Antimicrobialstewardship Andpandemicpreparedness: Harnessinglessonslearnedto Advanceourmission

A n t i m i c ro b i a l S t e w a rd s h i p
a n d P a n d e m i c Pre p a red n e s s :
H ar n e s s in g L es s o n s L ea r ne d t o
Advance Our Mission
Terrence McSweeney, PharmDa,*, Mei H. Chang, PharmD
a,1
,
Payal Patel, MD, MPHb,c, Priya Nori, MDd
KEYWORDS
Antimicrobial stewardship Pandemic stewardship Antimicrobial resistance
KEY POINTS
Public health policy addressing the threat of antimicrobial resistance (AMR) has greatly
increased momentum for antimicrobial stewardship programs (ASPs) worldwide.
ASPs reoriented traditional responsibilities to better serve the COVID-19 pandemic
response. Such “pandemic stewardship” functions can be escalated and de-escalated
as needed to serve emerging public health emergencies.
Although ASPs were assuming functions outside their traditional roles, they were unable
to monitor antibiotic use or provide audit and feedback to the usual extent. Increased anti-
biotic use, hospital-acquired infections, and AMR were observed during the height of
COVID-19. In the event of future pandemics, increased resources for stewardship pro-
grams will be required to meet the needs of health systems.
ASPs have evolved to offer more robust services within the health care system; as such,
current metrics used to measure impact and staffing ratios should be reevaluated.
The future of ASP is likely to involve health system expansion, expansion into outpatient
and post-acute care settings, and stewarding of immune-based and microbiome
therapeutics.
INTRODUCTION
The increase of carbapenem-resistant Acinetobacter baumannii and pan-resistant

Candida auris reminds us of multiple intersecting public health crises, such as
a
Department of Pharmacy, Montefiore Health System, Bronx, NY, USA; b Division of Infectious
Diseases and Clinical Epidemiology, Intermountain Healthcare, Murray, UT, USA; c Infectious
Diseases Clinic, Intermountain Medical Center, 5171 Cottonwood Street Suite 350, Murray, UT
84107, USA; d Division of Infectious Diseases, Department of Medicine, Montefiore Health
System, Albert Einstein College of Medicine, 3411 Wayne Avenue #4H, Bronx, NY 10467, USA
1
Present address: 1825 Eastchester Road, Bronx, NY 10461.
* Corresponding author. 3411 Wayne Avenue #4H, Bronx, NY 10467.
E-mail address: tmcsweeney@montefiore.org
Infect Dis Clin N Am 37 (2023) 669–681

