Multiple periodontal abscesses with atypical segmental teeth mobility in a nonperiodontitis case: A periodontal alarm of postcoronavirus disease-2019 mucormycosis

Abstract

The coronavirus pandemic, constantly mutating virus, and newer complications arising with each passing day have put health workers in jeopardy. One such serious complication being reported is mucormycosis. It is a deadly and rapidly spreading infection resulting in angioinvasion and tissue necrosis. In precoronavirus disease (COVID) era mucormycosis was observed mainly in patients having comorbidities such as diabetes, neutropenia, or previous history of organ transplant. In the present case report, a systemically healthy patient presented with mucormycosis postcoronavirus disease-2019 infection. The patient presented with atypical periodontal findings such as multiple periodontal abscesses, segmental teeth mobility, and deep periodontal pockets confined to the maxillary right quadrant. This form of presentation should be a wake-up call for all dental professionals to be in the constant lookout for any signs and symptoms of mucormycosis even in seemingly nonhigh-risk patients.

INTRODUCTION

“Fungi are the interface organisms between life and death.”

-Paul Stamets

“Coronavirus disease-2019 (COVID-19) caused by severe acute respiratory syndrome coronavirus-2 (SARS-CoV-2)” which began in Wuhan, China, in late 2019 has gripped the entire globe with devastating effects on the entire human community. Currently, the world and specifically the Southeast Asian countries are going through a third wave of the deadly virus taking a heavy toll on the overall medical and health-care system.[¹]

The understanding of the pathogenesis, spread, and treatment for COVID-19 has undergone extensive changes in the last year or so. The treatment protocol has become more defined and specific with the use of systemic antiviral drugs to decrease the viral load in the early part of the disease and corticosteroids which have been proved effective in reducing the cytokine storm caused by the disease. The use of these drugs is gaining more popularity for the management of moderate-to-severe symptomatic cases. The mortality rate has drastically reduced with the use of these medications but the long-term effects of these immunity-suppressing medications need to be gauged properly against the benefits that they offer in managing COVID-19 infection.[¹]

Post-COVID-19 complications reported during the recovery period of the disease include disseminated intravascular coagulation (DIC), opportunistic infections such as pulmonary aspergillosis and rhino-orbital mucormycosis which can lead to increased mortality. The incidence of complications related to opportunistic infections is more dreadful in the current second wave possibly due to mutant strains of the virus and injudicious use of medication in individuals with preexisting diabetes and immunocompromised conditions.[²]

SARS-COV-2 is known to cause a diminished host response in patients leading to decreased CD4+ T and CD8+ T cell counts. Patients suffering from severe COVID-19 symptoms who require hospitalization are usually treated with high doses of corticosteroids and drugs like tocilizumab which themselves are known to cause immunosuppression. Steroids are also known to elevate blood sugar levels in diabetics making patients prone to diabetic ketoacidosis. Such immunocompromised patients with a history of COVID-19 are at a much higher risk of contact opportunistic fungal infections like mucormycosis.[³⁴]

Mucormycosis is a fast-spreading, potentially lethal, angioinvasive fungal infection that is caused by filamentous fungi from the class zygomycetes and order Mucorales. The most common organism that has been isolated from patients affected by mucormycosis is Rhizopus oryzae.[⁵] Mucormycosis is predisposed by conditions such as diabetes mellitus, injudicious use of corticosteroids and immunosuppressive drugs, primary or secondary immunodeficiency, iron overload, malignancies, and stem cell or solid organ transplantation. The incidence of rhino-orbito-cerebral mucormycosis in the COVID-19 pandemic, especially in India has become a matter of grave concern.[⁶] The classic signs and symptoms of rhino-orbital mucormycosis include nasal stuffiness, foul smell, epistaxis, nasal discharge, eyelid, periorbital and facial edema, pain or discoloration, severe headache, dental pain, sudden loss of vision, facial paresthesia, fever, altered sensorium, or even focal seizures.[⁷]

Currently, there are a few case reports of mucormycosis with associated comorbidities and history of COVID-19 infection available in the literature. However, to the best of our knowledge, there is no reported case of mucormycosis with periodontal involvement in COVID-19 recovered systemically healthy patients.

This article presents a case of multiple periodontal abscesses with concurrent segmental mobility of teeth in the affected quadrant of the maxillary arch with an absolutely healthy periodontium in an otherwise systemically healthy patient who just recovered from COVID-19 infection. The atypical findings in a nonperiodontitis patient could possibly be seen as an alarming sign in the diagnosis of fulminating mucormycotic infection with high incidence of mortality rate if left undiagnosed and untreated.

