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Table of Contents
ORIGINAL ARTICLE
Year : 2022  |  Volume : 19  |  Issue : 2  |  Page : 89-95

Imaging spectrum of mucormycosis in COVID-19 patients using computed tomography and magnetic resonance imaging


1 Department of Radiodiagnosis, Dr. Baba Saheb Ambedkar Hospital, New Delhi, India
2 Department of Radiodiagnosis, Mayo Institute of Medical Sciences, Barabanki, India
3 Department of Radiodiagnosis, ESI Model Hospital, Noida, India
4 Deaprtment of Radiodiagnosis & Pathology, Rohilkhand Medical College and Hospital, Bareilly, Uttar Pradesh, India

Date of Submission30-Jan-2022
Date of Decision09-Mar-2022
Date of Acceptance11-Mar-2022
Date of Web Publication27-Apr-2022

Correspondence Address:
Manish Kumar
Associate Professor, Department of Radiodiagnosis, Mayo Institute of Medical Sciences, Barabanki, UttarPradesh
India
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/am.am_18_22

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  Abstract 


Introduction: COVID-19 is an ongoing pandemic caused by severe acute respiratory syndrome coronavirus 2. Imaging plays an essential role in the diagnosis and management of symptomatic patients. Mucormycosis has gained popularity recently as a complication in COVID-19-affected patients. Various types of mucormycosis are rhino-orbito-cerebral, pulmonary, gastrointestinal, cutaneous, disseminated, and uncommon forms. Aim and Objective: We aimed to evaluate various radiological features of different types of mucormycosis infection in COVID-19 patients. Materials and Methods: We studied thirty COVID-19 patients retrospectively who were referred to our hospital over a period of 6 months (January to June 2021). Computed tomography (CT) and magnetic resonance imaging (MRI) were used for imaging evaluation of the patients. Imaging diagnosis was confirmed on histopathology in 21 patients. Results: We identified thirty cases of mucormycosis in COVID-19 patients in our tertiary center. Out of total cases, 18 were of pulmonary form, 9 of rhino-orbital form, and 3 of rhinocerebral form. Bird's nest pattern of cavitation was the most common feature in pulmonary form of mucormycosis. Acute unilateral rhinosinusitis with the presence of T2 hypointensities within periantral and intraorbital fat stranding was found to be the most specific imaging appearance in rhino-orbital form of mucormycosis. Rhinocerebral form showed contiguous spread of the disease from the sinuses to the meninges and brain parenchyma. Conclusion: Imaging plays a decisive role for early identification of the mucormycosis infection in COVID-19 patients and determination of the disease extent. CT and MRI help in accurate diagnosis of the disease and follow-up in postoperative patients.

Keywords: Bird's nest sign, mucormycosis, reversed halo sign


How to cite this article:
Chhikara R, Kumar M, Kaushik R, Gupta S, Kumar L, Mohan N. Imaging spectrum of mucormycosis in COVID-19 patients using computed tomography and magnetic resonance imaging. Apollo Med 2022;19:89-95

How to cite this URL:
Chhikara R, Kumar M, Kaushik R, Gupta S, Kumar L, Mohan N. Imaging spectrum of mucormycosis in COVID-19 patients using computed tomography and magnetic resonance imaging. Apollo Med [serial online] 2022 [cited 2022 Jul 1];19:89-95. Available from: https://www.apollomedicine.org/text.asp?2022/19/2/89/344210


  Introduction Top


COVID-19 is an ongoing pandemic caused by severe acute respiratory syndrome coronavirus 2 (SARS CoV-2). Infection ranges from asymptomatic condition to severe disease, which can be fatal sometimes.[1]

Imaging plays an essential role in the diagnosis and management of symptomatic patients second to Reverse Transcription–Polymerase Chain Reaction (RT-PCR) test. Chest computed tomography (CT) is indicated only in moderate-to-severe disease and to assess the course of the disease in these patients.[2]

COVID-19 can give variable imaging appearances ranging from ground-glass opacities to consolidation, interstitial septal thickening, and many more. Characteristic imaging features of COVID-19 on high-resolution computed tomography (HRCT) are bilateral peripheral opacities in the form of ground-glass opacities having lower lobe predominance.

