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Manchanda S, Bhalla AS, Nair AD, Sikka K, Verma H, Thakar A, Kakkar A, Khan MA. Proposed computed tomography severity index for the evaluation of invasive fungal sinusitis: Preliminary results. World J Radiol 2024; 16:771-781. [PMID: 39801668 PMCID: PMC11718521 DOI: 10.4329/wjr.v16.i12.771] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 06/05/2024] [Revised: 10/24/2024] [Accepted: 12/03/2024] [Indexed: 12/27/2024] Open
Abstract
BACKGROUND Invasive fungal sinusitis (IFS) can present as a mild disease to life-threatening infection. A recent surge in cases was seen due to the coronavirus disease 2019 (COVID-19) pandemic. Many patients require surgical debridement and hence imaging [contrast-enhanced computed tomography (CECT) of the paranasal sinuses (PNS)] to document the extent of the disease. However, there was no scoring system using CECT to describe the severity of IFS. This study proposes a computed tomography (CT) severity index (CTSI) to describe the severity of rhino-orbital-cerebral involvement in symptomatic COVID-19 patients and hypothesizes that higher CTSI correlates with disease severity and thus slow response/non-response to treatment. AIM To propose a scoring system using CECT to describe the severity of IFS and correlate it with clinical outcomes. METHODS A prospective study on 66 COVID-19 positive patients with CECT PNS done for IFS was performed. Split-bolus single-phase CT technique was used. Based on the extent of involvement, a CTSI was designed. Disease in four major subsite areas was assessed. Each subsite involvement was given points according to this model and then summated. Based on the final summated CTSI, the disease was classified as mild, moderate, or severe. Two subsets were subsequently analyzed including survival and death; and responders and non-responders. RESULTS The study cohort was 66 COVID-19-positive patients with suspected IFS with a median age of 48.5 years. Mild disease was noted in 34 (51.52%), moderate in 28 (42.42%), and severe disease in 4 (6.06%) patients. There was a significant association of mortality and poor clinical response (P = 0.02) with disease bilaterality. Laterality and CTSI were significant predictors of response to treatment. The mean CTSI of responders was 6.3, of non-responders was 12.9 and the response to treatment was significantly associated with CTSI (t-test, P < 0.001). Receiver operating characteristic curve analysis (Liu method) to distinguish between responders and non-responders showed that the cut-off value for CTSI of 11 had a sensitivity of 78.26% and a specificity of 95.35% to predict response assessment. CONCLUSION CTSI can help in quantification of the disease burden, mapping out disease extent, triaging patients, and response assessment; especially patients with underlying comorbidities. A higher score would alert the clinician to initiate aggressive treatment, as severe disease correlates with slow response/non-response to the treatment.
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Affiliation(s)
- Smita Manchanda
- Department of Radiodiagnosis and Interventional Radiology, All India Institute of Medical Sciences, New Delhi 110029, India
| | - Ashu S Bhalla
- Department of Radiodiagnosis and Interventional Radiology, All India Institute of Medical Sciences, New Delhi 110029, India
| | - Ankita D Nair
- Department of Radiodiagnosis and Interventional Radiology, All India Institute of Medical Sciences, New Delhi 110029, India
| | - Kapil Sikka
- Department of Otorhinolaryngology and Skull Base Surgery, All India Institute of Medical Sciences, New Delhi 110029, India
| | - Hitesh Verma
- Department of Otorhinolaryngology and Skull Base Surgery, All India Institute of Medical Sciences, New Delhi 110029, India
| | - Alok Thakar
- Department of Otorhinolaryngology and Skull Base Surgery, All India Institute of Medical Sciences, New Delhi 110029, India
| | - Aanchal Kakkar
- Department of Pathology, All India Institute of Medical Sciences, New Delhi 110029, India
| | - Maroof A Khan
- Department of Biostatistics, All India Institute of Medical Sciences, New Delhi 110029, India
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Fitero A, Negrut N, John HT, Ferician A, Marian P. Corona-Associated Mucormycosis: Case Series Reports and Review of the Literature. J Fungi (Basel) 2024; 10:305. [PMID: 38786660 PMCID: PMC11122562 DOI: 10.3390/jof10050305] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 03/19/2024] [Revised: 04/17/2024] [Accepted: 04/22/2024] [Indexed: 05/25/2024] Open
Abstract
During the COVID-19 pandemic, a significant increase in cases of mucormycosis was observed in COVID-19 patients, especially in India, but not exclusively. The presented cases highlight the heterogeneous nature of mucormycosis, emphasizing the importance of recognizing predisposing factors, such as immunosuppression, due to comorbidities or medication. Diagnosing mucormycosis poses a challenge due to nonspecific clinical manifestations, requiring a multidisciplinary approach for accurate diagnosis. Treatment involves a multi-pronged approach centered around the early initiation of antifungal therapy alongside surgical intervention and the management of underlying conditions, with an emphasis on controlling immunosuppression. Understanding the relationship between COVID-19 and predisposing factors for mucormycosis is fundamental for developing prevention and treatment strategies.
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Affiliation(s)
- Andreea Fitero
- Department of Psycho-Neuroscience and Recovery, Faculty of Medicine and Pharmacy, University of Oradea, 410073 Oradea, Romania;
- Doctoral School of Biomedical Sciences, Faculty of Medicine and Pharmacy, University of Oradea, 410087 Oradea, Romania
| | - Nicoleta Negrut
- Department of Psycho-Neuroscience and Recovery, Faculty of Medicine and Pharmacy, University of Oradea, 410073 Oradea, Romania;
- Doctoral School of Biomedical Sciences, Faculty of Medicine and Pharmacy, University of Oradea, 410087 Oradea, Romania
| | - Harrie Toms John
- Department of Ear, Nose and Throat, University Hospitals of Northamptonshire, Cliftonville, Northampton NN1 5BD, UK;
| | - Anca Ferician
- Department of Medical Disciplines, Faculty of Medicine and Pharmacy, University of Oradea, 410073 Oradea, Romania; (A.F.); (P.M.)
| | - Paula Marian
- Department of Medical Disciplines, Faculty of Medicine and Pharmacy, University of Oradea, 410073 Oradea, Romania; (A.F.); (P.M.)
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Dallalzadeh LO, Ediriwickrema LS, Fung SE, Men CJ, Kossler AL, Kupcha AC, Mawn LA, Burkat CN, van Landingham SW, Conger JR, Simmons B, Pham C, Akella SS, Setabutr P, Ho T, Couch SM, Kim JS, Demirci H, Korn BS, Kikkawa DO, Liu CY. Transcutaneous retrobulbar amphotericin B for rhino-orbital-cerebral mucormycosis: a multi-center retrospective comparative study. Orbit 2024; 43:41-48. [PMID: 36880205 DOI: 10.1080/01676830.2023.2186435] [Citation(s) in RCA: 1] [Impact Index Per Article: 1.0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 10/14/2022] [Accepted: 02/25/2023] [Indexed: 03/08/2023]
Abstract
PURPOSE To assess whether transcutaneous retrobulbar amphotericin B injections (TRAMB) reduce exenteration rate without increasing mortality in rhino-orbital-cerebral mucormycosis (ROCM). METHODS In this retrospective case-control study, 46 patients (51 eyes) with biopsy-proven ROCM were evaluated at 9 tertiary care institutions from 1998 to 2021. Patients were stratified by radiographic evidence of local orbital versus extensive involvement at presentation. Extensive involvement was defined by MRI or CT evidence of abnormal or loss of contrast enhancement of the orbital apex with or without cavernous sinus, bilateral orbital, or intracranial extension. Cases (+TRAMB) received TRAMB as adjunctive therapy while controls (-TRAMB) did not. Patient survival, globe survival, and vision/motility loss were compared between +TRAMB and -TRAMB groups. A generalized linear mixed effects model including demographic and clinical covariates was used to evaluate the impact of TRAMB on orbital exenteration and disease-specific mortality. RESULTS Among eyes with local orbital involvement, exenteration was significantly lower in the +TRAMB group (1/8) versus -TRAMB (8/14) (p = 0.04). No significant difference in mortality was observed between the ±TRAMB groups. Among eyes with extensive involvement, there was no significant difference in exenteration or mortality rates between the ±TRAMB groups. Across all eyes, the number of TRAMB injections correlated with a statistically significant decreased rate of exenteration (p = 0.048); there was no correlation with mortality. CONCLUSIONS Patients with ROCM with local orbital involvement treated with adjunctive TRAMB demonstrated a lower exenteration rate and no increased risk of mortality. For extensive involvement, adjunctive TRAMB does not improve or worsen these outcomes.
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Affiliation(s)
- Liane O Dallalzadeh
- Division of Oculofacial Plastic and Reconstructive Surgery, Viterbi Family Department of Ophthalmology, Shiley Eye Institute, UC San Diego, La Jolla, California, USA
| | - Lilangi S Ediriwickrema
- Division of Ophthalmic Plastic and Reconstructive Surgery, Gavin Herbert Eye Institute, UC Irvine, Irvine, California, USA
| | - Sammie E Fung
- Division of Oculofacial Plastic and Reconstructive Surgery, Viterbi Family Department of Ophthalmology, Shiley Eye Institute, UC San Diego, La Jolla, California, USA
| | - Clara J Men
- Division of Oculoplastic and Orbital Surgery, Byers Eye Institute, Stanford University, Palo Alto, California, USA
| | - Andrea L Kossler
- Division of Oculoplastic and Orbital Surgery, Byers Eye Institute, Stanford University, Palo Alto, California, USA
| | - Anna C Kupcha
- Division of Oculoplastics and Orbital Disease, Vanderbilt Eye Institute, Vanderbilt University, Nashville, Tennessee, USA
| | - Louise A Mawn
- Division of Oculoplastics and Orbital Disease, Vanderbilt Eye Institute, Vanderbilt University, Nashville, Tennessee, USA
| | - Cat N Burkat
- Oculoplastic, Orbital, & Cosmetic Facial Surgery, Department of Ophthalmology and Visual Sciences, University of Wisconsin Madison, Madison, Wisconsin, USA
| | - Suzanne W van Landingham
- Oculoplastic, Orbital, & Cosmetic Facial Surgery, Department of Ophthalmology and Visual Sciences, University of Wisconsin Madison, Madison, Wisconsin, USA
| | - Jordan R Conger
- Division of Ophthalmic Plastic and Reconstructive Surgery, Gavin Herbert Eye Institute, UC Irvine, Irvine, California, USA
| | - Brittany Simmons
- Division of Oculoplastic, Orbit, and Reconstructive Surgery, Department of Ophthalmology and Visual Sciences, University of Iowa, Iowa City, Iowa, USA
| | - Chau Pham
- Division of Oculoplastic, Orbit, and Reconstructive Surgery, Department of Ophthalmology and Visual Sciences, University of Iowa, Iowa City, Iowa, USA
| | - Sruti S Akella
- Oculoplastic and Reconstructive Surgery Service, Illinois Eye and Ear Infirmary, University of Illinois, Chicago, Illinois, USA
| | - Pete Setabutr
- Oculoplastic and Reconstructive Surgery Service, Illinois Eye and Ear Infirmary, University of Illinois, Chicago, Illinois, USA
| | - Tiffany Ho
- Division of Oculofacial Plastic and Reconstructive Surgery, Department of Ophthalmology and Visual Sciences, Washington University in St. Louis, St. Louis, Missouri, USA
| | - Steven M Couch
- Division of Oculofacial Plastic and Reconstructive Surgery, Department of Ophthalmology and Visual Sciences, Washington University in St. Louis, St. Louis, Missouri, USA
| | - Jane S Kim
- Division of Eye Plastic, Orbital and Facial Cosmetic Surgery, Kellogg Eye Center, University of Michigan, Ann Arbor, Michigan, USA
| | - Hakan Demirci
- Division of Eye Plastic, Orbital and Facial Cosmetic Surgery, Kellogg Eye Center, University of Michigan, Ann Arbor, Michigan, USA
| | - Bobby S Korn
- Division of Oculofacial Plastic and Reconstructive Surgery, Viterbi Family Department of Ophthalmology, Shiley Eye Institute, UC San Diego, La Jolla, California, USA
- Division of Plastic and Reconstructive Surgery, UC San Diego Department of Surgery, La Jolla, California, USA
| | - Don O Kikkawa
- Division of Oculofacial Plastic and Reconstructive Surgery, Viterbi Family Department of Ophthalmology, Shiley Eye Institute, UC San Diego, La Jolla, California, USA
- Division of Plastic and Reconstructive Surgery, UC San Diego Department of Surgery, La Jolla, California, USA
| | - Catherine Y Liu
- Division of Oculofacial Plastic and Reconstructive Surgery, Viterbi Family Department of Ophthalmology, Shiley Eye Institute, UC San Diego, La Jolla, California, USA
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Erami M, Raiesi O, Momen-Heravi M, Mirhendi H, Aboutalebian S, Getso MI, Matini AH, Ahsaniarani AH, Ganjizadeh M, Hassani Josheghani H, Amiri S, Pakzad R, Hashemi SJ. COVID-19 associated mucormycosis (CAM) in Kashan, Iran: clinical presentations, risk factors, management, and outcomes. Infect Dis (Lond) 2024; 56:81-90. [PMID: 37816067 DOI: 10.1080/23744235.2023.2267669] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 04/24/2023] [Accepted: 10/02/2023] [Indexed: 10/12/2023] Open
Abstract
BACKGROUND This study aimed to estimate the disease burden and describe the clinical presentation, risk factors, and outcome of CAM in a single centre in Iran. METHODS A case of mucormycosis was defined as one that had clinical and radiological features consistent with mucormycosis along with demonstration of the fungus in tissue via KOH mount/culture/histopathological and molecular examination. RESULTS We report 30 cases of COVID-19 associated mucormycosis (CAM). The results of this study showed the affected age group in the range of 40-79 years (median = 65.5; IQR = 5) with women (16/30, 53%) affected more than men (14/30, 47%). Among the fungi recovered, Rhizopus oryzae had the highest frequency (79%). Out of the 30 patients, 28 (93%) patients were diabetic with 24 (80%) patients having other co-morbidities. Headache followed by retro-orbital pain, proptosis/ptosis and rapid diminution of vision was a common sequence of symptoms reported by the majority of cases. Use of mechanical ventilation (58% vs. 6%, p = 0.003), O2 required (92% vs. 50%, p = 0.024), and development of renal dysfunction during hospital stay (17% vs. 0%, p = 0.041) was significantly higher in non-survivors than survivors. Temperature (C°), PR (pulse rate), mean levels of serum creatinine, BUN, troponin, and neutrophils were significantly higher in non-survivors (p < 0.05). Besides, Albumin and PO2 were also significantly higher in survivors than non-survivors. CONCLUSION Despite medical and surgical treatment, the mortality rate among CAM patients is still high. Thus, concerted efforts of revamping surveillance, diagnosis and management, along with public awareness and patient education, are the requisites for managing COVID-19 and mucormycosis.
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Affiliation(s)
- Mahzad Erami
- Department of Medical Mycology, School of Public Health, Tehran University of Medical Sciences, Tehran, Iran
| | - Omid Raiesi
- Department of Parasitology, School of Allied Medical Sciences, Ilam University of Medical Sciences, Ilam, Iran
- Zoonotic Diseases Research Center, Ilam University of Medical Sciences, Ilam, Iran
| | | | - Hossein Mirhendi
- Department of Medical Parasitology and Mycology, Isfahan University of Medical Sciences, Isfahan, Iran
| | - Shima Aboutalebian
- Department of Medical Parasitology and Mycology, Isfahan University of Medical Sciences, Isfahan, Iran
| | - Muhammad Ibrahim Getso
- Department of Medical Mycology, School of Public Health, Tehran University of Medical Sciences, Tehran, Iran
- Department of Medical Microbiology and Parasitology, College of Health Sciences, Bayero University Kano, Kano, Nigeria
| | - Amir Hassan Matini
- Department of Pathology and Histology, School of Medicine, Shahid Beheshti Hospital, Kashan University of Medical Sciences, Kashan, Iran
| | - Amir Hossein Ahsaniarani
- Head and Neck Surgery, Department, Otorhinolaryngology, School of Medicine, Matini Hospital, Kashan University of Medical Sciences, Kashan, Iran
| | - Mohsen Ganjizadeh
- Kashan Shahid Beheshti Hospital, Kashan University of Medical Sciences, Kashan, Iran
| | | | - Sasan Amiri
- Roozbeh hospital, School of Medicine, Tehran University of Medical Sciences, Tehran, Iran
| | - Reza Pakzad
- Department of Epidemiology, Ilam University of Medical Sciences, Ilam, Iran
- Student Research Committee, Ilam University of Medical Sciences, Ilam, Iran
| | - Seyed Jamal Hashemi
- Department of Medical Mycology, School of Public Health, Tehran University of Medical Sciences, Tehran, Iran
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5
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Sharma B, Nonzom S. Mucormycosis and Its Upsurge During COVID-19 Epidemic: An Updated Review. Curr Microbiol 2023; 80:322. [PMID: 37592083 DOI: 10.1007/s00284-023-03430-w] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 08/05/2022] [Accepted: 07/26/2023] [Indexed: 08/19/2023]
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.
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Affiliation(s)
- Bharti Sharma
- Department of Botany, University of Jammu, Jammu, Jammu and Kashmir, 180006, India
| | - Skarma Nonzom
- Department of Botany, University of Jammu, Jammu, Jammu and Kashmir, 180006, India.
