Candidemia Following Severe COVID-19 in Hospitalised and Critical Ill Patients: A Systematic Review and Meta-Analysis.


Journal

Mycoses
ISSN: 1439-0507
Titre abrégé: Mycoses
Pays: Germany
ID NLM: 8805008

Informations de publication

Date de publication:
Oct 2024
Historique:
revised: 27 08 2024
received: 28 07 2024
accepted: 30 08 2024
medline: 9 10 2024
pubmed: 9 10 2024
entrez: 8 10 2024
Statut: ppublish

Résumé

The epidemiology and clinical impact of COVID-19-associated candidemia (CAC) remained uncertain, leaving gaps in understanding its prevalence, risk factors and outcomes. A systematic review and meta-analysis were conducted by searching PubMed, Embase and Scopus for reports of CAC prevalence, risk factors and clinical outcomes up to June 18, 2024. The generalised linear mixed model was employed to determine the prevalence and 95% confidence intervals (CIs). The risk factors and clinical outcomes were compared between patients with and without CAC using the inverse variance method. From 81 studies encompassing 29 countries and involving 351,268 patients, the global prevalence of CAC was 4.33% (95% Cl, 3.16%-5.90%) in intensive care unit (ICU) patients. In ICUs, the pooled prevalence of CAC in high-income countries was significantly higher than that of lower-middle-income countries (5.99% [95% Cl, 4.24%-8.40%] vs. 2.23% [95% Cl, 1.06%-4.61%], p = 0.02). Resistant Candida species, including C. auris, C. glabrata (Nakaseomyces glabratus) and C. krusei (Pichia kudriavzveii), constituted 2% of ICU cases. The mortality rate for CAC was 68.40% (95% Cl, 61.86%-74.28%) among ICU patients. Several risk factors were associated with CAC, including antibiotic use, central venous catheter placement, dialysis, mechanical ventilation, tocilizumab, extracorporeal membrane oxygenation and total parenteral nutrition. Notably, the pooled odds ratio of tocilizumab was 2.59 (95% CI, 1.44-4.65). The prevalence of CAC is substantial in the ICU setting, particularly in high-income countries. Several risk factors associated with CAC were identified, including several that are modifiable, offering the opportunity to mitigate the risk of CAC.

Identifiants

pubmed: 39379339
doi: 10.1111/myc.13798
doi:

Substances chimiques

Antifungal Agents 0

Types de publication

Systematic Review Journal Article Meta-Analysis

Langues

eng

Sous-ensembles de citation

IM

Pagination

e13798

Informations de copyright

© 2024 Wiley‐VCH GmbH. Published by John Wiley & Sons Ltd.

