Invasive Candidiasis Coinfection in Patients with Severe COVID-19 Disease: Scoping Review
by
, , , , , , and
Omar Esteban Valencia-Ledezma
1, 
María del Rocío Reyes-Montes
2,
Gustavo Acosta-Altamirano
3,
María Guadalupe Frías-De-León
1,
Eduardo García-Salazar
1,
Esperanza Duarte-Escalante
2
,
Jesús Santiago-Abundio
1,
Zuleyma González-Miguel
4,
María de Lourdes García-Hernández
4,
Rebeca Martínez-Quezada
1,
Oscar Uriel Torres-Páez
1,
Evelyn Galindo-Oseguera
1,
Patricia Meza-Meneses
1 and
Nicolás Santiago-González
1,* 
1
Departamento de Investigación, Hospital Regional de Alta Especialidad de Ixtapaluca, Servicios de Salud del Instituto Mexicano de Seguro Social para el Bienestar (IMSS-BIENESTAR), Ixtapaluca 56530, Mexico
2
Departamento de Microbiología y Parasitología, Facultad de Medicina, Universidad Nacional Autónoma de México, Mexico City 04510, Mexico
3
Departamento de Investigación del Hospital General de México “Dr. Eduardo Liceaga”, Mexico City 06720, Mexico
4
Facultad de Enfermería y Obstetricia, Universidad Autónoma del Estado de México (UAEMex), Toluca 50000, Mexico
*
Author to whom correspondence should be addressed.
Pathogens 2025, 14(5), 466; https://doi.org/10.3390/pathogens14050466 (registering DOI)
Submission received: 3 April 2025
/
Revised: 6 May 2025
/
Accepted: 7 May 2025
/
Published: 10 May 2025
(This article belongs to the Special Issue An Update on Fungal Infections)
Abstract
:Coinfection rates of candidiasis in patients affected by COVID-19 had a significantly increase during the sanitary contingency. The objective of this scoping review is to analyze the available scientific evidence around the coinfection of invasive candidiasis in hospitalized patients with severe COVID-19 disease. Online databases such as PubMed, EBSCO, SciFinder, Scopus, and SciELO were used to analyze the different scientific studies published from January 2020 to December 2022, selecting 48 publications that reported comorbidity between invasive candidiasis and COVID-19 as a study variable. Based on the PRISMA-ScR extension for scoping reviews, we identified more than half of the publications (57%) as observational, descriptive, and analytic studies, while 43% were systematic reviews. Overall, up to 169,468 adult patients admitted to the intensive care unit were examined. Coinfection was due mainly to Candida albicans (75%), but some more species were reported such as Meyerozyma parapsilosis (formerly Candida parapsilosis); Meyerozyma guilliermondii (formerly Candida guilliermondii); Nakaseomyces glabratus (formerly Candida glabrata); Candida tropicalis; Candida dubliniensis; Clavispora lusitaniae (formerly Candida lusitaniae); and Pichia kudriavzevii (formerly Candida krusei). We concluded that patients infected by SARS-CoV-2 had a higher incidence of fungal coinfections, thus increasing the mortality rate, disease severity, and length of hospital stay in the intensive care unit.
1. Introduction
In America, until 2 December 2022, more than 182 million positive cases and almost 3 million deaths were reported according to the Pan-American Health Organization [1]. From the beginning, health providers had faced several challenges, including those related to diagnosis and treatment in secondary infections due to opportunistic pathogens in critically ill patients [2,3]. The Center for Disease Control and Prevention (CDC) pointed out that patients hospitalized due to COVID-19 had a higher risk of healthcare-associated coinfections, in which invasive candidiasis stands out.
Several studies had described the incidence of candidiasis and mortality rates in patients with COVID-19 as higher in relation to patients without said disease [3,4,5,6,7]. Risk factors related to invasive candidiasis development also associated with poor prognosis were admission to the ICU, the prolonged use of drugs such as antibiotics, steroids, and immunomodulators, and comorbidities like diabetes, lung diseases, or malignancy [3,4]. A study demonstrated that coinfection incidence due to Candida albicans was predominantly high in critical patients with COVID-19 in contrast to those without COVID-19 [3], thus founding a higher susceptibility in critical patients [8]. Said fungal infection is considered as opportunistic and had become more frequent worldwide [9]. Fungal coinfections in COVID-19 have a negative impact; in most of the cases of people living in developing countries with low incomes, therefore, a prevention approach must be established [10], necessitating further analysis in fungal coinfection in COVID-19 to improve diagnosis and treatment in order to avoid complications.
Nevertheless, data related to coinfection between COVID-19 and invasive candidiasis are still scarce. Invasive candidiasis continues to be a challenge in healthcare leading to this scoping review in published scientific evidence about the incidence in commonly found species in candidiasis and its association with COVID-19 in order to provide data to help diagnose, treat, and prevent complications in these patients. Based on the aforementioned, the objective in this study was to analyze the available scientific evidence around coinfection with invasive candidiasis in hospitalized patients with severe COVID-19 disease from January 2020 to December 2022.
2. Materials and Methods
2.1. Study Design
A scoping review was carried out according to the PRISMA extension for scoping reviews (PRISMA-ScR) [11,12]. The research was carried out in databases such as MEDLINE (PubMed), EBSCO, SciFinder, Scopus, and SciELO. Keywords in DeCS and MeSH included ((((((COVID-19) OR (SARS-CoV-2 Infection)) OR (2019-nCoV Disease)) AND (((Candidiasis) OR (Candida albicans)) OR (Invasive candidiasis))) AND ((Prevalence) OR (incidence))) AND (((Coinfection) OR (Comorbidity)) OR (Association))) AND (Adult). Research took into account papers published from January 2020 until December 2022 and limited to Spanish, Portuguese and English. Studies were analyzed if the title and abstract reported comorbidity between candidiasis and COVID-19 as a study variable.
2.2. Literature Selection Criteria
Research papers mentioning a coinfection of invasive candidiasis and COVID-19 during hospital stay in adult patients (male and female) were included, if available those with mortality rate comparison. About its study design: clinical trials with more than ten patients, systematic reviews with homogeneity, clinical trials meta-analysis, concurrent cohort studies, systematic reviews of level one diagnostic studies, individual clinical trials with narrow confidence interval and individual concurrent cohort studies with follow-ups higher than 80%.
Any paper in relation to pediatric population, animal intervention, any other pathogens not related to this study’s approach was excluded, as well as individual cohort studies, low-quality clinical trials, individual case–control studies, case series, and low-quality case–control studies, along with clinical experts’ opinions that lacked explicit critical evaluation.
2.3. Data Collection Process
The research, selection, and review of studies involved was carried out by eight authors (O.E.V.-L., M.R.R.-M., M.G.F.L., E.G.-S., E.D.-E., O.T.-P., P.M.-M., and N.S.-G.) in order to unify coherence between the reviewers. All of them examined the forty-eight papers chosen to be in this scoping review; they analyzed the variables and merged the data extraction before selecting the results.