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Patel VB, Patel A, Mishra G, Shah N, Shinde MK, Musa RK. Imaging spectrum, associations and outcomes in acute invasive fungal rhino-ocular-cerebral sinusitis in patients with COVID-19 pneumonia. J Family Med Prim Care 2023; 12:1055-1062. [PMID: 37636178 PMCID: PMC10451586 DOI: 10.4103/jfmpc.jfmpc_1189_22] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 06/02/2022] [Revised: 09/07/2022] [Accepted: 09/09/2022] [Indexed: 08/29/2023] Open
Abstract
Background Coronavirus Disease 2019 (COVID-19) has been speculated to enhance mucormycosis infection due to its immune-altering pathophysiology. Early identification of high-morbidity conditions is crucial for optimal treatment and improved outcomes. Methods A retrospective study was conducted on 63 patients with clinical and microbiological evidence of rhino-ocular-cerebral mucormycosis, who had a history of COVID-19 infection. The clinical, demographic, and imaging data were retrieved and analyzed. Descriptive statistics (mean [SD] and frequency [%]) were used to describe important characteristics across audit cycles. Results Out of 63 patients, 54 (85.71%) patients had associated comorbidities, with diabetes mellitus being common comorbidity and all patients had received injectable and/or oral corticosteroids. Imaging showed nasal and paranasal sinus, perisinus, maxillary alveolar arch, and hard palate involvement in 62 (98.41%), 33 (52.38%), 5 (7.94%) and 5 (7.94%) patients, respectively. Orbital involvement was seen in 24 (38.10%) patients. Skull base involvement was seen in 11 (17.46%) patients, and intracranial extension of disease was present in 11 (17.46%) patients. A total of 16 patients were on mechanical ventilation, of whom 3 succumbed. The mean (standard deviation [SD]) intensive care unit (ICU) stay was 13.2 days (6.8) for 5 patients who succumbed and 6.4 days (4.6) for 30 patients who survived (P value = 0.008). Conclusion Cross-sectional imaging not only provides the extent of disease spread but also plays a vital role in providing a surgical roadmap to treating surgeons and in predicting prognosis in patients with invasive fungal infections.
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Affiliation(s)
- Viral B. Patel
- Department of Radio Diagnosis, Pramukh Swami Medical College and Shree Krishna Hospital, Bhaikaka University, Karamsad, Gujarat, India
| | - Aashvi Patel
- Department of Otolaryngology, Medical Officer, IRIS Hospital, Anand Gujarat, India
| | - Girish Mishra
- Department of Otolaryngology, Pramukh Swami Medical College and Shree Krishna Hospital, Bhaikaka University, Karamsad, Gujarat, India
| | - Nilay Shah
- ENT and Head – Neck Surgeon, IRIS Hospital, Anand, Gujarat, India
| | - Mayur K. Shinde
- Department of Biostatistics, Pramukh Swami Medical College and Shree Krishna Hospital, Bhaikaka University, Karamsad, Gujarat, India
| | - Raish K. Musa
- Department of Radio Diagnosis, Pramukh Swami Medical College and Shree Krishna Hospital, Bhaikaka University, Karamsad, Gujarat, India
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Banerjee A, Das M, Verma P, Chatterjee A, Ramalingam K, Srivastava KC. COVID-19 and Mucormycosis of Orofacial Region: A Scoping Review. Cureus 2023; 15:e37984. [PMID: 37223184 PMCID: PMC10202344 DOI: 10.7759/cureus.37984] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Accepted: 04/22/2023] [Indexed: 05/25/2023] Open
Abstract
During the second wave of coronavirus disease, or COVID-19, infection due to severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) virus in the year 2021 around the globe, there is a surge in the number of cases of mucormycosis or "Black Fungus" that is directly/indirectly associated with COVID-19. In this review article, mucormycosis of the orofacial region has gained importance from the maximum published literature (45 articles) from various databases like PubMed, Google Scholar, Scopus, Web of Science, and Embase. Rhino-orbital cerebral mucormycosis (ROCM) is a fatal condition associated with COVID-19 among categories of mucormycosis such as pulmonary, oral, gastrointestinal, cutaneous, and disseminated. ROCM targets the maxillary sinus, also involving teeth of the maxilla, orbits, and ethmoidal sinus. These are of particular interest to dentists and oral pathologists for proper diagnosis and identification. Co-morbid conditions, especially diabetes mellitus type II, have to be monitored carefully in COVID-19 patients as they have a higher risk of developing mucormycosis. In this review article, various presentations of COVID-19-linked mucormycosis are mentioned having particular emphasis on pathogenesis, signs and symptoms, clinical presentation, various diagnostic modalities including histopathology, radiology like CT and MRI, serology, tissue culture, various laboratory investigations, treatment protocols, management with prognosis, and so on. Any suspected case of mucormycosis needs quick detection and treatment since it progresses quickly due to the destructive course of infection. Long-term follow-up along with proper care is a must to detect any kind of recurrence.
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Affiliation(s)
- Abhisek Banerjee
- Oral and Maxillofacial Pathology, Awadh Dental College and Hospital, Jamshedpur, IND
| | - Moumalini Das
- Oral and Maxillofacial Pathology, Awadh Dental College and Hospital, Jamshedpur, IND
| | - Pooja Verma
- Oral and Maxillofacial Pathology, Awadh Dental College and Hospital, Jamshedpur, IND
| | - Abhishek Chatterjee
- Dentistry, Rampurhat Government Medical College and Hospital, Rampurhat, IND
| | - Karthikeyan Ramalingam
- Oral pathology, Saveetha Dental College and Hospitals, Saveetha Institute of Medical and Technical Sciences, Chennai, IND
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Li CX, Gong ZC, Pataer P, Shao B, Fang C. A retrospective analysis for the management of oromaxillofacial invasive mucormycosis and systematic literature review. BMC Oral Health 2023; 23:115. [PMID: 36810012 PMCID: PMC9942087 DOI: 10.1186/s12903-023-02823-4] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 11/30/2022] [Accepted: 02/17/2023] [Indexed: 02/24/2023] Open
Abstract
PURPOSE Mucormycosis is a type of fatal infectious disease, rarely involved in the oromaxillofacial region. This study aimed to describe a series of 7 cases with oromaxillofacial mucormycosis and to discuss the epidemiology, clinical features, and treatment algorithm thereof. METHODOLOGY Seven patients in the author's affiliation have been treated. They were assessed and presented as per their diagnostic criteria, surgical approach, and mortality rates. Reported cases of mucormycosis originally happened in craniomaxillofacial region were synthesized through a systematic review so as to better discuss its pathogenesis, epidemiology, and management. RESULTS Six patients had a primary metabolic disorder, and one immunocompromised patient had a history of aplastic anemia. The criteria for a positive diagnosis of invasive mucormycosis were based on clinical presentation of signs and symptoms, and a biopsy for microbiological culture and histopathologic analysis. Each patient used antifungal drugs and five of them also underwent surgical resection at the same time. Four patients died due to the unregulated spread of mucormycosis, and one patient died owing to her main disease. CONCLUSIONS Although uncommon in clinical practice setting, mucormycosis should be of great concern in oral and maxillofacial surgery, due to the life-threatening possibility of this disease. The knowledge of early diagnosis and prompt treatment is of utmost importance for saving lives.
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Affiliation(s)
- Chen-xi Li
- grid.412631.3Department of Oral and Maxillofacial Oncology and Surgery, The First Affiliated Hospital of Xinjiang Medical University, School/Hospital of Stomatology, Xinjiang Medical University, Stomatological Research Institute of Xinjiang Uygur Autonomous Region, No.137 Liyushan South Road, Ürümqi, 830054 People’s Republic of China ,grid.33199.310000 0004 0368 7223Hubei Province Key Laboratory of Oral and Maxillofacial Development and Regeneration, Wuhan, 430022 People’s Republic of China
| | - Zhong-cheng Gong
- grid.412631.3Department of Oral and Maxillofacial Oncology and Surgery, The First Affiliated Hospital of Xinjiang Medical University, School/Hospital of Stomatology, Xinjiang Medical University, Stomatological Research Institute of Xinjiang Uygur Autonomous Region, No.137 Liyushan South Road, Ürümqi, 830054 People’s Republic of China
| | - Parekejiang Pataer
- grid.412631.3Department of Oral and Maxillofacial Oncology and Surgery, The First Affiliated Hospital of Xinjiang Medical University, School/Hospital of Stomatology, Xinjiang Medical University, Stomatological Research Institute of Xinjiang Uygur Autonomous Region, No.137 Liyushan South Road, Ürümqi, 830054 People’s Republic of China
| | - Bo Shao
- grid.412631.3Department of Oral and Maxillofacial Oncology and Surgery, The First Affiliated Hospital of Xinjiang Medical University, School/Hospital of Stomatology, Xinjiang Medical University, Stomatological Research Institute of Xinjiang Uygur Autonomous Region, No.137 Liyushan South Road, Ürümqi, 830054 People’s Republic of China
| | - Chang Fang
- grid.412631.3Department of Oral and Maxillofacial Oncology and Surgery, The First Affiliated Hospital of Xinjiang Medical University, School/Hospital of Stomatology, Xinjiang Medical University, Stomatological Research Institute of Xinjiang Uygur Autonomous Region, No.137 Liyushan South Road, Ürümqi, 830054 People’s Republic of China
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9
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Garg R, Bharangar S, Gupta S, Bhardwaj S. Post Covid-19 Infection Presenting as Rhino-Orbital Mycosis. Indian J Otolaryngol Head Neck Surg 2022; 74:3050-3057. [PMID: 34307112 PMCID: PMC8279101 DOI: 10.1007/s12070-021-02722-6] [Citation(s) in RCA: 8] [Impact Index Per Article: 2.7] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 06/15/2021] [Accepted: 06/27/2021] [Indexed: 01/12/2023] Open
Abstract
Rhino-orbital mycosis has been recently recognised as one of the sequelae in COVID-19 recovered patients. In India, detection of mucormycosis is declared as notifiable disease. In this article, the authors aim to describe the characteristics of patients presenting with post covid fungal infection which could be detected on 10% potassium hydroxide (KOH) wet mount and Giemsa stain put on crush biopsy smear. We describe 10 COVID-19 recovered patients admitted to ENT department of the hospital during second wave of COVID-19 infection. They presented with post covid fungal sinusitis and ophthalmic complications and planned for surgery. KOH mount and Giemsa stain were used for possible opinion and confirmed by culture. The observations were described in mean and percentages. All ten (100%) COVID-19 recovered patients were previously diagnosed with type 2 diabetes mellitus (DM) for 2-11 years. All 10 patients (100%) were given oral or intravenous corticosteroids for mean of 21 days (3 weeks-till presentation to ENT department). Simple procedures with 10% KOH mount and Giemsa stain could detect fungal hypae in all the cases and could provide possible opinion in 9 of 10 (90%) cases for timely management of the patients. The authors hypothesize that uncontrolled DM and prolonged use of corticosteroids may act as culprits of rhino-orbital mycosis in COVID-19 recovered patients. Simple and routine 10% KOH mount and Giemsa stain may provide early opinion of fungal hypae to ensure quick management and survival of the patients.
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Affiliation(s)
- Richa Garg
- Consultant Pathologist, Crest Hospital, Moradabad, Uttar Pradesh India
| | - Sandeep Bharangar
- Consultant Otolaryngologist, Crest Hospital, Moradabad, Uttar Pradesh India
| | - Sunil Gupta
- Consultant Opthalmologist, Sahu Rameshwar Saran Hospital and Research Centre, Moradabad, Uttar Pradesh India
| | - Samiksha Bhardwaj
- Consultant Radiologist, Crest Hospital, Moradabad, Uttar Pradesh India
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Shaban E, Saleh RA, Ammar MI, Ebeid K. Post-COVID-19 acute invasive fungal rhinosinusitis: a systematic radiological approach in the light of clinico-surgical characteristics. THE EGYPTIAN JOURNAL OF RADIOLOGY AND NUCLEAR MEDICINE 2022. [PMCID: PMC9472733 DOI: 10.1186/s43055-022-00880-3] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 11/18/2022] Open
Abstract
Background The objective is to describe the radiological imaging findings of post-COVID-19 acute invasive fungal rhinosinusitis (AIFRS), being familiar with the wide variety of imaging spectrum, thus raising the suspicion for early diagnosis. Methods: In this retrospective study, we reviewed the imaging findings in 54 patients with proven post-COVID-19 AIFRS who underwent endoscopic/surgical debridement from April 2020 to September 2021. Most of these patients presented with facial or orbital swelling or facial pain. Medical records with a special emphasis on radiological imaging (50 NCCT of the paranasal sinuses and 17 MRIs of the orbit) were reviewed regarding the degree of mucosal disease of sinuses, nasal cavity, and nasopharynx, extra sinus soft tissue infiltration, especially orbital and cerebral extension (parenchymal, cavernous sinus, vascular or neuro-invasion). Results We reported findings in 54 patients with post-COVID-19 AIFRS, of whom 30 were men and 24 were women with a mean age of 48.06. Unexpectedly, infiltration of pterygopalatine fossa was found to precede mucosal opacification of sinuses nasal cavity and affection of nasopharynx. Out of 54 patients, 49 showed inflammatory changes involving pterygopalatine fossa, 29.6% of patients showed infiltration of orbital tissues, 22 patients suffered from a fungal invasion of the cavernous sinus and 3 patients had carotid artery involvement. Conclusions Imaging findings of AIFRS significantly vary from subtle mucosal thickening of paranasal sinuses, up to orbital and intracranial extension with vascular thrombosis and neuroinvasion. The hallmark inflammatory tissue infiltration into the pterygopalatine fossa and facial soft tissue may precede mucosal disease.
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Ambasta A, Kusumesh R, Rajpal K, Kumar S, Singh V. Non-Mucormycetes Causes of Fungal Rhino Sinusitis With Periocular Swelling in COVID-19 With Delta Variant. Cureus 2022; 14:e28825. [PMID: 36225443 PMCID: PMC9535616 DOI: 10.7759/cureus.28825] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Accepted: 09/05/2022] [Indexed: 11/05/2022] Open
Abstract
Objective: To highlight fungi other than mucormycetes as causative agents of rhinosinusitis with periocular swelling in coronavirus (COVID-19) infection caused by Delta variant of SARS-CoV-2 virus and identify the presenting features, risk factors, intervention, and outcomes. Methods and analysis: A retrospective interventional study of 96 patients with fungal rhinosinusitis and periocular swelling was done in patients with concurrent or recovered COVID-19 infection with the Delta variant (B.1.617.2) of SARS-CoV-2 virus in India. All patients with mucormycetes infection were excluded. Clinical presentation, medical history, blood reports, and imaging were analyzed. Management was by intravenous (IV) liposomal amphotericin B and functional endoscopic sinus surgery (FESS) with paranasal sinus debridement. Limited orbital debridement with or without transcutaneous retrobulbar liposomal amphotericin B (TRAMB) was done in patients with orbital involvement. Postoperative antifungal therapy was decided on the basis of the causative fungi. Results: Four cases of Aspergillus and one each of Fusarium, Curvularia, and Penicillium-associated fungal rhinosinusitis with periocular swelling were seen. Signs of orbital involvement on MRI were present in all four of them. Two of these showed partial third-nerve palsy while one case with aspergillosis suffered cavernous sinus thrombosis. Proptosis was not witnessed in any case. History of diabetes and use of steroids was seen in all patients. All patients had mild to moderate COVID-19 with oxygen supplementation needed in one. No mortality, acute vision loss, or exenteration took place. Conclusion: Aspergillus, Fusarium, Curvularia, and Penicillium were non-mucormycetes causes of fungal rhinosinusitis with periocular swelling in COVID-19 infection with the Delta variant (B.1.617.2) of SARS COV-2 virus. Few cases showed orbital and intracranial involvement.
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12
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Mortality-Related Risk Factors for Coronavirus Disease (COVID-19)-Associated Mucormycosis: a systematic review and meta-analysis. CURRENT FUNGAL INFECTION REPORTS 2022; 16:143-153. [PMID: 35971380 PMCID: PMC9366801 DOI: 10.1007/s12281-022-00440-2] [Citation(s) in RCA: 3] [Impact Index Per Article: 1.0] [Reference Citation Analysis] [Abstract] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Accepted: 08/01/2022] [Indexed: 12/12/2022]
Abstract
Purpose of Review Severe Acute Respiratory Syndrome-Coronavirus-2 (SARS-CoV-2) can increase the susceptibility of individuals to contracting mucormycosis through several mechanisms. Nowadays, coronavirus disease (COVID-19)-associated mucormycosis (CAM) is a serious public health concern, particularly in developing countries. This meta-analysis aims to identify the risk factors that affect the mortality rate of patients with CAM. Recent Findings We systematically searched PubMed, Google Scholar, Scopus, Cochrane library, and preprint databases using pertinent keywords and the reference lists of the included relevant articles from inception till October 27, 2021. In order to reduce the effects of small-scale studies, we only selected cross-sectional, case–control, and cohort studies and case series with at least four patients. We identified 26 articles that included 821 patients with CAM. The effect size (ES) of mortality rate was 28% (95% confidence interval (CI) 20%–38%; I2 =82.28%; p for Cochran Q<0.001). The CAM patients with a history of comorbidities other than diabetes (malignancies, transplant, or renal failure), mechanical ventilation due to COVID-19, pulmonary and cerebral mucormycosis, and those who only received medical treatment for mucormycosis had the highest mortality rate. Summary Coronavirus disease (COVID-19)-associated mucormycosis (CAM) is a major public health problem, particularly in developing countries. Severe COVID-19 infection, history of mechanical ventilation, early CAM, comorbidities other than diabetes (malignancies, transplant, or renal failure), pulmonary and rhino-orbito-cerebral mucormycosis, and delivering only medical treatment for mucormycosis were the worst prognostic factors in CAM patients. Identifying the mortality-related risk factors in CAM patients may help reduce the mortality rate by implementing optimized treatment approaches. Supplementary Information The online version contains supplementary material available at 10.1007/s12281-022-00440-2.
