Candida auris: outbreak fungal pathogen in COVID-19 pandemic: a systematic review and meta-analysis
-
Kamran Bagheri Lankarani
,
Maryam Akbari
,
Reza Tabrizi
,
Mohebat Vali
,
Eghbal Sekhavati
,
Seyed Taghi Heydari
,
Hossein Khodadadi
,
Fariba Ahmadizar
Abstract
Background and Objectives: Candida auris (C. auris) is the first fungal pathogen considered a global health threat. Because, C. auris is associated with multidrug resistance and associated diseases such as diabetes, sepsis, lung and kidney disease. This study investigated the prevalence and mortality of C. auris infection during Covid-19 pandemic.
Materials and Methods: Databases were searched for peer-reviewed articles published in the English language up to Jan 18, 2022. Heterogeneity across studies was evaluated using Cochrane’s Q test and the I2 index. The pooled point prevalences and their corresponding 95% confidence intervals (CIs) were estimated usingthe random-effects model.
Results: In our meta-analysis, 11 eligible articles were included. The total pooled prevalence estimation of C. auris infection among COVID-19 patients was 13% (95% CI: 8%, 19%). The estimated pooled mortality rate of C. auris infection was 37% (95% CI: 15%, 61%). In terms of specific conditions, the pooled risk of mortality was higher in people with diabetes 65% (95% CI: 0.45%, 83%), in cases with >21 days admission inintensive care unit (ICU) 44% (95% CI: 21%, 0.68%), and after receiving steroids 43% (95% CI: 18%, 69%).
Conclusion: Our study highlights the high prevalence rate of C. auris infection, particularly among people with a history of metabolic disorders.
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2. Goyal P, Choi JJ, Pinheiro LC, Schenck EJ, Chen R, Jabri A, et al. Clinical Characteristics of Covid-19 in New York City. N Engl J Med 2020; 382:2372-2374.
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9. Sabino R, Veríssimo C, Pereira ÁA, Antunes F. Candida auris, an agent of hospital-associated outbreaks: which challenging issues do we need to have in mind? Microorganisms 2020; 8:181.
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14. Chow NA, de Groot T, Badali H, Abastabar M, Chiller TM, Meis JF. Potential fifth clade of Candida auris, Iran, 2018. Emerg Infect Dis 2019; 25:1780-1781.
15. Emara M, Ahmad S, Khan Z, Joseph L, Al-Obaid Im, Purohit P, et al. Candida auris candidemia in Kuwait, 2014. Emerg Infect Dis 2015; 21:1091-1092.
16. Khan Z, Ahmad S, Benwan K, Purohit P, Al-Obaid I, Bafna R, et al. Invasive Candida auris infections in Kuwait hospitals: epidemiology, antifungal treatment and outcome. Infection 2018; 46:641-650.
17. Ahmad S, Khan Z, Al-Sweih N, Alfouzan W, Joseph L. Candida auris in various hospitals across Kuwait and their susceptibility and molecular basis of resistance to antifungal drugs. Mycoses 2020; 63:104-112.
18. Ben-Ami R, Berman J, Novikov A, Bash E, Shachor-Meyouhas Y, Zakin S, et al. Multidrug-resistant candida haemulonii and C. auris, Tel Aviv, Israel. Emerg Infect Dis 2017; 23:195-203.
19. Mohsin J, Hagen F, Al-Balushi ZAM, de Hoog GS, Chowdhary A, Meis JF, et al. The first cases of Candida auris candidaemia in Oman. Mycoses 2017; 60:569-575.
20. Al Maani A, Paul H, Al-Rashdi A, Al Wahaibi A, Al-Jardani A, Al Abri AMA, et al. Ongoing challenges with healthcare-associated Candida auris outbreaks in Oman. J Fungi (Basel) 2019; 5:101.
21. Abdalhamid B, Almaghrabi R, Althawadi S, Omrani A. First report of Candida auris infections from Saudi Arabia. J Infect Public Health 2018; 11:598-599.
22. Almaghrabi RS, Albalawi R, Mutabagani M, Atienza E, Aljumaah S, Gade L, et al. Molecular characterisation and clinical outcomes of Candida auris infection: Single‐centre experience in Saudi Arabia. Mycoses 2020; 63:452-460.
