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An Update on COVID‐19 Associated Mucormycosis Characteristics, Risk Factors, and Outcomes: a Systematic Review and Meta-Analysis

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Abstract

Purpose of Review

This meta-analysis aimed to identify the CAM manifestations, clinical presentations, relevant risk factors, mortality risk factors, treatments, outcomes, and survival.

Recent Findings

COVID-19-associated mucormycosis (CAM) increased dramatically, with mucormycosis development estimated to be 50 times higher than before the COVID-19 pandemic. CAM is a high-mortality disease with significant morbidities in survivors. A significant association between uncontrolled diabetes and CAM has been indicated. In addition, high-dose corticosteroid therapy and ICU admission were present in many rhino-orbito-cerebral mucormycosis (ROCM) patients and non-ROCM, respectively. In the present study, we systematically searched PubMed, Scopus, WoS, and PMC, preprint databases, and the reference lists of the included relevant studies until Oct 2021. Studies that report mucormycosis cases (proven/probable) with individual patient details with confirmed COVID-19 infection were included according to the PRISMA statement. Pooling data of 210 CAM patients (proven, 87.6%; probable, 12.4%) was retrieved from 60 case reports/series studies from 17 countries.

Summary

Primary or corticosteroid-induced diabetes was the leading independent risk factor for rhino-maxillo-orbito-cerebral mucormycosis (RMOCM) development (OR:18.29). In contrast, ICU admission was the main independent risk factor for non-RMOCM development (OR:11.64). In the absence of the mentioned risk factors, the risk of CAM is low (3.33%). CAM mortality was high (43.5%), with significantly higher fatality in non-RMOCM (77.3%). Severe/critically ill COVID-19 (OR: 3.66), ICU admission (OR: 6.78), and mechanical ventilation (OR: 6.27) were associated with a higher risk of CAM mortality. Cerebral and orbital involvement increased mortality (OR: 3.253 and OR: 3.205) in RMOCM patients; conversely, the surgical intervention improved outcomes (OR: 18.922). Control of hyperglycemia and COVID-19 infection and evidence-based corticosteroid therapy is essential to prevent CAM development. Identifying and controlling the preexisting/predisposing and mortality risk factors of CAM combined with the implementation of aggressive evidence-based management with a multidisciplinary approach can reduce CAM-related morbidity and mortality. An update to the traditional mucormycosis classification was also introduced to refer to maxillary involvement.

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Data Availability

Data used in this study is available on reasonable request from the corresponding author.

Abbreviations

CAM:

COVID-19-associated mucormycosis

ROCM:

Rhino-orbito-cerebral mucormycosis

RMOCM:

Rhino-maxillo-orbito-cerebral mucormycosis

MCR:

Mucormycosis

DM:

Diabetes mellitus

OR:

Odds ratio

Amp-B:

Amphotericin-B

PRISMA:

Preferred reporting items for systematic review and meta-analyses

PROSPERO:

International Prospective Register of Systematic Reviews

IQR:

Interquartile range

References 

Papers of particular interest, published recently, have been highlighted as: • Of importance •• Of major importance

  1. White PL, Dhillon R, Cordey A, Hughes H, Faggian F, Soni S, et al. A national strategy to diagnose coronavirus disease 2019-associated invasive fungal disease in the intensive care unit. Clin Infect Dis. 2021;73(7):e1634–44.

    Article  CAS  PubMed  Google Scholar 

  2. Hussain S, Riad A, Singh A, Klugarova J, Antony B, Banna H, et al. Global prevalence of COVID-19-associated mucormycosis (CAM): living systematic review and meta-analysis. J Fungi (Basel). 2021;7(11):985.

    Article  CAS  PubMed  Google Scholar 

  3. Sen M, Honavar SG, Bansal R, Sengupta S, Rao R, Kim U, et al. Epidemiology, clinical profile, management, and outcome of COVID-19-associated rhino-orbital-cerebral mucormycosis in 2826 patients in India-Collaborative OPAI-IJO Study on Mucormycosis in COVID-19 (COSMIC), Report 1. Indian J Ophthalmol. 2021;69(7):1670.