https://doi.org/10.1016/j.idc.2023.07.001 id.theclinics.com
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670 McSweeney et al
antimicrobial resistance (AMR), viral pandemics, and the impacts of climate change.
The global surge of these pathogens is likely to outpace new drug development or
our ability to treat them. Despite recent approvals of over a dozen new antibacterials
in the last 3 years, few possess novel mechanisms, offer oral options, or sufficiently
cover extensively drug-resistant gram-negative bacteria.1 The Centers for Disease
Control and Prevention (CDC) estimate more than 3 million people acquire an
antimicrobial-resistant infection each year in the United States, leading to nearly
50,000 deaths.2 Globally, the United Nations (UN) estimates that 10 million deaths
will be attributed to AMR by 2050.3 Moreover, additional public health crises such
as natural disasters, urbanization, food insecurity, and famine are likely to further
worsen infectious disease outcomes and the disproportionate burden of AMR in
low- and middle-income countries.4,5
GLOBAL MILESTONES IN STEWARDSHIP
These pressing concerns are well-recognized security risks which have been priori-
tized by public health authorities leading to the development of global action plans
to slow AMR and promote judicious antibiotic use. In recent years, many countries
of a broad economic spectrum have instituted individualized national action plans
to focus on AMR.6 For instance, in the United States, the National Action Plan estab-
lished under President Barack Obama in 2015 set out 230 milestones for federal
agencies. As of 2021, 93% of 230 milestones had been completed.7 The National Ac-
tion Plan also launched the Presidential Advisory Council on Combating Antibiotic-
Resistant Bacteria (PACCARB) which provides recommendations to the Secretary
of Health and Human Services regarding policies intended to support and evaluate
the implementation of US government activities related to AMR. The updated 2020–
2025 National Action Plan expands on evidence-based activities proven to slow the
spread of AMR, such as infection prevention and stewardship programs, which are
exceedingly important in the aftermath of the pandemic.8 The PACCARB recently pub-
lished “Preparing for the Next Pandemic in the Era of Antimicrobial Resistance” with
specific recommendations that include a focus on antimicrobial stewardship, infection
prevention, workforce expansion, data sharing and security, and product innovation in
March 2023.9
As a result of key legislative milestones outlined in detail elsewhere in this text,
which significantly increased momentum for stewardship implementation, the per-
centage of US hospitals meeting all seven CDC Core Elements of antimicrobial stew-
ardship increased to 94.9% in 2021 (Fig. 1).10–14 However, stewardship guidelines,
position statements, and national policies have never addressed the role of antimicro-
bial stewardship programs (ASPs) in pandemic preparedness. ASPs had been lever-
aged on a small scale during the 2009 H1N1 influenza pandemic to develop treatment
protocols and vaccine prioritization schema.15 They would later be heavily used for the
COVID-19 pandemic response in myriad ways, as described herein.16–18
Internationally, the World Health Organization (WHO) greatly increased momentum
for stewardship by endorsing a global AMR action plan calling for ASPs to monitor and
promote the optimization of antimicrobial use at national and local levels within its
member nations, though the state of ASPs worldwide is still largely unknown, partic-
ularly in low- and middle-income countries.19 In 2017, a WHO expert committee devel-
oped the Access, Watch, Reserve (AWaRe) Classification in which antibiotics are
classified into three groups: Access, Watch, and Reserve, considering the impact of
different antibiotics/classes on AMR and to help member nations with their steward-
ship efforts.20 However, the implementation of ASPs in acute care hospitals in many
Antimicrobial Stewardship and Pandemic Preparedness 671
TJC An microbial
Stewardship
Standard eﬀec ve
CDC releases Core for hospitals,
Elements of U.S. develops Na onal cri cal access
Hospital Ac on Plan for hospitals, and PACCARB codiﬁed
Stewardship Comba ng An bio c- nursing care COVID19 pandemic
into legisla on
Programs Resistant Bacteria centers
2015 2016 2019
2014 2017 2020
WHO endorses IDSA & SHEA CMS releases CoP WHO releases U.S. Na onal
Global Ac on Plan provide Guidelines that requires acute Prac cal Toolkit for Ac on Plan for
on AMR for Implemen ng care hospitals to implemen ng ASPs Comba ng
an ASP develop & at na onal and An bio c-Resistant
implement an ASP health-care facility Bacteria 2020 –
level 2025
Fig. 1. Antimicrobial stewardship milestones in the United States. AMR, antimicrobial resis-
tance; ASP, antimicrobial stewardship program; CDC, Centers for Disease Control and Pre-
vention; CMS, Centers for Medicare and Medicaid Services; CoP, condition of
participation; IDSA, Infectious Diseases Society of America; SHEA, the Society for Healthcare
Epidemiology of America; TJC, The Joint Commission; PACCARB, Presidential Advisory Coun-
cil on Combating Antibiotic-Resistant Bacteria; WHO, World Health Organization.
countries still faces multiple barriers including lack of resources, unreliable infrastruc-
ture, and need for enhanced prescriber education.21,22 Although the focus of this re-
view is on stewardship in human health care, a global one health approach,
addressing excess antibiotic use in all facets of human and nonhuman health care,
is widely accepted as an important approach to addressing AMR globally, and a major
public health priority of the WHO, CDC, UN, and other key stakeholders.23 Consid-
ering that recent viral pandemics had origins in animal populations and that AMR
genes are prevalent in humans, livestock, and environmental reservoirs, a global
one health approach is crucial for addressing both crises.
WHAT IS PANDEMIC STEWARDSHIP?
Unlike Infection Prevention and Control programs, the role of ASPs in respiratory viral
pandemics was not immediately apparent before 2020, and stewards required
tremendous self-advocacy to gain a “seat at the table” during the COVID-19
pandemic. ASPs demonstrated poise and resilience in assisting with COVID-19 efforts
across the globe, harnessing expertise in diagnostic stewardship, therapeutics, proto-
col development, and use of technology to develop strategic collaborations, content
expertise, and contribute to the body of knowledge on COVID-19.24 Almost immedi-
ately, ASPs “stepped up” to develop testing and treatment guidelines, created path-
ways to access investigational therapies, built electronic decision support for testing
and antiviral treatments, assisted in vaccine planning and clinician education, devel-
oped outpatient COVID-19 therapeutics programs, among other important func-
tions.25,26 However, few programs received an increase in dedicated effort or
resources to perform this work on top of existing duties.27
Unfortunately, although ASPs were assuming functions outside their traditional roles,
they were unable to monitor antibiotic use or provide audit and feedback to the usual
extent.27 Moreover, early in the pandemic, there were significant increases in antibiotic
672 McSweeney et al
use in hospitalized patients for presumptive community-acquired bacterial pneumonia

