Antimicrobial Resistance in the Global Health Network: Known Unknowns and Challenges for Efficient Responses in the 21st Century
Abstract
:1. Antibiotic Resistance in the Global Healthcare Network: A Multifaceted Problem Involving Many Stakeholders of Disparate Sectors
1.1. The Modern Healthcare System: A Story of “Social Construction” with an Impact on AMR
1.2. The Understanding of AMR in the Healthcare Network: From Disease Ecology to Evolutionary Biology and Social Sciences
1.3. AMR at the Healthcare Network in the 21st Century: Novel Challenges in a Global World
2. Reframing AMR and Infectious Diseases in a Global Syndemic Scenario
2.1. Public Health to Control AMR in a Global Syndemic Scenario
2.2. AMR and Health, One-Health, and Global Health
2.3. Ecosystems and Their Feedback Loops: The Environmental Dimensions of AMR
3. Challenges in Measuring AMR in the Heterogeneous Healthcare Network
3.1. The Sample (The Unit of Analysis)
3.2. The Indicators
3.3. Validity, Reliability, and Comparability of the Information
4. Heterogeneity of Stakeholders Involved in the Global Health Network: Activities, Objectives and Challenges
4.1. Patient-Centered (Addressing Clinical Demands)
4.2. Population-Centered (Addressing Policy Demands)
4.3. Microbial-Centered (Addressing Novel and Old Infection-Control Needs and Community Demands)
Level | Stakeholders | Objectives | Required Information | Scope | Information Source | Gaps and Challenges |
---|---|---|---|---|---|---|
Patient-centered (addressing clinical demands) | Patients (and their families), doctors, clinical microbiologists, prescribers, and drug dispensers (pharmacists), and infection control practitioners. | Improving patient treatment. Design and implement standard treatment guidelines and essential drug lists. Expected burden of disease (BoD) at any geo-administrative level (individual setting). | Fine-scale information of individual risks for infection, colonization, and/or expected treatment outcome. Fine-scale information at setting level (identification of risks areas). | OUSs 1 Composite indexes (DRI, microbiome indexes) AMU | Real-time collection of local and stratified patient and AMC/AMU data. Lateral Public Health [208] | Develop criteria to define HAIs cases, still based on 48–72 h admission time [195,196]. Microbiome precision medicine [161,194]. Develop composite indexes [171,175]. Combine AMR and AMC/AMU trends in categorized patient populations [122,130,131,132,209,210]. Understand microbial transmission (plasmid, clones, and microbial consortiums). Plasmid surveillance: criteria, tools, and databases [156,160,211,212]. Evaluate the impact of the indoor microbiome on the health and safety of patients [164]. Implement AMU interventions based on behavioral models [13,213]. |
Population-centered (addressing policy demands) | Health managers, infection control practitioners, public health experts, and health insurance companies. Politicians, policymakers, economists, and economic growth sectors. | To estimate the impact of AMR at national, regional, or international levels (trends and benchmarking). Identifying the leading causes for AMR emergence and spread. Quantifying AMC (pharmaco-epidemiology, sales). | Information aligned with validity, reliability, and comparability data from local, regional AMR surveillance networks. | Surveillance. OUS (list of priority pathogens). AMC (sales). Composite indexes. | Real-time collection of local and stratified patient data linked to local, regional, and/or national databases. Active population-based surveillance at local and regional levels | Identify population-level factors/groups linked to the emergence of AMR Granularity of the information to extrapolate estimates. Harmonize units of analysis and indicators (with appropriate corrector indexes. See Section 3 (data quality and comparability issues). Omic tools and infrastructures (capacity building, harmonized and standardized tools) [149,161]. Put AMR in the context of other Public Health threats (syndemics). Real-time surveillance only available in a few countries [121]. Community level surveillance adapted to healthcare loops (hospital wastewater, and insurance health networks,) [138,198,214]. |
To design guidelines and policies. To monitor the effect of interventions. | Information aligned with validity, reliability and comparability data from regional AMR surveillance networks. | Aligned with National Antibiotic Plans (NAPs). | Active OneHealth sector-based surveillance aligned with NAPs | Harmonize NAPs according to local data and governance [181]. | ||
