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Abstract

Background

The COVID-19 pandemic and the emergence of have changed the epidemiological landscape of candidaemia worldwide.

Aim

We compared the epidemiological trends of candidaemia in a Greek tertiary academic hospital before (2009–2018) and during the early COVID-19 (2020–2021) and late COVID-19/early post-pandemic (2022–2023) era.

Methods

Incidence rates, species distribution, antifungal susceptibility profile and antifungal consumption were recorded, and one-way ANOVA or Fisher’s exact test performed. Species were identified by MALDI-ToF MS, and in vitro susceptibility determined with CLSI M27-Ed4 for and the EUCAST-E.DEF 7.3.2 for other spp.

Results

In total, 370 candidaemia episodes were recorded during the COVID-19 pandemic. Infection incidence (2.0 episodes/10,000 hospital bed days before, 3.9 during the early and 5.1 during the late COVID-19 era, p < 0.0001), (0%, 9% and 33%, p < 0.0001) and fluconazole-resistant species complex (SC) (20%, 24% and 33%, p = 0.06) infections increased over time, with the latter not associated with increase in fluconazole/voriconazole consumption. A significant increase over time was observed in fluconazole-resistant isolates regardless of species (8%, 17% and 41%, p < 0.0001). Resistance to amphotericin B or echinocandins was not recorded, with the exception of a single pan-echinocandin-resistant strain.

Conclusion

Candidaemia incidence nearly tripled during the COVID-19 era, with among the major causative agents and increasing fluconazole resistance in SC. Almost half of isolates were fluconazole-resistant, underscoring the need for increased awareness and strict implementation of infection control measures.

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This work is licensed under a Creative Commons Attribution 4.0 International License.
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2024-07-18
2024-07-26
http://instance.metastore.ingenta.com/content/10.2807/1560-7917.ES.2024.29.29.2300661
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References