Références

J. W. Baddley, G. R. Thompson, S. C.‐A. Chen, et al., “Coronavirus Disease 2019—Associated Invasive Fungal Infection,” Open Forum Infectious Diseases 8 (2021): ofab510.
M. Hoenigl, D. Seidel, R. Sprute, et al., “COVID‐19‐Associated Fungal Infections,” Nature Microbiology 7 (2022): 1127–1140.
F. Guo, Y. Yang, Y. Kang, et al., “Invasive Candidiasis in Intensive Care Units in China: A Multicentre Prospective Observational Study,” Journal of Antimicrobial Chemotherapy 68 (2013): 1660–1668.
J.‐L. Vincent, Y. Sakr, M. Singer, et al., “Prevalence and Outcomes of Infection Among Patients in Intensive Care Units in 2017,” JAMA 323 (2020): 1478–1487.
A. Arastehfar, A. Carvalho, M. H. Nguyen, et al., “COVID‐19‐Associated Candidiasis (CAC): An Underestimated Complication in the Absence of Immunological Predispositions?,” Journal of Fungi 6 (2020): 211.
A. Bhimraj, R. L. Morgan, A. H. Shumaker, et al., “Infectious Diseases Society of America Guidelines on the Treatment and Management of Patients With COVID‐19,” Clinical Infectious Diseases 78 (2022): ciac724, https://doi.org/10.1093/cid/ciac724.
N. Ilonzo, A. Rao, K. Soundararajan, et al., “The Importance of a Centralized Line Service During the COVID‐19 Pandemic,” Journal of Vascular Surgery 72 (2020): 403–404.
R. Thibault, P. Seguin, F. Tamion, C. Pichard, and P. Singer, “Nutrition of the COVID‐19 Patient in the Intensive Care Unit (ICU): A Practical Guidance,” Critical Care 24 (2020): 447.
D. Bouzid, B. Visseaux, C. Kassasseya, et al., “Comparison of Patients Infected With Delta Versus Omicron COVID‐19 Variants Presenting to Paris Emergency Departments: A Retrospective Cohort Study,” Annals of Internal Medicine 175 (2022): 831–837.
M. E. Modes, M. P. Directo, M. Melgar, et al., “Clinical Characteristics and Outcomes Among Adults Hospitalized With Laboratory‐Confirmed SARS‐CoV‐2 Infection During Periods of B.1.617.2 (Delta) and B.1.1.529 (Omicron) Variant Predominance—One Hospital, California, July 15‐September 23, 2021, and December 21, 2021‐January 27, 2022,” MMWR. Morbidity and Mortality Weekly Report 71 (2022): 217–223.
K. M. Hlaing, L. M. Monday, M. Nucci, S. A. Nouér, and S. G. Revankar, “Invasive Fungal Infections Associated With COVID‐19,” Journal of Fungi 9 (2023): 667.
L. Magnasco, M. Mikulska, D. R. Giacobbe, et al., “Spread of Carbapenem‐Resistant Gram‐Negatives and Candida auris During the COVID‐19 Pandemic in Critically Ill Patients: One Step Back in Antimicrobial Stewardship?,” Microorganisms 9 (2021): 95.
E. E. Seagle, B. R. Jackson, S. R. Lockhart, et al., “The Landscape of Candidemia During the Coronavirus Disease 2019 (COVID‐19) Pandemic,” Clinical Infectious Diseases 74 (2022): 802–811.
N. Vaseghi, J. Sharifisooraki, H. Khodadadi, et al., “Global Prevalence and Subgroup Analyses of Coronavirus Disease (COVID‐19) Associated Candida auris Infections (CACa): A Systematic Review and Meta‐Analysis,” Mycoses 65 (2022): 683–703.
F. Daneshnia, J. N. de Almeida Júnior, M. Ilkit, et al., “Worldwide Emergence of Fluconazole‐Resistant Candida parapsilosis: Current Framework and Future Research Roadmap,” Lancet. Microbe 4 (2023): e470–e480.
World Health Organization, “WHO Fungal Priority Pathogens List to Guide Research, Development and Public Health Action,” accessed September 9, 2023, https://www.who.int/publications‐detail‐redirect/9789240060241.
M. J. Page, J. E. McKenzie, P. M. Bossuyt, et al., “The PRISMA 2020 Statement: An Updated Guideline for Reporting Systematic Reviews,” BMJ 372 (2021): n71.
G. A. Stevens, L. Alkema, R. E. Black, et al., “Guidelines for Accurate and Transparent Health Estimates Reporting: The GATHER Statement,” Lancet 388 (2016): e19–e23.
A. Arastehfar, N. Ünal, T. Hoşbul, et al., “Candidemia Among Coronavirus Disease 2019 Patients in Turkey Admitted to Intensive Care Units: A Retrospective Multicenter Study,” Open Forum Infectious Diseases 9 (2022): ofac078.
E. Bishburg, A. Okoh, S. R. Nagarakanti, M. Lindner, C. Migliore, and P. Patel, “Fungemia in COVID‐19 ICU Patients, a Single Medical Center Experience,” Journal of Medical Virology 93 (2021): 2810–2814.
M. Blaize, A. Raoelina, D. Kornblum, et al., “Occurrence of Candidemia in Patients With COVID‐19 Admitted to Five ICUs in France,” Journal of Fungi 8 (2022): 678.
N. A. Boachie, J. P. Johnston, S. A. Philip, K. V. Sullivan, and M. Heaney, “Characteristics and Incidence of Candidemia in Hospitalized Coronavirus 2019 (COVID‐19) Patients,” American Journal of Infectious Diseases 18 (2022): 1–8.
M. A. Çavuş and H. Sav, “Opportunistic Candida Infections in Critical COVID‐19 Patients,” Polish Journal of Microbiology 71 (2022): 411–419.
D. Dixit, P. Jen, T. D. Maxwell, et al., “Risk Factors and Clinical Outcomes of Candidemia Associated With Severe COVID‐19,” Critical Care Explorations 4 (2022): e0762.
