Candida auris is a globally emerging fungal pathogen that has caused outbreaks in healthcare settings. 1 In the United States, C. auris cases have increased dramatically in recent years, with documented spread to 28 states and Washington, DC, by the end of 2022. Reference Lyman, Forsberg, Sexton, Chow, Lockhart, Jackson and Chiller2 Contaminated surfaces and reusable medical equipment have been implicated in transmission. 1,Reference Lyman, Forsberg, Sexton, Chow, Lockhart, Jackson and Chiller2 Therefore, the Centers for Disease Control and Prevention (CDC) recommends thorough cleaning and disinfection of surfaces and shared equipment using disinfectants effective against C. auris. 1 One concern regarding C. auris is that some commonly used disinfectants, particularly quaternary-ammonium products, may have limited efficacy. Reference Cadnum, Shaikh and Piedrahita3–Reference Sexton, Welsh, Bentz, Forsberg, Jackson, Berkow and Litvintseva5
In 2017, the Environmental Protection Agency (EPA) published recommended methods for evaluating the efficacy of antimicrobial products against Candida auris on hard, nonporous surfaces with Antibiotic Resistance Bank (AR) no. 0381 (clade II) as the test strain. 6 In 2021, the EPA published updated testing guidance that included the recommendation that C. auris AR-0385 (a drug-resistant clade IV strain) be used. 7 This change in test organism was based in part on evidence that C. auris isolates from clades III and/or IV might have reduced susceptibility to low concentrations of sodium hypochlorite and ultraviolet-C (UV-C) light in comparison to the clade II isolate initially recommended for standard testing. Reference Sexton, Welsh, Bentz, Forsberg, Jackson, Berkow and Litvintseva5,Reference Pearlmutter, Haq, Cadnum, Jencson, Carlisle and Donskey8 Products demonstrating efficacy against AR-0385 may claim effectiveness against C. auris and drug-resistant C. auris, whereas products demonstrating efficacy only against AR-0381 will only be able to maintain a claim of effectiveness against C. auris. 9 List P provides a listing of antimicrobial products registered with the EPA for claims against Candida auris. Given the rapid spread of C. auris in the United States, including clades III and IV, Reference Lyman, Forsberg, Sexton, Chow, Lockhart, Jackson and Chiller2 data regarding the effectiveness of a wide range of disinfectants used in healthcare settings are needed. In the current study, we tested the effectiveness of 23 disinfectant products used in healthcare facilities against isolates from the 4 major clades of C. auris.
Methods
Test organisms
The C. auris test strains included isolates from 4 phylogenetic clades, including AR-0381 (clade II; East Asia origin), AR-0389 (clade I; South Asia origin), AR-0383 (clade III; Africa origin), and AR-0385 (clade IV; South America origin). Candida albicans American Type Culture Collection (ATCC) strain 10231 was tested for comparison.
Disinfectants tested
The disinfectants that were tested were chosen based on the results of a 2019 survey of a convenience sample of 57 healthcare facilities from 30 states (authors’ unpublished data). All disinfectant brands used in the facilities were tested. All facilities reported use of sporicidal disinfectants in rooms of patients with Clostridioides difficile infection (CDI): 53 facilities used chlorine-based disinfectants and 4 used peracetic-acid–based disinfectants. In rooms of non-CDI patients, 28 facilities (49%) primarily used quaternary-ammonium disinfectants, 17 (30%) used improved hydrogen-peroxide disinfectants, 7 (12%) used chlorine-based disinfectants, and 5 (9%) used phenolic disinfectants. Table 1 shows the characteristics of the 23 disinfectants included in testing, including the active ingredients and recommended contact times for C. auris or Candida albicans.
Table 1. Characteristics of the 23 Disinfectants Tested Against Candida auris and Candida albicans
a Contact time for disinfectants based on manufacturers’ recommendations for Candida auris, or if no claim against C. auris the contact time for an alternative organism was used.
b Environmental Protection Agency–registered claim against Clostridioides difficile spores.
c Environmental Protection Agency–registered claim against Candida auris and alternative organisms used for contact time if no C. auris claim.
d Hydrogen-peroxide disinfectant that has sporicidal activity due to generation of low concentrations of peracetic acid during use (5-min C. difficile claim).
