Syndromes of invasive fungal sinusitis
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1 Medical Mycology 2009, 47 (Supplement 1), S309S314 Syndromes of invasive fungal sinusitis RICHARD D. DESHAZO University of Mississippi Medical Center, Department of Medicine, Jackson, Mississippi, USA Invasive fungal sinusitis should be suspected in immunocompromised or diabetic patients who present with acute sinusitis, inflammation of nasal septal mucosa, unexplained fever or cough, or the orbital apex syndrome. Histopathological studies are required to differentiate among these syndromes. Acute (fulminant) invasive fungal sinusitis has been called mucormycosis, zygomycosis and fulminant invasive sinusitis. Fever, cough, crusting of nasal mucosa, epistaxis, and headache are the most common presenting symptoms. Histopathological studies show hyphal invasion of blood vessels, vasculitis with thrombosis, and tissue infarction. Reports of granulomatous invasive fungal sinusitis come primarily from Sudan, but also from India, Pakistan, and the United States. Patients usually present with proptosis, appear to be immunocompetent and are infected almost exclusively with A. flavus. Chronic invasive fungal sinusitis can be distinguished from the two other forms of invasive fungal sinusitis by its chronic course, dense accumulation of hyphae resembling a mycetoma, and association with the orbital apex syndrome, diabetes mellitus, and corticosteroid treatment. Biopsy and orbital exploration show vascular invasion by fungal elements and only a sparse chronic inflammatory infiltrate. Keywords invasive fungal sinusitis, acute (fulminant) invasive fungal sinusitis, granulomatous invasive fungal sinusitis, chronic invasive fungal sinusitis Introduction Received 1 February 2008; Accepted 19 May 2008 Correspondence: Richard D. deshazo, University of Mississippi Medical Center, Department of Medicine, 2500 North State Street, Jackson, Mississippi 39216, USA. Tel: ; fax: rdeshazo@medicine.umsmed.edu Several years ago, in the course of treating a patient with fungal sinusitis, we reviewed the published literature on the topic. To our surprise, we could find no criteria for diagnosis or consensus on the classification of fungal sinusitis. Many reports of fungal sinusitis of various types were grouped under the heading of Aspergillus sinusitis, regardless of invasiveness or fungal agent. Because there was no consensus on classification, we found little clinically useful information on the natural history and treatment of those diseases. Therefore, our group began a reassessment of the syndromes of fungal sinusitis starting with their classification. Using published reports and case histories from our own clinics, clinical descriptions and diagnostic criteria for allergic fungal sinusitis, sinus mycetoma, and invasive fungal sinusitis were established. We have continued to participate with our colleagues in the treatment and follow up of patients with these syndromes [13]. We have learned a lot, but there is still much we do not know. Materials and methods In preparation for this paper, we reviewed the available medical literature on invasive fungal sinusitis in English using the search engines Medline, PubMed and Ovid. Distinguishing invasive from noninvasive fungal sinusitis Why some species of fungi cause fungal sinusitis and others do not is unclear, especially since fungi are the predominant airborne allergens in many parts of the United States. Nasal cultures for fungi have no role in the diagnosis of fungal sinusitis as fungi can be cultured from nasal secretions of most healthy 2009 ISHAM DOI: /
2 S310 DeShazo individuals in temperate climates, including those with allergic rhinitis. At present, diagnosis of a specific form of fungal sinusitis can be convincingly made only when fungal elements are visualized by histopathologic examination of tissue removed from a sinus. Although visible on staining, fungi may be difficult to culture from mucoid material in the noninvasive forms of fungal sinusitis: allergic fungal sinusitis and sinus mycetoma. This may reflect the limited viability of fungal elements in these conditions. Whether or not fungi can exist in sinus mucus without causing disease is unclear. We did not identify fungal elements on silver stains of the surgical material taken from 24 consecutive patients undergoing surgery for chronic bacterial sinusitis [3]. For now, the diagnosis of fungal sinusitis requires histopathological evaluation of sinus tissue and a familiarity with the characteristics of each of the clinical syndromes. Noninvasive fungal sinusitis In noninvasive fungal sinusitis, fungal elements are present in mucus material within the sinus but do not penetrate sinus mucosa, submucosa, blood vessels, or bone [4]. A history of chronic sinusitis is usually present, and many patients have nasal polyps. Sinus contents often have the consistency and appearance of peanut butter or cottage cheese