Z. B. Dursun, H. Sipahioğlu, R. C. Yüksel, H. Sav, and İ. Çelik, “Risk Factors and Lethality Associated With Candidemia in Severe COVID‐19 Patients,” Current Medical Mycology 8 (2022): 32–38.
B. Kayaaslan, F. Eser, D. Asilturk, et al., “Development and Validation of COVID‐19 Associated Candidemia Score (CAC‐Score) in ICU Patients,” Mycoses 66 (2023): 128–137.
A. S. Omrani, J. Koleri, F. Ben Abid, et al., “Clinical Characteristics and Risk Factors for COVID‐19‐Associated Candidemia,” Medical Mycology 59 (2021): 1262–1266.
E. Rajni, A. Singh, B. Tarai, et al., “A High Frequency of Candida auris Blood Stream Infections in Coronavirus Disease 2019 Patients Admitted to Intensive Care Units, Northwestern India: A Case Control Study,” Open Forum Infectious Diseases 8 (2021): ofab452.
D. Hoy, P. Brooks, A. Woolf, et al., “Assessing Risk of Bias in Prevalence Studies: Modification of an Existing Tool and Evidence of Interrater Agreement,” Journal of Clinical Epidemiology 65 (2012): 934–939.
G. Wells, B. Shea, D. O'Connell, et al., “The Newcastle‐Ottawa Scale (NOS) for Assessing the Quality of Nonrandomised Studies in Meta‐Analyses,” accessed June 20, 2020, https://www.ohri.ca/programs/clinical_epidemiology/oxford.asp.
G. H. Guyatt, A. D. Oxman, G. E. Vist, et al., “GRADE: An Emerging Consensus on Rating Quality of Evidence and Strength of Recommendations,” BMJ 336 (2008): 924–926.
World Health Organization, “Countries,” accessed September 27, 2023, https://www.who.int/countries.
N. Hamadeh, C. V. Rompaey, E. Metreau, and S. G. Eapen, “New World Bank Country Classifications by Income Level: 2022–2023,” 2022, accessed July 1, 2023, https://blogs.worldbank.org/opendata/new‐world‐bank‐country‐classifications‐income‐level‐2022‐2023.
J. P. T. Higgins and S. G. Thompson, “Quantifying Heterogeneity in a Meta‐Analysis,” Statistics in Medicine 21 (2002): 1539–1558.
J. P. T. Higgins, S. G. Thompson, J. J. Deeks, and D. G. Altman, “Measuring Inconsistency in Meta‐Analyses,” BMJ 327 (2003): 557–560.
L. Furuya‐Kanamori, J. J. Barendregt, and S. A. R. Doi, “A New Improved Graphical and Quantitative Method for Detecting Bias in Meta‐Analysis,” International Journal of Evidence‐Based Healthcare 16 (2018): 195–203.
J. P. Hunter, A. Saratzis, A. J. Sutton, R. H. Boucher, R. D. Sayers, and M. J. Bown, “In Meta‐Analyses of Proportion Studies, Funnel Plots Were Found to Be an Inaccurate Method of Assessing Publication Bias,” Journal of Clinical Epidemiology 67 (2014): 897–903.
M. A. Shamim, “Real‐Life Implications of Prevalence Meta‐Analyses? Doi Plots and Prediction Intervals Are the Answer,” Lancet Microbe 4 (2023): e490.
T. Adzic‐Vukicevic, M. Mladenovic, S. Jovanovic, I. Soldatović, and A. Radovanovic‐Spurnic, “Invasive Fungal Disease in COVID‐19 Patients: A Single‐Center Prospective Observational Study,” Frontiers in Medicine 10 (2023): 1084666.
A. Agrifoglio, L. Cachafeiro, J. C. Figueira, J. M. Añón, and A. García de Lorenzo, “Critically Ill Patients With COVID‐19 and Candidaemia: We Must Keep This in Mind,” Journal de Mycologie Médicale 30 (2020): 101012.
A. Al‐Baadani, N. Eltayeb, E. Alsufyani, et al., “Efficacy of Tocilizumab in Patients With Severe COVID‐19: Survival and Clinical Outcomes,” Journal of Infection and Public Health 14 (2021): 1021–1027.
F. Alessandri, G. Ceccarelli, G. Migliara, et al., “High Incidence of Candidemia in Critically Ill COVID‐19 Patients Supported by Veno‐Venous Extracorporeal Membrane Oxygenation: A Retrospective Study,” Journal of Fungi 9 (2023): 119.
F. Allaw, S. F. Haddad, N. Habib, et al., “COVID‐19 and C. auris: A Case‐Control Study From a Tertiary Care Center in Lebanon,” Microorganisms 10 (2022): 1011.
A. D. Alsheikh, M. A. Abdalla, M. Abdullah, and H. Hasan, “The Prevalence of Bacterial and Fungal Coinfections Among Critically Ill COVID‐19 Patients in the ICU in Jordan,” International Journal of Microbiology 2022 (2022): 9992881.
H. V. Andersen, V. R. L. Jørgensen, M. Steensen, F. M. Pedersen, and M. Helleberg, “Superinfections in COVID‐19 Patients Receiving Extracorporeal Membrane Oxygenation Support,” Acta Anaesthesiologica Scandinavica 67 (2023): 755–761.
S. S. Andreev, M. V. Ketskalo, P. O. Narusova, and M. A. Lysenko, “Secondary Infections in Patients With Extremely Severe COVID‐19 During ECMO Therapy,” Obshchaya Reanimatologiya 19 (2023): 4–13.
S. Antinori, C. Bonazzetti, G. Gubertini, et al., “Tocilizumab for Cytokine Storm Syndrome in COVID‐19 Pneumonia: An Increased Risk for Candidemia?,” Autoimmunity Reviews 19 (2020): 102564.
A. Arastehfar, T. Shaban, H. Zarrinfar, et al., “Candidemia Among Iranian Patients With Severe COVID‐19 Admitted to ICUs,” Journal of Fungi 7 (2021): 280.