2.4. Quality Evaluation
To evaluate the quality of these studies, Evidence Classification according to Burns [13] was used. This systematization organizes evidence into a hierarchy of levels from one to five, with one being the “best evidence” and five “the worst or least adequate”. Therefore, in this therapeutics, prevention, etiology, and damage scenario, the best-rated studies correspond to systematic reviews (SR) in clinical Randomized Controlled (RC) Trials. Quality evaluation was carried out individually by each author, later drawing a consensus to sort out any disagreement.
2.5. Data Analysis
Scientific papers were classified based on population, admission area and healthcare center, and design and year lapse; then, epidemiologic data were compiled, as well as the candidiasis characteristics, comorbidities factor, and complications. The inclusion criteria were evaluated in addition to the relation between COVID-19 and invasive candidiasis. The results were showed descriptively, performing a descriptive analysis when the variable allowed for it.
3. Results
Selection of Sources of Evidence
From the scoping review, around 206 papers mentioned the specific subject to analyze in this study. After deleting duplicates, checking the study’s inclusion and exclusion criteria, and performing a conscientious analysis, a sample of n = 48 studies meeting the aforementioned criteria was obtained (Figure 1).
Table 1 shows the relation of developing candidiasis in patients with COVID-19 where 48 studies were included, of which 43% were literature systematic reviews and meta-analysis, whereas 57% were observational, descriptive, and analytic studies. Said studies included in total 169,468 patients from 17 years old, admitted in the intensive care unit (ICU) in different hospitals around the world. Also, the studies displayed the commonly found Candida species, where C. albicans was reported in 75% of the cases along with two or more other species.
These studies cover hospitalized patients mainly admitted in the intensive care unit (ICU) in several regions such as Spain, the United Kingdom, Italy, Greece, Hungary, Australia, India, Turkey, Iran, Israel, Africa, the United Arab Emirates, China, South Korea, the United States, and Latin American countries. The studies’ designs include systematic reviews, retrospective studies, cohort analysis, case-series, and transversal studies. Sample size varies from small groups (11 in one paper) to bigger records of thousands of people (47,048 patients in a retrospective study carried out in Spain).
There are several risk factors for developing invasive candidiasis coinfection in patients with severe COVID-19 disease, which are described below: (A) related to COVID-19 infection: prolonged mechanical ventilation, tocilizumab, and steroid (dexamethasone) administration, immunosuppression, and antibiotic therapy, as well as comorbidities such as diabetes mellitus, chronic kidney disease, abdominal surgery, and neutropenia. (B) Related to hospital stay: long stay in the ICU, central venous catheter staying, invasive surgery, and gastrointestinal complications. (C) Patient related: advanced age (>65 years old), and specific COVID-19 immunological alterations, including a high level of pro-inflammatory cytokines and low levels of CD4/CD8 lymphocytes T.
The diagnostic methods used in disease identification—COVID-19 and candidiasis-—are shown in Table 2. The diagnostic method for candidiasis includes the common RT-PCR and blood cultures as standard methods to detect Candida spp. In cases of invasive candidiasis, serological tests such as β-D-glucan and mannan antigen are also used. Advance diagnostic methods: MALDI-TOF in rapid species identification, and molecular sequencing techniques (21-plex PCR), specific clinical tests, and histological examination in complex cases. Polymerase chain reaction (PCR) was reported in 40% of all studies, followed by various cultures in 20% and blood culture in 14%.
In the adjacent column, the treatment or therapy during the intervention is described in dosage, duration, and observations related to the therapeutic effect. Immunosuppressors, steroids, antibiotics, azole antifungal drugs, echinocandins, polyenes and antibody therapy are described. In several studies, the association of said therapeutic method and the presence of invasive candidiasis in patients with COVID-19 are mentioned.
The most commonly used drugs include echinocandins (caspofungin, micafungin, and anidulafungin), azole drugs (fluconazole, voriconazole, itraconazole, posaconazole, isavuconazole), polyens (liposomal B-amphotericin), and nystatin, especially in oropharyngeal infections.
4. Discussion
Our objective was to describe, according to the extant scientific evidence (2020–2022), coinfection with invasive candidiasis in hospitalized patients with severe COVID-19 disease. Severely compromised COVID-19 patients have a higher probability of developing candidemia due to exposure to risk factors (underlying pathologies and SARS-CoV-2 infection) in the ICU. COVID-19 disease can be complicated by secondary invasive candidiasis.
4.1. Coinfection Incidence
Opportunistic mycoses are one of the main factors of severe complications in viral infections due to SARS-CoV-2. Based on the data collected, the incidence rate in patients admitted in the ICU in several hospitals and clinics ranges from 10% to 60% when a COVID-19 diagnosis is present. It is also linked to a high mortality rate (more than 50%) when said coinfection is reported and, in some cases, it reaches 100% mortality with C. auris infection, in cases of invasive candidiasis, or when this pathogen is presented in a more aggressive systemic infection [20]. During the COVID-19 pandemic, fungal infection cases increased, especially in those patients with severe viral affection and thus at a higher risk of developing candidemia related to broad-spectrum antibiotics and steroid use; other risk factors include abdominal surgery, mechanical ventilation, parenteral nutrition, or central venous catheter or Foley catheter, on dialysis, with comorbidities (asthma, diabetes, or HIV), or advanced age. Hospital stays in the ICU due to healthcare-related pathogens and the aforementioned procedures are classified as an important risk factor [21,55,56]. The mean age of patients described in the analyzed papers ranged from 50 to 70 years old, thus underlying a more presumptive development of COVID-19 in senior adults in which several factors were not taken into account and representing a higher susceptibility for viral infections [23,29,57,58].
At this moment, when all the data has been compiled, it can be inferred that the pathogens involved in coinfection and increasing the level of lactic dehydrogenase as well as risk factors identified as responsible in the context of COVID-19 and invasive candidiasis coinfection represented a risk in mortality in patients admitted in the ICU. Placing emphasis in infection control through the early detection of both pathogens and treatment, social distancing, maintaining a good hygiene and antifungal prescription improve clinical outcomes when managing this coinfection [15,59,60]. Nowadays, it is well known that SARS-CoV-2 evolution is complicated when secondary infections are presented.
4.2. Candidiasis Diagnosis
Presumptive diagnosis in patients admitted in the ICU when COVID-19 is suspected include the rapid antigen test and real-time polymerase chain reaction (RT-PCR) in order to confirmed the viral infection. When talking about invasive candidiasis diagnosis and its several species, the gold standard is the mycological culture also used in most of the analyzed studies. The clinical observation of body areas with candidiasis manifestations reported the tongue as the most common site of infection followed by the soft palate, oropharynx and oral/lips mucosa. Some studies used exfoliative cytology, microbiological cultures, saliva test, and oral mucosa biopsy as diagnostic tools. Candidiasis was confirmed with the presence of yeast and pseudo-hyphae in blood and miscellaneous cultures of each patient. The literature reports symptomatic presentation of candidiasis after the symptoms of COVID-19 are present. Thus, considering sample contamination, to differentiate infection and colonization, the sensibility of the diagnostic tools used and the time when dealing with coinfection were assessed [28,32,38,40,61].
