Fungal rhinosinusitis†
A categorization and definitional schema addressing current controversies
Corresponding Author
Arunaloke Chakrabarti MD
Department of Medical Microbiology, Postgraduate Institute of Medical Education and Research, Chandigarh, India
Department of Medical Microbiology, Postgraduate Institute of Medical Education and Research, Chandigarh, Chandigarh 160012, IndiaSearch for more papers by this authorDavid W. Denning FRCP, FRCPATH
National Aspergillosis Centre, Education and Research Centre, University Hospital of South Manchester, Manchester, UK
Search for more papers by this authorBerrylin J. Ferguson MD
Department of Otolaryngology, University of Pittsburgh School of Medicine, Pittsburgh, Pennsylvania, U.S.A.
Search for more papers by this authorJens Ponikau MD
Otolaryngology Research, State University of New York at Buffalo, Buffalo, New York, U.S.A.
Search for more papers by this authorWalter Buzina PhD
Medical Mycology, Institute of Hygiene, Microbiology & Environmental Medicine, Medical University of Graz, Austria
Search for more papers by this authorHirohito Kita MD
Department of Allergic Diseases and Medicine, Mayo Clinic, Rochester, Minnesota, U.S.A.
Search for more papers by this authorBradley Marple MD
Department of Otolaryngology–Head and Neck Surgery, University of Texas Southwestern Medical Center, Dallas, Texas, U.S.A.
Search for more papers by this authorNaresh Panda MS
Department of Otolaryngology, Postgraduate Institute of Medical Education and Research, Chandigarh, India
Search for more papers by this authorStephan Vlaminck MD
Department of Rhinology, ENT, AZ, St. Jean Hospital, Bruges, Belgium
Search for more papers by this authorCatherine Kauffmann-Lacroix M. Pharm
Parasitology and Mycology Laboratory, University Hospital Centre, Poitiers, France
Search for more papers by this authorAshim Das MD
Department of Histopathology, Postgraduate Institute of Medical Education and Research, Chandigarh, India
Search for more papers by this authorParamjeet Singh MD
Department of Radiodiagnosis and Imaging, Postgraduate Institute of Medical Education and Research, Chandigarh, India
Search for more papers by this authorSaad J. Taj-Aldeen PhD
Laboratory of Medicine and Pathology, Hamad Medical Corporation, Doha, Qatar
Search for more papers by this authorA. Serda Kantarcioglu PhD
Deep Mycosis Laboratory, Department of Microbiology and Clinical Microbiology, Cerrahpasa Medical Faculty, Istanbul, Turkey
Search for more papers by this authorKumud K. Handa MS
Department of ENT, All India Institute of Medical Sciences, New Delhi, India
Search for more papers by this authorAshok Gupta MS
Department of Otolaryngology, Postgraduate Institute of Medical Education and Research, Chandigarh, India
Search for more papers by this authorM. Thungabathra PhD
Department of Biochemistry, Postgraduate Institute of Medical Education and Research, Chandigarh, India
Search for more papers by this authorMandya R. Shivaprakash MD
Department of Medical Microbiology, Postgraduate Institute of Medical Education and Research, Chandigarh, India
Search for more papers by this authorAmanjit Bal MD
Department of Histopathology, Postgraduate Institute of Medical Education and Research, Chandigarh, India
Search for more papers by this authorAnnette Fothergill BS, MBA
Department of Pathology, The University of Texas Health Science Center, San Antonio, Texas, U.S.A.
Search for more papers by this authorBishan D. Radotra MD
Department of Histopathology, Postgraduate Institute of Medical Education and Research, Chandigarh, India
Search for more papers by this authorCorresponding Author
Arunaloke Chakrabarti MD
Department of Medical Microbiology, Postgraduate Institute of Medical Education and Research, Chandigarh, India
Department of Medical Microbiology, Postgraduate Institute of Medical Education and Research, Chandigarh, Chandigarh 160012, IndiaSearch for more papers by this authorDavid W. Denning FRCP, FRCPATH
National Aspergillosis Centre, Education and Research Centre, University Hospital of South Manchester, Manchester, UK
Search for more papers by this authorBerrylin J. Ferguson MD
Department of Otolaryngology, University of Pittsburgh School of Medicine, Pittsburgh, Pennsylvania, U.S.A.