Various complications of COVID-19 are acute respiratory distress syndrome, pulmonary embolism, myocarditis, and pericardial effusion, with the most recent and dreadful complication being mucormycosis.

Mucormycosis is a well-known but uncommon opportunistic fungal disease caused by mucormycetes. It is usually seen in immunocompromised patients and diabetics. Recently, it has gained popularity as a complication in COVID-19-affected patients mainly due to significant lymphopenia, inadvertent use of corticosteroids, and industrial oxygen for ventilation and uncontrolled diabetes.[3],[4]

Various types of COVID-19-associated mucormycosis (CAM) are rhino-orbito-cerebral, pulmonary, gastrointestinal, cutaneous, disseminated, and uncommon forms.[5],[6] Rhino-orbito-cerebral type is the most common form and present as an acute infection of nose and paranasal sinuses (PNSs).[5]

The aim of this study is to describe various radiological features of different forms of CAM from India so as to facilitate timely diagnosis and early treatment initiation to reduce the associated morbidity and mortality.

Objective

The objective of this study was to evaluate various radiological features of different forms of mucormycosis infection in COVID-19 patients.


  Materials and Methods Top


We did a retrospective observational study on thirty COVID-19 patients who were referred to the Department of Radio-diagnosis at Rohilkhand Medical College and Hospital, Bareilly, UP, India, over a period of 6 months from January 2021 to June 2021. Convenience sampling was done, and all the histopathologically proven and clinically suspected cases were included.

Inclusion criteria were as follows: RT-PCR-positive COVID-19 patients of both sexes with clinical suspicion of mucormycosis.

Exclusion criteria were as follows:

  • Negative RT-PCR test
  • Patients with imaging evidence of disease in sinuses, brain, or lungs prior to January 2021.


Ethical clearance was taken for this study (No. IEC/09/2021/NOV).

CT and magnetic resonance imaging (MRI) were used for imaging evaluation of the patients. Imaging diagnosis was confirmed on histopathology in 21 of the patients. The rest of the patients had similar imaging patterns to the histopathologically proven cases and showed clinical improvement on antifungal treatment.

CT was performed on a 16-slice GE Brightspeed Elite third-generation scanner using standard CT protocol. Low-osmolar, nonionic contrast agent (iohexol, 300 mg/dl) was used for contrast studies.

MRI was performed on Siemens 1.5T scanner using standard protocol. Gadolinium was used for contrast studies. MR/CT angiography was done in patients with rhinocerebral form.


  Results Top


We identified thirty cases of mucormycosis in COVID-19 patients in our tertiary center. Out of total 30 cases, 18 were of pulmonary form, 9 of rhino-orbital form, and 3 of rhinocerebral form. All of the patients had moderate-to-severe COVID-19 with CT severity scores ranging from 13 to 22. Out of 30 cases, 23 cases were diabetics.

Among all the cases, eighty percent presented after recovery from COVID-19 infection, while rest 20% cases presented during treatment for COVID-19. Rodriguez-Morales et al.[4] also found that most cases of mucormycosis occurred 10–14 days after hospitalization. The age range was from 23 to 70 years. The male-female ratio was 11:9.

Three patients with rhino-orbital form of mucormycosis had undergone surgical debridement and came for follow-up. Recurrence of the disease was found in two out of three postsurgical cases.

Diagnosis was made using CT and MRI as imaging modalities. Twenty-one cases (~70%) were confirmed by histopathology.

