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Cited by 45Antifungal resistance and susceptibilityInfection Control in HealthcareAntimicrobial agents and applications

Augmenting the Activity of Chlorhexidine for Decolonization of Candida auris from Porcine skin

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Johnson, Chad J., Eix, Emily F., Lam, Brandon C., Wartman, Kayla M., Meudt, Jennifer J., Shanmuganayagam, Dhanansayan, Nett, Jeniel E.·2021·Journal of Fungi
DOI 10.3390/jof7100804PMC PMC8537331
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Abstract

Candida auris readily colonizes skin and efficiently spreads among patients in healthcare settings worldwide. Given the capacity of this drug-resistant fungal pathogen to cause invasive disease with high mortality, hospitals frequently employ chlorhexidine bathing to reduce skin colonization. Using an ex vivo skin model, we show only a mild reduction in C. auris following chlorhexidine application. This finding helps explain why chlorhexidine bathing may have failures clinically, despite potent in vitro activity. We further show that isopropanol augments the activity of chlorhexidine against C. auris on skin. Additionally, we find both tea tree (Melaleuca alternifolia) oil and lemongrass (Cymbopogon flexuosus) oil to further enhance the activity of chlorhexidine/isopropanol for decolonization. We link this antifungal activity to individual oil components and show how some of these components act synergistically with chlorhexidine/isopropanol. Together, the studies provide strategies to improve C. auris skin decolonization through the incorporation of commonly used topical compounds.

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  • C. auris eventually navigates into the pilosebaceous unit where there is available sebum.

    “This could explain why C. auris eventually navigates into the pilosebaceous unit where there is available sebum (22, 23).”

    From <i>Candida auris</i> metabolism and growth preferences in physiologically relevant skin-like conditions (2026) · cites this paper as [22]

    Results §3.1 reports C. auris within hair follicles in antiseptic-soap-treated porcine skin, and the Discussion describes follicular colonization. The paper does not establish that C. auris eventually moves into the pilosebaceous unit or that available sebum is involved. Page numbers were not available in our copy. (LLM, conf=0.86)

    Experimental — accuracy not yet measured

  • C. auris can grow and persist for extensive periods under skin-like conditions in simulation studies and animal models.

    “Several simulation studies and animal models have demonstrated that C. auris can grow and persist for extensive periods under skin-like conditions.”

    From <i>Candida auris</i> metabolism and growth preferences in physiologically relevant skin-like conditions (2026) · cites this paper as [22]

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Research works printed but not linked: 37

