Skip to main content

Advertisement

SpringerLink
Log in

Mucormycosis and Its Upsurge During COVID-19 Epidemic: An Updated Review

  • Review Article
  • Published:
Current Microbiology Aims and scope Submit manuscript

Abstract

Although mucormycosis may have reached an epidemic situation during the COVID-19 pandemic, the term was much more familiar even before the COVID-19 period. The year 2020 showed an outbreak of novel coronavirus (SARS-CoV-2) which affected millions of people all over the world. One of the noticeable complications observed to be associated with this disease is mucormycosis. It is an opportunistic infection caused by members of the Order Mucorales existing worldwide and has been commonly reported as a laboratory contaminant for a long time. However, nowadays due to the changes in the host environment, they have been emerging as potent opportunistic pathogens responsible for causing primary infections or coinfections with other diseases eventually resulting in morbidity and even mortality in severe cases. Although immunocompromised patients are more susceptible to this infection, few cases have been reported in immunocompetent individuals. Various risk factors which are responsible for the acquisition of mucormycosis include diabetes mellitus type 2, ketoacidosis, hematological malignancies, organ transplants, and chemotherapy recipients. Among the various etiological agents, Rhizopus is found to be the most common, and rhino-cerebral to be the most frequent clinical presentation. As far as pathogenesis is concerned, host cell invasion, thrombosis, and necrosis are the main events in the progression of this disease. The aim of the present review is to address a complete spectrum of mucormycosis and COVID-19-associated mucormycosis (CAM) in a single article. Both global and Indian scenarios of mucormycosis are taken into account while framing this review.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  1. Farnoosh G, Alishiri G, Hosseini Zijoud SR, Dorostkar R, Jalali FA (2020) Understanding the severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) and coronavirus disease (COVID-19) based on available evidence—a narrative review. J Mil Med 22:1–11

    Google Scholar 

  2. Wang X, Ding H, Chen Z et al (2020) CARD 9 deficiency in a Chinese man with cutaneous mucormycosis, recurrent deep dermatophytosis and a review of the literature. Mycopathologia 185:1041–1050. https://doi.org/10.1007/s11046-020-00487-0

    Article  CAS  PubMed  Google Scholar 

  3. Goyal P, Choi JJ, Pinheiro LC, Schenck EJ, Chen R, Jabri A, Satlin MJ, Campion TR et al (2020) Clinical characteristics of COVID-19 in New York City. N Engl J Med 382:2372–2374. https://doi.org/10.1056/nejmc2010419

    Article  CAS  PubMed  Google Scholar 

  4. World Health Organisation (WHO) (2023) Coronavirus (COVID-19) Dashboard. https://covid19.who.int/ Accessed 23 Mar 2023

  5. Goursaud S, Descamps R, Daubin C, du Cheyron D, Valette X (2020) Corticosteroid use in selected patients with severe acute respiratory distress syndrome related to COVID-19. J Infect 81:e89–e90. https://doi.org/10.1016/j.jinf.2020.05.023

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Peman J, Ruiz-Gaitan A, Garcia-Vidal C, Salavert M, Ramirez P, Puchades F et al (2020) Fungal co-infection in COVID-19 patients: should we be concerned? Rev Iberoam Micol 37:41–46. https://doi.org/10.1016/j.riam.2020.07.001

    Article  PubMed  PubMed Central  Google Scholar 

  7. Moorthy A, Gaikwad R, Krishna S, Hegde R, Tripathi KK, Kale PG et al (2021) 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 20:418–425. https://doi.org/10.1007/s12663-021-01532-1

    Article  PubMed  PubMed Central  Google Scholar 

  8. Torres-Narbona M, Guinea J, Martinez-Alarcon J et al (2007) Impact of mucormycosis on microbiology overload: a survey study in Spain. J Clin Microbiol 45:2051–2053. https://doi.org/10.1128/JCM.02473-06

    Article  PubMed  PubMed Central  Google Scholar 

  9. Ben-Ami R, Luna M, Lewis RE, Walsh TJ, Kontoyiannis DP (2009) A clinicopathological study of pulmonary mucormycosis in cancer patients: extensive angioinvasion but limited inflammatory response. J Infect 59:134–138. https://doi.org/10.1016/j.jinf.2009.06.002

    Article  PubMed  PubMed Central  Google Scholar 

  10. Mantadakis E, Samonis G (2009) Clinical presentation of zygomycosis. Clin Microbiol Infect 15:15–20. https://doi.org/10.1111/j.1469-0691.2009.02974.x

    Article  PubMed  Google Scholar 

  11. Richardson MD, Rautemaa-Richardson R (2020) Biotic environments supporting the persistence of clinically relevant mucormycetes. J Fungi 6:4. https://doi.org/10.3390/jof6010004

    Article  Google Scholar 

  12. Mousavi B, Botterel F, Costa JM, Arne P, Guillot J, Dannaoui E (2019) Occurrence and species diversity of human-pathogenic Mucorales in commercial food-stuffs purchased in Paris area. Med Mycol 57(6):739–744. https://doi.org/10.1093/mmy/myy121

    Article  PubMed  Google Scholar 

  13. Singh AK, Singh R, Joshi SR, Misra A (2021) Mucormycosis in COVID-19: a systematic review of cases reported worldwide and in India. Diabetes Meta Syndr 15:102146. https://doi.org/10.1016/j.dsx.2021.05.019

    Article  CAS  Google Scholar 

  14. Sharma K, Mishra S, Gautam A, Malviya R (2021) Mucormycosis—a fungal infection in patient recovered from COVID-19. Lette Appl Nanosci 11:3802–3810. https://doi.org/10.33263/LIANBS113.38023810

    Article  Google Scholar 

  15. Petrikkos G, Skiada A, Sambatakou TA, Vaiopoulos G, Giannopoulou M, Katsilambros N (2003) Mucormycosis: Ten-year experience at a tertiary-care center in Greece. Eur J Clin Microbiol Infect Dis 22:753–756. https://doi.org/10.1007/s10096-003-1035-y

    Article  CAS  PubMed  Google Scholar 

  16. Rammaert B, Lanternier F, Zahar JR et al (2012) Healthcare-associated mucormycosis. Clin Infect Dis 54:S44–S54. https://doi.org/10.1093/cid/cir867

    Article  PubMed  Google Scholar 

  17. Chakrabarti A, Chatterjee S, Das A et al (2009) Invasive zygomycosis in India: experience in a tertiary care hospital. Postgrad Med J 85:573–581. https://doi.org/10.1136/pgmj.2008.076463

    Article  CAS  PubMed  Google Scholar 

  18. Bala K, Chander J, Handa U, Puni RS, Attri AK (2015) A prospective study of mucormycosis in North India: experience from a tertiary care hospital. Med Mycol 53:248–257. https://doi.org/10.1093/mmy/myu086

    Article  PubMed  Google Scholar 

  19. Skiada A, Pagano L, Groll A, Zimmerli S, Dupont B, Lagrou K, Lass-Florl C, Bouza E, Klimko N, Gaustad P et al (2011) Zygomycosis in Europe: analysis of 230 cases accrued by the registry of the European confederation of medical mycology (ECMM) working Group on zygomycosis between 2005 and 2007. Clin Microbiol Infect 17:1859–1867. https://doi.org/10.1111/j.1469-0691.2010.03456.x

    Article  CAS  PubMed  Google Scholar 

  20. Prakash H, Ghosh AK, Rudramurthy SM, Singh XI, Savio J, Pamidimukkala U, Jillwin J, Varma S, Das A et al (2019) A prospective multicenter study on mucormycosis in India: Epidemiology, diagnosis, and treatment. Med Mycol 57:395–402. https://doi.org/10.1093/mmy/myy060

    Article  PubMed  Google Scholar 

  21. Patel A, Kaur H, Xess I, Michael JS, Savio J, Rudramurthy S, Singh R, Shastri P, Umabala P, Sardana R et al (2020) A multi-center observational study on the epidemiology, risk factors, management and outcomes of mucormycosis in India. Clin Microbiol Infect 26:944.e9-944.e15. https://doi.org/10.1016/j.cmi.2019.11.021

    Article  CAS  PubMed  Google Scholar 

  22. Fanfair RN, Benedict K, Bos J, Bennett SD, Lo YC, Adebanjo T, Etienne K, Deak E, Derado G, Shieh WJ, Drew C, Zaki S, Sugerman D, Gade L, Thompson EH, Sutton DA, Engelthaler DM, Schupp JM, Brandt ME, Harris JR, Lockhart SR, Turabelidze G, Park BJ et al (2012) Necrotizing cutaneous mucormycosis after a tornado in Joplin, Missouri, in 2011. N Engl J Med 367:2214–2225. https://doi.org/10.1056/NEJMoa1204781

