Overview on the Prevalence of Fungal Infections, Immune Response, and Microbiome Role in COVID-19 Patients
Abstract
:1. Introduction
2. Fungal Infections as a Co-Morbidity of COVID-19
2.1. Candidiasis
2.2. Aspergillosis
2.3. Histoplasmosis
2.4. Mucormycosis
2.5. Cryptococcus
2.6. Other Fungal Infections
3. Role of Immune Response against the Most Clinically Relevant Fungal Infections in COVID-19 Patients: Two Sides of a Coin
4. Antifungal Resistance and Therapeutic Approaches in COVID-19 Patients
5. Role of the Microbiome and Probiotics to Fight COVID-19
6. Final Remarks
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
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Fungal Infection in COVID-19 Infection | Observed Immune Response | Co-Morbidity/ Disease Models | Test/Diagnosis Performed | COVID-19 Treatment | Antifungals Used | Steroids? | Outcome after Treatment | References |
---|---|---|---|---|---|---|---|---|
Candidemia Candida duobushaemulonii Candida parapsilosis, Candida lusitaniae | Elevated pro-inflammatory markers (d-dimer, ferritin, CRP, progressive thrombocytosis) and neutrophilia | Acute pulmonary embolism with subarachnoid hemorrhage superimposed bacterial pneumonia | CT scan, Culture, RT-PCR Blood, urine, and DTA | Meropenem, Levofloxacin Trimethoprim/sulfamethoxazole, Amikacin, tigecycline, colistin | Intravenous fluconazole | NR | Dead | [32] |
Candidemia (Candida glabrata) | Leucocytes—normal, C-reactive protein and interleukin 6—altered | Type-2 diabetes ischemic heart disease stadium IV, leg amputation highly suspected bacterial superinfection | Chest X-ray and CT scan, RT-PCR, serology, MALDI-TOF | Darunavir/ritonavir, HCQ, piperacillin/tazobactam, teicoplanin, ertapenem, colistin | Caspofungin | NR | Dead | [39] |
Candidemia Candida auris (n = 10), Candida albicans (n = 3), Candida tropicalis (n = 1), Candida krusei (P. kudriavzevii) (n = 1) | NA | Underlying chronic conditions (e.g., hypertension, n = 7; DM, n = 6; and chronic kidney and liver disease, n = 2) | MALDI-TOF and molecular identification—sequencing | NR | Micafungin | NR | Dead (n = 8) | [4] |
Candidemia Candida auris (n = 3) | NA | DM, hypertension, chronic renal failure, coronary artery disease, obesity | Vitek 2 system, MALDI-TOF, sequencing, multiplex PCR | NR | Anidulafungin | NR | Dead | [36] |
Candidemia Candida auris (n = 12) | NA | DM (n = 6), hypertension (n = 6), multiple myeloma (n = 1), stem cell transplantation (n = 1), dyslipidemia (n = 1), end stage renal disease (n = 1), bladder cancer (n = 1), obesity (n = 1), systematic lupus erythematosus (n = 1) | PCR, MALDI-TOF, Vitek2, whole genome sequencing | Remdesivir (n = 9), HCQ (n = 1), | Amphotericin B Micafungin, | n = 10 | Dead (n = 6) Alive (n = 6) | [40] |
Fungal Infection in COVID-19 Infection | Observed Immune Response | Co-morbidity/ DiseaseModels | Test/Diagnosis Performed | COVID-19 Treatment | Antifungals Used | Steroids? | Outcome after Treatment | References |
---|---|---|---|---|---|---|---|---|
Aspergillosis Aspergillus spp., CAPA | Highly permissive inflammatory response | DM, CVD | CT scan, Culture | HCQ | Azoles, liposomal amphotericin B | NR | Alive | [43] |
Immunocompromised | ARD, HT | CT scan, RT-PCR, Culture, ELISA | NR | Voriconazole | Yes (n = 7) | Some alive and some dead | [44] | |
Aspergillosis Aspergillus fumigatus, CAPA | Immunocompromised | DM, HT | CT scan, Culture | NR | Isavuconazole, voriconazole | No | Alive | [42] |
HT, coronary heart disease, obesity | CT scan, RT-PCR, Culture, | HCQ, meropenem, azithromycin | Voriconazole | Yes | Dead | [26] | ||
