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Volume 29, Number 1—January 2023
CME ACTIVITY - Synopsis

Multicenter Case–Control Study of COVID-19–Associated Mucormycosis Outbreak, India

Valliappan Muthu, Ritesh Agarwal1Comments to Author , Shivaprakash Mandya Rudramurthy, Deepak Thangaraju, Manoj Radhakishan Shevkani, Atul K. Patel, Prakash Srinivas Shastri, Ashwini Tayade, Sudhir Bhandari, Vishwanath Gella, Jayanthi Savio, Surabhi Madan, Vinay Kumar Hallur, Venkata Nagarjuna Maturu, Arjun Srinivasan, Nandini Sethuraman, Raminder Pal Singh Sibia, Sanjay Pujari, Ravindra Mehta, Tanu Singhal, Puneet Saxena, Varsha Gupta, Vasant Nagvekar, Parikshit Prayag, Dharmesh Patel, Immaculata Xess, Pratik Savaj, Naresh Panda, Gayathri Devi Rajagopal, Riya Sandeep Parwani, Kamlesh Patel, Anuradha Deshmukh, Aruna Vyas, Srinivas Kishore Sistla, Priyadarshini A Padaki, Dharshni Ramar, Saurav Sarkar, Bharani Rachagulla, Pattabhiraman Vallandaramam, Krishna Prabha Premachandran, Sunil Pawar, Piyush Gugale, Pradeep Hosamani, Sunil Narayan Dutt, Satish Nair, Hariprasad Kalpakkam, Sanjiv Badhwar, Kiran Kumar Kompella, Nidhi Singla, Milind Navlakhe, Amrita Prayag, Gagandeep Singh, Poorvesh Dhakecha, and Arunaloke Chakrabarti1
Author affiliations: Postgraduate Institute of Medical Education and Research, Chandigarh, India (V. Muthu, R. Agarwal, S.M. Rudramurthy, N. Panda, A. Chakrabarti); Kovai Medical Center and Hospital, Coimbatore, India (D. Thangaraju, G.D. Rajagopal); Avron Hospitals, Ahmedabad, India (M.R. Shevkani, R.S. Parwani); Sterling Hospital, Ahmedabad (A.K. Patel, K. Patel); Sir Gangaram Hospital, New Delhi, India (P.S. Shastri); Kingsway Hospital, Nagpur, India (A. Tayade, A. Deshmukh); Sawai Man Singh Medical College, Jaipur, India (S. Bhandari, A. Vyas); Asian Institute of Gastroenterology, Hyderabad, India (V. Gella, S.K. Sistla); St. John’s Medical College and Hospital, Bengaluru, India (J. Savio, P.A. Padaki); Care Institute of Medical Sciences, Ahmedabad (S. Madan, D. Ramar); All India Institute of Medical Science Bhubaneswar, Odisha, India (V.K. Hallur, S. Sarkar); Yashoda Hospitals, Hyderabad (V.N. Maturu, B. Rachagulla); Royal Care Hospital, Coimbatore (A. Srinivasan, P. Vallandaramam); Apollo Hospitals, Chennai, India (N. Sethuraman, K.P. Premachandran); Government Medical College, Patiala, India (R.P.S. Sibia, S. Pawar); Poona Hospital and Research Centre, Pune, India (S. Pujari, P. Gugale); Apollo Hospitals, Bengaluru (R. Mehta, H. Kalpakkam, P. Hosamani, S.N. Dutt, S. Nair); Kokilaben Dhirubhai Ambani Hospital and Medical Research Institute, Mumbai, India (T. Singhal, S. Badhwar); Army Hospital (Research and Referral), New Delhi (P. Saxena, K.K. Kompella); Government Medical College, Chandigarh (V. Gupta, N. Singla); Global Hospital, Mumbai (V. Nagvekar, M. Navlakhe); Deenanath Mangeshkar Hospital, Pune (P. Prayag, A. Prayag); City Clinic and Bhailal Amin General Hospital, Vadodara, India (D. Patel); All India Institute of Medical Sciences, New Delhi (I. Xess, G. Singh); Institute of Infectious Disease and Critical Care Hospital, Surat, India (P. Savaj, P. Dhakecha)

Main Article

Table 1

Baseline features of CAM case-patients and COVID-19 control-patients at admission for COVID-19, India, January–June 2021*