    Article  CAS  Google Scholar 

  23. Benedict K, Park BJ (2014) Invasive fungal infections after natural disasters. Emerg Infect Dis 20:349. https://doi.org/10.3201/eid2003.131230

    Article  PubMed  PubMed Central  Google Scholar 

  24. Jeong W, Keighley C, Wolfe R et al (2019) The epidemiology and clinical manifestations of mucormycosis: a systematic review and meta-analysis of case reports. Clin Microbiol Infect 25:26–34. https://doi.org/10.1016/j.cmi.2018.07.011

    Article  CAS  PubMed  Google Scholar 

  25. Khatri A, Chang KM, Berlinrut I, Wallach F (2021) Mucormycosis after coronavirus disease 2019 infection in a heart transplant recipient—case report and review of literature. J Med Mycol 31:101125. https://doi.org/10.1016/j.mycmed.2021.101125

    Article  Google Scholar 

  26. Sen M, Honavar SG, Bansal R et al (2021) 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 69:1670–1692. https://doi.org/10.4103/ijo.IJO_1565_21

    Article  PubMed  PubMed Central  Google Scholar 

  27. Roden MM, Zaoutis TE, Buchanan WL et al (2005) Epidemiology and outcome of zygomycosis: a review of 929 reported cases. Clin Infect Dis 41:634–653. https://doi.org/10.1086/432579

    Article  PubMed  Google Scholar 

  28. Zilberberg MD, Shorr AF, Huang H, Chaudhari P, Paly VF, Menzin J (2014) Hospital days, hospitalization costs, and inpatient mortality among patients with mucormycosis: a retrospective analysis of US hospital discharge data. BMC Infect Dis 14:310. https://doi.org/10.1186/1471-2334-14-310

    Article  PubMed  Google Scholar 

  29. Meis JF, Chakrabarti A (2009) Changing epidemiology of an emerging infection: zygomycosis. Clin Microbiol Infect 15:10–14. https://doi.org/10.1111/j.1469-0691.2009.02973.x

    Article  PubMed  Google Scholar 

  30. Queiroz-Telles F, Nucci M, Colombo AL, Tobon A, Restrepo A (2011) Mycoses of implantation in Latin America: an overview of epidemiology, clinical manifestations, diagnosis and treatment. Med Mycol 49:225–236. https://doi.org/10.3109/13693786.2010.539631

    Article  PubMed  Google Scholar 

  31. Chakrabarti A, Das A, Sharma A et al (2001) Ten years’ experience in zygomycosis at a tertiary care centre in India. J Infect 42:261–266. https://doi.org/10.1053/jinf.2001.0831

    Article  CAS  PubMed  Google Scholar 

  32. Chakrabarti A, Das J, Mandal J et al (2006) The rising trend of invasive zygomycosis in patients with uncontrolled diabetes mellitus. Med Mycol 44:335–342. https://doi.org/10.1080/13693780500464930

    Article  PubMed  Google Scholar 

  33. Nithyanandam S, Jacob MS, Battu RR et al (2003) Rhino-orbito-cerebral mucormycosis. A retrospective analysis of clinical features and treatment outcomes. Indian J Ophthalmol 51:231–236

    PubMed  Google Scholar 

  34. Chander J (2018) Mucormycosis Textbook of Medical Mycology, 4th edn. Jaypee Brothers Medical Publishers Ltd, New Delhi, pp 534–596

    Google Scholar 

  35. Furbinger P (1876) Observations on lungenmycose beinmeschen. Arch Pathol Anat Physiol Klin Med 66:330–365

    Google Scholar 

  36. Paltauf A (1885) Mycosis mucorina, Archiv. Fur. Pathologische. Anatomie. Und Physiologie Und Fur Klinische Medicin 102:543–564

    Google Scholar 

  37. Gregory JE, Golden A, Haymaker W (1943) Mucormycosis of the central nervous system: a report of three cases. Bull Johns Hopkins Hosp 73:405–419

    Google Scholar 

  38. Baker RD (1957) Mucormycosis—a new disease? J Am Med Assoc 163:805–808

    Article  CAS  PubMed  Google Scholar 

  39. Balasubrahmanyan M, Chaudhuri S (1963) A case of pulmonary mucormycosis. Indian J Pathol Bacteriol 6:60–62

    CAS  PubMed  Google Scholar 

  40. Grover S, Naidu A, Jonarkar RV (1966) Rhinocerebral phycomycosis (a case report). Indian J Pathol Bacteriol 9:264

    CAS  PubMed  Google Scholar 

  41. Hazarika P, Ravikumar V, Nayak RG, Rao PS, Shivananda PG (1984) Rhinocerebral mycosis. Ear Nose Throat J 63:464–468

    CAS  PubMed  Google Scholar 

  42. Singh CM, Naik BN, Pandey S, Singh PK, Rajath Rao UR, Kokkayil P, Bhavana K, Singh PK (2022) Investigation of an acute surge of COVID-19 associated mucormycosis (CAM) cases reported to a tertiary health care institution in Bihar. India J Family Med Prim Care 11(6):2802–2810. https://doi.org/10.4103/jfmpc.jfmpc_1909_21

    Article  PubMed  Google Scholar 

  43. Ribes JA, Vanover-Sams CL, Baker DJ (2000) Zygomycetes in human disease. Clin Microbiol Rev 13:236–301. https://doi.org/10.1128/CMR.13.2.236

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Skiada A, Petrikkos G (2009) Cutaneous mucormycosis. Clin Microbiol Infect 15:41–45. https://doi.org/10.1111/j.1469-0691.2009.02979.x

    Article  PubMed  Google Scholar 

  45. Hutter RVP (1959) Phycomycetous infection (mucormycosis) in cancer patients: a complication of therapy. Cancer 12:330–350

    Article  CAS  PubMed  Google Scholar 

  46. Kontoyiannis DP, Yang H, Song J et al (2016) Prevalence, clinical and economic burden of mucormycosis-related hospitalizations in the United States: a retrospective study. BMC Infect Dis 16:730. https://doi.org/10.1186/s12879-016-2023-z

    Article  PubMed  PubMed Central  Google Scholar 

  47. Rees JR, Pinner RW, Hajjeh RA, Brandt ME, Reingold AL (1998) The epidemiological features of invasive mycotic infections in the San Francisco Bay area, 1992–1993: results of population-based laboratory active surveillance. Clin Infect Dis 27:1138–1147

    Article  CAS  PubMed  Google Scholar 

  48. Bitar D, Van Cauteren D, Lanternier F et al (2009) Increasing incidence of zygomycosis (mucormycosis), France, 1997–2006. Emerg Infect Dis 15:1395–1401. https://doi.org/10.3201/eid1509.090334

    Article  PubMed  PubMed Central  Google Scholar 

  49. Diwakar A, Dewan RK, Chowdhary A, Randhawa HS, Khanna G, Gaur SN (2007) Zygomycosis—a case report and overview of the disease in India. Mycoses 50:247–254. https://doi.org/10.1007/s12262-012-0429-4

    Article  PubMed  Google Scholar 

  50. Saegeman V, Maertens J, Meersseman W et al (2010) Increasing incidence of mucormycosis in University Hospital, Belgium. Emerg Infect Dis 16:1456–1458. https://doi.org/10.3201/eid1609.100276

    Article  PubMed  PubMed Central  Google Scholar 

  51. Yamazaki T, Kume H, Murase S et al (1999) Epidemiology of visceral mycoses: analysis of data in annual of the pathological autopsy cases in Japan. J Clin Microbiol 37:1732–1738. https://doi.org/10.1128/jcm.37.6.1732-1738.1999

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Dolatabadi S, Ahmadi B, Rezaei-Matehkolaei A, Zarrinfar H, Skiada A, Mirhendi H, Niknejad NF, Nazeri M, Rafiei A et al (2018) Mucormycosis in Iran: A six-year retrospective experience. J Mycol Med 28:269–273. https://doi.org/10.1016/j.mycmed.2018.02.014

    Article  CAS  PubMed  Google Scholar 

  53. Bhansali A, Bhadada S, Sharma A, Suresh V, Gupta A, Singh P, Chakarbarti RA, Dash J (2004) Presentation and outcome of rhino-orbital-cerebral mucormycosis in patients with diabetes. Postgrad Med J 80:670–674. https://doi.org/10.1136/pgmj.2003.016030