Pulmonary form [Table 1] came out to be the most common type of mucormycosis in COVID-19 patients, seen in 18 patients. Consolidation with variable degrees of cavitation, mass-like lesions with cavitation, and ground-glass opacities with surrounding consolidation were common imaging signs. Fifteen cases had multiple lesions, while 3 cases had a single lesion. Single or multiple lesions with cavitation and multiple internal septations, also referred to as bird's nest pattern of cavitation was the most common imaging appearance, seen in 13 of the cases [Figure 1]. Lesions with peripheral consolidation and central ground-glass attenuation, also referred as reversed halo sign [Figure 1], [Figure 2], [Figure 3] was the second most common imaging appearance. The reversed halo appearance was seen in ten of the cases. Mild peripheral enhancement was seen in five of the cases [Figure 4]. No significant postcontrast enhancement was seen in the rest of the 13 cases. The size of the lesions varied from multiple smaller nodular lesions to large mass-like lesions. Agrawal et al.[7] described reversed halo sign to be specific for pulmonary mucormycosis. Mediastinal lymphadenopathy was seen in only two cases. Enhancement was variable, with most of the lesions showing minimal to no enhancement. A background of multiple patchy peripheral areas of ground-glass attenuation with reticular opacities was seen in all the patients.
Figure 1: (a,b,c - axial; d- coronal) High resolution computed tomography image shows multiple thin-walled cavitatory lesions (yellow arrows) on the background of COVID-19. Few thin internal septations in this cavitatory lesion giving bird's nest appearance (red arrow)

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Figure 2: (a-c - Axial and d - coronal high-resolution computed tomography images) show multifocal cavitatory lesions and nodular areas of consolidation predominantly in the peripheral regions of bilateral lungs. Multifocal peripheral lesions having peripheral rim of consolidation (red arrow), central ground-glass attenuation, and cavitation (yellow arrow)

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Figure 3: (a, c, d - Axial and b - coronal high-resolution computed tomography images) show multiple thin-walled cavitatory lesions (red arrow) in both upper lobes and left lower lobe having internal septations within them. Images (c and d) show reversed halo sign

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Figure 4: (a - Axial, b - coronal, c - postcontrast axial, and d - postcontrast coronal high-resolution computed tomography images) show large mass-like cavitatory lesion in the left lower lobe with internal areas of ground-glass attenuation and air-fluid level. Mild heterogeneous enhancement in the wall of the lesion

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Multiple pulmonary nodules, pleural effusion, pulmonary thromboembolism, and pneumothorax were less commonly seen.

In the cases of rhino-orbital disease (n = 9), there was involvement of one or more PNSs. Perisinus fat stranding, spread of disease into the orbit, and bony erosion and destruction were noted. Maxillary sinus was the most commonly involved sinus and unilateral sinusitis was the predominant pattern.

Retromaxillary fat stranding was found to be typical for mucormycosis and was seen in all of the patients with involvement of maxillary sinus. In six of the patients, there was erosion of the posterior wall of the maxillary sinus, whereas in three of the patients, no signs of bony erosion were seen. The anterior premaxillary fat pad was involved in five of the patients [Table 2].
Table 1: Computed tomography chest findings in pulmonary mucormycosis (n=18)

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Table 2: Imaging findings in rhino-orbital mucormycosis (n=9)

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Unenhanced CT appearances of the involved sinus/turbinates varied from hypodense, heterogeneous to hyperdense soft tissue filling the sinuses. Contrast-enhanced computed tomography (CECT) showed heterogeneous enhancement. On MRI, heterogeneous appearance with ill-defined linear/curvilinear T2 hypointensities was characteristic of mucormycosis [Figure 5], [Figure 6], [Figure 7]. This is in coherence with a study done by Therakathu et al.[8]
Figure 5: (a and b - Axial and c - coronal T2 magnetic resonance imaging images) show mucosal thickening in bilateral maxillary, right sphenoid, and ethmoid sinuses with T2 hypointense components and showing diffusion restriction (d). There is extension of the disease into right orbital fat

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Figure 6: MRI of Brain & Orbit in a known postoperative case of mucormycosis showing residual disease. Axial T2WI (a-c), coronal T1 (e) and coronal T1 post contrast (d,f). T2 hyperintensity with postcontrast enhancement in the postdebridement cavity, the right frontal & ethmoid sinuses with extensions into the right orbital & masticator spaces (white arrows)

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Figure 7: Magnetic resonance imaging brain and orbit sagittal and coronal images in a known postoperative case of mucormycosis (a and b) show marked T2 hyperintensity showing postcontrast enhancement in the common cavity and left frontal sinus (c) around the left orbit, cheek, soft tissues of the left half of the nose. Enhancing soft tissue extending in the left masticator space, pterygoid bone, and muscles (yellow arrows)

