Advancing health equity through action in antimicrobial stewardship and healthcare epidemiology

Health equity is the state in which everyone has a fair and just opportunity to attain their highest level of health. ¹ Health inequities occur when unfair processes in the distribution of resources affecting health disproportionately prevent the attainment of that highest level of health in specific populations. ^2,3 Health inequities are pervasive and lead to differential patient outcomes for a variety of disease states, ranging from chronic diseases like Type 2 diabetes mellitus and hypertension to infections like coronavirus disease-2019 (COVID-19). ¹ Infection risk in health care and quality of antibiotic use vary by patient population. ^4–17 Thus, opportunities exist for education and awareness about health equity and how it applies to infectious diseases, healthcare epidemiology, and antimicrobial stewardship. To underscore the importance of preparing the healthcare workforce to understand, recognize, and respond to health inequities, Uehling et al ¹⁸ asked >200 hospital employees to describe their understanding of health equity as a concept, and perceptions of equity initiatives implemented in their hospital. In the results of their survey, published in 2023, <25% of respondents could correctly define either health equity or equity at a broader level. ¹⁸ Understanding definitions of health equity terminology can be an important first step toward identifying and differentiating health disparities and inequities occurring in our field (Table 1). However, clinicians and researchers need to move beyond mere documentation toward identification, investigation, and mitigation of these upstream drivers leading to the observed disparities. The purposes of this commentary are (1) to provide context for why health equity is important in healthcare epidemiology, infection prevention, and antimicrobial stewardship and (2) to share action steps for individuals, institutions, and health systems.

Table 1. Definitions of Health Equity Terminology ^a

^a For additional definitions visit the CDC National Center for Chronic Disease Prevention & Health Promotion, NCCDPHP Health Equity Glossary. (https://www.cdc.gov/chronicdisease/healthequity/health-equity-communications/nccdphp-health-equity-glossary.html, last reviewed December 8, 2022, and accessed November 6, 2023).

How social determinants of health (SDOH) interact to cause and exacerbate disparities within infectious diseases

Social determinants of health (SDOH) are defined as the nonmedical factors that influence health outcomes including (but not limited to) education quality, economic stability, neighborhood, housing environment, and healthcare access. ¹⁹ Many disparities observed in clinical outcomes among patients from minoritized backgrounds are likely driven by inequities in these factors, as well as additional systems of oppression that may themselves be considered separate SDOH (ie, racism, homophobia, ableism, sexism, and ageism). ²⁰ These factors can influence patient outcomes from infectious diseases.

For example, differences in access to quality educational opportunities can contribute to lower levels of literacy, which can severely affect the degree to which individuals can find, understand, and use information to inform their health-specific literacy or health-related decision making. ^21–23 More than 80 million American adults have low health literacy, with disproportionately higher representation among older adults and people from racially and ethnically minoritized backgrounds. ²³ Historical racial residential segregation has played a significant role in these inequities due to artificial limitations on quality educational access and in some cases, poorly funded education systems. Moreover, the specter of racism in healthcare with historical and contemporaneous medical mistreatment has resulted in justified healthcare mistrust across communities of racially and ethnically minoritized backgrounds. Several examples are well-known, such as the US Public Health Service–funded study of untreated syphilis in Black men at the Tuskegee Institute, the unauthorized retrieval and profits from the use of Mrs. Henrietta Lacks’ cervical cells without her consent, and the compulsory sterilization of Native American women at Indian Health Services hospitals. ^20,24,25 This mistrust can interfere with health literacy development because it can influence interactions with access to healthcare-related resources and overall health decision making. ^26,27 For example, during the COVID-19 pandemic, people from racially and ethnically minoritized backgrounds were disproportionately represented in rates of disease, hospitalization, and death from SARS-CoV-2, yet, once vaccines were available, these groups were the least represented among persons who received the COVID-19 vaccine. ^28–30 Higher reliance on social media as a source of COVID-19 education was noted among people from racially and ethnically minoritized groups, and widespread misinformation and disinformation campaigns on these platforms may have resulted in compromised health literacy, adversely impacting healthcare decision making. ³¹