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. Godara SM, Kute VB, Goplani KR et al (2011) Mucormycosis in renal transplant recipients: predictors and outcome. Saudi J Kidney Dis Transpl 22:751–756

    CAS  PubMed  Google Scholar 

  55. Patra S, Vij M, Chirla DK et al (2012) Unsuspected invasive neonatalgastrointestinal mucormycosis: a clinicopathological study of six cases from a tertiary care hospital. J Indian Assoc Pediatr Surg 17:153–156. https://doi.org/10.4103/0971-9261.102329

    Article  PubMed  PubMed Central  Google Scholar 

  56. Walther G, Wagner L, Kurzai O (2019) Updates on the taxonomy of mucorales with an emphasis on clinically important taxa. J Fungi 5:106. https://doi.org/10.3390/jof5040106

    Article  CAS  Google Scholar 

  57. Sharma B, Nonzom S (2021) Superficial mycoses, a matter of concern: global and Indian scenario-an updated analysis. Mycoses 64:890–908. https://doi.org/10.1111/myc.13264

    Article  PubMed  Google Scholar 

  58. Hemashettar BM, Patil RN, O’Donnell K, Chaturvedi V, Ren P, Padhye AA (2011) Chronic rhinofacial mucormycosis caused by Mucor irregularis (Rhizomucor variabilis) in India. J Clin Microbiol 49:2372–2375. https://doi.org/10.1128/JCM.02326-10

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. Prakash H, Chakrabarti A (2019) Global epidemiology of mucormycosis. J Fungi 5:26

    Article  CAS  Google Scholar 

  60. Kokkayil P, Pandey M, Agarwal R, Kale P, Singh G, Xess I (2017) Rhizopus homothallicus causing invasive infections: series of three cases from a single center in North India. Mycopathologia 182:921–926. https://doi.org/10.1007/s11046-017-0153-5

    Article  PubMed  Google Scholar 

  61. Tsyrkunou AV, Ellison RT, Akalin A, Wiederhold N, Sutton DA, Lindner J et al (2014) Multifocal Rhizopus microsporus lung infection following brush clearing. Med Mycol Case Rep 6:14–17. https://doi.org/10.1016/j.mmcr.2014.08.001

    Article  PubMed  PubMed Central  Google Scholar 

  62. Chakrabarti A, Singh R (2011) The emerging epidemiology of mould infections in developing countries. Curr Opin Infect Dis 24:521–526. https://doi.org/10.1097/QCO.0b013e32834ab21e

    Article  PubMed  Google Scholar 

  63. Xess I, Mohapatra S, Shivaprakash MR, Chakrabarti A, Benny GL, O’Donnell K et al (2012) Evidence implicating Thamnostylum lucknowense as an etiological agent of rhino-orbital mucormycosis. J Clin Microbiol 50:1491–1494. https://doi.org/10.1128/JCM.06611-11

    Article  PubMed  PubMed Central  Google Scholar 

  64. Chakrabarti A, Marak RS, Shivaprakash MR, Gupta S, Garg R, Sakhuja V et al (2010) Cavitary pulmonary zygomycosis caused by Rhizopus homothallicus. J Clin Microbiol 48:1965–1969. https://doi.org/10.1128/JCM.01272-09

    Article  PubMed  PubMed Central  Google Scholar 

  65. Kimura M, Udagawa S, Makimura K, Satoh K, Toyazaki N, Ito H (2009) Isolation and identification of Rhizomucor pusillus from pleural zygomycosis in an immunocompetent patient. Med Mycol 47:869–873. https://doi.org/10.3109/13693780903059485

    Article  PubMed  Google Scholar 

  66. Gomes MZR, Lewis RE, Kontoyiannis DP (2011) Mucormycosis caused by unusual mucormycetes, non-Rhizopus, Mucor and Lichtheimia species. Clin Microbiol Rev 24:411–445. https://doi.org/10.1128/CMR.00056-10

    Article  PubMed  PubMed Central  Google Scholar 

  67. Verma R, Nair V, Vasudevan B, Vijendran P, Behera V, Neema S (2014) Rare case of primary cutaneous mucormycosis of the hand caused by Rhizopus microsporus in an immunocompetent patient. Int J Dermatol 53:66–69. https://doi.org/10.1097/QCO.0b013e32834ab21e

    Article  Google Scholar 

  68. Pandey M, Singh AR, Dabas Y, Jyotsna VP, Kumar R et al (2018) Emerging Rhizopus microsporus infections in India. J Clin Microbio 56:1–5. https://doi.org/10.1128/JCM.00433-18

    Article  Google Scholar 

  69. Lanternier F, Dannaoui E, Morizot G, Elie C, Garcia-Hermoso D, Huerre M, Bitar D, Dromer F et al (2012) A global analysis of mucormycosis in France: the retro zygo study (2005–2007). Clin Infect Dis 54:S35–S43. https://doi.org/10.1093/cid/cir880

    Article  CAS  PubMed  Google Scholar 

  70. Kennedy KJ, Daveson K, Slavin MA, van Hal SJ, Sorrell TC, Lee A, Marriott DJ, Chapman B, Halliday CL, Australia and New Zealand Mycoses Interest Group of the Australasian Society for Infectious Diseases et al (2016) Mucormycosis in Australia: contemporary epidemiology and outcomes. Clin Microbiol Infect 22:775–781. https://doi.org/10.1016/j.cmi.2016.01.005

    Article  CAS  PubMed  Google Scholar 

  71. Stelzmueller I, Lass-Floerl C, Geltner C et al (2008) Zygomycosis and other rare filamentous fungal infections in solid organ transplant recipients. Transpl Int 21:534–546

    Article  PubMed  Google Scholar 

  72. International Diabetes Federation (IDF) Diabetes Atlas. https:// diabetesatlas.org/en/resources/2019s 10 May 2021

  73. Greenberg RN, Scott LJ, Vaughn HH, Ribe JA (2004) Zygomycosis (mucormycosis): emerging clinical importance and new treatments. Curr Opin Infect Dis 17:517–525. https://doi.org/10.1097/00001432-200412000-00003

    Article  CAS  PubMed  Google Scholar 

  74. Vaezi A, Moazeni M, Rahimi MT et al (2016) Mucormycosis in Iran: a systematic review. Mycoses 59:402–415. https://doi.org/10.1111/myc.12474

    Article  PubMed  Google Scholar 

  75. Corzo-Leon DE, Chora-Hernandez LD, Rodriguez-Zulueta AP, Walsh TJ (2018) Diabetes mellitus as the major risk factor for mucormycosis in Mexico: epidemiology, diagnosis, and outcomes of reported cases. Med Mycol 56:29–43. https://doi.org/10.1093/mmy/myx017

    Article  PubMed  Google Scholar 

  76. Pagano L, Valentini CG, Posteraro B, Girmenia C, Ossi C, Pan A, Candoni A, Nosari A, Riva M, Cattaneo C et al (2009) Zygomycosis in Italy: A survey of FIMUA-ECMM (Federazione Italiana di Micopatologia Umana ed Animale and European Confederation of Medical Mycology). J Chemother 21:322–329. https://doi.org/10.1179/joc.2009.21.3.322

    Article  CAS  PubMed  Google Scholar 

  77. Petrikkos G, Skiada A, Lortholary O, Roilides E, Walsh TJ, Kontoyiannis DP (2012) Epidemiology and clinical manifestations of mucormycosis. Clin Infect Dis 54:S23–S34. https://doi.org/10.1093/cid/cir866

    Article  PubMed  Google Scholar 

  78. Serris A, Danion F, Lanternier F (2019) Disease entities in mucormycosis. J Fungi 5:23. https://doi.org/10.3390/jof5010023

    Article  Google Scholar 

  79. Kursun E, Turunc T, Demiroglu Y, Alıskan HE, Arslan AH (2015) Evaluation of 28 cases of mucormycosis. Mycoses 58:82–87. https://doi.org/10.1111/myc.12278

    Article  PubMed  Google Scholar 

  80. Lelievre L, Garcia-Hermoso D, Abdoul H et al (2014) Posttraumatic mucormycosis. Medicine (Baltimore) 93:373–382. https://doi.org/10.1097/MD.0000000000000221

    Article  Google Scholar 

  81. Sulis G, Daniels B, Kwan A, Gandra S, Daftary A, Das J et al (2020) Antibiotic overuse in the primary health care setting: a secondary data analysis of standardised patient studies from India China and Kenya. BMJ Glob Health 5(9):e003393. https://doi.org/10.1136/bmjgh-2020-003393