and may be foulsmelling. Patients are immunocompetent but often have allergic rhinitis or asthma. In patients with diabetes or in those who are otherwise immunosuppressed, the diagnosis of noninvasive fungal sinusitis is suspect without a biopsy of sinus mucosa and bone. Invasive fungal sinusitis Clinical setting. Except for the rare case of granulomatous invasive fungal sinusitis [5], North American patients with invasive fungal sinusitis (IFS) are almost always immunocompromised [4]. Malignancy, chemotherapy for malignancy, organ transplantation, autoimmune disease, malnutrition, or diabetes are common comorbid conditions. Fungal elements are present on histopathologic evaluation within sinus mucosa, submucosa, blood vessels, or bone. Prominent tissue necrosis is also present, although the associated inflammatory infiltrate is variable. Fungal sinusitis should also be considered in any patient with chronic sinusitis when focal or diffuse areas of radiodensity are detected on computed tomography or with decreased T1- and T2- weighted signal intensities are present on magnetic resonance imaging of the sinuses [6]. The explanation of these radiological findings is unclear. Most patients with IFS do not have bone erosion or extension of the disease outside of the sinuses early in their course when salvage is most likely. Recent data suggest that unilateral thickening of nasal mucosa is the most common initial finding on CT and rhinoscopy in early disease [7] (see Fig. 1). At that stage, the nasal and sinus mucosa is usually not necrotic but pale or discolored on physical examination. Patients frequently seem more ill and have more pain and fever than physical examination would suggest. Later in the disease course, infected sinuses are frequently filled with large quantities of necrotic material, mucus, and polyps, especially with chronic invasive disease. Diagnosis. Delay in the diagnosis of invasive fungal sinusitis leads to increased mortality. Since diagnosis requires biopsies to establish tissue invasion by fungi, early endoscopic evaluation with biopsy of healthy and diseased tissue and culture of sinus contents is required when invasive fungal sinusitis is suspected [8,9]. Because concentrations of fungal elements vary from diffuse to dense, silver impregnation stains should be performed on all material submitted for histopathologic evaluation, including mucus, anytime fungal sinusitis is considered. Special stains for fungus must be obtained on all surgical specimens and should be routinely requested on material from any immunocompromised patient, including those with diabetes, hemochromatosis, neutropenic syndromes, or iatrogenic immunosuppression [10]. If endoscopic evaluation is negative and the diagnosis is still suspected, open biopsy of the sinuses should follow immediately so that adequate material may be obtained for evaluation. Fig. 1 Coronal computed tomographic scan from a patient with invasive fungal sinusitis showing unilateral left nasal cavity soft tissue thickening of the septum, turbinates, and nasal floor, with complete opacification of the left nasal cavity. From DelGaudio et al. [7]. Used with permission. Arch Otolaryngol 2003; 129: Copyright # (2003), American Medical Association. All Rights reserved.
3 Invasive fungal sinusitis S311 Serum aspergillous galactomannan Detection of fungemia before clinical sequella develop would be a major step forward in the diagnosis and treatment of fungal sinusitis. Although an international panel has recommended that histopathology or microscopy should continue to be used to diagnose invasive fungal reactions, that committee also noted that antigen detection testing could provide supportive evidence in the appropriate clinical setting [11]. Several antigen detection systems are now available for clinical use. Some studies have suggested that antigenemia with galactomannan is detectable as early as 58 days before clinical signs or symptoms of invasive aspergillosis. In a meta-analysis of 27 studies using consensus criteria for the diagnosis of invasive disease, ELISA sensitivity ranged from 6171%, specificity from 8993%, negative predictive value from 9598% and positive predictive value from 2653% [12]. Performance of the assay seemed to vary among patients with malignancy, hematological and organ transplants, but specific information is not available on those patients with invasive aspergillus sinusitis. Performance is adversely affected by the administration of certain medications, including penicillins, and the presence of other organisms such as Penicillium spp. The utility of PCR-based testing is unclear. Beta-D-glucan The US Food and Drug Agency (FDA) has approved a serum or plasma spectrophotometric assay for beta-dglucon (Fungitell assay), a cell wall component of all fungi except Cryptococcus and zygomycetes (Rhizopus, Absidia, Cunninghamella, Rhizomucor, Syncephalastrum, Saksenaea, Apophysomycetes and Mucor). Sensitivity