    Article  PubMed  PubMed Central  Google Scholar 

  4. John TM, Jacob CN, Kontoyiannis DP. When uncontrolled diabetes mellitus and severe COVID-19 converge: the perfect storm for mucormycosis. Journal of fungi. 2021;7(4):298. This study showed the close association between uncontrolled diabetes and rhino-orbito-cerebral mucormycosis development in COVID-19 infection.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Roden MM, Zaoutis TE, Buchanan WL, Knudsen TA, Sarkisova TA, Schaufele RL, et al. Epidemiology and outcome of zygomycosis: a review of 929 reported cases. Clin Infect Dis. 2005;41(5):634–53.

    Article  PubMed  Google Scholar 

  6. Cornely OA, Alastruey-Izquierdo A, Arenz D, Chen SCA, Dannaoui E, Hochhegger B, et al. Global guideline for the diagnosis and management of mucormycosis: an initiative of the European Confederation of Medical Mycology in cooperation with the Mycoses Study Group Education and Research Consortium. Lancet Infect Dis. 2019;19(12):e405–21.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Jeong W, Keighley C, Wolfe R, Lee WL, Slavin MA, Kong DCM, et al. The epidemiology and clinical manifestations of mucormycosis: a systematic review and meta-analysis of case reports. Clin Microbiol Infect. 2019;25(1):26–34.

    Article  CAS  PubMed  Google Scholar 

  8. Prakash H, Skiada A, Paul RA, Chakrabarti A, Rudramurthy SM. Connecting the dots: interplay of pathogenic mechanisms between COVID-19 disease and mucormycosis. Journal of Fungi. 2021;7(8):616.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Wu Z, McGoogan JM. Characteristics of and important lessons from the coronavirus disease 2019 (COVID-19) outbreak in China: summary of a report of 72 314 cases from the Chinese Center for Disease Control and Prevention. Jama. 2020;323(13):1239–42.

    Article  CAS  PubMed  Google Scholar 

  10. Wu CT, Lidsky PV, Xiao Y, Lee IT, Cheng R, Nakayama T, et al. SARS-CoV-2 infects human pancreatic beta cells and elicits beta cell impairment. Cell Metab. 2021;33(8):1565–76 (e5).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Hwang JL, Weiss RE. Steroid-induced diabetes: a clinical and molecular approach to understanding and treatment. Diabetes Metab Res Rev. 2014;30(2):96–102.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Yang W, Cao Q, Qin L, Wang X, Cheng Z, Pan A, et al. Clinical characteristics and imaging manifestations of the 2019 novel coronavirus disease (COVID-19): a multi-center study in Wenzhou city, Zhejiang. China J Infect. 2020;80(4):388–93.

    Article  CAS  PubMed  Google Scholar 

  13. Ahmadikia K, Hashemi SJ, Khodavaisy S, Getso MI, Alijani N, Badali H, et al. The double-edged sword of systemic corticosteroid therapy in viral pneumonia: a case report and comparative review of influenza-associated mucormycosis versus COVID-19 associated mucormycosis. Mycoses. 2021;64(8):798–808.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Patel A, Agarwal R, Rudramurthy SM, Shevkani M, Xess I, Sharma R, et al. Multicenter epidemiologic study of coronavirus disease-associated mucormycosis. India Emerg Infect Dis. 2021;27(9):2349–59.

    Article  CAS  PubMed  Google Scholar 

  15. Moher D, Liberati A, Tetzlaff J, Altman DG, Group* P. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. Annals Intern Med. 2009;151(4):264–9.

    Article  Google Scholar 

  16. Donnelly JP, Chen SC, Kauffman CA, Steinbach WJ, Baddley JW, Verweij PE, et al. Revision and update of the consensus definitions of invasive fungal disease from the European Organization for Research and Treatment of Cancer and the Mycoses Study Group Education and Research Consortium. Clin Infect Dis. 2020;71(6):1367–76.

    Article  PubMed  Google Scholar 

  17. Koehler P, Bassetti M, Chakrabarti A, Chen SCA, Colombo AL, Hoenigl M, et al. Defining and managing COVID-19-associated pulmonary aspergillosis: the 2020 ECMM/ISHAM consensus criteria for research and clinical guidance. Lancet Infect Dis. 2021;21(6):e149–62.

    Article  CAS  PubMed  Google Scholar 

  18. health Nio. COVID-19 treatment guidelines 2021 [Available from: https://www.covid19treatmentguidelines.nih.gov/management/clinical-management/hospitalized-adults--therapeutic-management/.