    Article  PubMed  PubMed Central  Google Scholar 

  82. Sulis G, Batomen B, Kotwani A, Pai M, Gandra S (2021) Sales of antibiotics and hydroxychloroquine in India during the COVID-19 epidemic: an interrupted time series analysis. PLoS Med 18:e1003682. https://doi.org/10.1371/journal.pmed.1003682

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  83. Waldorf AR (1989) Pulmonary defense mechanisms against opportunistic fungal pathogens. Immunol Ser 47:243–271

    CAS  PubMed  Google Scholar 

  84. Chinn RY, Diamond RD (1982) 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 38:1123–1129. https://doi.org/10.1128/iai.38.3.1123-1129.1982

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  85. Potenza L, Vallerini D, Barozzi P, Riva G, Forghieri F, Zanetti E, Quadrelli C, Candoni A, Maertens J, Rossi G et al (2011) Mucorales-specific T cells emerge in the course of invasive mucormycosis and may be used as a surrogate diagnostic marker in high-risk patients. Blood 118:5416–5419. https://doi.org/10.1371/journal.pone.0149108

    Article  CAS  PubMed  Google Scholar 

  86. Boelaert JR, de Locht M, Van Cutsem J et al (1993) Mucormycosis during deferoxamine therapy is a siderophore-mediated infection: in-vitro and in-vivo animal studies. J Clin Invest 91:1979–1986. https://doi.org/10.1172/JCI116419

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  87. Howard DH (1999) Acquisition, transport, and storage of iron by pathogenic fungi. Clin Microbiol Rev 12:394–404. https://doi.org/10.1128/CMR.12.3.394

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  88. Reid DW, Lam QT, Schneider H, Walters EH (2004) Airway iron and iron-regulatory cytokines in cystic fibrosis. Eur Respir J 24:286–291

    Article  CAS  PubMed  Google Scholar 

  89. Chamilos G, Lewis R, Lamaris G, Walsh TJ, Kontoyiannis DP (2008) Zygomycetes hyphae trigger an early, robust proinflammatory response in human polymorphonuclear neutrophils through toll-like receptor 2 induction but display relative resistance to oxidative damage. Antimicrob Agents Chemother 52:722–724. https://doi.org/10.1128/AAC.01136-07

    Article  CAS  PubMed  Google Scholar 

  90. Bouchara P, Oumeziane NA, Lissitzky JC, Larcher G, Tronchin G, Chabasse D (1996) Attachment of spores of the human pathogenic fungus Rhizopus oryzae to extracellular smatrixcomponents. Eur J Cell Biol 70:76–83

    CAS  PubMed  Google Scholar 

  91. Ibrahim AS, Spellberg B, Avanessian V, Fu Y, Edwards JE (2005) Rhizopus oryzae adheres to, is phagocytosed by, and damages endothelial cells in-vitro. Infect Immun 73(2):778–783. https://doi.org/10.1128/IAI.73.2.778-783.2005

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  92. Gebremariam T, Liu M, Luo G, Bruno V, Phan QT, Waring AJ et al (2014) CotH3 mediates fungal invasion of host cells during mucormycosis. J Clin Invest 124:237–250. https://doi.org/10.1172/JCI71349

    Article  CAS  PubMed  Google Scholar 

  93. Lee SC, Billmyre RB, Li A, Carson S, Sykes SM, Huh EY et al (2014) Analysis of a food-borne fungal pathogen outbreak: virulence and genome of a Mucor circinelloides isolate from yogurt. mBio 5(4):e01390-14. https://doi.org/10.1128/mBio.01390-14

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  94. Voigt K, Wolf T, Ochsenreiter K, Nagy G, Kaeger K, Shelest E et al (2016) Genetic and metabolic aspects of primary and secondary metabolism of the zygomycetes, In: D. Hoffmeister (Eds.), The Mycota Vol III: Biochemistry and Molecular Biology, 3rd Edition III ed: Springer Verlag, Berlin, pp. 361–385

  95. Effat KG, Karam M, El-Kabani A (2005) Pott’s puffy tumour caused by mucormycosis. J Laryngol Otol 119:643–645. https://doi.org/10.1258/0022215054516304

    Article  CAS  PubMed  Google Scholar 

  96. Gleissner A, Schilling A, Anagnostopolous I, Siehl I, Thiel E (2004) Improved outcome of zygomycosis in patients with hematological diseases? Leuk Lymphoma 45:1351–1360. https://doi.org/10.1080/10428190310001653691

    Article  CAS  PubMed  Google Scholar 

  97. Prabhu RM, Patel R (2004) Mucormycosis and entomophthoramycosis: a review of the clinical manifestations, diagnosis and treatment. Clin Microbiol Infect 10:31–47. https://doi.org/10.1111/j.1470-9465.2004.00843.x

    Article  PubMed  Google Scholar 

  98. Dobrilovic N, Wait MA (2005) Pulmonary mucormycosis. Ann Thorac Surg 79:354. https://doi.org/10.1016/S0003-4975(03)01287-6

    Article  PubMed  Google Scholar 

  99. Jaju MR, Sagar RV, Srivastav SK, Singh R, Kumar KV, Faisal M (2020) Different types of mucormycosis: case series. Int J Res Med Sci 8:2284–2296. https://doi.org/10.18203/2320-6012.ijrms20202281

    Article  Google Scholar 

  100. Dubey A, Patwardhan RV, Sampth S, Santosh V, Kolluri S, Nanda A (2005) Intracranial fungal granuloma: analysis of 40 patients and review of the literature. Surg Neurol 63:254–260. https://doi.org/10.1016/j.surneu.2004.04.020

    Article  PubMed  Google Scholar 

  101. Paparello SF, Robert L, Dougald CMG, Nadine B, Douglas LM (1992) Hospital-acquired wound mucormycosis. Clin Infect Dis 14:350–352. https://doi.org/10.1093/clinids/14.1.350

    Article  CAS  PubMed  Google Scholar 

  102. Ingram CW, Sennesh J, Cooper JN, Perfect JR (1989) Disseminated zygomycosis: report of four cases and review. Rev Infect Dis 11:741–754. https://doi.org/10.1093/clinids/11.5.741

    Article  CAS  PubMed  Google Scholar 

  103. Yu J, Li RY (2006) Primary renal zygomycosis due to Rhizopus oryzae. Med Mycol 44:461466. https://doi.org/10.1080/13693780500338951

    Article  Google Scholar 

  104. Weng DE, Wilson WH, Little R, Walsh TJ (1998) Successful medical management of isolated renal mucormycosis: case report and review. Clin Infect Dis 26:601–605. https://doi.org/10.1086/514562

    Article  CAS  PubMed  Google Scholar 

  105. Chkhotua A, Yussim A, Tovar A, Weinberger M, Sobolev V, Bar-Nathan N, Shaharabani E, Shapira Z, Mor E (2001) Mucormycosis of the renal allograft: case report and review of the literature. Transpl Int 14:438–441. https://doi.org/10.1007/s001470100010

    Article  CAS  PubMed  Google Scholar 

  106. Chen L, Xiao Y, Wang X (2005) Successful treatment of mucormycosis in the pulmonary artery after cardiac surgery. J Card Surg 20:186–188. https://doi.org/10.1111/j.0886-0440.2005.200382q.x

    Article  PubMed  Google Scholar 

  107. Zhang R, Zhang JW, Szerlip HM (2002) Endocarditis and hemorrhagic stroke caused by Cunninghamella bertholletiae infection after kidney transplantation. Am J Kidney Dis 40:842–846. https://doi.org/10.1053/ajkd.2002.35698

    Article  PubMed  Google Scholar 

  108. Wanishsawad C, Kimbrough RC, Chinratanalab S, Nugent K (1996) Mucormycotic osteolytic rib lesion presenting as subacute pleural effusion. Clin Infect Dis 22:715–716. https://doi.org/10.1093/clinids/22.4.715

    Article  CAS  PubMed  Google Scholar 

  109. Serna JH, Wanger A, Dosekun AK (2003) Successful treatment of mucormycosis peritonitis with liposomal amphotericin B in a patient on long-term peritoneal dialysis. Am J Kidney Dis 42:14–17. https://doi.org/10.1016/s0272-6386(03)00797-2

    Article  Google Scholar 

  110. Oliver MR, Van Voorhis WC, Boeckh M et al (1996) Hepatic mucormycosis in a bone marrow transplant recipient who ingested naturopathic medicine. Clin Infect Dis 22:521–524. https://doi.org/10.1093/clinids/22.3.521