Low B-cell and T-cell response | Severe dyspnea, hypertension, DM | CT scan, RT-PCR, Serology | RD, multiple antibiotics | Multiple antifungals | No | Alive | [45] | |
Systemic pro-inflammatory cytokine responses | Asthma, DM, Myeloma | CT scan, RT-PCR, Culture, | NR | Voriconazole, isavuconazole, liposomal amphotericin B, caspofungin, anidulafungin | Yes | Some alive and some dead | [46] | |
High inflammatory response and immunosuppression | ALL, AML | RT-PCR, CT scan, Culture, Serology | NR | Caspofungin, fluconazole, liposomal amphotericin B, caspofungin, itraconazole | No | Some alive and some dead | [47] | |
Aspergillosis Aspergillus spp., IA | Acquired immunodeficiency and immunosuppression | ARD | Antigen, CT scan, Culture, Serology | NR | NR | Yes | Death (quick evolution) | [48] |
Strong deregulation of core components of innate immune and inflammatory responses | RHAEM | NA | NA | NA | NA | NR | [49] |
Fungal Infection in COVID-19 Infection | Observed Immune Response | Co-morbidity/ Disease Models | Test/Diagnosis Performed | COVID-19 Treatment | Antifungals Used | Steroids? | Outcome after Treatment | References |
---|---|---|---|---|---|---|---|---|
Histoplasmosis Histoplasma capsulatum | Acquired immunodeficiency | HIV | CT-scan, RT-PCR | Tenofovir/lamivudine and atazanavir/ritonavir ceftriaxone, azithromycin | Itraconazole | Yes (dexamethasone) | Alive | [27,52] |
HIV | HIV | CT-scan, RT-PCR | Atazanavir/ritonavir, tenofovir/emtricitabine | Itraconazole, amphotericin B deoxycholate | No | Alive | [27] | |
Inflammatory response | NA | CT-scan, RT-PCR | Levofloxacin | Itraconazole | Yes (methylprednisolone) | Alive | [53] | |
NA | NA | CT scan, RT-PCR | NA | Itraconazole | No | Alive | [54] | |
Histoplasmosis Histoplasma capsulatum-like intracellular yeasts | Acquired immunodeficiency | HIV | CT-scan, RT-PCR | HCQ, lopinavir/ritonavir, tenofovir disoproxil fumarate/emtricitabine plus dolutegravir | Amphotericin B deoxycholate, itraconazole | No | Lost to follow-up | [55] |
Co-Morbidity/ DiseaseModels | Test/Diagnosis Performed | COVID-19 Treatment | Antifungals Used | Steroids? | Outcome after Treatment | References |
---|---|---|---|---|---|---|
Obesity HT | CT-scan, RT-PCR | None mentioned | Linezolid, meropenem | NA | Died | [67] |
Asthma HT DM | CT-scan, RT-PCR | Remdesivir | Amphotericin B | NA | Died | [68] |
DM Vascular disease | CT-scan, RT-PCR | Tocilizumab, methylprednisolone, dexamethasone | Amphotericin B | Methylprednisolone, dexamethasone | Died | [69] |
HT | CT-scan, RT-PCR | Hydrocortisone | Amphotericin B | Hydrocortisone | Died | [70] |
NA | CT-scan, RT-PCR | Remdesivir, tocilizumad, dexamethasone | Amphotericin B | Dexamethasone | Died | [71] |
Asthma HT DM | CT-scan, RT-PCR | Remdesivir, dexamethasone | Amphotericin B | Dexamethasone | Died | [72] |
HT | CT-scan, RT-PCR | HCQ, lopinavir–ritonavir | Amphotericin B | NA | Died | [73] |
DM ICM RD | CT-scan, RT-PCR | Meropenem | Amphotericin B | Dexamethasone | Alive | [74] |
DM | CT-scan, RT-PCR | NA | Amphotericin B | NA | Alive | [75] |
HT, DM | CT-scan, RT-PCR | NA | Liposomal amphotericin B, itraconazole | NA | Alive | [76] |
NA | RT-PCR CT-scan | Remdesivir, dexamethasone, metformin, glipizide | Amphotericin B, ceftriaxone | Dexamethasone | Live | [77] |
DM | CT-scan, RT-PCR | Meropenem, oseltamivir tocilizumab, sitagliptin/metformin | Amphotericin B | Methylprednisolone, dexamethasone | Died | [69] |
DM | CT-scan, RT-PCR | Remdesivir, ceftriaxone, azithromycin, dexamethasone | Voriconazole, liposomal amphotericin B | Dexamethasone | Live | [78] |
DM (1 patient) No co-morbidity (1 patient) | CT-scan | Remdesivir, convalescent plasma, vancomycin, piperacillin-tazobactam | Amphotericin B | NA | Live (n = 1) Died n = (1) | [68] |
