Preparedness and response to an emerging health threat—Lessons learned from Candida auris outbreaks in the United States

Abstract Objective: Candida auris infections continue to occur across the United States and abroad, and healthcare facilities that care for vulnerable populations must improve their readiness to respond to this emerging organism. We aimed to identify and better understand challenges faced and lessons learned by those healthcare facilities who have experienced C. auris cases and outbreaks to better prepare those who have yet to experience or respond to this pathogen. Design: Semi-structured qualitative interviews. Setting: Health departments, long-term care facilities, acute-care hospitals, and healthcare organizations in New York, Illinois, and California. Participants: Infectious disease physicians and nurses, clinical and environmental services, hospital leadership, hospital epidemiology, infection preventionists, emergency management, and laboratory scientists who had experiences either preparing for or responding to C. auris cases or outbreaks. Methods: In total, 25 interviews were conducted with 84 participants. Interviews were coded using NVivo qualitative coding software by 2 separate researchers. Emergent themes were then iteratively discussed among the research team. Results: Key themes included surveillance and laboratory capacity, inter- and intrafacility communication, infection prevention and control, environmental cleaning and disinfection, clinical management of cases, and media concerns and stigma. Conclusions: Many of the operational challenges noted in this research are not unique to C. auris, and the ways in which we address future outbreaks should be informed by previous experiences and lessons learned, including the recent outbreaks of C. auris in the United States.

(Received 22 September 2020; accepted 28 December 2020; electronically published 9 February 2021) Candida auris is an emerging, multidrug-resistant infectious fungus that first appeared in the United States in 2013. 1,2 As of October 31, 2020, the US Centers for Disease Control and Prevention (CDC) had reported 1,518 confirmed clinical cases in 21 states. 3 States that have reported the greatest number of clinical cases include New York (n = 655), New Jersey (n = 195), Illinois (n = 397), Florida (n = 100), and California (n = 102). 3 Cases have also been reported in several other countries. 3 To date, C. auris has been primarily identified in healthcare settings, including hospitals and postacute and long-term care facilities that care for long-term ventilator-dependent patients. It can be transmitted person-to-person (eg, by poor hand hygiene) and through contact with contaminated surfaces or sharing of contaminated equipment. 1 It is extremely persistent in the environment, and meticulous disinfection and infection prevention and control procedures are required to prevent transmission.
Candida auris can colonize a variety of different body sites; it is identified via screening protocols, such as swabbing key body sites for clinical laboratory analysis. Although those who are colonized do not have active infection (ie, they are asymptomatic), the organism is still capable of spreading throughout the environment and the person is at risk for developing invasive candidiasis. Those at risk for C. auris colonization and infection (ie, invasive candidemia) include people who have weakened immune systems, live in long-term care settings, have invasive long-term medical devices, and are on broad-spectrum antibiotics and antifungals. 1 The CDC estimates that between 30% and 60% of those with invasive C. auris infections die, but this statistic is based on limited cases and may not capture other risk factors or comorbidities that might increase the risk of death. 1 Although the number of health facilities that have had direct experience with this organism is relatively limited, the incidence of C. auris infections and outbreaks continues to rise across the United States. Thus, healthcare facilities that care for vulnerable populations must improve their readiness to respond to C. auris. To inform efforts to prepare for and respond to C. auris cases in health facilities, we conducted interviews with healthcare facilities, organizations, and public health departments in New York, California, and Illinois that have responded to cases and outbreaks of C. auris. The purpose of this research was to identify and better understand challenges faced and lessons learned to better prepare healthcare facilities who have yet to experience or respond to C. auris.