    Article  CAS  PubMed  Google Scholar 

  111. Garg PK, Gupta N, Gautam V, Hadke NS (2008) Gastric mucormycosis: unusual cause of gastric perforation in an immunocompetent patient. South Med J 101:449–450. https://doi.org/10.1097/smj.0b013e318167bb31

    Article  PubMed  Google Scholar 

  112. Sachdeva K (2013) Rhino-oculo-cerebral mucormycosis with multiple cranial nerve palsy in diabetic patient: review of six cases. Indian J Otolaryngol Head Neck Surg 65:375–379. https://doi.org/10.1007/s12070-013-0659-1

    Article  PubMed  PubMed Central  Google Scholar 

  113. Chander J, Kaur M, Singla N, Punia RPS, Singhal SK, Attri AK et al (2018) Mucormycosis: battle with the deadly enemy over a five-year period in India. J Fungi 4:46. https://doi.org/10.3390/jof4020046

    Article  CAS  Google Scholar 

  114. Sarvestani AS, Pishdad G, Bolandparvaz S (2013) Predisposing factors for mucormycosis in patients with diabetes mellitus; An experience of 21 years in southern Iran. Bull Emerg Trauma 1:164–170

    Google Scholar 

  115. Funada H, Matsuda T (1996) Pulmonary mucormycosis in a hematology ward. Intern Med 35:540–544. https://doi.org/10.2169/internalmedicine.35.540

    Article  CAS  PubMed  Google Scholar 

  116. Shpitzer T, Keller N, Wolf M et al (2005) Seasonal variations in rhinocerebral Mucor infection. Ann Otol Rhinol Laryngol 114:6958. https://doi.org/10.1177/000348940511400907

    Article  Google Scholar 

  117. El-Herte RI, Baban TA, Kanj SS (2012) Mucormycosis: a review on environmental fungal spores and seasonal variation of human disease. Adv Infect Dis 2:76–81. https://doi.org/10.4236/aid.2012.23012

    Article  Google Scholar 

  118. Ghosh AK, Singh R, Reddy S, Singh S, Rudramurthy SM, Kaur H, Choudhary H, Chakrabarti A (2022) Evaluation of environmental Mucorales contamination in and around the residence of COVID-19-associated mucormycosis patients. Front Cell Infect Microbiol 12:953750. https://doi.org/10.3389/fcimb.2022.953750

    Article  PubMed  PubMed Central  Google Scholar 

  119. Biswal M, Gupta P, Kanaujia R, Kaur K, Kaur H, Aruna V et al (2022) Evaluation of hospital environment for presence of mucorales during COVID-19 associated mucormycosis outbreak in India—a multi-centre study. J Hosp Infect 122:173–179. https://doi.org/10.1016/J.JHIN.2022.01.016

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  120. Iyer M, Tiwari S, Renu K, Pasha MY, Pandit S, Singh B, Raj N, Krothapalli S, Kwak HJ, Balasubramanian V, Jang SB, Kumar GD, Uttpal A, Narayanasamy A, Kinoshita M, Subramaniam MD, Nachimuthu SK, Roy A, Valsala Gopalakrishnan A, Ramakrishnan P, Cho SG, Vellingiri B (2021) Environmental survival of SARS-CoV-2—a solid waste perspective. Environ Res 197:111015. https://doi.org/10.1016/j.envres.2021.111015

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  121. Sarkodie SA, Owusu PA (2020) Impact of COVID-19 pandemic on waste management. Environ Dev Sustain 23(5):7951–7960. https://doi.org/10.1007/s10668-020-00956-y

    Article  PubMed  PubMed Central  Google Scholar 

  122. Walsh TJ, Gamaletsou MN, McGinnis MR, Hayden RT, Kontoyiannis DP (2012) Early clinical and laboratory diagnosis of invasive pulmonary, extrapulmonary, and disseminated mucormycosis (zygomycosis). Clin Infect Dis 54:S55–S60. https://doi.org/10.1093/cid/cir868

    Article  PubMed  Google Scholar 

  123. Kontoyiannis DP, Lewi RE, Lortholary O et al (2012) Future directions in mucormycosis research. Clin Infect Dis 54:79–85. https://doi.org/10.1093/cid/cir886

    Article  Google Scholar 

  124. Millon L, Herbrecht R, Grenouillet F, Morio F, AlanioLetscher-Bru A, Cassaing Sophie et al (2016) Early diagnosis and monitoring of mucormycosis by detection of circulating DNA in serum: retrospective analysis of 44 cases collected through the French Surveillance Network of Invasive Fungal Infections (RESSIF). Clin Microbiol Infect 22:810.e1-810.e8. https://doi.org/10.1016/j.cmi.2015.12.006

    Article  CAS  PubMed  Google Scholar 

  125. Smith HW, Kirchner JA (1950) Cerebral mucor-mycosis: a report of 3 cases. Arch Otolaryng (Chicago) 68:715–726. https://doi.org/10.1001/archotol.1958.00730020739010

    Article  Google Scholar 

  126. Prakash H, Ghosh AK, Rudramurthy S, Paul RA, Gupta S, Negi V, Chakrabarti A (2016) The environmental source of emerging Apophysomyces variabilis infection in India. Med Mycol 54:567–575. https://doi.org/10.1093/mmy/myw014

    Article  CAS  PubMed  Google Scholar 

  127. Wang L, Wang C, Shen Y et al (2015) Phaeohyphomycosis caused by Exophiala sinifera: an increasing disease in young females in mainland China? two case reports and review of five cases reported from mainland China. Mycoses 5:193–196. https://doi.org/10.1111/myc.12295

    Article  Google Scholar 

  128. Song G, Liang G, Liu W (2020) Fungal Co-infections associated with global COVID-19 pandemic: a clinical and diagnostic perspective from China. Mycopathologia 185:599–606. https://doi.org/10.1007/s11046-020-00462-9

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  129. Zaman K, Rudramurthy SM, Das A, Panda N, Honnavar NP, Kaur H, Chakrabarti A (2017) Molecular diagnosis of rhino-orbito-cerebral mucormycosis from fresh tissue samples. J Med Microbiol 66:1124–1129. https://doi.org/10.1099/jmm.0.000560

    Article  CAS  PubMed  Google Scholar 

  130. Aranjani JM, Manuel A, Abdul Razack HI, Mathew ST (2021) COVID-19–associated mucormycosis: evidence-based critical review of an emerging infection burden during the pandemic’s second wave in India. PLoS Negl Trop Dis 15:e0009921. https://doi.org/10.1371/journal.pntd.0009921

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  131. Cornely OA, Alastruey-Izquierdo A, Arenz D, Chen SC, Dannaoui E, Hochhegger B, Hoenigl M, Jensen HE, Lagrou K, Lewis RE, Mellinghoff SC (2019) 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 19:e405–e421. https://doi.org/10.1016/S1473-3099(19)30312-3

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  132. Shoham S, Magill SS, Merz WG, Gonzalez C, Seibel N, Buchanan WL, Knudsen TA, Sarkisova TA, Walsh TJ (2010) Primary treatment of zygomycosis with liposomal amphotericin B: analysis of 28 cases. Med Mycol 48:511–517. https://doi.org/10.3109/13693780903311944

    Article  CAS  PubMed  Google Scholar 

  133. Skiada A, Lanternier F, Groll AH, Pagano L, Zimmerli S, Herbrecht R, Lortholary O, Petrikkos GL (2013) Diagnosis and treatment of mucormycosis in patients with haematological malignancies: guidelines from the 3rd European Conference on Infections in Leukemia (ECIL3). Haematologica 98:492–504. https://doi.org/10.3324/haematol.2012.065110

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  134. Ellsworth M, Ostrosky-Zeichner L (2020) Isavuconazole: Mechanism of action, clinical efficacy and resistance. J Fungi 6:324. https://doi.org/10.3390/jof6040324

    Article  CAS  Google Scholar 

  135. Macedo A, Leonardelli F, Dudiuk C, Vitale RG, Del Valle E, Giusiano G, Gamarra S, Garcia-Effron G (2019) In vitro and in vivo evaluation of voriconazole-containing antifungal combinations against Mucorales using a Galleria mellonella model of mucormycosis. J Fungi 5:5. https://doi.org/10.3390/jof5010005

    Article  CAS  Google Scholar 

  136. John B, Chamilos G, Kontoyiannis D (2005) Hyperbaric oxygen as an adjunctive treatment for zygomycosis. Clin Microbiol Infect 11:515–517. https://doi.org/10.1111/j.1469-0691.2005.01170.x

    Article  CAS  PubMed  Google Scholar 

  137. Dokmetas HS, Canbay YS et al (2002) Diabetic ketoacidosis and rhino-orbital mucormycosis. Diabetes Res Clin Prac 57:139–142. https://doi.org/10.1016/s0168-8227(02)00021-9