  1. [1]Lockhart S.R. Etienne K.A. Vallabhaneni S. Farooqi J. Chowdhary A. Govender N.P. Colombo A.L. Calvo B. Cuomo C.A. Desjardins C.A. Simultaneous emergence of multidrug-resistant Candida auris on 3 continents confirmed by whole-genome sequencing and epidemiological analyses Clin. Infect. Dis. 2017 64 134 140 10.1093/cid/ciw691 27988485 PMC5215215 · DOI · Paper page
  2. [3]Mathur P. Hasan F. Singh P.K. Malhotra R. Walia K. Chowdhary A. Five-year profile of candidaemia at an Indian trauma centre: High rates of Candida auris blood stream infections Mycoses 2018 61 674 680 10.1111/myc.12790 29738604 · DOI
  3. [4]Rudramurthy S.M. Chakrabarti A. Paul R.A. Sood P. Kaur H. Capoor M.R. Kindo A.J. Marak R.S.K. Arora A. Sardana R. Candida auris candidaemia in Indian ICUs: Analysis of risk factors J. Antimicrob. Chemother. 2017 72 1794 1801 10.1093/jac/dkx034 28333181 · DOI · Paper page
  4. [5]Schelenz S. Hagen F. Rhodes J.L. Abdolrasouli A. Chowdhary A. Hall A. Ryan L. Shackleton J. Trimlett R. Meis J.F. First hospital outbreak of the globally emerging Candida auris in a European hospital Antimicrob. Resist. Infect. Control 2016 5 35 10.1186/s13756-016-0132-5 27777756 PMC5069812 · DOI · Paper page
  5. [6]Lamoth F. Kontoyiannis D.P. The Candida auris alert: Facts and perspectives J. Infect. Dis. 2018 217 516 520 10.1093/infdis/jix597 29390110 · DOI
  6. [7]Bergeron G. Bloch D. Murray K. Kratz M. Parton H. Ackelsberg J. Antwi M. Del Rosso P. Dorsinville M. Kubinson H. Candida auris colonization after discharge to a community setting: New York City, 2017–2019 Open Forum Infectious Diseases Oxford University Press Oxford, UK 2021 Volume 8 ofaa620 10.1093/ofid/ofaa620 PMC7814391 33511238 · DOI
  7. [10]Sherry L. Ramage G. Kean R. Borman A. Johnson E.M. Richardson M.D. Rautemaa-Richardson R. Biofilm-forming capability of highly virulent, multidrug-resistant Candida auris Emerg. Infect. Dis. 2017 23 328 331 10.3201/eid2302.161320 28098553 PMC5324806 · DOI · Paper page
  8. [12]Mulet Bayona J.V. Tormo Palop N. Salvador Garcia C. Herrero Rodriguez P. Abril Lopez de Medrano V. Ferrer Gomez C. Gimeno Cardona C. Characteristics and management of candidaemia episodes in an established Candida auris outbreak Antibiotics 2020 9 558 10.3390/antibiotics9090558 PMC7559407 32872580 · DOI
  9. [13]Biswal M. Rudramurthy S.M. Jain N. Shamanth A.S. Sharma D. Jain K. Yaddanapudi L.N. Chakrabarti A. Controlling a possible outbreak of Candida auris infection: Lessons learnt from multiple interventions J. Hosp. Infect. 2017 97 363 370 10.1016/j.jhin.2017.09.009 28939316 · DOI
  10. [14]Eyre D.W. Sheppard A.E. Madder H. Moir I. Moroney R. Quan T.P. Griffiths D. George S. Butcher L. Morgan M. A Candida auris outbreak and its control in an intensive care setting N. Engl. J. Med. 2018 379 1322 1331 10.1056/NEJMoa1714373 30281988 · DOI · Paper page
  11. [15]Liu Y. Chen J.Y. Shang H.T. Liu C.E. Wang Y. Niu R. Wu J. Wei H. Light microscopic, electron microscopic, and immunohistochemical comparison of Bama minipig (Sus scrofa domestica) and human skin Comp. Med. 2010 60 142 148 20412690 PMC2855042
  12. [16]Eaglstein W.H. Mertz P.M. New methods for assessing epidermal wound healing: The effects of triamcinolone acetonide and polyethelene film occlusion J. Invest. Dermatol. 1978 71 382 384 10.1111/1523-1747.ep12556814 722115 · DOI · Paper page
  13. [18]Summerfield A. Meurens F. Ricklin M.E. The immunology of the porcine skin and its value as a model for human skin Mol. Immunol. 2015 66 14 21 10.1016/j.molimm.2014.10.023 25466611 · DOI · Paper page
  14. [19]Lohse M.B. Gulati M. Valle Arevalo A. Fishburn A. Johnson A.D. Nobile C.J. Assessment and optimizations of Candida albicans in vitro biofilm assays Antimicrob. Agents Chemother. 2017 61 10.1128/AAC.02749-16 28289028 PMC5404589 · DOI
  15. [20]Tobudic S. Kratzer C. Lassnigg A. Graninger W. Presterl E. In vitro activity of antifungal combinations against Candida albicans biofilms J. Antimicrob. Chemother. 2010 65 271 274 10.1093/jac/dkp429 19996142 · DOI
  16. [21]Schomberg D.T. Tellez A. Meudt J.J. Brady D.A. Dillon K.N. Arowolo F.K. Wicks J. Rousselle S.D. Shanmuganayagam D. Miniature swine for preclinical modeling of complexities of human disease for translational scientific discovery and accelerated development of therapies and medical devices Toxicol. Pathol. 2016 44 299 314 10.1177/0192623315618292 26839324 · DOI · Paper page
  17. [22]Digison M.B. A review of anti-septic agents for pre-operative skin preparation Plast. Surg. Nurs. 2007 27 185 189 10.1097/01.PSN.0000306182.50071.e2 18165724 · DOI
  18. [23]Mimoz O. Lucet J.C. Kerforne T. Pascal J. Souweine B. Goudet V. Mercat A. Bouadma L. Lasocki S. Alfandari S. Skin antisepsis with chlorhexidine-alcohol versus povidone iodine-alcohol, with and without skin scrubbing, for prevention of intravascular-catheter-related infection (CLEAN): An open-label, multicentre, randomised, controlled, two-by-two factorial trial Lancet 2015 386 2069 2077 10.1016/S0140-6736(15)00244-5 26388532 · DOI
  19. [24]Wade R.G. Burr N.E. McCauley G. Bourke G. Efthimiou O. The comparative efficacy of chlorhexidine gluconate and povidone-iodine antiseptics for the prevention of infection in clean surgery: A systematic review and network meta-analysis Ann. Surg. 2020 10.1097/SLA.0000000000004076 32773627 · DOI