Obesity DM | CT-scan, RT-PCR | Amoxicillin-clavulanate, imipenem/linezolid | Amphotericin B | NA | Died | [79] |
DM (n = 8) CRF (n = 3) | CT-scan | Broad-spectrum antibiotics | Liposomal amphotericin B | Dexamethasone | Died (n = 7) Alive (n = 4) | [80] |
DM HT (all patients) | RT-PCR | HCQ, glucocorticoids | Systemic antifungals | Glucocorticoids | Died (n = 7) Live (n = 8) | [81] |
T2DM (4) T2DM with HT (1) HT (1) Kidney Disease (1) | CT-scan, RT-PCR | Tocilizumab, prednisolone, piperacillin/tazobac, linezolid | Voriconazole | Prednisolone | Died (n = 3) Alive (n = 4) | [82] |
DM (21-cases) HT (14-cases) Renal failure (1-case) | CT-scan, RT-PCR | HCQ, azithromycin | Caspofungin | Combination of steroids | All Live | [76] |
DM (16) | RT-PCR | Corticosteroids | Liposomal amphotericin B, voriconazole, posaconazole | On Steroid | Alive (n = 10) Died n = (6) | [83] |
HT, UTI | CT-scan, RT-PCR | Either dexamethasone or methylprednisolone (7 patients); interferon (2 patient); remdesivir (1 patient); flavipiravir and HCQ (1 patient) | Amphotericin B, posaconazole | Dexamethasone or Methylprednisolone (n = 7) | Live | [84] |
DM | RT-PCR CT-scan | Remdesivir, levofloxacin, dexamethasone, meropenem, vancomycin, piperacillin/tazobactam | Amphotericin B, posaconazole | Dexamethasone | Live | [85] |
No co-morbidity | CT-scan, RT-PCR | HCQ | Amphotericin B | NA | Died | [86] |
chronic lymphocytic leukemia DM | RT-PCR | NA | Amphotericin B | NA | Died | [87] |
DM HT asthma | RT-PCR | NA | Amphotericin B | No | Died | [88] |
AML | CT-scan, RT-PCR | HCQ lopinavir-ritonavir | Amphotericin B | NA | Died | [73] |
renal disease | CT-scan, RT-PCR | Remdesivir, vancomycin, cefepime | Liposomal amphotericin B, posaconazole | Dexamethasone | Died | [72] |
ICM HF s/p OHT DM HT CKD | RT-PCR | Remdesivir methylprednisolone | Fluconazole | Methylprednisolone, dexamethasone | Died | [89] |
No history of any co-morbidity | CT-scan, RT-PCR | Tocilizumab | Liposomal amphotericin B, posaconazole, isavuconazole | Dexamethasone | Live | [90] |
DM HT | Piperacillin/tazobactam, HCQ, azithromycinlopin, vir/ritonavir, prednisone Dexamethasone | Liposomal amphotericin B, isavuconazole, posaconazole | Prednisone, Dexamethasone | Live | [91] | |
HT | RT-PCR | Remdesivir, dexamethasone | Amphotericin B | Dexamethasone | Died | [92] |
T2DM (all 6 patients) | CT-scan, RT-PCR | Prednisolone, dexamethasone, methylprednisolone | Amphotericin B, posaconazole | Prednisolone, Dexamethasone, methylprednisolone | All Live | [93] |
DM HT | CT-scan, RT-PCR | Remdesivir, interferon-alpha | Systemic antifungals | Systemic corticosteroid | Died | [94] |
T2DM, HT (2) T2DM (3) | CT-scan, RT-PCR | Tocilizumab, convalescent plasma, methylprednisolone | Liposomal amphotericin B, posaconazole | Methylprednisolone | Died (n = 2) Alive (n = 3) | [95] |
T1DM | CT-scan, RT-PCR | Ceftriaxone, azithromycin, dexamethasone, remdesivir, tocilizumab | Amphotericin B | Dexamethasone | Live | [71] |
Obesity hypothyroidism | CT-scan, RT-PCR | HCQ, remdesivir, vancomycin, meropenem | Liposomal amphotericin B, posaconazole | Prednisone | Died | [96] |
HT Asthma | RT-PCR | Meropenem, remdesivir, dexamethasone | Liposomal amphotericin B | Dexamethasone, prednisolone | Died | [97] |
Fungal Infection in COVID-19 Infection | Observed Immune Response | Co-morbidity/ Disease Models | Test/Diagnosis Performed | COVID-19 Treatment | Antifungals Used | Steroids? | Outcome after Treatment | References |
---|---|---|---|---|---|---|---|---|
Cryptococcus neoformans | High inflammatory response and immunosuppression | HAT, HBV | CT-scan, RT-PCR | meropenem, vancomycin | Fluconazole | Yes (tacrolimus, prednisone) | Death | [102] |