    Article  Google Scholar 

  138. Cornely OA, Arikan-Akdagli S, Dannaoui E, Groll AH, Lagrou K, Chakrabarti A, Lanternier F, Pagano L, Skiada A, Akova M, Arendrup MC, Boekhout T, Chowdhary A, Cuenca-Estrella M, Freiberger T, Guinea J, Guarro J, de Hoog S, Hope W et al (2014) ESCMID and ECMM joint clinical guidelines for the diagnosis and management of mucormycosis. Clin Microbiol Infect 3:5–26. https://doi.org/10.1111/1469-0691.12371

    Article  CAS  Google Scholar 

  139. Sojinrin T, Conde J, Liu K, Curtin J, Byrne HJ, Cui D et al (2017) Plasmonic gold nanoparticles for detection of fungi and human cutaneous fungal infections. Anal Bioanal Chem 409:4647–4658. https://doi.org/10.1007/s00216-017-0414-7

    Article  CAS  PubMed  Google Scholar 

  140. Garcia A, Fan YY, Vellanki S, Huh EY, Vanegas D, Wang SH et al (2019) Nanoemulsion as an effective treatment against human-pathogenic fungi. mSphere 4(6):e00729-19. https://doi.org/10.1128/mSphere.00729-19

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  141. Rai M, Yadav A, Bridge P, Gade A (2009) Myconanotechnology: A new and emerging science. In: Rai M, Bridge PD (eds) Appl Mycol. CABI, Wallingford, pp 258–267

    Chapter  Google Scholar 

  142. Lau AF, Walchak RC, Miller HB et al (2019) Multicenter study demonstrates standardization requirements for mold identification by MALDI-TOF MS. Front Microbiol 10:2098. https://doi.org/10.3389/fmicb.2019.02098

    Article  PubMed  PubMed Central  Google Scholar 

  143. Zacharioudakis IM, Zervou FN, Mylonakis E (2018) T2 magnetic resonance assay: overview of available data and clinical implications. J Fungi 4:45. https://doi.org/10.3390/jof4020045

    Article  CAS  Google Scholar 

  144. Bhatnagar I, Mahato K, Ealla KKR et al (2018) Chitosan stabilized gold nanoparticle mediated self-assembled gliP nanobiosensor for diagnosis of invasive Aspergillosis. Int J Biol Macromol 110:449–456

    Article  CAS  PubMed  Google Scholar 

  145. Asghar W, Sher M, Khan NS et al (2019) Microfluidic chip for detection of fungal infections. ACS Omega 4:7474–7481. https://doi.org/10.1021/acsomega.9b00499

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  146. Gohil K, Samson R, Dastager S, Dharne M (2021) Probiotics in the prophylaxis of COVID-19: something is better than nothing. 3 Biotech 11(1):1. https://doi.org/10.1007/s13205-020-02554-1

    Article  PubMed  Google Scholar 

  147. Arasu MV, Al-Dhabi NA (2017) In-vitro antifungal, probiotic, and antioxidant functional properties of a novel Lactobacillus paraplantarum isolated from fermented dates in Saudi Arabia. J Sci Food Agric 97:5287–5295. https://doi.org/10.1002/jsfa.8413

    Article  CAS  PubMed  Google Scholar 

  148. Azizkhani M, Saris PEJ, Baniasadi M (2021) An in-vitro assessment of antifungal and antibacterial activity of cow, camel, ewe, and goat milk kefir and probiotic yogurt. J Food Meas Charact 15:406–415. https://doi.org/10.1007/s11694-020-00645-4

    Article  Google Scholar 

  149. Hu L, Zhou M, Young A et al (2019) In-vivo effectiveness and safety of probiotics on prophylaxis and treatment of oral candidiasis: a systematic review and meta-analysis. BMC Oral Health 19:140. https://doi.org/10.1186/s12903-019-0841-2

    Article  PubMed  Google Scholar 

  150. Thomas S, Patel D, Bittel B et al (2021) Effect of high-dose zinc and ascorbic acid supplementation vs usual care on symptom length and reduction among ambulatory patients with SARS-CoV-2 infection: the COVID A to Z randomized clinical trial. JAMA Netw Open 4(2):e210369. https://doi.org/10.1001/jamanetworkopen.2021.0369

    Article  PubMed  PubMed Central  Google Scholar 

  151. Staats CC, Kmetzsch L, Schrank A, Vainstein MH (2013) Fungal zinc metabolism and its connections to virulence. Front Cell Infect Microbiol 3:65. https://doi.org/10.3389/fcimb.2013.00065

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  152. Leonardelli F, Macedo D, Dudiuk C, Theill L, Cabeza MS, Gamarra S et al (2019) In-vitro activity of combinations of zinc chelators with amphotericin B and posaconazole against six Mucorales species. Antimicrob Agents Chemother 63(5):e00266. https://doi.org/10.1128/AAC.00266-19

    Article  CAS  PubMed  Google Scholar 

  153. Lulloff SJ, Hahn BL, Sohnle PG (2004) Fungal susceptibility to zinc deprivation. J Lab Clin Med 144:208–214. https://doi.org/10.1016/j.lab.2004.07.007

    Article  CAS  PubMed  Google Scholar 

  154. Nath S, Baidya DK (2021) Mucormycosis in COVID-19: is zinc a silent killer in India? Indian. J Crit Care Med 25:1079–1080. https://doi.org/10.5005/jp-journals-10071-23938

    Article  CAS  Google Scholar 

  155. Muthu V, Kumar M, Paul RA et al (2021) Is there an association between zinc and COVID-19–associated mucormycosis? results of an experimental and clinical study. Mycoses 64:1291–1297. https://doi.org/10.1111/myc.13365

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  156. Vuorio A, Kovanen PT (2021) Statins as adjuvant therapy for COVID-19 to calm the stormy immunothrombosis and beyond. Front Pharmacol 11:579548. https://doi.org/10.3389/fphar.2020.579548

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  157. Chatterjee S, Vardhan B, Singh DK, Maitra A, Ojha UK (2021) Should statins be considered for the management of mucormycosis in COVID-19? Diabetes Metab Syndr 15(4):102162. https://doi.org/10.1016/j.dsx.2021.05.035

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  158. Manesh A, Rupali P, Sullivan MO, Mohanraj P, Rupa V, George B, Michael JS (2019) Mucormycosis—a clinicoepidemiological review of cases over 10 years. Mycoses 62:391–398. https://doi.org/10.1111/myc.12897

    Article  PubMed  Google Scholar 

  159. Priya P, Ganesan V, Rajendran T, Geni VG (2020) Mucormycosis in a tertiary care center in South India: a 4-Year experience. Indian J Crit Care Med 24:168–171. https://doi.org/10.5005/jp-journals-10071-23387

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  160. Pakdel A, Ahmadikia K, Salehi M et al (2021) Mucormycosis in patients with COVID-19: a cross-sectional descriptive multicentre study from Iran. Mycoses 64:1238–1252. https://doi.org/10.1111/myc.13334

    Article  CAS  PubMed  Google Scholar 

  161. Lortholary O, Petrikkos G, Akova M, Arendrup MC, Arikan-Akdagli S, Bassetti M, Bille J, Calandra T, Castagnola E, Cornely OA et al (2012) ESCMID guideline for the diagnosis and management of Candida diseases 2012: patients with HIV infection or AIDS. Clin Microbiol Infect 18(7):68–77. https://doi.org/10.1111/1469-0691.12042

    Article  CAS  PubMed  Google Scholar 

  162. Kubin CJ, McConville TH, Dietz D et al (2021) Characterization of bacterial and fungal infections in hospitalized patients with COVID-19 and factors associated with healthcare-associated infections. Open Forum Infect Dis 8:ofab201. https://doi.org/10.1093/ofid/ofab201

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  163. John TM, Jacob CN, Kontoyiannis DP (2021) When uncontrolled diabetes mellitus and severe COVID-19 converge: the perfect storm for mucormycosis. Journal of Fungi 7(4):298. https://doi.org/10.3390/jof7040298

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  164. Sharma B, Nonzom S (2021) Talaromyces stipitatus, a novel agent causing superficial mycosis in a diabetic patient from North India. Microbes Infect 24(2):104887. https://doi.org/10.1016/j.micinf.2021.104887

    Article  CAS  PubMed  Google Scholar 

  165. Hoang K, Abdo T, Reinersman JM, Lu R, Higuita NIA (2020) A case of invasive pulmonary mucormycosis resulting from short courses of corticosteroids in a well-controlled diabetic patient. Med Mycol Case Rep 29:22–24. https://doi.org/10.1016/j.mmcr.2020.05.008

    Article  PubMed  PubMed Central  Google Scholar 

  166. The Hindustan Times, 2021. India reported over 45,000 black fungus cases so far, says Mandaviya in RS. https://www.hindustantimes.com/india-news/india-reported-over-45-000-black-fungus-cases-so-far-says-mandaviya-in-rs-101626781531292.html.

