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ORIGINAL RESEARCH
Year :   |  Volume :   |  Issue :   |  Page :  

A new diagnostic criteria and grading system of rhino-maxillary mucormycosis based on cone beam computed tomographic findings


1 Face 3D CBCT Center, Aurangabad, Maharashtra, India
2 Department of Oral Radiology, Faculty of Dentistry, SEGi University, Malaysia
3 Department of Oral and Maxillofacial Surgery, MGM Medical College and Hospital, Aurangabad, Maharashtra, India
4 Department of Periodontology, Faculty of Dentistry, SEGi University, Malaysia
5 Department of Oral Medicine and Radiology, JSSAHER Dental College and Hospital, Mysore, Karnataka, India
6 Department of Oral Pathology and Microbiology, Gian Sagar Dental College and Hospital, Rajpura, Punjab, India

Date of Submission30-May-2021
Date of Decision28-Nov-2021
Date of Acceptance05-Jan-2022
Date of Web Publication03-Nov-2022

Correspondence Address:
Pooja Muley,
Shivpooja, 229/B, Nandanvan Colony, Aurangabad - 431 001, Maharashtra
India
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Source of Support: None, Conflict of Interest: None

DOI: 10.4103/ccd.ccd_413_21

   Abstract 


Background: Mucormycosis is a rare opportunistic fungal infection, which has a rapidly progressive and fulminant course with fatal outcome. It is the need of the hour to diagnose and treat the increasing cases urgently. Aim: The aim of this article is to study the common radiographic features of rhinomaxillary mucormycosis (RMM), find diagnostic criteria, and grade the disease according to the radiographic features. Settings: This study was conducted at Face Three-Dimensional Cone-Beam Computed Tomography (CBCT) Center, Aurangabad, Maharashtra. Materials and Methods: CBCT scans of 30 patients who were referred for CBCT scanning of suspected RMM were retrospectively evaluated for relevant radiological data. Results: The most common CBCT features of RMM were osteolytic lesions in alveolar bone, palate, nose and nasal cavity, and zygoma along with involvement of paranasal sinuses. About 76.66% of patients had a history of COVID-19 infection. Conclusion: According to the collected data, the scans of probable rhinomaxillary mucormycosis were graded in three groups – mild, moderate, and severe. The goal of this article is to emphasize the most overlook diagnostic entity – CBCT and its significant importance in early diagnosis, treatment, and prognosis of RMM. Early diagnosis of RMM can save the patients from the extent of morbidity and mortality.

Keywords: Cone-beam computed tomography, grade assessment, mucormycosis, osteolytic lesions, radiology



How to cite this URL:
Muley P, Garg R, Jambure R, Gupta VV, Mahesh K P, Thind G. A new diagnostic criteria and grading system of rhino-maxillary mucormycosis based on cone beam computed tomographic findings. Contemp Clin Dent [Epub ahead of print] [cited 2023 Feb 2]. Available from: https://www.contempclindent.org/preprintarticle.asp?id=360368




   Introduction Top


The current scenario of rising cases of mucormycosis is very alarming and bewildering. Although the incidence rate of this fungal infection is 0.005–1.7 per million population, recently there has been a huge surge in the cases due to the ongoing COVID-19 pandemic.[1] With limited literature on this type of fungal infection (mucormycosis) and partial exposure of the dental surgeons to this kind of disease, there is a chaos in the dental fraternity. The health workers are navigating in the sea of multiple guidelines, trying to connect the dots and tie the loose ends. Furthermore, there are limited awareness and guidelines about the role of cone-beam computed tomography (CBCT) in the early diagnosis and prevention of spread of this disease.[1],[2]

Mucormycosis is an opportunistic fungal infection caused by the saprophytic fungi commonly found in the environment, so most humans are exposed to them daily. The occurrence of the disease usually in subjects with an underlying immunodeficiency pattern is a proof of the efficiency of the immune system against these agents. Despite adequate treatment, this infection has high mortality (40%–63%), and its prevalence has increased, probably due to the growing number and higher survival rates of immunosuppressed patients.[2]

Most of these infections are life threatening, as this fungus has particular affinity for vascular walls that cause irreversible damage through thrombosis and ischemic necrosis.[3] In the current scenario, many cases of post-COVID-19 rhinocerebral mucormycosis are being noticed. Most of the cases are rhinomaxillary mucormycosis (RMM) type of mucormycosis which predominantly report to the dental surgeons.[3],[4]

It has been observed that CBCT is one of the most underrated imaging modalities in the early diagnosis of mucormycosis. There is a paucity of literature about the use of CBCT in diagnosis of RMM. Hence, in this study, we aimed to study the common radiographic features of RMM in CBCT images, find diagnostic criteria, and grade the disease according to the radiographic features.