  1. Hoenigl M, Seidel D, Sprute R, Cunha C, Oliverio M, Goldman GH, et al. COVID-19-associated fungal infections. Nat Microbiol. 2022;7(8):1127-40.  https://doi.org/10.1038/s41564-022-01172-2  PMID: 35918423 
  2. Witt LS, Howard-Anderson JR, Jacob JT, Gottlieb LB. The impact of COVID-19 on multidrug-resistant organisms causing healthcare-associated infections: a narrative review. JAC Antimicrob Resist. 2022;5(1):dlac130.  https://doi.org/10.1093/jacamr/dlac130  PMID: 36601548 
  3. Lyman M, Forsberg K, Sexton DJ, Chow NA, Lockhart SR, Jackson BR, et al. Worsening Spread of Candida auris in the United States, 2019 to 2021. Ann Intern Med. 2023;176(4):489-95.  https://doi.org/10.7326/M22-3469  PMID: 36940442 
  4. Kohlenberg A, Monnet DL, Plachouras D, Willinger B, Lagrou K, Philipova I, et al. Increasing number of cases and outbreaks caused by Candida auris in the EU/EEA, 2020 to 2021. Euro Surveill. 2022;27(46):2200846.  https://doi.org/10.2807/1560-7917.ES.2022.27.46.2200846  PMID: 36398575 
  5. Giannitsioti E, Louka C, Mamali V, Kousouli E, Velentza L, Papadouli V, et al. Bloodstream Infections in a COVID-19 Non-ICU Department: Microbial Epidemiology, Resistance Profiles and Comparative Analysis of Risk Factors and Patients’ Outcome. Microorganisms. 2022;10(7):1314.  https://doi.org/10.3390/microorganisms10071314  PMID: 35889033 
  6. Katsiari M, Mavroidi A, Kesesidis N, Palla E, Zourla K, Ntorlis K, et al. Emergence of Clonally-Related South Asian Clade I Clinical Isolates of Candida auris in a Greek COVID-19 Intensive Care Unit. J Fungi (Basel). 2023;9(2):243.  https://doi.org/10.3390/jof9020243  PMID: 36836357 
  7. Koukaki E, Rovina N, Tzannis K, Sotiropoulou Z, Loverdos K, Koutsoukou A, et al. Fungal Infections in the ICU during the COVID-19 Era: Descriptive and Comparative Analysis of 178 Patients. J Fungi (Basel). 2022;8(8):881.  https://doi.org/10.3390/jof8080881  PMID: 36012869 
  8. Routsi C, Meletiadis J, Charitidou E, Gkoufa A, Kokkoris S, Karageorgiou S, et al. Epidemiology of Candidemia and Fluconazole Resistance in an ICU before and during the COVID-19 Pandemic Era. Antibiotics (Basel). 2022;11(6):771.  https://doi.org/10.3390/antibiotics11060771  PMID: 35740177 
  9. Pappas PG, Kauffman CA, Andes DR, Clancy CJ, Marr KA, Ostrosky-Zeichner L, et al. Clinical Practice Guideline for the Management of Candidiasis: 2016 Update by the Infectious Diseases Society of America. Clin Infect Dis. 2016;62(4):e1-50.  https://doi.org/10.1093/cid/civ933  PMID: 26679628 
  10. Cornely OA, Bassetti M, Calandra T, Garbino J, Kullberg BJ, Lortholary O, et al. ESCMID* guideline for the diagnosis and management of Candida diseases 2012: non-neutropenic adult patients. Clin Microbiol Infect. 2012;18(Suppl 7):19-37.  https://doi.org/10.1111/1469-0691.12039  PMID: 23137135 
  11. Soriano A, Honore PM, Puerta-Alcalde P, Garcia-Vidal C, Pagotto A, Gonçalves-Bradley DC, et al. Invasive candidiasis: current clinical challenges and unmet needs in adult populations. J Antimicrob Chemother. 2023;78(7):1569-85.  https://doi.org/10.1093/jac/dkad139  PMID: 37220664 
  12. Wang Y, McGuire TM, Hollingworth SA, Dong Y, Van Driel ML. Antifungal agents for invasive candidiasis in non-neutropenic critically ill adults: What do the guidelines recommend? Int J Infect Dis. 2019;89:137-45.  https://doi.org/10.1016/j.ijid.2019.10.016  PMID: 31639522 
  13. Papadimitriou-Olivgeris M, Kolonitsiou F, Kefala S, Spiliopoulou A, Aretha D, Bartzavali C, et al. Increased incidence of candidemia in critically ill patients during the Coronavirus Disease 2019 (COVID-19) pandemic. Braz J Infect Dis. 2022;26(2):102353.  https://doi.org/10.1016/j.bjid.2022.102353  PMID: 35500645 
  14. Kokkoris S, Papachatzakis I, Gavrielatou E, Ntaidou T, Ischaki E, Malachias S, et al. ICU-acquired bloodstream infections in critically ill patients with COVID-19. J Hosp Infect. 2021;107:95-7.  https://doi.org/10.1016/j.jhin.2020.11.009  PMID: 33217490 
  15. Siopi M, Tarpatzi A, Kalogeropoulou E, Damianidou S, Vasilakopoulou A, Vourli S, et al. Epidemiological trends of fungemia in Greece with a focus on candidemia during the recent financial crisis: A 10-year survey in a tertiary care academic hospital and review of literature. Antimicrob Agents Chemother. 2020;64(3):1-17.  https://doi.org/10.1128/AAC.01516-19  PMID: 31871083 
