Severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2), the most significant global health event since Spanish influenza in the early 20th century, is alarmingly on the rising and threatens human health and public safety [ 1 , 2 ]. Unlike influenza outbreaks, coronavirus disease 2019 (COVID-19) has spread fast all over the world, and over 100 countries have reported cases of this disease [ 1 , 3 , 4 ]. SARS-CoV-2 ranks third among members of the Coronavirus family regarding its pathogenicity; however, due to its rapid spreading, it has posed the severest threat to global health in this century [ 1 ].
The hospital mortality of COVID-19 is estimated to range from 15% to 20% and increases to 40% among patients requiring intensive care unit (ICU) admission [ 5 ]. Meanwhile, early estimates suggested that the true burden of disease and an actual number of deaths may be as much as 10 times higher than reported cases [ 4 , 6 , 7 ]. Patients with severe COVID-19 need intensive care, including mechanical ventilation, extracorporeal membrane oxygenation, continuous renal replacement therapy, glucocorticoids, and intravenous immune-globulin therapy. These interventions could predispose patients to co-infections by different microorganisms including fungi (both filamentous fungi and yeasts) [ 8 - 10 ]. Co-infections by Candida auris, due to its persistence on hospital surfaces and high resistance to antifungal drugs, are of significant value, and COVID-19 has provided a potential bed for these infections [ 11 , 12 ]. Patients admitted to ICU have the greatest risk factors for such infections [ 11 , 13 ].
Antimicrobial resistance (AMR) as another threat to global health and the economy is likely to be overshadowed by the COVID-19 pandemic [ 2 ]. Currently, infections caused by antimicrobial-resistant pathogens are responsible for nearly 700,000 deaths every year worldwide. It can be anticipated that AMR-related deaths due to the catastrophe status of the COVID-19 pandemic can reach up to 10 million deaths per year by 2050 if the world could not tackle these current states [ 14 , 15 ].
So far, cases or outbreaks of C. auris infection/colonization among COVID-19 patients have been reported [ 16 - 18 ]. In this study, we have a particular focus on the C. auris infection/colonization in patients with COVID-19 and the potential impact of this viral pandemic on antifungal drug resistance.
Candida auris in the era of COVID-19
C. auris, first isolated in Japan in 2009, is an emerging member of the Metschnikowiaceae family within the Candida/Clavispora clade [ 19 ]. To date, C. auris has been reported from at least 40 countries; therefore, it has a global distribution [ 11 , 20 , 21 ]. C. auris has been isolated as an infecting or colonizing agent from various specimens or parts of the human body including blood, urine, wounds, bile, the nares, the skin, the axilla, and the rectum of patients [ 22 , 23 ]. Furthermore, this fungus can survive on environmental surfaces and human skin for several weeks and can even tolerate some frequently used disinfectants [ 24 - 26 ]. These traits can be associated with intrahospital transmission of C. auris, leading to outbreaks [ 27 , 28 ]. In the past decade, C. auris has led to several outbreaks in hospitals worldwide and become a global health threat [ 29 ]. Invasive infections by this pathogen are usually observed in critically ill patients in ICUs and are related to high mortality rates [ 30 ].
COVID-19 has presented a great challenge for health care settings. During this viral pandemic, patients admitted to ICUs are at the greatest risk for C. auris infection/colonization [ 31 ]. In the second half of 2020, several countries, such as India, Lebanon, Italy, Brazil, Guatemala, Mexico, Peru, Panama, Colombia, and the United States, reported cases/outbreaks of co-infection by C. auris in COVID-19 patients. [ 32 - 35 ]. Accordingly, attention should be drawn to this topic to characterize various features of these co-infections. By a literature review up to September 12, 2022, 27 studies were found, of which data of COVID-19-associated C. auris infections were extractable in 14 studies (75 cases, Table 1).