P. P. Asif, R. C. Tellis, A. S. Lobo, and A. Motagi, “Blood Culture and Profile of Inflammatory Biomarkers Among COVID‐19 Patients in an Intensive Care Unit of a Tertiary Care Hospital,” Biomedicine 43 (2023): 722–727.
V. Avkan‐Oğuz, M. Çelİk, O. Ö. Eren‐Kutsoylu, et al., “Fungal Colonization and Infections in Patients With COVID‐19 in Intensive Care Units: A Real‐Life Experience at a Tertiary‐Care Hospital,” Respiratory Medicine and Research 82 (2022): 100937.
O. Ayalon, M. J. Cohen, E. Orenbuch‐Harroch, S. Sviri, P. V. van Heerden, and M. Korem, “Invasive Fungal Infections in Critically Ill COVID‐19 Patients in a Large Tertiary University Hospital in Israel,” Journal of Critical Care 69 (2022): 154004.
K. A. Bauer, K. Yu, P. A. Moise, et al., “Morbidity and Mortality of Hospitalised Patients With Candidemia During the Various Severe Acute Respiratory Syndrome Coronavirus 2 Pandemic Waves: A Multicentre Evaluation of 248 US Hospitals,” Mycoses 66 (2023): 483–487.
D. Borg, J. Farrugia, and C. M. Azzopardi, “SARS‐CoV‐2 Related ARDS and Invasive Fungal Infections in Intensive Care Patients,” Clinical Infection in Practice 13 (2022): 100127.
A. M. Borman, H. Fountain, R. Guy, et al., “Increased Mortality in COVID‐19 Patients With Fungal Co‐ and Secondary Infections Admitted to Intensive Care or High Dependency Units in NHS Hospitals in England,” Journal of Infection 84 (2022): 579–613.
S. Brikman, G. Dori, C. Kasher, et al., “Candida Bloodstream Infection, a Dire Complication in Hospitalized COVID‐19 Patients: Three Cases From a Single Center in Northern Israel,” Israel Medical Association Journal 23 (2021): 615–617.
B. J. Burger, S. M. Epps, V. M. Cardenas, R. Jagana, N. K. Meena, and W. T. Atchley, “Tocilizumab Is Associated With Increased Risk of Fungal Infections Among Critically Ill Patients With COVID‐19 and Acute Renal Failure: An Observational Cohort Study,” Lifestyles 13 (2023): 1752.
C. Campochiaro, E. Della‐Torre, G. Cavalli, et al., “Efficacy and Safety of Tocilizumab in Severe COVID‐19 Patients: A Single‐Centre Retrospective Cohort Study,” European Journal of Internal Medicine 76 (2020): 43–49.
M. A. Cataldo, N. Tetaj, M. Selleri, et al., “Incidence of Bacterial and Fungal Bloodstream Infections in COVID‐19 Patients in Intensive Care: An Alarming “Collateral Effect”,” Journal of Global Antimicrobial Resistance 23 (2020): 290–291.
L. Cattaneo, A. R. Buonomo, C. Iacovazzo, et al., “Invasive Fungal Infections in Hospitalized Patients With COVID‐19: A Non‐Intensive Care Single‐Centre Experience During the First Pandemic Waves,” Journal of Fungi 9 (2023): 86.
M. Ceccarelli, A. Marino, S. Pulvirenti, et al., “Bacterial and Fungal Co‐Infections and Superinfections in a Cohort of COVID‐19 Patients: Real‐Life Data From an Italian Third Level Hospital,” Infectious Disease Reports 14 (2022): 372–382.
A. Chowdhary, B. Tarai, A. Singh, and A. Sharma, “Multidrug‐Resistant Candida auris Infections in Critically Ill Coronavirus Disease Patients, India, April–July 2020,” Emerging Infectious Diseases 26 (2020): 2694–2696.
A. S. Coşkun and Ş. Ö. Durmaz, “Fungal Infections in COVID‐19 Intensive Care Patients,” Polish Journal of Microbiology 70 (2021): 395–400.
R. Datta, A. Barrett, M. Burk, et al., “Surveillance of Adverse Drug Events Associated With Tocilizumab in Hospitalized Veterans With Coronavirus Disease 2019 (COVID‐19) to Inform Patient Safety and Pandemic Preparedness,” Infection Control and Hospital Epidemiology 43 (2022): 1488–1491.
A. Dravid, R. Kashiva, Z. Khan, et al., “Combination Therapy of Tocilizumab and Steroid for Management of COVID‐19 Associated Cytokine Release Syndrome: A Single Center Experience From Pune, Western India,” Medicine 100 (2021): e26705.
M. Elbaz, M. Korem, O. Ayalon, et al., “Invasive Fungal Diseases in Hospitalized Patients With COVID‐19 in Israel: A Multicenter Cohort Study,” Journal of Fungi 8 (2022): 721.
M. Froidefond, J. Sevestre, H. Chaudet, and S. Ranque, “COVID‐19 Is a Confounder of Increased Candida Airway Colonisation,” Pathogens 12 (2023): 463.
J.‐P. Gangneux, E. Dannaoui, A. Fekkar, et al., “Fungal Infections in Mechanically Ventilated Patients With COVID‐19 During the First Wave: The French Multicentre MYCOVID Study,” Lancet Respiratory Medicine 10 (2022): 180–190.
C. Garcia‐Vidal, G. Sanjuan, E. Moreno‐García, et al., “Incidence of Co‐Infections and Superinfections in Hospitalized Patients With COVID‐19: A Retrospective Cohort Study,” Clinical Microbiology and Infection 27 (2021): 83–88.
I. Gregorczyk‐Maga, M. Kania, B. Sulik‐Tyszka, et al., “Oral Myco‐ and Bacteriobiota and Yeast Infections in Mechanically Ventilated COVID‐19 Patients,” Microorganisms 11 (2023): 1442.
R.‐C. Huang, C.‐H. Chiu, T.‐T. Chiang, et al., “Hospital‐Acquired Infections in Patients Hospitalized With COVID‐19: First Report From Taiwan,” Journal of the Chinese Medical Association 85 (2022): 922–927.