Search for more papers by this authorJens Ponikau MD
Otolaryngology Research, State University of New York at Buffalo, Buffalo, New York, U.S.A.
Search for more papers by this authorWalter Buzina PhD
Medical Mycology, Institute of Hygiene, Microbiology & Environmental Medicine, Medical University of Graz, Austria
Search for more papers by this authorHirohito Kita MD
Department of Allergic Diseases and Medicine, Mayo Clinic, Rochester, Minnesota, U.S.A.
Search for more papers by this authorBradley Marple MD
Department of Otolaryngology–Head and Neck Surgery, University of Texas Southwestern Medical Center, Dallas, Texas, U.S.A.
Search for more papers by this authorNaresh Panda MS
Department of Otolaryngology, Postgraduate Institute of Medical Education and Research, Chandigarh, India
Search for more papers by this authorStephan Vlaminck MD
Department of Rhinology, ENT, AZ, St. Jean Hospital, Bruges, Belgium
Search for more papers by this authorCatherine Kauffmann-Lacroix M. Pharm
Parasitology and Mycology Laboratory, University Hospital Centre, Poitiers, France
Search for more papers by this authorAshim Das MD
Department of Histopathology, Postgraduate Institute of Medical Education and Research, Chandigarh, India
Search for more papers by this authorParamjeet Singh MD
Department of Radiodiagnosis and Imaging, Postgraduate Institute of Medical Education and Research, Chandigarh, India
Search for more papers by this authorSaad J. Taj-Aldeen PhD
Laboratory of Medicine and Pathology, Hamad Medical Corporation, Doha, Qatar
Search for more papers by this authorA. Serda Kantarcioglu PhD
Deep Mycosis Laboratory, Department of Microbiology and Clinical Microbiology, Cerrahpasa Medical Faculty, Istanbul, Turkey
Search for more papers by this authorKumud K. Handa MS
Department of ENT, All India Institute of Medical Sciences, New Delhi, India
Search for more papers by this authorAshok Gupta MS
Department of Otolaryngology, Postgraduate Institute of Medical Education and Research, Chandigarh, India
Search for more papers by this authorM. Thungabathra PhD
Department of Biochemistry, Postgraduate Institute of Medical Education and Research, Chandigarh, India
Search for more papers by this authorMandya R. Shivaprakash MD
Department of Medical Microbiology, Postgraduate Institute of Medical Education and Research, Chandigarh, India
Search for more papers by this authorAmanjit Bal MD
Department of Histopathology, Postgraduate Institute of Medical Education and Research, Chandigarh, India
Search for more papers by this authorAnnette Fothergill BS, MBA
Department of Pathology, The University of Texas Health Science Center, San Antonio, Texas, U.S.A.
Search for more papers by this authorBishan D. Radotra MD
Department of Histopathology, Postgraduate Institute of Medical Education and Research, Chandigarh, India
Search for more papers by this authorThis work is a summary of the panel discussion during the Workshop on Fungal Sinusitis, Chandigarh, India, February 9–11, 2008. The major sponsors of the workshop were the International Society for Human and Animal Mycology, Lifecare Innovations, India, Pfizer Inc., and Merek Sharp & Dohme.
Abstract
Background:
Fungal (rhino-) sinusitis encompasses a wide spectrum of immune and pathological responses, including invasive, chronic, granulomatous, and allergic disease. However, consensus on terminology, pathogenesis, and optimal management is lacking. The International Society for Human and Animal Mycology convened a working group to attempt consensus on terminology and disease classification.