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In rhinocerebral form [Table 3], two cases had contiguous intracranial spread of the disease from the ethmoid sinuses. In one of the patients, only edema was seen in the right frontal lobe. The other case had intracranial extension along the cribriform plate into the left frontal lobe as an abscess having thickened and enhancing wall. There was left-sided pansinusitis with T2 hypointense and T1 hyperintense contents [Figure 8]. MRI showed extension of the disease in the third case along the foramen rotundum into the extradural space of the left temporal lobe in the form of a nonenhancing collection. The collection showed diffusion restriction in the center. There was no evidence of cavernous sinus thrombosis in any of the cases. This is in contrast to a study done by Lone et al. where they found invasion of cavernous sinus.
Figure 8: Magnetic resonance imaging brain and orbit shows (a-d) bilateral ethmoid, frontal, and left maxillary sinusitis with enhancement and extension into left frontal lobe through the cribriform plate. There is a ring-like enhancing lesion in the left frontal lobe showing central diffusion restriction (arrow) and surrounding edema (a-d)

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Table 3: Imaging findings in rhinocerebral form (n=3)

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We did not find any case of gastrointestinal form of mucormycosis or involvement of other organ systems (other than sinuses, brain, or lungs).

Histopathology showed necrotic tissue with marked inflammatory areas composed of predominantly eosinophils, lymphocytes, and plasma cells. Numerous broad aseptate ribbon-like hyphae showing branching at right angles and fungal spores were also noted [Figure 9].
Figure 9: Histopathological images at ×100 (a and b) show numerous septate hyphae showing branching at acute angles with focal necrosis, extensive hemorrhage, and neutrophilic inflammatory infiltrate

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  Discussion Top


Fungal diseases such as aspergillosis and mucormycosis are opportunistic infections.

Mucormycosis has seen a spike in number of cases in COVID-19 pandemic due to multiple predisposing factors such as immunosuppression and diabetes mellitus. Due to high incidence of mortality associated with this disease, timely diagnosis and management is pivotal for better prognosis.

In our study on thirty COVID-19 patients affected with mucormycosis, pulmonary form was the most common of all, seen in 60%. Consolidation with bird's nest pattern of cavitation was found to be classically associated with mucormycosis. Reversed halo sign was another most common imaging appearance.

Garg et al. in their study on “Spectrum of imaging findings in pulmonary infections” described CT feature of pulmonary mucormycosis as nodules or consolidation with ground-glass opacities (GGOs) and reversed halo sign on subsequent imaging.

Agarwal et al. described reversed halo sign as a specific sign for diagnosis of pulmonary mucormycosis, occurring in 19%–94% of patients.

Unilateral rhinosinusitis with perisinus fat stranding, spread of disease into surrounding areas like orbit, with or without bony erosion are salient imaging manifestations of rhino-orbital mucormycosis.

Lone et al. in their study on rhino-orbito-cerebral mucormycosis found MRI to be a highly useful imaging modality for diagnosis. MRI shows T2W high signal intensity in sinonasal mucosa and infiltrating lesion in orbit. Diffusion-weighted imaging may add specificity to the diagnosis by showing diffusion restriction. CT features include mucosal thickening, absence of air-fluid level, and destruction medial orbital wall subsequently with invasion of rectus muscle, orbital apex, and cavernous sinus.

Meningitis due to spread of disease from sinuses, extra-axial collections/abscesses, cerebritis, abscesses with diffusion restriction in the walls, and/or infarcts are the different imaging findings in rhinocerebral form. Thrombosis of the internal carotid arteries may be seen if there is involvement of cavernous sinuses, and so angiographic sequences are a must.

Therakathu et al. in their study titled “imaging features of rhinocerebral mucormycosis” concluded that imaging of rhinocerebral mucormycosis shows heterogeneous variable appearance on T2WI, different enhancement patterns, and involvement of different sinuses.

Imaging features

CT and MRI are the imaging modalities of choice for accurate evaluation of involved structures and spaces.[1],[2],[8] MRI has excellent soft-tissue characterization capability, while CT gives better details about bony involvement. HRCT is the imaging modality of choice for COVID-19 patients. Early imaging is crucial for prompt diagnosis and determination of extent of involvement. Imaging features of different types of mucormycosis have been described below:

  1. Rhino-orbito-cerebral form: Most common type of mucormycosis.[5] Patients commonly present clinically with fever, headache, nasal discharge, and facial swelling.[8] Orbital swelling, limited ocular movement, chemosis, and proptosis are seen in orbital involvement.


