillance-in-castries-st-lucia-on-15-to-17-october-2018&Itemid=0&lang=en#gsc.tab=0.
https://www3.paho.org/hq/index.php?optio...
). Furthermore, IPC and AMS core competencies overlap; the WHO Competency Framework for healthcare workers (2018) urges policy actors to understand and promote this linkage (3434. World Health Organization. WHO competency framework for health workers’ education and training on antimicrobial resistance. Geneva: WHO; 2018. Available from: https://apps.who.int/iris/handle/10665/272766.
https://apps.who.int/iris/handle/10665/2...
). This multimodal approach to quality improvement is also described in the 2018 WHO manual on improving IPC at the health facility (3636. World Health Organization. Improving infection prevention and control at the health facility: Interim practical manual supporting implementation of the WHO guidelines on core components of infection prevention and control programmes. Geneva: WHO; 2018 [cited 2021 Aug 20]. Available from: https://apps.who.int/iris/handle/10665/279788.
https://apps.who.int/iris/handle/10665/2...
).

Secondly, because of the health education infrastructure currently in place, pre-service and in-service AMS education and training could be supported by health education and research institutions such as regional and state universities. In Barbados, the WHO PPS principal investigator and AMS champion was on staff at the university and the national referral hospital during the CRKP outbreak. The other tertiary care institutions examined, in addition to their dual roles as the national referral hospitals and largest public tertiary hospitals in these countries, are also both clinical training/research institutions (1717. Guyana, Department of Public Information [Internet]. Georgetown: DPI; 2017 Jun 27. National Action Plan on Antimicrobial Resistance drafted, stakeholders consulted. [cited 2021 May 30]. Available from: https://dpi.gov.gy/national-action-plan-on-antimicrobial-resistance-drafted-stakeholders-consulted/.
https://dpi.gov.gy/national-action-plan-...
, 2929. Forde C, Stierman B, Ramon-Pardo P, Dos Santos T, Singh N. Carbapenem-resistant Klebsiella pneumoniae in Barbados: Driving change in practice at the national level. PLoS One [Internet]. 2017;12(5):e0176779. [cited 2020 Dec 29]. Available from: https://doi.org/10.1371/journal.pone.0176779.
https://doi.org/10.1371/journal.pone.017...
). Notably, all three scholarly works found in this document review were contributed by preclinical and clinical university researchers. As scholarly works suggest, pre-service training may be a crucial step to nurturing an ethos of AMS championing among newly graduated prescribers.

Challenges to AMS policy development and implementation from structure, process, outcome (SPO) elements

AMS falls under the five strategic objectives in the WHO-GAP and NAPs to “optimize the use of antimicrobial medicines in human and animal health” (66. World Health Organization. Global Action Plan on Antimicrobial Resistance. Geneva: WHO; 2015. Available from: https://apps.who.int/iris/handle/10665/193736.
https://apps.who.int/iris/handle/10665/1...
). However, the NAPs do not contain a clear description of elements of the formal AMS program at the institutional level, although the tertiary hospitals of all three countries are governed at the national level. Drawing on the Donabedian structure, process, outcome approach for measuring quality care (1717. Guyana, Department of Public Information [Internet]. Georgetown: DPI; 2017 Jun 27. National Action Plan on Antimicrobial Resistance drafted, stakeholders consulted. [cited 2021 May 30]. Available from: https://dpi.gov.gy/national-action-plan-on-antimicrobial-resistance-drafted-stakeholders-consulted/.
https://dpi.gov.gy/national-action-plan-...
), we explore limitations to ASP implementation by analyzing elements of the WHO-GAP-aligned NAPs.

Structure. The One Health approach, emphasizing multisectoral consensus in AMR policy development, is one recurrent and demonstrable cause of delayed rollout of the NAP; yet, the purpose of One Health is to encourage strategic leadership among all stakeholders (3737. World Health Organization [Internet]. Geneva: WHO; 2017 Sep 21 [cited 2022 Mar 16]. One Health. Available from: https://www.who.int/news-room/questions-and-answers/item/one-health.
https://www.who.int/news-room/questions-...
). In its 2021 Policy Guidance on integrated AMS activities (3333. World Health Organization. WHO policy guidance on integrated antimicrobial stewardship activities. Geneva: WHO; 2021. Available from: https://apps.who.int/iris/handle/10665/341432.
https://apps.who.int/iris/handle/10665/3...
), WHO acknowledges that “effective implementation of AMS activities in health-care facilities requires a comprehensive approach, beyond the facilities, at national policy and programme levels,” citing a request from Member States for further guidance on “how to facilitate the implementation of national AMS activities in an integrated and programmatic approach” (3333. World Health Organization. WHO policy guidance on integrated antimicrobial stewardship activities. Geneva: WHO; 2021. Available from: https://apps.who.int/iris/handle/10665/341432.
https://apps.who.int/iris/handle/10665/3...
). This includes, but is not limited to, the design of locally relevant antibiotic use guidelines, establishing leadership structures (national coordinating committee), and ensuring physical infrastructure and human resources are in place before implementation (3333. World Health Organization. WHO policy guidance on integrated antimicrobial stewardship activities. Geneva: WHO; 2021. Available from: https://apps.who.int/iris/handle/10665/341432.
https://apps.who.int/iris/handle/10665/3...
). In this case, leadership structures, guidelines, and human resources “hardware” may not be enough to ensure implementation, particularly due to the perceived “software” interdependency of consensus.