  19. Ma L-L, Wang Y-Y, Yang Z-H, Huang D, Weng H, Zeng X-T. Methodological quality (risk of bias) assessment tools for primary and secondary medical studies: what are they and which is better? Mil Med Res. 2020;7(1):1–11.

    Google Scholar 

  20. Bayram N, Ozsaygili C, Sav H, Tekin Y, Gundogan M, Pangal E, et al. Susceptibility of severe COVID-19 patients to rhino-orbital mucormycosis fungal infection in different clinical manifestations. Jpn J Ophthalmol. 2021;65(4):515–25.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Fouad YA, Abdelaziz TT, Askoura A, Saleh MI, Mahmoud MS, Ashour DM, et al. Spike in rhino-orbital-cerebral mucormycosis cases presenting to a tertiary care center during the COVID-19 pandemic. Front Med (Lausanne). 2021;8:645270.

    Article  PubMed  PubMed Central  Google Scholar 

  22. Ashour MM, Abdelaziz TT, Ashour DM, Askoura A, Saleh MI, Mahmoud MS. Imaging spectrum of acute invasive fungal rhino-orbital-cerebral sinusitis in COVID-19 patients: a case series and a review of literature. J Neuroradiol. 2021;48(5):319–24.

    Article  PubMed  PubMed Central  Google Scholar 

  23. Pakdel F, Ahmadikia K, Salehi M, Tabari A, Jafari R, Mehrparvar G, et al. Mucormycosis in patients with COVID-19: a cross-sectional descriptive multicentre study from Iran. Mycoses. 2021;64(10):1238–52.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Arjun R, Felix V, Niyas VKM, Kumar MAS, Krishnan RB, Mohan V, et al. COVID-19-associated rhino-orbital mucormycosis: a single-centre experience of 10 cases. QJM: An Int J Med. 2021;114(11):831–4.

    Article  CAS  Google Scholar 

  25. Mishra N, Mutya VSS, Thomas A, Rai G, Reddy B, Mohanan AA, et al. A case series of invasive mucormycosis in patients with COVID-19 infection. Int J Otorhinolaryngol Head Neck Surg. 2021;7(5):867–70.

    Article  Google Scholar 

  26. Moorthy A, Gaikwad R, Krishna S, Hegde R, Tripathi KK, Kale PG, et al. SARS-CoV-2, uncontrolled diabetes and corticosteroids-an unholy trinity in invasive fungal infections of the maxillofacial region? A retrospective, multi-centric analysis. J Maxillofac Oral Surg. 2021;20(3):418–25.

    Article  PubMed  PubMed Central  Google Scholar 

  27. Nehara HR, Puri I, Singhal V, Ih S, Bishnoi BR, Sirohi P. Rhinocerebral mucormycosis in COVID-19 patient with diabetes a deadly trio: case series from the north-western part of India. Indian J Med Microbiol. 2021;39(3):380–3.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Sarkar S, Gokhale T, Choudhury SS, Deb AK. COVID-19 and orbital mucormycosis. Indian J Ophthalmol. 2021;69(4):1002.

    Article  PubMed  PubMed Central  Google Scholar 

  29. Sen M, Lahane S, Lahane TP, Parekh R, Honavar SG. Mucor in a viral land: a tale of two pathogens. Indian J Ophthalmol. 2021;69(2):244–52.

    Article  PubMed  PubMed Central  Google Scholar 

  30. Saidha PK, Kapoor S, Das P, Gupta A, Kakkar V, Kumar A, et al. Mucormycosis of paranasal sinuses of odontogenic origin post COVID19 infection: a case series. Indian J Otolaryngol Head Neck Surg. 2022;74(Suppl 2):3437–41.

  31. Singh Y, Ganesh V, Kumar S, Patel N, Aggarwala R, Soni KD, et al. Coronavirus disease-associated mucormycosis from a tertiary care hospital in India: a case series. Cureus. 2021;13(7):e16152.

    PubMed  PubMed Central  Google Scholar 

  32. Hooli SA, Gadre VN, Bage S, Gilvarkar MD. The aftermath of COVID-19 pandemic: rhino-orbital mucormycosis. Indian J Anaesth. 2021;65(7):548–53.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Shah D, Talwar D, Kumar S, Acharya S, Dubey A. Mucormycosis as a complication of LONG COVID: a case series. J Med Sci. 2021;25(112):1331–7.

