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CASE REPORT
Year : 2021  |  Volume : 25  |  Issue : 5  |  Page : 443-447  

Diagnosis of the misdiagnosed: Mucormycosis depicting periodontitis


Department of Oral Medicine and Radiology, JSS Dental College and Hospital, JSS Academy of Higher Education and Research, Mysore, Karnataka, India

Date of Submission09-Oct-2020
Date of Decision02-Apr-2021
Date of Acceptance04-Apr-2021
Date of Web Publication01-Sep-2021

Correspondence Address:
Prasannasrinivas Deshpande
Department of Oral Medicine and Radiology, JSS Dental College and Hospital, JSS Academy of Higher Education and Research, S.S Nagar, Bannimantap, Mysore - 570 015, Karnataka
India
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/jisp.jisp_720_20

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   Abstract 


Oral cavity is habitat for plethora of micro-organism causing various diseases. The most common includes dental caries, periodontal diseases, etc. Dental practice may rarely encounter unusual and subtle symptoms with nonpathognomonic clinical signs of several fatal diseases which may pretend like a common oral disease. Hence, the knowledge and clinical acumen of diagnostician are necessary for the early diagnosis of such fatal infections to prevent untoward consequences. Mucormycosis is an angioinvasive necrotic fungal infection with a high morbidity and mortality rate. It commonly occurs in patients with debilitating diseases and immunocompromised individuals. Clinically, it manifests as rhino-orbito-cerebral, pulmonary, cutaneous, gastrointestinal, renal, and disseminated form. Disease affecting the facial region is a challenge as it often disseminates with orbital and cranial involvement at the time of diagnosis. This article presents a case of mucormycosis which mimicked as severe periodontitis in a patient leading to delay in the diagnosis and challenges during the treatment.

Keywords: Antifungal agents, mucormycosis, mycoses, periodontal diseases, zygomycosis


How to cite this article:
Deshpande P, Patil K, Guledgud MV, Prashanthi N M. Diagnosis of the misdiagnosed: Mucormycosis depicting periodontitis. J Indian Soc Periodontol 2021;25:443-7

How to cite this URL:
Deshpande P, Patil K, Guledgud MV, Prashanthi N M. Diagnosis of the misdiagnosed: Mucormycosis depicting periodontitis. J Indian Soc Periodontol [serial online] 2021 [cited 2021 Sep 28];25:443-7. Available from: https://www.jisponline.com/text.asp?2021/25/5/443/325009




   Introduction Top


Oral infections can be caused by bacteria, viruses, or fungi and can manifest in various forms affecting the hard and soft tissues of the oral cavity. Periodontium can be afflicted with numerous such infections, often displaying similar clinical features as that of periodontitis. Although superficial fungal infections of the oral cavity such as candidiasis are a common occurrence, deep fungal infections are infrequently encountered.

Mucormycosis is a life-threatening deep fungal infection first described by Paultauf in 1885 and nearly after 58 years case series were reported by Gregory et al. in 1943.[1],[2] Different myocytes such as Rhizopus, Mucor, and Lichtheimia along with 24 species of other mucorales cause Mucormycosis. Inoculation occurs by inhalation of spores and nose, paranasal air sinuses, and lungs are the most common sites of involvement.[3],[4] The incidence of mucormycosis is estimated to be 1.7 cases per million people per year.[5] Often associated with compromised immunity patients, it presents with characteristic black necrotic eschar and necrosis.[6],[7] Among the several clinical forms of this diseases, the rhino-orbito-cerebral form is of particular significance to the oral clinician as it can manifest in the orofacial region.

This article reports an atypical case of mucormycosis, clinically simulating the more common periodontitis hence posing greater challenges in the diagnosis and treatment.


   Case Report Top


A 46-year-old female patient presented with complaint of pain and mobility in left upper teeth of 3 months' duration associated with mild left facial swelling. She had multiple dental consultations with different dentists for the same in the past and had undergone extraction of one or more regional teeth in each appointment owing to mobility. The procedure had aggravated the pain and swelling leading to difficulty in mouth opening. Consequently, she developed partial nasal blockage and nasal discharge on the left side along with burning and epiphora of the left eye.

Medical history revealed her to be a diabetic with poor glycemic control and also a hypertensive for past 4 years for which she was on oral medications.

Clinically, an indistinct, insignificant swelling over the left middle third of the face with mild obliteration of nasolabial fold was noted [Figure 1]a. Intraorally, a mild diffuse tender palatal swelling extending from lateral incisor to the first molar region and mild buccal vestibular obliteration without any secondary changes was appreciated. Teeth 11, 12, 23, 24 elicited Grade I mobility; 21, 22 and 25 were clinically missing (extracted) and 26, 27 were endodontically treated with metal crowns [Figure 1]b. Deep periodontal pockets (~7–9 mm) were noted with tooth 23, 24 ( Fédération Dentaire Internationale [FDI] numbering system).
Figure 1:Extraoral(a)andintraoral; (b) pictures of the regions with swelling

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Hematological investigations disclosed a decreased hemoglobin level of 8.4gm%. Her fasting and postprandial blood sugar levels were 308 mg/dl and 389 mg/dl, respectively.