Acquired immunodeficiency and immunosuppression | HIV | CT-scan, RT-PCR | Tenofovir-DF/ Emtricitabine-atazanavir/ritonavir | Amphotericin B deoxycholate plus fluconazole | No | Death | [103] | |
High inflammatory response and immunosuppression | Stage IV prostate cancer HT, colon-sigma diverticulosis | CT-scan | No | Fluconazole Amphotericin B plus flucytosine | Dexamethasone | Death | [104] | |
High inflammatory response and immunosuppression | HT, DM | NA but COVID19 positive mentioned | Tocilizumab and corticosteroids | Anidulafungin, Amphotericin, flucytosine | Methylprednisolone | Death | [98] | |
Coccidioidomycosis (Coccidioides immitis, C. posadasii) | Impaired cytokine signaling from CD4+ Th1 and cytotoxic CD8+ T-cells among patients | No associated respiratory symptoms & disease | CT scan, Culture, Serology | NR | Liposomal Amphotericin B | No | Alive | [105] |
Coccidioidomycosis (Coccidioides immitis) | Depressed cellular immunity | Progressive respiratory symptoms, hypoxemia | CT scan, Culture, | Remdesivir | Fluconazole | No | Alive | [106] |
Pneumocystis jirovecii | Cytokine release storm | RA | CT scan, Culture, Serology | HCQ, Tocilizumab | Caspofungin, ganciclovir, cefoperazone | Glucocorticoids | NR | [107] |
Functional immune suppression related to CD4+ lymphocytopenia | HIV, progressive hypoxemia | RT-PCR, Culture, Serology, CT | NR | Trimethoprim- sulfamethoxazole | NR | NR | [108] | |
Immunocompromised | ARD, DM, HT | RT-PCR, Culture, Serology, | HCQ, Lopinavir-ritonavir | Antifungals and antibacterials | Yes | Some alive and some dead | [109] | |
Low CD4 count (35.6%) | HIV | CT, RT-PCR, Multiplex PCR | NR | Co-trimoxazole and oral prednisolone | No | Alive | [110] | |
Anemia, lymphopenia, raised C-reactive protein, immunosuppression | HIV | CT, RT-PCR | NR | Co-trimoxazole, IV pentamidine | No | Death | [111] | |
Severe depletion of CD4+ cells | HIV | RT-PCR, Culture, CT | Emtricitabine, Ritonavir | Trimethoprim-sulfamethoxazole | No | NR | [99] | |
Immunocompetent patient | Recovered from COVID-19 | RT-PCR, Culture, CT | Enoxaparin, ceftaroline | Trimethoprim-sulfamethoxazole, methylprednisolone | Yes | Alive | [100] | |
Immunocompromised patients | HT, hepatic steatosis, massive lung thromboses | RT-PCR, Culture, CT, Histopathology | Remdesivir | Trimethoprim-sulfamethoxazole, prednisone | Yes | Some alive and some dead | [101] | |
Saccharomyces cerevisiae (boulardii) (n = 2) | Immunosuppression | HT (first) Diabetes (Second) | RT-PCR | Oseltamivir HCQ | Anidulafungin, fluconazole | No treated with Ultra-Levure [preparation of Saccharomyces cerevisiae (boulardii)] | Both live | [112] |
Fusarium proliferatum | immunocompetent diabetic patient | HAT substituted hypothyroidism | RT-PCR | No | Amphotericin B caspofungin | No | Live | [113] |
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Roudbary, M.; Kumar, S.; Kumar, A.; Černáková, L.; Nikoomanesh, F.; Rodrigues, C.F. Overview on the Prevalence of Fungal Infections, Immune Response, and Microbiome Role in COVID-19 Patients. J. Fungi 2021, 7, 720. https://doi.org/10.3390/jof7090720
Roudbary M, Kumar S, Kumar A, Černáková L, Nikoomanesh F, Rodrigues CF. Overview on the Prevalence of Fungal Infections, Immune Response, and Microbiome Role in COVID-19 Patients. Journal of Fungi. 2021; 7(9):720. https://doi.org/10.3390/jof7090720
Chicago/Turabian StyleRoudbary, Maryam, Sunil Kumar, Awanish Kumar, Lucia Černáková, Fatemeh Nikoomanesh, and Célia F. Rodrigues. 2021. "Overview on the Prevalence of Fungal Infections, Immune Response, and Microbiome Role in COVID-19 Patients" Journal of Fungi 7, no. 9: 720. https://doi.org/10.3390/jof7090720