Multicenter Epidemiologic Study of Coronavirus Disease-Associated Mucormycosis, India

Abstract

During September-December 2020, we conducted a multicenter retrospective study across India to evaluate epidemiology and outcomes among cases of coronavirus disease (COVID-19)-associated mucormycosis (CAM). Among 287 mucormycosis patients, 187 (65.2%) had CAM; CAM prevalence was 0.27% among hospitalized COVID-19 patients. We noted a 2.1-fold rise in mucormycosis during the study period compared with September-December 2019. Uncontrolled diabetes mellitus was the most common underlying disease among CAM and non-CAM patients. COVID-19 was the only underlying disease in 32.6% of CAM patients. COVID-19-related hypoxemia and improper glucocorticoid use independently were associated with CAM. The mucormycosis case-fatality rate at 12 weeks was 45.7% but was similar for CAM and non-CAM patients. Age, rhino-orbital-cerebral involvement, and intensive care unit admission were associated with increased mortality rates; sequential antifungal drug treatment improved mucormycosis survival. The COVID-19 pandemic has led to increases in mucormycosis in India, partly from inappropriate glucocorticoid use.

Keywords: COVID-19; India; SARS; SARS-CoV-2; amphotericin; coronavirus; coronavirus disease; diabetes; epidemiology; fungi; isavuconazole; mucormycosis; posaconazole; respiratory infections; severe acute respiratory syndrome coronavirus 2; viruses; zoonoses.

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 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 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 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 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.