TABLE 5.
Internal documents

Process. Limitations related to process have also resulted in programmatic delays in monitoring and surveillance, antibiotic use surveillance, financial commitment, and education and training. A key recommendation for using the WHO PPS is that it is carried out at least annually to monitor and evaluate the ASP (3838. Zumaya-Estrada FA, Alpuche-Aranda CM, Saturno-Hernandez PJ. The WHO methodology for point prevalence surveys on antibiotics use in hospitals should be improved: Lessons from pilot studies in four Mexican hospitals. Int J Infect Dis. 2021 Jul;108:13–17. https://doi.org/10.1016/j.ijid.2021.04.079.
https://doi.org/10.1016/j.ijid.2021.04.0...
). However, it has only been carried out as a monitoring tool once in each of these countries in the last 4–8 years – a delay that may extend due to reassigning of resources to the COVID-19 efforts across the subregion (88. Majumder MAA, Rahman S, Cohall D, Bharatha A, Singh K, Haque M, et al. Antimicrobial Stewardship: Fighting Antimicrobial Resistance and Protecting Global Public Health. Infect Drug Resist. 2020;13:4713–38. https://doi.org/10.2147/IDR.S290835.
https://doi.org/10.2147/IDR.S290835...
, 2929. Forde C, Stierman B, Ramon-Pardo P, Dos Santos T, Singh N. Carbapenem-resistant Klebsiella pneumoniae in Barbados: Driving change in practice at the national level. PLoS One [Internet]. 2017;12(5):e0176779. [cited 2020 Dec 29]. Available from: https://doi.org/10.1371/journal.pone.0176779.
https://doi.org/10.1371/journal.pone.017...
). Additionally, overlapping recommendations for training prescribers and allied healthcare professionals in AMR, IPC, AMR surveillance, One Health, and WASH through decentralized strategies can lead to oversaturation and clouding of the message on AMS (66. World Health Organization. Global Action Plan on Antimicrobial Resistance. Geneva: WHO; 2015. Available from: https://apps.who.int/iris/handle/10665/193736.
https://apps.who.int/iris/handle/10665/1...
). For example, in one of the three NAPs there are two separate objectives related to corresponding competencies. Firstly, this highlights a potential duplication of efforts, and furthermore, there is no reference to the core elements within the WHO Competency Framework (3434. World Health Organization. WHO competency framework for health workers’ education and training on antimicrobial resistance. Geneva: WHO; 2018. Available from: https://apps.who.int/iris/handle/10665/272766.
https://apps.who.int/iris/handle/10665/2...
), developed in 2018, which could guide pre- and in-service educational activities. Finally, limited funding source is described in two of the three NAPs to mobilize and allocate resources. Without adequate funding, there is low potential for successfully sustained NAP or ASP (3333. World Health Organization. WHO policy guidance on integrated antimicrobial stewardship activities. Geneva: WHO; 2021. Available from: https://apps.who.int/iris/handle/10665/341432.
https://apps.who.int/iris/handle/10665/3...
). Following review of the NAP in Guyana in 2019, one priority WHO recommendation was to “create a funded National Antimicrobial Stewardship Strategy, to support healthcare facility Antimicrobial Stewardship Programs (ASP)/ interventions and strategies” (2828. World Health Organization. Tripartite AMR Country Self-Assessment Survey (TrACSS) Country Report on the Implementation of National Action Plan on Antimicrobial Resistance (AMR) Guyana. [no place]: WHO; 2020.).