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Alkhamiss AS, Ahmed AA, Rasheed Z, Alghsham R, Shariq A, Alsaeed T, Althwab SA, Alsagaby S, Aljohani ASM, Alhumaydhi FA, Alduraibi SK, Alduraibi AK, Alhomaidan HT, Allemailem KS, Alharbi RA, Alamro SA, Alqusayer AM, Alharbi SA, Alharby TA, Almujaydil MS, Mousa AM, Alghaniam SA, Alghunaim AA, Alghamdi R, Fernández N, Al Abdulmonem W. Mucormycosis co-infection in COVID-19 patients: An update. Open Life Sci 2022; 17:917-937. [PMID: 36045713 PMCID: PMC9372758 DOI: 10.1515/biol-2022-0085] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 03/02/2022] [Revised: 04/09/2022] [Accepted: 04/15/2022] [Indexed: 01/08/2023] Open
Abstract
Mucormycosis (MCM) is a rare fungal disorder that has recently been increased in parallel with novel COVID-19 infection. MCM with COVID-19 is extremely lethal, particularly in immunocompromised individuals. The collection of available scientific information helps in the management of this co-infection, but still, the main question on COVID-19, whether it is occasional, participatory, concurrent, or coincidental needs to be addressed. Several case reports of these co-infections have been explained as causal associations, but the direct contribution in immunocompromised individuals remains to be explored completely. This review aims to provide an update that serves as a guide for the diagnosis and treatment of MCM patients' co-infection with COVID-19. The initial report has suggested that COVID-19 patients might be susceptible to developing invasive fungal infections by different species, including MCM as a co-infection. In spite of this, co-infection has been explored only in severe cases with common triangles: diabetes, diabetes ketoacidosis, and corticosteroids. Pathogenic mechanisms in the aggressiveness of MCM infection involves the reduction of phagocytic activity, attainable quantities of ferritin attributed with transferrin in diabetic ketoacidosis, and fungal heme oxygenase, which enhances iron absorption for its metabolism. Therefore, severe COVID-19 cases are associated with increased risk factors of invasive fungal co-infections. In addition, COVID-19 infection leads to reduction in cluster of differentiation, especially CD4+ and CD8+ T cell counts, which may be highly implicated in fungal co-infections. Thus, the progress in MCM management is dependent on a different strategy, including reduction or stopping of implicit predisposing factors, early intake of active antifungal drugs at appropriate doses, and complete elimination via surgical debridement of infected tissues.
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Affiliation(s)
- Abdullah S. Alkhamiss
- Department of Pathology, College of Medicine, Qassim University, Buraidah, Saudi Arabia
| | - Ahmed A. Ahmed
- Research Center, College of Medicine, Qassim University, Buraidah, Saudi Arabia
| | - Zafar Rasheed
- Department of Medical Biochemistry, College of Medicine, Qassim University, Buraidah, Saudi Arabia
| | - Ruqaih Alghsham
- Department of Pathology, College of Medicine, Qassim University, Buraidah, Saudi Arabia
| | - Ali Shariq
- Departments of Microbiology, College of Medicine, Qassim University, Buraidah, Saudi Arabia
| | - Thamir Alsaeed
- Department of Pathology, College of Medicine, Qassim University, Buraidah, Saudi Arabia
| | - Sami A. Althwab
- Department of Food Science and Human Nutrition, College of Agriculture and Veterinary Medicine, Qassim University, Buraidah, Saudi Arabia
| | - Suliman Alsagaby
- Department of Medical Laboratories Sciences, College of Applied Medical Sciences, Majmaah University, Majmaah, Saudi Arabia
| | - Abdullah S. M. Aljohani
- Department of Veterinary Medicine, College of Agricultural and Veterinary Medicine, Qassim University, Buraidah, Saudi Arabia
| | - Fahad A. Alhumaydhi
- Department of Medical Laboratories, College of Applied Medical Sciences, Qassim University, Buraidah, Saudi Arabia
| | - Sharifa K. Alduraibi
- Department of Radiology, College of Medicine, Qassim University, Buraidah, Saudi Arabia
| | - Alaa K. Alduraibi
- Department of Radiology, College of Medicine, Qassim University, Buraidah, Saudi Arabia
| | - Homaidan T. Alhomaidan
- Department of Family and Community Medicine, College of Medicine, Qassim University, Buraidah, Saudi Arabia
| | - Khaled S. Allemailem
- Department of Medical Laboratories, College of Applied Medical Sciences, Qassim University, Buraidah, Saudi Arabia
| | - Raya A. Alharbi
- Department of Food Science and Human Nutrition, College of Agriculture and Veterinary Medicine, Qassim University, Buraidah, Saudi Arabia
| | - Samar A. Alamro
- Department of Food Science and Human Nutrition, College of Agriculture and Veterinary Medicine, Qassim University, Buraidah, Saudi Arabia
| | - Arwa M. Alqusayer
- Department of Food Science and Human Nutrition, College of Agriculture and Veterinary Medicine, Qassim University, Buraidah, Saudi Arabia
| | - Sahim A. Alharbi
- Department of Food Science and Human Nutrition, College of Agriculture and Veterinary Medicine, Qassim University, Buraidah, Saudi Arabia
| | - Thekra A. Alharby
- Department of Food Science and Human Nutrition, College of Agriculture and Veterinary Medicine, Qassim University, Buraidah, Saudi Arabia
| | - Mona S. Almujaydil
- Department of Food Science and Human Nutrition, College of Agriculture and Veterinary Medicine, Qassim University, Buraidah, Saudi Arabia
| | - Ayman M. Mousa
- Department of Basic Health Sciences, College of Applied Medical Sciences, Qassim University, Buraidah, Saudi Arabia
- Department of Histology and Cell Biology, Faculty of Medicine, Benha University, Benha, Egypt
| | - Sultan A. Alghaniam
- Department of Clinical Nutrition, Qassim Health Affairs, Ministry of Health, Buraidah, Saudi Arabia
| | | | - Rana Alghamdi
- Department of Chemistry, Science and Arts College, Rabigh Campus, King Abdulaziz University, Jeddah, Saudi Arabia
| | | | - Waleed Al Abdulmonem
- Department of Pathology, College of Medicine, Qassim University, Buraidah, Saudi Arabia
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COVID-19-Associated Mucormycosis: A Matter of Concern Amid the SARS-CoV-2 Pandemic. Vaccines (Basel) 2022; 10:vaccines10081266. [PMID: 36016154 PMCID: PMC9415927 DOI: 10.3390/vaccines10081266] [Citation(s) in RCA: 1] [Impact Index Per Article: 0.3] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 06/17/2022] [Revised: 08/04/2022] [Accepted: 08/05/2022] [Indexed: 12/16/2022] Open
Abstract
Mucormycosis is an invasive fungal infection caused by fungi belonging to order Mucorales. Recently, with the increase in COVID-19 infections, mucormycosis infections have become a matter of concern globally, because of the high morbidity and mortality rates associated with them. Due to the association of mucormycosis with COVID-19 disease, it has been termed COVID-19-associated mucormycosis (CAM). In the present review, we focus on mucormycosis incidence, pathophysiology, risk factors, immune dysfunction, interactions of Mucorales with endothelial cells, and the possible role of iron in Mucorales growth. We review the limitations associated with current diagnostic procedures and the requirement for more specific, cost-effective, convenient, and sensitive assays, such as PCR-based assays and monoclonal antibody-based assays for the effective diagnosis of mucormycosis. We discuss the current treatment options involving antifungal drug therapies, adjunctive therapy, surgical treatment, and their limitations. We also review the importance of nutraceuticals-based therapy for the prevention as well as treatment of mucormycosis. Our review also highlights the need to explore the potential of novel immunotherapeutics, which include antibody-based therapy, cytokine-based therapy, and combination/synergistic antifungal therapy, as treatment options for mucormycosis. In summary, this review provides a complete overview of COVID-19-associated mucormycosis, addressing the current research gaps and future developments required in the field.
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Seyedjavadi SS, Bagheri P, Nasiri MJ, Razzaghi-Abyaneh M, Goudarzi M. Fungal Infection in Co-infected Patients With COVID-19: An Overview of Case Reports/Case Series and Systematic Review. Front Microbiol 2022; 13:888452. [PMID: 35875562 PMCID: PMC9298665 DOI: 10.3389/fmicb.2022.888452] [Citation(s) in RCA: 29] [Impact Index Per Article: 9.7] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 03/02/2022] [Accepted: 06/03/2022] [Indexed: 01/08/2023] Open
Abstract
Fungal co-infections are frequent in patients with coronavirus disease 2019 (COVID-19) and can affect patient outcomes and hamper therapeutic efforts. Nonetheless, few studies have investigated fungal co-infections in this population. This study was performed to assess the rate of fungal co-infection in patients with COVID-19 as a systematic review. EMBASE, MEDLINE, and Web of Science were searched considering broad-based search criteria associated with COVID-19 and fungal co-infection. We included case reports and case series studies, published in the English language from January 1, 2020 to November 30, 2021, that reported clinical features, diagnosis, and outcomes of fungal co-infection in patients with Severe Acute Respiratory Syndrome Coronavirus 2 (SARS-CoV-2). Totally, 54 case reports and 17 case series were identified, and 181 patients (132 men, 47 women, and 2 not mentioned) co-infected with COVID-19 and fungal infection enrolled. The frequency of fungal co-infection among patients with COVID-19 was 49.7, 23.2, 19.8, 6.6, and 0.5% in Asia, America, Europe, Africa, and Australia, respectively. Diabetes (59.6%) and hypertension (35.9%) were found as the most considered comorbidities in COVID-19 patients with fungal infections. These patients mainly suffered from fever (40.8%), cough (30.3%), and dyspnea (23.7%). The most frequent findings in the laboratory results of patients and increase in C-reactive protein (CRP) (33.1%) and ferritin (18.2%), and lymphopenia (16%) were reported. The most common etiological agents of fungal infections were Aspergillus spp., Mucor spp., Rhizopus spp., and Candida spp. reported in study patients. The mortality rate was 54.6%, and the rate of discharged patients was 45.3%. Remdesivir and voriconazole were the most commonly used antiviral and antifungal agents for the treatment of patients. The global prevalence of COVID-19-related deaths is 6.6%. Our results showed that 54.6% of COVID-19 patients with fungal co-infections died. Thus, this study indicated that fungal co-infection and COVID-19 could increase mortality. Targeted policies should be considered to address this raised risk in the current pandemic. In addition, fungal infections are sometimes diagnosed late in patients with COVID-19, and the severity of the disease worsens, especially in patients with underlying conditions. Therefore, patients with fungal infections should be screened regularly during the COVID-19 pandemic to prevent the spread of the COVID-19 patients with fungal co-infection.
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Affiliation(s)
| | - Parmida Bagheri
- Department of Biotechnology, Faculty of Life Sciences and Biotechnology, Shahid Beheshti University, Tehran, Iran
| | - Mohammad Javad Nasiri
- Department of Microbiology, School of Medicine, Shahid Beheshti University of Medical Sciences, Tehran, Iran
| | | | - Mehdi Goudarzi
- Department of Microbiology, School of Medicine, Shahid Beheshti University of Medical Sciences, Tehran, Iran
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Current Treatment Options for COVID-19 Associated Mucormycosis: Present Status and Future Perspectives. J Clin Med 2022; 11:jcm11133620. [PMID: 35806905 PMCID: PMC9267579 DOI: 10.3390/jcm11133620] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 03/11/2022] [Revised: 05/12/2022] [Accepted: 05/17/2022] [Indexed: 12/04/2022] Open
Abstract
Mucormycosis has become increasingly associated with COVID-19, leading to the use of the term “COVID-19 associated mucormycosis (CAM)”. Treatment of CAM is challenging due to factors such as resistance to many antifungals and underlying co-morbidities. India is particularly at risk for this disease due to the large number of patients with COVID-19 carrying comorbidities that predispose them to the development of mucormycosis. Additionally, mucormycosis treatment is complicated due to the atypical symptoms and delayed presentation after the resolution of COVID-19. Since this disease is associated with increased morbidity and mortality, early identification and diagnosis are desirable to initiate a suitable combination of therapies and control the disease. At present, the first-line treatment involves Amphotericin B and surgical debridement. To overcome limitations associated with surgery (invasive, multiple procedures required) and amphotericin B (toxicity, extended duration and limited clinical success), additional therapies can be utilized as adjuncts or alternatives to reduce treatment duration and improve prognosis. This review discusses the challenges associated with treating CAM and the critical aspects for controlling this invasive fungal infection—early diagnosis and initiation of therapy, reversal of risk factors, and adoption of a multipronged treatment strategy. It also details the various therapeutic options (in vitro, in vivo and human case reports) that have been used for the treatment of CAM.
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17
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Donovan MR, Miglani A, Lal D, Marino MJ. Factors associated with invasive fungal sinusitis in patients with
COVID
‐19: A systematic review and single‐center case series. Laryngoscope Investig Otolaryngol 2022; 7:913-919. [PMID: 35942423 PMCID: PMC9350302 DOI: 10.1002/lio2.833] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 05/06/2022] [Accepted: 05/24/2022] [Indexed: 11/30/2022] Open
Abstract
Objective Invasive fungal sinusitis (IFS) in patients with active or recent COVID‐19 have been reported throughout the world. The primary purpose of the systematic review is to describe factors associated with IFS in patients with COVID‐19. The goal of the case series was to also characterize these factors in addition to evaluating the incidence of IFS at our institution after the onset of the pandemic. Methods A systematic review using the preferred reporting in systematic reviews and meta‐analyses (PRISMA) framework identified publications of IFS cases associated with COVID‐19 (IFSAC). Search terms were “COVID‐19,” “invasive,” “fungal,” and “sinusitis.” IFS cases were evaluated for COVID‐19 status, fungal etiology, comorbidities, treatment, and outcome. A case series of patients at our center with IFS between December 1, 2018 to March 31, 2020 (“pre‐covid”) and April 1, 2020 to August 1, 2021 (“post‐covid”) was also performed with the above parameters. Results Fourteen studies totaling 206 cases of IFSAC were identified. Most cases came from India (140/206, 68.0%), followed by Egypt (62/206, 30.1%), and North America (4/206, 1.9%). Diabetes was the most common comorbidity (151/206, 73.3%). Recent or prolonged steroid use was noted in 65.0% of cases (134/206). In our series, five pre‐covid and four post‐covid cases were identified. One had recent COVID‐19 infection. Acute myeloid leukemia was the most common pre‐covid comorbidity (3/5, 60.0%). Diabetes was the most frequent post‐covid comorbidity (2/4, 50.0%). Chronic steroid usage was noted in two pre‐covid and one post‐covid cases. Conclusion Diabetes and steroid use are common factors in reported cases of IFSAC. IFS incidence in our case series did not change appreciably after the onset of the pandemic. Level of Evidence: 4.
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Affiliation(s)
| | - Amar Miglani
- Department of Otorhinolaryngology—Head and Neck Surgery, Mayo Clinic College of Medicine Phoenix Arizona USA
| | - Devyani Lal
- Department of Otorhinolaryngology—Head and Neck Surgery, Mayo Clinic College of Medicine Phoenix Arizona USA
| | - Michael J. Marino
- Department of Otorhinolaryngology—Head and Neck Surgery, Mayo Clinic College of Medicine Phoenix Arizona USA
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Vitale RG, Afeltra J, Seyedmousavi S, Giudicessi SL, Romero SM. An overview of COVID-19 related to fungal infections: what do we know after the first year of pandemic? Braz J Microbiol 2022; 53:759-775. [PMID: 35315001 PMCID: PMC8936386 DOI: 10.1007/s42770-022-00704-6] [Citation(s) in RCA: 2] [Impact Index Per Article: 0.7] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Download PDF] [Journal Information] [Subscribe] [Scholar Register] [Received: 09/11/2021] [Accepted: 02/01/2022] [Indexed: 02/07/2023] Open
Abstract
In 2019, severe acute respiratory syndrome caused by CoV-2 virus became a pandemic worldwide, being the fast spread of the disease due to the movement of infected people from one country to another, from one continent to another, or within the same country. Associated comorbidities are important factors that predispose to any fungal coinfections. Because of the importance of fungal infections in COVID-19 patients, the aim of this work was to collect data of the more encountered mycoses related to patients undergoing this disease. Aspergillosis was the first COVID-19-related fungal infection reported, being A. fumigatus the most frequent species for CAPA. Other fungal infections related include mainly candidiasis and mucormycosis, being Rhizopus spp. the more prevalent species found. Influenza-associated pulmonary aspergillosis is well documented; thus, similar complications are expected in severe forms of COVID-19 pneumonia. Therefore, in patients with COVID-19, it is important to take special attention to the surveillance and suspicion of fungal coinfections that might worsen the patient's prognosis.
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Affiliation(s)
- R G Vitale
- Consejo Nacional de Investigaciones Científicas Y Tecnológicas (CONICET), Buenos Aires, Argentina.