S. Hughes, O. Troise, H. Donaldson, N. Mughal, and L. S. P. Moore, “Bacterial and Fungal Coinfection Among Hospitalized Patients With COVID‐19: A Retrospective Cohort Study in a UK Secondary‐Care Setting,” Clinical Microbiology and Infection 26 (2020): 1395–1399.
P. Ioannou, D. P. Kofteridis, K. Alexakis, et al., “Candida Species Isolation From Hospitalized Patients With COVID‐19—A Retrospective Study,” Diagnostics 12 (2022): 3065.
A. Khavandegar, Z. Siami, S. Goudarzi, A. Rasooli, and Y. Ettehad, “Investigation of Microbial Coinfection in 453 Septic COVID‐19 Patients Admitted to Hospital; A Retrospective Study,” Future Science OA 9 (2023): FSO884.
S. Kokkoris, I. Papachatzakis, E. Gavrielatou, et al., “ICU‐Acquired Bloodstream Infections in Critically Ill Patients With COVID‐19,” Journal of Hospital Infection 107 (2021): 95–97.
E. Koukaki, N. Rovina, K. Tzannis, et al., “Fungal Infections in the ICU During the COVID‐19 Era: Descriptive and Comparative Analysis of 178 Patients,” Journal of Fungi 8 (2022): 881.
G. Kumar, A. Adams, M. Hererra, et al., “Predictors and Outcomes of Healthcare‐Associated Infections in COVID‐19 Patients,” International Journal of Infectious Diseases 104 (2021): 287–292.
P. Macauley and O. Epelbaum, “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 64 (2021): 634–640.
M. Machado, A. Estévez, C. Sánchez‐Carrillo, et al., “Incidence of Candidemia Is Higher in COVID‐19 Versus Non‐COVID‐19 Patients, but Not Driven by Intrahospital Transmission,” Journal of Fungi 8 (2022): 305.
A. C. Martins, E. M. Psaltikidis, T. C. de Lima, et al., “COVID‐19 and Invasive Fungal Coinfections: A Case Series at a Brazilian Referral Hospital,” Journal de Mycologie Médicale 31 (2021): 101175.
F. J. Membrillo de Novales, G. Ramírez‐Olivencia, M. T. Mata Forte, et al., “The Impact of Antibiotic Prophylaxis on a Retrospective Cohort of Hospitalized Patients With COVID‐19 Treated With a Combination of Steroids and Tocilizumab,” Antibiotics 12 (2023): 1515.
B. Minihan, E. McAuliffe, J. Powell, et al., “Association Between Tocilizumab Treatment of Hyperinflammatory Patients With COVID‐19 in a Critical Care Setting and Elevated Incidence of Hospital‐Acquired Bacterial and Invasive Fungal Infections,” Journal of Hospital Infection 126 (2022): 29–36.
S. Moin, J. Farooqi, S. Rattani, N. Nasir, S. Zaka, and K. Jabeen, “C. auris and Non‐C. auris Candidemia in Hospitalized Adult and Pediatric COVID‐19 Patients: Single Center Data From Pakistan,” Medical Mycology 59 (2021): 1238–1242.
M. Z. Mushtaq, S. B. Z. Mahmood, A. Almas, S. Ather Wasti, and A. S. Ahsan, “Tocilizumab in Critically Ill COVID‐19 Patients: An Observational Study,” International Immunopharmacology 102 (2022): 108384.
K. Nakagawara, H. Kamata, S. Chubachi, et al., “Diagnostic Significance of Secondary Bacteremia in Patients With COVID‐19,” Journal of Infection and Chemotherapy 29 (2023): 422–426.
E. M. Negm, M. S. Mohamed, R. A. Rabie, et al., “Fungal Infection Profile in Critically Ill COVID‐19 Patients: A Prospective Study at a Large Teaching Hospital in a Middle‐Income Country,” BMC Infectious Diseases 23 (2023): 246.
V. K. Niyas, S. D. Rahulan, R. Arjun, and A. Sasidharan, “ICU‐Acquired Candidemia in COVID‐19 Patients: An Experience From a Tertiary Care Hospital in Kerala, South India,” Indian Journal of Critical Care Medicine: Peer‐Reviewed, Official Publication of Indian Society of Critical Care Medicine 25 (2021): 1207–1208.
P. Nori, K. Cowman, V. Chen, et al., “Bacterial and Fungal Coinfections in COVID‐19 Patients Hospitalized During the New York City Pandemic Surge,” Infection Control and Hospital Epidemiology 42 (2021): 84–88.
M. Nucci, G. Barreiros, L. F. Guimarães, V. A. S. Deriquehem, A. C. Castiñeiras, and S. A. Nouér, “Increased Incidence of Candidemia in a Tertiary Care Hospital With the COVID‐19 Pandemic,” Mycoses 64 (2021): 152–156.
S. Orhan, K. Y. Gülsoy, A. Sari, and N. Demi̇rtürk, “Evaluation of Secondary Infections in COVID‐19 PatientsHospitalized in Intensive Care Unit:Retrospective Observational Study,” Turkiye Klinikleri Journal of Medical Sciences 42 (2022): 164–170.
N. Pandak, F. Khamis, Z. Al Balushi, et al., “Low Rate of Bacterial Coinfections and Antibiotic Overprescribing During COVID‐19 Pandemic: A Retrospective Study From Oman,” Oman Medical Journal 38 (2023): e525.
M. Papadimitriou‐Olivgeris, F. Kolonitsiou, S. Kefala, et al., “Increased Incidence of Candidemia in Critically Ill Patients During the Coronavirus Disease 2019 (COVID‐19) Pandemic,” Brazilian Journal of Infectious Diseases 26 (2022): 102353.
B. Posteraro, G. De Angelis, G. Menchinelli, et al., “Risk Factors for Mortality in Adult COVID‐19 Patients Who Develop Bloodstream Infections Mostly Caused by Antimicrobial‐Resistant Organisms: Analysis at a Large Teaching Hospital in Italy,” Journal of Clinical Medicine 10 (2021): 1752.