   Materials and Methods Top


The CBCT scans of 30 patients who were referred for CBCT scanning of suspected RMM were retrospectively evaluated for relevant radiological data. The scans were retrieved from the date – April 16, 2021, to May 15, 2021, taken Face Three-Dimensional (3D) CBCT Center, India. Power analysis (≥0.8) was undertaken to determine the sample size of 30 required for the study with a minimum kappa agreement value of 80%. The expected effect size of 1.2 was considered for the study. The whole study was designed based on the Declaration of Helsinki, where no patient was scanned for study purpose only. In this study, we have used the CBCT scans of the patients who were referred to the CBCT Center by other dentists for the confirmed radiographic diagnosis of RMM. The written informed consent and ethical clearance were obtained from the concerned authorities of the CBCT Center.

Inclusion and exclusion criteria

  • Scans of patients with clinical features of rhinomaxillary mucormycosis were selected
  • Scans with only maxillary involvement were selected
  • Scans with mandibular findings were excluded
  • Scans with other pathologies such as cysts, tumors, and fractures were excluded.


Limitations of the study

The study is based mainly on the basis of radiographic features as seen on CBCT. The clinical, histopathological features and surgical notes are only used to support the study outcomes. Details of history, clinical picture, and surgical, postoperative, and medicinal outcomes are not included in the study because the aim is to study the common radiographic features of RMM, find diagnostic criteria, and grade the disease according to the radiographic features.

The CBCT scan was performed on an Osstem T1 CBCT machine using a routine CBCT protocol. 3D imaging data were acquired at 95 kV and 6 mA. The scan time was within a range of 22 s and voxel size was 200 μm. Scans were then obtained in sagittal, axial, and coronal views. Each multiplanar data measuring 200 × 200 × 200 μm pixels at 32 bits was stored in the computer. A retrospective review was performed by an oral radiologist to look for sites and extent of involvement, other characteristics, and complications. Permission and consent of the patient were obtained for using the scans for study purposes. Histological evidence of confirmed mucormycosis was later retrieved.

Technique

  1. The DICOM data were imported into CS 3D software and CBCT images were analyzed. The brightness and the contrast of images were optimally adjusted so that the structures were clearly visualized. All interpretations and assessments were done in appropriate best-visualized sections. The scan was assessed for any osteolytic changes, paranasal sinus, and nasal abnormalities. The following areas were used to measure the involvement.
  2. Oral cavity


    1. Palatal bone involvement with decreased bone density, sparse trabecular pattern, osteolytic moth-eaten appearance, and palatal perforation
    2. Involvement of alveolar bone – decreased bone density, sparse trabecular pattern, erosion, and osteolytic moth-eaten appearance and loss of cortical plates
    3. Dental findings may or may not be present such as periapical and periodontal abscesses, changes in the periodontal ligament space and lamina dura, and uneven interdental bone loss.


  3. Paranasal sinuses – maxillary, ethmoidal, frontal, and sphenoidal

    Mucositis, opacification, air entrapment, ostia, bone, rarefaction, erosions, and permeative destruction of walls.
  4. Nose – thickening of nasal mucosa, osteolysis of nasal bone, nasal septa, lateral wall of nasal cavity, and floor of nasal cavity. Turbinates – hypertrophy, osteolysis, or air entrapment.
  5. Orbit – changes in floor of orbit, lamina papyracea, and walls of orbit.
  6. Other bones – erosion and osteolysis of zygomatic complex and sphenoid sinus cortices.


Based on the above parameters, CBCT diagnostic criteria were developed for mucormycosis [Table 1].
Table 1: Developed cone-beam computed tomography diagnostic criteria

Click here to view



   Results Top


All the 30 scans were studied and graded and the data obtained were tabulated immediately. Among the 30 patients, 11 patients were operated and histopathological report of 11 patients was available. Hence, out of 30 scans of probable RMM, 11 scans (36.66%) were confirmed cases of RMM. Twenty-two (76.66%) patients had history of COVID-19 infection and hospitalization for the same. The remaining 23% of patients were labeled as probable RMM on the basis of their history, clinical features, and nasal endoscopic findings.