or sepsis.28 Diagnostic uncertainty, lack of effective anti-SARS-CoV-2 therapies early
on, and inability of ASPs to conduct usual activities contributed to excess antibiotic
use.28,29 In parallel, hospitals also experienced excess hospital-acquired infections
(HAIs) in 2020 and 2021 due to deviation from usual infection prevention and control
practices.30 Compounding the impact of increased HAIs was the substantial increase
in antibiotic-resistant pathogens during this timeframe. A 2022 CDC special report
detailed an alarming increase in infections due to multidrug-resistant (MDR) organisms
such as carbapenem-resistant Acinetobacter, extended-spectrum beta-lactamase-
producing Enterobacterales, vancomycin-resistant Enterococcus, MDR Pseudo-
monas aeruginosa, and methicillin-resistant Staphylococcus aureus.31 Increased
incidence of COVID-19-associated candidiasis was also observed, including infection
with MDR Candida auris.32 The increase in infections due to MDR pathogens is likely
multifactorial due to deviations from evidence-based infection prevention and
control practices, increases in antibiotic use, and complications of severe COVID-19
infection.
ASPs expanded roles during COVID-19, now coined “pandemic stewardship,”
leveraged their knowledge, skills, expertise, and infrastructure, to reorient traditional
responsibilities to better serve COVID-19 response efforts.16 These functions can
be escalated and de-escalated as needed to respond to other public health emergen-
cies (eg, mpox) provided ASPs are supported with adequate staffing and resources.
Examples of pandemic stewardship functions include.
Case Identification
Before widespread availability of testing, ASPs collaborated with infection prevention
programs and microbiology laboratories to create guidelines for SARS-CoV-2
testing.17 To preserve limited supply of nasal swabs for diagnosis of COVID-19,
ASPs helped curtail the use of respiratory pathogen panels and shift Staphylococcus
aureus nasal polymerase chain reaction (PCR) testing to standard culture testing
methods.33 With the introduction of universal COVID-19 screening, ASPs continued
to assist with early case identification, screening protocol development, and provider
communication. In collaboration with information technology, existing ASP modules
and electronic reports were repurposed to identify COVID-19 patients in real time
and optimize patient review.34
A future viral pandemic, such as pandemic influenza, may require similar develop-
ment of testing triage protocols, whereas laboratory testing capacity is being scaled
up.9
Repurposing prospective audit and feedback

With the surge in inappropriate antibiotic use in COVID-19 patients despite low rates of
bacterial coinfection, prospective audit and feedback (PAF) was an important stew-
ardship tool to minimize the collateral damage. A 2020 systematic review found that
despite a 6.9% rate of bacterial coinfection in patients with COVID-19, 70% of those
with COVID-19 infections received antibiotics.35 A prospective noninferiority trial
demonstrated PAF during COVID-19 was a safe and effective means to reduce unnec-
essary antibiotic prescribing.36
ASPs also applied PAF toward.
The appropriate use of COVID-19 inpatient and outpatient therapies
Review and adjust the frequency of medication administrations to limit the need
to enter isolation rooms
Assist with medication safety monitoring (eg, liver function tests while on remde-
sivir, drug–drug interactions with nirmatrelvir/ritonavir)
Future viral pandemics may require similar use of ASP PAF for appropriate use of
antibiotics and experimental agents and monitoring of drug–drug interactions.
Formulary restriction and preauthorization