- Unidad de Parasitología. Sector Micología. Hospital J.M. Ramos Mejía, Buenos Aires, Argentina.
| | - J Afeltra
- Unidad de Parasitología. Sector Micología. Hospital J.M. Ramos Mejía, Buenos Aires, Argentina
| | - S Seyedmousavi
- Microbiology Service, Department of Laboratory Medicine, Clinical Center, National Institutes of Health, Bethesda, MD, USA
| | - S L Giudicessi
- Facultad de Farmacia Y Bioquímica, Cátedra de Biotecnología, Universidad de Buenos Aires (UBA), Buenos Aires, Argentina
- Instituto de Nanobiotecnología (NANOBIOTEC), CONICET-UBA, Buenos Aires, Argentina
| | - S M Romero
- Consejo Nacional de Investigaciones Científicas Y Tecnológicas (CONICET), Buenos Aires, Argentina
- Instituto Multidisciplinario de Biología Vegetal (IMBIV), CONICET, FCEFyN, Universidad Nacional de Córdoba, Córdoba, Argentina
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García-Carnero LC, Mora-Montes HM. Mucormycosis and COVID-19-Associated Mucormycosis: Insights of a Deadly but Neglected Mycosis. J Fungi (Basel) 2022; 8:445. [PMID: 35628701 PMCID: PMC9144279 DOI: 10.3390/jof8050445] [Citation(s) in RCA: 9] [Impact Index Per Article: 3.0] [Reference Citation Analysis] [Abstract] [Key Words] [Grants] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 03/28/2022] [Revised: 04/22/2022] [Accepted: 04/22/2022] [Indexed: 02/04/2023] Open
Abstract
The ongoing COVID-19 pandemic has quickly become a health threat worldwide, with high mortality and morbidity among patients with comorbidities. This viral infection promotes the perfect setting in patients for the development of opportunistic infections, such as those caused by fungi. Mucormycosis, a rare but deadly fungal infection, has recently increased its incidence, especially in endemic areas, since the onset of the pandemic. COVID-19-associated mucormycosis is an important complication of the pandemic because it is a mycosis hard to diagnose and treat, causing concern among COVID-19-infected patients and even in the already recovered population. The risk factors for the development of mucormycosis in these patients are related to the damage caused by the SARS-CoV-2 itself, the patient's overstimulated immune response, and the therapy used to treat COVID-19, causing alterations such as hyperglycemia, acidosis, endothelial and lung damage, and immunosuppression. In this review, the molecular aspects of mucormycosis and the main risk factors for the development of COVID-19-associated mucormycosis are explained to understand this virus-fungi-host interaction and highlight the importance of this neglected mycosis.
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Affiliation(s)
- Laura C. García-Carnero
- Departamento de Biología, División de Ciencias Naturales y Exactas, Campus Guanajuato, Universidad de Guanajuato, Noria Alta s/n, col. Noria Alta, C.P., Guanajuato 36050, Mexico
| | - Héctor M. Mora-Montes
- Departamento de Biología, División de Ciencias Naturales y Exactas, Campus Guanajuato, Universidad de Guanajuato, Noria Alta s/n, col. Noria Alta, C.P., Guanajuato 36050, Mexico
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Veerabathula P, Singh S, Koshy PG, Dave TV, Rao RN, Naik MN. Local Infiltration Anesthesia for Orbital Exenteration in Patients With Rhino-Orbital Cerebral Mucormycosis: A Case Series. A A Pract 2022; 16:e01581. [PMID: 35421003 DOI: 10.1213/xaa.0000000000001581] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 11/05/2022]
Abstract
Orbital exenteration is occasionally required for rhino-orbital cerebral mucormycosis. Multiple associated comorbidities can pose a risk for general anesthesia. There is only 1 report of exenteration being performed under trigeminal nerve block. We describe 5 patients who underwent orbital exenteration under local infiltration anesthesia with sedation. Patients and surgeons reported satisfactory conditions, with stable hemodynamics and successful day care management. Orbital exenteration under local infiltration anesthesia can be a safe and effective alternative for patients with rhino-orbital mucormycosis who are at risk with use of general anesthesia.
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Affiliation(s)
| | - Swati Singh
- Ophthalmic Plastic Surgery Service, LV Prasad Eye Institute, Hyderabad, India
| | | | - Tarjani Vivek Dave
- Ophthalmic Plastic Surgery Service, LV Prasad Eye Institute, Hyderabad, India
| | | | - Milind N Naik
- Ophthalmic Plastic Surgery Service, LV Prasad Eye Institute, Hyderabad, India
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21
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Kundu R, Singla N. COVID-19 and Plethora of Fungal Infections. CURRENT FUNGAL INFECTION REPORTS 2022; 16:47-54. [PMID: 35432691 PMCID: PMC8994097 DOI: 10.1007/s12281-022-00432-2] [Citation(s) in RCA: 5] [Impact Index Per Article: 1.7] [Reference Citation Analysis] [Abstract] [Track Full Text] [Download PDF] [Journal Information] [Subscribe] [Scholar Register] [Accepted: 03/23/2022] [Indexed: 12/15/2022]
Abstract
Purpose of Review Severe-acute respiratory coronavirus 2 (SARS-CoV-2) causing corona virus disease 2019 (COVID-19) has been the single most important pathogen driving health care delivery system for the last one and half years. Now, as the time is passing, many issues related to co-infections/secondary infections/superinfections in COVID-19 patients are emerging. The literature is getting enriched everyday by addition of reports from all over the world for the same. The purpose of this review is to decipher the plethora of fungal infections in COVID-19. Recent Findings COVID-19 infection along with it brought many risk factors namely lung injury, immunosuppression, need for oxygen therapy, monoclonal antibodies, steroid therapy, etc. which are known predisposing factors for fungal infections. Rather the extent and severity of fungal pathogens has been so much that it has led to new terminologies like CAC (COVID-19-associated Candida), CAPA (COVID-19-associated pulmonary aspergillosis) and CAM (COVID-19-associated mucormycosis). There is increase in invasiveness of Candida, prevalence of aspergillosis in COVID-19 damaged lung and outbreak of mucormycosis in COVID-19 patients resulting in “double trouble,” keeping laboratory personnel, clinicians, and intensivists on their toes in managing these patients. Summary Awareness and understanding regarding these possible complications is necessary to decrease the morbidity and mortality among patients. The COVID-19 and fungal coinfections may bring more insight into ways of pathogenesis of fungal infections, need for better antifungal agents, quick diagnostic modalities, and better management policies in the near future.
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Affiliation(s)
- Reetu Kundu
- Department of Cytology and Gynecological Pathology, Post Graduate Institute of Medical Education and Research (PGIMER), Chandigarh, India
| | - Nidhi Singla
- Department of Microbiology, Government Medical College Hospital, Chandigarh, India
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22
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Azhar A, Khan WH, Khan PA, Alhosaini K, Owais M, Ahmad A. Mucormycosis and COVID-19 pandemic: Clinical and diagnostic approach. J Infect Public Health 2022; 15:466-479. [PMID: 35216920 PMCID: PMC8855610 DOI: 10.1016/j.jiph.2022.02.007] [Citation(s) in RCA: 13] [Impact Index Per Article: 4.3] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 09/08/2021] [Revised: 02/08/2022] [Accepted: 02/17/2022] [Indexed: 01/08/2023] Open
Abstract
The pandemic caused by severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) is yet to be controlled worldwide, especially in India. The second wave of coronavirus disease 2019 (COVID-19) led to panic and confusion in India, owing to the overwhelming number of the population that fell prey to this highly infectious virus of recent times. In the second wave of COVID-19, the patients had to fight both the virus and opportunistic infections triggered by fungi and bacteria. Repeated use of steroids, antibiotics, and oxygen masks during the management of severely and critically ill COVID-19 patients nurtured opportunistic infections such as mucormycosis. Despite mucormycosis being a decades-old disease, it has gained notice of its widespread occurrence in COVID-19 patients throughout India. Instances of mucormycosis are usually unearthed in immunocompromised individuals and are caused by the inhalation of filamentous fungi, either from the natural environment or through supportive care units. In the recent outbreak during the second wave of COVID-19 in India, it has been seen to cause secondary infection as it grows along with the treatment of COVID-19. Furthermore, COVID-19 patients with comorbidities such as diabetes were more likely to have the mucormycosis co-infection because of their challenged immune systems' inability to fight it. Despite the hype, mucormycosis still remains neglected and least studied, which is predominantly due to all focus on diagnostics, vaccine, and therapeutic research. In this review, we emphasize mainly on the association of mucormycosis in COVID-19 patients. We also present the molecular mechanism of mucormycosis for a better understanding of the fungal infections in patients who have recently been infected with SARS-CoV-2. Better understanding of fungal pathogens, immediate diagnosis, and management of the infections are crucial in COVID-19 patients, as high mortalities have been recorded in co-infected patients despite recovery from COVID-19.
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Affiliation(s)
- Asim Azhar
- Interdisciplinary Biotechnology Unit, Aligarh Muslim University, Aligarh, Uttar Pradesh, India.
| | - Wajihul Hasan Khan
- Department of Chemical Engineering, Indian Institute of Technology Delhi, New Delhi, India; Department of Microbiology, All India Institute of Medical Sciences, New Delhi, India
| | - Parvez Anwar Khan
- Department of Microbiology, Jawaharlal Nehru Medical College, Aligarh Muslim University Aligarh, Uttar Pradesh, India
| | - Khaled Alhosaini
- Department of Pharmacology & Toxicology, College of Pharmacy, King Saud University, Post Box 2457, Riyadh 11451, Saudi Arabia
| | - Mohammad Owais
- Interdisciplinary Biotechnology Unit, Aligarh Muslim University, Aligarh, Uttar Pradesh, India
| | - Aijaz Ahmad
- Clinical Microbiology and Infectious Diseases, School of Pathology, Health Sciences, University of the Witwatersrand, Johannesburg 2193, South Africa; Infection Control, Charlotte Maxeke Johannesburg Academic Hospital, National Health Laboratory Service, Johannesburg 2193, South Africa.
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23
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Risk Factors for COVID-19 Associated Mucormycosis: The Ophthalmologist’s Perspective. J Fungi (Basel) 2022; 8:jof8030271. [PMID: 35330273 PMCID: PMC8948853 DOI: 10.3390/jof8030271] [Citation(s) in RCA: 5] [Impact Index Per Article: 1.7] [Reference Citation Analysis] [Abstract] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 01/17/2022] [Revised: 03/03/2022] [Accepted: 03/07/2022] [Indexed: 02/04/2023] Open
Abstract
The COVID-19 pandemic has led to a dramatic rise in the incidence of rhino-orbito-cerebral mucormycosis (ROCM) in India. The purpose of our report is to describe the prevalence of ROCM in the context of SARS-CoV-2 infection during the second Indian COVID-19 wave, as well as its diagnostics proceeding, and to discuss the challenges met in the time frame from the suspected diagnosis to the therapeutic decision in such patients. We conducted a retrospective multicentre case series study at six centres of Sudhalkar and Raghudeep group of hospitals in India. ROCM was confirmed in 38 (2.5%) of the 1546 patients admitted with SARS-CoV-2 infection. The average time to establish a diagnosis was 16 days. In total, 19 (50%) patients suffered from type 2 diabetes and were mostly treated with hypoglycaemic agents (in 90% of cases). The standard of care for SARS-CoV-2 management included systemic steroids therapy, intravenous remdesivir for 5 days, and concomitant prophylactic antibiotic therapy following admission. The median (IQR) blood glucose levels in all patients during the course of hospitalisation was 320 (250.5–375) mg/dl. A total of 16% of patients had an irreparable functional loss, and the mortality was 5%. We may hypothesise that excessive administration of antibiotics that profoundly affects human microbiota, coupled with poorly controlled glycaemia and unprotocolised haphazard steroid administration, contribute to a favourable setting for mucormycosis infections.
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24
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Samaranayake LP, Fakhruddin KS, Ngo HC, Bandara MHMN, Leung YY. Oro-facial Mycoses in Coronavirus Disease-2019 (COVID-19): A Systematic Review. Int Dent J 2022; 72:607-620. [PMID: 35367044 PMCID: PMC8885299 DOI: 10.1016/j.identj.2022.02.010] [Citation(s) in RCA: 5] [Impact Index Per Article: 1.7] [Reference Citation Analysis] [Abstract] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 02/09/2022] [Revised: 02/21/2022] [Accepted: 02/22/2022] [Indexed: 12/22/2022] Open
Abstract
Objectives Studies reviewing orofacial mycoses in coronavirus disease-2019 (COVID-19) caused by severe acute respiratory syndrome 2 (SARS-CoV-2) infection are sparse. Here we review the major oral and maxillofacial mycoses of COVID-19, the associated comorbidities, and the probable precipitating factors. Methods English-language manuscripts published between March 2020 and October 2021 were searched using PubMed, OVID, SCOPUS, and Web of Science databases, using appropriate keywords. Results We identified 30 articles across 14 countries, which met the inclusion criteria of PRISMA guidelines. These yielded a total of 292 patients with laboratory-confirmed COVID-19, 51.4% (n = 150) of whom presented with oral and maxillofacial fungal infections, mainly comprising candidosis, mucormycosis, and aspergillosis. Candida infections were the most prevalent, present in 64% (n = 96), followed by mucormycosis, and only a single case of aspergillosis was noted. Oral and maxillofacial mycoses were predominantly seen in those with comorbidities, especially in those with diabetes (52.4%). Oral mucormycosis was noted in 8.6% (n = 13) and mainly manifested on the hard palate. An overall event rate of oral/maxillofacial mucormycosis manifestation in patients with COVID-19 with diabetes mellitus type 1/2 was about 94% (49/52; 95% confidence interval, 0.73%-0.89%), implying a very high association between diabetes mellitus and the latter condition. All fungal infections appeared either concurrently with COVID-19 symptoms or during the immediate recovery period. Conclusions SARS-CoV-2 infection–related immunosuppression, steroid therapy, as well as comorbidities such as diabetic hyperglycemia appear to be the major predisposing factors for the onset of oral and maxillofacial mycoses in patients with COVID-19 across all age groups.
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Kandasamy S, Muthuraju S, Vasugi A, Chandrasekar M, Murugan R, Inbasekaran P, R P. Clinicopathological Study of Mucormycosis in COVID-19 Patients: Experience From a Tertiary Care Center in South India. Cureus 2022; 14:e23016. [PMID: 35419223 PMCID: PMC8994129 DOI: 10.7759/cureus.23016] [Citation(s) in RCA: 2] [Impact Index Per Article: 0.7] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Accepted: 03/09/2022] [Indexed: 12/24/2022] Open
Abstract
Background: The coronavirus disease 2019 (COVID-19) pandemic has taken the world to different dimensions. With the surge of the second wave in India, the number of cases with mucormycosis has increased. Mucormycosis is a potentially life-threatening, opportunistic, invasive, fungal infection that can occur in immunocompromised states. The aim of the study is to analyze the clinicopathological parameters of patients with mucormycosis in the surge of the second wave of COVID-19. Materials and Methods: All cases of mucormycosis reported in the Department of Pathology in a tertiary care centre in South India from March 2021 to June 2021 were included in the study. The patient details were retrieved from the Medical Records section. The patient characteristics, location, associated comorbidities, management and treatment outcomes were analyzed and compared to similar studies reported worldwide. Results: Of 58 cases, 38 (65%) were males and 20 (35%) were females. The ages ranged from 34 to 77 years. Severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) was detected in 46 patients in reverse transcription polymerase chain reaction (RT-PCR) with high-resolution computed tomography (HRCT) Chest changes noted in 54 patients. Associated comorbidities were noted in 52 patients, with uncontrolled diabetes mellitus (46 patients; 88%) being the most common. Location was commonly in nasal and paranasal sinuses (43%), followed by orbital (2%), cerebral (10%) and pulmonary (8%) areas. Among the paranasal sinuses, the maxillary sinus was commonly involved. Mixed fungal infections (Aspergillus sp. and Candida sp.) were noted in eight (14%) cases. Oxygen therapy was given in 85% of cases; 30% of cases needed ventilator support; corticosteroid therapy was initiated in 49 patients, tocilizumab in six patients as treatment for mucormycosis. Amphotericin B was administered in 59% of patients based on clinical findings alone. After histopathological confirmation, 90% of them received amphotericin. Functional endoscopic sinus surgery (FESS) was done in 96% of cases, among them 45% underwent extensive surgical debridement and 15% underwent orbital decompression. Orbital exenteration (2%) was the other modality of management. Conclusion: Detailed analysis of clinicopathological features suggests the possibilities of immunosuppression (due to diabetes and use of corticosteroids in treatment of COVID-19) and COVID-19 (endothelial damage, cytokine storm) being the pathogenesis associated with the sudden surge of mucormycosis.