It was found that both the maxillary sinuses were involved in 66.66% of cases with more predilection toward the right side showing 76.66% involvement. Enlarged ostium was seen in 40% of scans, while changes in the discontinuity in the floor or wall of at least one maxillary sinus were seen in 76.6% of cases. Ethmoidal sinus was involved in 66.66% of cases with destruction of lateral wall of ethmoid seen in 36.6% of scans. Frontal sinus of at least one side was involved in 43.33% of cases and sphenoid sinus of at least one side was involved in 33.33% of cases.

Osteolytic changes like erosion of bone, loss of cortices and changes in the trabecular pattern was seen in 96.66% scans. The remaining 3.33% of scans showed a significant increase in the density of alveolar bone with tightly packed trabeculae along with involvement of both maxillary sinuses, while 60% of scans showed palatal involvement and 16% showed palatal perforation. The nasal involvement was seen in 70% of cases. Zygomatic and sphenoidal involvement was seen in 3.33% of cases. Dental findings were found in 66.66% of cases [Table 2] and [Table 3].
Table 2: Cone-beam computed tomography features of paranasal sinuses

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Table 3: Cone-beam computed tomography features of involvement of bones

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In the present study, it was found that only 6.6% of cases were in Grade 1 (mild), while 53.5% were in Grade 2 (moderate), and 40% were in Grade 3 (severe) [Table 4].
Table 4: Classification of patients based on the severity of rhinomaxillary mucormycosis

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   Discussion Top


Mucormycosis most commonly affects patients with poorly controlled diabetes mellitus, especially during ketoacidosis attacks, which corresponds to 88% of reported cases of rhinocerebral mucormycosis. Other immunocompromised patients at risk are those with malignancies, transplanted organs, or long-term immunosuppressive or corticosteroid treatment.[4]

COVID-19 disease has a propensity to cause extensive pulmonary disease and subsequent alveolo-interstitial pathology. This by itself may predispose to invasive fungal infections of the airways including the sinuses and the lungs.[5] Furthermore, there is an alteration of the innate immunity due to COVID-19-associated immune dysregulation characterized by decreased T cells, including CD4 and CD8 cells.[6] Other factors like steroid administration, immunomodulating drugs like tocilizumab, and high doses of Vitamin C, oxygen therapy, and prolonged hospitalization predispose the development of mucormycosis.[7],[8] It has been highlighted in the published literature that in the past 14 months (December 2019–April 21), India has contributed up to 71% of mucormycosis cases in COVID-19-positive patients globally.[9] In the present study, it was found that seven patients were not having a history of COVID-19. Among these, all of the patients had a long-term history of underlying diseases (like uncontrolled diabetes mellitus and autoimmune diseases) and/or the use of immunosuppressive drugs. Another important and most overlooked factor is that there is a possibility of the patients to have developed COVID-19 infection (asymptomatic or mild) which was not diagnosed.

Mucormycosis has been categorized under six variants including the rhinocerebral form which is one of the most common types occurring in the maxillofacial region, having high mortality rate. This form of mucormycosis is further subclassified as rhinomaxillary, rhino-orbital, and rhino-orbito-cerebral forms. In this type of variant, there is widespread involvement of maxillary alveolar bone, palate, and teeth along with the paranasal sinuses.[4] These patients can clinically develop the symptoms such as mucositis, headache, nasal blockage, black eschar formation, ulcerations, facial pain, or even bone necrosis.[5] This case study is focused on the rhinomaxillary variant of the mucormycosis having more intracranial and orbital complications.

Diagnosis is based on the clinical symptoms and signs are supported by diagnostic nasal endoscopy findings, or advanced imaging modalities such as contrast-enhanced magnetic resonance imaging (MRI), medical CT (MDCT), or CBCT, coupled with microbiological confirmation on direct microscopy or culture or histopathology.[10] Each of these imaging modalities has their own indications and guidelines to be used in the head-and-neck region. In most of the cases of mucormycosis, medical computed tomography has been widely used to diagnose the extension of lesion in the rhinomaxillary region. MRI is deemed to be suitable to evaluate the soft-tissue changes. Cone-beam CT (CBCT), which is a comparatively recent imaging technology in dentistry, provides images equivalent to MDCT at reduced costs and radiation doses. Although the MDCT provides with the better image quality, CBCT shows small spatial variations like initial bone changes. However, some of the studies have proved that CBCT scan shows the superior module transfer function as compared to CT scan with relatively low screening time.[11],[12] This helps in evaluating the minute changes in trabecular pattern or decrease in cortical thickness in RMM cases. However, if indicated, MRI can be used as the complimentary imaging modality to look for soft-tissue details in certain cases.