  20. [25]Hammer K.A. Treatment of acne with tea tree oil (melaleuca) products: A review of efficacy, tolerability and potential modes of action Int. J. Antimicrob. Agents 2015 45 106 110 10.1016/j.ijantimicag.2014.10.011 25465857 · DOI
  21. [26]Abd Rashed A. Rathi D.G. Ahmad Nasir N.A.H. Abd Rahman A.Z. Antifungal properties of essential oils and their compounds for application in skin fungal Infections: Conventional and nonconventional approaches Molecules 2021 26 1093 10.3390/molecules26041093 33669627 PMC7922942 · DOI
  22. [27]Ergin A. Arikan S. Comparison of microdilution and disc diffusion methods in assessing the in vitro activity of fluconazole and Melaleuca alternifolia (tea tree) oil against vaginal Candida isolates J. Chemother. 2002 14 465 472 10.1179/joc.2002.14.5.465 12462426 · DOI
  23. [28]Silva Cde B. Guterres S.S. Weisheimer V. Schapoval E.E. Antifungal activity of the lemongrass oil and citral against Candida spp. Braz. J. Infect. Dis. 2008 12 63 66 10.1590/S1413-86702008000100014 18553017 · DOI · Paper page
  24. [29]Lulekal E. Tesfaye S. Gebrechristos S. Dires K. Zenebe T. Zegeye N. Feleke G. Kassahun A. Shiferaw Y. Mekonnen A. Phytochemical analysis and evaluation of skin irritation, acute and sub-acute toxicity of Cymbopogon citratus essential oil in mice and rabbits Toxicol. Rep. 2019 6 1289 1294 10.1016/j.toxrep.2019.11.002 31867219 PMC6906703 · DOI
  25. [30]Krzysko-Lupicka T. Sokol S. Piekarska-Stachowiak A.A. Evaluation of fungistatic activity of eight selected essential oils on four heterogeneous Fusarium isolates obtained from cereal grains in Southern Poland Molecules 2020 25 292 10.3390/molecules25020292 31936864 PMC7024206 · DOI
  26. [31]Gao S. Liu G. Li J. Chen J. Li L. Li Z. Zhang X. Zhang S. Thorne R.F. Zhang S. Antimicrobial activity of lemongrass essential oil (Cymbopogon flexuosus) and its active component citral against dual-species biofilms of Staphylococcus aureus and Candida species Front. Cell Infect. Microbiol. 2020 10 603858 10.3389/fcimb.2020.603858 33415085 PMC7783362 · DOI
  27. [32]Lepak A.J. Zhao M. Berkow E.L. Lockhart S.R. Andes D.R. Pharmacodynamic optimization for treatment of invasive Candida auris infection Antimicrob. Agents Chemother. 2017 61 S73 10.1128/AAC.00791-17 PMC5527602 28584152 · DOI
  28. [33]Borman A.M. Szekely A. Johnson E.M. Comparative pathogenicity of United Kingdom isolates of the emerging pathogen Candida auris and other key pathogenic Candida species mSphere 2016 1 e00189-16 10.1128/mSphere.00189-16 27547827 PMC4990711 · DOI · Paper page
  29. [34]Forgacs L. Borman A.M. Prepost E. Toth Z. Kardos G. Kovacs R. Szekely A. Nagy F. Kovacs I. Majoros L. Comparison of in vivo pathogenicity of four Candida auris clades in a neutropenic bloodstream infection murine model Emerg. Microbes Infect. 2020 9 1160 1169 10.1080/22221751.2020.1771218 32486923 PMC7448943 · DOI · Paper page
  30. [35]Larkin E. Hager C. Chandra J. Mukherjee P.K. Retuerto M. Salem I. Long L. Isham N. Kovanda L. Borroto-Esoda K. The emerging pathogen Candida auris: Growth phenotype, virulence factors, activity of antifungals, and effect of SCY-078, a novel glucan synthesis inhibitor, on growth morphology and biofilm formation Antimicrob. Agents Chemother. 2017 61 10.1128/AAC.02396-16 28223375 PMC5404565 · DOI · Paper page
  31. [36]Karpanen T.J. Worthington T. Conway B.R. Hilton A.C. Elliott T.S. Lambert P.A. Penetration of chlorhexidine into human skin Antimicrob. Agents Chemother. 2008 52 3633 3636 10.1128/AAC.00637-08 18676882 PMC2565868 · DOI
  32. [37]Huang X. Hurabielle C. Drummond R.A. Bouladoux N. Desai J.V. Sim C.K. Belkaid Y. Lionakis M.S. Segre J.A. Murine model of colonization with fungal pathogen Candida auris to explore skin tropism, host risk factors and therapeutic strategies Cell Host Microbe 2021 29 210 221 e216 10.1016/j.chom.2020.12.002 33385336 PMC7878403 · DOI · Paper page
  33. [38]Moore G. Schelenz S. Borman A.M. Johnson E.M. Brown C.S. Yeasticidal activity of chemical disinfectants and antiseptics against Candida auris J. Hosp. Infect. 2017 97 371 375 10.1016/j.jhin.2017.08.019 28865738 · DOI
  34. [39]Herman A. Herman A.P. Essential oils and their constituents as skin penetration enhancer for transdermal drug delivery: A review J. Pharm. Pharmacol. 2015 67 473 485 10.1111/jphp.12334 25557808 · DOI
  35. [40]Cal K. Kupiec K. Sznitowska M. Effect of physicochemical properties of cyclic terpenes on their ex vivo skin absorption and elimination kinetics J. Dermatol. Sci. 2006 41 137 142 10.1016/j.jdermsci.2005.09.003 16260121 · DOI
  36. [41]Carson C.F. Mee B.J. Riley T.V. Mechanism of action of Melaleuca alternifolia (tea tree) oil on Staphylococcus aureus determined by time-kill, lysis, leakage, and salt tolerance assays and electron microscopy Antimicrob. Agents Chemother. 2002 46 1914 1920 10.1128/AAC.46.6.1914-1920.2002 12019108 PMC127210 · DOI · Paper page
  37. [42]Youn B.H. Kim Y.S. Yoo S. Hur M.H. Antimicrobial and hand hygiene effects of Tea Tree Essential Oil disinfectant: A randomised control trial Int. J. Clin. Pract. 2021 e14206 10.1111/ijcp.14206 33950544 · DOI