A panoramic image which was acquired by the previous dentist was available and showed advanced supporting bone loss around teeth 21, 23, and 24. Keen observation of the same revealed permeative type of osteolysis in the maxillary left anterior alveolar bone with breach in the floor of the left maxillary sinus suggesting its involvement [Figure 2].
Figure 2: Orthopantomogram showing diffuse radiolucency over left Maxilla

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Computed tomography (CT) images depicted an irregular bone destruction of moth-eaten pattern extensively involving left alveolus, left maxilla, left zygoma, and zygomatic arch crossing the midline over the hard palate. Breach in the floor of the left nasal cavity was noted. Maxillary antrum on the left showed soft-tissue shadow completely obliterating the sinus with destruction of the medial wall and orbital floor with patchy hyperdensity in the floor. Left buccal soft tissue appeared enlarged as compared to the contralateral side [Figure 3].
Figure 3: Computed tomography image in coronal, sagittal and three-dimensional reconstruction showing irregular permeative destruction of left maxilla and zygomaticboneswithsinusinfiltrationanddestructionofpremaxilla,nasalandsinus walls

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Histopathologic evaluation of the lesion revealed the areas of necrosis with thick-walled broad nonseptate fungal hyphae of mucor. Dense acute and chronic inflammatory cells and few epithelioid cell granulomas along with multinucleated giant cells were also noted [Figure 4]. Potassium hydroxide (KOH) staining confirmed the presence of hyphae. The Periodic–acid–Schiff staining confirmed the presence of right-angled hyphae [Figure 5].
Figure 4: NonseptatehyphaeofmucormycosisnotedonHandEstainingat×40

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Figure 5: RightangledhyphaenotedonPeriodic-acid-Schiffstainat×100

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The patient was hospitalized immediately and was switched on to insulin from oral hypoglycemics. Liposomal Amphotericin B in a dosage of 5 mg/Kg was administered intravenously for a week. De-lining of the left maxillary sinus was carried out as the patient did not consent for excision of bone involved, regardless of the consequences explained. Further, the patient got discharged against medical advice when she was detailed regarding wide spread involvement and questionable prognosis.


   Discussion Top


Fungal infections are classified as superficial, subcutaneous, or deep/systemic based on the clinical involvement. Deep fungal infections are those with a pronounced systemic involvement and a tendency for invasion and dissemination and are associated with a high mortality rate.

Mucormycosis, also termed zygomycosis or phycomycosis, is an opportunistic fungal infection which exist in soil, air, food, compost piles, and decomposing organic matter.[8] Majority of these organisms usually require aerobic conditions for their growth; however, some organisms manage to survive in the anaerobic and microaerophilic conditions.[9]

Immunocompromised states such as uncontrolled diabetes mellitus, hematological malignancies, bone marrow transplants or organ transplantations, use of drugs such as corticosteroids and deferoxamine therapy, severe and prolonged neutropenia, immature babies or babies with low birth weight are a few common predisposing conditions triggering mucormycosis.[10]

In uncontrolled diabetic state, low PH and availability of micronutrients such as iron helps in the rapid multiplication of microorganisms. Rhizoferrin actively binds to the iron molecules in forming iron-rhizoferrin complex which is taken up by the fungus for cellular processes causing rapid spread of infection.[11],[12]

Mucormycosis manifests as rhino-orbito-cerebral, pulmonary, cutaneous, gastrointestinal, renal, and disseminated mucor disease. The infection occurs due to inhalation, ingestion, or contamination of traumatized mucosa such as ulcer or extraction socket by fungal spores.[10] Mucor fungi are angioinvasive, causing thrombosis in vessels leading to necrosis of tissues supplied by them [Figure 6]. This results in pathognomonic black eschar formation followed by the exposure of dry necrotic bone, especially in the oral cavity. Verrucous or granulomatous lesions, indurated and painful ulcers, especially of the tongue, gingiva, or palate are some other clinical manifestations of the disease. The absence of the pathognomonic eschar feature in the present case along with mere presence of mobile teeth and swelling leads to an erroneous diagnosis of advanced periodontitis.
Figure 6: Pathophysiology of mucormycosis with predisposing factors

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Rhino-orbital-cerebral mucormycosis may also initially presents with facial pain, swelling, running nose, and rhinosinusitis which is challenging to differentiate from common cold and sinusitis.[13] Ophthalmoplegia, ptosis, periorbital edema, and loss of vision along with infection spreading to the brain may be seen in advanced cases.[14]

Imaging studies are vital for the diagnosis of rhino-orbital-cerebral mucormycosis. Literature highlights the need for accurate imaging to assess the extent of disease, identify complications and for surgical planning. Conventional imaging is of little use in diagnosing early mucormycosis as it involves soft tissue and may have perivascular spread to brain through fissures and soft-tissue spaces without actual bone destruction.[15],[16],[17] Panoramic imaging in the current case showed only subtle bony changes which were appreciable by a proficient maxillofacial radiologist.