|Ref.||Publication Year||Country||Sex||Age||Underlying Conditions||Risk Factors||Clade (I,II,III,IV,V)||Site of infection OR Colonization||Resistance Pattern||Hospital stay (day)||Antifungal Treatment||Outcome|
|[ 12 ]||2020||Mexico||M||51||HT, DS, Obesity||MV, PICCs, UC, Antibiotic use, Steroid therapy||IV||Blood||AMB, FLC||20-70||CAS, ANF||Died|
|[ 12 ]||2020||Mexico||M||54||HT, DS, Obesity, Asthma||MV, PICCs, UC, Antibiotic use, Steroid therapy,||IV||Urine||AMB||20-70||ISA, CAS||Survived|
|[ 12 ]||2020||Mexico||M||55||HT, DS, CAD||MV, PICCs, UC, Antibiotic use, Steroid therapy||IV||Blood||AMB||20-70||ANF||Died|
|[ 12 ]||2020||Mexico||M||51||Obesity||MV, PICCs, UC, Antibiotic use, Steroid therapy||IV||Urine||AMB||20-70||ISA, ANF||Died|
|[ 12 ]||2020||Mexico||M||64||AKD||MV, PICCs, UC, Antibiotic use, Steroid therapy||IV||Blood, Urine||AMB, FLC||20-70||CAS, VRC, AMB||Died|
|[ 12 ]||2020||Mexico||M||64||HT, Smoking, Obesity, Hypothyroidism||MV, PICCs, UC, Antibiotic use, Steroid therapy||IV||Blood, PIC line, Urine||AMB||20-70||ANF, ISA||Died|
|[ 12 ]||2020||Mexico||F||54||HT, Obesity||MV, PICCs, UC, Antibiotic use, steroid therapy||IV||Blood||AMB, FLC||20-70||AMB, CAS, VRC||Died|
|[ 12 ]||2020||Mexico||F||60||Obesity||MV, PICCs, UC, Antibiotic use, Steroid therapy,||IV||Urine||AMB||20-70||CAS, ANF, VRC||Died|
|[ 12 ]||2020||Mexico||M||58||HT, Obesity||MV, PICCs, UC, Antibiotic use, Steroid therapy||IV||Urine||AMB, FLC||20-70||ANF||Died|
|[ 12 ]||2020||Mexico||M||36||DS, Obesity||MV, PICCs, UC, Antibiotic use, Steroid therapy||IV||Urine||AMB, FLC||20-70||CAS||Survived|
|[ 12 ]||2020||Mexico||M||66||HT, DS, CAD, VHD||MV, PICCs, UC, Antibiotic use, Steroid therapy,||IV||Urine||AMB, ANF||20-70||VRC, CAS||Survived|
|[ 12 ]||2020||Mexico||M||46||Obesity||MV, PICCs, UC, Antibiotic use, Steroid therapy||IV||Blood||AMB||20-70||VRC, CAS||Survived|
|[ 42 ]||2020||USA||F||49||Seizure disorder||ND||ND||Blood||ND||14||MFG||Survived|
|[ 33 ]||2020||India||F||25||CLD, AKD||Antibiotic use, CVC, UC||ND||Blood||FLC, VOR, 5-FC||35||AMB||Survived|
|[ 33 ]||2020||India||M||52||HT, DS||Antibiotic use, Steroid therapy, CVC, and UC||ND||Blood||FLC||20||MFG, AMB||Died|
|[ 33 ]||2020||India||F||82||HT, DS, Hypothyroidism, CKD||Antibiotic use, Steroid therapy, CVC, UC||ND||Blood||FLC||60||MFG||Died|
|[ 33 ]||2020||India||F||86||CLD, IHD, DS||Antibiotic use, Steroid therapy, CVC, UC||ND||Blood||FLC||21||MFG||Died|
|[ 33 ]||2020||India||M||66||HT, DS, asthma||Antibiotic use, CVC, UC||ND||Blood||FLC, AMB||20||MFG, AMB||Survived|
|[ 33 ]||2020||India||M||71||Hypothyroidism, CKD||Antibiotic use, Steroid therapy, CVC, UC||ND||Blood||FLC, 5-FC||32||MFG||Died|
|[ 33 ]||2020||India||M||67||HT, DS, COPD||Antibiotic use, steroid therapy, CVC, and UC||ND||Blood||FLC, AMB, 5- FC||21||MFG, AMB||Survived|
|[ 33 ]||2020||India||M||72||HT, CLD||Antibiotic use, Steroid therapy, CVC, UC||ND||Blood||FLC, VOR, AMB, 5-FC||27||MFG||Died|
|[ 33 ]||2020||India||M||81||HT, DS, IHD||Antibiotic use, Steroid therapy, CVC, UC||ND||Blood||FLC, VOR, 5- FC||20||MFG||Died|
