Skip to main content
Log in

Outbreak of Candida parapsilosis fungemia in an intensive care unit during a COVID surge: an epidemic within a pandemic

  • Original Article
  • Published:
European Journal of Clinical Microbiology & Infectious Diseases Aims and scope Submit manuscript

Abstract

We sought to investigate epidemiology, risk factors, clinical features, and outcome of the C. parapsilosis blood stream infection (BSI) outbreaks observed during the first surges of COVID-19 pandemic in our population. Retrospective, monocentric observational study in the 24 bed intensive care unit (ICU) of a tertiary care medical center in northern Italy, from 2019 to 2021 first 5 months. 2030 patients were enrolled, of whom 239 were COVID-19 positive. The total incidence of Candida-BSI was 41.9 per 1000 admissions, with two outbreaks during 2020 spring and winter’s COVID surges. The total numbers of C. parapsilosis BSI cases are 94, of which 21 during the first outbreak and 20 during the second. In our population, COVID-19 was strongly associated with C. parapsilosis BSI (OR 4.71, p < 0.001), as well as continuous renal replacement therapy (CRRT) (OR 3.44, p = 0.001), prolonged antibiotic therapy (OR 3.19, p = 0.004), and delayed infusion sets replacements (OR 2.76, p = 0.015). No statistically significant association was found between Candida-BSI episodes and mortality, when adjusted for other known outcome risk factors. COVID surges undermined the infectious control measures in our ICU, leading to two outbreak of C. parapsilosis BSI. A stricter, thorough management of intravascular devices and infusion set is crucial in prevention of catheter related BSI, and awareness must be kept high, especially in emergencies circumstances, such as the ongoing COVID-19 pandemic.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

Data availability

The anonymized dataset is available from the corresponding author on reasonable request.

Code availability

Not applicable.

References

  1. Shoham S, Marwaha S (2010) Invasive fungal infections in the ICU. J Intensive Care Med 25:78–92. https://doi.org/10.1177/0885066609355262

    Article  PubMed  Google Scholar 

  2. Ishikane M, Hayakawa K, Kutsuna S, Takeshita N, Ohmagari N (2016) Epidemiology of blood stream infection due to Candida species in a tertiary care hospital in Japan over 12 years: importance of peripheral line-associated candidemia. PLoS One 31(11):e0165346. https://doi.org/10.1371/journal.pone.0165346

    Article  CAS  Google Scholar 

  3. Vannini M, Emery S, Lieutier-Colas F, Legueult K, Mondain V, Retur N et al (2022) Epidemiology of candidemia in NICE area, France: a five-year study of antifungal susceptibility and mortality. J Mycol Med 32:101210. https://doi.org/10.1016/j.mycmed.2021.101210

    Article  CAS  PubMed  Google Scholar 

  4. Prigitano A, Cavanna C, Passera M, Ossi C, Sala E, Lombardi G et al (2016) CAND-LO 2014–15 study: changing epidemiology of candidemia in Lombardy (Italy). Infection 44:765–780. https://doi.org/10.1007/s15010-016-0951-6

    Article  PubMed  Google Scholar 

  5. Giacobbe DR, Battaglini D, Enrile EM, Dentone C, Vena A, Robba C et al (2021) Incidence and prognosis of ventilator-associated pneumonia in critically ill patients with COVID-19: a multicenter study. J Clin Med 3:10. https://doi.org/10.3390/jcm10040555

    Article  CAS  Google Scholar 

  6. Pinhati HMS, Casulari LA, Souza ACR, Siqueira RA, Damasceno CMG, Colombo AL (2016) Outbreak of candidemia caused by fluconazole resistant Candida parapsilosis strains in an intensive care unit. BMC Infect Dis 20(16):433. https://doi.org/10.1186/s12879-016-1767-9

    Article  Google Scholar 

  7. Kozhushnaya OS, Solopova GG, Voropaev AD, Markova ZHV, Satsuk AV, Balamozhnova AO et al (2020) Investigation of a candidemia outbreak caused by C. parapsilosis in a pediatric hematology/oncology center. CMAC 22:266–70. https://doi.org/10.36488/cmac.2020.4.266-270