C. M. Roman‐Montes, S. Bojorges‐Aguilar, E. A. Corral‐Herrera, et al., “Fungal Infections in the ICU During the COVID‐19 Pandemic in Mexico,” Journal of Fungi 9 (2023): 583.
F. Romanelli, S. Stolfa, L. Ronga, et al., “Coinfections in Intensive Care Units. Has Anything Changed With Covid‐19 Pandemia?,” Acta Biomed 94 (2023): e2023075.
R. Rossotti, G. Travi, N. Ughi, et al., “Safety and Efficacy of Anti‐il6‐Receptor Tocilizumab Use in Severe and Critical Patients Affected by Coronavirus Disease 2019: A Comparative Analysis,” Journal of Infection 81 (2020): e11–e17.
C. Routsi, J. Meletiadis, E. Charitidou, et al., “Epidemiology of Candidemia and Fluconazole Resistance in an ICU Before and During the COVID‐19 Pandemic Era,” Antibiotics 11 (2022): 771.
A. Saade, G. Moratelli, G. Dumas, et al., “Infectious Events in Patients With Severe COVID‐19: Results of a Cohort of Patients With High Prevalence of Underlying Immune Defect,” Annals of Intensive Care 11 (2021): 83.
L. Sang, Y. Xi, Z. Lin, et al., “Secondary Infection in Severe and Critical COVID‐19 Patients in China: A Multicenter Retrospective Study,” Annals of Palliative Medicine 10 (2021): 8557–8570.
H. K. Sarvestani, S. Mahmoudi, P. Afarinesh Khaki, et al., “Epidemiology, Risk Factors, Species Distribution, and Antifungal Susceptibility of Candidemia Among Hospitalized Patients With COVID‐19,” Current Medical Mycology 7 (2021): 12–18.
T. Seitz, J. Holbik, J. Hind, et al., “Rapid Detection of Bacterial and Fungal Pathogens Using the T2MR Versus Blood Culture in Patients With Severe COVID‐19,” Microbiology Spectrum 10 (2022): e0014022.
D. L. Silva, C. M. Lima, V. C. R. Magalhães, et al., “Fungal and Bacterial Coinfections Increase Mortality of Severely Ill COVID‐19 Patients,” Journal of Hospital Infection 113 (2021): 145–154.
E. C. Somers, G. A. Eschenauer, J. P. Troost, et al., “Tocilizumab for Treatment of Mechanically Ventilated Patients With COVID‐19,” Clinical Infectious Diseases 73 (2021): e445–e454.
B. G. Szabo, B. Lakatos, I. Bobek, E. Szabo, J. Szlavik, and I. Vályi‐Nagy, “Invasive Fungal Infections Among Critically Ill Adult COVID‐19 Patients: First Experiences From the National Centre in Hungary,” Journal de Mycologie Médicale 31 (2021): 101198.
L. Taramasso, L. Magnasco, F. Portunato, et al., “Clinical Presentation of Secondary Infectious Complications in COVID‐19 Patients in Intensive Care Unit Treated With Tocilizumab or Standard of Care,” European Journal of Internal Medicine 94 (2021): 39–44.
G. Tiseo, V. Galfo, S. Occhineri, et al., “Risk Factors and Outcomes of Fungal Superinfections in Patients With Severe COVID‐19: An Observational Study From Pisa Academic Hospital,” Le Infezioni in Medicina 31 (2022): 55–61.
P. L. White, R. Dhillon, A. Cordey, et al., “A National Strategy to Diagnose Coronavirus Disease 2019‐Associated Invasive Fungal Disease in the Intensive Care Unit,” Clinical Infectious Diseases 73 (2021): e1634–e1644.
H. Zhang, Y. Zhang, J. Wu, et al., “Risks and Features of Secondary Infections in Severe and Critical Ill COVID‐19 Patients,” Emerging Microbes & Infections 9 (2020): 1958–1964.
J. Zhang, P. Lan, J. Yi, et al., “Secondary Bloodstream Infection in Critically Ill Patients With COVID‐19,” Journal of International Medical Research 49 (2021): 3000605211062783.
P. G. Pappas, M. S. Lionakis, M. C. Arendrup, L. Ostrosky‐Zeichner, and B. J. Kullberg, “Invasive candidiasis,” Nature Reviews Disease Primers 4 (2018): 18026.
V. Soulountsi, T. Schizodimos, and S. C. Kotoulas, “Deciphering the Epidemiology of Invasive Candidiasis in the Intensive Care Unit: Is It Possible?,” Infection 49 (2021): 1107–1131.
F. Lamoth, S. R. Lockhart, E. L. Berkow, and T. Calandra, “Changes in the Epidemiological Landscape of Invasive Candidiasis,” Journal of Antimicrobial Chemotherapy 73 (2018): i4–i13.
F. Bongomin, S. Gago, R. O. Oladele, and D. W. Denning, “Global and Multi‐National Prevalence of Fungal Diseases‐Estimate Precision,” Journal of Fungi 3 (2017): 57.
B. Ortiz, K. Aguilar, C. Galindo, L. Molina, and G. Fontecha, “Candida Species Isolated From Clinical Samples in a Tertiary Hospital in Honduras: Where Is Candida auris?,” Current Medical Mycology 8 (2022): 1–8.
A. J. Browne, M. G. Chipeta, G. Haines‐Woodhouse, et al., “Global Antibiotic Consumption and Usage in Humans, 2000–18: A Spatial Modelling Study,” Lancet Planetary Health 5 (2021): e893–e904.
E. J. Harvey, C. De Brún, E. Casale, V. Finistrella, and D. Ashiru‐Oredope, “Influence of Factors Commonly Known to Be Associated With Health Inequalities on Antibiotic Use in High‐Income Countries: A Systematic Scoping Review,” Journal of Antimicrobial Chemotherapy 78 (2023): 861–870.