  167. COVID: Mumbai records first mucormycosis cases in 2022 amid omicron surge. https://www.republicworld.com/india-news/city-news/mumbai-records-first mucormycosis-case-as-india-continues-to-grapple-with-covid-articleshow.html

  168. Wei LW, Zhu PQ, Chen XQ et al (2022) Mucormycosis in mainland China: a systematic review of case reports. Mycopathologia 187:1–14. https://doi.org/10.1007/s11046-021-00607-4

    Article  CAS  PubMed  Google Scholar 

  169. Tak K, Rastogi V, Verma P, Gehlot V, Gupta M, Rawat D, Prajapati S, Parihar G (2022) A clinico-mycological study of suspected mucormycosis in post-COVID patients attending a tertiary care hospital. Med Mycol 60:myac072P299. https://doi.org/10.1093/mmy/myac072.P299

    Article  PubMed Central  Google Scholar 

  170. Tyagi A, Gupta M, Mittal A, Sengupta A (2022) A rare case of post-COVID mucormycosis of the kidney. Curr Med Res Pract 12:35–37. https://doi.org/10.4103/cmrp.cmrp_85_21

    Article  Google Scholar 

  171. Meshram HS, Kute VB, Chauhan S, Desai S (2021) Mucormycosis in post-COVID-19 renal transplant patients: a lethal complication in follow-up. Transpl Infect Dis 23(4):e13663. https://doi.org/10.1111/tid.13663

    Article  CAS  PubMed  Google Scholar 

  172. Rao VU, Arakeri G, Madikeri G, Shah A, Oeppen RS, Brennan PA (2021) COVID-19 associated mucormycosis (CAM) in India: a formidable challenge. Br J Oral Maxillofac Surg 59:1095–1098. https://doi.org/10.1016/j.bjoms.2021.06.013

    Article  PubMed  PubMed Central  Google Scholar 

  173. Mishra N, Mutya VSS, Thomas A, Rai G, Reddy B, Mohanan AA, Ray S, Thiruvengadem AV, Siddini V, Hegde R (2021) A case series of invasive mucormycosis in patients with COVID-19 infection. Int J Otorhinolaryngol Head Neck Surg 7:867–870. https://doi.org/10.18203/issn.2454-5929.ijohns20211583

    Article  Google Scholar 

  174. Satish D, Joy D, Ross A, Balasubramanya, (2021) Mucormycosis coinfection associated with global COVID-19: a case series from India. Int. J. Otorhinolaryngol Head Neck Surg 7:815–820. https://doi.org/10.18203/issn.2454-5929.ijohns20211574

    Article  Google Scholar 

  175. Garg D, Muthu V, Sehgal IS, Ramachandran R, Kaur H, Bhalla A, Puri GD, Chakrabarti A, Agarwal R (2021) Coronavirus disease (Covid-19) associated mucormycosis (CAM): case report and systematic review of literature. Mycopathologia 186:289–298. https://doi.org/10.1007/s11046-021-00528-2

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  176. Krishna V, Morjaria J, Jalandari R, Omar F, Kaul S (2021) Autoptic identification of disseminated mucormycosis in a young male presenting with cerebrovascular event, multi-organ dysfunction and COVID-19 infection. IDCases 25:e01172. https://doi.org/10.1016/j.idcr.2021.e01172

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  177. Saldanha M, Reddy R, Vincent MJ (2021) Paranasal mucormycosis in COVID-19 patient. Indian J Otolaryngol Head Neck Surg. https://doi.org/10.1007/s12070-021-02574-0

    Article  PubMed  PubMed Central  Google Scholar 

  178. Revannavar SM, Supriya PS, Samaga L, Vineeth V (2021) COVID-19 triggering mucormycosis in a susceptible patient: a new phenomenon in the developing world? BMJ Case Rep 14(4):e241663. https://doi.org/10.1136/bcr-2021-241663

    Article  PubMed  PubMed Central  Google Scholar 

  179. Maini A, Tomar G, Khanna D, Kini Y, Mehta H, Bhagyasree V (2021) Sino-orbital mucormycosis in a COVID-19 patient: a case report. Int J Surg Case Rep 82:105957. https://doi.org/10.1016/j.ijscr.2021.105957

    Article  PubMed  PubMed Central  Google Scholar 

  180. Mehta S, Pandey A (2020) Rhino-orbital mucormycosis associated with COVID-19. Cureus 12(9):e10726. https://doi.org/10.7759/cureus.10726

    Article  PubMed  PubMed Central  Google Scholar 

  181. Sharma S, Grover M, Bhargava S, Samdani S, Kataria T (2021) Post coronavirus disease mucormycosis: a deadly addition to the pandemic spectrum. J Laryngol Otol 135(5):442–447. https://doi.org/10.1017/S0022215121000992

    Article  CAS  PubMed  Google Scholar 

  182. Sarkar S, Gokhale T, Choudhury SS, Deb AK (2021) COVID-19 and orbital mucormycosis. Indian J Ophthalmol 69:1002. https://doi.org/10.4103/ijo.IJO_3763_20

    Article  PubMed  PubMed Central  Google Scholar 

  183. Nehara HR, Puri I, Singhal V, Sunil IH, Bishnoi BR, Sirohi P (2021) Rhinocerebral mucormycosis in COVID-19 patient with diabetes a deadly trio: Case series from the north-western part of India. Indian J Med Microbiol 39:380–383. https://doi.org/10.1016/j.ijmmb.2021.05.009

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  184. Kandasamy S, Muthuraju S, Vasugi A, Chandrasekar M, Murugan R, Inbasekaran P, Prabhu R (2022) Clinicopathological study of mucormycosis in COVID-19 patients: experience from a tertiary care center in South India. Cureus 14(3):e23016. https://doi.org/10.7759/cureus.23016

    Article  PubMed  PubMed Central  Google Scholar 

  185. Chakravarty J, Gupta MK, Tilak R, Kumar R, Maurya RP, Kumar N, Aggarwal SK, Siva S, Sharma NK, Dhiman NK, Chaubey M, Singh V, Verma A, Banerjee T, Agrawal NK, Prasad RS (2022) COVID-19-associated Mucormycosis: a clinico-epidemiological study. J Diabetes Complications 36(9):108284. https://doi.org/10.1016/j.jdiacomp.2022.108284

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  186. Viswamithra P, Muralikrishna V, Sultana SS, Sindusha K, Rani BS (2023) Rhino-orbito-cerebral mucormycosis in a pregnant woman: a case report. Indian J Ophthalmol Case Rep 3:167–169. https://doi.org/10.4103/ijo.IJO_1734_22

    Article  Google Scholar 

  187. Zurl C, Hoenigl M, Schulz E, Hatzl S, Gorkiewicz G, Eller RP, Prattes J (2021) Autopsy proven pulmonary mucormycosis due to Rhizopus microsporus in a critically ill COVID-19 patient with underlying hematological malignancy. Journal of Fungi 7(2):88. https://doi.org/10.3390/jof7020088

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  188. Monte Junior ESD, Santos M, Ribeiro IB, Luz GO, Baba GO, Hirsch BS et al (2020) Rare and fatal gastrointestinal mucormycosis (Zygomycosis) in a COVID-19 patient: a case report. Clin Endosc 53:746–749. https://doi.org/10.5946/ce.2020.180

    Article  PubMed  PubMed Central  Google Scholar 

  189. Bonates P, Joao GAP, Cruz KS, Ferreira MS, Baia-da-Silva DC, Farias MEL et al (2021) Fatal rhino-orbito-cerebral mucormycosis infection associated with diabetic ketoacidosis post-COVID-19. Rev Bras Med Trop 54:1–6. https://doi.org/10.1590/0037-8682-0358-2021

    Article  Google Scholar 

  190. Ashour MM, Abdelaziz TT, Ashour DM, Askour A, Saleh MI, Mahmoud MS (2021) Imaging spectrum of acute invasive fungal rhino-orbital-cerebral sinusitis in COVID-19 patients: a case series and a review of literature. J Neuroradiol 48:319–324. https://doi.org/10.1016/j.neurad.2021.05.007