Furthermore, inadequate options to appropriately communicate with individuals with limited English proficiency also compromise health literacy and negatively influence outcomes for those patient populations. Individuals with limited English proficiency experience barriers to accessing healthcare coverage, which may delay treatment seeking and the receipt of appropriate care. ³² These inequities likely have major downstream effects, including longer emergency room visits and hospital admissions in pediatric and adult patients who speak a language other than English. ^33,34 Differences in infection prevalence, due to language barriers, have also been observed among pediatric populations. Higher rates of central-line–related bloodstream infections (CLABSIs) have been documented in pediatric patients with limited English proficiency. ³⁵ Reducing the negative impacts of language barriers in infection prevention and antimicrobial stewardship is essential for HAI prevention, especially given the importance of patient education (eg, preoperative chlorhexidine bathing or wound care and antibiotic education at patient discharge). ¹²

Biases in hiring policies and practices as well as inequities in access to quality education and lower rates of advanced education result in a disproportionately high representation of individuals from minoritized backgrounds in low-wage employment. These biases likely contribute to the disproportionate high levels of social and economic vulnerability, including low socioeconomic status (SES) observed across groups from minoritized backgrounds, compared with individuals from privileged backgrounds less harmed by racism. ³⁶ Because employment guides monetary income, and income is required for housing, higher proportions of people from racially and ethnically minoritized backgrounds reportedly live in multigenerational or overcrowded housing, which may facilitate infection transmission through close contact. ²⁰ This situation was highlighted during the COVID-19 pandemic. People from racially or ethnically minoritized backgrounds were more likely to work in lower-income healthcare personnel roles (eg, certified nursing assistants and medical assistants) and were at higher risk of contracting COVID-19 due to presumed increased exposures in either or both work and nonwork settings. ¹⁶

Low SES can influence access to healthcare, which further exacerbates disparities in infectious diseases. For example, disproportionate rates of Clostridium difficile infection (CDI) have been frequently reported in individuals who reside in areas of low SES when compared to those who live in areas of higher SES. ^37–39 People who are uninsured or underinsured may experience challenges that hinder their ability to receive care for the management of chronic illnesses, which may subsequently increase their risk of infectious complications. ⁴⁰ Patients from racially and ethnically minoritized backgrounds who were diagnosed with CDI at a hospital serving primarily low SES communities were more likely to be under- or uninsured. ⁸ They were also more likely to have been diagnosed with diabetes and chronic kidney disease (CKD), and a pre-existing CKD diagnosis contributed to the increased odds of severe CDI seen in minoritized patients. ⁸ This gap will likely continue to widen as areas of low SES are less likely to have an adequate number of healthcare resources and/or professionals to provide necessary services.

Challenges with identifying and mitigating health inequities in infection prevention and antimicrobial stewardship

Several challenges exist in identifying and mitigating health inequities in infection prevention and antimicrobial stewardship. These can be broadly grouped into themes including (1) diversity of the healthcare workforce and patient access to clinicians, where many minoritized communities are underrepresented, and (2) challenges with availability and quality of data, affecting patient care and community health outcomes.

Challenges with healthcare workforce diversity and access

Patient–clinician cultural concordance can promote positive clinical outcomes, demonstrating that a diverse healthcare epidemiology, infection prevention, and antimicrobial stewardship workforce is essential to mitigate health inequities and serve diverse populations. ⁴¹ Black, Hispanic/Latino, American Indian/Alaska Native, and Native Hawaiian/Pacific Islander individuals are underrepresented as trainees and practicing physicians in the United States relative to their census demographics. ^42–45 Furthermore, individuals with these minoritized racial and ethnic identities are underrepresented in leadership positions, ⁴⁴ have fewer speaking opportunities at national conferences, ^46,47 and experience lower pay. ⁴⁸ Intentional efforts to address leadership and speaking opportunities for women have led to improvements in gender equity ^44,46,49 ; however, gaps remain related to pay ⁴⁸ and promotion. ^50–52