Efficacy of the disinfectants against C. auris
EPA MLB SOP MB-35-03 was used to test the efficacy of the 23 disinfectants against the test organisms. 7 A 3-part soil load containing bovine serum albumin, yeast extract, and mucin was used. 7 For wipe products, the liquid disinfectant was expressed from the saturated wipes for testing. 7 Contact times were based on the manufacturer’s recommendations. Cultures were performed by plating specimens on Sabouraud dextrose agar (Becton Dickinson, Sparks, MD) and incubating them at 37ºC for 72 hours. Log10 reductions were calculated by subtracting viable organisms recovered from treated versus untreated control carriers. The tests were performed in triplicate. Disinfectants were classified as effective if a >5 log10 reduction in C. auris was achieved after the contact time recommended by the manufacturer. 6,7
Results
Table 2 shows the mean log10 reductions achieved by the 23 disinfectants against the 4 C. auris strains and C. albicans. Overall, 5 chlorine-based disinfectants and the peracetic-acid–based disinfectant consistently reduced all the C. auris strains and C. albicans by >5 log10. Also, 3 (75%) hydrogen-peroxide–based disinfectants reduced all the test strains by >5 log10. However, a fourth hydrogen-peroxide–based disinfectant (Alpha HP) with a relatively low hydrogen-peroxide concentration of 0.06% did not achieve a >5 log10 reduction of any of the test strains. Of the 4 quaternary-ammonium–alcohol disinfectants (Super Sani Cloth and Kinzua KE 15), 2 (50%) consistently reduced all the test organisms by >5 log10. One quaternary-ammonium–alcohol disinfectant (CaviCide) reduced the clade II isolate by >5 log10 but did not reduce the clade I, III, or IV isolates by >5 log10.
Table 2. Mean (SE) Log10 Reductions in Candida auris and Candida albicans for the 23 Tested Disinfectants
Note. C. auris Clade II, Antibiotic Resistance Bank (AR) 0381; clade I, AR-0389; clade III, AR-0383, and clade IV, AR-0385).
a Candida albicans American Type Culture Collection strain 10231.
b Recent formulations of these products (CaviWipes 1 and Cavicide 1) with increased concentrations of the quaternary-ammonium compound and alcohol are listed on EPA List P as effective against C. auris with a 1-min claim.
None of the quaternary-ammonium–based products achieved a >5 log10 reduction in the clade IV AR-0385 isolate. However, 1 quaternary-ammonium disinfectant (Kinzua TB) did achieve a >5 log10 reduction in the clade II AR-0381 isolate. A phenolic-acid–based disinfectant did not achieve a >5 log10 reduction of any of the test strains.
Discussion
Our results are consistent with previous evidence demonstrating that sporicidal disinfectants are effective against C. auris, whereas quaternary-ammonium disinfectants have limited activity. Reference Cadnum, Shaikh and Piedrahita3–Reference Sexton, Welsh, Bentz, Forsberg, Jackson, Berkow and Litvintseva5 None of the 8 quaternary-ammonium disinfectants tested achieved the >5 log10 reduction in C. auris AR-0385 required for a claim against drug-resistant C. auris. The limited efficacy of quaternary-ammonium disinfectants is important given the widespread use of these products in healthcare facilities in the context of the rapid spread of C. auris. The fact that many patients with C. auris are colonized and only detected through screening increases the likelihood that unrecognized cases may enter facilities where cleaning and disinfection practices may not be sufficient to limit spread.
Our results highlight the fact that different products within categories of disinfectants may vary in effectiveness against C. auris. Two quaternary-ammonium–alcohol disinfectants achieved a >5 log10 reduction in C. auris AR-0385 and the other test organisms, suggesting that the addition of alcohol to quaternary-ammonium disinfectants may enhance activity against C. auris. However, testing of individual quaternary-ammonium–alcohol products is required because 2 other products in this category (CaviWipes and CaviCide Spray) did not achieve a >5 log10 reduction in C. auris AR-0385, although CaviCide Spray did achieve a >5 log10 reduction in C. auris AR-0381. Notably, recent formulations of these products (Cavicide 1 and CaviWipes 1) with increased concentrations of the quaternary-ammonium compound and alcohol are listed on EPA List P as effective against C. auris with a 1-minute claim. Similarly, 3 hydrogen-peroxide–based disinfectants were effective against all the test strains and are on List P, but a fourth product with a relatively low hydrogen-peroxide concentration of 0.06% (Alpha HP) did not achieve a >5 log10 reduction of any of the test strains and is not on List P.
Our study had several limitations. Only 1 isolate from each of the 4 predominant clades was tested. Additional studies are needed with more strains. We only studied chlorine-based disinfectants with ≥4,306 parts per million free chlorine. Chlorine-based products with lower free chlorine are sometimes used and may be less effective against C. auris. Reference Rutala, Kanamori, Gergen, Sickbert-Bennett and Weber4,Reference Sexton, Welsh, Bentz, Forsberg, Jackson, Berkow and Litvintseva5,Reference Kumar, Cadnum, Jencson and Donskey10 We only completed laboratory assessments of the products. Real-world studies are needed. Finally, for wipes we tested the efficacy of liquid expressed from the towelette. This procedure may have led to the underestimation of reductions achieved by wipes, which also reduce pathogens by physical removal.
Acknowledgements
Financial support
The authors acknowledge funding from the Centers for Disease Control and Prevention’s investments to combat antibiotic resistance under award no. 2019-37809 to C.J.D.
Competing interests
C.J.D. has received research funding from Clorox, PDI, and Pfizer. The other authors report no conflicts of interest relevant to this article.