ASPs ensured appropriate distribution of limited therapeutics through formulary re-
strictions and preauthorization.37 Investigational use of hydroxychloroquine for
COVID-19 negatively impacted patients who required it for underlying rheumatologic
conditions.38 By restricting hydroxychloroquine, ASPs helped safeguard medication
allocation and minimize misuse. Later, with the advent of monoclonal antibodies
and oral antiviral agents, formulary restrictions helped ensure that limited allocations
were being prioritized for those patients at highest risk of disease progression.
Formulary restrictions can be reinstated as needed during future viral pandemics
requiring judicious use of novel therapeutics.
Multidisciplinary collaborations to develop treatment guidelines
ASPs ideally consist of physicians and pharmacists with specialized infectious diseases
training who are uniquely poised to evaluate rapidly evolving data and incorporate into
clinical practice. ASPs across the globe reported updating treatment guidelines innu-
merable times as new data and therapeutics emerged. ASPs collaborate closely with
infection prevention departments, microbiology laboratories, and frontline clinicians to
develop guidelines for management of both common and emerging pathogens.37 Inter-
disciplinary collaborations greatly increased during the pandemic and helped secure a
recurring role for ASPs within hospital incident command centers. Leading the develop-
ment and maintenance of treatment guidelines is a specialized ASP function that will un-
doubtedly be required in future viral pandemics as well.
Diagnostic stewardship
Diagnostic stewardship was heavily used early on to prioritize SARS-CoV-2 testing
especially as swab and reagent shortages were encountered. As the pandemic
unfolded, ASPs additionally developed and disseminated best practices around pro-
calcitonin testing and methicillin resistant Staphylococcus aureus (MRSA) nares PCR
testing in hospitalized COVID-19 patients, which helped limit both unnecessary testing
and excess antibiotics.39,40
Managing drug shortages
Widespread supply chain disruption combined with increased demand for essential
medications during the COVID-19 pandemic led to an unprecedented number of medi-
cation shortages. Shortages of essential medications such as amoxicillin, oseltamivir,
and antipyretics resurfaced during concurrent influenza, respiratory syncytial virus
(RSV), and COVID-19 surges of 2022 to 2023, which unfortunately impacted pediatric
populations the most. ASPs played a key role in managing medication shortages
through enhanced communication with pharmacy personnel, developing intravenous
(IV) to per os (by mouth) (PO) switch protocols, and implementing formulary restric-
tions.33,41 Shortages of generic drugs such as antimicrobials occur frequently in part
due to lack of incentives to produce these in the United States; therefore, shortage miti-
gation is an ASP skill set habitually required regardless of pandemic surges.
Participation in Clinical Trials

Stewardship program physicians and pharmacists served as primary or co-primary in-
vestigators for clinical trials for COVID-19 therapeutics or assisted with clinical trial
674 McSweeney et al
recruitment of patients flagged during routine PAF.42 As a result, valuable clinical trials
skills were garnered, which can be applied to expand the future scope of stewardship
programs.
Effective Communication
Stewardship leaders are uniquely poised to effectively communicate new and evolving
information to frontline clinicians, executive leaders, patients, and families given their
long-standing organizational roles pertaining to education and dissemination of infor-
mation to stakeholders. This also involves routine maintenance of Web sites and inter-
nal portals housing up-to-date clinical guidelines and pathways. Effective
communication skills further refined during COVID-19 can be applied to several situ-
ations such as advocating for resources internally or persuading policy makers to
devote attention to passing legislation to combat AMR.
Allocation of Emergency Use Authorization therapeutics

A rapid expansion of clinical trials of COVID-19 therapeutics led to US Food and Drug
Administration Emergency Use Authorization for multiple monoclonal antibodies for
treatment and prophylaxis, antiviral medications, and vaccines. However, initially, de-
mand for these agents greatly outweighed supply, and stewardship programs took the
lead on establishing and disseminating allocation protocols prioritizing patients at
greatest risk of SARS-CoV-2 acquisition and poor COVID-19 outcomes.25,43–45 Stew-
ardship programs oversaw the triage/allocation of therapeutics in the inpatient and
outpatient settings, including IV remdesivir and oral nirmatrelvir/ritonavir (before full
Food and Drug Administration [FDA] approval), and monoclonal antibodies (during
the period of maximal effectiveness). Creating criteria inclusive of race/ethnicity, so-
cioeconomic status, essential worker status in addition to comorbid health conditions
allowed stewardship programs to promote health equity, a major priority of public
health departments and health systems.
WHAT ROLE DID ANTIMICROBIAL STEWARDSHIP PROGRAM PLAY DURING THE

