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Cited by 485Antifungal resistance and susceptibilityCOVID-19 Clinical Research StudiesInfectious Diseases and Mycology

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Multicenter Epidemiologic Study of Coronavirus Disease-Associated Mucormycosis, India

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Patel, Atul, Agarwal, Ritesh, Rudramurthy, Shivaprakash M., Shevkani, Manoj, Xess, Immaculata, Sharma, Ratna, Savio, Jayanthi, Sethuraman, Nandini, Madan, Surabhi, Shastri, Prakash, Thangaraju, Deepak, Marak, Rungmei, Tadepalli, Karuna, Savaj, Pratik, Sunavala, Ayesha, Gupta, Neha, Singhal, Tanu, Muthu, Valliappan, Chakrabarti, Arunaloke, MucoCovi Network3·2021·Emerging Infectious Diseases
DOI 10.3201/eid2709.210934PMC PMC8386807
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Abstract

econdary infections are known to complicate the clinical course of coronavirus disease .Bacterial infections are the most common secondary infections, but increasing reports of systemic fungal infections are causing concern.In the early part of the COVID-19 pandemic, <1% of secondary infections reported in COVID-19 patients were fungal (1,2).Preexisting conditions, indiscriminate use of antimicrobial and glucocorticoid drugs, and lapses in infection control practices are putative factors contributing to the emergence of systemic fungal infections in severe COVID-19 cases (3).After incidence of candidemia and invasive aspergillosis in COVID-19 patients increased (4,5), awareness of possible fungal co-infections increased among clinicians and microbiologists.One study reported invasive fungal infections in ≈6% of hospitalized COVID-19 patients (6).Occasional reports of COVID-19-associated mucormycosis (CAM) from various centers (7,8) and a series of 18 cases from a city in South India increased our concerns about CAM (9).India has a high burden of mucormycosis among patients with uncontrolled diabetes mellitus, and many severe COVID-19 patients have diabetes (8,10).India also is one of the countries worst affected by the COVID-19 pandemic.Thus, we would expect India to have many CAM cases.We conducted a nationwide multicenter study to evaluate the epidemiology and outcomes of CAM and compare the results with cases of mucormycosis unrelated to COVID-19 (non-CAM).

