Imaging spectrum of rhino-orbital-cerebral mucormycosis secondary to COVID-19 infection: a reporting checklist

Abstract

In recent times, India has been in the midst of a notifiable epidemic of mucormycosis (a rare angio-invasive fungal infection), within the ongoing global coronavirus disease 2019 (COVID-19) pandemic. Epidemiological studies have reported the estimated prevalence of mucormycosis to be around 70 times higher in India as compared to the global data, even in the pre-COVID era. However, in the last 3 months, our city witnessed an unprecedented surge in cases of post-COVID-19-associated rhino-orbital-cerebral (ROC) mucormycosis. This pictorial review aims to illustrate the entire imaging spectrum of mucormycosis in the head-neck-face region. Along with the usual sites (nose, paranasal sinuses, orbits), this disease also involves the skull base, palate, temporal bone, and deep neck spaces. Many cases also demonstrated morbid and, at times, fatal intracranial and neurovascular complications. This review also aims to provide a structured reporting template that will prove useful to the radiologists interpreting imaging studies of ROC mucormycosis.

Keywords: COVID-19; diagnostic imaging; mucormycosis; rhino-orbital-cerebral.

Figure 1

Early imaging findings in a patient with COVID-19 and rhino-orbital-cerebral (ROC) mucormycosis. Axial (A, C) and coronal (B, D) computed tomography images of the paranasal sinuses in the soft tissue (A, B) and bone window settings (C, D) show irregular mucosal outlines with soft-tissue thickening along the nasal septum (white arrows) and the middle turbinate (red arrows) on the left side

Figure 2

“Black-turbinate sign” on magnetic resonance imaging in a COVID-19-positive patient with rhino-orbital-cerebral (ROC) mucormycosis. A) Axial post-contrast fat-suppressed T1-weighted (T1W) image shows poorly enhancing mucosa along the nasal septum on the right side. B) Coronal short-tau inversion recovery (STIR) image of the nasal cavity shows low signal intensity of the affected left middle turbinate (red arrow), compared to the normal signal intensity on the right side. Axial (C) and coronal (D) post-contrast fat-suppressed T1W images in the same patient show non-enhancing mucosa over the left middle turbinate – “black-turbinate sign” (red arrows). This indicates necrotic eschar

Figure 3

“Black turbinate sign” – a potential diagnostic pitfall magnetic resonance imaging in a normal immunocompetent patient – axial (A) and coronal (B) post-contrast fat-suppressed T1-weighted (T1W) images demonstrate benign non-enhancing inferior turbinates with non-enhancement most pronounced in the posterior aspects of both the inferior turbinates (white arrows). The turbinates show preserved thin peripheral rim enhancement along with thin enhancing internal septa. This potential diagnostic pitfall is to be considered while reporting the characteristic “black turbinate sign” seen in suspected acute invasive fungal rhinosinusitis (AIFRS)

Figure 4

Right maxillary sinus mucormycosis and spread to peri-sinus tissues in a patient with COVID-19. Axial computed tomography (CT) images of the paranasal sinuses (PNS) in soft tissue window (A, B) show mild soft-tissue mucosal thickening along the walls of the right maxillary sinus (red arrows). Axial CT images in the bone window (C, D) demonstrate thinning, erosion, and dehiscence of the anterior and lateral walls of the right maxillary sinus (thick white arrows). Mild soft tissue thickening with loss of normal fat planes seen along the anterior and posterior walls of the right maxillary sinus (thin white arrows), indicating peri-sinus extension of infection through the bony dehiscence

Figure 5

Magnetic resonance imaging (MRI) of maxillary sinus mucormycosis and peri-sinus spread of infection. Axial (A) and coronal (B) post-contrast fat-suppressed (FS) T1-weighted (T1W) MRI images in a COVID-19-positive patient, demonstrate soft tissue mucosal thickening along the walls of both the maxillary sinuses with focal areas of non-enhancement and focal areas of break in the enhancing mucosal lining (white arrows). Post-contrast FS T1W coronal image (C) in another patient shows focal discontinuity in the enhancing mucosal lining of the right maxillary sinus (thick white arrow) with spread of disease to the peri-sinus tissues. As a result, swelling and hyperintense signal abnormality of the right temporalis and masseter muscles (yellow arrows) is seen with loss of intervening fat planes

Figure 6

In a patient with COVID-19-related paranasal sinus mucormycosis, the coronal computed tomography image in bone window (A) shows thinning, erosion, and dehiscence of the roof, floor, and medial bony wall of the left maxillary sinus (white arrows). Soft tissue window images (B, C) reveal mucosal thickening of the maxillary and ethmoid sinuses on the left side. The fungal disease is infiltrating the left infra-orbital nerve canal and is extending into the left orbit to involve the left inferior rectus muscle that appears thickened (yellow arrows). Note the normal infra-orbital nerve canal on the right side (red arrow)