Case Report

A 33-year-old, systemically healthy, female patient reported to the department of periodontology on April 29, 2021, with the complaint of swelling in the gums of the teeth on the right side of the upper jaw for the past 3 weeks.

The patient has a history of COVID-19 infection and was hospitalized for the same at a private hospital for 10 days. The patient’s high-resolution computed tomography (HRCT) score was 17 which indicated the extent of lobar involvement of the lungs and the severity of the disease [Figure 1]. The patient was given antiviral therapy (injection remdesivir 5 doses) and high doses of steroids (injection dexamethasone) during hospitalization.

Figure 1: HRCT with a score of 17. HRCT High-resolution computed tomography

The pain and swelling in the maxillary right quadrant that started during hospitalization did not subside even after completing the course of antibiotics for 5 days as prescribed by a physician.

On extraoral examination, there was the absence of classic symptoms of mucormycosis such as epistaxis, nasal discharge, edema, and pain or discoloration of the face and eyelid. The patient also did not have headache, nasal stuffiness, foul smell, sudden loss of vision, facial paresthesia, fever, altered sensorium, or focal seizures.

On periodontal examination, multiple periodontal abscesses with draining sinus were seen with respect to the teeth numbers 11, 12, 13, 14, 15, and 16 on the buccal aspect [Figure 2]. An abscess was also seen on the palatal aspect with respect to tooth number 14 [Figure 3]. Grade 3 segmental mobility was seen with tooth numbers 11, 12, 13, 14, and 15 involving the alveolar component. Deep periodontal pockets were seen in most of the affected teeth with >10 mm probing depth with tooth number 13 [Figure 4].

Figure 2: Periodontal abscesses with draining sinus w.r.t. 11, 12, 13, 14, 15, and 16

Figure 3: Abscess on the palatal aspect w.r.t. 14

Figure 4: More than 10 mm probing depth with tooth number 13

On performing a pulp vitality test using a stick of hot gutta-percha, it was observed that teeth numbers 11, 12, 13, 14, and 15 showed negative responses suggesting they were nonvital, and immediately adjacent teeth 21, 22 and 16, 17 showed positive response suggesting they were vital.

Surprisingly, the periodontal condition of the teeth in other quadrants was stable without any predisposing factors.

Radiographic findings

Intraoral periapical radiographs in the form of radiovisiography (RVG) from the left lateral to right molar were advised. Radiographic findings appeared to be normal without any significant changes when correlated to the clinical findings.

Following which orthopantomagram (OPG) was advised which showed an ill-defined radiopacity in the right maxillary sinus on its posterolateral part indicative of opacification. The anterior border was not traceable. There were no signs of any destruction of the right maxillary sinus. IOPA (RVG) and OPG were advised to rule out any periodontal etiology for mobility. For further clarification, computed tomography (CT) paranasal sinus (PNS) with contrast was advised.

Computed tomography findings

The right maxillary sinus showed opacification with thickened polypoidal mucosa lining. The floor of the right maxillary sinus and right maxillary alveolar ridge shows an irregular osteolytic area measuring approximately 19 mm × 16 mm in the region of the right second premolar and first molar teeth. Other sinuses, orbits, lamina papyracea, and bony walls of the other sinuses appeared intact [Figure 5].

Figure 5: CT maxillary sinus showing opacification with thickened polypoid mucosal lining. CT – Computed tomography

Fungal culture of pus samples showed the presence of nonseptate hyphae which brought us to the final diagnosis of mucormycosis of the right maxillary sinus and right maxillary alveolar ridge.

The patient was referred to the department of oral and maxillofacial surgery for further medical and surgical management to be followed by reconstruction of the dentoalveolar area postresection.

The patient was monitored with regular follow-up visits. Maxillectomy (dentoalveolar process and right maxillary sinus) [Figure 6] of the affected region was performed and an obturator was given. Histopathological examination of the resected maxillary bone along with sinus and respiratory mucosa showed focal necrotic areas and broad aseptate fungal hyphae with right-angle branching [Figure 7] which confirmed our diagnosis of mucormycosis. The patient received systemic antifungal therapy (liposomal amphotericin B – 5–10 mg/kg/day). This will be followed by prosthetic rehabilitation of the resected area after healing is completed.