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Figures

Figure 1 Locations of 16 healthcare centers participating in MucoCovi Network study on coronavirus disease–associated mucormycosis, India. AIIMS, All India Institute of Medical Sciences; CIMS, Care Institute of Medical Sciences; PD Hinduja, Parmanand Deepchand Hinduja; PGIMER, Post Graduate Institute of Medical Education & Research; SGPI, Sanjay Gandhi Postgraduate Institute
Figure 1 Locations of 16 healthcare centers participating in MucoCovi Network study on coronavirus disease–associated mucormycosis, India. AIIMS, All India Institute of Medical Sciences; CIMS, Care Institute of Medical Sciences; PD Hinduja, Parmanand Deepchand Hinduja; PGIMER, Post Graduate Institute of Medical Education & Research; SGPI, Sanjay Gandhi Postgraduate InstituteCC BY · PubMed Central
Figure 2 Cumulative number of mucormycosis cases during September–December 2019 and September–December 2020 in 10 health centers, India. White bar section indicates coronavirus disease–associated mucormycosis (CAM); black bar sections indicate non-CAM cases. During 2019, 112 cases of mucormycosis were detected, but a total of 231 cases, 92 non-CAM and 139 CAM, were detected in 2020.
Figure 2 Cumulative number of mucormycosis cases during September–December 2019 and September–December 2020 in 10 health centers, India. White bar section indicates coronavirus disease–associated mucormycosis (CAM); black bar sections indicate non-CAM cases. During 2019, 112 cases of mucormycosis were detected, but a total of 231 cases, 92 non-CAM and 139 CAM, were detected in 2020.CC BY · PubMed Central
Figure 3 Radiographic images and surgical specimens demonstrating rhino-orbital-cerebral coronavirus disease–associated mucormycosis in patients from India, 2020. A) Three-dimensional reconstruction of computed tomography scan of 54-year-old male patient. Black arrows indicate patchy osteonecrosis involving the upper jaw, right orbital wall, and paranasal sinuses. B) Surgical specimen from the maxilla of 54-year-old male patient showing black necrotic paranasal sinus with palatal involvement indicated by yellow arrows. C, D) Magnetic resonance imaging (MRI) of coronal section of paranasal sinus and brain of 51-year-old female patient. Red arrow in panel C indicates enhancing cavernous sinus lesion; D) red arrow in panel D indicates right ethmoid and maxillary sinusitis. Scale bar indicates 7 cm.
Figure 3 Radiographic images and surgical specimens demonstrating rhino-orbital-cerebral coronavirus disease–associated mucormycosis in patients from India, 2020. A) Three-dimensional reconstruction of computed tomography scan of 54-year-old male patient. Black arrows indicate patchy osteonecrosis involving the upper jaw, right orbital wall, and paranasal sinuses. B) Surgical specimen from the maxilla of 54-year-old male patient showing black necrotic paranasal sinus with palatal involvement indicated by yellow arrows. C, D) Magnetic resonance imaging (MRI) of coronal section of paranasal sinus and brain of 51-year-old female patient. Red arrow in panel C indicates enhancing cavernous sinus lesion; D) red arrow in panel D indicates right ethmoid and maxillary sinusitis. Scale bar indicates 7 cm.CC BY · PubMed Central
Figure 4 Noncontrast computed tomography scan of the thorax of a patient with coronavirus disease–associated mucormycosis, India, 2020. A) Pulmonary mucormycosis demonstrated as a large area of consolidations with patchy air trapping (black arrow), patchy ground-glass opacities, and septal thickening; B) large thick-walled cavity (red arrow) with surrounding ground-glass opacities.
Figure 4 Noncontrast computed tomography scan of the thorax of a patient with coronavirus disease–associated mucormycosis, India, 2020. A) Pulmonary mucormycosis demonstrated as a large area of consolidations with patchy air trapping (black arrow), patchy ground-glass opacities, and septal thickening; B) large thick-walled cavity (red arrow) with surrounding ground-glass opacities.CC BY · PubMed Central
Figure 5 Waterfall plot showing the number of days between the diagnosis of coronavirus disease (COVID-19) and COVID-19–associated mucormycosis (CAM). Each vertical line represents a case-patient. Red indicates late CAM (mucormycosis developing >8 days after COVID-19 diagnosis); black indicates early CAM (mucormycosis developing <7 days of COVID-19 diagnosis). Among early CAM cases, mucormycosis was diagnosed before (n = 8), concurrently with (n = 8), or after (n = 13) COVID-19 diagnosis. Dotted line represents the median duration (18 days) after COVID-19 diagnosis for the diagnosis of CAM.
Figure 5 Waterfall plot showing the number of days between the diagnosis of coronavirus disease (COVID-19) and COVID-19–associated mucormycosis (CAM). Each vertical line represents a case-patient. Red indicates late CAM (mucormycosis developing >8 days after COVID-19 diagnosis); black indicates early CAM (mucormycosis developing <7 days of COVID-19 diagnosis). Among early CAM cases, mucormycosis was diagnosed before (n = 8), concurrently with (n = 8), or after (n = 13) COVID-19 diagnosis. Dotted line represents the median duration (18 days) after COVID-19 diagnosis for the diagnosis of CAM.CC BY · PubMed Central

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Metadata

Authors
Patel, A., Agarwal, R., Rudramurthy, S. M., Shevkani, M., Xess, I., Sharma, R., Savio, J., Sethuraman, N., Madan, S., Shastri, P., Thangaraju, D., Marak, R., Tadepalli, K., Savaj, P., Sunavala, A., Gupta, N., Singhal, T., Muthu, V., Chakrabarti, A., & Network3, M.
Affiliations
  • Sterling Hospitals (IN)
  • Medanta The Medicity (IN)
Corresponding author
Chakrabarti, Arunaloke
ORCID
Venue
Emerging Infectious Diseases
Publisher
Centers for Disease Control and Prevention (CDC)
Published
2021-09
Volume
27
Issue
9
Pages
2349-2359
ISSN
  • 1080-6040 (ISSN-L)
  • 1080-6059
DOI
10.3201/eid2709.210934
PMC
PMC8386807
OpenAlex
W3164172839
Cited by
479
References
30
Citations by year
2026: 26 · 2025: 35 · 2024: 60 · 2023: 114 · 2022: 163 · 2021: 81
FWCI
33.10
Type
journal article
Language
en
Open access
Licence
cc-by
Locations
  • Emerging infectious diseases (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Topics
  • Health Sciences › Medicine › Infectious Diseases › Antifungal resistance and susceptibility
  • Health Sciences › Medicine › Infectious Diseases › COVID-19 Clinical Research Studies
  • Health Sciences › Medicine › Infectious Diseases › Infectious Diseases and Mycology
Keywords
COVID-19-associated mucormycosis, mucormycosis, SARS-CoV-2, secondary fungal infection, invasive fungal infections, clinical outcomes, diabetes mellitus, glucocorticoid use
MeSH terms
COVID-19, SARS-CoV-2, Antifungal Agents, Humans, India, Mucormycosis, Retrospective Studies, Pandemics

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