23. Alatoom A, Sartawi M, Lawlor K, AbdelWareth L, Thomsen J, Nusair A, et al. Persistent candidemia despite appropriate fungal therapy: first case of Candida auris from the United Arab Emirates. Int J Infect Dis 2018; 70:36-37.
24. Abastabar M, Haghani I, Ahangarkani F, Rezai MS, Taghizadeh Armaki M, Roodgari S, et al. Candida auris otomycosis in Iran and review of recent literature. Mycoses 2019; 62:101-105.
25. Shaukat A, Al Ansari N, Al Wali W, Karic E, El Madhoun I, Mitwally H, et al. Experience of treating Candida auris cases at a general hospital in the state of Qatar. IDCases 2021; 23: e01007.
26. Moola S, Munn Z, Sears K, Sfetcu R, Currie M, Lisy K, et al. Conducting systematic reviews of association (etiology): the Joanna Briggs Institute's approach. Int J Evid Based Healthc 2015; 13:163-169.
27. Dos Santos WM, Aromataris E, Secoli SR, Matuoka JY. Cost-effectiveness of antimicrobial treatment for inpatients with carbapenem-resistant Klebsiella pneumoniae infection: a systematic review of economic evidence. JBI Database System Rev Implement Rep 2019; 17:2417-2451.
28. Allaw F, Kara Zahreddine N, Ibrahim A, Tannous J, Taleb H, Bizri AR, et al. First Candida auris outbreak during a COVID-19 pandemic in a tertiary-care center in Lebanon. Pathogens 2021;10:157.
29. Chowdhary A, Tarai B, Singh A, Sharma A. Multidrug-resistant Candida auris infections in critically Ill Coronavirus disease patients, India, April–July 2020. Emerg Infect Dis 2020; 26:2694-2696.
30. Pilato VD, Codda G, Ball L, Giacobbe DR, Willison E, Mikulska M, et al. Molecular epidemiological investigation of a nosocomial cluster of C. auris: evidence of recent emergence in Italy and ease of transmission during the COVID-19 pandemic. J Fungi (Basel) 2021; 7:140.
31. Pemán J, Ruiz-Gaitán A, García-Vidal C, Salavert M, Ramírez P, Puchades F, et al. Fungal co-infection in COVID-19 patients: Should we be concerned? Rev Iberoam Micol 2020; 37:41-46.
32. Prestel C, Anderson E, Forsberg K, Lyman M, de Perio MA, Kuhar D, et al. Candida auris outbreak in a COVID-19 specialty care unit—Florida, July–August 2020. MMWR 2021; 70:56-57.
33. Rodriguez JY, Le Pape P, Lopez O, Esquea K, Labiosa AL, Alvarez-Moreno C. Candida auris: A latent threat to critically Ill patients with Coronavirus disease 2019. Clin Infect Dis 2021;73(9):e2836-e2837.
34. Villanueva-Lozano H, Treviño-Rangel RdJ, González GM, Ramírez-Elizondo MT, Lara-Medrano R, Aleman-Bocanegra MC, et al. Outbreak of Candida auris infection in a COVID-19 hospital in Mexico. Clin Microbiol Infect 2021;27:813-816.
35. Zuo T, Zhan H, Zhang F, Liu Q, Tso EY, Lui GC, et al. Alterations in fecal fungal microbiome of patients with COVID-19 during time of hospitalization until discharge. Gastroenterology 2020; 159:1302-1310.e5.
36. Price TK, Mirasol R, Ward KW, Dayo AJ, Hilt EE, Chandrasekaran S, et al. Genomic Characterizations of Clade III Lineage of Candida auris, California, USA. Emerg Infect Dis 2021; 27:1223-1227.
37. 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.
38. Weber DJ, Sickbert-Bennett EE, Kanamori H, Rutala WA. New and emerging infectious diseases (Ebola, Middle Eastern respiratory syndrome coronavirus, carbapenem-resistant Enterobacteriaceae, Candida auris): Focus on environmental survival and germicide susceptibility. Am J Infect Control 2019; 47S:A29-A38.
2. Goyal P, Choi JJ, Pinheiro LC, Schenck EJ, Chen R, Jabri A, et al. Clinical Characteristics of Covid-19 in New York City. N Engl J Med 2020; 382:2372-2374.
3. Mendelson M, Matsoso MP. The World Health Organization Global Action Plan for antimicrobial resistance. S Afr Med J 2015; 105:325.