Many of these gaps reported for physicians undoubtedly exist for other healthcare team members such as pharmacists, infection preventionists, advanced practice clinicians, etc; however, data from these professional groups are sparse. ^53–56 Furthermore, there is a dearth of data describing the contribution and impacts of infectious disease healthcare workers from lesbian, gay, bisexual, transgender, queer and nonbinary gender (LGBTQ+) communities or healthcare workers with disabilities. To address these gaps, medical societies can commit to identifying and mitigating these workforce inequities through coordinated strategies, ^46,47 ranging from intentional recruitment to retention and recognition. Concurrent with existing efforts to inspire interest in infectious diseases (ID), pathway programs (starting as early as elementary school) can expose young learners to ID careers, and their development and execution should be intentional to ensure that individuals from backgrounds historically excluded have access to these career opportunities. ⁵⁷

Ensuring an adequate workforce serving rural and community hospitals is also necessary. Patients in smaller community hospitals, particularly in the Southeastern United States, were disproportionately affected by CDI, catheter-associated urinary tract infections (CAUTIs), and CLABSIs during the height of the COVID-19 pandemic. ⁵⁸ Children living in rural counties (compared to children living in urban counties) have increased rates of inappropriate antibiotic use. ⁵⁹ To address these geographic differences in HAIs and antibiotic prescribing quality, improving access to ID expertise (local or telehealth) is warranted to serve smaller rural community hospitals. ⁶⁰ Academic healthcare facilities are often overrepresented in research, limiting the generalization of published data, with inadvertent exclusion of rural populations. In a survey assessing collection of SDOH data as a routine part of HAI surveillance in US-based hospitals, 7 (27%) of 26 responding facilities represented community hospitals and only 4 (16%) included public and federal hospitals. ¹⁰ Furthermore, of the responding facilities, only 1 (4%) of 26 responding facilities were from Western states (11 were from Southern states), which likely influenced the inclusion of indigenous persons living in Western states in these studies. Only 8 (30%) of 27 facilities collected SDOH patient variables and, of these 8 facilities, 7 (88%) were academic centers. ¹⁰ More than 70% of US hospitals have <200 beds, and many of these facilities serve communities in need and those from minoritized communities. ^11,61

Inclusive cultures must be developed and fostered during health professions training and patient care, ^43,45,62 as well as through intentional assembly of healthcare epidemiology–infection prevention–antimicrobial stewardship teams to include intersectional identities. Unconscious or implicit bias describes “associations or attitudes that reflexively alter our perceptions, thereby affecting behavior, interactions, and decision making,” ⁶³ and can contribute to inequities in antimicrobial stewardship. In one study, female antimicrobial stewardship pharmacists were less likely to have their antibiotic recommendations accepted by prescribing clinicians than male antimicrobial stewardship pharmacists. ¹⁴ Approaches to counter unconscious bias are multidimensional; however, at the core they operate in conjunction with methods to increase diversity, equity, and inclusion, which includes diversifying the healthcare workforce. ^44,63

The case for supporting equity, diversity, inclusion, and access in the antimicrobial stewardship and infection prevention workforce is multifaceted. In addition to greater opportunity for clinician–patient concordant relationships, some data have demonstrated that diverse teams function better and are more successful in research. ⁶⁴ Diverse teams produced more innovative research and published in higher-impact journals, which may allow for an increase in the dissemination of the innovative findings. ⁶⁵ Importantly, addressing healthcare workforce inequities contributes directly to improved patient care. ⁶⁶

Challenges with availability and quality of data

Medical research typically captures demographic information on sex, age, race, and ethnicity, but addressing inequities is rarely the objective, which prompted a call to expand the literature evaluating inequities in HAI incidence. ^17,67,68 In a scoping review of health-equity antibiotic prescribing studies, only 23% of studies reported a specific equity objective, whereas 48% of the included studies reported patient or prescriber characteristics. ¹⁷ Among studies reporting any health equity markers, people from racial and ethnic minoritized groups were less likely to receive antibiotics overall ^15,69 or were less likely to receive firstline antibiotic treatment. ⁷⁰ Further disparities were observed based on geographic location, with higher antibiotic prescribing in southern regions ⁷¹ and rural areas. ⁵⁹ Additionally, socioeconomic status also influenced equitable prescribing; privately insured people were more likely to receive antibiotics compared with the uninsured. ⁷² Despite these disparities, research regarding potential drivers (or upstream causes) of observed disparities is lacking. ¹⁷