    Google Scholar 

  34. Avatef Fazeli M, Rezaei L, Javadirad E, Iranfar K, Khosravi A, AminiSaman J, et al. Increased incidence of rhino-orbital mucormycosis in an educational therapeutic hospital during the COVID-19 pandemic in western Iran: an observational study. Mycoses. 2021;64(11):1366–77.

    Article  CAS  Google Scholar 

  35. Nair AG, Adulkar NG, D’Cunha L, Rao PR, Bradoo RA, Bapaye MM, et al. Rhino-orbital mucormycosis following COVID-19 in previously non-diabetic, immunocompetent patients. Orbit. 2021;40(6):499–504.

    Article  PubMed  Google Scholar 

  36. Paul SS, Kumar R, Meena VP, Ramprasad A, Garg P, Keri VC, et al. Clinical characteristics and outcomes of 16 cases with COVID19 and mucormycosis: experience from a tertiary care center in India and review of literature. Research Square. 2021. https://doi.org/10.21203/rs.3.rs-533347/v1.

  37. Veisi A, Bagheri A, Eshaghi M, Rikhtehgar MH, RezaeiKanavi M, Farjad R. Rhino-orbital mucormycosis during steroid therapy in COVID-19 patients: a case report. Eur J Ophthalmol. 2022;32(4):NP11–6.

    Article  PubMed  PubMed Central  Google Scholar 

  38. Karimi‐Galougahi M, Arastou S, Haseli S, editors. Fulminant mucormycosis complicating coronavirus disease 2019 (COVID‐19). Int Forum Allergy Rhinol. 2021;11(6):1029.

  39. Farid HA, Hashim AR, Hasrat NH. Rhinocerebral mucormycosis as a COVID-19-related complication: a case report from Basra City, Southern Iraq. J Global Sci Res. 2021;6(5):1369–74.

    Google Scholar 

  40. Alekseyev K, Didenko L, Chaudhry B. Rhinocerebral mucormycosis and COVID-19 pneumonia. J Med Cases. 2021;12(3):85–9.

    Article  PubMed  PubMed Central  Google Scholar 

  41. Baskar HC, Chandran A, Reddy CS, Singh S. Rhino-orbital mucormycosis in a COVID-19 patient. BMJ Case Rep. 2021;14(6):e244232.

    Article  PubMed  PubMed Central  Google Scholar 

  42. Buil JB, van Zanten AR, Bentvelsen RG, Rijpstra TA, Goorhuis B, van der Voort S, et al. Case series of four secondary mucormycosis infections in COVID-19 patients, the Netherlands, December 2020 to May 2021. Eurosurveillance. 2021;26(23):2100510.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Krishna V, Morjaria J, Jalandari R, Omar F, Kaul S. Autoptic identification of disseminated mucormycosis in a young male presenting with cerebrovascular event, multi-organ dysfunction and COVID-19 infection. IDCases. 2021;25:e01172.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Mekonnen ZK, Ashraf DC, Jankowski T, Grob SR, Vagefi MR, Kersten RC, et al. Acute invasive rhino-orbital mucormycosis in a patient with COVID-19-associated acute respiratory distress syndrome. Ophthalmic Plast Reconstr Surg. 2021;37(2):e40–80.

    Article  PubMed  Google Scholar 

  45. Pauli MA, Pereira LM, Monteiro ML, de Camargo AR, Rabelo GD. Painful palatal lesion in a patient with COVID-19. Oral Surg Oral Med Oral Pathol Oral Radiol. 2021;131(6):620–5.

    Article  PubMed  PubMed Central  Google Scholar 

  46. Revannavar SM, Supriya PS, Samaga L, Vineeth V. COVID-19 triggering mucormycosis in a susceptible patient: a new phenomenon in the developing world? BMJ Case Rep. 2021;14(4):e241663.

    Article  PubMed  PubMed Central  Google Scholar 

  47. Maini A, Tomar G, Khanna D, Kini Y, Mehta H, Bhagyasree V. Sino-orbital mucormycosis in a COVID-19 patient: a case report. Int J Surg Case Rep. 2021;82:105957.