E. Y. Klein, T. P. Van Boeckel, E. M. Martinez, et al., “Global Increase and Geographic Convergence in Antibiotic Consumption Between 2000 and 2015,” Proceedings of the National Academy of Sciences of the United States of America 115 (2018): E3463–E3470.
Z.‐D. Pana, E. Farmaki, and E. Roilides, “Host Genetics and Opportunistic Fungal Infections,” Clinical Microbiology and Infection 20 (2014): 1254–1264.
J. D. Jenks, C. I. Aneke, M. M. Al‐Obaidi, et al., “Race and Ethnicity: Risk Factors for Fungal Infections?,” PLoS Pathogens 19 (2023): e1011025.
M. A. Pfaller, G. J. Moet, S. A. Messer, R. N. Jones, and M. Castanheira, “Candida Bloodstream Infections: Comparison of Species Distributions and Antifungal Resistance Patterns in Community‐Onset and Nosocomial Isolates in the SENTRY Antimicrobial Surveillance Program, 2008–2009,” Antimicrobial Agents and Chemotherapy 55 (2011): 561–566.
A. A. Cleveland, M. M. Farley, L. H. Harrison, et al., “Changes in Incidence and Antifungal Drug Resistance in Candidemia: Results From Population‐Based Laboratory Surveillance in Atlanta and Baltimore, 2008–2011,” Clinical Infectious Diseases 55 (2012): 1352–1361.
B. Posteraro, T. Spanu, B. Fiori, et al., “Antifungal Susceptibility Profiles of Bloodstream Yeast Isolates by Sensititre YeastOne Over Nine Years at a Large Italian Teaching Hospital,” Antimicrobial Agents and Chemotherapy 59 (2015): 3944–3955.
D. J. Sexton, M. L. Bentz, R. M. Welsh, et al., “Positive Correlation Between Candida auris Skin‐Colonization Burden and Environmental Contamination at a Ventilator‐Capable Skilled Nursing Facility in Chicago,” Clinical Infectious Diseases 73 (2021): 1142–1148.
R. Biran, R. Cohen, T. Finn, et al., “Nationwide Outbreak of Candida auris Infections Driven by COVID‐19 Hospitalizations, Israel, 2021–2022,” Emerging Infectious Diseases 29 (2023): 1297–1301.
C. Prestel, E. Anderson, K. Forsberg, et al., “Candida auris Outbreak in a COVID‐19 Specialty Care Unit—Florida, July–August 2020,” MMWR. Morbidity and Mortality Weekly Report 70 (2021): 56–57.
J. Y. Rodriguez, P. Le Pape, O. Lopez, K. Esquea, A. L. Labiosa, and C. Alvarez‐Moreno, “Candida auris: A Latent Threat to Critically Ill Patients With Coronavirus Disease 2019,” Clinical Infectious Diseases 73 (2021): e2836–e2837.
H. Villanueva‐Lozano, R. J. De Treviño‐Rangel, G. M. González, et al., “Outbreak of Candida auris Infection in a COVID‐19 Hospital in Mexico,” Clinical Microbiology and Infection 27 (2021): 813–816.
R. Nelson, “Emergence of Resistant Candida auris,” Lancet Microbe 4 (2023): e396.
O. Dire, A. Ahmad, S. Duze, and M. Patel, “Survival of Candida auris on Environmental Surface Materials and Low‐Level Resistance to Disinfectant,” Journal of Hospital Infection 137 (2023): 17–23.
F. Lamoth and D. P. Kontoyiannis, “The Candida auris Alert: Facts and Perspectives,” Journal of Infectious Diseases 217 (2018): 516–520.
M. Lyman, K. Forsberg, J. Reuben, et al., “Notes From the Field: Transmission of Pan‐Resistant and Echinocandin‐Resistant Candida auris in Health Care Facilities—Texas and the District of Columbia, January–April 2021,” MMWR. Morbidity and Mortality Weekly Report 70 (2021): 1022–1023.
National Institute for Health and Care Excellence, “COVID‐19 Rapid Guideline: Managing COVID‐19,” 2021, https://www.nice.org.uk/guidance/ng191.
B. J. Langford, M. So, S. Raybardhan, et al., “Antibiotic Prescribing in Patients With COVID‐19: Rapid Review and Meta‐Analysis,” Clinical Microbiology and Infection 27 (2021): 520–531.
H. Getahun, I. Smith, K. Trivedi, S. Paulin, and H. H. Balkhy, “Tackling Antimicrobial Resistance in the COVID‐19 Pandemic,” Bulletin of the World Health Organization 98 (2020): 442–442A.
B. D. Huttner, G. Catho, J. R. Pano‐Pardo, C. Pulcini, and J. Schouten, “COVID‐19: Don't Neglect Antimicrobial Stewardship Principles!,” Clinical Microbiology and Infection 26 (2020): 808–810.
J. Pierce and M. P. Stevens, “COVID‐19 and Antimicrobial Stewardship: Lessons Learned, Best Practices, and Future Implications,” International Journal of Infectious Diseases 113 (2021): 103–108.
K. Blot, J. Bergs, D. Vogelaers, S. Blot, and D. Vandijck, “Prevention of Central Line‐Associated Bloodstream Infections Through Quality Improvement Interventions: A Systematic Review and Meta‐Analysis,” Clinical Infectious Diseases 59 (2014): 96–105.
L. Papazian, M. Klompas, and C.‐E. Luyt, “Ventilator‐Associated Pneumonia in Adults: A Narrative Review,” Intensive Care Medicine 46 (2020): 888–906.
P. Cotogni, “Management of Parenteral Nutrition in Critically Ill Patients,” World Journal of Critical Care Medicine 6 (2017): 13–20.
T. Avni, L. Leibovici, and M. Paul, “PCR Diagnosis of Invasive Candidiasis: Systematic Review and Meta‐Analysis,” Journal of Clinical Microbiology 49 (2011): 665–670.

