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. 2023 Jan 17;11(12):7891–7896. doi: 10.4103/jfmpc.jfmpc_1433_22

Trends of rhino-orbito-cerebral mucormycosis in COVID-19 patients: An observational study

Nimmi Singh 1, Swati Singh 1,✉, Priyankar Singh 2, Navin Mishra 1, Bibhuti P Sinha 3, Arbind K Shrama 1
PMCID: PMC10041009  PMID: 36994064

ABSTRACT

Background and Aim:

Mucormycosis is a potentially lethal but rare fungal infection that is rapidly progressive. Rhino-orbito-cerebral mucormycosis (ROCM) was the predominant presentation of COVID-19-associated mucormycosis (CAM). Hence, the present study aimed to assess the oral manifestations in CAM patients admitted to the Indira Gandhi Institute of Medical Sciences—A Tertiary Health Care Center.

Materials and Methods:

This study was conducted on hospitalized patients admitted to our tertiary health care center during the second wave of the COVID-19 pandemic. A total of 54 patients were included in the study and were further evaluated for oral manifestations. Detailed history, clinical examination, and surgical exploration was done for all the subjects. All cases were confirmed by MRI and histopathology.

Results:

Data collected was subjected to descriptive and inferential statistical analyses. Patients with oral manifestations were mostly in the age range of ≤50 years which was 56.7% (n = 17). Male patients 56.7% were affected more as compared to female patients and most of the patients in our study were from rural areas 56.7%. RBS [Mean ± standard deviation (SD)] was 304.60 ± 100.073. On intra-oral examination 96.7% had a gingival and palatal abscess, 63.3% had tooth mobility, and palatal ulcer/perforation was seen among 56.7% of the patients.

Conclusion:

The second wave of the COVID-19 pandemic had also created an alarming situation in India and worldwide. Mucormycosis had come as a sudden storm which has created an emergency situation in our hospital and for dental practitioners also. This was also an alarming situation for a dental practitioner for evaluating early signs and symptoms, especially in high-risk patients and decreasing mortality.

Keywords: COVID-19, diabetes mellitus, mucormycosis, oral manifestations, random blood sugar

Introduction

Mucormycosis is a potentially lethal but rare fungal infection caused by fungi belonging to class zygomycetes/phycomycetes and order Mucorales which was first described by Paultauf.[1,2] The organisms are found throughout the world growing in their natural state on various decaying materials.[3] Spores are liberated in the air and enter the human host through inhalation, ingestion, or direct inoculation.[4] This angioinvasive fungal infection manifests in four forms, rhinocerebral, pulmonary, gastrointestinal, and disseminated.[5] Currently, Mucorales fungi are the next most common invasive opportunistic fungal infection in patients with diabetes, which is the commonest underlying risk factor globally.[6] In India, the prevalence of mucormycosis is approximately 0.14 cases per 1,000 population, which is about 80 times the prevalence of mucormycosis in developed countries.[7]

The most important conditions that predispose to mucormycosis, according to various studies, include diabetes mellitus (DM), malignancies, transplantation, prolonged neutropenia, corticosteroids, trauma, iron overload, illicit intravenous drug use, neonatal prematurity, and malnourishment.[8-10]

In patients with DM invasive fungal infection, mucormycosis is one of the most life-threatening conditions. The rising trend of mucormycosis associated with diabetes is commonly seen in uncontrolled DM and has a fatality rate ranging from 32 to 57%. Type-2 diabetes is more frequently associated with mucormycosis, whereas type-1 accounted for 20% of the diabetes cases in the largest retrospective cohort so far.[11] In India, uncontrolled DM was the most commonly found predisposing factor in 74% (n = 131) of the 178 cases identified between 2000 and 2004.[12]

DM is an immunocompromised state due to changes in the pathophysiology, that is, alteration in innate immunity and impaired adaptive immunity. Inflammatory cytokine production, including interleukin-1 (IL-1), IL-6, tumor necrosis factor-alpha (TNF-a), and interferon-gamma (IFN-g), is also reduced.[13,14] The impaired cellular pathway is responsible for Mucorales invasion in diabetes. Platelets also play an important role by hampering the development and germination of Mucorale hyphae.[15] The association between DM and sinus-cavity involvement has been extensively described in the literature and is strongly linked to Rhizopus spp. which leads to more frequent rhino-orbito-cerebral involvement. Fungal hyphae produce a substance called rhizoferrin which binds with iron to form iron-rhizoferrin complex. The low pH, hyperglycaemic state, and iron-rich environment in diabetic patients favor the fungal growth, and the complex is taken by this fungus and becomes available for the vital intercellular process.[16]