Recent studies have evaluated disparities related to multidrug resistance, infection prevention efforts and outbreak response, HAIs, and specific conditions, including candidemia, CDI, and COVID-19. ^{4–8,12,13,16,35,73} Data regarding health inequities in inpatient antibiotic prescribing are very limited. Kim et al ¹⁷ reported that 55 (90%) of 61 articles in their scoping review described outpatient settings and only 1 (1.6%) was from the acute-care setting. Their review also noted very few stewardship intervention studies, only 4 (6.6%) of 61 studies. ¹⁷ Considering that patients who are uninsured and underinsured often do not have access to outpatient clinics and may use the emergency department or hospital as their only form of healthcare, the lack of published data in the inpatient setting is a significant limitation in the consideration of health inequities in antibiotic prescribing.

As researchers evaluate these disparities, even within what many consider to be basic demographic variables, they must be aware of how they are collecting the information and what methodologic biases may be introduced. For example, age is quantifiable, but age stratification (eg, who are considered “older adults”) and how disparities in infection incidence and antimicrobial use affect various age categories are all important considerations for researchers. Accurate identification of sex, race, and ethnicity is also key for both clinicians and researchers. Gender identity and biological sex are different constructs, and knowledge of both are necessary not only to provide high-level medical care but also to perform quality research, especially when disparities might exist among different groups. ⁷⁴ Clinicians and researchers also tend to make assumptions about race and ethnicity that may not align with their patients’ and study participants’ self-identified race and ethnicity, especially when these characteristics are limited to finite categories. ⁷⁵ Such assumptions can affect the care these patients receive if clinicians’ implicit racial biases translate into decision making either consciously or subconsciously and can in turn affect study analyses on racial disparities in infectious diseases. Race and ethnicity are sociopolitical, not biological constructs; therefore, they should not be used in clinical practice to make inferences about physiologic function. Care should be taken in research to understand structural barriers causing racialized disparities rather than assigning race itself as a risk factor. ^76–79

Finally, some SDOH variables are often not collected or are overlooked in medical research, such as disability status and housing or food insecurity. The charge to incorporate such variables into medical research extends beyond the individual clinician and researcher. Regulatory and government agencies should consider these when determining standard metrics for reportable infectious diseases and conditions. The National Healthcare Safety Network (NHSN) captures HAI and antimicrobial use data from acute and postacute care facilities. ⁸⁰ HAI case reporters can include race and ethnicity data, but the field is optional. The antimicrobial use module captures only aggregate facility-level or unit-level information. Although this information may be helpful to assess facility-level interventions, analysis of disparities in care or prescribing based on age, gender, race, or ethnicity cannot be performed.

Next steps and call to action

Prioritizing elimination of healthcare disparities requires individual, institutional, and public health level interventions. Here, we provide actionable recommendations for mitigating the equity gaps at each level (Fig. 1).

Figure 1. Actions for individuals, institutions, and public health organizations to mitigate impacts of health inequities.

Individuals

A starting point for clinicians is an urgent commitment to creating a culture of equity and inclusion in healthcare spaces (Fig. 1). To create environments that provide patients and staff with what they need to succeed through a lens of equity, thorough assessments of individual practices should be conducted to determine areas of greatest need. For example, Fortin-Leung et al ⁸¹ raised questions about the paucity of race and ethnicity data built into antimicrobial stewardship programs. Acknowledging that patient-level characteristics from birth to death can affect antimicrobial prescribing, use, and administration, they suggested that prescribers could seek to understand how cultural differences along racial, ethnic or gender lines affect nonprescription antibiotic use, medication adherence, and drive differences in prescribing behavior.