Estimating the cost–benefit impact on public health, environment, and economy (BoD, biodiversity). | Return estimation ISOR. Social impact. | Public Health economics. | Public Health and Social data repositories. | Integrate the human, animal, and environmental policy outcomes with the economy markers. | ||
Efficient awareness tools and campaigns between stakeholders and lay public to inform alerts or interventions (control, drug policies,…). | Awareness through feedback influencing consumers, policies, and investment. | Awareness Tailored according to social and cultural norms. | Consumers-public polls and enquiries. Data from patient’s associations (ITUs). | Develop efficient communication tools and channels (intra and inter-sectorial) [203]. Assure updating of messages [203]. Revise prescription models. | ||
Revise market and marketing practices (pharma and food industry). | Evolution of sales and prescriptions. Control good practices. | Market and marketing. | National Health and Consumer services. | Strengthening governance, management, innovation, and financing [181]. | ||
Pathogen-centered (addressing infection-control demands) 2 | Scientists and researchers, pharmaceutical industry, funding bodies, and global health donors. | Identification of transmission routes and microorganisms. Identify diagnostic biomarkers. Identification of reservoirs of MDR bacteria, plasmids, and hotspots for horizontal gene tranfer Identify PD parameters as minimal selective concentrations. Identify PD parameters as ecotoxicological concentrations. | Scientific publications, grey literature, workshop reports, international dossiers, white papers, and society reports. | Strains of microbial species (bacteria, fungi) of biomedical relevance from catalogued repositories and type strain collections. | Determine ethe effects of AMU (antibiotics and non-antibiotic antimicrobials) on dysbiosis patterns [164,215]. Understand microbial transmission (plasmid, clones, and microbial consortiums) Understand transmission pathways. (e.g., effects of particulate matters in the bacterial and fungal transmission, particularly in water–soil edges [216]. Plasmid surveillance: criteria, tools and databases [156,160,211,212]. Involve engineers in Public Health policies and guidelines. Environmental impact of sanitation measures [38]. Effects of interkingdom microbial interactions in the dynamics of MDR bacteria and ARGs [150]. Actions targeting the reduction of pharmaceuticals in the environment including the design, synthesis, and production of pharmaceuticals [38]. Determine the concentration of selective antibiotics for AMR in local environments [205,217,218]. Determine the impact of drugs in the environment to regulate microbial residue limits (MRLs) [218] 3. |
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Acknowledgments
Conflicts of Interest
Appendix A
Terms | Definition/Comments |
---|---|
Abiotic reservoirs | The part of an ecosystem where a microorganism or a chemical accumulates or is stockpiled outside of living organisms. Abiotic surfaces are composed of a diversity of materials. The impact of environmental factors on the selection of bacteria on abiotic reservoirs is largely unexplored [38,217]. |
AMR surveillance system | A structured and systematic procedure to measure the prevalence or incidence of AMR through continuous or periodical surveillance performed with a defined methodology and with specified indicators. Heterogeneities in the sampling, methods, or targets, for example, made current AMR surveillance systems inefficient for decision-making [85]. |
Antibiotic resistance | See Table S1. |
Bystander selection | The inadvertent pressure imposed by therapeutic treatments on microbes other than the targeted pathogen [215]. The effects of antibiotics on human microbiomes (at individual levels or at micro- and mesosystems) and on environmental microbiomes remain unexplored. |
Disease ecology | The ecological study of host–pathogen interactions within the context of their environment and evolution as relating to the impact of diseases on populations. This field grows out of the awareness of the pervasive role of pathogens in ecosystems. While medical researchers, such as Theobald Smith, Frank Macfarlane Burnet, and Frank Fenner, approached ecological interactions at the level of human populations, René Dubos focused on the interface of human hosts and microbes in the physiological environments of individuals [59]. This view influenced the way to approach medical microbiology. |
Community ecology | A subfield of ecology that investigates the factors that influence biodiversity, community structure, and the distribution and abundance of species (e.g., in the microbiosphere, interactions with the abiotic world, interactions between species, and between individuals of the same species (microbiome heterogeneity). Community ecology is the framework to analyze and interpret the human microbiome and resistome, including microbiomes of hospitalized patients, and hospital-built environment [73,169]. |