MPOX OUTBREAK?
In May 2022, 2 years into the COVID-19 pandemic, the first cases of mpox were re-
ported in the United States. By February 2023, a total of 86,231 laboratory-
confirmed cases, 1087 probable cases, and 200 deaths were reported.46 Most cases
were identified in the United States. (>30,000 cases). We were again confronted with
limited information to guide testing, treatment, and vaccination. Despite the probable
involvement, to date, there are no published accounts of the role of ASPs during
mpox. Our ASP, such as others in New York City and elsewhere, collaborated with
infection preventionists, outpatient infectious disease providers, microbiology, local
department of health, and the investigational pharmacy to setup expedited pathways
for identification, testing, enrollment in trials, drug procurement, and treatment with
tecovirimat.
WHAT ANTIMICROBIAL STEWARDSHIP PROGRAM METRICS CAN BE APPLIED TO

PANDEMIC STEWARDSHIP?
ASP metrics are covered in detail elsewhere in this text. However, metrics which accu-
rately encompass the contributions and successes of stewardship programs during
pandemics may include.
Monitoring adherence to evidence-based clinical guidelines and protocols
Clinical outcomes of patients infected with novel viruses of emerging MDR path-
ogens (eg, length of stay, readmissions, and mortality)
Monitoring reductions in antibiotic resistance after implementation of steward-
ship interventions to curb unnecessary use during pandemics
Percentage of patients meeting criteria for antiviral treatment who receive pre-
scriptions, especially those from non-white minority groups
Tracking outpatient antibiotic prescriptions for positive viral tests.
As the stewardship community moves past pandemic activities, we can once again
focus on metrics, data-reporting mandates, and reassess which metrics are most
meaningful to demonstrating the value of stewardship programs. As such, steward-
ship metrics and reporting into National Healthcare Safety Network’s Antibiotic Use
and Resistance Module are addressed in detail elsewhere in this text.
STAFFING
Despite many ASPs meeting all CDC Core Elements, staffing models are not robust.
Most ASP staffing proposals recommend a combined physician and pharmacist full
time equivalent (FTE) of roughly one to every 100–250 beds, with a suggested
physician-to-pharmacist ratio of 1:3.47 However, national surveys of ASPs routinely
cite insufficient financial resources and staffing as barriers to program success.48–50
During the COVID-19 pandemic, staffing burdens only increased. A survey of stew-
ardship leaders across 51 Michigan hospitals indicated substantially increased duties,
similar or fewer resources, more work hours, and increased burnout.27 Sustained and
more likely increased stewardship funding will be required to meet the expanding
needs of health systems, avoid burnout and staffing shortages, combat AMR, and
contend with future pandemics. Optimal staffing for outpatient and tele-stewardship
is an area of research need.
FUTURE DIRECTIONS BEYOND THE PANDEMIC: NONANTIBIOTIC THERAPIES FOR

INFECTIOUS DISEASES AND THE ROLE OF ANTIMICROBIAL STEWARDSHIP
Historically, therapeutic approaches to infectious diseases heavily focused on