and specificity in the diagnosis of invasive fungal disease has been as high as 93 and 77% respectively [12]. Again, no specific data are available on invasive aspergillus sinusitis. Classification of invasive fungal sinusitis Criteria for diagnosis of invasive fungal sinusitis have been established and are based on confirmation of tissue invasion (Table 1) [3]. Granulomatous invasive fungal sinusitis. Granulomatous invasive fungal sinusitis, also called primary paranasal granuloma and indolent fungal sinusitis, is a curious syndrome of chronic granulomatous sinusitis associated with proptosis [5] (Table 2). Reports have come primarily from Sudan, but also from India and Pakistan. Only a few reports have come from the United States. Patients appear to be immunocompetent and are infected almost exclusively with Aspergillus flavus. Histopathological evaluation shows there is profuse fungal growth with regional tissue invasion, noncaseating granulomas with giant cells, and plasma cells. Unless removed surgically, the resulting fibrous fungal mass may spread into the orbit, dura, and brain [13]. Treatment with itraconazole at a dose of 8 to 10 mg per kilogram per day appears to decrease the otherwise high postoperative relapse rate [14]. Acute fulminant invasive fungal sinusitis. Acute fulminant invasive fungal sinusitis results from the rapid spread of fungi from the nasal mucosa and sinus by way of vascular invasion into the orbit, vessels, and parenchyma of the brain [1520]. Patients are usually immunocompromised by human immunodeficiency virus infection, chemotherapy, or diabetes, but the condition has been reported in association with hemochromatosis and rarely in apparently healthy individuals [15]. Classically reported sentinel signs and symptoms include dark-colored nasal septal or palatal ulcers (eschars), fever, headache, nasal crusting, epistaxis, cough and mental status changes. This symptom complex was previously called at least four names, including mucormycosis depending on the organism. When this syndrome has been caused by saprophytic fungi of the order Mucorales, including rhizopus, rhizomucor, absidia, mucor, cunninghamella, mortierella, saksenaea, and apophysomyces, it has been called zygomycosis. An identical syndrome has been described with Aspergillus, Fusarium, and Pseudallescheria boydii infections and has been called fulminant invasive sinusitis. Histopathological studies show hyphal invasion of blood vessels, including the carotid arteries and cavernous sinuses, vasculitis with thrombosis, hemorrhage and tissue infarction. Table 1 Diagnostic criteria for invasive fungal sinusitis 1. Mucosal thickening or air fluid levels compatible with sinusitis on radiologic imaging. 2. Histopathologic evidence of hyphal forms within sinus mucosa, submucosa, blood vessels, or bone. 3. To diagnose granulomatous invasive fungal sinusitis, histopathologic evidence of hyphal forms within sinus mucosa, submucosa, blood vessel or bone in association with granuloma containing giant cells is required. Concomitant stains for mycobacteria must be negative. Adapted from deshazo et al. [3].
4 Table 2 Comparative features of invasive fungal sinusitis S312 DeShazo Syndrome Representative fungi Geographic distribution Host Associated conditions Histopathology Clinical presentation Treatment Prognosis Acute (fulminant) invasive fungal sinusitis Chronic invasive fungal sinusitis Granulomatous invasive fungal sinusitis Fungi of the order of Mucorales, and Aspergillus fumigatus Aspergillus fumigatus Aspergillus flavus No specific geographic location No specific geographic location Predominately in North America CT, computed tomography. Adapted from deshazo et al. [4]. Immunocompromised and rarely in immunocompetent Diabetes, malignancy, immunosuppressive therapy Sparse fungal elements in mucosa, submucosa, blood-vessels or bone with extensive tissue necrosis and neutrophilic inflammation Immunocompromised Diabetes mellitus Dense accumulation of fungal elements in a mucoid matrix forming an expansile mass. Low-grade chronic inflammatory response in adjacent mucosa Immunocompetent None Fungal elements in mucosa, submucosa, blood vessels or bone with extensive tissue necrosis and neutrophilic inflammation. Chronic pan-sinusitis, nasal polyps, calcification within sinus on CT, proptosis or eye muscle entrapment in children Rhinosinusitis (often unilateral) nasal obstruction, green-brown nasal discharge, calcification in the sinus on CT. Fever, cough, crusting of nasal mucosa, epistaxis, headache, mental status changes. Debridement, aeration, oral and topical corticosteroids and allergen immunotherapy. No evidence that oral antifungals are helpful Debridement, aeration. Antifungals not required Radical debridement to histopathologically normal tissue, antifungal antibiotic treatment of underlying conditions. Recurrence common Excellent Fair when limited to sinus; poor with intracranial involvement.
