COVID-19-associated acute invasive fungal sinusitis: Clinical and imaging findings

Ali H Elmokadem 1 2, Dalia Bayoumi 1, Manar Mansour 1, Mahitab Ghonim 1, Eman A Saad 3, Doaa Khedr 1


 

Affiliations

01 July 2022

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doi: 10.1111/jon.12967

Abstract

Background and purpose: The purpose is to provide a comprehensive report describing the clinical and imaging features of Coronavirus disease 2019 (COVID-19)-related acute invasive fungal sinusitis (AIFS) and associated comorbidities.

Methods: A retrospective study was conducted on 25 patients (12 males and 13 females, mean age of 53.9±9.1 years). All patients had positive polymerase chain reaction test for COVID-19 and histopathological proof of AIFS. Patients underwent computed tomography (CT) and magnetic resonance examinations to assess sinonasal, orbital, and cranial spread.

Results: The most prevalent comorbidity among the study cohort was diabetes mellitus (DM). Twenty-one patients (84%) were diagnosed in the post-COVID-19 period after hospital discharge, with a mean interval of 19.1±9.2 days. Steroid treatment was given to 19 patients (76%). Orbital manifestations were the presenting symptoms in all patients, followed by facial edema, nasal discharge, and neurological symptoms. Sinonasal involvement ranged from mucosal thickening to complete sinus opacification by a predominant isodensity on CT, low T1, and high T2 signal intensity with variable enhancement patterns. Twenty-four patients had a unilateral orbital extension, and 12 patients showed signs of intracranial extension. Bone involvement was detected in 16 patients (64%). Follow-up scans in 18 patients (72%) showed rapid progression of the disease. Eight patients (32%) died, six from neurological complications and two from severe respiratory failure.

Conclusion: Steroids, DM, and severe COVID-19 are the major risk factors of AIFS in the post-COVID-19 era. Imaging scans in all patients revealed different sinonasal, facial, orbital features, and intracranial involvement with rapid progression of the findings on follow-up scans.

Keywords: COVID-19; Sars-Cov-2; corona virus; fungi; sinusitis.

References

 