    Article  PubMed  PubMed Central  Google Scholar 

  48. Rao R, Shetty AP, Nagesh CP. Orbital infarction syndrome secondary to rhino-orbital mucormycosis in a case of COVID-19: clinico-radiological features. Indian J Ophthalmol. 2021;69(6):1627–30.

    Article  PubMed  PubMed Central  Google Scholar 

  49. Waizel-Haiat S, Guerrero-Paz JA, Sanchez-Hurtado L, Calleja-Alarcon S, Romero-Gutierrez L. A case of fatal rhino-orbital mucormycosis associated with new onset diabetic ketoacidosis and COVID-19. Cureus. 2021;13(2):e13163.

    PubMed  PubMed Central  Google Scholar 

  50. Dallalzadeh LO, Ozzello DJ, Liu CY, Kikkawa DO, Korn BS. Secondary infection with rhino-orbital cerebral mucormycosis associated with COVID-19. Orbit. 2022;41(5):616–9.

    Article  PubMed  Google Scholar 

  51. Arana C, Cuevas Ramirez RE, Xipell M, Casals J, Moreno A, Herrera S, et al. Mucormycosis associated with COVID-19 in two kidney transplant patients. Transpl Infect Dis. 2021;23(4):e13652.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Mehta S, Pandey A. Rhino-orbital mucormycosis associated with COVID-19. Cureus. 2020;12(9):e10726.

    PubMed  PubMed Central  Google Scholar 

  53. Saldanha M, Reddy R, Vincent MJ. Title of the article: paranasal mucormycosis in COVID-19 patient. Indian J Otolaryngol Head Neck Surg. 2022;74(Suppl 2):3407–10. https://doi.org/10.1007/s12070-021-02574-0.

  54. Sargin F, Akbulut M, Karaduman S, Sungurtekin H. Severe rhinocerebral mucormycosis case developed after COVID 19. J Bacteriol Parasitol. 2021;12(1):1000386.

    Google Scholar 

  55. Tabarsi P, Khalili N, Pourabdollah M, Sharifynia S, Naeini AS, Ghorbani J, et al. COVID-19 associated rhinosinusitis mucormycosis due to Rhizopus oryzae: a rare but potentially fatal infection occurring after treatment with corticosteroids. Am J Trop Med Hyg. 2021;105:449–53.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Werthman-Ehrenreich A. Mucormycosis with orbital compartment syndrome in a patient with COVID-19. Am J Emerg Med. 2021;42(264):e5–8.

    Google Scholar 

  57. Sethi HS, Sen KK, Mohanty SS, Panda S, Krishna KR, Mali C. COVID-19-associated rhino-orbital mucormycosis (CAROM)—a case report. Egypt J Radiol Nucl Med. 2021;52(1):1–6.

    Article  Google Scholar 

  58. Shakir M, Maan MHA, Waheed S. Mucormycosis in a patient with COVID-19 with uncontrolled diabetes. BMJ Case Rep. 2021;14(7):e245343.

    Article  PubMed  PubMed Central  Google Scholar 

  59. Gupta SK, Jyotsana P, Singh A, Phuyal D, Allam P. Rhinocerebral mucormycosis in a covid-19 patient from Nepal: a case report. JNMA J Nepal Med Assoc. 2021;59(239):703.

    PubMed Central  Google Scholar 

  60. Ostovan VR, Rezapanah S, Behzadi Z, Hosseini L, Jahangiri R, Anbardar MH, et al. Coronavirus disease (COVID-19) complicated by rhino-orbital-cerebral mucormycosis presenting with neurovascular thrombosis: a case report and review of literature. J Neurovirol. 2021;27(4):644–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  61. Palou EY, Ramos MA, Cherenfant E, Duarte A, Fuentes-Barahona IC, Zambrano LI, et al. COVID-19 associated rhino-orbital mucormycosis complicated by gangrenous and bone necrosis-a case report from Honduras. Vaccines (Basel). 2021;9(8):826.

    Article  CAS  PubMed  Google Scholar 

  62. Eswaran S, Balan SK, Saravanam PK. Acute fulminant mucormycosis triggered by COVID 19 infection in a young patient. Indian J Otolaryngol Head Neck Surg. 2022;74(Suppl 2):3442–6. https://doi.org/10.1007/s12070-021-02689-4.