  16. Clinical and Laboratory Standards Institute (CLSI). Reference method for broth dilution antifungal susceptibility testing of yeasts. M27 4th ed. Clinical and Laboratory Standards Institute; Wayne, PA, USA: 2017.
  17. Centers for Disease Control and Prevention (CDC). Antifungal Susceptibility Testing and Interpretation. Candida auris. Fungal Diseases. Atlanta: CDC. [Accessed: 3 Jul 2024]. Available from: https://www.cdc.gov/candida-auris/hcp/laboratories/antifungal-susceptibility-testing.html
  18. Arendrup MC, Prakash A, Meletiadis J, Sharma C, Chowdhary A. Comparison of EUCAST and CLSI reference microdilution mics of eight antifungal compounds for candida auris and associated tentative epidemiological cutoff values. Antimicrob Agents Chemother. 2017;61(6):e00485-17.  https://doi.org/10.1128/AAC.00485-17  PMID: 28416539 
  19. Arendrup MC, Meletiadis J, Mouton JW, Lagrou K, Hamal P, Guinea J. 2020. EUCAST definitive document E.DEF 7.3.2. Method for the determination of broth dilution minimum inhibitory concentrations of antifungal agents for yeasts. Växjö: EUCAST; 2020. Available from: https://www.eucast.org/fileadmin/src/media/PDFs/EUCAST_files/AFST/Files/EUCAST_E_Def_7.3.2_Yeast_testing_definitive_revised_2020.pdf
  20. Ramos-Martínez A, Pintos-Pascual I, Guinea J, Gutiérrez-Villanueva A, Gutiérrez-Abreu E, Díaz-García J, et al. Impact of the COVID-19 Pandemic on the Clinical Profile of Candidemia and the Incidence of Fungemia Due to Fluconazole-Resistant Candida parapsilosis. J Fungi (Basel). 2022;8(5):451.  https://doi.org/10.3390/jof8050451  PMID: 35628707 
  21. Seagle EE, Jackson BR, Lockhart SR, Georgacopoulos O, Nunnally NS, Roland J, et al. The Landscape of Candidemia During the Coronavirus Disease 2019 (COVID-19) Pandemic. Clin Infect Dis. 2022;74(5):802-11.  https://doi.org/10.1093/cid/ciab562  PMID: 34145450 
  22. Nucci M, Barreiros G, Guimarães LF, Deriquehem VAS, Castiñeiras AC, Nouér SA. Increased incidence of candidemia in a tertiary care hospital with the COVID-19 pandemic. Mycoses. 2021;64(2):152-6.  https://doi.org/10.1111/myc.13225  PMID: 33275821 
  23. Arastehfar A, Ünal N, Hoşbul T, Alper Özarslan M, Sultan Karakoyun A, Polat F, et al. Candidemia Among Coronavirus Disease 2019 Patients in Turkey Admitted to Intensive Care Units: A Retrospective Multicenter Study. Open Forum Infect Dis. 2022;9(4):ofac078.  https://doi.org/10.1093/ofid/ofac078  PMID: 35345665 
  24. Macauley P, Epelbaum O. Epidemiology and Mycology of Candidaemia in non-oncological medical intensive care unit patients in a tertiary center in the United States: Overall analysis and comparison between non-COVID-19 and COVID-19 cases. Mycoses. 2021;64(6):634-40.  https://doi.org/10.1111/myc.13258  PMID: 33608923 
  25. Díaz-García J, Gómez A, Machado M, Alcalá L, Reigadas E, Sánchez-Carrillo C, et al. Candida Genotyping of Blood Culture Isolates from Patients Admitted to 16 Hospitals in Madrid: Genotype Spreading during the COVID-19 Pandemic Driven by Fluconazole-Resistant C. parapsilosis. J Fungi (Basel). 2022;8(11):1228.  https://doi.org/10.3390/jof8111228  PMID: 36422050 
  26. Franconi I, Rizzato C, Tavanti A, Falcone M, Lupetti A. Paradigm Shift: Candida parapsilosis sensu stricto as the Most Prevalent Candida Species Isolated from Bloodstream Infections with Increasing Azole-Non-Susceptibility Rates: Trends from 2015-2022 Survey. J Fungi (Basel). 2023;9(10):1012.  https://doi.org/10.3390/jof9101012  PMID: 37888268 
  27. Boattini M, Pinto MF, Christaki E, Fasciana T, Falces-Romero I, Tofarides A, et al. Multicentre Surveillance of Candida Species from Blood Cultures during the SARS-CoV-2 Pandemic in Southern Europe (CANCoVEU Project). Microorganisms. 2023;11(3):560.  https://doi.org/10.3390/microorganisms11030560  PMID: 36985134 
  28. Satoh K, Makimura K, Hasumi Y, Nishiyama Y, Uchida K, Yamaguchi H. Candida auris sp. nov., a novel ascomycetous yeast isolated from the external ear canal of an inpatient in a Japanese hospital. Microbiol Immunol. 2009;53(1):41-4.  https://doi.org/10.1111/j.1348-0421.2008.00083.x  PMID: 19161556 
  29. Lee WG, Shin JH, Uh Y, Kang MG, Kim SH, Park KH, et al. First three reported cases of nosocomial fungemia caused by Candida auris. J Clin Microbiol. 2011;49(9):3139-42.  https://doi.org/10.1128/JCM.00319-11  PMID: 21715586 
  30. Daneshnia F, de Almeida Júnior JN, Ilkit M, Lombardi L, Perry AM, Gao M, et al. Worldwide emergence of fluconazole-resistant Candida parapsilosis: current framework and future research roadmap. Lancet Microbe. 2023;4(6):e470-80.  https://doi.org/10.1016/S2666-5247(23)00067-8  PMID: 37121240 
  31. Díaz-García J, Machado M, Alcalá L, Reigadas E, Pérez-Ayala A, Gómez-García de la Pedrosa E, et al. Trends in antifungal resistance in Candida from a multicenter study conducted in Madrid (CANDIMAD study): fluconazole-resistant C. parapsilosis spreading has gained traction in 2022. Antimicrob Agents Chemother. 2023;67(11):e0098623.  https://doi.org/10.1128/aac.00986-23  PMID: 38092562 
  32. Pfaller MA, Carvalhaes CG, DeVries S, Rhomberg PR, Castanheira M. Impact of COVID-19 on the antifungal susceptibility profiles of isolates collected in a global surveillance program that monitors invasive fungal infections. Med Mycol. 2022;60(5):28.  https://doi.org/10.1093/mmy/myac028  PMID: 35511210 
  33. Trevijano-Contador N, Torres-Cano A, Carballo-González C, Puig-Asensio M, Martín-Gómez MT, Jiménez-Martínez E, et al. Global Emergence of Resistance to Fluconazole and Voriconazole in Candida parapsilosis in Tertiary Hospitals in Spain During the COVID-19 Pandemic. Open Forum Infect Dis. 2022;9(11):ofac605.  https://doi.org/10.1093/ofid/ofac605  PMID: 36467290 
  34. Mamali V, Siopi M, Charpantidis S, Samonis G, Tsakris A, Vrioni G, On Behalf Of The Candi-Candi Network. Increasing Incidence and Shifting Epidemiology of Candidemia in Greece: Results from the First Nationwide 10-Year Survey. J Fungi (Basel). 2022;8(2):116.  https://doi.org/10.3390/jof8020116  PMID: 35205870 
  35. Politi L, Vrioni G, Hatzianastasiou S, Lada M, Martsoukou M, Sipsas NV, et al. Candida auris in Greek healthcare facilities: Active surveillance results on first cases and outbreaks from eleven hospitals within Attica region. J Mycol Med. 2024;34(2):101477.  https://doi.org/10.1016/j.mycmed.2024.101477  PMID: 38574412 
  36. Ioannou P, Kofteridis DP, Alexakis K, Koutserimpas C, Papakitsou I, Maraki S, et al. Candida Species Isolation from Hospitalized Patients with COVID-19-A Retrospective Study. Diagnostics (Basel). 2022;12(12):365.  https://doi.org/10.3390/diagnostics12123065  PMID: 36553072 
Increase in candidemia cases and emergence of fluconazole-resistant Candida parapsilosis and C. auris isolates in a tertiary care academic hospital during the COVID-19 pandemic, Greece, 2020 to 2023
<p class="citation"> <span>Citation style for this article:</span> <span class="meta-value authors"> <a href="/search?value1=Maria+Siopi&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Siopi Maria</a>, <a href="/search?value1=Panagiota-Christina+Georgiou&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Georgiou Panagiota-Christina</a>, <a href="/search?value1=Paschalis+Paranos&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Paranos Paschalis</a>, <a href="/search?value1=Maria-Ioanna+Beredaki&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Beredaki Maria-Ioanna</a>, <a href="/search?value1=Aikaterini+Tarpatzi&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Tarpatzi Aikaterini</a>, <a href="/search?value1=Eleni+Kalogeropoulou&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Kalogeropoulou Eleni</a>, <a href="/search?value1=Sofia+Damianidou&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Damianidou Sofia</a>, <a href="/search?value1=Alexandra+Vasilakopoulou&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Vasilakopoulou Alexandra</a>, <a href="/search?value1=Polyxeni+Karakosta&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Karakosta Polyxeni</a>, <a href="/search?value1=Spyros+Pournaras&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Pournaras Spyros</a>, <a href="/search?value1=Joseph+Meletiadis&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Meletiadis Joseph</a></span>. Increase in candidemia cases and emergence of fluconazole-resistant Candida parapsilosis and C. auris isolates in a tertiary care academic hospital during the COVID-19 pandemic, Greece, 2020 to 2023. <a href="/content/ecdc">Euro Surveill.</a> 2024;29(29):pii=2300661. <a href="https://doi.org/10.2807/1560-7917.ES.2024.29.29.2300661" title="doi link" target="_blank">https://doi.org/10.2807/1560-7917.ES.2024.29.29.2300661</a> <span class="ES_Article_citation"> <span class="generated">Received</span>: 21 Nov 2023;&nbsp;&nbsp; <span class="generated">Accepted</span>: 04 May 2024 </span> </p>
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