  1. Segrelles-Calvo G, de S Araújo GR, Frases S. Systemic mycoses: a potential alert for complications in COVID-19 patients. Future Microbiol 2020;15:1405-13.
  2. Gangneux JP, Bougnoux ME, Dannaoui E, Cornet M, Zahar JR. Invasive fungal diseases during COVID-19: we should be prepared. J Mycol Med 2020;30:100971.
  3. Song G, Liang G, Liu W. Fungal co-infections associated with global COVID-19 pandemic: a clinical and diagnostic perspective from China. Mycopathologia 2020;185:599-606.
  4. Dyer O. Covid-19: India sees record deaths as "black fungus" spreads fear. BMJ 2021;373:1238.
  5. El-Kholy NA, El-Fattah AMA, Khafagy YW. Invasive fungal sinusitis in post COVID-19 patients: a new clinical entity. Laryngoscope 2021;10:29632.
  6. Ismaiel WF, Abdelazim MH, Eldsoky I, et al. The impact of COVID-19 outbreak on the incidence of acute invasive fungal rhinosinusitis. Am J Otolaryngol 2021;42:103080.
  7. Villar J, Ferrando C, Martínez D, et al. Dexamethasone treatment for the acute respiratory distress syndrome: a multicentre, randomised controlled trial. Lancet Respir Med 2020;8:267-76.
  8. Marcolino VA, Pimentel TC, Barão CE. What to expect from different drugs used in the treatment of COVID-19: a study on applications and in vivo and in vitro results. Eur J Pharmacol 2020;887:173467.
  9. Fernandez IJ, Crocetta FM, Demattè M, et al. Acute invasive fungal rhinosinusitis in immunocompromised patients: role of an early diagnosis. Otolaryngol Head Neck Surg 2018;159:386-93.
  10. Chen N, Zhou M, Dong X, et al. Epidemiological and clinical characteristics of 99 cases of 2019 novel coronavirus pneumonia in Wuhan, China: a descriptive study. Lancet 2020;395:507-13.
  11. 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.
  12. Gavito-Higuera J, Mullins CB, Ramos-Duran L, Sandoval H, Akle N, Figueroa R. Sinonasal fungal infections and complications: a pictorial review. J Clin Imaging Sci 2016;6:23.
  13. Groppo ER, El-Sayed IH, Aiken AH, Glastonbury CM. Computed tomography and magnetic resonance imaging characteristics of acute invasive fungal sinusitis. Arch Otolaryngol Head Neck Surg 2011;137:1005-10.
  14. Li K, Fang Y, Li W, et al. CT image visual quantitative evaluation and clinical classification of coronavirus disease (COVID-19). Eur Radiol 2020;30:4407-16.
  15. Abo-Hedibah SA, Tharwat N, Elmokadem AH. Is chest X-ray severity scoring for COVID-19 pneumonia reliable? Pol J Radiol 2021;86:e432-39.
  16. Sebastian SK, Kumar VB, Gupta M, Sharma Y. Covid assossiated invasive fungal sinusitis. Indian J Otolaryngol Head Neck Surg 2021;25:1-4.
  17. Mehta S, Pandey A. Rhino-orbital mucormycosis associated with COVID-19. Cureus 2020;12:e10726.
  18. Werthman-Ehrenreich A. Mucormycosis with orbital compartment syndrome in a patient with COVID-19. Am J Emerg Med 2021;42:e2645-8.
  19. Rawson TM, Moore LSP, Zhu N, et al. Bacterial and fungal coinfection in individuals with coronavirus: a rapid review to support COVID-19 antimicrobial prescribing. Clin Infect Dis 2020;71:2459-68.
  20. White PL, Dhillon R, Cordey A, et al. A national strategy to diagnose COVID-19 associated invasive fungal disease in the ICU. Clin Infect Dis 2020;73:e1634-44.
  21. Ahmadikia K, Hashemi SJ, Khodavaisy S, et al. The double-edged sword of systemic corticosteroid therapy in viral pneumonia: a case report and comparative review of influenza-associated mucormycosis versus COVID-19 associated mucormycosis. Mycoses 2021;64:798-08.
  22. Moorthy A, Gaikwad R, Krishna S, et al. SARS-CoV-2, uncontrolled diabetes and corticosteroids-an unholy trinity in invasive fungal infections of the maxillofacial region? A retrospective, multi-centric analysis. J Maxillofac Oral Surg 2021;20:1-8.
  23. Patel A, Agarwal R, Rudramurthy SM, et al. Multicenter epidemiologic study of coronavirus disease-associated mucormycosis, India. Emerg Infect Dis 2021;27:2349-59.
  24. Sen M, Lahane S, Lahane TP, Parekh R, Honavar SG. Mucor in a viral land: a tale of two pathogens. Indian J Ophthalmol 2021;69:244-52.
  25. Ashour MM, Abdelaziz TT, Ashour DM, Askoura A, Saleh MI, Mahmoud MS. Imaging spectrum of acute invasive fungal rhino-orbital-cerebral sinusitis in COVID-19 patients: a case series and a review of literature. J Neuroradiol 2021;48:319-24.
  26. Sumi DV, Loureiro RM, Collin SM, et al. Sinus computed tomography findings in patients with COVID-19. Einstein (Sao Paulo) 2021;19:eAO6255.