Commonly seen clinical features are nasal obstruction or congestion with noisy breathing, headache, odontalgia, sinusitis with low-grade fever and unilateral facial swelling, maxillary pain, and hyposmia or anosmia. Unilateral or bilateral orbital swelling may be observed with ophthalmoplegia and ptosis, in severe cases, necrosis of skin and eye can be seen as a blackened eschar which are indicators of rapidly invasive disease. Intra-oral changes may manifest as osteomyelitis of the maxilla, perforation of the hard palate, gingival ulcerations, sinus formation, and tooth mobility. Central nervous system involvement may manifest as cranial nerve palsy, seizure, hemiplegia, etc. Cases of mucormycosis can be diagnosed by clinical findings and any associated host factor (i.e. DM is considered a risk factor), radiological signs of disease, and microbiological culture of samples isolated from the pathological site. The treatment protocol is the correction of underlying disease, antifungal drugs as monotherapy or combination therapy, and surgical treatment.

The present study was conducted to assess the oral manifestations in COVID-19-associated mucormycosis (CAM) patients admitted to the Indira Gandhi Institute of Medical Sciences-A Tertiary Health Care Center.

Aim and Objectives

  1. To assess the oral condition in patients diagnosed with COVID-19-associated ROCM.

  2. To evaluate the status of COVID-19 vaccination in the urban and rural areas.

  3. To evaluate the blood sugar level in COVID-19-associated ROCM.

  4. To bring awareness among patients suffering from DM for early detection and treatment of mucormycosis.

Materials and Methods

Study population

The study protocol was approved by the ethical committee and was conducted in accordance with the Declaration of Helsinki. This study conformed with the Strenghtening the Reporting of Observational studies in Epidemiology (STROBE) guidelines for conducting human observational studies. The study was conducted on hospitalized patients admitted to our tertiary health care center during the second wave of COVID-19 pandemic. A total of 60 stable COVID-19 patients with ROCM reporting to emergency Out Patient Department (OPD) of Indira Gandhi Institute of Medical Sciences (IGIMS), Patna, were enrolled in the study. Out of 60 patients, 6 were excluded from the study as they became unstable and were shifted to the intensive care unit. All the volunteers who participated in the study provided written informed consent. Detailed history, clinical examination, and surgical exploration were done for all the subjects. All cases were confirmed by Magnetic Resonance Imaging (MRI) and histopathology. Patients were excluded if the following conditions were observed: 1) Patients reporting from other hospitals, 2) Patients suffering from diseases other than ROCM.

Collection of clinical data

Clinical data was collected from the subjects who were admitted in wards of IGIMS during the second wave of the COVID-19 pandemic between May and June 2021. There were separate wards for COVID-19 positive with mucormycosis and COVID-19 negative with mucormycosis stable and unstable patients. By taking all the precautionary measures data was collected by a single examiner visiting the ward. Intra-oral, extra-oral examination and a detailed history regarding age, gender, place, vaccination history, diabetic history, and others were taken from all the 54 stable COVID-19 positive or negative patients with mucormycosis.

Statistical analysis

Descriptive and inferential statistical analyses were carried out in the present study. Results on continuous measurements were presented on Mean ± standard deviation (SD) and results on categorical measurement were presented in number (%). The level of significance was fixed at P = 0.05 and any value ≤0.05 was considered to be statistically significant.

Chi-square analysis was used to find the significance of study parameters on a categorical scale.

Based on the results of the normality test (Kolmogorov–Smirnov and Shapiro–Wilk test), it was concluded that part of the data is not following the normal distribution; hence, non-parametric test was used. Mann–Whitney U test was used to find the significance of study parameters on a continuous scale between two groups. Kruskal–Wallis test was used to find the significance of study parameters between three and more groups.

The statistical software IBM Statistical Package for Social Sciences (SPSS) statistics 20.0 (IBM Corporation, Armonk, NY, USA) was used for the analyses of the data, and Microsoft word and Excel were used to generate graphs, tables, etc.