Auteurs

Karan Srisurapanont (K)

Faculty of Medicine, Chiang Mai University, Chiang Mai, Thailand.

Bhoowit Lerttiendamrong (B)

Faculty of Medicine, Chulalongkorn University, Bangkok, Thailand.

Tanaporn Meejun (T)

Faculty of Medicine, Chiang Mai University, Chiang Mai, Thailand.

Jaedvara Thanakitcharu (J)

Panyananthaphikkhu Cholprathan Medical Center, Srinakharinwirot University, Nonthaburi, Thailand.

Kasama Manothummetha (K)

Department of Medicine, Johns Hopkins University School of Medicine, Baltimore, Maryland, USA.

Achitpol Thongkam (A)

Department of Microbiology, Faculty of Medicine, Chulalongkorn University, Bangkok, Thailand.

Nipat Chuleerarux (N)

Department of Medicine, University of Miami/Jackson Memorial Hospital, Miami, Florida, USA.

Anawin Sanguankeo (A)

Department of Preventive and Social Medicine, Faculty of Medicine Siriraj Hospital, Mahidol University, Bangkok, Thailand.

Lucy X Li (LX)

Department of Medicine, Johns Hopkins University School of Medicine, Baltimore, Maryland, USA.

Surachai Leksuwankun (S)

Department of Medicine, Faculty of Medicine, Chulalongkorn University and King Chulalongkorn Memorial Hospital, Bangkok, Thailand.
Thai Red Cross Emerging Infectious Diseases Clinical Center, King Chulalongkorn Memorial Hospital, Bangkok, Thailand.

Nattapong Langsiri (N)

Panyananthaphikkhu Cholprathan Medical Center, Srinakharinwirot University, Nonthaburi, Thailand.

Pattama Torvorapanit (P)

Department of Medicine, Faculty of Medicine, Chulalongkorn University and King Chulalongkorn Memorial Hospital, Bangkok, Thailand.
Thai Red Cross Emerging Infectious Diseases Clinical Center, King Chulalongkorn Memorial Hospital, Bangkok, Thailand.

Navaporn Worasilchai (N)

Department of Transfusion Medicine and Clinical Microbiology, Faculty of Allied Health Sciences, and Research Unit of Medical Mycology Diagnosis, Chulalongkorn University, Bangkok, Thailand.

Rongpong Plongla (R)

Department of Medicine, Faculty of Medicine, Chulalongkorn University and King Chulalongkorn Memorial Hospital, Bangkok, Thailand.

Chatphatai Moonla (C)

Department of Medicine, Faculty of Medicine, Chulalongkorn University and King Chulalongkorn Memorial Hospital, Bangkok, Thailand.
Center of Excellence in Translational Hematology, Faculty of Medicine, Chulalongkorn University and King Chulalongkorn Memorial Hospital, Bangkok, Thailand.

Saman Nematollahi (S)

Department of Medicine, University of Arizona College of Medicine, Tucson, Arizona, USA.

Olivia S Kates (OS)

Department of Medicine, Johns Hopkins University School of Medicine, Baltimore, Maryland, USA.

Nitipong Permpalung (N)

Department of Medicine, Johns Hopkins University School of Medicine, Baltimore, Maryland, USA.
Department of Microbiology, Faculty of Medicine, Chulalongkorn University, Bangkok, Thailand.

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