4. Christaki E, Marcou M, Tofarides A. Antimicrobial resistance in bacteria: mechanisms, evolution, and persistence. J Mol Evol 2020; 88:26-40.
5. Magnasco L, Mikulska M, Giacobbe DR, Taramasso L, Vena A, Dentone C, 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 2021; 9:95.
6. 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; 53:41-44.
7. Meis JF, Chowdhary A. Candida auris: a global fungal public health threat. Lancet Infect Dis 2018; 18:1298-1299.
8. Cortegiani A, Misseri G, Fasciana T, Giammanco A, Giarratano A, Chowdhary A. Epidemiology, clinical characteristics, resistance, and treatment of infections by Candida auris. J Intensive Care 2018; 6:69.
9. Sabino R, Veríssimo C, Pereira ÁA, Antunes F. Candida auris, an agent of hospital-associated outbreaks: which challenging issues do we need to have in mind? Microorganisms 2020; 8:181.
10. Sharma C, Kumar N, Pandey R, Meis JF, Chowdhary A. Whole genome sequencing of emerging multidrug resistant Candida auris isolates in India demonstrates low genetic variation. New Microbes New Infect 2016; 13:77-82.
11. Romera D, Aguilera-Correa JJ, Gadea I, Viñuela-Sandoval L, García-Rodríguez J, Esteban J. Candida auris: a comparison between planktonic and biofilm susceptibility to antifungal drugs. J Med Microbiol 2019; 68:1353-1358.
12. Lockhart SR, Etienne KA, Vallabhaneni S, Farooqi J, Chowdhary A, Govender NP, et al. 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.
13. Mahmoudi S, Agha Kuchak Afshari S, Aghaei Gharehbolagh S, Mirhendi H, Makimura K. Methods for identification of Candida auris, the yeast of global public health concern: A review. J Mycol Med 2019; 29:174-179.
14. Chow NA, de Groot T, Badali H, Abastabar M, Chiller TM, Meis JF. Potential fifth clade of Candida auris, Iran, 2018. Emerg Infect Dis 2019; 25:1780-1781.
15. Emara M, Ahmad S, Khan Z, Joseph L, Al-Obaid Im, Purohit P, et al. Candida auris candidemia in Kuwait, 2014. Emerg Infect Dis 2015; 21:1091-1092.
16. Khan Z, Ahmad S, Benwan K, Purohit P, Al-Obaid I, Bafna R, et al. Invasive Candida auris infections in Kuwait hospitals: epidemiology, antifungal treatment and outcome. Infection 2018; 46:641-650.
17. Ahmad S, Khan Z, Al-Sweih N, Alfouzan W, Joseph L. Candida auris in various hospitals across Kuwait and their susceptibility and molecular basis of resistance to antifungal drugs. Mycoses 2020; 63:104-112.
18. Ben-Ami R, Berman J, Novikov A, Bash E, Shachor-Meyouhas Y, Zakin S, et al. Multidrug-resistant candida haemulonii and C. auris, Tel Aviv, Israel. Emerg Infect Dis 2017; 23:195-203.
19. Mohsin J, Hagen F, Al-Balushi ZAM, de Hoog GS, Chowdhary A, Meis JF, et al. The first cases of Candida auris candidaemia in Oman. Mycoses 2017; 60:569-575.
20. Al Maani A, Paul H, Al-Rashdi A, Al Wahaibi A, Al-Jardani A, Al Abri AMA, et al. Ongoing challenges with healthcare-associated Candida auris outbreaks in Oman. J Fungi (Basel) 2019; 5:101.
21. Abdalhamid B, Almaghrabi R, Althawadi S, Omrani A. First report of Candida auris infections from Saudi Arabia. J Infect Public Health 2018; 11:598-599.
22. Almaghrabi RS, Albalawi R, Mutabagani M, Atienza E, Aljumaah S, Gade L, et al. Molecular characterisation and clinical outcomes of Candida auris infection: Single‐centre experience in Saudi Arabia. Mycoses 2020; 63:452-460.
23. Alatoom A, Sartawi M, Lawlor K, AbdelWareth L, Thomsen J, Nusair A, et al. Persistent candidemia despite appropriate fungal therapy: first case of Candida auris from the United Arab Emirates. Int J Infect Dis 2018; 70:36-37.