|[ 33 ]||2020||India||M||69||HT, Asthma||Antibiotic use, Steroid therapy, CVC, UC||ND||Blood||FLC, AMB, 5- FC||21||MFG||Survived|
|[ 34 ]||2021||Italy||M||70||DS, Obesity||ND||ND||BAL (BSI)||AMB, azoles||ND||ND||Died|
|[ 34 ]||2021||Italy||M||62||None||Antibiotic use||ND||Surveillance swab (BSI)||AMB, azoles||48||CAS||Survived|
|[ 34 ]||2021||Italy||M||69||CAD||Antibiotic use||ND||Surveillance swab (BSI)||AMB, azoles||26||AMB, CAS||Died|
|[ 34 ]||2021||Italy||M||50||None||Antibiotic use||ND||Surveillance swab||AMB, azoles||ND||ND||Survived|
|[ 34 ]||2021||Italy||M||62||HT||Antibiotic use||ND||BAL (BSI)||AMB, azoles||24||CAS||Survived|
|[ 34 ]||2021||Italy||M||64||Asthma, HT||Antibiotic use||ND||Blood (BSI)||AMB, azoles||29||CAS||Died|
|[ 41 ]||2021||Italy||ND||ND||ND||ND||I||BAL||AMB, VRC, FLC||ND||ND||Died|
|[ 41 ]||2021||Italy||ND||ND||ND||ND||I||BAL||AMB, VRC, FLC||ND||ND||Survived|
|[ 41 ]||2021||Italy||ND||ND||ND||ND||I||Blood||AMB, VRC, FLC||ND||ND||Died|
|[ 41 ]||2021||Italy||ND||ND||ND||ND||I||BAL||AMB, VRC, FLC||ND||ND||Died|
|[ 41 ]||2021||Italy||ND||ND||ND||ND||I||Urine||AMB, VRC, FLC||ND||ND||Survived|
|[ 36 ]||2021||Brazil||M||59||DVT||MV, HD, Steroid therapy||I||CVC-tip||MDS||49||ANF||Survived|
|[ 36 ]||2021||Brazil||F||74||CKD, DS, HT||DVT , Noninvasive ventilation, HD, Steroid therapy, Antibiotic use, HD||I||Blood||MDS||70||ANF||Died|
|[ 40 ]||2021||USA||M||72||DLP||MV, Use of vasopressor agents, Antecedent Steroid therapy, Antibiotic use||III||Blood||Echino, FLC||14||MFG||Survived|
|[ 40 ]||2021||USA||M||77||DS, HT, DLP||MV, Use of vasopressor agents, Antecedent Steroid therapy, Antibiotic use||III||Urine||FLC||28||ND||Died|
|[ 40 ]||2021||USA||F||71||MM, SCT||MV, Use of vasopressor agents, Antecedent Steroid therapy, Antibiotic use||III||Blood||FLC||24||MFG, AMB||Died|
|[ 40 ]||2021||USA||M||71||DS, HT||MV, Use of vasopressor agents, Antecedent Steroid therapy, Antibiotic use||III||Blood||FLC||24||ND||Died|
|[ 40 ]||2021||USA||F||38||SLE, HT, DS, Obesity||MV, Use of vasopressor agents, Antecedent Steroid therapy, Antibiotic use||III||Wound||FLC||32||ND||Survived|
|[ 40 ]||2021||USA||M||71||DS, HT, DLP||MV, use of vasopressor agents, Antecedent Steroid therapy, Antibiotic use||III||Blood||FLC||30||ND||Died|
|[ 40 ]||2021||USA||F||75||DS, HT, DLP||MV, use of vasopressor agents, Antecedent Steroid therapy, Antibiotic use||III||Blood||FLC||12||MFG||Survived|
|[ 40 ]||2021||USA||F||68||DS, bladder cancer||MV, use of vasopressor agents, Antecedent Steroid therapy, Antibiotic use||III||Urine||FLC||32||ND||Survived|
|[ 40 ]||2021||USA||M||65||HT||MV, use of vasopressor agents, Antecedent Steroid therapy, Antibiotic use||III||BAL||FLC||12||ND||Died|
|[ 40 ]||2021||USA||M||69||HT||MV, use of vasopressor agents, Antecedent Steroid therapy, Antibiotic use||III||Blood||FLC||28||MFG||Died|
|[ 40 ]||2021||USA||M||41||HT, CKD||MV, use of vasopressor agents, Antibiotic use||III||Blood||FLC||20||MFG||Survived|