4.3. Candidiasis’ Causal Agent
As part of diagnosis in invasive candidiasis, the commonly found Candida species involved are reported as follows: C. albicans, N. glabratus, M. parapsilosis, M. guilliermondii, C. tropicalis, C. dubliniensis, C. lusitaniae, and P. kudriavzevii. The most reported species were C. albicans, C. auris, M. parapsilosis, and N. glabratus, with C. albicans being the predominant causal agent in 75% of all the analyzed studies—also the most frequent organism in invasive candidiasis in patients with COVID-19 [28,37,40,62].
In relation to the persistence pathogens in coinfection, there are several hypotheses remaining unchecked, such as M. parapsilosis being acquired in external sources, or C. albicans and glabrata being causal agents that break the normal defense host mechanisms in SARS-CoV-2 infection (epithelial barrier rupture). Other risk factors favor colonization and infection by opportunistic Candida spp. commonly found in the human microbiome. For it, the hypothesis of epithelial intestinal interruption in COVID-19 favors yeast migration to deep tissues and organs [55,63,64].
4.4. Develop and Treatment of Candidiasis
Steroids and immunosuppressor therapeutics increase fungal risk infection, thus increasing mortality rate in coinfected patients. Based on the analysis performed, tocilizumab (TCZ) use could boost the risk to develop systemic candidiasis [14]. TCZ, along with steroid use, was not associated with candidiasis [65]. No association between broad-spectrum antibiotics and Central Line-Associated Bloodstream Infection (CLABSI) due to Candida species was found [16]. In case of a fungal indicator in respiratory infections, body fluids are recommended to start an early antifungal therapy based on the patient’s status [18]. Invasive candidiasis treatment is focus in symptoms, signs and culture’s results [21]. A higher mortality rate in late treatment with fluconazole instead of echinocandins as first-line antifungal drugs was presented [55]. International studies reviewed in this article documented that the use of prophylactic antibiotics without strict criteria contributed to intestinal dysbiosis and allowed for the translocation of Candida from mucosal tissues to the bloodstream, causing candidemia. In Iran and India, in addition to candidiasis, there was a surge in mixed fungal infections, such as mucormycosis, partly also related to the overuse of steroids and prophylactic antibiotics. In Spain and Brazil, hospital registries reported that COVID-19 patients who received multiple lines of prophylactic antibiotics had a higher risk of nosocomial fungal infections. In the United States, the CDC warned in 2021 that the overuse of antibiotics during the pandemic could be fueling epidemics of infections by Candida auris, a multidrug-resistant fungus [14,16,21,55,65].
One review in COVID-19 treatments did not mention the antifungal therapy efficacy, since it was uncertain if the mortality was due to the disease itself or fungal infection and its treatment based on early diagnosis [23]. ICU stay, mechanical ventilation, CVC placing, steroid and immunosuppressor therapy were 1.3 times more common in patients with COVID-19, thus increasing hospital mortality [2]. Patients with invasive candidiasis treated with tocilizumab, dexamethasone, continuous renal replacement therapy and ECMO presented more infections and longer ICU stays with ventilation support [6]. B-amphotericin and caspofungin were effective against species of Candida and were recommended in pulmonary candidiasis associated with COVID-19 [66]. Steroid drug use is a risk factor that increases mortality in invasive candidiasis associated with COVID-19 [7].
4.5. Treatment Duration and Its Effects
All patients affected with Candida spp. remained much longer in the ICU in comparison to those who tested negative [14]. Incidence rate in invasive candidiasis associated with COVID-19 was 2.43 per 1000 days in the ICU [2]. Prolonged use of mechanical ventilation and infections were associated with developing invasive candidiasis [67]. Corticosteroids and IL-6 receptor blockers (tocilizumab) were associated with opportunistic infections in COVID-19; thus, its use must be regulated [19]. Fungal infection treatment in critical patients is a challenge due to the comorbidities’ prevalence, toxicity’s risks, and pharmacological interactions [20]. The infection between the host and pathogens must be studied to prompt strategies that helps fight antifungal resistance, scarce in antifungal drugs [68].
The risk of developing invasive candidiasis is higher in advanced-age patients and those with a severe disease [65]. Coinfection with bacteria, drug-resistant pathogens, and several pathogens is associated with higher mortality rates [15]. Patients with COVID-19 and bacterial or viral infections undergoing immunosuppressor therapy had a higher risk of developing opportunistic infections associated with COVID-19: aspergillosis, candidiasis, mucormycosis, cryptococcosis, pneumonia due to Pneumocystis jirovecci, and histoplasmosis, amongst others [19]. The increase in invasive candidiasis’s incidence was related to the increase in admissions in patients affected by COVID-19 [17]. Healthcare related fungal infections, in particular due to Candida spp., raise the morbidity and mortality rate in critical and severely immunocompromised patients [69]. A high prevalence of candidiasis with COVID-19 disease was identified, about 12% from 889 patients, representing a risk for added infection [24]. In a retrospective study, opportunistic fungal infection was identified to increase mortality rate in patients with COVID-19 [25]. Pulmonary aspergillosis and mucormycosis associated with COVID-19 are the most common fungal infections reported in the literature [4]. Morbidity and mortality rates are linked to invasive candidiasis [5], increasing due to pre-existent conditions, risk factors, and pathophysiological mechanisms [70]. Fungal coinfection between Aspergillus spp. and Candida spp. are frequent in admitted patients with COVID-19 [71].
4.6. Relation Between COVID-19 and Invasive Candidiasis
It is possible that the incidence rate in COVID-19 patients with invasive candidiasis is much higher than reported. All patients positive for Candida spp. remained much longer in the ICU compared to those who tested negative; even mortality was also more closely associated with advanced age, coinfection by one or more viruses, bacteria or fungi, influenced by low neutrophil and lymphocyte count and high levels of lactate dehydrogenase. All patients coinfected by COVID-19 and invasive candidiasis were on mechanical ventilation support and CVC placing, receiving broad-spectrum antibiotics, parenteral nutrition, and steroid therapy, reporting an increased incidence of CLABSI due to Candida spp., with CVC placing and steroids being risk factors that contribute to fungal infection and a longer stay in the ICU. Meanwhile, factors that worsen COVID-19 evolution/severity include physical barrier and microbiota alterations, vascular catheters, mucositis, GI surgery, immunosuppression, lung disease, steroid or azole use, underlying systemic conditions control and prophylactic and broad-spectrum antibiotics regimen, diabetes mellitus, neutropenia, advanced age, patients with organ transplantation, and invasive candidiasis.
Catheter-related invasive candidiasis was the common entryway in COVID-19 patients, thus increasing morbidity and mortality in severely compromised patients, presenting a high incidence of fungal infection in COVID-19 patients admitted in the ICU. As for early presentation and higher mortality due to invasive candidiasis in said patients, invasive candidiasis coinfection with COVID-19 could worsen the prognosis and recovery.