Consumptogenic systems | The systems that promote the consumption of goods and services to the detriment of either population or environmental health. Excess consumption is arguably a product of societal pressures from cultural and economic actors encouraging market transactions to individual consumers that forge daily routines around consumption and trading money for goods and symbols to reflect their social status. An emphasis on the consumptogenic system attempts to shift the focus away from just individual choices to consume to the structural conditions that enable and promote excess consumption. |
Environment, ecosystem, and assignation of these terms to the hospital space | The concept of “hospitals as environments” implies “hospitals as ecosystems”, comprising populations of individuals. Environment refers to “the sum total of all the conditions which surround man at a given space and time” [224], and, accordingly with the classic definition of ecosystem “the system resulting from the integration of all the living and non-living factors of the environment” [225,226]. |
Exposome | The measure of all the exposures from our environment (diet, lifestyle, and professional) of an individual in a lifetime and how those exposures interact with our own unique characteristics (e.g., genetics, physiology, and epigenetics) relate to health [227]. |
Evolutionary biology | A branch of biology focused on understanding the drivers’ (what/how) causal and stochastic processes and determined the evolutionary mechanisms (natural selection, common descent, and speciation-clonalization) that led to the current biodiversity of organisms on our planet [71]. |
Globalization | The growing interdependence of the world’s economies, cultures, and populations brought about by cross-border trade in goods and services, technology, and flows of investment, people, and information [different articles/analysis by the World Bank, https://www.worldbank.org/, accessed on 28 March 2023 or World Economic Forum, https://www.weforum.org/, accessed on 28 March 2023]. |
The Great Acceleration and the Anthropocene | The 1950s are the starting point of “The Great Acceleration” period which defines the sharp increase of the human activities (population, economy, resource use, and technologies) that drove rapid and unprecedented changes to the structure and functioning of the Earth System, such as the climate change. The “Great Acceleration” is the basis for a proposed new geologic epoch in Earth history, “the Anthropocene”. Both the Great Acceleration and the Anthropocene are often linked to the problem of AMR [14,228]. |
Feedback loops | The part of a system in which some part (or all) of the system’s output is used as input for future actions. |
Hybrid lineages | Biological lineages as bacterial species and clones, or mobile genetic elements that resulted from hybridization between two or more distinct lineages, frequently favored by DNA exchange [146]. |
Health | The WHO defines it as “a state of complete physical, mental and social wellbeing and not merely the absence of disease or infirmity” in its Constitution of 1948 [29]. The definition implies to see health as a fundamental human right. However, the definition remains inadequately implemented at the level of national law and standardized codes of practice despite WHO requests, and with significant consequences (identify “health” with “wellbeing” and “health care” with “disease care [229]. Thus, it inadvertently contributes to the ‘over-medicalization’ of the population. It also allows a platform for industry, medical technologies, and professionals to redefine our health status. This results in unequal access to health care and ultimately social inequality by excluding most potential users from the development of standards and policy. |
Health system | The WHO defines them as the totality of “organizations, people and actions whose primary intent is to promote, restore or maintain health”. The WHO health systems framework identifies the building blocks of a health system as related to governance, financial arrangements, medicines and technologies, health information systems, human resources, and health service delivery. This health system view is essential to approach the AMR problem [229]. |