Results

A total of 54 patients were included in the study among which 30 patients with mucormycosis presented oral symptoms. Patients with oral manifestations were mostly in the age range of ≤50 years which was 56.7% (n = 17). Male patients 56.7% were affected more as compared to female patients and most of the patients in our study were from rural areas 56.7% [Table 1]. Most of the patients in the above-mentioned group were non-vaccinated 63.3% during the second wave of the pandemic. The one vaccinated had mostly taken only the first dose 26.7% and only 10% had taken the second dose. In our study about 70% of patients had shown a positive association between intake of steroids and mucormycosis [Figure 1]. On intra-oral examination 96.7% had a gingival and palatal abscess, 63.3% had tooth mobility, palatal ulcer/perforation [Figure 2] was seen among 56.7% of patients [Table 1]. Tooth mobility was seen most involving upper premolar and molar teeth. On extra-oral examination, facial/periorbital swelling was seen in 100% of all the patients, 33.3% of patients had discharge/blocked nose, and 30% of patients had drooping of eyelids/blurred vision.

Table 1.

Descriptive statistics (n=30)

Variables Sub-groups n %
Age group ≤50 years 17 56.7
>50 years 13 43.3
Gender Male 17 56.7
Female 13 43.3
Location Urban 13 43.3
Rural 17 56.7
Vaccination status Not vaccinated 19 63.3
First dose 8 26.7
Second dose 3 10.0
Intake of steroids No 9 30.0
Yes 21 70.0
Gingival/Palatal abscess Absent 1 3.3
Present 29 96.7
Tooth mobility Absent 11 36.7
Present 19 63.4
Palatal ulcer Absent 13 43.3
Present 17 56.7
Facial/Periorbital swelling Absent 0 0.0
Present 30 100.0
Discharged/Blocked nose Absent 20 66.7
Present 10 33.3
Drooping of eyelid/blurred vision Absent 21 70.0
Present 9 30.0
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Figure 1.

Figure 1

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Graph showing percentage of patients showing a positive association with intake of steroids and oral symptoms

Figure 2.

Figure 2

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Graph showing palatal ulcer in ROCM patients

Random Blood Sugar (RBS) (Mean ± SD) was 304.60 ± 100.073 among these patients and DM (Mean ± SD) was 45.10 ± 50.440. Most of the patients in our study gave a recent history of a sudden rise in blood sugar level after diagnosis of mucormycosis [Figure 3].

Figure 3.

Figure 3

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RBS (Mean ± SD)

Comparison of RBS and DM in terms of Mean and SD among both genders using Mann–Whitney U showed both the parameters were higher in female patients. The difference of Mean of RBS was highly significant, whereas DM was non-significant. The reason behind higher blood sugar level among female patients was the negligent attitude toward health and medical check-up.

Discussion

Mucormycosis is an acute and rapidly progressing disease caused by Mucorales species and has a high mortality. In humans, these fungi invade the blood vessels leading to the formation of mycotic thrombi and necrosis on the walls of blood vessels.[17] Immunocompromised patients are generally much more vulnerable to the angioinvasive hyphal forms of these fungi.[18]

Mucormycosis has various forms among which rhinocerebral or sino-orbital types are common among diabetic patients, especially those who are poorly controlled.[19] The disease can be characterized by atypical symptoms of sinusitis, nasal congestion, headache, earache, toothache, and facial pain.[20]

In our study, we have also observed the association of mucormycosis with COVID-19-positive patients. A literature review revealed that the rhino-orbito-cerebral mucormycosis (ROCM) was the predominant presentation of CAM.[21,22]

Mucormycosis of the oral cavity is usually due to transpalatal extension of rhinocerebral infection, and mucormycosis localized to the periodontal tissues (i.e., gingiva and alveolar bone). The ROCM type is the most common form of the disease in India, followed by the pulmonary and cutaneous types.[23-25] This is the first study in our knowledge where we have seen many patients with ROCM having oral involvement during the second wave of the COVID-19 pandemic admitted to our tertiary health care center, and most of the patients were medically compromised. Only few cases of mucormycosis with oral manifestations have been recorded in past literature.[26-28]

In our study, we have assessed the association of COVID-19-positive patients with ROCM, vaccination status, age and gender of the patient, risk factors associated with ROCM, that is, intake of steroids and DM, and the most common intra-oral and extra-oral findings. We found more of the male patients were involved as compared to females; the age group most commonly affected was 50 years or less. This age group was more vulnerable to the disease as vaccination was given on a priority basis to health care workers and senior citizens (60 and above), and as the second wave hit during April 2021, the one vaccinated were in the age range of 44 years and above. Later the age range was reduced to 18–44 years during May and 18 years above during June. We also found that more patients were from rural areas and most of them were either non-vaccinated or taken only the first dose. The reason behind this may be the age range of vaccination, lack of awareness and knowledge regarding the importance of vaccination, and hesitation toward vaccination.