Methods
Semi-structured interviews were conducted with staff from healthcare facilities, public health departments, and healthcare organizations in New York, California, and Illinois from October 2019 to January 2020. One interview was also conducted with an epidemiologist from the CDC who was involved in the response in one of the locations. Prior to the interviews, a nonsystematic literature review was conducted to identify existing literature and reports on C. auris and associated challenges with preventing, detecting, reporting, and treating this emerging fungus. A preliminary meeting was also conducted between the Johns Hopkins research team and their partner, New York City Health þ Hospitals, to also identify potential interview topics of interest. These helped to inform the drafting of a semi-structured interview script (Appendix A online), which was used to help guide the interview process but was not strictly adhered to.
Potential facilities were contacted by both the Johns Hopkins University Center for Health Security and New York City Health þ Hospitals partners. The facilities then self-identified relevant personnel for the study based on their involvement in C. auris outbreak preparedness and response activities. Potential interviewees were also identified through the nonsystematic literature review and through snowball sampling. Recruitment commenced when thematic saturation was reached.
In total, 25 interviews were conducted with 84 participants. Although some interviews took place with a single person, others were conducted as a larger group. Interviewees included staff from health departments, long-term care facilities, hospitals, and healthcare organizations located primarily in New York, which has seen the greatest burden of C. auris cases (Table 1). Additional interviewees from California and Illinois were also recruited, as both states have experienced C. auris outbreaks. Participants covered a vast range of expertise, including infectious disease physicians and nurses, clinical and environmental services (EVS), hospital leadership (eg, director of nursing), hospital epidemiology, infection preventionists, emergency management, and laboratory scientists. All interviews were jointly led by 2 interviewers (D.M. and J.B.N.). Interviews were conducted on a not-for-attribution basis, meaning that no comments were directly attributable to a person or organization. Notes and audio recordings were taken during each interview with the participant's consent.
After completion of the interviews, all notes were coded using NVivo qualitative coding software. A thematic coding framework was developed prior to the coding process using the interview guide, with the addition of interview themes that had arisen during the interviews. Each interview was coded by 2 of the authors (D.M. and E.M.), and the coding results were then analyzed by the Johns Hopkins authors (D.M., E.M., and J.B.N.). Emergent themes were then iteratively discussed amongst the Johns Hopkins authors and their New York City Health þ Hospitals partners to identify lessons learned and challenges faced that might help inform other's preparedness and response efforts to C. auris or other similar emerging infectious diseases.
This research was determined to not be human subjects research by the Johns Hopkins Bloomberg School of Public Health Institutional Review Board.

Results
Each of the thematic areas that emerged in the interviews are summarized below. Key lessons learned are highlighted in Table 2.

Surveillance and laboratory capacity
Candida auris surveillance policies varied among the facilities interviewed. Many facilities conducted point prevalence surveys and environmental sampling of high-touch surfaces to determine C. auris presence within the facility. Facilities also conducted a variety of different screening mechanisms to identify potential cases, including within the emergency department and the intensive care units. Screening questions often included whether the individual had a history of hospitalization overseas, history of infection with a multidrug-resistant organism (MDRO), or whether they currently had a medically invasive device. Another facility noted that they were not conducting active surveillance cultures but that they had started speciating all yeasts (including those obtained from nonsterile sites) to make sure that C. auris cases were not going unrecognized. Most facilities agreed that screening protocols should be tailored to match the risk of the population served. For example, one facility noted that a blanket-wide screening protocol for C. auris is not necessary because the disease is relatively rare and that knowing the population well (eg, those who engage in medical tourism) may help identify those at higher risk for infection who should be screened.
Lack of laboratory capacity to test for C. auris was also noted as a limitation. Key informants spoke of the "double-edged sword" of surveillance, where increased surveillance could improve case detection, decrease transmission, and potentially improve clinical outcomes. However, they added that it could also strain healthcare resources, including bed, isolation, laboratory, and staffing capacity. Additionally, few facilities had the ability to conduct on-site PCR testing. Instead, they had to send samples to state public health laboratories. Some facilities isolated "patients under investigation" in single rooms, which were often in short supply, until their test results came back, which for some facilities took weeks. As a result, patients were often discharged before their test results came back. Enhanced surveillance also inherently meant enhanced detection of colonized individuals, who were often more difficult to discharge to long-term care facilities.

Inter-and intrafacility communication
Lack of communication around patient colonization status was a challenge, according to key informants. In some instances, individuals who presented for care did not divulge their status because they did not know that they had C. auris. Others spoke of communication challenges when accepting or discharging colonized patients, particularly between facilities that were in different healthcare systems that did not utilize the same electronic medical record (EMR) system. Occasionally, information on C. auris status was intentionally left out because some facilities would otherwise refuse admission of that patient. Notifying emergency medical system transport about a patient's status was also identified as a gap.
To address these communication challenges, one facility educated its transfer center nurses to ask about previous isolation precautions when getting in-coming patient histories and paged the on-call infection preventionist when a positive C. auris history was identified. Others used the CDC infection control transfer form to communicate isolation history or flagged it in the patient's EMR. One health department shepherded colonized patients from facility to facility (ie, conducted follow-up phone calls), recognizing that they had not found a method for facilities to track this information on their own. Another facility made identification cards for discharged patients to bring with them the next time they needed to get medical care. Finally, a close network of infection preventionists and other infection prevention and control (IPC) staff was highlighted as critical to communication and information exchange between different facilities regarding C. auris status.
Although they are not currently in use, most key informants believed that the creation of state-level databases that could track individuals who had previously been identified as being colonized with C. auris would be extremely useful. One state had implemented a similar database to track infections with MDROs, so there was a precedent for this kind of repository. However, limitations remained, including the funding required to establish this system and the inability to track patients across state lines.