  2. Radiography may show opacification of PNSs with/without bony erosion

    CT features are polypoidal mucosal thickening, partial or complete opacification of paranasal sinuses and absence of air-fluid levels. CT scan of PNSs and orbit may show periosteal thickening and bone destruction.[9] Hyperdense mucosal thickening is highly specific for fungal etiology[9]

    MRI appearance may range from T2 hyperintense sinus walls, T2 hyperintense lesion with internal hypointense foci extended from sinuses to orbital apex, or intracranial extension.[10] Contrast-enhanced MRI will show heterogeneous enhancement of mucosal thickening and lack of absence of enhancement of turbinates, called the “black turbinate sign.”[11] Retro-orbital fat, retro-antral fat, and extraocular muscles will show fat stranding and postcontrast enhancement[11]

  3. Pulmonary form: Second most common form of mucormycosis. Chest radiograph will show lobar/multilobar consolidation, mass-like appearance, or single/multiple lung parenchymal nodules.[12] HRCT chest shows “reversed halo sign” which is focus of GGOs surrounded by consolidation, peripheral in location.[12],[13] There is relative paucity of air bronchograms in consolidation.[7] Areas of consolidation can develop internal cavitation subsequently.[12] Irregular intersecting areas of stranding can also be seen in the area of ground-glass opacity, called “bird's nest sign.”[14] Lymphadenopathy and pleural effusion can also be found. “Vascular cutoff sign,” which is abrupt cutoff of pulmonary artery branch, can also be a feature[13]
  4. Gastrointestinal form: It occurs due to angioinvasive nature of the fungus leading to bowel infarction.[15] Stomach is the most common site in gastrointestinal tract followed by colon, small intestine, and esophagus. CT features of stomach involvement include gastric pneumatosis with reduced wall enhancement. Diffuse dilatation of bowel with wall edema, reduced enhancement and thickening involving multiple segments are seen on CECT[15]
  5. Disseminated form: Involvement of two or more parts of body contiguously[15]
  6. Uncommon form: Bone and joint involvement and renal, peritoneal, pericardial involvement.[15]



  Conclusion Top


Recent surge in mucormycosis has been noted in COVID-19 patients, especially in India. In our study, various forms of mucormycosis were found in COVID-19 patients, which had a direct correlation with the severity of COVID-19 infection and thus the degree of immunosuppression in the host.

Single or multiple cavitatory lesions with multiple internal septations producing bird's nest pattern was the most common imaging pattern seen in pulmonary form of mucormycosis in our study.

Acute invasive unilateral rhinosinusitis with the presence of T2 hypointense areas within the sinuses/nasal cavity and presence of periantral fat stranding, even in the absence of bony erosion, was the most common pattern of rhino-orbital disease. Maxillary sinus walls are most commonly involved sinus. Nonenhancing turbinates or black turbinate sign was also observed.

The rhinocerebral form of mucormycosis in our study showed contiguous involvement of the brain through the ethmoid/maxillary sinuses. Extra-axial collections, edema in the frontal lobe, and peripherally enhancing ill-defined abscess in the left temporal lobe were three different patterns observed.

Imaging was also helpful in planning the surgical management and the degree of debridement as undertreatment was found to be highly associated with recurrence (2 of 3 patients).

Knowledge of imaging spectrum of mucormycosis is of prime importance in the current COVID-19 period. A high index of clinical suspicion coupled with knowledge of the imaging signs is necessary for earliest diagnosis of the disease.

The major limitation of our study was less number of cases observed. Furthermore, only 21 of the 30 cases were confirmed histopathologically. The rest of the patients were treated for fungal infection on the basis of clinical suspicion and imaging patterns similar to histopathologically confirmed cases. These patients were kept on follow-up. Five of these patients were lost to follow-up and the rest four showed complete resolution of disease.

Based on our study, CT and MRI had an accuracy of approximately 80% (21 + 3/30 × 100) in the diagnosis of mucormycosis.