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Affiliation(s)
- Sangeetha Kandasamy
- Pathology, Vinayaka Missions Kirupananda Variyar Medical College & Hospitals, Salem, IND
| | | | - Arumugam Vasugi
- Pathology, Sri Ramachandra Institute of Higher Education and Research (SRIHER), Chennai, IND
| | - Megala Chandrasekar
- Pathology, Vinayaka Missions Kirupananda Variyar Medical College & Hospitals, Salem, IND
| | - Roopmala Murugan
- Pathology, Vinayaka Missions Kirupananda Variyar Medical College & Hospitals, Salem, IND
| | - Poovizhi Inbasekaran
- Pathology, Vinayaka Missions Kirupananda Variyar Medical College & Hospitals, Salem, IND
| | - Prabu R
- General Internal Medicine, Vinayaka Missions Kirupananda Variyar Medical College & Hospitals, Salem, IND
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26
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Dravid A, Kashiva R, Khan Z, Bande B, Memon D, Kodre A, Mane M, Pawar V, Patil D, Kalyani S, Raut P, Bapte M, Saldanha C, Chandak D, Patil T, Reddy MS, Bhayani K, Laxmi SS, Vishnu PD, Srivastava S, Khandelwal S, More S, Shakeel A, Pawar M, Nande P, Harshe A, Kadam S, Hallikar S, Kamal N, Andrabi D, Bodhale S, Raut A, Chandrashekhar S, Raman C, Mahajan U, Joshi G, Mane D. Epidemiology, clinical presentation and management of COVID-19 associated mucormycosis: A single center experience from Pune, Western India. Mycoses 2022; 65:526-540. [PMID: 35212032 PMCID: PMC9115310 DOI: 10.1111/myc.13435] [Citation(s) in RCA: 2] [Impact Index Per Article: 0.7] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 09/16/2021] [Revised: 02/17/2022] [Accepted: 02/22/2022] [Indexed: 12/15/2022]
Abstract
Background The second COVID‐19 wave in India has been associated with an unprecedented increase in cases of COVID‐19 associated mucormycosis (CAM), mainly Rhino‐orbito‐cerebral mucormycosis (ROCM). Methods This retrospective cohort study was conducted at Noble hospital and Research Centre (NHRC), Pune, India, between 1 April, 2020, and 1 August, 2021, to identify CAM patients and assess their management outcomes. The primary endpoint was incidence of all‐cause mortality due to CAM. Results 59 patients were diagnosed with CAM. Median duration from the first positive COVID‐19 RT PCR test to diagnosis of CAM was 17 (IQR: 12,22) days. 90% patients were diabetic with 89% having uncontrolled sugar level (HbA1c >7%). All patients were prescribed steroids during treatment for COVID‐19. 56% patients were prescribed steroids for non‐hypoxemic, mild COVID‐19 (irrational steroid therapy), while in 9%, steroids were prescribed in inappropriately high dose. Patients were treated with a combination of surgical debridement (94%), intravenous liposomal Amphotericin B (91%) and concomitant oral Posaconazole (95.4%). 74.6% patients were discharged after clinical and radiologic recovery while 25.4% died. On relative risk analysis, COVID‐19 CT severity index ≥18 (p = .017), presence of orbital symptoms (p = .002), presence of diabetic ketoacidosis (p = .011) and cerebral involvement (p = .0004) were associated with increased risk of death. Conclusions CAM is a rapidly progressive, angio‐invasive, opportunistic fungal infection, which is fatal if left untreated. Combination of surgical debridement and antifungal therapy leads to clinical and radiologic improvement in majority of cases.
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Affiliation(s)
- Ameet Dravid
- Department of Infectious diseases and HIV/AIDS, Noble hospitals and Research Centre, Pune, Maharashtra, India
| | - Reema Kashiva
- Department of Medicine, Noble hospital and Research Centre, Pune, Maharashtra, India
| | - Zafer Khan
- Department of Critical Care Medicine, Noble hospital and Research Centre, Pune, Maharashtra, India
| | - Balasaheb Bande
- Department of Critical Care Medicine, Noble hospital and Research Centre, Pune, Maharashtra, India
| | - Danish Memon
- Department of Medicine, Noble hospital and Research Centre, Pune, Maharashtra, India
| | - Aparna Kodre
- Department of Medicine, Noble hospital and Research Centre, Pune, Maharashtra, India
| | - Milind Mane
- Department of Critical Care Medicine, Noble hospital and Research Centre, Pune, Maharashtra, India
| | - Vishal Pawar
- Department of Critical Care Medicine, Noble hospital and Research Centre, Pune, Maharashtra, India
| | - Dattatraya Patil
- Department of Critical Care Medicine, Noble hospital and Research Centre, Pune, Maharashtra, India
| | - Suraj Kalyani
- Department of Critical Care Medicine, Noble hospital and Research Centre, Pune, Maharashtra, India
| | - Prathamesh Raut
- Department of Critical Care Medicine, Noble hospital and Research Centre, Pune, Maharashtra, India
| | - Madhura Bapte
- Department of Critical Care Medicine, Noble hospital and Research Centre, Pune, Maharashtra, India
| | - Charlotte Saldanha
- Department of Critical Care Medicine, Noble hospital and Research Centre, Pune, Maharashtra, India
| | - Dinesh Chandak
- Department of Critical Care Medicine, Noble hospital and Research Centre, Pune, Maharashtra, India
| | - Teerthagouda Patil
- Department of Critical Care Medicine, Noble hospital and Research Centre, Pune, Maharashtra, India
| | - M Sateesh Reddy
- Department of Medicine, Noble hospital and Research Centre, Pune, Maharashtra, India
| | - Krushnadas Bhayani
- Department of Medicine, Noble hospital and Research Centre, Pune, Maharashtra, India
| | - S S Laxmi
- Department of Medicine, Noble hospital and Research Centre, Pune, Maharashtra, India
| | - P D Vishnu
- Department of Medicine, Noble hospital and Research Centre, Pune, Maharashtra, India
| | - Shipra Srivastava
- Department of Medicine, Noble hospital and Research Centre, Pune, Maharashtra, India
| | - Shubham Khandelwal
- Department of Medicine, Noble hospital and Research Centre, Pune, Maharashtra, India
| | - Sailee More
- Department of Medicine, Noble hospital and Research Centre, Pune, Maharashtra, India
| | - Atif Shakeel
- Department of Medicine, Noble hospital and Research Centre, Pune, Maharashtra, India
| | - Mohit Pawar
- Department of Medicine, Noble hospital and Research Centre, Pune, Maharashtra, India
| | - Pranava Nande
- Department of Medicine, Noble hospital and Research Centre, Pune, Maharashtra, India
| | - Amol Harshe
- Department of Pathology, Noble hospital and Research Centre, Pune, Maharashtra, India
| | - Sagar Kadam
- Department of Radiology, Noble hospital and Research Centre, Pune, Maharashtra, India
| | - Sudhir Hallikar
- Department of Otorhinolaryngology, Noble hospital and Research Centre, Pune, Maharashtra, India
| | - Nudrat Kamal
- Department of Otorhinolaryngology, Noble hospital and Research Centre, Pune, Maharashtra, India
| | - Danish Andrabi
- Department of Otorhinolaryngology, Noble hospital and Research Centre, Pune, Maharashtra, India
| | - Sachin Bodhale
- Department of Ophthalmology, Noble hospital and Research Centre, Pune, Maharashtra, India
| | - Akshay Raut
- Department of Maxillo-facial surgery, Noble hospital and Research Centre, Pune, Maharashtra, India
| | | | - Chandrashekhar Raman
- Department of Neurosurgery, Noble hospital and Research Centre, Pune, Maharashtra, India
| | - Uma Mahajan
- Statistician, VMK Diagnostics private limited, Pune, Maharashtra, India
| | - Gaurav Joshi
- Independent statistical consultant, Chicago, USA
| | - Dilip Mane
- Department of Medicine, Noble hospital and Research Centre, Pune, Maharashtra, India
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27
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Nagalli S, Kikkeri NS. Mucormycosis in COVID-19: A systematic review of literature. LE INFEZIONI IN MEDICINA 2022; 29:504-512. [PMID: 35146358 DOI: 10.53854/liim-2904-2] [Citation(s) in RCA: 10] [Impact Index Per Article: 3.3] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Subscribe] [Scholar Register] [Received: 10/01/2021] [Accepted: 10/20/2021] [Indexed: 11/03/2022]
Abstract
Coronavirus disease 2019 (COVID-19) is an acute viral illness caused by severe acute respiratory syndrome coronavirus-2 (SARS-CoV-2). Opportunistic infections such as mucormycosis have been reported among COVID-19 patients particularly in South Asian countries during the second wave of this pandemic. It is necessary to re-evaluate any changes in traditional risk factors associated with mucormycosis such as diabetes mellitus, organ transplant, etc in the precedent of ongoing COVID-19 pandemic. We conducted a systematic review using electronic databases. A total of 115 COVID-19 patients who were diagnosed with mucormycosis were included in this study. Diabetes mellitus was the most common co-morbidity with 77.1%, followed by hypertension (29.5%) and renal disease (14.3%). 55.2% of the patients had received dexamethasone for COVID-19 infection. Ten patients (11.5%) had received tocilizumab. Sinuses were the most common site of mucormycosis among COVID-19 patients at 79.4% with maxillary sinus (47.4%) being most commonly infected. Orbits were the second most prevalent site at 56.7% and lungs were infected with mucor at 11.3%. The mean duration between the diagnosis of COVID-19 infection and mucormycosis was 16.15 days (range 2-90 days). Cavernous sinus was either infiltrated or encased in 14 patients (14.4%). Cerebral involvement was seen in terms of abscess, infarcts, or edema in 12 patients (12.4%). Only 76 patients had data on the outcomes, out of which 37 (48.7%) patients had died. Diabetes mellitus is still the most common co-morbidity similar to non-COVID-19 patients. More than 90% of the patients with COVID-19 infection had received steroids. Complications such as cavernous sinus thrombosis, cerebral infarcts, abscesses were common. Indiscriminate use of steroids in patients needs to be avoided and focus needs to be put on tight blood sugar control in diabetic patients. Studies are needed to confirm the role of the SARS-CoV-2 virus in causing immune dysfunction and mucormycosis.
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Affiliation(s)
- Shivaraj Nagalli
- Department of Internal Medicine, Brookwood Baptist Health, Alabaster, USA
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28
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Chao CM, Lai CC, Yu WL. COVID-19 associated mucormycosis - An emerging threat. JOURNAL OF MICROBIOLOGY, IMMUNOLOGY, AND INFECTION = WEI MIAN YU GAN RAN ZA ZHI 2022; 55:183-190. [PMID: 35074291 PMCID: PMC8755409 DOI: 10.1016/j.jmii.2021.12.007] [Citation(s) in RCA: 18] [Impact Index Per Article: 6.0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Subscribe] [Scholar Register] [Received: 07/27/2021] [Revised: 11/22/2021] [Accepted: 12/29/2021] [Indexed: 02/06/2023]
Abstract
Coronavirus disease 2019 (COVID-19) caused by severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) rapidly become a global threaten since its emergence in the end of 2019. Moreover, SARS-CoV-2 infection could also present with co-infection or secondary infection by other virus, bacteria, or fungi. Among them, mucormycosis is a rare but aggressive fungal disease and it mainly affects patients particularly with poorly controlled diabetes mellitus with diabetic ketoacidosis (DKA). We here did a comprehensive review of literature reporting COVID-19 associated with mucormycosis (CAM) cases, which have been reported worldwide. The prevalence is higher in India, Iran, and Egypt than other countries, particularly highest in the states of Gujarat and Maharashtra in India. Poor diabetic control and the administration of systemic corticosteroids are the common precipitating factors causing mucormycosis in the severe and critical COVID-19 patients. In addition, COVID-19 itself may affect the immune system resulting in vulnerability of the patients to mucormycosis. Appropriate treatments of CAM include strict glycemic control, extensive surgical debridement, and antifungal therapy with amphotericin B formulations.
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Affiliation(s)
- Chien-Ming Chao
- Department of Intensive Care Medicine, Chi Mei Medical Center, Liouying, Tainan, 73657, Taiwan; Department of Dental Laboratory Technology, Min-Hwei College of Health Care Management, Tainan, 73657, Taiwan.
| | - Chih-Cheng Lai
- Department of Internal Medicine, Kaohsiung Veterans General Hospital, Tainan Branch, Tainan, 71051, Taiwan.
| | - Wen-Liang Yu
- Department of Intensive Care Medicine, Chi Mei Medical Center, Tainan, 71004, Taiwan; Department of Medicine, School of Medicine, College of Medicine, Taipei Medical University, Taipei, 11031, Taiwan.
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29
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Ghosh D, Dey S, Chakraborty H, Mukherjee S, Halder A, Sarkar A, Chakraborty P, Ghosh R, Sarkar J. Mucormycosis: A new threat to Coronavirus disease 2019 with special emphasis on India. CLINICAL EPIDEMIOLOGY AND GLOBAL HEALTH 2022; 15:101013. [PMID: 35342843 PMCID: PMC8934183 DOI: 10.1016/j.cegh.2022.101013] [Citation(s) in RCA: 7] [Impact Index Per Article: 2.3] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 09/07/2021] [Revised: 12/10/2021] [Accepted: 03/10/2022] [Indexed: 01/03/2023] Open
Abstract
The main reason for the growth of mucormycosis in people with Coronavirus disease-2019 (COVID-19) is mainly produced by Rhizopus spp. The infective mechanisms and issues recognized in Rhizopus spp. are the cell wall, germination proteins, and enzymes assisted to iron sequestration, CotH protein, and positive regulation of the GRP78 cell receptor. Mucormycosis is mainly caused by the Rhizopus spp. such as R. oryzae, R. microsporus, R. arrhizus, R. homothallicus, etc. that are gifted to numerous host defense mechanisms and attribute to the endothelium via specific receptors, GRP78 simplifying their endocytosis and angio-invasion. Factors such as hyperglycemia, elevated iron concentrations, and ketoacidosis have been shown to contribute to the pathogenesis in the tentative situation. The analytical data of 'black fungus disease' or 'mucormycosis', specify India reported for about 42.3% of published cases, followed by the USA about 16.9%, Iraq, Bangladesh, Iran, Paraguay, and 1 case each from Brazil, Mexico, Italy, UK, China, France, Uruguay, Turkey, and Austria. The COVID-19 infection is maybe a predisposing factor for mucormycosis and is related to a high mortality rate. Early recognition and restriction of hyperglycemia, liposomal amphotericin B, and surgical debridement are the bases in the successful managing of mucormycosis.
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Affiliation(s)
- Deganta Ghosh
- Department of Botany, Dinabandhu Andrews College, Garia, Kolkata, West Bengal, India, 700084
| | - Sagardeep Dey
- Department of Botany, Dinabandhu Andrews College, Garia, Kolkata, West Bengal, India, 700084
| | - Himanko Chakraborty
- Department of Botany, Dinabandhu Andrews College, Garia, Kolkata, West Bengal, India, 700084
| | - Sneha Mukherjee
- Department of Botany, Dinabandhu Andrews College, Garia, Kolkata, West Bengal, India, 700084
| | - Ankita Halder
- Department of Botany, Dinabandhu Andrews College, Garia, Kolkata, West Bengal, India, 700084
| | - Akash Sarkar
- Department of Botany, Dinabandhu Andrews College, Garia, Kolkata, West Bengal, India, 700084
| | - Pallab Chakraborty
- Department of Botany, Acharya Prafulla Chandra College, New Barrakpur, Kolkata, West Bengal, India, 700131
| | - Rajdeep Ghosh
- GSL Medical College and General Hospital, Rajahmundry, Andhra Pradesh, India, 533296
| | - Joy Sarkar
- Department of Botany, Dinabandhu Andrews College, Garia, Kolkata, West Bengal, India, 700084,Corresponding author
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Ray SK, Mukherjee S. COVID-19-Associated Mucormycosis, A New Incident in Recent Time: Is An Emerging Disease in The Near Future Impending? Avicenna J Med 2021; 11:210-216. [PMID: 34881204 PMCID: PMC8648408 DOI: 10.1055/s-0041-1735383] [Citation(s) in RCA: 3] [Impact Index Per Article: 0.8] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 11/01/2022] Open
Abstract
Mucormycosis (also known as black fungus) is caused by fungi of the Zygomycetes class and is the third most common invasive mycosis after candidiasis and aspergillosis. They colonize a large number of patients without invading them. Systemic glucocorticoids are currently used to treat severe Coronavirus disease 19 (COVID-19). In such patients, opportunistic fungal infections are a problem. Although COVID-19-related pulmonary aspergillosis is becoming more common, mucormycosis is still uncommon. Mucormycosis normally appears 10 to 14 days after being admitted to the hospital. Mucormycosis is a rare but dangerous infection that can make extreme COVID-19 worse. Mucormycosis is more likely to occur in people who have diabetes mellitus and other risk factors. Mucormycosis is most likely exacerbated by concurrent glucocorticoid treatment. To improve outcomes, a high index of suspicion and aggressive management is required. Excessive usage of steroids, monoclonal antibodies, and broad-spectrum antibiotics might cause the formation or worsen of a fungal infection. A high index of suspicion and aggressive management are needed. In patients with COVID-19 infection, physicians should be vigilant of the likelihood of subsequent invasive fungal infections. To enhance results in pulmonary mucormycosis, early diagnosis and treatment are critical. Confirmation of the clinical form necessitates a combination of symptoms that are consistent with tissue invasion histologically. Combining various clinical data and the isolation of the fungus from clinical samples in culture is needed for the probable diagnosis of mucormycosis. The organism that causes mucormycosis is identified using macroscopic and microscopic morphological criteria, carbohydrate assimilation, and the maximum temperature at which they can expand. Mucormycosis must be treated with antifungal medication prescribed by a doctor. It may necessitate surgery in some circumstances, and it can result in the loss of the upper jaw and, in some situations, an eye.
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Affiliation(s)
- Suman Kumar Ray
- Department of Applied Sciences, Indira Gandhi Technological and Medical Sciences University, Arunachal Pradesh, India
| | - Sukhes Mukherjee
- Department of Biochemistry, All India Institute of Medical Sciences, Bhopal, Madhya Pradesh, India
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Muthu V, Rudramurthy SM, Chakrabarti A, Agarwal R. Epidemiology and Pathophysiology of COVID-19-Associated Mucormycosis: India Versus the Rest of the World. Mycopathologia 2021; 186:739-754. [PMID: 34414555 PMCID: PMC8375614 DOI: 10.1007/s11046-021-00584-8] [Citation(s) in RCA: 138] [Impact Index Per Article: 34.5] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 06/25/2021] [Accepted: 08/06/2021] [Indexed: 01/08/2023]
Abstract
The coronavirus disease 2019 (COVID-19) pandemic has led to a concerning resurgence of mucormycosis. More than 47,000 cases of mucormycosis were reported in three months from India. We update our systematic review on COVID-19-associated mucormycosis (CAM) till June 21st, 2021, comparing cases reported from India and elsewhere. We included individual patient details of 275 cases of CAM, of which 233 were reported from India and 42 from the rest of the world. Diabetes mellitus was the most common underlying risk factor for CAM in India than in other countries. The fatality rate of cases reported from India (36.5%) was less than the globally reported cases (61.9%), probably due to the predominance of rhino-orbital mucormycosis. On a multivariate analysis, we found that pulmonary or disseminated mucormycosis cases and admission to the intensive care unit were associated with increased mortality, while combination medical therapy improved survival. The paucity of pulmonary and disseminated mucormycosis cases from India suggests that these cases were either not diagnosed or reported, further supported by a trend of search data from the Google search engine. In this review, we discuss the factors explaining the substantial rise in cases of CAM. We also propose a hypothetical model describing the epidemiologic triad of CAM.