|[ 40 ]||2021||USA||M||68||ND||MV, use of vasopressor agents, Antibiotic use||III||Wound||FLC||33||MFG||Survived|
|[ 38 ]||2021||Brazil||M||59||DVT||CVC, HD, MV, UC, Antifungal therapy, Antibiotic use||I||CVC‐tip||MDS||42||Yes||Survived|
|[ 38 ]||2021||Brazil||M||79||Biliary lithiasis||CVC, MV, UC, Antifungal therapy, Antibiotic use||I||CVC‐tip, Axillae, Groin, Nostrils and Ear swab||MDS||46||Yes||Survived|
|[ 38 ]||2021||Brazil||M||72||Stroke, dementia||CVC, MV, UC, Antifungal therapy, Antibiotic use||I||Urine||MDS||36||Yes||Died|
|[ 38 ]||2021||Brazil||M||58||HT, DS, obesity||CVC, Antibiotic use||I||Axillae, Groins swabs||MDS||27||No||Survived|
|[ 38 ]||2021||Brazil||M||63||HT, DS, Obesity||CVC, Antibiotic use||I||Axillae, Groin and nostril Swabs||MDS||18||No||Survived|
|[ 38 ]||2021||Brazil||F||75||HT, DS, Hypothyroidism||CVC, HD, MV, UC, Antifungal therapy, Antibiotic use||I||Axillae, Groins swabs||MDS||32||Yes||Survived|
|[ 38 ]||2021||Brazil||M||63||HT, DS, CKD||CVC, HD, MV, UC, Antifungal therapy, Antibiotic use||I||Axillae, groin, nostrils and ear swabs||MDS||22||Yes||Survived|
|[ 38 ]||2021||Brazil||M||77||COPD, Stroke, CKD||UC, Antibiotic use||I||Axillae, groin, Nostrils and Ear swabs||MDS||22||No||Survived|
|[ 38 ]||2021||Brazil||F||74||DS, HT, CKD, Coronary artery disease||CVC, MV, HD||I||Blood||MDS||34||Yes||Died|
|[ 39 ]||2021||Qatar||M||64||None||MV, Antibiotic use, HD||ND||Blood||AMB, FLC||47||ANF||Died|
|[ 32 ]||2021||Lebanon||M||75||ARDS ,Metastatic prostate cancer||Intubated, MV, CVC, UC, Antibiotic use, Steroid therapy, Antifungal therapy||ND||DTA, Urine, Blood||ND||40||Yes||Survived|
|[ 32 ]||2021||Lebanon||F||82||COPD, Respiratory failure||MV, CVC, UC, Antibiotic use, Steroid therapy, Antifungal therapy||ND||DTA||FLC, AMB||26||No||Survived|
|[ 32 ]||2021||Lebanon||M||68||ARDS||Intubated MV, CVC, UC, Antibiotic use, Steroid therapy, Antifungal therapy||ND||DTA||ND||50||No||Survived|
|[ 32 ]||2021||Lebanon||F||68||ARDS||Intubated, MV, CVC,UC, Antibiotic use, Steroid therapy, Antifungal therapy||ND||DTA||FLC, AMB||40||Yes||Survived|
|[ 32 ]||2021||Lebanon||M||71||Cutaneous T cell lymphoma||Intubated, MV, CVC,UC, Antibiotic use, Steroid therapy, Antifungal therapy||ND||DTA||FLC, AMB||15||Yes||Survived|
|[ 32 ]||2021||Lebanon||M||85||ARDS||Intubated, MV, CVC,UC Antibiotic use, Steroid therapy, Antifungal therapy||ND||DTA||ND||10||Yes||Survived|
|[ 32 ]||2021||Lebanon||M||79||ARDS, CLL||Intubated, MV, CVC,UC, Antibiotic use, Steroid therapy, Antifungal therapy||ND||DTA||ND||48||No||Survived|
|[ 37 ]||2021||Turkey||M||71||Stroke, DS, Donation of a single kidney, lobectomy surgery due to lung cancer||Favipiravir and intravenous Dexamethasone therapy, Antibiotic use||ND||Blood||AMB, FLC||ND||CAS||Died|
|[ 44 ]||2022||India||M||36||Hepatomegaly, Aplastic anemia, Malignancy, sHLH, HRF, ARDS, MOF, AKD||Steroid therapy, MV||ND||Blood||FLC||29||FLC, CAS||Died|
|[ 45 ]||2022||Germany||F||65||ARDS||Steroid therapy, MV||I||Urine, BAL||FLC, CAS||90||VRC||Survived|