  27. Fouad YA, Abdelaziz TT, Askoura A, et al. Spike in rhino-orbital-cerebral mucormycosis cases presenting to a tertiary care center during the COVID-19 pandemic. Front Med (Lausanne) 2021;8:645270.
  28. Revannavar SM, Supriya PS, Samaga L, Vineeth KV. COVID-19 triggering mucormycosis in a susceptible patient: a new phenomenon in the developing world? BMJ Case Rep 2021;14:e241663.
  29. Sharma S, Grover M, Bhargava S, Samdani S, Katari T. Post coronavirus disease mucormycosis: a deadly addition to the pandemic spectrum. J Laryngol Otol 2021;135:442-47.
  30. Fouad YA, Bakre HM, Nassar MA, Gad MOA & Shaat AAK. Characteristics and Outcomes of a Series of COVID-Associated Mucormycosis Patients in Two Different Settings in Egypt Through the Third Pandemic Wave. Clin Ophthalmol 2021;15:4795-4800.
  31. Rajendra Santosh AB, Muddana K, Bakki SR. Fungal infections of oral cavity: diagnosis, management, and association with COVID-19. SN Compr Clin Med 2021;27:1-12.
  32. Nehara HR, Puri I, Singhal V, Ih S, Bishnoi BR, Sirohi P. Rhinocerebral mucormycosis in COVID-19 patient with diabetes a deadly trio: case series from the north-western part of India. Indian J Med Microbiol 2021;39:380-83.
  33. Tabarsi P, Khalili N, Pourabdollah M, Sharifynia S, Naeini AS, Ghorbani J, Mohamadnia A, Abtahian Z & Askari E. Case Report: Coronavirus Disease 2019-associated Rhinosinusitis Mucormycosis Caused by Rhizopus arrhizus: A Rare but Potentially Fatal Infection Occurring After Treatment with Corticosteroids. Am J Trop Med Hyg 2021;105(2):449-53.
  34. Fung M, Babik J, Humphreys IM, Davis GE. Diagnosis and treatment of acute invasive fungal sinusitis in cancer and transplant patients. Curr Infect Dis Rep 2019;21:53.
  35. Gutiérrez-Delgado EM, Treviño-González JL, Montemayor-Alatorre A, et al. Chronic rhino-orbito-cerebral mucormycosis: a case report and review of the literature. Ann Med Surg (Lond) 2016;6:87-91.
  36. Drissi C. Black fungus, the darker side of COVID-19. J Neuroradiol 2021;48:318-8.
  37. Choi YR, Kim JH, Min HS, et al. Acute invasive fungal rhinosinusitis: MR imaging features and their impact on prognosis. Neuroradiology 2018;60:715-3.
  38. Groppo ER, El-Sayed IH, Aiken AH, Glastonbury CM. Computed tomography and magnetic resonance imaging characteristics of acute invasive fungal sinusitis. Arch Otolaryngol Head Neck Surg 2011;137:1005-10.
  39. Choi YR, Kim JH, Min HS, et al. Acute invasive fungal rhinosinusitis: MR imaging features and their impact on prognosis. Neuroradiology 2018;60:715-23.
  40. Han Q, Escott EJ. The Black Turbinate Sign, A Potential Diagnostic Pitfall: Evaluation of the Normal Enhancement Patterns of the Nasal Turbinates. AJNR Am J Neuroradiol. 2019;40(5):855-861.
  41. 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.
  42. Sarkar S, Gokhale T, Choudhury SS, Deb AK. COVID-19 and orbital mucormycosis. Indian J Ophthalmol. 2021;69:1002-4.
  43. Ghabrial R, Ananda A, van Hal SJ, et al. Invasive fungal sinusitis presenting as acute posterior ischemic optic neuropathy. Neuroophthalmology 2017;42:209-14.
  44. Silverman CS, Mancuso AA. Periantral soft-tissue infiltration and its relevance to the early detection of invasive fungal sinusitis: CT and MR findings. AJNR Am J Neuroradiol 1998;19:321-5.
  45. Salamah MA, Al-Shamani M. Allergic fungal otomastoiditis in a patient without allergic fungal rhinosinusitis: a case report. Am J Case Rep 2019;20:877-81.
  46. Chen CM, Chiang CW. Allergic fungal otomastoiditis: a case report. Laryngoscope 2013;123:1040-2.
  47. Baeesa SS, Bokhari RF, Alghamdi KB, Alem HB, Al-Maghrabi JA, Madani TA. Invasive aspergillus sinusitis with orbitocranial extension. Asian J Neurosurg 2017;12:172-9.
  48. Parikh SL, Venkatraman G, DelGaudio JM. Invasive fungal sinusitis: a 15-year review from a single institution. Am J Rhinol 2004;18:75-81.
  49. Siddiqui A, Shah AA, Bashir SH. Craniocerebral aspergillosis of sinonasal origin in immunocompetent patients: clinical spectrum and outcome in 25 cases. Neurosurgery 2004;55:602-13.
  50. Azar MM, Assi R, Patel N, Malinis MF. Fungal mycotic aneurysm of the internal carotid artery associated with sphenoid sinusitis in an immunocompromised patient: a case report and review of the literature. Mycopathologia 2016;181:425-33.
  51. Turner JH, Soudry E, Nayak JV, Hwang PH. Survival outcomes in acute invasive fungal sinusitis: a systematic review and quantitative synthesis of published evidence. Laryngoscope 2013;123:1112-8.

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