Discussion

In this mixed-methods study of the first 140 C. auris case-patients identified in the state of Maryland, we found both individual-level and facility-level indices of neighborhood socioeconomic vulnerability to be associated with C. auris. Case-patient residence in SNFs and presence of wound(s) were frequent, and infection control deficiencies in SNFs were identified.

In our individual-level analysis of neighborhood characteristics of C. auris case-patients in Maryland, we found that this cohort belonged to neighborhoods that are less insured, have lower socioeconomic status and higher concentrations of racial/ethnic minorities, relative to the Maryland average. Similarly, 28% of case-patients resided in neighborhoods that were in the top quintile of deprivation by the ADI, a measure that describes socioeconomic disadvantage. However, it is unclear if these findings of somewhat higher socioeconomic vulnerability relative to the state average are specific to the case-patients’ C. auris status or represents individuals with healthcare contact.

For methicillin-resistant Staphylococcus aureus (MRSA), neighborhood characteristics such as poverty, lack of education, and access to health care at the census tract level are associated with racial disparities in MRSA infections. ^{Reference See, Wesson and Gualandi15} Neighborhood deprivation and socioeconomic disadvantage have also previously been linked to increased risk of readmission and frequent contact with healthcare facilities which are risk factors for C. auris. ^{Reference Kind, Jencks and Brock16}

Prior research has shown that individual-level patient characteristics, such as membership in marginalized groups that experience structural racism and ageism, contributed to poor health outcomes during the COVID-19 pandemic in SNFs. ^{Reference Abrams, Loomer, Gandhi and Grabowski17} More research needs to be done to understand the role of individual risk factors in addition to the neighborhood risk factors that may contribute to multidrug-resistant organism (MDRO) transmission.

When evaluating socioeconomic vulnerability at the facility-level, we found that one-third of all SNFs were in areas with severe disadvantages. In addition, SNFs in neighborhoods with lower socioeconomic status and high numbers of racial minorities were more likely to experience C. auris transmission. Prior research shows that SNFs in socioeconomically disadvantaged neighborhoods have less staff, lower quality ratings, and more financial strain. ^{Reference Falvey, Hade and Friedman8,Reference Yuan, Louis, Cabral, Schneider, Ryan and Kazis18,Reference Park and Martin19} Future research should clarify the relationship between SNF neighborhood socioeconomic disadvantages and differential environmental exposure or built environment that could contribute to MDRO outbreaks and infection control deficiencies.

Our findings on the clinical characteristics of C. auris case-patients are similar to those from previous studies that showed most patients infected or colonized with C. auris had multiple comorbidities. ^{Reference Eyre, Sheppard and Madder4,Reference Adams, Quinn and Tsay20} Particularly, patients were noted to require ventilation, central lines, wound care, and feeding tubes. Many also had extensive prior contact with healthcare facilities which has been shown to be a risk factor for infection. ^{Reference Rossow, Ostrowsky and Adams2,Reference Caceres, Rivera and Armstrong21} Almost half of Maryland case-patients were directly associated with SNFs. Additionally, C. auris outbreaks disproportionately occurred in SNFs with ventilator-capable units and infection control practices in SNFs with outbreaks had notable deficiencies. Prior research has highlighted the role that long-term care facilities have played in driving transmission in group settings, particularly in ventilator-capable SNFs. ^{Reference Pacilli, Kerins and Clegg22}

ICARs were completed at multiple SNFs with ongoing transmission of C. auris, and common themes emerged. Poor hand hygiene adherence was noted at multiple SNFs and audits were not routinely performed by infection control staff. Many SNFs were not using appropriate disinfectants for C. auris, noting that there was inconsistent access to cleaning supplies throughout the SNF. Staff including environmental services were not always aware of correct cleaning processes and infection control policies. These observations are consistent with prior infection control assessments during C. auris outbreaks and further support the role that strong IPC practices serve in preventing and stopping the spread of infection. ^{Reference Karmarkar, O’Donnell and Prestel5,Reference Aldejohann, Wiese-Posselt, Gastmeier and Kurzai23,Reference Caceres, Forsberg and Welsh24}

We observed that many patients in this study had wounds that required wound care. Prior studies have noted that a substantial proportion of C. auris case-patients had documented wounds. ^{Reference Karmarkar, O’Donnell and Prestel5,Reference Pacilli, Kerins and Clegg22} This prompted attention to wound care practices during infection control observations conducted by the MDH IPC team, and lapses in proper infection control during delivery of wound care were observed frequently. Although the relative contribution of risk of colonization due to the presence of wounds and the risk of transmission due to infection control lapses during provision of wound care remains unclear, these findings are consistent with previous studies on other MDROs and suggest the need for focused attention to wound presence and care. ^{Reference van Buul, van der Steen and Veenhuizen25,Reference McKinnell, Miller, Eells, Cui and Huang26}

This study has several notable limitations. Although we found high comorbidity and higher than expected socioeconomic vulnerability relative to the state average in C. auris case-patients, we did not compare individuals with C. auris to a control group without C. auris. Further, this cohort does not include all case-patients occurring during the period under review; it is likely that additional case-patients of C. auris went undetected due to limitations in existing laboratory or epidemiological methods, and while MDH used an aggressive approach to case-patient finding during this period, this also led to surveillance bias toward increased detection in SNFs with initial case-patients. Despite these limitations, we believe that these data suggest a complex interplay between individual- and facility-level neighborhood vulnerability due to both socioeconomic and medical characteristics (Figure 1). Medical conditions that are risk factors for acquisition of C. auris or other MDROs may be more prevalent in individuals who are marginalized; these individuals may be more likely to be residents of SNFs that are less able to halt the spread of emerging pathogens due to inadequate resources. Therefore, although infection control opportunities can be identified and addressed in real time in response to transmission and outbreaks, these responses may be short-lived and inadequate. That similar risk factors exist for both risk of infection and MDRO transmission across time and geographic regions suggests that unless underlying systemic factors are addressed, we are likely to see limited success in control of these organisms and to see a replacement of one organism with another in the same vulnerable groups. A longer-term approach to preventing infectious disease transmission and emergence will require policy solutions based on a critical evaluation of underlying socioeconomic vulnerability and targeted, commensurate allocation of resources.

Figure 1. Conceptual model of C. auris transmission.