There was a positive correlation between patients giving the history of diabetes and intake of steroids with mucormycosis. Almost all the patients had given a history of DM or a recently diagnosed case of DM and steroid intake. The prevalence of DM is nearly 80 times higher (0.14 per 1,000) in India compared to developed countries, in a recent estimate of the years 2019–2020.[29] India has the highest cases of mucormycosis and the second largest population with DM in the world.[30] Few studies have shown mucormycosis resulting from even a short course (5–14 days) of steroid therapy, especially in people with DM. Surprisingly, 46% of the patients had received corticosteroids within the month before the diagnosis of mucormycosis in the European Confederation of Medical Mycology study.[31] A systematic review was conducted that reported the findings of 41 confirmed mucormycosis cases in people with COVID-19, DM was reported in 93% of cases, while 88% were receiving corticosteroids.[32] The results are consistent with the results of our study.

Managing patients with the oral manifestation of mucormycosis was challenging as it had a great impact on patients’ mental and physical well-being. The first and the most presenting symptom was a palatal ulcer, followed by gingival/palatal abscess and tooth mobility [Figure 4]. Dental practitioners played an important role in evaluating early signs and symptoms, especially in high-risk patients and decreasing mortality.[33,34] In our study, we have seen mobility mostly involving maxillary premolar and molar teeth as the disease has rhinomaxillary or rhinocerebral involvement. Extraoral findings most commonly seen were facial/periorbital swelling, blocked nose, discharge from the nose, drooping of eyelids, blurred vision, and black eschar.

Figure 4.

Figure 4

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Palatal ulcer in ROCM

In our study, all the cases of ROCM were confirmed by MRI and histopathological examination. MRI showed sinus mucosal thickening, opacification of sinuses, and bone destruction [Figure 5].[2] Surgical exploration was done in a patient with ROCM and the tissue specimen was sent for histopathological examination [Figure 4]. Histopathological picture of necrotic tissue presented abundant broad aseptate fungal hyphae consistent with mucor species and scant viable tissue with dense acute and chronic inflammatory cells infiltrate [Figure 6]. The COVID-19 status of patients was confirmed by Real- Time Reverse Transcription Polymerase Chain Reaction (RT-PCR) test, many patients had COVID-19 negative reports at the time of admission in the triage zone but gave a previous history of COVID-19 infection. According to the RT-PCR reports patients were shifted to different wards assigned for COVID-19 positive and negative patients.

Figure 5.

Figure 5

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MRI image of ROCM showing sinus mucosal thickening, opacification, and bone destruction

Figure 6.

Figure 6

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Histopathology of ROCM showing predominantly necrotic tissue with abundant broad aseptate fungal hyphae consistent with mucor species

Conclusion

Mucormycosis had come as a sudden storm that has created an emergency worldwide, especially in developing countries like India. The reason for the high prevalence of cases in India might be negligent behavior toward health, larger number of high-risk patients, and lack of knowledge and awareness which also increased mortality. The second wave of the COVID-19 pandemic had also created an alarming situation in our hospital. Due to the high risk of infection data collection from patients was challenging, despite which we have gathered the relevant information. In our study, it was proved that the risk factors associated with mucormycosis were uncontrolled diabetes and the injudicious use of steroids.

Limitations

In our study, we have gathered information with a smaller sample size as that was the peak of COVID-19 pandemic so, further studies with a larger sample size should be conducted to generalize the results.

Declaration of patient consent

The authors certify that they have obtained all appropriate patient consent forms. In the form, the patient(s) has/have given his/her/their consent for his/her/their images and other clinical information to be reported in the journal. The patients understand that their names and initials will not be published and due efforts will be made to conceal their identity, but anonymity cannot be guaranteed.

Author contributions

Author 1: Dr. Nimmi Singh contributed to writing and designing.

Author 2: Dr. Swati Singh conception and data acquisition.

Author 3–6: Dr. Priyankar Singh, Dr. Navin Mishra, Dr. Bibhuti P. Sinha, Dr. Arbind Shrama support and critically revising manuscript.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.

Acknowledgements

The authors would like to thank the institution for granting the permission to conduct this research during the COVID-19 pandemic. The authors would like to express their adoration and wholehearted gratitude to the head of the department and other departments who have inspired and benefited in one or the other way during the course of research. The authors would like to thank all the health care workers, hospital attendants, and security personnel for their dedication toward their work during the challenging pandemic situations.

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