Health center or community-health centers (CHCs) | Community-based and patient-directed organizations that deliver comprehensive, culturally competent, high-quality primary healthcare services to the nation’s most vulnerable individuals and families, including people experiencing homelessness, agricultural workers, residents of public housing, and veterans. Health centers integrate access to pharmacy, mental health, substance use disorder, and oral health services in areas where economic, geographic, or cultural barriers limit access to affordable health care. |
Hothouses | Closed and regulated environments with a high density and diversity of biological entities, favoring interactions between them. |
Individual agency, agency relationship | Individual agency is the level of freedom and self-decision to act whereby people act as individual members of society (within cultures, countries) or given collective community (practitioners). Factors that determine or limit individual agency include social class, religion, gender, ethnicity, ability, customs, and professional sector. Individualism represents a cultural shift from and juxtaposition to collectivism. Agency relationship is a fiduciary relationship where one person (called the “principal”) allows an agent to act on his or her behalf (e.g., practitioner and patients). These terms are derived from sociology and are increasingly relevant in AMU/AMC policies [145,146]. |
Koch’s postulates (or the Henle-Koch postulates) | Koch’s postulates (or Henle–Koch postulates) are four criteria designed to establish a causal relationship between a causative microbe and a disease. They were originally formulated by Friedrich Gustav Jacob Henle in the mid 1880s and refined and published by Robert Koch in 1890. Although they are still valid for a relatively small number of defined circumstances in which bacteria can be precisely tied to the cause of a particular clinical syndrome, they are revised under the light of available current knowledge [68,230]. |
Miracle drugs | Sulfa drugs were coined as “magic bullets” and a “growing miracle” because they were credited with declines in mortality from childbirth, pneumonia, and other diseases by the late 1930s [11,201]. Shortly after, penicillin was hailed as a “miracle drug” when it proved its efficiency in curing untreatable infection episodes of septicemia [201]. These adjectives have been applied to drugs with antibiotic effect. |
Risk assessment | A systematic and science-based approach to estimate the risks to the health and safety of persons arising out or in contact with AMR genes/pathogens, and also to support authorities in policymaking about the detection of critical points, and assessment of control and intervention strategies. Used in food safety [178] and infection control [180]. |
Pandemics | A pandemic is “an epidemic occurring worldwide, or over a very wide area, crossing international boundaries, and usually affecting a large number of people” [231]. Although the definition has traditionally been associated with infectious diseases, it is increasingly applied to communicable and non-communicable diseases [77]. |
Patches, landscape, and patches landscape | A patch is an area in a landscape that is different from surrounding areas. The patches generate what is called landscape heterogeneity, the diversity within a landscape. The diversity and uneven distribution that defines a landscape’s heterogeneity is based on many different features of an ecosystem (e.g., species and resources distribution and land-use patterns). The changes that occur in the separate spatial components of an ecosystem are described as patch dynamics. Patch dynamics is also a theoretical approach according to which the dynamics of an ecosystem can be understood through the analysis of its smaller spatial components (“patches”) that interact mutually. |
Plasmid | The term “plasmid” was coined by Joshua Lederberg in 1952 to define any extrachromosomal determinant of heredity [232]. Outbreaks of MDR organisms in hospitals during 1950s or in farms in 1960s, demonstrated the transferability of single or combined (multiresistance) AMR phenotypes and represented the landmark discovery of non-Mendelian heredity. They are unique MGEs because of their ability to cross species barriers, to generate novel entities resulting from recombination events, and to increase the copy number (and thus the mutation rate) after gene acquisition [26,151,233]. |
Population | The term “population” applies to the sets of individuals or evolutionary units with replication capacity that, at the subcellular (genes, plasmids, transposons, clones) and supracellular (bacterial communities, microbiomes, holobiome) level, are genetically and demographically connected. Thus, the ecological conditions (selection) in the system affect the adaptability of the units at each level (selective units) individually or cooperatively according to their degree of connectivity within a dynamic system (“evolution by association) [139,234]. |