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Affiliation(s)
- Valliappan Muthu
- Department of Pulmonary Medicine, Department of Medical Microbiology, Institute of Medical Education and Research (PGIMER), Sector-12, Chandigarh, 160012, India
| | - Shivaprakash M Rudramurthy
- Department of Pulmonary Medicine, Department of Medical Microbiology, Institute of Medical Education and Research (PGIMER), Sector-12, Chandigarh, 160012, India
| | - Arunaloke Chakrabarti
- Department of Pulmonary Medicine, Department of Medical Microbiology, Institute of Medical Education and Research (PGIMER), Sector-12, Chandigarh, 160012, India
| | - Ritesh Agarwal
- Department of Pulmonary Medicine, Department of Medical Microbiology, Institute of Medical Education and Research (PGIMER), Sector-12, Chandigarh, 160012, India.
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Lin TP, Ko CN, Zheng K, Lai KH, Wong RL, Lee A, Zhang S, Huang SS, Wan KH, Lam DS. COVID-19: Update on Its Ocular Involvements, and Complications From Its Treatments and Vaccinations. Asia Pac J Ophthalmol (Phila) 2021; 10:521-529. [PMID: 34839344 PMCID: PMC8673850 DOI: 10.1097/apo.0000000000000453] [Citation(s) in RCA: 25] [Impact Index Per Article: 6.3] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Download PDF] [Journal Information] [Subscribe] [Scholar Register] [Received: 07/28/2021] [Accepted: 10/10/2021] [Indexed: 01/08/2023] Open
Abstract
ABSTRACT The coronavirus disease 2019 (COVID-19) came under the attention of the international medical community when China first notified the World Health Organization of a pneumonia outbreak of then-unknown etiology in Wuhan in December 2019. Since then, COVID-19 caused by the severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) has appalled the world by spreading at a pandemic speed. Although ophthalmologists do not directly engage in the clinical care of COVID-19 patients, the ophthalmology community has become aware of the close ties between its practice and the pandemic. Not only are ophthalmologists at heightened risk of SARS-CoV-2 exposure due to their physical proximity with patients in routine ophthalmic examinations, but SARS-CoV-2 possesses ocular tropism resulting in ocular complications beyond the respiratory tract after viral exposure. Furthermore, patients could potentially suffer from adverse ocular effects in the therapeutic process. This review summarized the latest literature to cover the ophthalmic manifestations, effects of treatments, and vaccinations on the eye to aid the frontline clinicians in providing effective ophthalmic care to COVID-19 patients as the pandemic continues to evolve.
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Affiliation(s)
- Timothy P.H. Lin
- Department of Ophthalmology and Visual Sciences, The Chinese University of Hong Kong, Hong Kong
| | | | - Ke Zheng
- C-MER (Beijing) Dennis Lam Eye Hospital, Beijing, China
| | - Kenny H.W. Lai
- Department of Ophthalmology and Visual Sciences, The Chinese University of Hong Kong, Hong Kong
- C-MER International Eye Care Group, Hong Kong
| | - Raymond L.M. Wong
- Department of Ophthalmology and Visual Sciences, The Chinese University of Hong Kong, Hong Kong
- C-MER International Eye Care Group, Hong Kong
| | - Allie Lee
- Department of Ophthalmology, LKS Faculty of Medicine, The University of Hong Kong, Hong Kong
| | | | - Suber S. Huang
- Retina Center of Ohio, Cleveland, OH, US
- Bascom Palmer Eye Institute, Miami, FL, US
| | - Kelvin H. Wan
- Department of Ophthalmology and Visual Sciences, The Chinese University of Hong Kong, Hong Kong
| | - Dennis S.C. Lam
- C-MER International Eye Research Center of The Chinese University of Hong Kong (Shenzhen), China
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Dilek A, Ozaras R, Ozkaya S, Sunbul M, Sen EI, Leblebicioglu H. COVID-19-associated mucormycosis: Case report and systematic review. Travel Med Infect Dis 2021; 44:102148. [PMID: 34454090 PMCID: PMC8387131 DOI: 10.1016/j.tmaid.2021.102148] [Citation(s) in RCA: 56] [Impact Index Per Article: 14.0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 06/28/2021] [Revised: 07/26/2021] [Accepted: 08/23/2021] [Indexed: 12/16/2022]
Abstract
BACKGROUND Increasing number of patients with COVID-19-associated mucormycosis have been reported, especially from India recently. We have described a patient with COVID-19-associated mucormycosis and, searched and analyzed current medical literature to delineate the characteristics of COVID-19-associated mucormycosis. METHOD We reported a patient developed mucormycosis during post-COVID period. We searched literature to describe the incidence, clinical features, and outcomes of COVID-19-associated mucormycosis. Demographic features, risk factors, clinical features, diagnostic methods, treatment and outcome were analyzed. RESULTS We describe a 54-year-old male, hospitalized due to severe COVID-19 pneumonia. He was given long-term, high doses of systemic steroids. He developed maxillo-fascial mucormycosis and died of sepsis. Our literature search found 30 publications describing 100 patients including present case report. The majority (n = 68) were reported from India. 76% were male. The most commonly seen risk factors were corticosteroid use (90.5%), diabetes (79%), and hypertension (34%). Also, excessive use of broad-spectrum antibiotics were noted in cases. Most frequent involvements were rhino-orbital (50%), followed by rhino-sinusal (17%), and rhino-orbito-cerebral (15%). Death was reported as 33 out of 99 patients (33,3%). CONCLUSIONS Steroid use, diabetes, environmental conditions, excessive use of antibiotics, and hypoxia are main risk factors. Despite medical and surgical treatment, mortality rate is high. A multidisciplinary approach is essential to improve the conditions facilitating the emergence of COVID-19-associated mucormycosis.
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Affiliation(s)
- Ahmet Dilek
- Intensive Care Unit, VM Medicalpark Samsun Hospital, Samsun, Turkey; Istinye University, Faculty of Medicine, Istanbul, Turkey.
| | - Resat Ozaras
- Department of Infectious Diseases, Medilife Health Group, Istanbul, Turkey.
| | - Sevket Ozkaya
- Department of Pulmonology, VM Medicalpark Samsun Hospital, Samsun, Turkey; Department of Pulmonology, Bahcesehir University Medical School, Istanbul, Turkey.
| | - Mustafa Sunbul
- Department of Infectious Diseases, Samsun Liv Hospital, Samsun, Turkey.
| | - Elif Itir Sen
- Intern, Bahcesehir University, Medical School, Istanbul, Turkey.
| | - Hakan Leblebicioglu
- Department of Infectious Diseases, VM Medicalpark Samsun Hospital, Samsun, Turkey.
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Casalini G, Giacomelli A, Ridolfo A, Gervasoni C, Antinori S. Invasive Fungal Infections Complicating COVID-19: A Narrative Review. J Fungi (Basel) 2021; 7:921. [PMID: 34829210 PMCID: PMC8620819 DOI: 10.3390/jof7110921] [Citation(s) in RCA: 57] [Impact Index Per Article: 14.3] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Journal Information] [Subscribe] [Scholar Register] [Received: 09/24/2021] [Revised: 10/27/2021] [Accepted: 10/28/2021] [Indexed: 12/15/2022] Open
Abstract
Invasive fungal infections (IFIs) can complicate the clinical course of COVID-19 and are associated with a significant increase in mortality, especially in critically ill patients admitted to an intensive care unit (ICU). This narrative review concerns 4099 cases of IFIs in 58,784 COVID-19 patients involved in 168 studies. COVID-19-associated invasive pulmonary aspergillosis (CAPA) is a diagnostic challenge because its non-specific clinical/imaging features and the fact that the proposed clinically diagnostic algorithms do not really apply to COVID-19 patients. Forty-seven observational studies and 41 case reports have described a total of 478 CAPA cases that were mainly diagnosed on the basis of cultured respiratory specimens and/or biomarkers/molecular biology, usually without histopathological confirmation. Candidemia is a widely described secondary infection in critically ill patients undergoing prolonged hospitalisation, and the case reports and observational studies of 401 cases indicate high crude mortality rates of 56.1% and 74.8%, respectively. COVID-19 patients are often characterised by the presence of known risk factors for candidemia such as in-dwelling vascular catheters, mechanical ventilation, and broad-spectrum antibiotics. We also describe 3185 cases of mucormycosis (including 1549 cases of rhino-orbital mucormycosis (48.6%)), for which the main risk factor is a history of poorly controlled diabetes mellitus (>76%). Its diagnosis involves a histopathological examination of tissue biopsies, and its treatment requires anti-fungal therapy combined with aggressive surgical resection/debridement, but crude mortality rates are again high: 50.8% in case reports and 16% in observational studies. The presence of other secondary IFIs usually diagnosed in severely immunocompromised patients show that SARS-CoV-2 is capable of stunning the host immune system: 20 cases of Pneumocystis jirovecii pneumonia, 5 cases of cryptococcosis, 4 cases of histoplasmosis, 1 case of coccidioides infection, 1 case of pulmonary infection due to Fusarium spp., and 1 case of pulmonary infection due to Scedosporium.
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Affiliation(s)
- Giacomo Casalini
- Luigi Sacco Department of Biomedical and Clinical Sciences, Università degli Studi di Milano, 20157 Milan, Italy; (G.C.); (A.G.)
| | - Andrea Giacomelli
- Luigi Sacco Department of Biomedical and Clinical Sciences, Università degli Studi di Milano, 20157 Milan, Italy; (G.C.); (A.G.)
- III Division of Infectious Diseases, ASST Fatebenefratelli Sacco, 20157 Milan, Italy; (A.R.); (C.G.)
| | - Annalisa Ridolfo
- III Division of Infectious Diseases, ASST Fatebenefratelli Sacco, 20157 Milan, Italy; (A.R.); (C.G.)
| | - Cristina Gervasoni
- III Division of Infectious Diseases, ASST Fatebenefratelli Sacco, 20157 Milan, Italy; (A.R.); (C.G.)
| | - Spinello Antinori
- Luigi Sacco Department of Biomedical and Clinical Sciences, Università degli Studi di Milano, 20157 Milan, Italy; (G.C.); (A.G.)
- III Division of Infectious Diseases, ASST Fatebenefratelli Sacco, 20157 Milan, Italy; (A.R.); (C.G.)
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Riad A, Shabaan AA, Issa J, Ibrahim S, Amer H, Mansy Y, Kassem I, Kassem AB, Howaldt HP, Klugar M, Attia S. COVID-19-Associated Mucormycosis (CAM): Case-Series and Global Analysis of Mortality Risk Factors. J Fungi (Basel) 2021; 7:837. [PMID: 34682258 PMCID: PMC8540212 DOI: 10.3390/jof7100837] [Citation(s) in RCA: 30] [Impact Index Per Article: 7.5] [Reference Citation Analysis] [Abstract] [Key Words] [Grants] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 08/10/2021] [Revised: 10/03/2021] [Accepted: 10/05/2021] [Indexed: 02/06/2023] Open
Abstract
BACKGROUND Since the novel coronavirus disease (COVID-19) outbreak, the cases of COVID-19 co-infections have been increasingly reported worldwide. Mucormycosis, an opportunistic fungal infection caused by members of the Mucorales order, had been frequently isolated in severely and critically ill COVID-19 patients. METHODS Initially, the anamnestic, clinical, and paraclinical features of seven COVID-19-associated mucormycosis (CAM) cases from Egypt were thoroughly reported. Subsequently, an extensive review of the literature was carried out to describe the characteristics of CAM cases globally, aiming to explore the potential risk factors of mortality in CAM patients. RESULTS Out of the seven reported patients in the case series, five (71.4%) were males, six (85.7%) had diabetes mellitus, and three (42.9%) had cardiovascular disease. All patients exhibited various forms of facial deformities under the computed tomography scanning, and two of them tested positive for Mucorales using the polymerase chain reaction (PCR) testing. Liposomal amphotericin B (LAmB) was prescribed to all cases, and none of them died until the end of the follow-up. On reviewing the literature, 191 cases were reported worldwide, of which 74.4% were males, 83.2% were from low-middle income countries, and 51.4% were aged 55 years old or below. Diabetes mellitus (79.1%), chronic hypertension (30%), and renal disease/failure (13.6%) were the most common medical comorbidities, while steroids (64.5%) were the most frequently prescribed medication for COVID-19, followed by Remdesivir (18.2%), antibiotics (12.7%), and Tocilizumab (5.5%). CONCLUSIONS As the majority of the included studies were observational studies, the obtained evidence needs to be interpreted carefully. Diabetes, steroids, and Remdesivir were not associated with increased mortality risk, thus confirming that steroids used to manage severe and critical COVID-19 patients should not be discontinued. Lung involvement, bilateral manifestation, and Rhizopus isolation were associated with increased mortality risk, thus confirming that proactive screening is imperative, especially for critically ill patients. Finally, surgical management and antimycotic medications, e.g., amphotericin B and posaconazole, were associated with decreased mortality risk, thus confirming their effectiveness.
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Affiliation(s)
- Abanoub Riad
- Czech National Centre for Evidence-Based Healthcare and Knowledge Translation (Cochrane Czech Republic, Czech EBHC: JBI Centre of Excellence, Masaryk University GRADE Centre), Institute of Biostatistics and Analyses, Faculty of Medicine, Masaryk University, 625 00 Brno, Czech Republic;
- Department of Public Health, Faculty of Medicine, Masaryk University, 625 00 Brno, Czech Republic
| | - Alshaimaa Ahmed Shabaan
- Department of Oral and Maxillofacial Surgery, Faculty of Dentistry, Fayoum University, Fayoum 635 14, Egypt;
| | - Julien Issa
- Department of Biomaterials and Experimental Dentistry, Poznań University of Medical Sciences, 60-781 Poznan, Poland;
| | - Sally Ibrahim
- Department of Oral and Maxillofacial Pathology, Faculty of Dentistry, Fayoum University, Fayoum 635 14, Egypt;
| | - Hatem Amer
- Department of Oral and Maxillofacial Pathology, Faculty of Dentistry, Cairo University, Cairo 115 62, Egypt;
| | - Yossef Mansy
- Department of Oral and Maxillofacial Surgery, Maadi Military Hospital, Cairo 117 11, Egypt;
| | - Islam Kassem
- Private Oral and Maxillofacial Surgery Practice, Alexandria 215 54, Egypt;
| | - Amira Bisher Kassem
- Department of Clinical Pharmacy and Pharmacy Practice, Faculty of Pharmacy, Damanhur University, Damanhur 225 11, Egypt;
| | - Hans-Peter Howaldt
- Department of Oral and Maxillofacial Surgery, Justus-Liebig-University, Klinikstrasse 33, 35392 Giessen, Germany;
| | - Miloslav Klugar
- Czech National Centre for Evidence-Based Healthcare and Knowledge Translation (Cochrane Czech Republic, Czech EBHC: JBI Centre of Excellence, Masaryk University GRADE Centre), Institute of Biostatistics and Analyses, Faculty of Medicine, Masaryk University, 625 00 Brno, Czech Republic;
| | - Sameh Attia
- Department of Oral and Maxillofacial Surgery, Justus-Liebig-University, Klinikstrasse 33, 35392 Giessen, Germany;
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Post-COVID fungal infections of maxillofacial region: a systematic review. Oral Maxillofac Surg 2021; 26:357-363. [PMID: 34622312 PMCID: PMC8497068 DOI: 10.1007/s10006-021-01010-5] [Citation(s) in RCA: 7] [Impact Index Per Article: 1.8] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 05/18/2021] [Accepted: 09/23/2021] [Indexed: 01/08/2023]
Abstract
With the advent of coronavirus disease (COVID-19) pandemic, a wide range of life-threatening maxillofacial fungal coinfections have also been observed in patients. We conducted this systematic review to collate and evaluate the data to enable clinicians to understand the disease pattern and types of mycosis and provide meticulous management of these infections in COVID-19 patients. The review was carried out in accordance with Preferred Reporting Items for Systematic Review and Meta-analysis guidelines. A systematic electronic literature search was conducted on major databases using keywords in combination with Boolean Operators. Manuscripts discussing cases of maxillofacial fungal infections in COVID-19 patients were included. A total of 11 studies were systematically reviewed to assess the fungal coinfections in COVID-19 patients. Twenty-one cases of mucormycosis, 58 of candidiasis, and 1 each of aspergillosis and mixed infection were observed in the region of head and neck. Significant increase in invasive fungal infection is evident in patients suffering from COVID-19 which could be due to immunosuppression and other pre-existing comorbidities. Early diagnosis and intervention like systemic antifungals or surgical debridement is mandatory to reduce morbidity and mortality.