Figure 6: Maxillectomy of the affected region – dentoalveolar process and right maxillary sinus

Figure 7: Histopathological examination of the resected maxillary bone along with sinus and respiratory mucosa showing focal necrotic areas and broad aseptate fungal hyphae with right-angle branching

DISCUSSION

Mucormycosis or zygomycosis, first described by Paltauf in 1885, is a rapidly spreading, life-threatening fungal infection that can cause necrosis of the affected tissues. Mucor may be present as a commensal organism in the nasal mucosa of healthy people. However, in an immunosuppressed patient, this fungus can multiply and grow within the PNSs as well as spread to other intracranial structures.[⁸]

In the pre-COVID era, a higher number of mucormycosis cases reported in India were attributed to the hot and humid climate and high incidence of uncontrolled diabetes in the majority of the population.[⁹]

Uncontrolled diabetes leads to ketoacidosis where the phagocytic function is impaired along with decreased CD4+ and CD8+ lymphocytes leading to impaired immunity. Acidemic state and hyperglycemia can induce the endothelial receptor glucose-regulated protein 78 and the Mucorales adhesion spore coat protein homologs (CotH), which may result in Mucorales adhering and penetrating the endothelium. Such patients are more prone to an attack by mucormycotic fungi and their impaired immune system is unable to ward off the infection.[⁷]

During this COVID-19 pandemic, the late increasing incidence of mucormycosis is seen in COVID-19 recovered patients with a history of treatment with systemic steroids, antiviral drugs, and associated comorbidities such as diabetes and immunosuppression.

In this case report, the patient presented with periodontal symptoms such as deep probing depths, loss of CAL, segmental tooth mobility, toothache, and multiple abscesses, which was confined to the maxillary right quadrant. But these periodontal findings were not in commensurate with the severity of the local factors which is a characteristic feature of any case with periodontitis. Moreover other than the affected areas, remaining teeth with the periodontium looks clinically healthy without any PPD,CAL or radiographic bone loss. And also, the segmental periodontal findings were noticed by the patient post COVID infection. The overall above findings made us to conclude this case as a non-periodontitis one.

Real-time–polymerase chain reaction test was considered for early detection of SARS-CoV infection in the current case. The assay can discriminate SARS-CoV from other human and animal coronaviruses with higher sensitivity and high specificity.[¹⁰]

The patient’s HRCT score was 17. The case falls under stage 2A according to the revised and restructured staging of rhino-orbito-cerebral mucormycosis.[¹¹]

After performing various radiographic and microbiologic examinations, a final diagnosis of COVID-19-associated mucormycosis was confirmed. The diagnosis of mucormycosis is challenging, and it should be treated as early as possible. A deep nasal swab with KOH staining can be done to detect the fungus. Nasal endoscopy and biopsy may be performed. Histology or culture characteristics of the organism can be studied from culture tests of samples from the affected sites.[⁶]

The possible reason for the development of mucormycosis, in this case, could be explained by the following mechanisms:

1. Immunosuppression which was caused by the steroids and antiviral drugs that were used to treat her COVID-19 infection. These drugs result in a diminished host response in the patient, thereby leading to decreased CD4+ T and CD8+ T cell counts and thus increasing the risk of mucormycosis infection[⁹]
2. Severe COVID-19 infection results in the release of cytokines like interleukin-6 which will in turn increase ferritin synthesis. High levels of ferritin will increase the intracellular iron overload leading to increased production of reactive oxygen species within the cell that will further intensify the tissue damage. This tissue damage will subsequently result in an increase in the free iron in circulation. One of the key risk factors for mucormycosis is this excessive overload of free iron within the cell as well as in the circulation.[⁷]
3. Endothelialitis can associate COVID-19 with mucormycosis. Endothelial adhesion and penetration are one of the initial steps in the development of mucormycosis various autopsy reports of patients who died of COVID-19 have also shown severe and extensive endothelial injury. This endothelial injury may predispose a COVID-19 recovered patient to the development of mucormycosis.[⁷]

The increased incidence of mucormycosis in the maxilla is due to its rich vascularity. Mucormycosis most commonly affects the ethmoid sinus followed by the maxillary sinus.[⁸]

In this era of the COVID pandemic which is seeing an alarming rise of new signs and symptoms along with a wide variety of complications, early diagnosis and treatment are the key to preventing fatalities. Hence, clinicians must be alert and should implement a few precautions that could help in preventing the occurrence of mucormycosis such as the judicious use of steroids and antiviral drugs, constant blood sugar level monitoring and maintenance (110–180 mg/dl), hygiene maintenance of O₂ delivery system and use of distilled water in humidifiers, and delay of any nonemergent invasive oral or dental procedure for 3 months after COVID-19 infection.

CONCLUSION

With each passing day, we are coming across newer complications of COVID-19 infection, which include fungal infections like mucormycosis that could prove to be life-threatening if not given serious consideration.

Therefore, it is of utmost importance that doctors treating COVID-19 patients including dental professionals be on the constant lookout for early signs of mucormycosis, and patients themselves should be educated about the signs and symptoms of mucormycosis which can help in early detection and treatment.

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.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.