Because SDOH may have varying impacts on patient health, healthcare personnel should intentionally seek out education on the impact of SDOH and SES on patient health. ⁴ Healthcare professionals remain the most trusted sources of health information in our current era of declining health literacy and access to high-quality health information. Staying appropriately informed can help clinicians maintain this trust and properly advocate for patients. Patient advocacy may be strengthened by recruiting and retaining a diverse workforce. Through mentorship and sponsorship for people from different backgrounds, healthcare personnel can prioritize support for successful career advancement.

Organizational

Healthcare systems and facility leadership are responsible for creating a culture of equity in their institutions. ⁸² Steps to be taken at institutions include the following: (1) assessing whether care delivery is equitable; (2) prioritizing quality improvement interventions that address differential care delivery; (3) providing high-quality health equity and implicit bias training for healthcare professionals; (4) leveraging data for individual-level clinician feedback on health equity measures; and (5) making public statements of goals and actions to improve equity, in addition to internal commitments (Fig. 1). For example, during the COVID-19 pandemic, infectious disease, and antimicrobial stewardship leadership at one hospital recognized that access to monoclonal antibody infusion for COVID-19 management was inequitable. They leveraged an emergency department fast-track location and existing staff to make the treatment available for an underserved community. ¹¹

Sustainable measures to mitigate disparities require accountability. Public and private institutions, including societies dedicated to healthcare epidemiology and antibiotic stewardship, have made public declarations of diversity equity and inclusion commitments. ^83,84 Yet, without high-quality data collection and publicized data reviews, accountability may not be feasible for health systems. ¹⁰ Additionally, the validity of SDOH, race, and ethnicity data entered into the electronic health record (EHR) have often been called into question, creating challenges for collecting and interpreting HAI inequity data. ⁷⁵ However, interventions to correct these patterns might have limited impact in the absence of data validity tools for EHR systems to capture accurate data points. Despite these challenges, healthcare institutions can still develop anchor missions focused on addressing inequities for their local communities. For example, a Chicago-based health system crafted a multipronged framework that named racism and poverty as targeted causes of inequities. They embarked on a health equity mission to invest locally, collaborated with their surrounding community across all care spectrums, and they developed performance improvement plans to improve their patient outcomes. ⁸⁵ The level of commitment to equity may not be replicable for every institution, but we recommend that institutions identify and tackle a singular equity mission that is achievable and feasible within an established timeline. Healthcare system and facility leadership should be purposeful in recruiting a diverse and skilled workforce in healthcare epidemiology, infection prevention, and antimicrobial stewardship. Institutions can frequently conduct equity reviews and proactively correct identified deficiencies.

Public health systems

Public health engagement at the federal, state, and local levels is needed to address health inequities (Fig. 1). National, state, and community policies, structural inequities, and differential access to reliable information sources are important factors. The COVID-19 pandemic revealed the need for future public health initiatives to address systematic inequalities that can perpetuate and lead to differences in population and individual outcomes. ⁹ Action steps for public health include the following: (1) requiring surveillance and research activities that include health equity objectives and capture the needed data to support decision making and implementation science to address inequities; (2) providing necessary analytic resources to help characterize health inequities at the national, community, healthcare system, and facility levels to provide a compass for where action is needed; (3) communicating health information effectively to a variety of different audiences and health literacy levels; (4) facilitating access to subject matter expertise in healthcare epidemiology, infection prevention, antibiotic stewardship in health departments across the country; and (5) incorporating a health equity lens into guidance and policies for healthcare epidemiology, infection prevention, and antibiotic stewardship implementation. Regulatory and accreditation partners, such as The Joint Commission, can facilitate policy change. For example, in 2023 new health equity standards were released by The Joint Commission to establish a new baseline of equitable delivery of healthcare. ⁸⁶

In conclusion, inequities in healthcare occur at every resource level. Steps to advance health equity should be considered at every level, whether a well-resourced health system or a rural critical-access hospital. Advancing health equity includes delivery of safe and equitable patient care and recruiting individuals with diverse backgrounds to healthcare epidemiology, infection prevention, and antimicrobial stewardship career paths.