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Pakdel F, Ahmadikia K, Salehi M, Tabari A, Jafari R, Mehrparvar G, Rezaie Y, Rajaeih S, Alijani N, Barac A, Abdollahi A, Khodavaisy S. Mucormycosis in patients with COVID-19: A cross-sectional descriptive multicentre study from Iran. Mycoses 2021; 64:1238-1252. [PMID: 34096653 PMCID: PMC8242414 DOI: 10.1111/myc.13334] [Citation(s) in RCA: 94] [Impact Index Per Article: 23.5] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 03/05/2021] [Revised: 05/23/2021] [Accepted: 05/31/2021] [Indexed: 12/28/2022]
Abstract
PURPOSE The aim of the study was to report clinical features, contributing factors and outcome of patients with coronavirus disease 2019 (COVID-19)-associated mucormycosis (CAM). METHODS A cross-sectional descriptive multicentre study was conducted on patients with biopsy-proven mucormycosis with RT-PCR-confirmed COVID-19 from April to September 2020. Demographics, the time interval between COVID-19 and mucormycosis, underlying systemic diseases, clinical features, course of disease and outcomes were collected and analysed. RESULTS Fifteen patients with COVID-19 and rhino-orbital mucormycosis were observed. The median age of patients was 52 years (range 14-71), and 66% were male. The median interval time between COVID-19 disease and diagnosis of mucormycosis was seven (range: 1-37) days. Among all, 13 patients (86%) had diabetes mellitus, while 7 (46.6%) previously received intravenous corticosteroid therapy. Five patients (33%) underwent orbital exenteration, while seven (47%) patients died from mucormycosis. Six patients (40%) received combined antifungal therapy and none that received combined antifungal therapy died. CONCLUSION Clinicians should be aware that mucormycosis may be complication of COVID-19 in high-risk patients. Poor control of diabetes mellitus is an important predisposing factor for CAM. Systematic surveillance for control of diabetes mellitus and educating physician about the early diagnosis of CAM are suggested.
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Affiliation(s)
- Farzad Pakdel
- Department of Oculo‐Facial Plastic SurgeryDepartment of OphthalmologyFarabi HospitalTehran University of Medical SciencesTehranIran
| | - Kazem Ahmadikia
- Department of Medical Parasitology and MycologySchool of Public HealthTehran University of Medical SciencesTehranIran
| | - Mohammadreza Salehi
- Department of infectious diseases and Tropical MedicineImam Khomeini Hospital ComplexTehran University of Medical SciencesTehranIran
| | - Azin Tabari
- Otorhinolaryngology Research CenterImam Khomeini Hospital complexTehran University of Medical SciencesTehranIran
| | - Rozita Jafari
- Department of ENTImam Hossein HospitalShahid Beheshti University of Medical SciencesTehranIran
| | - Golfam Mehrparvar
- Department of ENTImam Hossein HospitalShahid Beheshti University of Medical SciencesTehranIran
| | - Yasaman Rezaie
- Department of infectious diseases and Tropical MedicineImam Khomeini Hospital ComplexTehran University of Medical SciencesTehranIran
| | - Shahin Rajaeih
- ENT and Head and Neck Research Center and DepartmentThe Five Senses Health InstituteFiroozgar HospitalIran University of Medical SciencesTehranIran
| | - Neda Alijani
- Department of Infectious DiseaseShariati HospitalTehran University of Medical SciencesTehranIran
| | - Aleksandra Barac
- Clinic for Infectious and Tropical DiseasesClinical Centre of SerbiaFaculty of MedicineUniversity of BelgradeBelgradeSerbia
| | - Alireza Abdollahi
- Department of PathologyImam Khomeini Hospital complexTehran University of Medical SciencesTehranIran
| | - Sadegh Khodavaisy
- Department of Medical Parasitology and MycologySchool of Public HealthTehran University of Medical SciencesTehranIran
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Hussain S, Baxi H, Riad A, Klugarová J, Pokorná A, Slezáková S, Líčeník R, Najmi AK, Klugar M. COVID-19-Associated Mucormycosis (CAM): An Updated Evidence Mapping. INTERNATIONAL JOURNAL OF ENVIRONMENTAL RESEARCH AND PUBLIC HEALTH 2021; 18:10340. [PMID: 34639637 PMCID: PMC8508302 DOI: 10.3390/ijerph181910340] [Citation(s) in RCA: 25] [Impact Index Per Article: 6.3] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Download PDF] [Figures] [Subscribe] [Scholar Register] [Received: 07/29/2021] [Revised: 09/23/2021] [Accepted: 09/25/2021] [Indexed: 12/17/2022]
Abstract
Mucormycosis, a serious and rare fungal infection, has recently been reported in COVID-19 patients worldwide. This study aims to map all the emerging evidence on the COVID-19-associated mucormycosis (CAM) with a special focus on clinical presentation, treatment modalities, and patient outcomes. An extensive literature search was performed in MEDLINE (Ovid), Embase (Ovid), Cochrane COVID-19 Study Register, and WHO COVID-19 database till 9 June 2021. The primary outcome was to summarize the clinical presentation, treatment modalities, and patient outcomes of CAM. Data were summarized using descriptive statistics and presented in tabular form. This evidence mapping was based on a total of 167 CAM patients with a mean age of 51 ± 14.62 years, and 56.28% of them were male. Diabetes mellitus (73.65% (n = 123)), hypertension (22.75% (n = 38)), and renal failure (10.77% (n = 18)) were the most common co-morbidities among CAM patients. The most common symptoms observed in CAM patients were facial pain, ptosis, proptosis, visual acuity, and vision loss. Survival was higher in patients who underwent both medical and surgical management (64.96%). Overall mortality among CAM patients was found to be 38.32%. In conclusion, this study found a high incidence of CAM with a high mortality rate. Optimal glycemic control and early identification of mucormycosis should be the priority to reduce the morbidity and mortality related to CAM.
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Affiliation(s)
- Salman Hussain
- Czech National Centre for Evidence-Based Healthcare and Knowledge Translation (Cochrane Czech Republic, Czech EBHC: JBI Centre of Excellence, Masaryk University GRADE Centre), Institute of Biostatistics and Analyses, Faculty of Medicine, Masaryk University, Kamenice 5, 62500 Brno, Czech Republic; (A.R.); (J.K.); (A.P.); (S.S.); (R.L.)
| | - Harveen Baxi
- Independent Researcher, New Delhi 110062, India;
| | - Abanoub Riad
- Czech National Centre for Evidence-Based Healthcare and Knowledge Translation (Cochrane Czech Republic, Czech EBHC: JBI Centre of Excellence, Masaryk University GRADE Centre), Institute of Biostatistics and Analyses, Faculty of Medicine, Masaryk University, Kamenice 5, 62500 Brno, Czech Republic; (A.R.); (J.K.); (A.P.); (S.S.); (R.L.)
- Department of Public Health, Faculty of Medicine, Masaryk University, Kamenice 5, 62500 Brno, Czech Republic
| | - Jitka Klugarová
- Czech National Centre for Evidence-Based Healthcare and Knowledge Translation (Cochrane Czech Republic, Czech EBHC: JBI Centre of Excellence, Masaryk University GRADE Centre), Institute of Biostatistics and Analyses, Faculty of Medicine, Masaryk University, Kamenice 5, 62500 Brno, Czech Republic; (A.R.); (J.K.); (A.P.); (S.S.); (R.L.)
| | - Andrea Pokorná
- Czech National Centre for Evidence-Based Healthcare and Knowledge Translation (Cochrane Czech Republic, Czech EBHC: JBI Centre of Excellence, Masaryk University GRADE Centre), Institute of Biostatistics and Analyses, Faculty of Medicine, Masaryk University, Kamenice 5, 62500 Brno, Czech Republic; (A.R.); (J.K.); (A.P.); (S.S.); (R.L.)
- Department of Nursing and Midwifery, Faculty of Medicine, Masaryk University, Kamenice 5, 62500 Brno, Czech Republic
| | - Simona Slezáková
- Czech National Centre for Evidence-Based Healthcare and Knowledge Translation (Cochrane Czech Republic, Czech EBHC: JBI Centre of Excellence, Masaryk University GRADE Centre), Institute of Biostatistics and Analyses, Faculty of Medicine, Masaryk University, Kamenice 5, 62500 Brno, Czech Republic; (A.R.); (J.K.); (A.P.); (S.S.); (R.L.)
| | - Radim Líčeník
- Czech National Centre for Evidence-Based Healthcare and Knowledge Translation (Cochrane Czech Republic, Czech EBHC: JBI Centre of Excellence, Masaryk University GRADE Centre), Institute of Biostatistics and Analyses, Faculty of Medicine, Masaryk University, Kamenice 5, 62500 Brno, Czech Republic; (A.R.); (J.K.); (A.P.); (S.S.); (R.L.)
| | - Abul Kalam Najmi
- Department of Pharmacology, School of Pharmaceutical Education and Research, Jamia Hamdard, New Delhi 110062, India;
| | - Miloslav Klugar
- Czech National Centre for Evidence-Based Healthcare and Knowledge Translation (Cochrane Czech Republic, Czech EBHC: JBI Centre of Excellence, Masaryk University GRADE Centre), Institute of Biostatistics and Analyses, Faculty of Medicine, Masaryk University, Kamenice 5, 62500 Brno, Czech Republic; (A.R.); (J.K.); (A.P.); (S.S.); (R.L.)
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Soni S, Namdeo Pudake R, Jain U, Chauhan N. A systematic review on SARS-CoV-2-associated fungal coinfections. J Med Virol 2021; 94:99-109. [PMID: 34570905 PMCID: PMC8661750 DOI: 10.1002/jmv.27358] [Citation(s) in RCA: 18] [Impact Index Per Article: 4.5] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 06/19/2021] [Revised: 08/16/2021] [Accepted: 09/23/2021] [Indexed: 01/08/2023]
Abstract
A severe pandemic of Coronavirus Disease (COVID‐19) has been sweeping the globe since 2019, and this time, it did not stop, with frequent mutations transforming into virulent strains, for instance, B.1.1.7, B.1.351, and B.1.427. In recent months, a fungal infection, mucormycosis has emerged with more fatal responses and significantly increased mortality rate. To measure the severity and potential alternative approaches against black fungus coinfection in COVID‐19 patients, PubMed, Google Scholar, World Health Organization (WHO) newsletters, and other online resources, based on the cases reported and retrospective observational analysis were searched from the years 2015–2021. The studies reporting mucormycosis with Severe Acute Respiratory Syndrome Coronavirus 2 (SARS‐CoV‐2) coinfection and/or demonstrating potential risk factors, such as a history of diabetes mellitus or suppressed immune system were included, and reports published in non‐English language were excluded. More than 20 case reports and observational studies on black fungus coinfection in COVID‐19 patients were eligible for inclusion. The results indicated that diabetes mellitus, hyperglycemic, and immunocompromised COVID‐19 patients with mucormycosis were at a higher risk. We found that it was prudent to assess the potential risk factors and severity of invasive mycosis via standardized diagnostic and clinical settings. Large‐scale studies need to be conducted to identify early biomarkers and optimization of diagnostic methods has to be established per population and geographical variation. This will not only help clinicians around the world to detect the coinfection in time but also will prepare them for future outbreaks of other potential pandemics.
Observational studies and case reports of Post‐COVID black fungus co‐infection highlighted in review. Along with risk factors, radiological interventions of black fungus co‐infection in COVID‐19 patients and challenges for accurate diagnosis were elaborated. The review discusses interconnection between fungus and SARS‐CoV‐2 co‐infection of mechanism to identify potential biomarkers. Our conclusion will contribute to motivate researchers to design follow‐up plans for black fungus infection in COVID‐19.
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Affiliation(s)
- Shringika Soni
- Amity Institute of Nanotechnology (AINT), Amity University Uttar Pradesh (AUUP), Noida, India
| | - Ramesh Namdeo Pudake
- Amity Institute of Nanotechnology (AINT), Amity University Uttar Pradesh (AUUP), Noida, India
| | - Utkarsh Jain
- Amity Institute of Nanotechnology (AINT), Amity University Uttar Pradesh (AUUP), Noida, India
| | - Nidhi Chauhan
- Amity Institute of Nanotechnology (AINT), Amity University Uttar Pradesh (AUUP), Noida, India
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Yasmin F, Najeeb H, Naeem A, Dapke K, Phadke R, Asghar MS, Shah SMI, De Berardis D, Ullah I. COVID-19 Associated Mucormycosis: A Systematic Review from Diagnostic Challenges to Management. Diseases 2021; 9:65. [PMID: 34698143 PMCID: PMC8544552 DOI: 10.3390/diseases9040065] [Citation(s) in RCA: 29] [Impact Index Per Article: 7.3] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 07/25/2021] [Revised: 09/02/2021] [Accepted: 09/07/2021] [Indexed: 01/08/2023] Open
Abstract
The coronavirus disease 2019 (COVID-19) outbreak has caused significant destruction, claiming over three million lives worldwide. Post SARS-COV-2 invasion, immunosuppression with hyperglycemia and elevated ferritin levels along with steroidal treatment creates a perfect storm for opportunistic infections. There is increasing evidence of mucormycosis co-infection in COVID-19 patients, during or post-treatment. A worse prognosis, a late diagnosis, and limited guidelines of screening and management of COVID-19 associated mucormycosis have made healthcare professionals fear an epidemic alongside a pandemic. This review geographically reports cases of COVID-19 associated mucormycosis (CAM), evaluates characteristics, clinical manifestations, and outcomes of mucormycosis in COVID-19 active or recovered patients. It further describes preventive strategies and recommendations for optimal management therapy that can be adopted worldwide to curtail an impending threat to the healthcare system.
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Affiliation(s)
- Farah Yasmin
- Department of Internal Medicine, Dow University of Health Sciences, Karachi 74200, Pakistan; (F.Y.); (A.N.)
| | - Hala Najeeb
- Department of Internal Medicine, Dow University of Health Sciences, Karachi 74200, Pakistan; (F.Y.); (A.N.)
| | - Aisha Naeem
- Department of Internal Medicine, Dow University of Health Sciences, Karachi 74200, Pakistan; (F.Y.); (A.N.)
| | - Kartik Dapke
- Indira Gandhi Government Medical College, Nagpur 440018, India; (K.D.); (R.P.)
| | - Rachana Phadke
- Indira Gandhi Government Medical College, Nagpur 440018, India; (K.D.); (R.P.)
| | | | | | - Domenico De Berardis
- NHS, Department of Mental Health, Psychiatric Service for Diagnosis and Treatment, Hospital “G. Mazzini”, ASL 4, 64100 Teramo, Italy;
| | - Irfan Ullah
- Department of Internal Medicine, Kabir Medical College, Gandhara University, Peshawar 25000, Pakistan;
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Mohammadi F, Badri M, Safari S, Hemmat N. 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 2021; 21:906. [PMID: 34479495 PMCID: PMC8415695 DOI: 10.1186/s12879-021-06625-3] [Citation(s) in RCA: 17] [Impact Index Per Article: 4.3] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 03/09/2021] [Accepted: 08/27/2021] [Indexed: 12/17/2022] Open
Abstract
BACKGROUND COVID-19 disease may be associated with a wide range of bacterial and fungal infections. We report a patient with COVID-19 infection who developed rhino-facial mucormycosis during treatment with corticosteroids. CASE PRESENTATION A 59-year-old non-diabetic male patient was admitted with a diagnosis of COVID-19 based on positive RT-PCR and CT of the lungs. Due to sever lung involvement, he was treated with methylprednisolone. The patient was re-admitted to hospital, due to nasal obstruction and left side facial and orbital swelling, several days after discharge. In sinus endoscopic surgery, debridement was performed and the specimens were sent to pathology and mycology laboratories. A nasal biopsy showed wide hyphae without septa. The sequenced PCR product revealed Rhizopus oryzae. Despite all medical and surgical treatment, the patient died. In addition, the characteristics of patients with COVID-19-associated mucormycosis were reviewed in 44 available literatures. In most studies, diabetes mellitus was the most common predisposing factor for mucormycosis. CONCLUSION Our report highlights the need for assessing the presence of mucormycosis in patients with COVID-19 and also it shows that physicians should consider the potential for secondary invasive fungal infections in COVID-19 cases.
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Affiliation(s)
- Faezeh Mohammadi
- Department of Medical Parasitology and Mycology, School of Medicine, Qazvin University of Medical Sciences, Shahid Bahonar Blvd, PO Box: 34199-15315, Qazvin, Iran.
| | - Milad Badri
- Medical Microbiology Research Center, Qazvin University of Medical Sciences, Qazvin, Iran
- Metabolic Diseases Research Center, Research Institute for Prevention of Non-Communicable Diseases, Qazvin University of Medical Sciences, Qazvin, Iran
| | - Shapoor Safari
- Department of Otolaryngologist, Fellowship of Rhinology, Razi Hospital, Qazvin, Iran
| | - Nima Hemmat
- Department of Cellular and Molecular Research Center, Qazvin University of Medical Sciences, Qazvin, Iran
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Garg M, Prabhakar N, Muthu V, Farookh S, Kaur H, Suri V, Agarwal R. CT Findings of COVID-19-associated Pulmonary Mucormycosis: A Case Series and Literature Review. Radiology 2021; 302:214-217. [PMID: 34463553 PMCID: PMC8717687 DOI: 10.1148/radiol.2021211583] [Citation(s) in RCA: 24] [Impact Index Per Article: 6.0] [Reference Citation Analysis] [MESH Headings] [Track Full Text] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 01/03/2023]
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Badali H, Cañete-Gibas C, McCarthy D, Patterson H, Sanders C, David MP, Mele J, Fan H, Wiederhold NP. Epidemiology and Antifungal Susceptibilities of Mucoralean Fungi in Clinical Samples from the United States. J Clin Microbiol 2021; 59:e0123021. [PMID: 34232068 PMCID: PMC8373021 DOI: 10.1128/jcm.01230-21] [Citation(s) in RCA: 46] [Impact Index Per Article: 11.5] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 05/26/2021] [Accepted: 07/01/2021] [Indexed: 01/12/2023] Open
Abstract
The global incidence of mucormycosis has increased in recent years owing to higher numbers of individuals at risk for these infections. The diagnosis and treatment of this aggressive fungal infection are of clinical concern due to differences in species distribution in different geographic areas and susceptibility profiles between different species that are capable of causing highly aggressive infections. The purpose of this study was to evaluate the epidemiology and susceptibility profiles of Mucorales isolates in the United States over a 52-month period. Species identification was performed by combined phenotypic characteristics and DNA sequence analysis, and antifungal susceptibility testing was performed by CLSI M38 broth microdilution for amphotericin B, isavuconazole, itraconazole, and posaconazole. During this time frame, 854 isolates were included, representing 11 different genera and over 26 species, of which Rhizopus (58.6%) was the predominant genus, followed by Mucor (19.6%). The majority of isolates were cultured from the upper and lower respiratory tracts (55%). Amphotericin B demonstrated the most potent in vitro activity, with geometric mean (GM) MICs of ≤0.25 μg/ml against all genera with the exception of Cunninghamella species (GM MIC of 1.30 μg/ml). In head-to-head comparisons, the most active azole was posaconazole, followed by isavuconazole. Differences in azole and amphotericin B susceptibility patterns were observed between the genera with the greatest variability observed with isavuconazole. Awareness of the epidemiology of Mucorales isolates and differences in antifungal susceptibility patterns in the United States may aide clinicians in choosing antifungal treatment regimens. Further studies are warranted to correlate these findings with clinical outcomes.