5 Invasive fungal sinusitis S313 The prognosis of acute fulminant invasive fungal sinusitis is grave unless diagnosed early, where the best outcomes report only 50% survival. Treatment includes simultaneous surgical removal of devitalized tissue down to healthy tissue planes, and antifungal therapy, previously given at conventional doses [21]. Clinical experience has led most experts to recommend high does intravenous ampthotericin B to treat invasive fungal sinusitis (ampthotericin B deoxycholate 1mg/ kg/day or liposumal amphotericin B 57.5mg/kg/day). Exceptions include P. boydii which is often resistant and better treated with voriconazole and Aspergillus species which seem more responsive to voriconazole, at least in other locations. Surgery should be performed for histopathological evaluation and to debride the devitalized tissue supporting fungal growth. When histopathological studies confirm tissue invasion, treatment with high dose antifungal therapy should be initiated immediately, without waiting for the results of fungal cultures, and for intervals determined by the clinical response. Close collaboration between medical and surgical specialists is essential in the care of these patients. Obviously, treatment of underlying immunodeficiency, or reconstitution of the iatrogenic immunodeficiency, is desirable but often difficult. The condition may recur after apparently successful treatment when immunosuppression is ongoing and requires chronic suppressive therapy. Chronic invasive fungal sinusitis. Although sporadic reports of patients with a syndrome resembling chronic invasive fungal sinusitis have been published, it has only recently been recognized as a specific form of fungal sinusitis [3,4]. Chronic invasive fungal sinusitis results from a slowly progressive fungal infection that elicits limited inflammation, usually in diabetic patients. As opposed to the neutrophil-rich, highly necrotic, and angiotrophic process seen in acute invasive fungal sinusitis, there is a low-grade mixed cellular infiltrate in affected tissues [22]. Thick nasal polyposis and thick purulent mucus, like that seen grossly in allergic fungal sinusitis and mycetoma, are also common. When the infection expands out of the ethmoid sinuses medically into the orbit, orbital apex syndrome has been a common clinical presentation [23,24] (Fig. 2). This condition results from erosion of the fungal mass into the orbital apex, causing decreasing vision and abnormalities of ocular mobility. Proptosis may also occur. Chronic invasive fungal sinusitis may be advanced by the time of diagnosis, with posterior erosion out of the ethmoid sinus, resulting in cerebrovascular accidents from cavernous venous thrombosis and death. Treatment is the same as for Fig. 2 Axial computed tomographic scan in a patient with invasive fungal sinusitis showing bone erosion of the left lamina papyracea (arrow) with soft tissue thickening of the lateral nasal and medial canthal areas. There is also extensive unilateral nasal cavity soft tissue thickening on the left side. From DelGaudio et al. [7]. Used with permission. Arch Otolaryngol 2003; 129: Copyright # (2003), American Medical Association. All Rights reserved. acute invasive disease, with surgery and antifungal therapy. The role of newer oral antifungal agents in invasive fungal sinusitis is unclear but promising [25]. In infections with organisms resistant to amphotericin B, such as Pseudallescheria boydii, azole therapy has been reported to be lifesaving. Antimicrobial treatment of invasive aspergillous sinusitis An increasing array of antimicrobial agents is available to treat invasive fungal sinusitis. Examples include the azoles (itraconazole), traizoles (voriconazole) and echinocandins (caspofungin) in addition to the goldstandard polyene, amphotericin B deoxycholate and its lipid-based cousins. In the case of aspergillosis, no controlled studies are available on antimicrobial treatment of invasive fungal sinusitis. Amphotericin-B treatment requires 11.5 mg/ kg/day, a dose almost always associated with nephrotoxicity. Therefore, lipid formulations became the standard of care for polyene therapy in invasive aspergillosis (Abelcet or AmBisome). Even then, Aspergillus species such as A. terreus may be resistant to the drug. Therefore, voriconazole has become the treatment of choice for invasive aspergillus sinusitis when the diagnosis is established as such [26]. The usual adult dose is 6mg/kg i.v. twice a day on day one followed by 4 mg/kg i.v. twice a day for 7 days with the option to decrease to 200 mg orally, twice a day thereafter. Patients with acute invasive aspergillosis who were not ventilator dependent showed a greater percentage of complete or partial response, lower mortality rate and a lower incidence of side effects