    Article  Google Scholar 

  8. Thomaz DY, de Almeida JN, Lima GME, de Nunes MO, Camargo CH, de Grenfell RC et al (2018) An azole-resistant Candida parapsilosis outbreak: clonal persistence in the intensive care unit of a Brazilian teaching hospital. Front Microbiol 9:2997. https://doi.org/10.3389/fmicb.2018.02997

    Article  PubMed  PubMed Central  Google Scholar 

  9. Montagna MT, Lovero G, Borghi E, Amato G, Andreoni S, Campion L et al (2014) Candidemia in intensive care unit: a nationwide prospective observational survey (GISIA-3 study) and review of the European literature from 2000 through 2013. Eur Rev Med Pharmacol Sci 18:661–674

    CAS  PubMed  Google Scholar 

  10. Ataee RA, Ataee MH, Mehrabi Tavana A, Salesi M (2017) Bacteriological aspects of hand washing: a key for health promotion and infections control. Int J Prev Med 10(8):16. https://doi.org/10.4103/2008-7802.201923

    Article  Google Scholar 

  11. Abad CL, Barker AK, Safdar N (2020) A systematic review of the effectiveness of cohorting to reduce transmission of healthcare-associated C difficile and multidrug-resistant organisms. Infect Control Hosp Epidemiol 41:691–709. https://doi.org/10.1017/ice.2020.45

    Article  PubMed  PubMed Central  Google Scholar 

  12. Sun Jin L, Fisher D (2021) MDRO transmission in acute hospitals during the COVID-19 pandemic. Curr Opin Infect Dis 1(34):365–371. https://doi.org/10.1097/QCO.0000000000000735

    Article  CAS  Google Scholar 

  13. Palmore TN, Henderson DK (2021) Healthcare-associated infections during the coronavirus disease 2019 (COVID-19) pandemic. Infect Control Hosp Epidemiol 42:1372–1373. https://doi.org/10.1017/ice.2021.377

    Article  PubMed  Google Scholar 

  14. Baker MA, Sands KE, Huang SS, Kleinman K, Septimus EJ, Varma N et al (2022) The impact of coronavirus disease 2019 (COVID-19) on healthcare-associated infections. Clin Infect Dis 30(74):1748–1754. https://doi.org/10.1093/cid/ciab688

    Article  CAS  Google Scholar 

  15. Cultrera R, Barozzi A, Libanore M, Marangoni E, Pora R, Quarta B et al (2021) Co-infections in critically ill patients with or without COVID-19: a comparison of clinical microbial culture findings. Int J Environ Res Public Health 20:18. https://doi.org/10.3390/ijerph18084358

    Article  CAS  Google Scholar 

  16. Silva S, Negri M, Henriques M, Oliveira R, Williams DW, Azeredo J (2012) Candida glabrata, Candida parapsilosis and Candida tropicalis: biology, epidemiology, pathogenicity and antifungal resistance. FEMS Microbiol Rev 36:288–305. https://doi.org/10.1111/j.1574-6976.2011.00278.x

    Article  CAS  PubMed  Google Scholar 

  17. Delfino D, Scordino F, Pernice I, Lo Passo C, Galbo R, David A et al (2014) Potential association of specific Candida parapsilosis genotypes, bloodstream infections and colonization of health workers’ hands. Clin Microbiol Infect 20:O946–O951. https://doi.org/10.1111/1469-0691.12685

    Article  CAS  PubMed  Google Scholar 

  18. Caggiano G, Coretti C, Bartolomeo N, Lovero G, De Giglio O, Montagna MT (2015) Candida bloodstream infections in Italy: changing epidemiology during 16 years of surveillance. Biomed Res Int 2015(7):256580. https://doi.org/10.1155/2015/256580

    Article  PubMed  PubMed Central  Google Scholar 

  19. Mencarini J, Mantengoli E, Tofani L, Riccobono E, Fornaini R, Bartalesi F et al (2018) Evaluation of candidemia and antifungal consumption in a large tertiary care Italian hospital over a 12-year period. Infection 46:469–476. https://doi.org/10.1007/s15010-018-1139-z