24. Abastabar M, Haghani I, Ahangarkani F, Rezai MS, Taghizadeh Armaki M, Roodgari S, et al. Candida auris otomycosis in Iran and review of recent literature. Mycoses 2019; 62:101-105.
25. Shaukat A, Al Ansari N, Al Wali W, Karic E, El Madhoun I, Mitwally H, et al. Experience of treating Candida auris cases at a general hospital in the state of Qatar. IDCases 2021; 23: e01007.
26. Moola S, Munn Z, Sears K, Sfetcu R, Currie M, Lisy K, et al. Conducting systematic reviews of association (etiology): the Joanna Briggs Institute's approach. Int J Evid Based Healthc 2015; 13:163-169.
27. Dos Santos WM, Aromataris E, Secoli SR, Matuoka JY. Cost-effectiveness of antimicrobial treatment for inpatients with carbapenem-resistant Klebsiella pneumoniae infection: a systematic review of economic evidence. JBI Database System Rev Implement Rep 2019; 17:2417-2451.
28. Allaw F, Kara Zahreddine N, Ibrahim A, Tannous J, Taleb H, Bizri AR, et al. First Candida auris outbreak during a COVID-19 pandemic in a tertiary-care center in Lebanon. Pathogens 2021;10:157.
29. Chowdhary A, Tarai B, Singh A, Sharma A. Multidrug-resistant Candida auris infections in critically Ill Coronavirus disease patients, India, April–July 2020. Emerg Infect Dis 2020; 26:2694-2696.
30. Pilato VD, Codda G, Ball L, Giacobbe DR, Willison E, Mikulska M, et al. Molecular epidemiological investigation of a nosocomial cluster of C. auris: evidence of recent emergence in Italy and ease of transmission during the COVID-19 pandemic. J Fungi (Basel) 2021; 7:140.
31. Pemán J, Ruiz-Gaitán A, García-Vidal C, Salavert M, Ramírez P, Puchades F, et al. Fungal co-infection in COVID-19 patients: Should we be concerned? Rev Iberoam Micol 2020; 37:41-46.
32. Prestel C, Anderson E, Forsberg K, Lyman M, de Perio MA, Kuhar D, et al. Candida auris outbreak in a COVID-19 specialty care unit—Florida, July–August 2020. MMWR 2021; 70:56-57.
33. Rodriguez JY, Le Pape P, Lopez O, Esquea K, Labiosa AL, Alvarez-Moreno C. Candida auris: A latent threat to critically Ill patients with Coronavirus disease 2019. Clin Infect Dis 2021;73(9):e2836-e2837.
34. Villanueva-Lozano H, Treviño-Rangel RdJ, González GM, Ramírez-Elizondo MT, Lara-Medrano R, Aleman-Bocanegra MC, et al. Outbreak of Candida auris infection in a COVID-19 hospital in Mexico. Clin Microbiol Infect 2021;27:813-816.
35. Zuo T, Zhan H, Zhang F, Liu Q, Tso EY, Lui GC, et al. Alterations in fecal fungal microbiome of patients with COVID-19 during time of hospitalization until discharge. Gastroenterology 2020; 159:1302-1310.e5.
36. Price TK, Mirasol R, Ward KW, Dayo AJ, Hilt EE, Chandrasekaran S, et al. Genomic Characterizations of Clade III Lineage of Candida auris, California, USA. Emerg Infect Dis 2021; 27:1223-1227.
37. 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.
38. Weber DJ, Sickbert-Bennett EE, Kanamori H, Rutala WA. New and emerging infectious diseases (Ebola, Middle Eastern respiratory syndrome coronavirus, carbapenem-resistant Enterobacteriaceae, Candida auris): Focus on environmental survival and germicide susceptibility. Am J Infect Control 2019; 47S:A29-A38.
| Files | ||
| Issue | Vol 14 No 3 (2022) | |
| Section | Review Article(s) | |
| DOI | https://doi.org/10.18502/ijm.v14i3.9753 | |
| Keywords | ||
| Candida auris infection; COVID-19; Disease outbreaks; Meta-analysis | ||
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How to Cite
1.
Lankarani K, Akbari M, Tabrizi R, Vali M, Sekhavati E, Heydari ST, Khodadadi H, Ahmadizar F. Candida auris: outbreak fungal pathogen in COVID-19 pandemic: a systematic review and meta-analysis. Iran J Microbiol. 2022;14(3):276-284.