Discussion:
Key conclusions reached were: rhinosinusitis is preferred to sinusitis; acute invasive fungal rhinosinusitis is preferred to fulminant, or necrotizing and should refer to disease of <4 weeks duration in immunocompromised patients; both chronic invasive rhinosinusitis and granulomatous rhinosinusitis were useful terms encompassing locally invasive disease over at least 3 months duration, with differing pathology and clinical settings; fungal ball of the sinus is preferred to either mycetoma or aspergilloma of the sinuses; localized fungal colonization of nasal or paranasal mucosa should be introduced to refer to localized infection visualized endoscopically; eosinophilic mucin is preferred to allergic mucin; and allergic fungal rhinosinusitis (AFRS), eosinophilic fungal rhinosinusitis, and eosinophilic mucin rhinosinusitis (EMRS) are imprecise and require better definition. In particular, to implicate fungi (as in AFRS and EMRS), hyphae must be visualized in eosinophilic mucin, but this is often not processed or examined carefully enough by histologists, reducing the universality of the disease classification. A schema for subclassifying these entities, including aspirin-exacerbated rhinosinusitis, is proposed allowing an overlap in histopathological features, and with granulomatous, chronic invasive, and other forms of rhinosinusitis. Recommendations for future research avenues were also identified. Laryngosope, 2009
Supporting Information
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BIBLIOGRAPHY
- 1 International Rhinosinusitis Advisory Board. Infectious rhinosinusitis in adults: classification, etiology and management. Ear Nose Throat J 1997; 76: 5–22.
- 2 Hora JF. Primary aspergillosis of the paranasal sinuses and associated areas. Laryngoscope 1965; 75: 768–773.
- 3 Jahrsdoerfer RA, Ejercito VS, Johns MME, Contrell RW, Sydnor JB. Aspergillosis of the nose and paranasal sinuses. Am J Otol 1979; 1: 6–14.
- 4 Lowe J, Bradley J. Cerebral and orbital Aspergillus infection due to invasive aspergillosis of ethmoid sinus. J Clin Pathol 1986; 39: 774–778.
- 5 McGill TJ, Simpson G, Healy GB. Fulminant aspergillosis of the nose and paranasal sinuses: a new clinical entity. Laryngoscope 1980; 90: 748–754.
- 6 Safirstein B. Allergic broncho-pulmonary aspergillosis with obstruction of the upper respiratory tract. Chest 1976; 70: 788–790.
- 7 Millar JN, Johnston A, Lamb D. Allergic aspergillosis of the maxillary sinuses. Thorax 1981; 36: 710.
- 8 Katzenstein AA, Sole SR, Greenberger PA. Allergic Aspergillus sinusitis: a newly recognized form of sinusitis. J Allergy Clin Immunol 1983; 72: 82–93.
- 9 Allphin AL, Strauss M, Abdul Karim FW. Allergic fungal sinusitis: problems in diagnosis and treatment. Laryngoscope 1991; 101: 815–820.
- 10 Manning SC, Schaefer SD, Close LG, Vuitch F. Culture positive allergic fungal sinusitis. Arch Otolaryngol 1991; 117: 174–178.
- 11 Bent JP, Kuhn FA. Diagnosis of allergic fungal sinusitis. Otolaryngol Head Neck Surg 1994; 111: 580–588.
- 12 Ponikau JU, Sherris DA, Kern EB, et al. The diagnosis and incidence of allergic fungal sinusitis. Mayo Clin Proc 1999; 74: 877–884.
- 13 Braun H, Buzina W, Freudenschuss K, Beham A, Stammberger H. “Eosinophilic fungal rhinosinusitis”: a common disorder in Europe? Laryngoscope 2003; 113: 264–269.
- 14 deShazo RD, Chapin K, Swain R. Fungal sinusitis. N Eng J Med 1997; 337: 254–259.
- 15 Ferguson BJ. Eosinophilic mucin rhinosinusitis: a distinct clinicopathological entity. Laryngoscope 2000; 110: 799–813.
- 16 Gowing NFC, Hamlin IME. Tissue reaction to Aspergillus in cases of Hodgkin's disease and leukemia. J Clin Pathol 1960; 13: 396–413.
- 17 deShazo RD. Fungal sinusitis. Am J Med Sci 1998; 316: 39–45.
- 18 Ferguson BJ. Mucormycosis of the nose and paranasal sinuses. Otolaryngol Clin North Am 2000; 33: 349–365.
- 19 Adelson RT, Marple BF. Fungal rhinosinusitis: state-of-art diagnosis and treatment. J Otolaryngol 2005; 34( suppl 1): S18–S23.