4.7. Study Limitations
This study has several limitations. First, it was a scoping review and did not apply the methodological rigor required for a systematic review, despite using the PRISMA methodology in both cases. This can lead to bias and therefore make a generalization of results impossible. Second, only studies written in Spanish, Portuguese, and English were reviewed. Furthermore, retrospective data published after this study were not considered. Third, we were faced with the lack of methodological models addressing the association between invasive candidiasis and severe COVID-19. This study also has strengths, such as the thorough review and analysis of the literature on invasive candidiasis coinfection in patients with severe COVID-19.
5. Conclusions
We concluded that patients infected with SARS-CoV-2 had a higher incidence of invasive candidiasis coinfection, especially due to C. albicans. The most common complications were a longer hospital stay in the ICU, higher mortality rate, and a more severe disease in coinfected patients. Management in patients diagnosed with COVID-19 is still deficient and clinical outcomes vary in relation to procedures and treatments. Coinfection according to the clinical pictures is attributed to various reported factors; it is also crucial that in case of evidence of coinfection, the clinical picture is not attributed exclusively to SARS-CoV-2 infection. Diagnostic tests are the biggest challenge, from which it is derived that the care and treatment are the most appropriate and effects of pathogens involved are counteracted. The data collected provide medical evidence to generate approach strategies for invasive candidiasis coinfection in patients diagnosed with COVID-19, as well as to design prophylaxis programs for improving the quality of care for patients admitted to intensive care units due to COVID-19.
Author Contributions
Conceptualization, O.E.V.-L., M.d.R.R.-M., G.A.-A. and M.G.F.-D.-L.; methodology, O.E.V.-L., M.d.R.R.-M., G.A.-A. and M.G.F.-D.-L.; software, E.G.-S., E.D.-E., J.S.-A. and Z.G.-M.; validation, R.M.-Q., P.M.-M. and N.S.-G.; formal analysis, R.M.-Q., P.M.-M., N.S.-G., M.d.L.G.-H., O.U.T.-P. and E.G.-O. investigation, E.G.-S., E.D.-E., J.S.-A., Z.G.-M., M.d.L.G.-H., O.U.T.-P. and E.G.-O. resources, R.M.-Q., P.M.-M. and N.S.-G.; data curation, E.G.-S., E.D.-E., J.S.-A., Z.G.-M.; writing—original draft preparation, O.E.V.-L., M.d.R.R.-M., G.A.-A., M.G.F.-D.-L., M.d.L.G.-H., O.U.T.-P. and E.G.-O.; writing—review and editing, E.G.-S., E.D.-E., J.S.-A., Z.G.-M., M.d.L.G.-H., O.U.T.-P. and E.G.-O.; visualization, O.E.V.-L., M.d.R.R.-M., G.A.-A. and M.G.F.-D.-L.; supervision, R.M.-Q., P.M.-M. and N.S.-G.; project administration, O.E.V.-L., M.d.R.R.-M., G.A.-A. and M.G.F.-D.-L.; funding acquisition, R.M.-Q., P.M.-M. and N.S.-G. All authors have read and agreed to the published version of the manuscript.
Funding
This research received no external funding.
Data Availability Statement
The data supporting the findings of this study are available upon reasonable request from the corresponding author.
Acknowledgments
This work was carried out within the framework of the research activities of the Hospital Regional de Alta Especialidad de Ixtapaluca, Servicios de Salud del Instituto Mexicano de Seguro Social para el Bienestar (IMSS-BIENESTAR).
Conflicts of Interest
The authors declare no conflicts of interest.
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Figure 1.
Flux diagram. PRISMA extension for scoping reviews (PRISMA-ScR) [11].
Figure 1.
Flux diagram. PRISMA extension for scoping reviews (PRISMA-ScR) [11].
Table 1.
The relation of candidiasis developing in patients with COVID-19 admitted in the intensive care unit in different hospitals around the world, related factors, prevalence, incidence, mortality, and Candida species found.
Table 1.
The relation of candidiasis developing in patients with COVID-19 admitted in the intensive care unit in different hospitals around the world, related factors, prevalence, incidence, mortality, and Candida species found.
| First Author (Year) | Admission | N Patients/Age | Study Design and Settings | Observation Period | Prevalence | Candida Species Found | Risk Factors in COVID-19/Candida coinfection |
|---|---|---|---|---|---|---|---|
| Segrelles-Calvo G. (2021) [14] | ICU | 215/>18 | Systematic review Observational and prospective study | February–April 2022 | Invasive candidiasis 14.4% | C. albicans M. parapsilosis | All patients were positive to Candida spp. Remaining for longer periods in the ICU in comparison to those who tested negative |
| Jeong S (2022) [15] | ICU | 57 admitted 379 outpatient/advanced age | More recent prevalence in coinfection by virus, bacteria and fungi. Observational and prospective study | August 2020– October 2021 | Fungal rate 10.5% 6/57 | C. albicans M. parapsilosis C. tropicalis | Advanced age Coinfection involving more than one virus, bacteria or fungi Neutrophil and lymphocyte count, as well as lactate dehydrogenase, were associated with higher mortality rate. |
| Porto Ana P.M (2022) [16] | ITU, ICU | 4563/adults | Ecological observational and prospective study | April–June 2020 | CLABSI’s incidence: 1.60 (IQR, 0.44–4.20) | Candida spp. | Higher incidence of Central Line-Associated Bloodstream Infection (CLABSI) due to Candida spp. |
| Nucci M (2021) [17] | ICU, | 41/mean age 62 years | Review study Retrospective | January 2019–February 2020 / March–September 2020 | Ranged from 0.7% to 23.5% | C. albicans | All patients with candidemia associated with COVID-19 were on mechanical ventilation with a central venous catheter, broad-spectrum antibiotics, steroids, and parental nutrition. |
| Peman J (2020) [18] | ICU | 1095/NR | Review study | 2019–2020 | NR | C. albicans M. parapsilosis C. tropicalis N. glabratus C. auris M. guilliermondii | Higher levels of pro-inflammatory (IL-1, IL-2, IL-6, TNF-α) and anti-inflammatory (IL-4, IL-10) cytokines. Less IFN-γ, CD4, and CD8 cell expression, thus raising the risk for severe fungi infections. |
| Abdoli A (2022) [19] | ICU | NR | Review study | NR | NR | C. albicans C. tropicalis M. parapsilosis, N. glabratus M. orthopsilosis | Prolonged ICU stay, central venous catheters, and steroid use as main risk factors in fungal infection. |
| Chiurlo M (2021) [20] | ICU | NR | Review study Systematic review | 2020–2021 | 10% of admitted patients due to COVID-19 infection High mortality rate >50% | C. albicans Candida spp. | Physical barriers’ alterations, vascular catheters, mucositis, GI surgery, immunosuppression, microbiota alterations, severe lung disease, diabetes or advanced age |
| Rajendra Santosh A.B. (2021) [21] | ICU | NR | Review study Systematic review | 2019–2020 | Frequency in infections due to fungi is rising due to the human immunodeficiency virus and immunosuppressive drugs | Candida spp. | Organ-transplanted patients, steroid use, azole drug use, control of systemic underlying pathologies, and prophylactic antibiotic regimen. Diabetes mellitus, broad-spectrum antibiotics, neutropenia, steroids, and voriconazole. |