Cited by

Sorted by citations

Authors
Johnson, C. J., Eix, E. F., Lam, B. C., Wartman, K. M., Meudt, J. J., Shanmuganayagam, D., & Nett, J. E.
Affiliations
University of Wisconsin–Madison (US)
Corresponding author
Nett, Jeniel E.
ORCID
Venue
Journal of Fungi
Publisher
MDPI AG
Published
2021-09-25
Volume
7
Issue
10
Pages
804
ISSN
2309-608X (ISSN-L)
DOI
10.3390/jof7100804
PMC
PMC8537331
OpenAlex
W3202736615
Cited by
45
References
5
Citations by year
2026: 12 · 2025: 10 · 2024: 8 · 2023: 10 · 2022: 5
FWCI
1.82
Type
journal article
Language
en
Open access
Licence
Locations
  • Journal of Fungi (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Funders
  • Burroughs Wellcome Fund (1012299)
  • National Institutes of Health (R01AI145939, R21AI159583)
  • National Science Foundation (DGE-1747503)
Topics
  • Health Sciences › Medicine › Infectious Diseases › Antifungal resistance and susceptibility
  • Health Sciences › Medicine › Infectious Diseases › Infection Control in Healthcare
  • Physical Sciences › Chemistry › Organic Chemistry › Antimicrobial agents and applications
Keywords
Candida auris, chlorhexidine, isopropanol, tea tree oil, lemongrass essential oil, Melaleuca alternifolia, Cymbopogon flexuosus, topical antifungal agents, antifungal synergy, ex vivo skin model, chlorhexidine bathing

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