- 20 Zapico ADV, Suarez AR, Encinas PM, Angulo CM, Pozuelo EC. Mucormycosis of the sphenoid sinus in an otherwise healthy patient. Case report and literature review. J Layngol Otol 1996; 110: 471–473.
- 21 Sridhara SR, Paragache G, Panda NK, Chakrabarti A. Mucormycosis in immunocompetent individuals: an increasing trend. J Otolaryngol 2005; 34: 402–406.
- 22 Chakrabarti A, Das A, Mandal J, et al. The rising trend of invasive zygomycosis in patients with uncontrolled diabetes mellitus. Med Mycol 2006; 44: 335–342.
- 23 Chakrabarti A, Sharma SC, Chander J. Epidemiology and pathogenesis of paranasal sinus mycoses. Otolaryngol Head Neck Surg 1992; 107: 745–750.
- 24
Veress B,
Malik OA,
el-Tayeb AA,
el-Daoud S,
Mahgoub ES,
el-Hassan AM.
Further observations on primary paranasal Aspergillus granuloma in the Sudan. A morphological study of 46 cases.
Am J Trop Med Hyg
1973;
2:
765–772.
10.4269/ajtmh.1973.22.765 Google Scholar
- 25 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: 1181–1188.
- 26 Milroy CM, Blanshard JD, Lucas S, Michaels L. Aspergillosis of the nose and paranasal sinuses. J Clin Pathol 1989; 42: 123–127.
- 27 Ferguson BJ. Definitions of fungal rhinosinusitis. Otolaryngol Clin North Am 2000; 33: 227–235.
- 28 Grosjean P, Weber R. Fungus balls of the paranasal sinuses: a review. Eur Arch Otorhinolaryngol 2007; 264: 461–470.
- 29 deShazo RD, O'Brien M, Chapin K, et al. Criteria for the diagnosis of sinus mycetoma. J Allergy Clin Immunol 1997; 99: 475–485.
- 30 Dufour X, Kauffmann-Lacroix C, Ferrie JC, Goujon JM, Rodier MH, Klossek JM. Paranasal sinus fungal ball epidemiology, clinical features and diagnosis. A retrospective analysis of 173 cases from a single center in France, 1989-2002. Med Mycol 2006; 44: 61–67.
- 31 Gungor A, Adusumilli V. Fungal sinusitis: progression of diseases in immunosuppression—a case report. Ear Nose Throat J 1998; 77: 207–215.
- 32 Graham SM, Ballas ZK. Postoperative steroids confuse the diagnosis of allergic fungal sinusitis. J Allergy Clin Immunol 1998; 101: 139–140.
- 33 Dhong HJ, Jung JY, Park JH. Diagnostic accuracy in sinus fungus balls: CT scan and operative findings. Am J Rhinol 2000; 14: 227–231.
- 34 Horst M, Hejjaoni A, Horst V, Michel FB, Bonsquent J. Double-blind, placebo controlled rush immunotherapy with a standardized Alternaria extract. J Allergy Clin Immunol 1990; 85: 460–472.
- 35 Marple BF. Allergic fungal rhinosinusitis: current theories and management strategies. Laryngoscope 2001; 111: 1006–1019.
- 36 Downs S, Mitkakis T, Marks G, et al. Clinical importance of Alternaria exposure in children. Am J Respir Crit Care Med 2001; 164: 455–459.
- 37 Honser SM, Corey JP. Allergic fungal rhinosinusitis: pathophysiology, epidemiology, and diagnosis. Otolaryngol Clin North Am 2000; 33: 399–408.
- 38 Ghegan MD, Lee FS, Schlosser RJ. Incidence of skull base and orbital erosion in allergic fungal rhinosinusitis (AFRS) and non-AFRS. Otolaryngol Head Neck Surg 2006; 134: 592–595.
- 39 Nussenbaum B, Marple BF, Schwade ND. Characteristics of bony erosion in allergic fungal rhinosinusitis. Otolaryngol Head Neck Surg 2001; 124: 150–154.
- 40 Kuhn FA, Swan R. Allergic fungal sinusitis: diagnosis and treatment. Curr Opin Otolarynogol Head Neck Surg 2003; 11: 1–5.
- 41 Marple BF, Gibbs SR, Newcomer MT, Mabry RL. Allergic fungal sinusitis-induced visual loss. Am J Rhinol 1999; 13: 191–195.