| Arastehfar A. (2021) [22] | ICU | 1988/NR | Ecological observational and retrospective study | November 2020–January 2021 | C. albicans (57%) N. glabratus (28%) | C. albicans N. glabratus M. parapsilosis | Candidemia as a worsening factor in COVID-19 severity, broad-spectrum antibiotics, central venous catheter, mechanical ventilation, IL-6 inhibitor, and tocilizumab use. |
| Frías-De-León M. G. (2021) [23] | ICU | NR/>40 | Bibliographic research | January 2020–February 2021 | NR | C. albicans M. parapsilosis N. glabratus C. tropicalis C. auris P. kudriavzevii C. lusitaniae C. inconspicua C. dubliniensis M. orthopsilosis | COVID-19 pathophysiology characteristics (high levels of inflammatory cytokines and reduced T-Cells) favor fungal colonization and infection along with mechanical ventilation, central venous catheters, and prolonged hospitalization stay. |
| Katz J. (2021) [24] | Several hospitals and clinics | 889/NR | Using i2b2 database | Year 2019–2021 | Disproportionate compromised in Afro-American population (40% of COVID-19 cases and/invasive candidiasis) | C. albicans | Invasive candidiasis was associated with a higher risk in COVID-19 |
| Coskun A (2021) [25] | ICU | 627/mean of 73.5 | Review study Electronic clinical archives | March 2020–February 2021 | Ranging from 5% to 70% in mortality due to fungal infection in the ICU | C. albicans M. parapsilosis C. tropicalis | High scores in APACHE II, diabetes mellitus, neutropenia, kidney disease, abdominal surgery, broad-spectrum antibiotics, parenteral nutrition, hemodialysis, mechanical ventilation, central venous catheter, and immunosuppression treatments. |
| Machado M (2022) [3] | ICU | 47,048 on 2019 | Retrospective study | January 2019– December 2020 | Candidemia’s incidence: 4.73 patients with COVID in 1000 admissions, 0.85 patients without COVID in 1000 admissions | C. albicans M. parapsilosis C. tropicalis N. glabratus P. kudriavzevii K. marxianus | Central venous catheter-related candidemia was the most common entry way for patients with COVID-19 |
| Shishido AA (2022) [4] | ICU | 65 /NR | Review study | NR | High mortality rates | C. albicans | High incidence and mortality in patients with COVID-19, longer stays in the ICU and CVC longer stay in place, steroids use, sepsis, age higher than 65 years |
| Szabo BG (2021) [5] | ICU | 90 /advanced age (mean of 75.0 ± 13.0 years old) | Case series Retrospective observational study | March–July 2020 | C. albicans 50%, N. glabratus 37.5%, M. parapsilosis 12.5% and M. metapsilosis 12.5% | C. albicans N. glabratus M. parapsilosis M. metapsilosis | Candidemia increases morbidity and mortality in adult patients with severe COVID-19 disease. |
| Seagle EE (2022) [2] | NR | 251/NR | Case analysis | April–August 2020 | Up to 25.5% of all patients had a coinfection of Candida and SARS-CoV-2 | C. albicans, N. glabratus M. parapsilosis C. tropicalis C. dubliniensis C. lusitaniae P. kudriavzevii M. guilliermondii | Patients with COVID-19 had a higher risk of coinfection due to candidemia even when they did not have a commonly associated risk factor for candidemia |
| Koukaki E (2022) [6] | ICU | 178/66 | Retrospective observational study | August 2020– November 2021 | 5 out of 178 patients developed candidemia associated with COVID-19 but only one more patient was affected by candidemia and aspergillosis | M. parapsilosis (one patient) C. auris (one patient) N. glabratus(one patient) Candida spp. (three patients) | Higher incidence rate of fungal infections in patients admitted in the ICU due to COVID-19 disease |
| Erami M (2022) [26] | ICU | 69 a 100/61.1 (range = 21–88) | Descriptive study | NR | C. albicans (55; 79.7%) N. glabratus (12; 17.4%) and two more patients due to (2.9%) C. africana | C. albicans N. glabratus C. africana | Infection due to Candida spp. did not influence the variables of infection and death due to COVID-19. Airway colonization by C. albicans was commonly found, especially in patients with comorbidities such as diabetes, malignancy, and affected by renal alterations. |
| Kayaaslan B (2021) [7,27] | ICU | 2487/72 | Retrospective study | March 2020–March 2021 | Candidemia’s incidence was higher in the COVID-19 group (2.16, IC 95% 1.77–2.60) than those without COVID-19 (1.06, IC 95% 0.89–0.125) | C. albicans M. parapsilosis N. glabratus C. tropicalis and others | Higher incidence and early presentation with increased mortality rate due to candidemia in patients with COVID-19 |
| Salehi M (2020) [27] | ICU | NR | Review study | 2020 | Until May 25 2020, up to 133,521 confirmed cases of COVID-19 and 7359 deaths were reported in Iran * | C. albicans | Inadequate treatment increases the probability to develop a fungal infection, thus increasing the mortality rate. |
| Vitale RG (2022) [28] | ICU | 146/35–88 | Review study | 2021 | Estimated mortality due to invasive candidiasis ranged from 19% to 40% and up to 70% in the ICU | C. albicans C. auris N. glabratus C. tropicalis M. parapsilosis C. dubliniensis M. orthopsilosis P. kudriavzevii | In patients with COVID-19, fungal infections could worsen the prognosis and recovery |
| White, PL (2021) [29] | ICU | 51/mean age of: 57, M/F: 2.2/1 | Evaluation of a prospective cohort study | NR | Incidence of 26.7% (14.1% in aspergillosis and 12.6% in invasive candidiasis) | C. albicans | Invasive fungal disease associated with COVID-19 |
| Salehi M (2020) [30] | Several hospitals and clinics | 53/27 to 90 | Transversal study | March 2020– April 2020 | During the study, up to 53 (5%) out of 1059 iranian patients with COVID-19 confirmed infections had OPC* | C. albicans N. glabratus C. dubliniensis M. parapsilosis M. tropicalis P. kudriavzevii | * Invasive candidiasis (OPC) in patients with COVID-19 |
| Senok, A. (2021) [31] | Dubai’s hospital electronic system | 29.802/49.3 ± 12.5 | Retrospective review | February 31–July 2020 | 1.3% presented coinfection | C. auris M. parapsilosis | Coinfection in patients with COVID-19 |
| Sang, L. (2021) [32] | Several hospitals and clinics | 190/NR | Retrospective review of medical records of adult patients | January 2020 –April 2020 | C. albicans (6.8%) | C. albicans | Secondary infection in patients with COVID-19 |
| Jeong, S. (2022) [15] | Several hospitals and clinics | 436 samples of 57 admitted patients and 379 outpatients/65.7% were >60 years old | Prevalence evaluation in coinfection due to virus, bacteria and fungi in patients with COVID-19 | August 2020–October 2021 | Incidence rate in coinfections due to bacteria or fungi were 52.6% and 10.5%, respectively, in patients admitted due to COVID-19 | C. albicans | Higher coinfection rate in patients with COVID-19 disease |
| Mastrangelo A. (2021) [33] | ICU | 72/NR | Prospective cohort study comparing historical control patients without COVID-19 | February 2020–June 2020 | 35 (48.6%) | C. albicans | A characteristics description of candidemia in patients affected by SARS-CoV-2 |
