Background: Coronavirus disease 2019 (COVID-19) has predisposed to secondary fungal infections, particularly when it is associated with varied comorbidities and immunocompromised situations.
Materials andmethods: We performed a retrospective clinico-epidemiological evaluation on 45 patients with a history of COVID-19 who presented with clinical features of fungal infections and their association with preexisting comorbid risk factors. The clinico-demographic information of the patients was obtained using a pro forma. Samples from representative clinical sites were collected, like respiratory secretions, pus, or tissue samples from nasal cavities and paranasal sinuses. These samples were processed as per the standard mycological procedures and the fungal isolates, so obtained, were identified according to their culture and microscopic characteristics.
Results: The median time interval for the appearance of clinical features of fungal infections from the time of COVID-19 diagnosis was 17 days. Diabetes mellitus (DM) (84.44%) was found to be the leading comorbidity. History of administration of glucocorticoids was noted in 62.22% of the patients. The most frequent presentation was rhinosinusitis in 86.67% of the individuals. Different kinds of molds were isolated in 73.33% of the specimens, with Mucorales (78.89%) being the dominant one. The 32 admitted patients were managed by antifungal therapy and/or surgery. A total of nine patients did not respond to the treatment and succumbed to the disease.
Conclusion: Though the true prevalence of these mold infections is not known, but timely diagnosis and management are extremely important in view of their high mortality.
WHO Coronavirus (COVID-19) Dashboard. WHO Health Emergency Dashboard. World Health organization [Online]. 2022 May 15 [cited 2022 May 15]; Available from: https://covid19.who.int/
Li X, Xu S, Yu M, et al. Risk factors for severity and mortality in adult COVID-19 inpatients in Wuhan. J Allergy Clin Immunol 2020;146(1):110–118. DOI: 10.1016/j.jaci.2020.04.006
Zheng Z, Peng F, Xu B, et al. Risk factors of critical & mortal COVID-19 cases: a systematic literature review and meta-analysis. J Infect 2020;81(2):e16–e25. DOI: 10.1016/j.jinf.2020.04.021
Chen N, Zhou M, Dong X, et al. Epidemiological and clinical characteristics of 99 cases of 2019 novel coronavirus pneumonia in Wuhan, China: a descriptive study. Lancet 2020;395(10223):507–513. DOI: 10.1016/S0140-6736(20)30211-7
Hoenigl M. Invasive fungal disease complicating coronavirus disease 2019: when it rains, it spores. Clin Infect Dis 2021;73(7):e1645–e1648. DOI: 10.1093/cid/ciaa1342
Pasero D, Sanna S, Liperi C, et al. A challenging complication following SARS-CoV-2 infection: a case of pulmonary mucormycosis. Infection 2021;49:1055–1060. DOI: 10.1007/s15010-020-01561-x
Skiada A, Pavleas I, Drogari-Apiranthitou M. Epidemiology and diagnosis of mucormycosis: an update. J Fungi (Basel) 2020;6(4):265. DOI: 10.3390/jof6040265
Prakash H, Chakrabarti A. Global epidemiology of mucormycosis. J Fungi 2019;5:26. DOI: 10.3390/jof5010026
Clinical management protocol: COVID-19. Government of India, Ministry of Health and Family Welfare, Directorate General of. Health Services (EMR Division) [Online]. 2020 June 27 [cited 2020 Jul 10]; Version 3. Available from: https://www.mohfw.gov.in/pdf/ClinicalManagementProtocolforCOVID19dated27062020.pdf
Moorthy A, Gaikwad R, Krishna S, 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):418–425. DOI: 10.1007/s12663-021-01532-1
Arastehfar A, Carvalho A, van de Veerdonk FL, et al. COVID-19 associated pulmonary aspergillosis (CAPA)—from immunology to treatment. J Fungi (Basel) 2020;6(2):91. DOI: 10.3390/jof6020091