|[ 45 ]||2022||Germany||M||60||Lung transplant, EAA, AKD||MV||I||Blood, TBS||FLC, CAS||73||AMB, CAS, MFG, POS||Survived|
|[ 43 ]||2022||Italy||M||64||ARDS||MV, Steroid therapy, Antibiotic use||ND||Skin||FLC||100||ANF||Survived|
|[ 43 ]||2022||Italy||M||64||Respiratory disease, Smoker, HTA, DS, ARDS||MV, Steroid therapy, Antibiotic use, Antifungal therapy||ND||Skin||FLC||16||No||Died|
|[ 43 ]||2022||Italy||F||49||Respiratory disease, HTA, DS, Autoimmune disease, ARDS||MV , Steroid therapy, Antibiotic use||ND||Skin||FLC||25||No||Died|
|[ 43 ]||2022||Italy||M||57||Autoimmune disease, ARDS||MV, Steroid therapy, Immunomodulatory Agents, Antibiotic use, Antifungal therapy||ND||Urine||FLC||28||No||Died|
|[ 43 ]||2022||Italy||F||55||HTA, Hematological disease, Malignancy, ARDS||MV, Steroid therapy, Immunomodulatory Agents, Antibiotic use, Antifungal therapy||ND||Respiratory tract, Blood||FLC||100||ANF, AMB||Survived|
|[ 43 ]||2022||Italy||F||58||Respiratory disease, HTA, DS, Autoimmune disease, ARDS||MV, Steroid therapy, Antibiotic use, Antifungal therapy||ND||Skin||FLC||66||No||Survived|
|Abbreviations: MV: mechanical ventilation, PICCs: peripherally inserted central lines, UC: urinary catheters, CLD: chronic liver disease, AKD: acute kidney disease, HT: hypertension, DS: diabetes, IHD: Ischemic heart disease, DLP: dyslipidemia, MM: multiple myeloma, SCT: stem cell transplantation, CVC: central venous catheter, COPD: chronic obstructive pulmonary disease, DVT: Deep-seated venous thrombosis, ARDS: Acute respiratory distress syndrome, HD: HD, SLE: Systemic lupus erythematosus, CAD: Coronary artery Disease, CKD: Chronic kidney disease, BSI: blood stream infection, CLL: Chronic lymphocytic leukemia, ANF: Anidulafungin, CAS: Caspofungin, MFG: Micafungin, ISA: Isavuconazole, VRC: Voriconazole, POS: posaconazole, MAR: Multiazole-resistant, Echino: Echinocandins, MDS: Multidrug-susceptible, AMB: Amphotericin B, FLC: Fluconazole, MDS: Multidrug-susceptible, sHLH: Secondary Hemophagocytic Lymphohistiocytosis, HRF: hypoxemic respiratory failure, MOF: multi-organ failure, EAA: Exogenous allergic alveolitis, TBS: Tracheo-bronchial secretion, HTA: Arterial Hypertension, DTA: Deep Tracheal Aspirates, ND: Not define|
COVID-19-associated C. auris infection was more common in males (51/70, 72.86%) than females (19/70, 27.14%; data were not available for 5 patients). The mean±SD age of patients was 63.8±12.09 years [ 12 , 32 - 34 , 36 - 45 ]. Antibiotic use (63/68, 92.65%; data were not available for 7 patients) was the most common risk factor, followed by steroid therapy (48/68, 70.59%; data were not available for 7 patients), mechanical ventilation (48/68, 70.59%; data were not available for 7 patients), the use of urinary catheters (35/68, 51.47%; data were not available for 7 patients), central venous catheter (25/68, 36.76%; data were not available for 7 patients), peripherally inserted central lines (12/68, 17.65%; data were not available for 7 patients), and vasopressor drugs (12/68, 17.65%; data were not available for 7 patients). Regarding the comorbidities, hypertension (33/69, 47.82%; data were not available for 6 patients), diabetes mellitus (25/69, 36.23%; data were not available for 6 patients), acute respiratory distress syndrome (13/69, 18.84%; data were not available for 6 patients), and obesity (13/69, 18.84%; data were not available for 6 patients) were recorded for the patients in descending order of prevalence.
COVID-19-associated C. auris infections (cases/outbreaks) are not limited to a specific geographical region. As shown in Figure 1, they have been reported from American, European, and Asian countries. Lack of reports from other parts of the world does not necessarily mean a lack of such infections, but a lack of sufficient data, which indicates the need for further studies.
According to genetic traits, C. auris is classified in five clades [ 46 ] with different geographic distribution patterns. According to the results of the included studies, from 42 isolates with available data, 18 (42.86%), 12 (28.57%), and 12 (28.57%) were classified as clade I, III, and IV, respectively [ 12 , 36 , 38 , 40 , 41 , 45 ]. Clade I was found in Italy, Brazil, Germany, and Lebanon, while Clade III and Clade IV were mainly reported from the United States and Mexico, respectively [ 12 , 36 , 38 , 40 , 41 , 45 , 47 ].
Inter-clade difference in susceptibility pattern of C. auris is reported in some studies [ 48 ]. Results of the present review confirm the inter-clade difference. While all isolates of clades III and IV were resistant to at least one antifungal drug, 11 out of 18 isolates of clade I were susceptible to antifungal agents. As the available data might be still scarce to make a firm conclusion, special attention to genetic characterization of C. auris isolates in different studies would be beneficial in this regard and is recommended.
Due to some features, C. auris is more likely to cause a hospital outbreak than other Candida species [ 27 , 49 , 50 ]. Biofilm formation is one of these pathogenesis traits that lead to withstanding desiccation and persistence in environments and health care settings [ 51 ]. Elongated survival on environmental surfaces and healthcare-mediated exogenous transmission between patients are other facilitating factor for this fungus. As a result, outbreaks, which continue for several months and sometimes lead to the closing of intensive care units, continuously have been described [ 33 , 52 ]. During the current pandemic, the overload of ICUs has been a breeding ground for the emergence and expansion of C. auris [ 12 , 17 , 34 , 38 ]. Based on our literature review, 9 COVID-19-associated C. auris outbreaks have been reported [ 12 , 17 , 32 - 34 , 38 , 40 , 47 , 53 ]. It is noteworthy that in some of these countries including Lebanon, Brazil, Mexico, and Peru, no isolates of this pathogen had been noted prior to this period [ 12 , 32 , 35 , 38 ]. Details of the outbreaks are presented in Table 2.