| Amorim dos Santos J (2021) [34] | Worldwide study | 64,876/NR | Systematic review | January 2021, six months after the initial research (June 2020) | Eight studies reported invasive candidiasis | C. albicans | It reported oral signs and symptoms in patients with COVID-19 disease |
| Roudbary, M. (2021) [35] | Several hospitals and clinics | NR | Literature research | Between 2020 and 2021 | Common fungal infections were invasive candidiasis and aspergillosis | C. albicans | It reported opportunistic fungal diseases in patients with COVID-19 disease |
| Denny S. (2021) [36] | Several hospitals and clinics | 11/> 17 years old | Retrospective review in candidemia | March 2020–May 2020 | C. albicans in 63.6% | C. albicans M. parapsilosis N. glabratus C. dubliniensis | It describes the high incidence of candidemia in patients with COVID-19 disease |
| Norberg, C M. (2021) [37] | Scientific literature analysis, different regions of the world | NR | Bibliographic review | 2021 | 8 out of 9 patients had a coinfection due to Candida spp. (N. glabratus (4), C. auris (3) and C. albicans (1) | C. auris | Despite the high risk of developing fungal coinfection in patients infected by SARS-CoV-2, the data are scarce in relation to incidence and risks of secondary infections |
| Samaranayake, L. P. (2022) [38] | Database (Pubmed, OVID, SCOPUS and Web of Science) | 292/NR | Systematic review | March 2020– October 2021 | Candida infection was the most common coinfection, 64% (n = 96) | C. albicans | Orofacial mycoses in COVID-19 disease |
| Brandi, N. (2022) [39] | ICU | 95/NR | One center observational and retrospective study | October 2020–January 2021 | 27 (42.9%) patients tested positive for bacterial and fungal infections and 3 patients (4.8%) were affected exclusively by fungi | Candida spp. | Fungal coinfections are frequent in patients with COVID-19 admitted in the ICU and are associated with poor outcomes |
| Rafat, Z. (2022) [40] | ICU | 73/NR | Transversal study in which sputum samples and endotracheal aspirate of patients with COVID-19 in the ICU were collected | May to October 2020 | 15 cases (20.5%) confirmed with fungal coinfections | C. albicans | Patients with severe COVID-19 disease in the ICU were prone to develop fungal infections |
| Ayalon, O. (2022) [41] | ICU | 311/NR | Case–control study | 1 September 2020–31 March 2021 | Candidemia 3.5% | C. albicans | Incidence of invasive candidiasis in patients with COVID-19 disease |
| Soltani S. (2021) [42] | NR | 2246 patients | Systematic review and meta-analysis | 1 December 2019–30 December 2020 | Grouped prevalence of fungal coinfection 12.6% | Aspergillus 2.39% Candida 0.39% | NR |
| Kamali Sarvestani (2021) [43] | ICU | 153 patients | Transversal review | March 2020–March 2021 | NR | C. albicans (7/12, 58.3%), C. dubliniensis (2/12, 16.6%), C. tropicalis (1/12, 8.3%), N. glabratus(1/12, 8.3%), P. kudriavzevii (1 /12, 8.3%) | Presence and treatment of candidemia due to C. albicans and related species (C. dubliniensis) in Iranian patients with COVID-19 |
| Kubin CJ. (2021) [44] | Manhattan, New York, EEUU | 516/3028 patients | Retrospective cohort study | 2 March and 31 May 2020 | NR | NR | Fungal infections manly due to healthcare-related Candida spp. |
| Cataldo MA (2020) [45] | ICU | 2 | Retrospective cohort study | March–April 2020 | The incidence of invasive candidiasis in patients admitted in the ICU was higher in those affected by COVID-19 than prior the pandemic | C. albicans M. parapsilosis N. glabratus | Patients with COVID-19 had a higher risk to develop candidemia during stay in the ICU |
| Agrifoglio A (2020) [46] | ICU | 139 | Retrospective analysis | February to June 2020 | The four months candidemia incidence was 10.8%, much higher in comparison to the seven years prior data | C. albicans M. parapsilosis N. glabratus | It was identified an exponential raise in invasive candidiasis cases |
| Hughes S (2020) [47] | Several hospitals | 836 | Observational study | February 20– April 20 2020 | The incidence of bacterial and fungal coinfection was observed in patients admitted with severe acute respiratory distress syndrome | C. albicans | The main pathogen involved in fungal coinfection was C. albicans |
| Antinori S. (2020) [48] | ICU | 99 | Review article | 2020 and January 2022 | NR | N. glabratus C. albicans | Evidence reveals bacterial and fungal coinfection in COVID-19 patients |
| Papadimitriou-Olivgeris M. (2022) [49] | ICU | 3572 | Retrospective study | 2010–August 2021 | Steroid therapy was evaluated in relation to develop candidemia during the COVID-19 pandemic | M. parapsilosis C. auris | A significant increase in candidemia incidence was evaluated during the COVID-19 pandemic in patients with and without COVID-19 |
| Baddley JW. (2021) [50] | ICU | 37 studies | Retrospective study | June 2021 and November 2021 | Fungal coinfection’s incidence varies and it is related to the population heterogeneity, surveillance protocols, and fungal infection definition | Invasive candidiasis and endemic mycoses | Invasive fungal infections are associated with severe lung injury and immunological deficits such as HIV or immunomodulatory drugs |
| Macauley P. (2022) [51] | ICU | 3568 | Overall analysis and comparison | May 2021 and October 2021 | 12 cases in COVID-19 group (5.1% incidence) 51/1.000 admissions | C. albicans accounted for a minority of isolates | Increase in cases in the SARS-CoV-2 pandemic. |
| Basile K. (2022) [52] | ICU | Not specified | Review article | 6 December 2021 and 6 January 2022 | Not specified | Aspergillus fungal infections including invasive candidiasis, cryptococcosis, pneumocystosis, mucormycosis, and endemic mycoses | Increase in fungal infection associated with COVID-19 disease |
| Kayaaslan B. (2021) [7] | ICU | 1229 | Retrospective study | August 2020 to August 2021 | The candidemia incidence was evaluated in critical patients affected by COVID-19 with risk factors | C. albicans | Patients with severe COVID-19 disease had a higher risk of developing candidemia due to exposure to classical risk factors and specific risks in COVID-19 in the ICU |
| Elbaz M- (2022) [53] | ICU | 1000 | Multicenter Cohort Study | February 2020 and May 2021. | Variation in incidence of lung disease due to mold, ranging between 0 and 51.2 per 1000 critical hospitalizations. | Lung disease due to mold associated with COVID-19 and invasive candidiasis | Very variable data on mold conditions have been reported. |
Source: Scoping review database about the relation between COVID-19 and invasive candidiasis. N= 48 studies. NR: not recorded; ICU: intensive care unit; CLASBI: Central Line-Associated Blood Stream Infections; OFC: Orofacial Candidiasis; * OPC: Oropharyngeal Candidiasis; APACHE II: Acute Physiology and Chronic Health Disease Classification System II; IL: interleukin; INF: interferon gamma.