Pal R, Singh B, Bhadada SK, et al. COVID-19-associated mucormycosis: an updated systematic review of literature. Mycoses 2021;64(12): 1452–1459. DOI: 10.1111/myc.13338
Nasir N, Farooqi J, Mahmood SF, et al. COVID-19-associated pulmonary aspergillosis (CAPA) in patients admitted with severe COVID-19 pneumonia: an observational study from Pakistan. Mycoses 2020;63(8):766–770. DOI: 10.1111/myc.13135
Garg D, Muthu V, Sehgal IS, et al. Coronavirus disease (Covid-19) associated mucormycosis (CAM): case report and systematic review of literature. Mycopathologia 2021;186(2):289–298. DOI: 10.1007/s11046-021-00528-2
Mishra N, Mutya VSS, Thomas A, et al. A case series of invasive mucormycosis in patients with COVID-19 infection. Int J Otorhinolaryngol Head Neck Surg 2021;7(5):867–870. DOI: 10.18203/issn.2454-5929.ijohns20211583
Hope WW, Walsh TJ, et al. The invasive and saprophytic syndromes due to Aspergillus spp. Med Mycol 2005;43(Suppl 1):S207–S238. DOI: 10.1080/13693780400025179
Ghazanfari M, Arastehfar A, Davoodi L, et al. Pervasive but neglected: a perspective on COVID-19-associated pulmonary mold infections among mechanically ventilated COVID-19 patients. Front Med (Lausanne) 2021;8:6469675. DOI: 10.3389/fmed.2021.649675
Sarkar S, Gokhale T, Choudhury SS, et al. COVID-19 and orbital mucormycosis. Indian J Ophthalmol 2021;69(4):1002–1004. DOI: 10.4103/ijo.IJO_3763_20
Sharma S, Grover M, Bhargava S, et al. Post coronavirus disease mucormycosis: a deadly addition to the pandemic spectrum. J Laryngol Otol 2021;135(5):442–447. DOI: 10.1017/S0022215121000992
Patel A, Agarwal R, Rudramurthy SM, et al. Multicenter epidemiologic study of coronavirus disease-associated mucormycosis, India. Emerg Infect Dis 2021;27(9):2349–2359. DOI: 10.3201/eid2709.210934
Waldorf AR. Pulmonary defense mechanisms against opportunistic fungal pathogens. Immunol Ser 1989;47:243–271. PMID: 2490078.
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):1123–1129. DOI: 10.1128/iai.38.3.1123-1129
White PL, Dhillon R, Cordey A, 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–e1644. DOI: 10.1093/cid/ciaa1298
Rutsaert L, Steinfort N, Van Hunsel T, et al. COVID-19-associated invasive pulmonary aspergillosis. Ann Intensive Care 2020;10(1):71. DOI: 10.1186/s13613-020-00686-4
Silva LN, de Mello TP, de Souza Ramos L, et al. Fungal infections in COVID-19-positive patients: a lack of optimal treatment options. Curr Top Med Chem 2020;20(22):1951–1957. DOI: 10.2174/156802662022200917110102
Patel A, Kaur H, Xess I, et al. A multicentre observational study on the epidemiology, risk factors, management and outcomes of mucormycosis in India. Clin Microbiol Infect 2020;26(7):944.e9–944.e15. DOI: 10.1016/j.cmi.2019.11.021
Prakash H, Chakrabarti A. Epidemiology of mucormycosis in India. Microorganisms 2021;9(3):523. DOI: 10.3390/microorganisms9030523
Bouza E, Guinea J, Pelaez T, et al. Workload due to Aspergillus fumigatus and significance of the organism in the microbiology laboratory of a general hospital. J Clin Microbiol 2005;43(5):2075–2079. DOI: 10.1128/JCM.43.5.2075-2079.2005
Revannavar SM, PSS, Samaga L, et al. COVID-19 triggering mucormycosis in a susceptible patient: a new phenomenon in the developing world? BMJ Case Rep 2021;14(4):e241663. DOI: 10.1136/bcr-2021-241663
Ahmadikia K, Hashemi SJ, Khodavaisy S, 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. DOI: 10.1111/myc.13256
Mucormycosis epidemic: another dark side to the COVID-19 pandemic [Online]. 2021 Aug 18 [cited 2021 Sept 16]; Available from: https://rstmh.org/news-blog/blogs/mucormycosis-epidemic-another-dark-side-to-the-covid-19-pandemic
Chakrabarti A, Chatterjee SS, Das A, et al. Invasive aspergillosis in developing countries. Med Mycol 2011;49(1):S35–S47. DOI: 10.3109/13693786.2010.505206