Figure 7

Axial soft-tissue window computed tomography images of the paranasal sinuses (PNS) (A, B) in a COVID-19-positive patient. Severe soft tissue mucosal thickening resulting in complete opacification of the right maxillary sinus (white star) with soft tissue infiltration and fat stranding involving the premaxillary and retro-maxillary spaces on the right side (white arrows). This peri-sinus extension of the fungal disease has occurred through an intact intervening bone. Note the normal premaxillary and retro-maxillary fat planes on the left side

Figure 8

Computed tomography (CT) and magnetic resonance imaging (MRI) of the paranasal sinuses in a patient with COVID-19-related mucormycosis. Axial CT images in soft tissue (A) and bone window (B) show complete opacification of the right maxillary sinus by soft tissue thickening with dehiscent medial and postero-medial walls of the sinus. Extension of the disease process seen into the right pterygopalatine fossa (yellow arrows). Post-contrast fat-suppressed T1-weighted (T1W) axial MR images (C, D) demonstrate hypointense, non-enhancing right maxillary sinus along with oedematous changes and abnormal enhancement along the right pterygopalatine fossa

Figure 9

Permeative osteolysis of the hard palate and alveolar process of maxilla in a patient with COVD-19-related mucormycosis. Coronal post-contrast fat-suppressed T1-weighted (T1W) image (A) shows right maxillary sinus soft-tissue mucosal thickening. Areas of focal discontinuity seen along the enhancing mucosal lining of the sinus (red arrow). Coronal computed tomography (CT) (bone window) (B) shows dehiscence of the medial and lateral walls and erosion along the floor of the sinus (white arrows). Coronal CT as well as coronal (A) and axial (C, D) post-contrast, fat-suppressed T1W MRI images demonstrate peri-sinus extension of fungal disease, resulting in permeative osteolysis of the alveolar process of maxilla and hard palate on the right side (yellow arrows). They also demonstrate enhancing, inflammatory soft tissue thickening along the undersurface of the hard palate on the right side (blue arrows)

Figure 10

In a patient with COVID-related mucormycosis, bilateral ethmoid sinus soft-tissue mucosal thickening seen on the axial short-tau inversion recovery (STIR) (B) and axial unenhanced, fat-suppressed T1-weighted (T1W) (D) images (blue asterisk). Intra-orbital extension of the disease into the extra-conal and intra-conal compartments seen on the left side (B, D – blue arrows). Proptosis of the left eyeball with pre-septal thickening and fat stranding is evident (A, B, D – white arrows). Retro-orbital fat stranding with involvement of medial and lateral rectus (extra-ocular) muscles seen on the left (B, D – yellow arrows). Oedema and fat stranding noted in the left pre-maxillary space (C – thick white arrow). Disease extension seen into the left pterygomaxillary fissure (C – red arrow)

Figure 11

Lacrimal sac and nasolacrimal duct involvement in a COVID-19-positive patient with right maxillary sinus mucormycosis. Coronal computed tomography (CT) image (A) shows soft tissue thickening resulting in opacification of the right lacrimal sac (thin white arrow); note the fully aerated left lacrimal sac (blue arrow). This soft tissue thickening is seen extending into the nasolacrimal canal and is involving the nasolacrimal duct on the right side (red arrows) on the coronal (B) and axial (C) CT images. Soft tissue thickening and infiltration seen in the right premaxillary subcutaneous region (D – thick white arrow). Severe mucosal thickening causing opacification of the right maxillary sinus (asterisk) is noted (C, D)

Figure 12

Orbital apex syndrome in a patient with COVID-19-related mucormycosis. Post-contrast fat-suppressed T1-weighted (T1W) axial (A, B) and coronal (C, D) magnetic resonance (MR) images show enhancing mucosal thickening of both the ethmoid sinuses, more on the left side. Soft tissue thickening with post-contrast enhancement is seen at the left orbital apex (A – white arrows) and the left superior orbital fissure (B, C – yellow arrows). Thickening and enhancement is seen along the posterior intra-orbital (B) and intracanalicular portions of left optic nerve (white arrows). These imaging features depict orbital apex syndrome related to posterior ethmoid and onodi cell sinusitis (C, D – thick white arrow)

Figure 13

Magnetic resonance imaging of the orbits in a patient with COVID-19 related mucormycosis. Axial (A) and coronal (B) FLAIR images show mild focal swelling with hyperintense signal abnormality of intra-orbital segment of the right optic nerve (white arrows), suggesting right optic neuritis. Pre-septal thickening and oedema is also seen on the right side (yellow arrow). Soft-tissue mucosal thickening is seen involving the anterior and posterior ethmoid air-cells, bilaterally (black asterisk)