6 S314 DeShazo with this regimen. Since this drug has little activity against zygomycetes, it should not be used unless the diagnosis of aspergillosis has been made. Itraconazole is one of several second line drugs for treatments for aspergillosis since voriconazole has greater activity with fewer side effects. Caspofungin is approved for treatment of invasive aspergillosis in patients who cannot tolerate or are refractory to voriconazole. After an initial dose of 70mg i.v., 50mg/ day is given i.v. as salvage therapy [27]. Conclusion With an ever increasing number of effective therapies for cancer and autoimmune disease that also cause suppression of cell mediated immunity, fungal disease and fungal sinusitis will be a growing problem. Now that diagnostic criteria are available, multicenter trials comparing diagnostic and therapeutic approaches are greatly needed. Acknowledgements The author thanks Leigh Wright, BA for her assistance with the preparation and Stanley Chapman for review of this manuscript. Sources of funding: The author has received no source of funding for this paper. Declaration of interest: The author reports no conflicts of interest. The author alone is responsible for the content and writing of the paper. References 1 deshazo RD, Swain RE. Diagnostic criteria for allergic fungal sinusitis. J Allergy Clin Immunol 1995; 96: deshazo RD, O Brien M, Chapin K, et al. Criteria for the diagnosis of sinus mycetoma. J Allergy Clin Immunol 1997; 99: deshazo RD, O Brien M, Chapin K, et al. A new classification and diagnostic criteria for invasive fungal sinusitis. Arch Otolaryngol Head Neck Surg 1997; 123: deshazo RD, deshazo MD, Chapin K, Swain R. Current concepts: fungal sinusitis. N Engl J Med 1997; 337: Milosev B, Mahgoub ES, Aal OA, El Hassan AM. Primary aspergilloma of paranasal sinuses in the Sudan. Br J Surg 1969; 56: Zinreich SJ, Kennedy DW, Malat J, et al. Fungal sinusitis: diagnosis with CT and MR imaging. Radiology 1988; 169: DelGaudio JM, Swain RE Jr, Kingdom TT, et al. Computed tomographic findings in patients with invasive fungal sinusitis. Arch Otol Head Neck Surg 2003; 129: Blitzer A, Lawson W, Meyers BR, Biller HF. Patient survival factors in paranasal sinus mucormycosis. Laryngoscope 1980; 90: Loftus BC. General principles of management of fungal infections of the head and neck. Otolaryngol Clin North Am 1993; 26: Brandwein M. Histopathology of sinonasal fungal disease. Otolaryngol Clin North Am 1993; 26: Pfeiffer CD, Fine JP, Safdar N. Diagnosis of invasive aspergillosis using a galactomannan array: a metaanalysis. Clin Infect Dis 2006; 42: Odabasi A, Matiuzzi G, Estey Z, et al. Beta-D-glucon as a diagnostic adjunct for invasive fungal infections: validation, cutoff development and performance in patients with acute myelogenous leukemia and myleodysplastic syndrome. Clin Infect Dis 2004; 39: Veress B, Malik OA, El Tayeb AA, et al. Further observations on the primary paranasal Aspergillus granuloma in the Sudan: a morphological study of 46 cases. Am J Trop Med Hyg 1973; 22: Gumaa SA, Mahgoub ES, Hay RJ. Postoperative responses of paranasal Aspergillus granuloma to itraconazole. Trans R Soc Trop Med Hyg 1992; 86: Radner AB, Witt MD, Edwards JE Jr. Acute invasive rhinocerebral zygomycosis in an otherwise healthy patient: case report and review. Clin Infect Dis 1995; 20: Talbot GH, Huang A, Provencher M. Invasive Aspergillus rhinosinusitis in patients with acute leukemia. Rev Infect Dis 1991; 13: Gonzalez-Crespo MR, Gomez-Reino JJ. Invasive aspergillosis in systemic lupus erythematosus. Semin Arthritis Rheum 1995; 24: Meyer RD, Gaultier CR, Yamashita JT, et al. Fungal sinusitis in patients with AIDS: report of 4 cases and review of the literature. Medicine 1994; 73: The W, Matti BS, Marisiddaiah H, Minamoto GY. Aspergillus sinusitis in patients with AIDS: report of three cases and review. Clin Infect Dis 1995; 21: Choi SS, Milmoe GJ, Dinndorf PA, Quinones RR. Invasive Aspergillus sinusitis in pediatric bone marrow transplant patients: evaluation and management. Arch Otolaryngol Head Neck Surg 1995; 121: Graybill JR. The future of antifungal therapy. Clin Infect Dis 1996; 22(Suppl. 1): S166S Milro CM, Blanshard JD, Lucas S, Michaels L. Aspergillosis of the nose and paranasal sinuses. J Clin Pathol 1989; 42: Dooley DP, Hollsten DA, Grimes Sr, Moss J Jr. Indolent orbital apex syndrome caused by occult mucormycosis. J Clin Neuroophthalmol 1992; 12: Young CN, Swart J, Ackermann D, Davidge-Pitts K. Nasal obstruction and bone erosion caused by Drechslera hawaiiensis. J Laryngol Otol 1978; 92: Georgeopapadakou NH, Walsh TJ. Antifungal agents: chemotherapeutic targets and immunologic strategies. Antimicrob Agents Chemother 1996; 40: Herbrecht R, Denning DW, Patterson TF, et al. Voriconazole versus amphotercin B for primary therapy of invasive aspergillosis. N Eng J Med 2002; 347: Muertens J, Road I, