J Neurol Surg B Skull Base
DOI: 10.1055/a-2148-2259
Original Article

Changing Spectrum of Invasive Fungal Infections of the Anterior Skull Base

1   Neurotology Unit, Department of Neurosurgery, Sanjay Gandhi Postgraduate Institute of Medical Sciences, Lucknow, Uttar Pradesh, India
,
Amit Kumar Keshri
1   Neurotology Unit, Department of Neurosurgery, Sanjay Gandhi Postgraduate Institute of Medical Sciences, Lucknow, Uttar Pradesh, India
,
Malathy Seduchidambaram
2   Department of Maternal and Reproductive Health, Sanjay Gandhi Postgraduate Institute of Medical Sciences, Lucknow, Uttar Pradesh, India
,
Abhishek Dubey
1   Neurotology Unit, Department of Neurosurgery, Sanjay Gandhi Postgraduate Institute of Medical Sciences, Lucknow, Uttar Pradesh, India
,
Nazrin Hameed
1   Neurotology Unit, Department of Neurosurgery, Sanjay Gandhi Postgraduate Institute of Medical Sciences, Lucknow, Uttar Pradesh, India
,
Kalyan Chidambaram
1   Neurotology Unit, Department of Neurosurgery, Sanjay Gandhi Postgraduate Institute of Medical Sciences, Lucknow, Uttar Pradesh, India
,
Manjul Muraleedharan
1   Neurotology Unit, Department of Neurosurgery, Sanjay Gandhi Postgraduate Institute of Medical Sciences, Lucknow, Uttar Pradesh, India
,
3   Department of Neurosurgery, Sanjay Gandhi Postgraduate Institute of Medical Sciences, Lucknow, Uttar Pradesh, India
,
Anant Mehrotra
3   Department of Neurosurgery, Sanjay Gandhi Postgraduate Institute of Medical Sciences, Lucknow, Uttar Pradesh, India
,
Arun Srivastava
3   Department of Neurosurgery, Sanjay Gandhi Postgraduate Institute of Medical Sciences, Lucknow, Uttar Pradesh, India
,
Awadesh Jaiswal
3   Department of Neurosurgery, Sanjay Gandhi Postgraduate Institute of Medical Sciences, Lucknow, Uttar Pradesh, India
,
Raj Kumar
3   Department of Neurosurgery, Sanjay Gandhi Postgraduate Institute of Medical Sciences, Lucknow, Uttar Pradesh, India
,
1   Neurotology Unit, Department of Neurosurgery, Sanjay Gandhi Postgraduate Institute of Medical Sciences, Lucknow, Uttar Pradesh, India
› Author Affiliations

Abstract

Objective To study the etiological and anatomical factors in pathophysiology of invasive fungal rhinosinusitis affecting the skull base.

Design Retrospective clinical study over 5 years.

Setting Single-center tertiary referral hospital.

Materials and Methods All cases of invasive fungal rhinosinusitis with clinicoradiological and/or operative evidence of anterior and central skull base, orbit, and orbital apex involvement with or without intracranial disease were included in the study. Patients with a sinonasal-palatal disease without the involvement of the skull base or orbit were excluded from the study. In addition, we assessed the risk factors such as coronavirus disease 2019 (COVID-19) infection, diabetes mellitus (DM), and other immunocompromised conditions.

Results There were 79 patients, of which 65.8% had skull base rhino-oribitocerebral mucormycosis (ROCM), and 34.2% had Aspergillus infection. The mean duration from onset of the symptom to presentation of ROCM was 36.75 ± 20.97 days, while for the Aspergillus group was 21 weeks. The majority of patients (66%) with ROCM presented after 30 days of symptom onset. Among ROCM patients, 88.7% had a history of COVID-19 infection, and 96% had DM. In 40.8% of patients with Aspergillus infection, the tissue diagnosis was unavailable, and galactomannan assay and clinicoradiological assessment were used for diagnosis. The most common area of the skull base involved was the pterygopalatine fossa (88.5%), followed by the infratemporal fossa (73.1%). The most common neurovascular structure (75%) involved was the pterygopalatine ganglion and the infraorbital nerve.

Conclusion With the increasing incidence of invasive fungal infections worldwide, particularly after the COVID-19 pandemic, it is crucial to understand the evolving nature of this disease. ROCM, documented in the literature to cause fulminant disease, became a chronic illness, possibly due to the improvement of the patient's immunity during the disease course.



Publication History

Received: 19 April 2023

Accepted: 30 July 2023

Accepted Manuscript online:
03 August 2023

Article published online:
29 August 2023

© 2023. Thieme. All rights reserved.

Georg Thieme Verlag KG
Rüdigerstraße 14, 70469 Stuttgart, Germany

 
  • References

  • 1 deShazo RD, O'Brien M, Chapin K, Soto-Aguilar M, Gardner L, Swain R. A new classification and diagnostic criteria for invasive fungal sinusitis. Arch Otolaryngol Head Neck Surg 1997; 123 (11) 1181-1188
  • 2 Manogaran RS, Mathialagan A. Invasive fungal diseases of the skull base. In: Turgut M, Challa M, Akhaddar A. ed. Fungal Infections of the Central Nervous System: Pathogens, Diagnosis, and Management. Switzerland: Springer; 2019: 275-288
  • 3 Gillespie MB, O'Malley BW. An algorithmic approach to the diagnosis and management of invasive fungal rhinosinusitis in the immunocompromised patient. Otolaryngol Clin North Am 2000; 33 (02) 323-334
  • 4 Garg RK, Malhotra HS, Pandey S. Neurological infections in 2021: a spotlight on India. Lancet Neurol 2022; 21 (01) 17-18
  • 5 Baghel SS, Keshri AK, Mishra P. et al. The spectrum of invasive fungal sinusitis in COVID-19 patients: experience from a tertiary care referral center in Northern India. J Fungi (Basel) 2022; 8 (03) 223
  • 6 Daudia A, Jones NS. Advances in management of paranasal sinus aspergillosis. J Laryngol Otol 2008; 122 (04) 331-335
  • 7 Bretagne S, Marmorat-Khuong A, Kuentz M, Latgé JP, Bart-Delabesse E, Cordonnier C. Serum Aspergillus galactomannan antigen testing by sandwich ELISA: practical use in neutropenic patients. J Infect 1997; 35 (01) 7-15
  • 8 Baker RD. Mucormycosis; a new disease?. J Am Med Assoc 1957; 163 (10) 805-808
  • 9 Vignale R, Mackinnon JE, Casella de Vilaboa E, Burgoa F. Chronic, destructive, mucocutaneous phycomycosis in man. Sabouraudia 1964; 3 (02) 143-147
  • 10 Harrill WC, Stewart MG, Lee AG, Cernoch P. Chronic rhinocerebral mucormycosis. Laryngoscope 1996; 106 (10) 1292-1297
  • 11 Bitar D, Van Cauteren D, Lanternier F. et al. Increasing incidence of zygomycosis (mucormycosis), France, 1997-2006. Emerg Infect Dis 2009; 15 (09) 1395-1401
  • 12 Chakrabarti A, Das A, Mandal J. et al. The rising trend of invasive zygomycosis in patients with uncontrolled diabetes mellitus. Med Mycol 2006; 44 (04) 335-342
  • 13 Skiada A, Pavleas I, Drogari-Apiranthitou M. Epidemiology and diagnosis of mucormycosis: an update. J Fungi (Basel) 2020; 6 (04) 265
  • 14 Singh AK, Singh R, Joshi SR, Misra A. Mucormycosis in COVID-19: a systematic review of cases reported worldwide and in India. Diabetes Metab Syndr 2021; 15 (04) 102146
  • 15 Sen M, Honavar SG, Bansal R. et al; members of the Collaborative OPAI-IJO Study on Mucormycosis in COVID-19 (COSMIC) Study Group. Epidemiology, clinical profile, management, and outcome of COVID-19-associated rhino-orbital-cerebral mucormycosis in 2826 patients in India - Collaborative OPAI-IJO Study on Mucormycosis in COVID-19 (COSMIC), Report 1. Indian J Ophthalmol 2021; 69 (07) 1670-1692
  • 16 Hoenigl M, Seidel D, Carvalho A. et al; ECMM and ISHAM collaborators. The emergence of COVID-19 associated mucormycosis: a review of cases from 18 countries. Lancet Microbe 2022; 3 (07) e543-e552
  • 17 Devnath P, Dhama K, Tareq AM, Emran TB. Mucormycosis coinfection in the context of global COVID-19 outbreak: a fatal addition to the pandemic spectrum. Int J Surg 2021; 92: 106031
  • 18 Clancy CJ, Nguyen MH. Invasive sinus aspergillosis in apparently immunocompetent hosts. J Infect 1998; 37 (03) 229-240
  • 19 Alrajhi AA, Enani M, Mahasin Z, Al-Omran K. Chronic invasive aspergillosis of the paranasal sinuses in immunocompetent hosts from Saudi Arabia. Am J Trop Med Hyg 2001; 65 (01) 83-86
  • 20 Khudyakov A, Ahmed R, Huynh CD, Dehghani A, Li Z, Rose M. A rare indolent course of rhinocerebral mucormycosis. Case Rep Infect Dis 2021; 2021: 4381254
  • 21 Yang JK, Lin SS, Ji XJ, Guo LM. Binding of SARS coronavirus to its receptor damages islets and causes acute diabetes. Acta Diabetol 2010; 47 (03) 193-199
  • 22 Sahu AK, Mathew R, Bhat R. et al. Steroids use in non-oxygen requiring COVID-19 patients: a systematic review and meta-analysis. QJM 2021; 114 (07) 455-463
  • 23 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 (03) 418-425
  • 24 Turhan O, Bostanci A, Ozbudak IH, Turhan M. Chronic invasive nongranulomatous fungal rhinosinusitis in immunocompetent individuals. Case Rep Otolaryngol 2016; 2016: 6854121
  • 25 D'Anza B, Stokken J, Greene JS, Kennedy T, Woodard TD, Sindwani R. Chronic invasive fungal sinusitis: characterization and shift in management of a rare disease. Int Forum Allergy Rhinol 2016; 6 (12) 1294-1300
  • 26 Spellberg B, Edwards Jr J, Ibrahim A. Novel perspectives on mucormycosis: pathophysiology, presentation, and management. Clin Microbiol Rev 2005; 18 (03) 556-569
  • 27 DelGaudio JM, Swain Jr RE, Kingdom TT, Muller S, Hudgins PA. Computed tomographic findings in patients with invasive fungal sinusitis. Arch Otolaryngol Head Neck Surg 2003; 129 (02) 236-240
  • 28 Aribandi M, McCoy VA, Bazan III C. Imaging features of invasive and noninvasive fungal sinusitis: a review. Radiographics 2007; 27 (05) 1283-1296
  • 29 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 (10) 1005-1010
  • 30 Howells RC, Ramadan HH. Usefulness of computed tomography and magnetic resonance in fulminant invasive fungal rhinosinusitis. Am J Rhinol 2001; 15 (04) 255-261
  • 31 Herrera DA, Dublin AB, Ormsby EL, Aminpour S, Howell LP. Imaging findings of rhinocerebral mucormycosis. Skull Base 2009; 19 (02) 117-125
  • 32 Reddy CE, Gupta AK, Singh P, Mann SB. Imaging of granulomatous and chronic invasive fungal sinusitis: comparison with allergic fungal sinusitis. Otolaryngol Head Neck Surg 2010; 143 (02) 294-300
  • 33 Kim JH, Kang BC, Lee JH, Jang YJ, Lee BJ, Chung YS. The prognostic value of gadolinium-enhanced magnetic resonance imaging in acute invasive fungal rhinosinusitis. J Infect 2015; 70 (01) 88-95
  • 34 Chan LL, Singh S, Jones D, Diaz Jr EM, Ginsberg LE. Imaging of mucormycosis skull base osteomyelitis. AJNR Am J Neuroradiol 2000; 21 (05) 828-831
  • 35 Alarifi I, Alsaleh S, Alqaryan S. et al. Chronic granulomatous invasive fungal sinusitis: a case series and literature review. Ear Nose Throat J 2021; 100 (5_suppl, suppl): 720S-727S
  • 36 Goel A, Kini U, Shetty S. Role of histopathology as an aid to prognosis in rhino-orbito-cerebral zygomycosis. Indian J Pathol Microbiol 2010; 53 (02) 253-257
  • 37 Castillo L, Hofman V, Bétis F. et al. Longterm survival in acute rhinocerebral mucormycosis with giant cell arteritis and foreign body granulomas. Pathol Res Pract 2001; 197 (03) 199-203
  • 38 Donnelly JP, Chen SC, Kauffman CA. et al. Revision and Update of the Consensus Definitions of Invasive Fungal Disease From the European Organization for Research and Treatment of Cancer and the Mycoses Study Group Education and Research Consortium. Clin Infect Dis 2020; 71 (06) 1367-1376
  • 39 Melancon CC, Lindsey J, Russell GB, Clinger JD. The role of galactomannan Aspergillus antigen in diagnosing acute invasive fungal sinusitis. Int Forum Allergy Rhinol 2019; 9 (01) 60-66
  • 40 Kauffmann-Lacroix C, Rodier MH, Jacquemin JL, Goujon JM, Klossek JM. Detection of galactomannan for diagnosis of fungal rhinosinusitis. J Clin Microbiol 2001; 39 (12) 4593-4594
  • 41 Keshri A, Mathialagan A, Aishwarya A. et al. Is mucormycosis the end? A comprehensive management of orbit in COVID associated rhino-orbital-cerebral mucormycosis: preserving the salvageable. Eur Arch Otorhinolaryngol 2023; 280 (02) 819-827
  • 42 Ellis D. Amphotericin B: spectrum and resistance. J Antimicrob Chemother 2002; 49 (Suppl. 01) 7-10
  • 43 Smith C, Lee SC. Current treatments against mucormycosis and future directions. PLoS Pathog 2022; 18 (10) e1010858
  • 44 Lat A, Thompson III GR. Update on the optimal use of voriconazole for invasive fungal infections. Infect Drug Resist 2011; 4: 43-53
  • 45 Mehta R, Panda NK, Mohindra S, Chakrabarti A, Singh P. Comparison of efficacy of amphotericin B and itraconazole in chronic invasive fungal sinusitis. Indian J Otolaryngol Head Neck Surg 2013; 65 (Suppl. 02) 288-294