  63. Meshram HS, Kute VB, Chauhan S, Desai S. Mucormycosis in post-COVID-19 renal transplant patients: a lethal complication in follow-up. Transpl Infect Dis. 2021;23(4):e13663.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  64. Deshmukh R, Upadhyay K, Patwadkar R, Patil S. Mucor mycosis in COVID-19. Journal of Advanced Research in Medicine (E-ISSN: 2349–7181 & P-ISSN: 2394–7047). 2020;7(3):20–3.

  65. Zurl C, Hoenigl M, Schulz E, Hatzl S, Gorkiewicz G, Krause R, et al. Autopsy proven pulmonary mucormycosis due to Rhizopus microsporus in a critically ill COVID-19 patient with underlying hematological malignancy. J Fungi. 2021;7(2):88.

    Article  CAS  Google Scholar 

  66. Placik DA, Taylor WL, Wnuk NM. Bronchopleural fistula development in the setting of novel therapies for acute respiratory distress syndrome in SARS-CoV-2 pneumonia. Radiol Case Rep. 2020;15(11):2378–81.

    Article  PubMed  PubMed Central  Google Scholar 

  67. Pasero D, Sanna S, Liperi C, Piredda D, Branca GP, Casadio L, et al. A challenging complication following SARS-CoV-2 infection: a case of pulmonary mucormycosis. Infection. 2021;49(5):1055–60.

    Article  CAS  PubMed  Google Scholar 

  68. Garg D, Muthu V, Sehgal IS, Ramachandran R, Kaur H, Bhalla A, et al. Coronavirus disease (COVID-19) associated mucormycosis (CAM): case report and systematic review of literature. Mycopathologia. 2021;186(2):289–98.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  69. Kanwar A, Jordan A, Olewiler S, Wehberg K, Cortes M, Jackson BR. A fatal case of Rhizopus azygosporus pneumonia following COVID-19. J Fungi (Basel). 2021;7(3):174.

    Article  CAS  PubMed  Google Scholar 

  70. Johnson AK, Ghazarian Z, Cendrowski KD, Persichino JG. Pulmonary aspergillosis and mucormycosis in a patient with COVID-19. Med Mycol Case Rep. 2021;32:64–7.

    Article  PubMed  PubMed Central  Google Scholar 

  71. Bellanger AP, Navellou JC, Lepiller Q, Brion A, Brunel AS, Millon L, et al. Mixed mold infection with Aspergillus fumigatus and Rhizopus microsporus in a severe acute respiratory syndrome Coronavirus 2 (SARS-CoV-2) patient. Infect Dis Now. 2021;51(7):633–5.

    PubMed  PubMed Central  Google Scholar 

  72. Khan N, Gutierrez CG, Martinez DV, Proud KC. A case report of COVID-19 associated pulmonary mucormycosis. Arch Clin Cases. 2020;7(3):46–51.

    Article  PubMed  Google Scholar 

  73. do Monte Junior ES, Dos Santos MEL, Ribeiro IB, de Oliveira Luz G, Baba ER, Hirsch BS, et al. Rare and fatal gastrointestinal mucormycosis (Zygomycosis) in a COVID-19 patient: a case report. Clinical Endoscopy. 2020;53(6):746–9.

    Article  PubMed  PubMed Central  Google Scholar 

  74. Singh RP, Gupta N, Kaur T, Gupta A. Rare case of gastrointestinal mucormycosis with colonic perforation in an immunocompetent patient with COVID-19. BMJ Case Rep. 2021;14(7):e244096.

    Article  PubMed  PubMed Central  Google Scholar 

  75. Jain M, Tyagi R, Tyagi R, Jain G. Post-COVID-19 gastrointestinal invasive mucormycosis. Indian J Surg. 2022;84(3):545–7.

    Article  PubMed  Google Scholar 

  76. Hanley B, Naresh KN, Roufosse C, Nicholson AG, Weir J, Cooke GS, et al. Histopathological findings and viral tropism in UK patients with severe fatal COVID-19: a post-mortem study. Lancet Microbe. 2020;1(6):e245–53.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  77. Choudhary GR, Aggarwal A, Jain V, Jena R. COVID-19 and fatal renal mucormycosis: contributory or coincidental? Indian J Urol. 2021;37(3):270–3.

    Article  PubMed  PubMed Central  Google Scholar 

  78. Singh T, Chaudhari R, Gupta A. Renal artery thrombosis and mucormycosis in a COVID-19 patient. Indian J Urol. 2021;37(3):267–9.