Infection prevention and control
Infection prevention and control was an issue presented across all facilities, which often implemented stringent IPC guidelines like those used for Clostridoides difficile. Facilities implemented a range of interventions including just-in-time training for clinical and nonclinical staff, tailored to the specific needs of different healthcare worker roles. Some facilities also implemented additional interventions such as computer screen savers and signage to remind staff of measures that needed to be taken when caring for C. auris patients. Facilities repeatedly emphasized that the key to preventing C. auris transmission was "bread and butter infection control": cleaning and disinfection, diligent hand hygiene, and personal protective equipment. Wherever possible, facilities tried to reduce other responsibilities for staff caring for C. auris patients to assure adequate time to comply with the additional IPC measures that were put into place. Infection prevention and control was particularly challenging in the long-term care setting due to lack of dedicated IPC staff, fewer resources for EVS, and high staff turnover.
In the outpatient setting, facilities reported the need for coordinated logistics in scheduling colonized patients to ensure that proper IPC measures could be taken. Facilities recommended scheduling patients as "last of the day" or planning for a room to be out of use after the patient was seen to ensure adequate cleaning. In the outpatient setting, the biggest barrier to implementing proper IPC was knowing the status of the patient. Additional education with patients and families around notifying new facilities of colonization status to allow for implementation of IPC measures was important.

Environmental cleaning and disinfection
Facilities implemented additional training for staff who cleaned C. auris rooms, dedicated certain staff and equipment to these rooms to enable more time for cleaning, and used disposable supplies wherever possible. Some facilities implemented additional technologies, such as vaporized hydrogen peroxide after routine cleaning and disinfection and ATP environmental surface sampling, to ensure that cleaning and disinfection were completed appropriately. Emphasizing that cleaning assessments were nonpunitive was noted as key to earning buy-in from staff and to improved communication Additional guidelines on surveillance within acute, sub-acute, and long-term care facilities for Candida auris are needed and should be adaptable to local epidemiological contexts. Increased local laboratory capacity is needed to test for C. auris so that screening can be enhanced. Specifically, this will require the training of additional laboratory technicians, who are already in short supply.
Infection prevention and control Follow basic infection prevention and control principles (eg, hand hygiene, PPE use) because they will prevent spread of C. auris. Additional guidelines are needed on the disinfection of mobile equipment (eg, ultrasounds), as federal and other guidelines often conflict with manufacturer's recommendations. Have dedicated staff (including clinical and support staff) take care of colonized patients to decrease the chances of further nosocomial transmission. Conduct regular "huddles" to discuss patient isolation status. EVS and other support staff who directly interact with patients should be included. Reduce internal movement of C. auris patients as much as possible (eg, bring ultrasound to patient) and as last case of the day for procedures to enable more time for cleaning and disinfection.
Communication between facilities A state-level database would be helpful in tracking individuals who have been identified as being colonized with C. auris. Universal transfer forms that include C. auris colonization status should be utilized, and these should be integrated with existing electronic medical records (including inpatient and outpatient).
Education and communication Facilities should use consistent and evidence-based messaging to communicate about C. auris with their staff. Just-in-time training should be conducted to educate staff about C. auris and the precautions necessary to prevent its spread (eg, decontamination, PPE donning and doffing). Programs should be combined with structural changes to support behavior change. Balancing emphasizing the importance of this emerging infection without inducing fear and panic among staff.
Note. PPE, personal protective equipment; EVS, environmental services. and collaboration between frontline staff and management. Some facilities collaborated with state and local health officials to conduct cleaning and disinfection assessments of high-touch surfaces to ensure patient safety and better understand the dynamics of how C. auris persists and moves through the environment.
Tailoring education and training for EVS staff required a balance of emphasizing the importance of diligent cleaning and disinfection, the threat posed by C. auris, and the significance of their roles, without inducing fear among staff. In addition, care needed to be taken to ensure that frontline EVS staff received training in a way that they understood and was cognizant of potential language barriers. High staff turnover and understaffing was also noted as a challenge, creating a barrier to having dedicated EVS staff for rooms occupied by patients either infected or colonized with C. auris. One facility suggested an "EVS staff-to-patient" staffing ratio, like current regulations and requirements for nurse-topatient staffing ratios.