Category Controls, n = 3,911 CAM, n = 1,733 p value
Age, y, mean (SD)
 52.7 (13.5)
 52.6 (12.5)
 0.66
Male sex
2,738/3,911 (70.0)
 1,285/1,733 (74.1)
 0.002
Rural residence, n = 3,924
 309/2,615 (11.8)
 360/1,309 (27.5)
 0.0001
Risk factors for mucormycosis 0.0001
None 2,076/3,911 (53.1) 316/1,733 (18.2)
1 risk factor 1,743/3,911 (44.5) 1,374/1,733 (79.3)
>1 risk factors
 92/3,911 (2.4)
 43/1,733 (2.5)
Details of potential risk factors for mucormycosis†
Diabetes mellitus 1,763/3,911 (45.1) 1,402/1,733 (80.9) 0.0001
Hyperglycemia at admission, n = 5,236 998/3,625 (27.5) 758/1,611 (47.1) 0.0001
Plasma glucose at admission, mg/dL, mean (SD), n = 3,487 195 (94) 235 (106) 0.0001
Glycated hemoglobin, mean (SD), n = 1,856 7.7 (2.5) 10.1 (2.9) 0.0001
Duration of diabetes, y, mean (SD), n = 861 9.6 (9.5) 8.4 (6.8) 0.04
Recent onset of diabetes mellitus 319/1,763 (18.1) 246/1,402 (17.5) 0.66
DKA at the time of admission for COVID-19 48/1,763 (2.7) 73/1,402 (5.2) 0.0003
Renal transplant 36/3,911 (0.9) 31/1,733 (1.8) 0.005
Bone marrow transplant 0/3,911 (0) 1/1,733 (0.1) 0.31
Hematological malignancy 36/3,911 (0.9) 6/1,733 (0.3) 0.02
Immunosuppressive therapy 76/3,911 (1.9) 22/1,733 (1.3) 0.07
HIV 7/3,911 (0.2) 6/1,733 (0.3) 0.23
Others‡
 2/3,911 (0.0)
 2/1,733 (0.1)
 0.23
Comorbidities
Any comorbidity 828/3,911 (21.5) 265/1,733 (15.3) 0.0001
Coronary artery disease 285/3,911 (7.3) 126/1,733 (7.3) 0.98
Chronic kidney disease 284/3,911 (7.3) 98/1,733 (5.7) 0.03
Chronic heart failure 59/3,911 (1.5) 17/1,733 (1.0) 0.11
Chronic liver disease 71/3,911 (1.8) 13/1,733 (0.8) 0.002
Chronic respiratory disease 104/3,911 (2.7) 17/1,733 (1.0) 0.0001
Others§
 151/3,911 (3.9)
 35/1,733 (2.0)
 0.0001
Laboratory parameters during COVID-19 illness
Hemoglobin, g/dL, mean (SD), n = 4,506 12.2 (2.4) 12.1 (2.2) 0.11
Total leukocyte count, cells/µL, mean (SD), n = 4,501 9,853 (6,844) 11,396 (6,110) 0.0001
Median absolute lymphocyte count, cells/µL (IQR), n = 4,129 1,135 (720–1,706) 1,275 (803–1,833) 0.0001
Median absolute neutrophil count, cells/µL (IQR), n = 4,071 6,177 (3,658–10,244) 7,858 (4,943–11,867) 0.0001
Median NLR (IQR), n = 4,061 5.5 (2.7–11.4) 5.7 (3.2–11.7) 0.04
Platelet count, × 103/µL, mean (SD), n = 4,454 222 (107) 240 (105) 0.0001
Median C-reactive protein mg/dL (IQR), n = 3,972 26.7 (8.4–79.3) 48.8 (20–102.5) 0.0001
Median serum ferritin, µg/L (IQR) n = 3,168
 454 (189–977)
 580 (238–1,052)
 0.02
Details of COVID-19 illness
Hypoxemia, n = 5,476 2,100/3,851 (54.5) 751/1,625(46.2) 0.0001
ICU admission, n = 5,425 1,551/3,809 (40.7) 331/1,616 (20.5) 0.0001
Mechanical ventilation, n = 5,376
 1,126/3,765 (29.9)
 153/1,611 (9.5)
 0.0001
Management during COVID-19
Glucocorticoid therapy, n = 5,431 2,690/3,827 (70.3) 1,200/1,604 (74.8) 0.001
Glucocorticoid use in the absence of hypoxemia, n = 5,021 789/3,532 (22.3) 509/1,489 (34.2) 0.0001
Median cumulative dose of glucocorticoids in milligram 
equivalent of dexamethasone (IQR), n = 2,809 52.8 (30–84) 62.6 (30.2–120) 0.0001
Median no. days on glucocorticoid treatment (IQR), n = 2,887 8 (5–12) 10 (6.3–14) 0.0001
Zinc supplementation, n = 5,179 1,502/3,633 (41.3) 741/1,546 (47.9) 0.0001
Remdesivir, n = 5,167 1,785/3,631 (49.2) 317/1,536 (20.6) 0.0001
Tocilizumab, n = 5,167 72/3,631 (2.0) 37/1,536 (2.4) 0.41
Baricitinib, n = 5,167 38/3,631 (1.0) 13/1,536 (0.8) 0.50
Antibacterial therapy, n = 5,396 2,467/3,841 (64.2) 952/1,555 (61.2) 0.04
Antifungal therapy before CAM, n = 5,039 174/3,513 (5.0) 68/1,526 (4.5) 0.45

*Values are no. observed/total no. (%) unless otherwise indicated. CAM, COVID-19–associated mucormycosis; DKA, diabetic ketoacidosis; DM, diabetes mellitus; ICU, intensive care unit; IQR, interquartile range; NLR, neutrophil-to-lymphocyte ratio. †A single person might have had >1 risk factor; hence the numbers do not sum to 5,644. ‡Others include neutropenia (n = 3) and primary immunodeficiency (n = 1). §Others include neurologic, endocrinologic, and rheumatologic illnesses.

Main Article

1These senior authors contributed equally to this article.

Page created: November 10, 2022
Page updated: December 19, 2022
Page reviewed: December 19, 2022
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