pathogen-directed therapies (eg, antibiotics targeting bacterial targets such as
penicillin-binding proteins or ribosomal subunits; antivirals inhibiting viral DNA poly-
merase). As seen during the COVID-19 pandemic and preceding years, there will likely
be a continued shift toward.
Immune-based therapies designed to provide passive immunity (eg, monoclonal
antibodies) or minimize host-mediated damage (eg, interleukin [IL]-6 inhibitors)
Microbiome therapies designed to restore host microbiome and limit the ability of
opportunistic pathogens to proliferate
Phage therapies
This new therapeutic landscape offers ample opportunity for ASPs to extend their
expertise and provide additional services.
Immune-Based Therapies
Examples of successful ASP-led COVID-19 therapeutics programs offer insight into
the potential role of ASPs in adoption and dissemination of immunotherapies.25 How-
ever, as the impacts of the COVID-19 pandemic recede, stewardship programs could
translate this work and focus on infectious diseases representing a large global burden
such as tuberculosis. According to the WHO Mycobacterium tuberculosis is the 13th
676 McSweeney et al
leading cause of death and the second leading infectious cause of death second to
COVID-19.51 Novel immunotherapies may improve our current arsenal to combat
such infections.52 Research and development into tuberculosis (TB)-specific immuno-
therapy is currently underway with hopes to offer equally efficacious, less toxic, and
shorter therapies.53
Microbiome Therapies
Antibiotic use may be linked with emerging health issues including obesity, endocrine
diseases, early-onset asthma, celiac disease, inflammatory bowel disease, and al-
lergies.54 These signals are driving increased research into the human microbiome
and associated health implications (short term, long term, and generational).
Alterations in host microbiomes due to antibiotic use are associated with the devel-
opment of CDI. Fecal microbiota transplantation is an alternative treatment approach
to normalize the host microbiome and prevent recurrences, but adoption has been
limited.55 Two commercially available fecal spores were FDA-approved for use.
Vowst and Rebyota are both indicated to prevent recurrent CDI in adult patients
18 years and older following antibacterial treatment.56,57
Vowst dosing: Four capsules taken orally once daily for 3 consecutive days (to
be administered after a washout period of 2–4 days after completing CDI
antibiotics).
Rebyota dosing: 150 mL per rectum once (to be administered 24–72 hours af-
ter the last dose of antibiotics for CDI).
ASPs can help incorporate these new microbiome therapies into CDI treatment
guidelines and coordinate access to therapy.
Phage Therapies
Phage therapies have long been investigated for the treatment of infectious diseases
but have not been widely adopted. Phages are highly specific for select bacterial spe-
cies, offering the advantage of precise pathogen targeting. However, challenges asso-
ciated with personalized phage matching for individual patient isolates have limited
phage use largely to two scenarios: through compassionate use for serious MDR in-
fections or through clinical trials. With increasing resistance to antimicrobials, phage
therapy may provide additional options. There are several successful case reports
of phage therapy used for treatment of MDR Acinetobacter, P aeruginosa, and
difficult-to-treat Mycobacterium abscessus infections.58–61
Given the complexity in obtaining phage therapy, ASPs can help develop guidance/
protocols in collaboration with site primary investigators to link patients to clinical trials
and offer education to the health care team.
SUMMARY
Original guideline and policy definitions of antimicrobial stewardship described “coor-

dinated interventions designed to improve and measure the appropriate use of antimi-
crobial agents by promoting the selection of the optimal antimicrobial drug regimen
including dosing, duration of therapy, and route of administration.”62 Antimicrobial
resistance was a major factor driving public policy and legislation requiring global
adoption of ASPs. However, original definitions did not anticipate the vastly increased
role and influence of ASPs during the COVID-19 or mpox crises. Innumerable skills
and robust infrastructure can again be scaled up and used during future viral pan-
demics but requires further investments in ASP resources, specifically staffing
Hospital
Administra on
An microbial
Microbiology Stewardship
Program
Frontline Informa on
Nursing Technology
Pa ents
Fig. 2. Seat at the table.
commensurate to patient volume and complexity. Future directions of ASPs include

stewarding of immune-based and microbiome therapeutics, among other arenas.
Moving forward it is critical for ASPs to secure their “seat at the table” as health sys-
tems continue to expand and adapt to future public health crises (Fig. 2).
DISCLOSURE
All the authors of this work have nothing to disclose.
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A n t i m i c ro b i a l S t e w a rd s h i p

The increase of carbapenem-resistant Acinetobacter baumannii and pan-resistant

Infect Dis Clin N Am 37 (2023) 669–681

GLOBAL MILESTONES IN STEWARDSHIP

2015 2016 2019

2014 2017 2020

WHAT IS PANDEMIC STEWARDSHIP?

use in hospitalized patients for presumptive community-acquired bacterial pneumonia

Repurposing prospective audit and feedback

Formulary restriction and preauthorization

Participation in Clinical Trials

Allocation of Emergency Use Authorization therapeutics

WHAT ROLE DID ANTIMICROBIAL STEWARDSHIP PROGRAM PLAY DURING THE

WHAT ANTIMICROBIAL STEWARDSHIP PROGRAM METRICS CAN BE APPLIED TO

FUTURE DIRECTIONS BEYOND THE PANDEMIC: NONANTIBIOTIC THERAPIES FOR

Historically, therapeutic approaches to infectious diseases heavily focused on

Original guideline and policy definitions of antimicrobial stewardship described “coor-

Fig. 2. Seat at the table.

commensurate to patient volume and complexity. Future directions of ASPs include

All the authors of this work have nothing to disclose.

1. 2021 Antibacterial agents in clinical and preclinical development: an overview

22. Mathew P, Ranjalkar J, Chandy SJ. Challenges in implementing antimicrobial

39. Cowman K, Rossi J, Gendlina I, et al. Elucidating the role of procalcitonin as a

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