The present study is consistent with the findings of various case reports of RMM in the aspect of osteolytic lesions in alveolar bone, palate, nose and nasal cavity, and zygoma along with involvement of paranasal sinuses.[13],[14],[15],[16]

In this study, a significant relation between the history of COVID-19 infection and mucormycosis was found, about 80% of patients, which is consistent with a few similar studies.[7],[8]

According to the collected data, the scans of probable rhinomaxillary mucormycosis were graded in three groups – mild, moderate, and severe:

  1. Mild – decreased bone density in localized area, at least one sinus involvement, increased thickening of nasal mucosa, or hypertrophy of at least one nasal turbinates [Figure 1]
  2. Moderate – decreased bone density AND/OR osteolytic lesions in alveolar bone, walls of maxillary and ethmoidal sinus, breach in sinus floor/walls, involvement of maxillary and ethmoid sinuses, mild destruction of nasal turbinates, or nasal septum [Figure 2]
  3. Severe – decreased bone density AND/OR osteolytic lesions in alveolar bone, multiple osteolytic lesions in walls of sinuses, multiple perforations including palatal perforation, and involvement of all sinuses including sphenoid sinus [Figure 3].
Figure 1: Mild: (a) Coronal section showing sinusitis of right maxillary sinus and normal ethmoid sinus. (b) Sagittal section showing no involvement of frontal and sphenoidal sinuses (c) Axial section showing sinusitis of right maxillary sinus. (d) Three-dimensional reconstruction showing normal surface appearance of maxilla

Click here to view
Figure 2: Moderate: (a) Coronal section showing maxilla with osteolytic lesion of alveolar bone with moth eaten, loss of cortication, and breach in lateral wall of maxillary sinus and palate. (b) Sagittal section showing no involvement of sphenoidal sinuses. (c) Axial section showing sinusitis of right ethmoid sinus. (d) Three-dimensional 3D reconstruction showing surface resorption of right maxilla

Click here to view
Figure 3: Severe: (a) Coronal section showing complete osteolysis of right side of maxilla with palate, walls of maxillary sinus, and turbinates. (b) Sagittal section showing involvement of frontal and sphenoidal sinuses (c) Axial section showing sinusitis of right ethmoid sinus along with osteolysis of turbinates. (d) Three-dimensional reconstruction showing osteolysis of right maxilla

Click here to view


Grading of the rhinomaxillary mucormycosis based on radiographic features as seen in CBCT scans was developed [Table 5].
Table 5: Cone-beam computed tomography grading of rhinomaxillary mucormycosis

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The significance of grading is to categorize the patients according to the treatment needed and their prognosis. In the present study, it was observed that Grade 1 patients can be treated by endoscopic sinus evacuation and surgical removal of soft-tissue lesion if any. These patients have a good prognosis.

Grade 2 and 3 cases have to undergo aggressive debridement of dead tissues by open surgeries – partial or complete maxillectomy, debridement of zygoma, orbital floor, and exenteration of eye in the case of orbital involvement. The prognosis of Grade 2 patients can be said to be fair while that of Grade 3 patients can have a poor prognosis.

Till now, there is no robust staging system to categorize the disease severity of RMM based on radiographic features as seen in CBCT images. The proposed staging system is simple and follows the general anatomical progression of rhino-orbital-cerebral mucormycosis. CBCT is useful in the diagnosis of rhinomaxillary mucormycosis, providing detailed information about extension of the lesion in the adjacent vital structures, but in case of orbital and intracranial extensions, MDCT or MRI is indicated.[14]

The limited sample size has been used in the study with the targeted regional population, and within the limited time frame of a month. However, the current study can be considered to be the first study to categorize the cases of the RMM based on the CBCT findings. In future, this study can be used as the reference for studying the validity of CBCT as the early diagnostic tool for diagnosing the cases of RMM in the larger sample size.


   Conclusion Top


RMM being a rapidly progressive disease, even a slight delay in the diagnosis or appropriate management, can have devastating implications on patient survival. However, the outcome can be optimized by early diagnosis which can be achieved by using CBCT as an early diagnostic modality.

Acknowledgments

We specially thank Face 3D CBCT Center for the data and CBCT scans.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.



 
   References Top

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Martínez-Herrera E, Julián-Castrejón A, Frías-De-León MG, Moreno-Coutiño G. Rhinocerebral mucormycosis to the rise? The impact of the worldwide diabetes epidemic. An Bras Dermatol 2021;96:196-9.  Back to cited text no. 3
    
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    Figures

  [Figure 1], [Figure 2], [Figure 3]
 
 
    Tables

  [Table 1], [Table 2], [Table 3], [Table 4], [Table 5]



 

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