    Article  PubMed  PubMed Central  Google Scholar 

  79. Khatri A, Chang KM, Berlinrut I, Wallach F. Mucormycosis after coronavirus disease 2019 infection in a heart transplant recipient - case report and review of literature. J Mycol Med. 2021;31(2):101125.

    Article  PubMed  PubMed Central  Google Scholar 

  80. Tan T, Khoo B, Mills EG, Phylactou M, Patel B, Eng PC, et al. Association between high serum total cortisol concentrations and mortality from COVID-19. Lancet Diabetes Endocrinol. 2020;8(8):659–60.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  81. Lionakis MS, Kontoyiannis DP. Glucocorticoids and invasive fungal infections. Lancet. 2003;362(9398):1828–38.

    Article  CAS  PubMed  Google Scholar 

  82. Habib HM, Ibrahim S, Zaim A, Ibrahim WH. The role of iron in the pathogenesis of COVID-19 and possible treatment with lactoferrin and other iron chelators. Biomed Pharmacother. 2021;136:111228.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  83. Ibrahim AS, Spellberg B, Walsh TJ, Kontoyiannis DP. Pathogenesis of mucormycosis. Clin Infect Dis. 2012;54(suppl_1):16–22.

    Article  Google Scholar 

  84. Gavriilaki E, Anyfanti P, Gavriilaki M, Lazaridis A, Douma S, Gkaliagkousi E. Endothelial dysfunction in COVID-19: lessons learned from coronaviruses. Curr Hypertens Rep. 2020;22(9):63.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  85. Pal R, Singh B, Bhadada SK, Banerjee M, Bhogal RS, Hage N, et al. COVID-19-associated mucormycosis: an updated systematic review of literature. Mycoses. 2021;64(12):1452–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  86. Hoenigl M, Seidel D, Carvalho A, Rudramurthy SM, Arastehfar A, Gangneux JP, et al. The emergence of COVID-19 associated mucormycosis: a review of cases from 18 countries. Lancet Microbe. 2022;3(7):e543–52. This study showed high mortality of CAM, especially in pulmonary, disseminated, and cerebral involvement. An association between ICU admission and non-ROCM mucormycosis was also demonstrated.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  87. Chinn RY, Diamond RD. Generation of chemotactic factors by Rhizopus oryzae in the presence and absence of serum: relationship to hyphal damage mediated by human neutrophils and effects of hyperglycemia and ketoacidosis. Infect Immun. 1982;38(3):1123–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  88. Muthu V, Rudramurthy SM, Chakrabarti A, Agarwal R. Epidemiology and pathophysiology of COVID-19-associated mucormycosis: India versus the rest of the world. Mycopathologia. 2021;186(6):739–54.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Authors and Affiliations

  1. Director of Residency Program, Department of Oral & Maxillofacial Surgery, School of Dentistry, Ahvaz Jundishapur University of Medical Sciences, Ahvaz, Iran

    Kazem Khiabani

  2. Department of Research & Development, Farinroshaan Medical & Health Co. LTD, Tehran, Iran

    Mohammad Hosein Amirzade-Iranaq

  3. Student Research Committee, Shiraz University of Medical Sciences, Shiraz, Iran

    Hanie Ahmadi

Authors
  1. Kazem Khiabani
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  2. Mohammad Hosein Amirzade-Iranaq
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  3. Hanie Ahmadi
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Contributions

The conceptualization of the study was performed with K.K. Everyone contributed to the design and data acquisition. M.H.A and K.K performed data analysis. K.K performed the final interpretation of the findings. All contributed to drafting and critically revising the manuscript. All authors gave final approval and agreed to be accountable for all aspects of the work.

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Correspondence to Kazem Khiabani.

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Figure S2. The overall risk of bias assessment. Risk of Bias assessed by the Joanna Briggs Institute Critical Appraisal Tools for case reports/series studies (JPEG 573 KB)

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Khiabani, K., Amirzade-Iranaq, M.H. & Ahmadi, H. An Update on COVID‐19 Associated Mucormycosis Characteristics, Risk Factors, and Outcomes: a Systematic Review and Meta-Analysis. Curr Fungal Infect Rep 17, 282–295 (2023). https://doi.org/10.1007/s12281-023-00477-x

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