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Affiliation(s)
- Hamid Badali
- Fungus Testing Laboratory & Molecular Diagnostics Laboratory, University of Texas Health Science Center at San Antonio, San Antonio, Texas, USA
- Invasive Fungi Research Center, Communicable Diseases Institute, Mazandaran University of Medical Sciences, Sari, Iran
| | - Connie Cañete-Gibas
- Fungus Testing Laboratory & Molecular Diagnostics Laboratory, University of Texas Health Science Center at San Antonio, San Antonio, Texas, USA
| | - Dora McCarthy
- Fungus Testing Laboratory & Molecular Diagnostics Laboratory, University of Texas Health Science Center at San Antonio, San Antonio, Texas, USA
| | - Hoja Patterson
- Fungus Testing Laboratory & Molecular Diagnostics Laboratory, University of Texas Health Science Center at San Antonio, San Antonio, Texas, USA
| | - Carmita Sanders
- Fungus Testing Laboratory & Molecular Diagnostics Laboratory, University of Texas Health Science Center at San Antonio, San Antonio, Texas, USA
| | - Marjorie P. David
- Fungus Testing Laboratory & Molecular Diagnostics Laboratory, University of Texas Health Science Center at San Antonio, San Antonio, Texas, USA
| | - James Mele
- Fungus Testing Laboratory & Molecular Diagnostics Laboratory, University of Texas Health Science Center at San Antonio, San Antonio, Texas, USA
| | - Hongxin Fan
- Fungus Testing Laboratory & Molecular Diagnostics Laboratory, University of Texas Health Science Center at San Antonio, San Antonio, Texas, USA
| | - Nathan P. Wiederhold
- Fungus Testing Laboratory & Molecular Diagnostics Laboratory, University of Texas Health Science Center at San Antonio, San Antonio, Texas, USA
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Affiliation(s)
- Sharad Pandey
- Department of Neurosurgery, A.B.V.I.M.S. and Dr Ram Manohar Lohia Hospital, New Delhi, India
| | - Abrar Ahad Wani
- Department of Neurosurgery, S.K.I.M.S. Srinagar, Jammu and Kashmir, India
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Abstract
BACKGROUND The recent emergence of the Coronavirus Disease (COVID-19) disease had been associated with reports of fungal infections such as aspergillosis and mucormycosis especially among critically ill patients treated with steroids. The recent surge in cases of COVID-19 in India during the second wave of the pandemic had been associated with increased reporting of invasive mucormycosis post COVID-19. There are multiple case reports and case series describing mucormycosis in COVID-19. PURPOSE In this review, we included most recent reported case reports and case-series of mucormycosis among patients with COVID-19 and describe the clinical features and outcome. RESULTS Many of the mucormycosis reports were eported from India, especially in COVID-19 patients who were treated and recovered patients. The most commonly reported infection sites were rhino-orbital/rhino-cerebral mucormycosis. Those patients were diabetic and had corticosteroids therapy for controlling the severity of COVID-19, leading to a higher fatality in such cases and complicating the pandemic scenario. The triad of severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2), corticosteroid use and uncontrolled diabetes mellitus have been evident for significant increase in the incidence of angioinvasive maxillofacial mucormycosis. In addition, the presence of spores and other factors might play a role as well. CONCLUSION With the ongoing COVID-19 pandemic and increasing number of critically ill patients infected with SARS-CoV-2, it is important to develop a risk-based approach for patients at risk of mucormycosis based on the epidemiological burden of mucormycosis, prevalence of diabetes mellitus, COVID-19 disease severity and use of immune modulating agents including the combined use of corticosteroids and immunosuppressive agents in patients with cancer and transplants.
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Abstract
Purpose: To report and validate an objective staging system for COVID-related Rhino-Orbito-Cerebral mucormycosis (ROCM).Methods: Proof of concept of a new ROC staging system was devised for COVID-related ROCM. The staging system was based on data points drawn from a comprehensive ophthalmic examination, diagnostic endoscopy, and appropriate imaging of orbit, paranasal sinuses and brain in post-COVID ROCM patients to formulate the final staging expressed as R0-3O0-3C0-3. Each stage in the sinus, orbit and brain was graded into three levels of severity of disease. Progressive stages necessitated more active and urgent intervention and poorer prognosis. Finally, ten consecutive ROCM patients were independently staged by two blinded clinicians by examining clinical photographs and radiological images and the results matched for concordance.Results: Each component of the staging: Rhino, Orbital, and Cerebral were graded 0-3 based on severity. Each stage was matched with a recommended management plan. The final ROC grading by two independent clinicians showed a high degree of concordance - maximum for orbit grade (100%) followed by brain (90%) and sinuses (80%). Overall R0-3O0-3C0-3 staging had 70% concordance. Extrapolation of final ROC staging of two clinicians showed 60% match. When we allowed for one-point difference in the ROC staging system the concordance between two clinicians improved to 100% and the management plan matched in 90%.Conclusion: The proposed ROC staging system based on objectively defined clinico-radiological criteria of the three components of COVID-related ROCM is simple-to-use and has high concordance when validated by independent clinicians. The staging helps devise a management plan and has prognostic value.
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Affiliation(s)
- Milind N Naik
- Ophthalmic Plastic Surgery Service, L.V. Prasad Eye Institute, Hyderabad, India
| | - Suryasnata Rath
- Ophthalmic Plastic Surgery Service, L.V. Prasad Eye Institute, Bhubaneshwar, India
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47
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Selarka L, Sharma S, Saini D, Sharma S, Batra A, Waghmare VT, Dileep P, Patel S, Shah M, Parikh T, Darji P, Patel A, Goswami G, Shah A, Shah S, Lathiya H, Shah M, Sharma P, Chopra S, Gupta A, Jain N, Khan E, Sharma VK, Sharma AK, Chan ACY, Ong JJY. Mucormycosis and COVID-19: An epidemic within a pandemic in India. Mycoses 2021; 64:1253-1260. [PMID: 34255907 PMCID: PMC8446956 DOI: 10.1111/myc.13353] [Citation(s) in RCA: 97] [Impact Index Per Article: 24.3] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 05/28/2021] [Revised: 06/25/2021] [Accepted: 06/30/2021] [Indexed: 02/06/2023]
Abstract
Importance Coronavirus disease (COVID‐19) causes an immunosuppressed state and increases risk of secondary infections like mucormycosis. We evaluated clinical features, predisposing factors, diagnosis and outcomes for mucormycosis among patients with COVID‐19 infection. Methods This prospective, observational, multi‐centre study included 47 consecutive patients with mucormycosis, diagnosed during their course of COVID‐19 illness, between January 3 and March 27, 2021. Data regarding demography, underlying medical conditions, COVID‐19 illness and treatment were collected. Clinical presentations of mucormycosis, imaging and biochemical characteristics and outcome were recorded. Results Of the 2567 COVID‐19 patients admitted to 3 tertiary centres, 47 (1.8%) were diagnosed with mucormycosis. Mean age was 55 ± 12.8years, and majority suffered from diabetes mellitus (n = 36, 76.6%). Most were not COVID‐19 vaccinated (n = 31, 66.0%) and majority (n = 43, 91.5%) had developed moderate‐to‐severe pneumonia, while 20 (42.6%) required invasive ventilation. All patients had received corticosteroids and broad‐spectrum antibiotics while most (n = 37, 78.7%) received at least one anti‐viral medication. Mean time elapsed from COVID‐19 diagnosis to mucormycosis was 12.1 ± 4.6days. Eleven (23.4%) subjects succumbed to their disease, mostly (n = 8, 72.7%) within 7 days of diagnosis. Among the patients who died, 10 (90.9%) had pre‐existing diabetes mellitus, only 2 (18.2%) had received just one vaccine dose and all developed moderate‐to‐severe pneumonia, requiring oxygen supplementation and mechanical ventilation. Conclusions Mucormycosis can occur among COVID‐19 patients, especially with poor glycaemic control, widespread and injudicious use of corticosteroids and broad‐spectrum antibiotics, and invasive ventilation. Owing to the high mortality, high index of suspicion is required to ensure timely diagnosis and appropriate treatment in high‐risk populations.
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Affiliation(s)
| | - Suktara Sharma
- Department of ENT, GCS Medical College, Ahmedabad, India
| | | | - Sanjay Sharma
- Department of Neurology, Ramkrishna Care Hospitals, Raipur, India
| | - Amit Batra
- Department of Neurology, Max Hospital, New Delhi, India
| | | | | | | | | | | | | | - Amit Patel
- Zydus Hospital, Ahmedabad, Gujarat, India
| | | | - Anand Shah
- Zydus Hospital, Ahmedabad, Gujarat, India
| | | | - Harsh Lathiya
- Department of Neurology, Ramkrishna Care Hospitals, Raipur, India
| | | | - Pranita Sharma
- Department of Neurology, Ramkrishna Care Hospitals, Raipur, India
| | - Surabhi Chopra
- Department of Neurology, Ramkrishna Care Hospitals, Raipur, India
| | - Ankur Gupta
- Department of Neurology, Ramkrishna Care Hospitals, Raipur, India
| | - Neha Jain
- Department of Neurology, Ramkrishna Care Hospitals, Raipur, India
| | - Erum Khan
- BJ Medical College and Civil Hospital, Ahmedabad, India
| | - Vijay K Sharma
- Division of Neurology, Department of Medicine, National University Hospital and Yong Loo Lin School of Medicine, National University of Singapore, Singapore
| | | | - Amanda C Y Chan
- Division of Neurology, Department of Medicine, National University Hospital and Yong Loo Lin School of Medicine, National University of Singapore, Singapore
| | - Jonathan J Y Ong
- Division of Neurology, Department of Medicine, National University Hospital and Yong Loo Lin School of Medicine, National University of Singapore, Singapore
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Pakdel F, Ahmadikia K, Salehi M, Tabari A, Jafari R, Mehrparvar G, Rezaie Y, Rajaeih S, Alijani N, Barac A, Abdollahi A, Khodavaisy S. Mucormycosis in patients with COVID‐19: A cross‐sectional descriptive multicentre study from Iran. Mycoses 2021. [DOI: 10.1111/myc.13334 10.1111/myc.13334] [Citation(s) in RCA: 1] [Impact Index Per Article: 0.3] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 01/12/2023]
Affiliation(s)
- Farzad Pakdel
- Department of Oculo‐Facial Plastic Surgery Department of Ophthalmology Farabi Hospital Tehran University of Medical Sciences Tehran Iran
| | - Kazem Ahmadikia
- Department of Medical Parasitology and Mycology School of Public Health Tehran University of Medical Sciences Tehran Iran
| | - Mohammadreza Salehi
- Department of infectious diseases and Tropical Medicine Imam Khomeini Hospital Complex Tehran University of Medical Sciences Tehran Iran
| | - Azin Tabari
- Otorhinolaryngology Research Center Imam Khomeini Hospital complex Tehran University of Medical Sciences Tehran Iran
| | - Rozita Jafari
- Department of ENT Imam Hossein Hospital Shahid Beheshti University of Medical Sciences Tehran Iran
| | - Golfam Mehrparvar
- Department of ENT Imam Hossein Hospital Shahid Beheshti University of Medical Sciences Tehran Iran
| | - Yasaman Rezaie
- Department of infectious diseases and Tropical Medicine Imam Khomeini Hospital Complex Tehran University of Medical Sciences Tehran Iran
| | - Shahin Rajaeih
- ENT and Head and Neck Research Center and Department The Five Senses Health Institute Firoozgar Hospital Iran University of Medical Sciences Tehran Iran
| | - Neda Alijani
- Department of Infectious Disease Shariati Hospital Tehran University of Medical Sciences Tehran Iran
| | - Aleksandra Barac
- Clinic for Infectious and Tropical Diseases Clinical Centre of Serbia Faculty of Medicine University of Belgrade Belgrade Serbia
| | - Alireza Abdollahi
- Department of Pathology Imam Khomeini Hospital complex Tehran University of Medical Sciences Tehran Iran
| | - Sadegh Khodavaisy
- Department of Medical Parasitology and Mycology School of Public Health Tehran University of Medical Sciences Tehran Iran
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49
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Singh AK, Singh R, Joshi SR, Misra A. Mucormycosis in COVID-19: A systematic review of cases reported worldwide and in India. Diabetes Metab Syndr 2021; 15:102146. [PMID: 34192610 PMCID: PMC8137376 DOI: 10.1016/j.dsx.2021.05.019] [Citation(s) in RCA: 567] [Impact Index Per Article: 141.8] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 05/14/2021] [Accepted: 05/15/2021] [Indexed: 02/08/2023]
Abstract
BACKGROUND AND AIMS There are increasing case reports of rhino-orbital mucormycosis in people with coronavirus disease 2019 (COVID-19), especially from India. Diabetes mellitus (DM) is an independent risk factor for both severe COVID-19 and mucormycosis. We aim to conduct a systematic review of literature to find out the patient's characteristics having mucormycosis and COVID-19. METHODS We searched the electronic database of PubMed and Google Scholar from inception until May 13, 2021 using keywords. We retrieved all the granular details of case reports/series of patients with mucormycosis, and COVID-19 reported world-wide. Subsequently we analyzed the patient characteristics, associated comorbidities, location of mucormycosis, use of steroids and its outcome in people with COVID-19. RESULTS Overall, 101 cases of mucormycosis in people with COVID-19 have been reported, of which 82 cases were from India and 19 from the rest of the world. Mucormycosis was predominantly seen in males (78.9%), both in people who were active (59.4%) or recovered (40.6%) from COVID-19. Pre-existing diabetes mellitus (DM) was present in 80% of cases, while concomitant diabetic ketoacidosis (DKA) was present in 14.9%. Corticosteroid intake for the treatment of COVID-19 was recorded in 76.3% of cases. Mucormycosis involving nose and sinuses (88.9%) was most common followed by rhino-orbital (56.7%). Mortality was noted in 30.7% of the cases. CONCLUSION An unholy trinity of diabetes, rampant use of corticosteroid in a background of COVID-19 appears to increase mucormycosis. All efforts should be made to maintain optimal glucose and only judicious use of corticosteroids in patients with COVID-19.
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Affiliation(s)
- Awadhesh Kumar Singh
- Department of Diabetes & Endocrinology, G. D Hospital & Diabetes Institute, Kolkata, West Bengal, India.
| | - Ritu Singh
- Department of Diabetes & Endocrinology, G. D Hospital & Diabetes Institute, Kolkata, West Bengal, India
| | - Shashank R Joshi
- Department of Diabetes & Endocrinology, Lilavati Hospital & Joshi Clinic, Mumbai, Maharashtra, India
| | - Anoop Misra
- Fortis C-DOC Hospital for Diabetes & Allied Sciences, New Delhi, India; National Diabetes, Obesity and Cholesterol Foundation, New Delhi, India; Diabetes Foundation (India), New Delhi, India
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50
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Rodriguez-Morales AJ, Sah R, Millan-Oñate J, Gonzalez A, Montenegro-Idrogo JJ, Scherger S, Franco-Paredes C, Henao-Martínez AF. COVID-19 associated mucormycosis: the urgent need to reconsider the indiscriminate use of immunosuppressive drugs. Ther Adv Infect Dis 2021; 8:20499361211027065. [PMID: 34211710 PMCID: PMC8216396 DOI: 10.1177/20499361211027065] [Citation(s) in RCA: 23] [Impact Index Per Article: 5.8] [Reference Citation Analysis] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 12/15/2022] Open
Affiliation(s)
- Alfonso J Rodriguez-Morales
- Grupo de Investigación Biomedicina, Faculty of Medicine, Fundación Universitaria Autónoma de las Américas, Belmonte, Pereira, Risaralda 660003, Colombia. Associate Editor, Therapeutic Advances in Infectious Disease
| | - Ranjit Sah
- Tribhuvan University Teaching Hospital, Institute of Medicine, Kathmandu, Nepal
| | - Jose Millan-Oñate
- Adult Infectious Diseases, Clínica Imbanaco QuirónSalud, Cali, Valle del Cauca, Colombia
| | - Angel Gonzalez
- Basic and Applied Microbiology Research Group (MICROBA), School of Microbiology, Universidad de Antioquia, Medellin, Colombia
| | | | - Sias Scherger
- Division of Infectious Diseases, University of Colorado Denver School of Medicine, Anschutz Medical Campus, Aurora, CO, USA
| | - Carlos Franco-Paredes
- Division of Infectious Diseases, University of Colorado Denver School of Medicine, Anschutz Medical Campus, Aurora, CO, USA
| | - Andrés F Henao-Martínez
- Division of Infectious Diseases, University of Colorado Denver School of Medicine, Anschutz Medical Campus, Aurora, CO, USA
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