Irregular bony changes extensively involving the left facial bones along with the maxillary sinus and orbit were conspicuous findings on three-dimensional tomographic images which implied the presence of an aggressive disease.

Based on the extent of regional involvement radiographically, rhino-orbito-cerebal mucormycosis has been divided into three stages by Rupa et al. [Table 1].[18] The current case fits into the Stage 2 as it involved only the alveolus, premaxilla, and maxilla.
Table 1: Radiographic staging of rhino-orbito-cerebal mucormycosis by Rupa et al.[18]

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Further, soft-tissue density causing opacification of paranasal sinuses, mucosal thickening without air-fluid level can be well appreciated in conventional imaging and CT scans[16],[17] and were also evident in the current case.

Middlebrooks proposed a CT-based model of seven variables, namely periantral fat, bone dehiscence, orbital invasion, septal ulceration, pterygopalatine fossa, nasolacrimal duct, and lacrimal sac to predict acute invasive fungal rhinosinusitis.[19] An irregular permeative bone destruction leading to moth-eaten pattern in facial bones as seen in the present case was similar to the findings of Therakathu et al.[15],[20]

Histology and culture are essential for the diagnosis even when the hallmark feature of eschar formation is seen clinically. Initial cultures may be negative and otherwise cause delay in the diagnosis. Histological staining with eosin and hematoxylin, KOH and Periodic-acid Schiff reveals the aseptate mucor hyphae branching at right angles in the necrosed area with angioinvasion. In contrast, aspergillosis smaller septate hyphae having with branching seen at the acute angle on microscope.[21] Recently, quantitative polymerase chain reaction has been tested in early diagnosis which showed high sensitivity in mucor identification.[22]

Management of the mucormycosis is complex. The success of the treatment depends on timely diagnosis, control of risk factors, immediate administration of antifungal therapy, and surgical debridement. Delay in early intervention may cause wide spread to surrounding bones causing necrosis and infiltration to eye, retromaxillary space, and brain. Orbital pain, proptosis, ptosis, diplopia, central retinal artery occlusion, dilated pupil, and loss of vision indicate orbital involvement. Along with these, facial palsy may manifest indicating involvement second, third, fourth, fifth, and sixth cranial nerves. Through orbital route, disease spreads to superior maxillary fissure or the cribriform plate and involves the brain leading to cavernous sinus and sometimes death.[11]

Gold standard pharmacological treatment is with first-line monotherapy of Amphotericin B. At present, available forms are “lipid” formulation – amphotericin B deoxycholate and “liposomal” amphotericin. Lipid form is safer at higher doses and for a longer duration as nephrotoxicity is least, while liposomal form is associated with a higher survival rate. Common antifungals such as fluconazole and itraconazole have shown least effectiveness in treating mucormycosis. Recently, combination therapy of amphotericin B – caspofungin has also demonstrated significantly improved outcomes compared to monotherapy, especially in rhino-orbito-cerebral type. Surgical debridement of necrotic tissue is critical as antifungals have least penetration in necrotic areas.[23] Of late, hyperbaric oxygen therapy has shown to be effective in the condition by improving the phagocytosis of the micro-organisms by neutrophils. Mortality rate reported has been more than 40% in spite of good pharmacological and surgical support which emphasizes on the fatality of mucormycosis.[24]


   Conclusion Top


Several systemic and aggressive lesions can involve periodontium mimicking the clinical features of the most common periodontal disease. A precise diagnosis is a prerequisite to specific and meticulous treatment of any disease. Nonspecific or atypical presentations of such rare diseases can complicate the clinical scenario and defy a prompt and accurate diagnosis.

Mucormycosis is a deep fungal infection of the oral cavity which is often associated with high morbidity and mortality rates. The incidence of it involving only periodontium with characteristic eschar has surged in the recent years secondary to increase in various lifestyle diseases. The present case is an extremely rare presentation which mimicked advanced periodontitis without any hallmark features clinically as reported earlier. Hence, clinicians should always consider such disease in their differential diagnosis.

Declaration of patient consent

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

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.



 
   References Top

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Mignogna MD, Fortuna G, Leuci S, Adamo D, Ruoppo E, Siano M, et al. Mucormycosis in immunocompetent patients: A case-series of patients with maxillary sinus involvement and a critical review of the literature. Int J Infect Dis 2011;15:e533-40.  Back to cited text no. 9
    
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Hingad N, Kumar G, Deshmukh R. Oral mucormycosis causing necrotizing lesion in a diabetic patient: A case report. Int J Oral Maxillofac Pathol 2012;3:08-12.  Back to cited text no. 10
    
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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. 15
    
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Middlebrooks EH, Frost CJ, De Jesus RO, Massini TC, Schmalfuss IM, Mancuso AA. Acute invasive fungal rhinosinusitis: A comprehensive update of CT findings and design of an effective diagnostic imaging model. AJNR Am J Neuroradiol 2015;36:1529-35.  Back to cited text no. 19
    
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[PUBMED]  [Full text]  


    Figures

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