    Article  PubMed  Google Scholar 

  20. Pienthong T, Visuttichaikit S, Apisarnthanarak P, Jantarathaneewat K, Weber DJ, Apisarnthanarak A (2023) Increase in the incidence of Candida parapsilosis and Candida tropicalis bloodstream infections during the coronavirus disease 2019 (COVID-19) pandemic. Antimicrob Steward Healthc Epidemiol 10(3):e2. https://doi.org/10.1017/ash.2022.354

    Article  Google Scholar 

  21. Díaz-García J, Gómez A, Machado M, Alcalá L, Reigadas E, Sánchez-Carrillo C, et al (2022) 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) 8 https://doi.org/10.3390/jof8111228

  22. Routsi C, Meletiadis J, Charitidou E, Gkoufa A, Kokkoris S, Karageorgiou S et al (2022) Epidemiology of candidemia and fluconazole resistance in an ICU before and during the COVID-19 pandemic era. Antibiotics (Basel) 4:11. https://doi.org/10.3390/antibiotics11060771

    Article  CAS  Google Scholar 

  23. Bojorges-Aguilar ES, Roman-Montes CM, Martinez-Gamboa A, Rangel-Cordero A, Diaz-Lomeli PG, Rivero-Sigarroa E et al (2021) 317 Invasive fungal infections in critically-ill patients with COVID-19 in Mexico City. Open Forum Infect Dis 8:S264–S264. https://doi.org/10.1093/ofid/ofab466.519

    Article  PubMed Central  Google Scholar 

  24. Presente S, Bonnal C, Normand A-C, Gaudonnet Y, Fekkar A, Timsit J-F et al (2023) Hospital clonal outbreak of fluconazole-resistant Candida parapsilosis harboring the Y132F ERG11p substitution in a French intensive care unit. Antimicrob Agents Chemother 16(67):e0113022. https://doi.org/10.1128/aac.01130-22

    Article  CAS  Google Scholar 

  25. Bassetti M, Giacobbe DR, Vena A, Trucchi C, Ansaldi F, Antonelli M et al (2019) Incidence and outcome of invasive candidiasis in intensive care units (ICUs) in Europe: results of the EUCANDICU project. Crit Care 14(23):219. https://doi.org/10.1186/s13054-019-2497-3

    Article  Google Scholar 

  26. Koehler P, Stecher M, Cornely OA, Koehler D, Vehreschild MJGT, Bohlius J et al (2019) Morbidity and mortality of candidaemia in Europe: an epidemiologic meta-analysis. Clin Microbiol Infect 25:1200–1212. https://doi.org/10.1016/j.cmi.2019.04.024

    Article  CAS  PubMed  Google Scholar 

  27. Mazzanti S, Brescini L, Morroni G, Orsetti E, Pocognoli A, Donati A et al (2021) Candidemia in intensive care units over nine years at a large Italian university hospital: comparison with other wards. PLoS One 26(16):e0252165. https://doi.org/10.1371/journal.pone.0252165

    Article  CAS  Google Scholar 

  28. Brunetti G, Navazio AS, Giuliani A, Giordano A, Proli EM, Antonelli G et al (2019) Candida blood stream infections observed between 2011 and 2016 in a large Italian university hospital: a time-based retrospective analysis on epidemiology, biofilm production, antifungal agents consumption and drug-susceptibility. PLoS One 7(14):e0224678. https://doi.org/10.1371/journal.pone.0224678

    Article  CAS  Google Scholar 

  29. Ghezzi MC, Brunetti G, Visconti V, Giordano A, Raponi G (2017) Candidaemia in a tertiary care academic hospital in Italy. The impact of C. parapsilosis complex on the species distribution and antifungal susceptibility. J Med Microbiol 66:990–8. https://doi.org/10.1099/jmm.0.000505

    Article  PubMed  Google Scholar 

  30. Mesini A, Mikulska M, Giacobbe DR, Del Puente F, Gandolfo N, Codda G et al (2020) Changing epidemiology of candidaemia: increase in fluconazole-resistant Candida parapsilosis. Mycoses 63:361–368. https://doi.org/10.1111/myc.13050