CAM is a highly morbid disease. Timely diagnosis and management is crucial to prevent disease spread and reduce recurrence and mortality. CT and MRI are highly accurate in diagnosing and characterizing mucormycosis in COVID patients as microbiological tests may be delayed.

Future recommendations

  • Every suspected case of rhino-orbital or rhinocerebral mucormycosis should be screened with MRI of the brain and Paranasal sinuses for early identification
  • Patients with immunosuppression and nonresolving pneumonia and those patients who show clinical deterioration on antibiotic therapy may be offered chest CT for early identification of fungal pathogens
  • Close collaboration with the clinical team and a combined clinical and radiological approach is essential for timely diagnosis.


Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.



 
  References Top

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Kanne JP, Bai H, Bernheim A, Chung M, Haramati LB, Kallmes DF, et al. COVID-19 imaging: What we know now and what remains unknown. Radiology 2021;299:E262-79.  Back to cited text no. 1
    
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Kwee TC, Kwee RM. Chest CT in COVID-19: What the radiologist needs to know. Radiographics 2020;40:1848-65.  Back to cited text no. 2
    
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Saidha PK, Kapoor S, Das P, Gupta A, Kakkar V, Kumar A, et al. Mucormycosis of Paranasal Sinuses of Odontogenic Origin Post COVID19 Infection: A Case Series. Indian J Otolaryngol Head Neck Surg. 2021:1-5. doi: 10.1007/s12070-021-02638-1. Epub ahead of print. PMID: 34178609; PMCID: PMC8211306.  Back to cited text no. 3
    
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Rodriguez-Morales AJ, Sah R, Millan-Oñate J, Gonzalez A, Montenegro-Idrogo JJ, Scherger S, et al. COVID-19 associated mucormycosis: the urgent need to reconsider the indiscriminate use of immunosuppressive drugs. Ther Adv Infect Dis. 2021;8:20499361211027065. doi: 10.1177/20499361211027065. PMID: 34211710; PMCID: PMC8216396.  Back to cited text no. 4
    
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Maini A, Tomar G, Khanna D, Kini Y, Mehta H, Bhagyasree V. Sino-orbital mucormycosis in a COVID-19 patient: A case report. Int J Surg Case Rep 2021;82:105957.  Back to cited text no. 6
    
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Agrawal R, Yeldandi A, Savas H, Parekh ND, Lombardi PJ, Hart EM. Pulmonary mucormycosis: Risk factors, radiologic findings, and pathologic correlation. Radiographics 2020;40:656-66.  Back to cited text no. 7
    
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Therakathu J, Prabhu S, Irodi A, Sudhakar SV, Yadav VK, Rupa V. Imaging features of rhinocerebral mucormycosis: A study of 43 patients. Egypt J Radiol Nucl Med 2018;49:447-52.  Back to cited text no. 8
    
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Garlapati K, Chavva S, Vaddeswarupu RM, Surampudi J. Fulminant mucormycosis involving paranasal sinuses: A rare case report. Case Rep Dent 2014;2014:465919.  Back to cited text no. 9
    
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Lone PA, Wani NA, Jehangir M. Rhino-orbito-cerebral mucormycosis: Magnetic resonance imaging. Indian J Otol 2015;21:215.  Back to cited text no. 10
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Awal SS, Biswas SS, Awal SK. Rhino-orbital mucormycosis in COVID-19 patients – A new threat? Egypt J Radiol Nucl Med 2021;52:1-6.  Back to cited text no. 11
    
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Garg M, Prabhakar N, Gulati A, Agarwal R, Dhooria S. Spectrum of imaging findings in pulmonary infections. Part 2: Fungal, mycobacterial, and parasitic. Pol J Radiol 2019;84:e214-23.  Back to cited text no. 12
    
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Hammer MM, Madan R, Hatabu H. pulmonary mucormycosis: Radiologic features at presentation and over time. AJR Am J Roentgenol 2018;210:742-7.  Back to cited text no. 13
    
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    Figures

  [Figure 1], [Figure 2], [Figure 3], [Figure 4], [Figure 5], [Figure 6], [Figure 7], [Figure 8], [Figure 9]
 
 
    Tables

  [Table 1], [Table 2], [Table 3]



 

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