Clinical management
Clinical care of patients was not a significant challenge for patients at the facilities interviewed. Patients who were clinically infected were noted to be critically ill due to other comorbidities; therefore, the only additional treatment required was an antifungal. Facilities did note concerns regarding the potential occurrence of pan-resistant organisms, but they had not encountered a clinical case for which there were no treatment options. Clinical management did become a challenge when the site of C. auris infection was not the bloodstream due to poor penetration of echinocandins. Clinicians did not recommend cohorting C. auris patients due to disruptions in workflow and concern for polymicrobial colonization of patients contributing to nosocomial spread of MDROs.

Media concerns and stigma
Media attention around C. auris created concern and stigma for facilities caring for patients who were colonized or infected because nosocomial spread was often associated with poor IPC measures. In one state, information on what facilities had C. auris patients was released to the public by the state health department. This, coupled with poor communication around the true risks of C. auris to the general population and the lack of distinction between C. auris colonization versus infection, further propagated fear in the community and stigmatized facilities. Interviewees noted that the disclosure of which facilities had C. auris patients was not tied to additional resources, so it felt very punitive. Additionally, some acute-care facilities found it difficult to discharge patients with C. auris colonization to subacute facilities, leading to unnecessarily long lengths of stay.

Discussion
Long-term care facilities care for some of the nation's most vulnerable populations, who are often elderly and suffer from a variety of underlying illnesses that put them at increased risk for infection. Unfortunately, these facilities often lack the infection prevention measures that are critical to reducing disease transmission, and they have been implicated in numerous disease outbreaks, including respiratory, gastrointestinal, and skin and soft-tissue infections. 4 For example, 61% of nursing home IPC managers who responded to a 2016 survey reported having no specific IPC training. 5 Additional training within these facilities pertaining to infection control, as well as addressing other challenges that might facilitate disease transmission, such as understaffing, could help prevent outbreaks of C. auris and other highly transmissible diseases.
Hospitals noted having limited tools to prevent C. auris transmission within their facilities. Colonized patients may be transferred from a long-term care facility or present via emergency departments without accompanying documentation of C. auris history, thereby preventing prompt isolation and increasing the risk for interfacility transmission. Furthermore, limited internal testing capacity for patients with an unknown history or potential active infection creates the possibly for transmission and environmental contamination before it is recognized. Expanded access to testing and the creation of a case registry that would enable facilities to search for a patient's colonization status may help to limit introduction and spread of C. auris in hospitals.
Media reporting around outbreaks and cases of C. auris in one state created challenges for health facilities. Efforts to disclose those facilities at which patients tested positive for C. auris was thought to stigmatize health facilities that had cases and created disincentives for others to accepting patients with a positive colonization history. Additional research on the true prevalence of C. auris colonization within the community could help reduce this stigma. Efforts to more clearly communicate about the case fatality rate of C. auris should also be undertaken, which can help clarify the broader risk to the general public.
Incentivizing long-term care facilities to accept patients with C. auris colonization history through Medicare or Medicaid reimbursements could help allay challenges in identifying postacute care options for patients. Additionally, identifying funding mechanisms to support emergency preparedness and response efforts within long-term care facilities could also help improve the readiness of these facilities for disease outbreaks like C. auris. For example, funding provided via the Assistant Secretary of Preparedness and Response's Hospital Preparedness Program has previously been used by New York City to build emergency response capabilities, including training on emergency management fundamentals, logistics, and resident evacuation. 6 Additional research is needed to better understand how to prevent C. auris outbreaks in healthcare settings. An estimated 1.5 million people die each year from fungal diseases, a threat that has "been continually neglected over the years despite their alarming impact on human health." 7 Unfortunately, lack of funding has stymied the research and development of tools needed to prevent, detect, and treat fungal infections. 8 For C. auris and other invasive fungal infections, additional research is imperative to better understand disease prevalence and epidemiology, to identify best practices for infection control, to understand case fatality, and to develop rapid diagnostics and new antifungals. 8,9 This study has several limitations. Some of the interviews were conducted in groups, which may have biased individual's responses to the interview questions. Additionally, the results of this study may not be generalizable to all facilities. However, we do believe that many of the operational challenges noted in this research are not unique to C. auris. The need for improved disease surveillance, increased testing capacity, enhanced infection prevention and control measures, and prompt risk communication is generalizable to other emerging infectious diseases. The ways we address these and other challenges that might emerge in the future should be informed by previous experiences and lessons learned responding to other outbreaks, including the recent outbreaks of C. auris in the United States.