|Publication Year||Continent||Country||City/State||Patients (NO.)||Clade (I,II,III,IV,V)||Resistance Pattern||Outcome||Ref.|
|2020||North America||Mexico||Monterrey, Nuevo Leon||12||IV (South American)||AMB:6 , AMB+FLU: 5, AMB+ANF : 1||Survived: 4 , Died: 8||[ 12 ]|
|2020||Asia||India||New Delhi||10||ND||FLC: 3, FLC+AMB: 1,||FLC+5-FC: 1,FLC+VOR+AMB+5-FC: 1, FLC+ AMB+5-FC: 2, FLC+VOR+5-FC: 2||Died:6, Survived:4||[ 33 ]|
|2021||North America||USA||Florida||35||ND||ND||Died:8||[ 17 ]|
|2021||Asia||Lebanon||Beirut||7||ND||FLU+AMB: 3||Survived (Still in ICU): 7||[ 32 ]|
|2021||Europe||Italy||Genoa||6||ND||AMB+azoles: 6||Died: 3, Survived: 3||[ 34 ]|
|2021||South America||Brazil||São Paulo||9||I (South Asian)||MDR||Died:2 , Survived:7||[ 38 ]|
|2021||North America||USA||Miami||12||III (South African)||Echino: 1, FLC: 12||Died:6, Survived:6||[ 40 ]|
|2021||Europe||Spain||Valencia||56||ND||Echino: 2, FLC: 56||ND||[ 53 ]|
|2022||Asia||Lebanon||Beirut||32||I||AMB, FLC, VOR||Died:19, Survived:13||[ 47 ]|
|Abbreviations: MAR: Multiazole-resistant، Echino: Echinocandins, FLC: Fluconazole: MDS: multidrug-susceptible, ANF: Anidulafungin, VOR: Voriconazole, AMB: Amphotericin B, 5-FC: 5-ﬂucytosine, ND: Not defined|
The impact of COVID-19 on AMR
One of the unforeseen and unavoidable consequences of the COVID-19 pandemic is the appearance of antimicrobial resistance [ 54 ]. It is anticipated that too much and inappropriate use of antibiotics, disinfectants, and biocides during this pandemic may raise devastating effects on antifungal resistance control and antibiotic stewardship programs [ 15 ].
In the current pandemic, hospitalized patients with COVID-19 are more predisposed to superinfections with bacterial and/or fungal pathogens which is likely to impact the mortality rates [ 55 ]. This phenomenon is especially important in the case of emerging resistant species, such as C. auris [ 55 ]. An association between antibiotic use and the emergence of candidemia by Candida species with high minimum inhibitory concentration and/or intrinsic resistance to fluconazole has been reported [ 56 , 57 ]. Along the same line, up to 94% of COVID-19 hospitalized patients receive antimicrobial agents [ 58 , 59 ], which may increase the colonization rate of Candida species, such as C. auris [ 60 ]. In our literature review, results of antifungal susceptibility testing showed that 59 out of 70 (84.29%) isolates with available data were resistant to at least one antifungal drug. Among them, 31 (44.29%) isolates were multidrug resistant, which is 14.29% higher than the CDC report (30%) [ 61 ]. As shown in Table 2, in all reported COVID-19-associated C. auris outbreaks, drug-resistant isolates play a key role, and it makes the management more complicated.
With the increased hospital stay and the higher need for intensive care, COVID-19 patients are at risk for C. auris infections. Regarding the specific features of this fungus, it can circulate within clinical settings and cause outbreaks. Moreover, due to the different conditions in COVID-19 patients which are in favor of the selection of drug-resistant organisms, these patients are at risk for coinfections by single or multi-drug resistant C. auris. Accordingly, attempts for timely diagnosis and targeted treatment of such infections in COVID-19 patients should be made.
Conceptualization: S.K., M.A., and S.M. Literature search: J.J., S.A.H, and I.H. Draft preparation: S.K., S.A.G, and S.M. Critical review: H.T., S.A.G, M.A, and S.M. All authors read and approved the final manuscript.
Conflicts of interest
The authors declare no competing interests.
This research received no specific grant from any funding agency, commercial or not-for-profit sectors.
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