    Article  CAS  PubMed  Google Scholar 

  31. Thomaz DY, Del Negro GMB, Ribeiro LB, da Silva M, Carvalho GOMH, Camargo CH et al (2022) A Brazilian inter-hospital candidemia outbreak caused by fluconazole-resistant Candida parapsilosis in the COVID-19 era. J Fungi (Basel) 20:8. https://doi.org/10.3390/jof8020100

    Article  CAS  Google Scholar 

  32. Tóth R, Nosek J, Mora-Montes HM, Gabaldon T, Bliss JM, Nosanchuk JD et al (2019) Candida parapsilosis: from genes to the bedside. Clin Microbiol Rev 20:32. https://doi.org/10.1128/CMR.00111-18

    Article  Google Scholar 

  33. Devrim İ, Topal S, Ceylan G, Oruç Y, Gülfidan G, Ayhan Y et al (2022) Changes in the incidence of Candida-related central line-associated bloodstream infections in pediatric intensive care unit: could central line bundle have a role? J Mycol Med 32:101277. https://doi.org/10.1016/j.mycmed.2022.101277

    Article  PubMed  Google Scholar 

  34. Ferrer J, Boelle P-Y, Salomon J, Miliani K, L’Hériteau F, Astagneau P et al (2014) Management of nurse shortage and its impact on pathogen dissemination in the intensive care unit. Epidemics 9:62–69. https://doi.org/10.1016/j.epidem.2014.07.002

    Article  PubMed  Google Scholar 

  35. Lindberg M, Skytt B, Lindberg M (2020) Continued wearing of gloves: a risk behaviour in patient care. Infect Prev Pract 2:100091. https://doi.org/10.1016/j.infpip.2020.100091

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Barchiesi F, Orsetti E, Osimani P, Catassi C, Santelli F, Manso E (2016) Factors related to outcome of bloodstream infections due to Candida parapsilosis complex. BMC Infect Dis 9(16):387. https://doi.org/10.1186/s12879-016-1704-y

    Article  Google Scholar 

  37. Daneshnia F, de Almeida Júnior JN, Ilkit M, Lombardi L, Perry AM, Gao M, et al (2023) Worldwide emergence of fluconazole-resistant Candida parapsilosis: current framework and future research roadmap. Lancet Microbe 27. https://doi.org/10.1016/S2666-5247(23)00067-8

Download references

Author information

Authors and Affiliations

Authors

Contributions

Conceptualization: A. A. and R. M. T.; formal analysis: A. A., F. M., and R. M. T.; investigation: M. V., P. C., C. C., and M. C.; project administration: A. A.; supervision: F. B. and F. M.; validation: A. A. and F. M.; writing—original draft: A. A. and R. M. T.; writing—review and editing: A. A., R. M. T., M. V., G. T., F. C. M., C. C., P. C., M. C., A. M., F. B., and F. M.. All authors agreed to be accountable for all aspects of the work, ensuring that questions related to the accuracy or integrity of any part of the work have been appropriately investigated and resolved. All authors revised the work critically for important intellectual content. All authors have read and agreed to the published version of the manuscript.

Corresponding author

Correspondence to Alessandro Amatu.

Ethics declarations

Ethics approval

Ethical approval was provided by the Local Ethics Committee (Comitato Etico Pavia, Pavia, Italy, protocol number 0014228/23, approval date 15/03/2023).

Consent to participate

Informed consent for data collection was obtained according to national regulations and to European General Data Protection Regulation.

Consent for publication

Not applicable.

Competing interests

FM declares fee for lectures from Hamilton Medical, GE Healthcare, SEDA Spa. The other authors declare no competing interests.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 458 KB)

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Amatu, A., Trani, R.M., Voltini, M. et al. Outbreak of Candida parapsilosis fungemia in an intensive care unit during a COVID surge: an epidemic within a pandemic. Eur J Clin Microbiol Infect Dis 42, 1347–1353 (2023). https://doi.org/10.1007/s10096-023-04670-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10096-023-04670-1

Keywords

Navigation