Outcome. Van den Bosch et al. (3939. Van den Bosch CMA, Geerlings SE, Natsch S, Prins JM, Hulscher MEJL, Perl TM. Quality Indicators to Measure Appropriate Antibiotic Use in Hospitalized Adults. Clin Infect Dis. 2015;60(2):281–91. https://doi.org/10.1093/cid/ciu747.
https://doi.org/10.1093/cid/ciu747...
) describe 51 internationally agreed-upon quality indicators concerning appropriate antibiotic use in hospitalized adults. Yet within the NAPs, which represent the only formal policy toward AMS discovered in all three countries, measures of outcome focus solely on antimicrobial consumption, ESKAPE pathogen decline, and Clostridium difficile infection at the national level, with no recommendations for the institutional level. Key indicators highlighted in the WHO AMS Toolkit (77. World Health Organization. Antimicrobial stewardship programmes in health-care facilities in low- and middle-income countries: a WHO practical toolkit. 1st edition. Geneva: WHO; 2019. Available from: https://apps.who.int/iris/handle/10665/329404.
https://apps.who.int/iris/handle/10665/3...
) not seen within NAPs are: process indicators around proper documentation, oral-switch, and surgical prophylaxis (77. World Health Organization. Antimicrobial stewardship programmes in health-care facilities in low- and middle-income countries: a WHO practical toolkit. 1st edition. Geneva: WHO; 2019. Available from: https://apps.who.int/iris/handle/10665/329404.
https://apps.who.int/iris/handle/10665/3...
); outcome indicators such as percentage of hospital patients receiving antibiotics according to the AWaRe (Access, Watch, Reserve) classification, patient length of stay (relative to specified indications), in-hospital mortality, and readmission rates (77. World Health Organization. Antimicrobial stewardship programmes in health-care facilities in low- and middle-income countries: a WHO practical toolkit. 1st edition. Geneva: WHO; 2019. Available from: https://apps.who.int/iris/handle/10665/329404.
https://apps.who.int/iris/handle/10665/3...
, 3939. Van den Bosch CMA, Geerlings SE, Natsch S, Prins JM, Hulscher MEJL, Perl TM. Quality Indicators to Measure Appropriate Antibiotic Use in Hospitalized Adults. Clin Infect Dis. 2015;60(2):281–91. https://doi.org/10.1093/cid/ciu747.
https://doi.org/10.1093/cid/ciu747...
).

TABLE 6.
Scholarly works

These indicators describe validated measures for assessing the impact of ASP to optimize clinical outcomes. The 2021 WHO global Policy Guidance (3333. World Health Organization. WHO policy guidance on integrated antimicrobial stewardship activities. Geneva: WHO; 2021. Available from: https://apps.who.int/iris/handle/10665/341432.
https://apps.who.int/iris/handle/10665/3...
) recommends the need for a national coordinating committee that would ensure the “development of AMS implementation plans aligned with national action plans with well-defined goals and indicators” (3333. World Health Organization. WHO policy guidance on integrated antimicrobial stewardship activities. Geneva: WHO; 2021. Available from: https://apps.who.int/iris/handle/10665/341432.
https://apps.who.int/iris/handle/10665/3...
).

Study limitations

Although search criteria looked for current documents, most formal policies were drafted in 2017 and remained in the draft phase. Because of this, we could not analyze how the policy is being implemented in each sector; e.g., education, public engagement, or non-human health sectors. Social media pages by reputable government agencies were not included in the document review but are becoming more formalized and used for community health education. However, these platforms were not detailed in policy documents. We received no response from stakeholders in any of the three countries, which led to a dearth of working documents that would aid in exploring current processes and implementation activities. We did not analyze documents from the private sector, through which health care is steadily growing in LMICs, influencing AMR rates (4040. Denny KJ, Gartside JG, Alcorn K, Cross JW, Maloney S, Keijzers G. Appropriateness of antibiotic prescribing in the Emergency Department. J Antimicrob Chemother. 2019;74(2):515–20. https://doi.org/10.1093/jac/dky447.
https://doi.org/10.1093/jac/dky447...
).

Conclusion

This document review sheds light on how different sources of information move through bidirectional knowledge exchange in the regional policy landscape between these countries. Formal policy documents officially establish political position and national guidance on stewardship. However, at this nascent stage of policy development, governmental bodies appear to have encountered difficulty coordinating the integration of AMS and achieving the ideal of multisectoral collaboration outlined in international policy recommendations. International organizations such as PAHO/WHO encourage contextualizing stewardship as a first step, endorsing adaptation of high quality, “bottom-up” local evidence. Correspondingly, one key theme was the significance of individual action by AMS champions in programmatic design and implementation, which suggests that successful national policy could have a global impact, as LMICs learn from each other. CARICOM regional coordination has positively impacted IPC–AMS integration across this knowledge network.

Disclaimer.

Authors hold sole responsibility for the views expressed in the manuscript, which may not necessarily reflect the opinion or policy of the RPSP/PAJPH and/or those of the Pan American Health Organization (PAHO).

Acknowledgments.

This work was a formal research activity for the MSc International Health and Tropical Medicine dissertation at the University of Oxford, conducted between April and September 2021. It was a collaboration between academics at the University of Oxford and technical experts at the Pan American Health Organization. Vicki Marsh and Aronrag Meeyai of the University of Oxford provided academic supervision and guidance toward the design and execution of the research plan. We extend gratitude to the participating countries who granted us access to confidential materials.

  • Author contributions.
    TR conceived the original idea and planned the search strategy and collected the data. All authors analyzed the data and interpreted the results. TR and A-AU wrote the paper. All authors reviewed and approved the final version.
  • Conflict of interest.
    None declared.

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Publication Dates

  • Publication in this collection
    31 July 2023
  • Date of issue
    2023

History

  • Received
    11 Nov 2022
  • Accepted
    03 Apr 2023
Organización Panamericana de la Salud Washington - Washington - United States
E-mail: contacto_rpsp@paho.org