Resistome | Initially defined by D’Costa in 2006 as the set of genes in the pan genome which encode antibiotic resistance [235]. Other genes coding for resistance to antimicrobials that co-select AMR (heavy metals, antiseptics,…) could join this category [236]. |
Social atomism | Atomism (or social atomism) is a sociological theory that refers to “the tendency for society to be made up of a collection of self-interested and largely self-sufficient individuals, operating as separate atoms”. Therefore, all social values, institutions, developments, and procedures evolve entirely out of the interests and actions of the individuals who inhabit any particular society. |
Social behaviour components and layers | See Figure S1. |
Syndemic or synergistic epidemic | The aggregation of two or more concurrent or sequential epidemics or diseases in a population with biological, psychological, or societal interactions and sharing common underlying societal drivers that exacerbate the prognosis and burden of disease. The syndemic approach contrasts with the biomedical approach to diseases that diagnostically isolate, study, and treat diseases as distinct entities separate from other diseases and independent of social contexts [75]. AMR is increasingly being approached as a syndemic threat (COVID, climate change, and emerging co-occurring infection). |
SDGs | The Sustainable Development Goals (SDGs), also known as the Global Goals, were adopted by the United Nations in 2015 as a universal call to action to end poverty, protect the planet, and ensure that by 2030 all people enjoy peace and prosperity. The 17 SDGs are integrated—they recognize that action in one area will affect outcomes in others, and that development must balance social, economic, and environmental sustainability. |
Therapeutic solutions to early major Public Health problems | Salvarsan represented the first effective treatment against syphilis; sulfonamides were the first effective options against infectious diseases of high mortality and morbidity, such as puerperal fever, pneumonia, scarlet fever, meningitis, gonorrhea, and erysipelas; and natural antibiotics (such as streptomycin and other aminoglycosides, penicillin, and tetracycline) were the first effective options for tuberculosis and safe alternatives to combat many infectious diseases. All were major public health problems in the early 20th century [15,16,18]. |
“Watch lists” or “priority lists” of pathogens for which new antibiotics are urgently needed | They are catalogues of bacteria/fungi families that pose the greatest threat to human health. Their goal is to guide and promote research and development (R and D) of new antibiotics, to align R and D priorities with public health needs, and to coordinate the fight against AMR bacteria based on epidemiologic control of the infectious agent, its accurate surveillance and detection, and implementation of effective treatments [237]. In 2013, the Centers for Disease Control and Prevention (CDC) published the first “watch list of antibiotic threats” (AMR bacteria) which ranked them as urgent, serious, or concerning threats to humans [189,238]. In 2017, the WHO categorized the same pathogens into critical, high, and medium-priority groups in what they called priority pathogen lists [237,239]. The first watch list of fungal antimicrobial resistance threats has been available since late 2022 [239]. |
World Antimicrobial Awareness Week (WAAW) | The WAAW is a global campaign that is celebrated annually to improve awareness and understanding of AMR and encourage best practices among the public, One Health stakeholders, and policymakers, who all play a critical role in reducing the further emergence and spread of AMR. |
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Coque, T.M.; Cantón, R.; Pérez-Cobas, A.E.; Fernández-de-Bobadilla, M.D.; Baquero, F. Antimicrobial Resistance in the Global Health Network: Known Unknowns and Challenges for Efficient Responses in the 21st Century. Microorganisms 2023, 11, 1050. https://doi.org/10.3390/microorganisms11041050
Coque TM, Cantón R, Pérez-Cobas AE, Fernández-de-Bobadilla MD, Baquero F. Antimicrobial Resistance in the Global Health Network: Known Unknowns and Challenges for Efficient Responses in the 21st Century. Microorganisms. 2023; 11(4):1050. https://doi.org/10.3390/microorganisms11041050
Chicago/Turabian StyleCoque, Teresa M., Rafael Cantón, Ana Elena Pérez-Cobas, Miguel D. Fernández-de-Bobadilla, and Fernando Baquero. 2023. "Antimicrobial Resistance in the Global Health Network: Known Unknowns and Challenges for Efficient Responses in the 21st Century" Microorganisms 11, no. 4: 1050. https://doi.org/10.3390/microorganisms11041050