Table 2.
Diagnostic-type descriptions of COVID-19, invasive candidiasis coinfection, and pharmacological therapeutic effect.
Table 2.
Diagnostic-type descriptions of COVID-19, invasive candidiasis coinfection, and pharmacological therapeutic effect.
| First Author (Year) | Country | Diagnosis Type COVID-19 | Diagnosis Type Invasive Candidiasis | Treatment |
|---|---|---|---|---|
| Segrelles-Calvo G. (2021) [14] | Spain | PCR and IgG | Blood culture | Immunosuppressant/anti-inflammatory (tocilizumab (TCZ)) immunosuppressants/systemic corticosteroids (tocilizumab and systemic steroids (SS)) immunomodulator/antiviral (interferon 1β (IFN-1 β)) antiviral (lopinavir–ritonavir) |
| Jeon S (2022) [15] | United Kingdom | NR | RT-PCR multiplex Matrix-assisted laser desorption ionization mass spectrometry (Vitek-MS) (MALDI) | Immunosuppressors including steroids and TCZ |
| Porto Ana PM (2022) [16] | Brazil | NR | NR | Antibacterial (piperacillin–tazobactam (PIP-TZ) meropenem and vancomycin) |
| Nucci M (2021) [17] | Brazil | NR | NR | Antifungal (anidulafungin and fluconazole) |
| Peman J (2020) [18] | USA Brazil, India, Russia, Peru, Chile, Mexico y South Africa | NR | NR | Antifungal (anidulafungin and isavuconazole) |
| Abdoli A (2022) [19] | NR | NR | Serological test with β-D-glucan (BDG) and mannan antigen | Echinocandins Azoles (voriconazole/fluconazole/ posaconazole/isavuconazole) Polyenes (liposomal amphotericin b) |
| Chiurlo M (2021) [20] | NR | RT-PCR-antigen test | Pathogen isolation serological test with β-D-glucan (BDG) and mannan antigen | Immunosuppressor drugs, TCZ use, steroids, and anti-IL-6 receptor agents |
| Rajendra Santosh AB. (2021) [21] | India | NR | Exfoliative cytology Pathogen culture Saliva test and oral mucosa biopsy | Polyenes (nystatin and b-amphotericin) Azoles (fluconazole, itraconazole and pozaconazole) Antimetabolites (flucytosine) |
| Rajendra Santosh AB. (2021) [54] | India | NR | Special care must be given to patients with a recent diagnosis of COVID-19 to detect and prevent mucormycosis | NR |
| Arastehfar A. (2021) [55] | Iran | RT-PCR | Positive blood culture, 21-plex PCR and sequencing | Antifungals (fluconazole or caspofungin) |
| Frías-De-León M. G. (2021) [23] | Several areas | RT-Q PCR | Molecular and microbiological | Azole antifungal drugs (fluconazole, voriconazole, isavuconazole) echinocandins (caspofungin, anidulafungin, micafungin) Polyenes (b-amphotericin, nystatin) |
| Katz J. (2021) [24] | Africa | NR | NR | NR |
| Coskun A (2021) [25] | Turkey | COVID-19 through electronic medical records and blood cultures | Blood culture | Carbapenem and glycopeptides 27 remaining patients with combination of carbapenem and oxazolidinone or glycopeptide family drug |
| Machado M (2022) [3] | Spain | PCR | Blood culture | Antifungal (echinocandins and fluconazole) |
| Shishido AA (2022) [4] | NR | NR | NR | Steroids and immunosuppressor therapy |
| Szabo BG (2021) [5] | Hungary | PCR | Blood culture | Antifungals (caspofungin, fluconazole, voriconazole, itraconazole, isavuconazole, B- amphotericin) |
| Seagle EE (2022) [6] | USA | PCR | Blood culture | NR |
| Koukaki E (2022) [6] | Greek | PCR | Blood culture | Half of all patients were treated with TCZ and a high dose of dexamethasone, two more received additional monoclonal antibody therapy |
| Erami M (2022) [26] | Iran | Diagnosed based on symptoms, radiological signs, PCR | Microbiological tests | Steroid dosage > 2 mg/kg dexamethasone Antifungals (b-amphotericin, voriconazole, itraconazole, fluconazole, caspofungin) |
| Kayaaslan B (2021) [7] | Turkey | PCR or common finding of COVID-19 in CT-SCAN with a positive antigen test | Blood culture | Antifungals (fluconazole, voriconazole, caspofungin and micafungin) |
| Salehi M (2020) [27] | Iran | Physical examination and PCR | Blood culture, MALDI-TOF (blood culture) and RT-PCR | Broad-spectrum antibiotics, immunosuppressors or steroids, invasive or non-invasive mechanical support Antifungals (fluconazole and nystatin) |
| Vitale RG (2022) [28] | India, Brazil, China, Italy, Iran, UK, USA, Mexico, Colombia | PCR | Blood culture | Antifungal and antibiotic treatment Steroids Antifungals (B-amphotericin, anidulafungin, liposomal, isavuconazole, micafungin, voriconazole) |
| White, P. L, 2021 [29] | NR | PCR | PCR for Pneumocystis NBL-BAL. Serological BDG proposed if positive more test should be run for fungi (PCR- GM-EIA) | Antifungal therapy (AFT) in this cohort study could be beneficial for survival if started early, but it needs prospective validation. Prophylactic AFT could be beneficial in this group |
| Salehi M. (2020) [27] | Iran | PCR and sequencing technique of internal transcribed spacing region (ITS1–5.8S-ITS2) | Presence of gemmating yeast and pseudo-hyphae in a 10% KOH preparation and culture | Most of the isolated Candida species were sensible for three antifungal drug families: azole (fluconazole, voriconazole and itraconazole), polyenes (B-amphotericin), and echinocandins (caspofungin, anidulafungin and micafungin). |
| Senok, A. (2021) [31] | Arab Emirates United | RT-PCR test for SARS-CoV-2 | Coinfection confirmed by laboratorial test and culture | Mean lapse to empiric antibiotic star was 1.2 ± 3.6 days after admission, with ceftriaxone, azithromycin, and piperacillin–tazobactam being the most common used drugs |
| Sang, L., (2021) [32] | China | NR | Bacterial and fungal frequency was measured in cultures of airway and blood samples | Antifungal and antibiotic treatment was administrated in 71 (43.8%) patients |
| Jeong, S., (2022) [15] | South Korea | PCR-RT | Culture with antibiogram to detect pathogens were carried out and underwent a Multiplex test | Poor immune response due to SARS-CoV-2 infection and immunosuppressor treatment (steroids and tocilizumab) and COVID-19 therapeutics may boost fungal infection |
| Mastrangelo, A. (2021) [33] | Italy | NR | NR | Antifungal |
| Amorim dos Santos J, (2021) [34] | Worldwide | PCR | Invasive candidiasis infection was confirmed in presence of germ tube; positive presence of pseudo-hyphae in a 10% KOH preparation and culture | NR |
| Roudbary, M., (2021) [35] | Several regions worldwide | PCR | MALDI-TOF (blood culture) Molecular sequencing technique | Antifungals (intravenous fluconazole, caspofungin, micafungin, anidulafungin, and b-amphotericin) |
| Denny, S. (2021) [36] | United Kingdom | PCR | Blood culture identified throughout spectroscopy | All isolated pathogens were sensitive to fluconazole, with the exception of one case, N. glabratus, that showed moderate sensibilization |
| Norberg, C. M. B. M. (2021) [37] | Brazil | PCR | Blood culture IgG test and germ tube test | An association exists between tocilizumab treatment and the development of candidemia in patients with COVID-19 |
| Vitale, R. G. (2022) [28] | Brazil | PCR | Culture | In Brazil, all species of C. auris were reported as sensible to azole, amphotericin, and echinocandins |
| Samaranayake, L. P. (2022) [38] | 14 countries | PCR | Clinical observation of sites with systemic candidiasis manifestation | Infections due to Candida spp. were treated with antifungals (oral nystatin, miconazole, or systemic fluconazole) |
| Brandi, N. (2022) [39] | Italy | PCR | Radiological images are a key component to detect coinfections | Non-specific therapy recorded |
| Rafat, Z. (2022) [40] | Iran | PCR | Direct microscopic observation 10% KOH preparation and culture | NR |
| Ayalon, O. (2022) [41] | Israel | PCR | Spectometry MALDI-TOF (blood culture) | NR |
| Salehi M (2020) [27] | Iran | PCR | Sequencing technique of internal transcribed spacing region (ITS1-5.8S-ITS2) and microbiological methods | Antifungals (fluconazole, itraconazole, voriconazole, B-amphotericin, caspofungin, micafungin, and anidulafungin) |
| Soltani S. (2021) [42] | Iran | NR | NR | Antifungals (amphotericin B, micafungin, and fluconazole) |
| Kamali sarvestani h. (2021) [43] | Iran | PCR | Blood cultures, mycological test and sequencing technique of internal transcribed spacing region | Antifungals (caspofungin alone, B-amphotericin, voriconazole, fluconazole, itraconazole) |
| Kubin CJ. (2021) [44] | USA | PCR | Blood cultures | Hydroxychloroquine, azithromycin, low-dosage methyl-prednisone, and fluconazole. Remdesivir (antiviral), vancomycin, and carbapenem (antibacterials). |
| Antinori S. (2020) [48] | Italy | NR | NR | Antifungals (voriconazole, voriconazole switched to isavuconazole, isavuconazole, caspofungin followed by voriconazole, liposomal amphotericin B) |
| Papadimitriou-olivgeris M. (2022) [49] | NR | NR | NR | Antifungals (fluconazole, voriconazole, echinocandins, anidulafungin, caspofungin, micafungin, liposomal-amphotericin b) |
| Basile K. (2022) [52] | Australia | PCR | Blood cultures | Antiviral Treatment |
| Kayaaslan B. (2022) [7] | Turkey | NR | NR | NR |
| Elbaz M. (2022) [53] | Israel | PCR | Blood cultures | NR |
Source: Scoping review database in coinfection between invasive candidiasis and COVID-19 in patients with clinical complications. NR: not recorded; TCZ: tocilizumab; SS: systemic steroids; INF 1B: interferon 1β; LPV-RTV: lopinavir–ritonavir; PIP-TZ: piperacillin–tazobactam; PCR-RT: polymerase chain reaction in real time; MALDI: matrix-assisted laser desorption ionization mass spectrometry; BDG: serological test with β-D-glucan; CT-SCAN: Computerized Tomography SCAN; CXR: Chest X-Ray; GM-EIA: Galactomannan Enzyme Immunoassay; NBL: Non-Bronchoscopic Lavage; BAL: Broncho-Alveolar Lavage; AFT: antifungal therapy; OPC: Oropharyngeal Candidiasis.
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Valencia-Ledezma, O.E.; Reyes-Montes, M.d.R.; Acosta-Altamirano, G.; Frías-De-León, M.G.; García-Salazar, E.; Duarte-Escalante, E.; Santiago-Abundio, J.; González-Miguel, Z.; García-Hernández, M.d.L.; Martínez-Quezada, R.; et al. Invasive Candidiasis Coinfection in Patients with Severe COVID-19 Disease: Scoping Review. Pathogens 2025, 14, 466. https://doi.org/10.3390/pathogens14050466
AMA Style
Valencia-Ledezma OE, Reyes-Montes MdR, Acosta-Altamirano G, Frías-De-León MG, García-Salazar E, Duarte-Escalante E, Santiago-Abundio J, González-Miguel Z, García-Hernández MdL, Martínez-Quezada R, et al. Invasive Candidiasis Coinfection in Patients with Severe COVID-19 Disease: Scoping Review. Pathogens. 2025; 14(5):466. https://doi.org/10.3390/pathogens14050466
Chicago/Turabian StyleValencia-Ledezma, Omar Esteban, María del Rocío Reyes-Montes, Gustavo Acosta-Altamirano, María Guadalupe Frías-De-León, Eduardo García-Salazar, Esperanza Duarte-Escalante, Jesús Santiago-Abundio, Zuleyma González-Miguel, María de Lourdes García-Hernández, Rebeca Martínez-Quezada, and et al. 2025. "Invasive Candidiasis Coinfection in Patients with Severe COVID-19 Disease: Scoping Review" Pathogens 14, no. 5: 466. https://doi.org/10.3390/pathogens14050466
APA StyleValencia-Ledezma, O. E., Reyes-Montes, M. d. R., Acosta-Altamirano, G., Frías-De-León, M. G., García-Salazar, E., Duarte-Escalante, E., Santiago-Abundio, J., González-Miguel, Z., García-Hernández, M. d. L., Martínez-Quezada, R., Torres-Páez, O. U., Galindo-Oseguera, E., Meza-Meneses, P., & Santiago-González, N. (2025). Invasive Candidiasis Coinfection in Patients with Severe COVID-19 Disease: Scoping Review. Pathogens, 14(5), 466. https://doi.org/10.3390/pathogens14050466
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