- 42 Meltzer E, Hamilos D, Hadley J, et al. Rhinosinusitis: establishing definitions for clinical research and patient care. J Allergy Clin Immunol 2004: 114( suppl): S155–S212.
- 43 Taylor MJ, Ponikau JU, Sherris DA, et al. Detection of fungal organisms in eosinophilic mucin using a fluorescein-labeled chitin-specific binding protein. Otolaryngol Head Neck Surg 2002; 127: 377–383.
- 44 Rao AK, Mathers PH, Ramadan HH. Detection of fungi in the sinus mucosa using polymerase chain reaction. Otolaryngol Head Neck Surg 2006; 134: 581–585.
- 45 Kim ST, Choi JH, Jeon HG, Cha HE, Hwang YJ, Chung YS. Comparison between polymerase chain reaction and fungal culture for the detection of fungi in patients with chronic sinusitis and normal controls. Acta Otolaryngol 2005; 125: 72–75.
- 46 Polzehl D, Weschta M, Podbielski A, Riechelmann H, Rimek D. Fungus culture and PCR in nasal lavage samples of patients with chronic rhinosinusitis. J Med Microbiol 2005; 54: 31–37.
- 47 Kostamo K, Richardson M, Eerola E, et al. Negative impact of Aspergillus galactomannan and DNA detection in the diagnosis of fungal rhinosinusitis. J Med Microbiol 2007; 56: 1322–1327.
- 48 Saravanan K, Panda NK, Chakrabarti A, Bapuraj RJ. Allergic fungal rhinosinusitis: an attempt to resolve the diagnostic dilemma. Arch Otolaryngol Head Neck Surg 2006; 132: 173–178.
- 49 Manning SC, Holman M. Further evidence for allergic pathophysiology in allergic fungal sinusitis. Laryngoscope 1998; 108: 1485–1496.
- 50 Chhabra A, Handa KK, Chakrabarti A, Mann SBS, Panda N. Allergic fungal sinusitis: clinicopathological characteristics. Mycoses 1996; 39: 437–441.
- 51 Panda NK, Sharma SC, Chakrabarti A, Mann SBS. Paranasal sinus mycoses in north India. Mycoses 1998; 41: 281–286.
- 52 Dhiwakar M, Thakar A, Bahadur S, et al. Pre-operative diagnosis of allergic fungal sinusitis. Laryngoscope 2003; 113: 688–694.
- 53 Taj-Aldeen SJ, Hilal AA, Schell WA. Allergic fungal rhinosinusitis: a report of 8 cases. Am J Otolaryngol 2004; 25; 213–218.
- 54 Ponikau JU, Sherris DA, Kephart GM, et al. Striking deposition of toxic eosinophil major basic protein in mucus: implications for chronic rhinosinusitis. J Allergy Clin Immunol 2005; 116: 362–369.
- 55 Shin SH, Ponikau JU, Sherris DA, et al. Chronic rhinosinusitis: an advanced immune response to ubiquitous airborne fungi. J Allergy Clin Immunol 2004; 114: 1369–1375.
- 56 Manning SC, Vuitch F, Weinberg AG, Brown OE. Allergic aspergillosis: a newly recognized form of sinusitis in the pediatric population. Laryngoscope 1989; 99: 681–685.
- 57 Borish L, Rosenwasser L, Steinke JW. Fungi in chronic hyperplastic eosinophilic sinusitis. Clin Rev Allergy Immunol 2006; 30: 1–9.
- 58 Bachert C, Gevaert P, Holtappels G, Johansson SG, Van Cauwenberge P. Total and specific IgE in the nasal polyps in related to local eosinophilic inflammation. J Allergy Clin Immunol 2001; 107: 607–614.
- 59 Thakar A, Sarkar C, Dhiwakar M, Bahadur S, Dahiya S. Allergic fungal sinusitis: expanding the clinicopathological spectrum. Otolaryngol Head Neck Surg 2004; 130: 209–216.
- 60 Venarske DL, deShazo RD. Sinobronchial allergic mycosis: the SAM Syndrome. Chest 2002; 121: 1670–1676.
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