    Article  PubMed  PubMed Central  Google Scholar 

  191. El-Kholy NA, El-Fatta AMA, Khafagy YW (2021) Invasive fungal sinusitis in post COVID-19 patients: a new clinical entity. Laryngoscop 131:2652–2658. https://doi.org/10.1002/lary.29632

    Article  CAS  Google Scholar 

  192. Riad A, Shabaan AA, Issa J, Ibrahim S, Amer H, Mansy Y, Kassem I, Kassem AB, Howaldt HP, Klugar M, Attia S (2021) COVID-19-Associated mucormycosis (CAM): case-series and global analysis of mortality risk factors. J Fungi (Basel, Switzerland) 7(10):837. https://doi.org/10.3390/jof7100837

    Article  CAS  Google Scholar 

  193. Youssif SF, Abdelrady MM, Thabet AA, Abdelhamed MA, Gad MOA, Abu-Elfatth AM, Saied GM, Goda I, Algammal AM, Batiha GE, Abd El-Rady NM, Hetta HF, Kasem SM (2022) COVID-19 associated mucormycosis in Assiut University Hospitals: a multidisciplinary dilemma. Sci Rep 12(1):10494. https://doi.org/10.1038/s41598-022-13443-3

    Article  CAS  Google Scholar 

  194. Bellanger P, Navellou JC, Lepiller Q, Brion A, Brunel AS, Millon L, Berceanu A (2021) Mixed mold infection with Aspergillus fumigatus and Rhizopus microsporus in a severe acute respiratory syndrome Coronavirus 2 (SARS-CoV-2) patient. Infect Dis Now 51:633–635. https://doi.org/10.1016/j.idnow.2021.01.010

    Article  PubMed  PubMed Central  Google Scholar 

  195. Danion F, Letscher-Bru V, Guitard J, Sitbon K, Delliere S, Angoulvant A, Desoubeaux G, Botterel F, Bellanger AP et al (2022) COVID-Mucor study group, coronavirus disease 2019-associated mucormycosis in France: a rare but deadly complication. Open Forum Infect Dis 9:566. https://doi.org/10.1093/ofid/ofab566

    Article  CAS  Google Scholar 

  196. Evert K, Dienemann T, Brochhausen C et al (2021) Autopsy findings after long-term treatment of COVID-19 patients with microbiological correlation. Virchows Arch 479:97–108. https://doi.org/10.1007/s00428-020-03014-0

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  197. Karimi-Galougahi M, Arastou S, Haseli S (2021) Fulminant mucormycosis complicating coronavirus disease 2019 (COVID-19). Int Forum Allergy Rhinol 11:1029–1030. https://doi.org/10.1002/alr.22785

    Article  PubMed  PubMed Central  Google Scholar 

  198. Veisi A, Bagheri A, Eshaghi M, Rikhtehgar MH, Rezaei Kanavi M, Farjad R (2022) Rhino-orbital mucormycosis during steroid therapy in COVID-19 patients: a case report. Eur J Ophthalmol 32(4):NP11–NP16. https://doi.org/10.1177/11206721211009450

    Article  PubMed  PubMed Central  Google Scholar 

  199. Mohammadi F, Badri M, Safari S, Hemmat N (2021) A case report of rhino-facial mucormycosis in a non-diabetic patient with COVID-19: a systematic review of literature and current update. BMC Infect Dis 2:1–7. https://doi.org/10.1186/s12879-021-06625-3

    Article  CAS  Google Scholar 

  200. Balushi AA, Ajmi AA, Sinani QA, Menon V, Berieki ZA, Shezawi AA, Azri SA, Rashdi AA, Jardani AA, Baluki TA, Ghaithi SA, Reesi AA, Al-Zaabi AT, Al Balushi MA, Maqbali TA (2022) COVID-19-Associated Mucormycosis: an opportunistic fungal infection. a case series and review. Int J Infect Dis 121:203–210. https://doi.org/10.1016/j.ijid.2022.05.005

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  201. Pasero D, Sanna S, Liperi C, Piredda D, Branca GP, Casadio L, Simeo R, Buselli A, Rizzo D, Bussu F, Rubino SA (2021) A challenging complication following SARS-CoV-2 infection: a case of pulmonary mucormycosis. Infection 49:1055–1060. https://doi.org/10.1007/s15010-020-01561-x

    Article  CAS  PubMed  Google Scholar 

  202. Waizel-Haiat S, Guerrero-Paz JA, Sanchez-Hurtado L, Calleja-Alarcon S, Romero-Gutierrez L (2021) A case of fatal rhino-orbital mucormycosis associated with new onset diabetic ketoacidosis and COVID-19. Cureus 13(2):e13163. https://doi.org/10.7759/cureus.13163

    Article  PubMed  PubMed Central  Google Scholar 

  203. Buil Jochem B, van Zanten Arthur R H, Bentvelsen Robbert G, Rijpstra Tom A, Goorhuis Bram, van der Voort Sanne, Wammes Linda J, Janson Jeroen A, Melchers Max, Heusinkveld Moniek, Melchers Willem JG, Kuijper Ed J, Verweij Paul E (2021) Case series of four secondary mucormycosis infections in COVID-19 patients the Netherlands December 2020 to May 2021. Euro Surveill. 26(23): 2100510. https://doi.org/10.2807/1560-7917.ES.2021.26.23.2100510

  204. Sargin F, Akbulut M, Karaduman S, Sungurtekin H (2021) Severe rhinocerebralmucormycosis case developed after COVID 19. J Bacteriol Parasitol 12:386

    Google Scholar 

  205. Hanley B, Naresh KN, Roufosse C (2020) Histopathological findings and viral tropism in UK patients with severe fatal COVID-19: a post-mortem study. Lancet Microbe 1:e245–e253. https://doi.org/10.1016/S2666-5247(20)30115-4

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  206. Werthman-Ehrenreich A (2021) Mucormycosis with orbital compartment syndrome in a patient with COVID-19. Am J Emerg Med 42:264.e5-264.e8. https://doi.org/10.1016/j.ajem.2020.09.032

    Article  PubMed  Google Scholar 

  207. Placik DA, Taylor WL, Wnuk NM (2020) Bronchopleural fistula development in the setting of novel therapies for acute respiratory distress syndrome in SARS-CoV-2 pneumonia. Radiol Case Rep 15:2378–2381. https://doi.org/10.1016/j.radcr.2020.09.026

    Article  PubMed  PubMed Central  Google Scholar 

  208. Alekseyev K, Didenko L, Chaudhr B (2021) Rhinocerebral mucormycosis and COVID-19 pneumonia. J Med Cases 12:85–89. https://doi.org/10.14740/jmc3637

    Article  PubMed  PubMed Central  Google Scholar 

  209. Kanwar A, Jordan A, Olewiler S, Wehberg K, Cortes M, Jackson BR (2021) A fatal case of Rhizopus azygosporus pneumonia following COVID-19. J Fungi 7:174. https://doi.org/10.3390/jof7030174

    Article  CAS  Google Scholar 

  210. Johnson AK, Ghazarian Z, Cendrowski KD, Persichino JG (2021) Pulmonary aspergillosis and mucormycosis in a patient with COVID-19. Med Mycol Case Rep 32:64–67. https://doi.org/10.1016/j.mmcr.2021.03.006

    Article  PubMed  PubMed Central  Google Scholar 

  211. Dallalzadeh LO, Ozzello DJ, Liu CY, Kikkawa DO, Korn BS (2021) Secondary infection with rhino-orbital cerebral mucormycosis associated with COVID-19. Orbit. https://doi.org/10.1080/01676830.2021.1903044

    Article  PubMed  Google Scholar 

Download references

Funding

This research did not receive any specific grant from funding agencies in the public, commercial or nonprofit sectors.

Author information

Authors and Affiliations

  1. Department of Botany, University of Jammu, Jammu, Jammu and Kashmir, 180006, India

    Bharti Sharma & Skarma Nonzom

Authors
  1. Bharti Sharma
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Skarma Nonzom
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

Both the authors have contributed to the manuscript. BS: Conceptualization, Resources and Writing-original draft. SN: Supervision, Review and Editing.

Corresponding author

Correspondence to Skarma Nonzom.

Ethics declarations

Conflict of interest

There are no conflicts of interest.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Sharma, B., Nonzom, S. Mucormycosis and Its Upsurge During COVID-19 Epidemic: An Updated Review. Curr Microbiol 80, 322 (2023). https://doi.org/10.1007/s00284-023-03430-w

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s00284-023-03430-w

Search

Navigation