Figure 14

Known case of post-COVID mucormycosis treated with surgical debridement. Secondary osteomyelitis seen involving the central skull base. Coronal computed tomography images (A, B) in bone window demonstrate permeative osteolysis and bone destruction of the basi-sphenoid, sphenoid sinus, greater wing of sphenoid, pterygoid process on the left side (white arrows). Soft tissue mucosal thickening in the sphenoid sinus (B – yellow arrow). Axial (C) and coronal (D) post-contrast fat-suppressed T1-weighted images show marked enhancement involving the structures in the left infra-temporal fossa and masticator space (red arrows). Dural enhancement is seen along the middle cranial fossa (blue arrow)

Figure 15

In a COVID-positive patient with sphenoid sinus mucormycosis, short-tau inversion recovery (STIR) coronal magnetic resonance images (A-C) and post-contrast fat-suppressed T1-weighted (T1W) coronal image (D) demonstrate asymmetric soft tissue thickening and enhancement of the left cavernous sinus (yellow arrows) and Meckel’s cave (white arrows), indicating extension of the fungal disease to these sites. Asymmetric thickening and enhancement of the cisternal segment of the left trigeminal nerve (red arrows), suggest peri-neural spread of the disease

Figure 16

COVID-positive patient with sphenoid sinus disease (asterisk). Post-contrast fat-suppressed (FS) T1-weighted (T1W) axial (A) image demonstrates extension of the fungal infection into left cavernous sinus and Meckel’s cave (white arrows). On the coronal post-contrast FS T1W image (B), the left trigeminal nerve appears thickened and shows post-contrast enhancement in its cisternal portion, close to the root exit zone (black arrows). Cisternal and cavernous segments of the left trigeminal nerve are infiltrated by the disease and show restricted diffusion (black arrows) on the DWI (C) and corresponding ADC images (D). Sphenoid sinus fungal infection also shows restricted diffusion (C, D – black asterisk)

Figure 17

Frontal bone osteomyelitis in a patient with COVID-related right frontal mucormycosis. Axial (A-C) and coronal (D) post-contrast fat-suppressed (FS) T1-weighted (T1W) images demonstrate right frontal sinusitis (yellow arrows). The anterior and lateral aspects of the frontal bone demonstrate signal abnormality (thick white arrow) with an overlying enhancing subperiosteal collection on the right side (thin white arrows). Adjacent pachy-meningeal thickening, enhancement in the right frontal region (red arrows). Intra-orbital, extra-conal extension of the disease process noted along the supero-lateral aspect of the right orbit (blue arrow)

Figure 18

Intracerebral fungal abscesses in a patient with COVID-related mucormycosis. Short-tau inversion recovery (STIR) coronal (A) and post-contrast fat-suppressed (FS) T1-weighted (T1W) axial (B) images show multiple focal fungal abscesses with surrounding perilesional oedema, in the frontal and parietal brain parenchyma, bilaterally. Their walls appear hypointense on STIR (white arrow) and show thin peripheral enhancement (yellow arrow) on the post-contrast images. The walls appear hyperintense on DWI image (C) and dark on corresponding ADC image (D), suggesting restricted diffusion (white arrows). They appear hypointense on SWI (black arrow) due to susceptibility artifacts (E)

Figure 19

In a known case of COVID-related mucormycosis, post-contrast fat-suppressed (FS) T1-weighted (T1W) axial (A) and coronal (B) images reveal arterial wall enhancement (white arrows) and mild luminal narrowing of the cavernous segment of right internal carotid artery (ICA), suggesting fungal arteritis. In another patient with COVID-related mucormycosis, DWI (C) and corresponding ADC (D) images of the brain show acute embolic infarcts (yellow arrows) in the left fronto-parietal brain parenchyma

Figure 20

Imaging of skull base in a patient with chronic symptoms of skull-base involvement following COVID-19 infection. Soft-tissue mucosal thickening of the sphenoid sinus (yellow arrow) with areas of dehiscence of its bony walls seen on coronal and axial computed tomography (CT) (A, B). Post-contrast fat-suppressed (FS) T1-weighted (T1W) coronal magnetic resonance (MR) image shows break in continuity of the enhancing mucosal lining of the sphenoid sinus (C), indicating peri-sinus spread of disease. Permeative osteolysis, bone destruction of the basi-sphenoid, greater wings of sphenoid and parts of the petrous temporal bone, better appreciated on CT (bone window – white arrows). Dural enhancement along the middle cranial fossa (red arrows) and in-flammatory enhancement of the infra-temporal fossae (blue arrows) seen on post-contrast MRI (C, D). Imaging diagnosis of central skull-base osteomyelitis, probably due to indolent mucormycosis, was considered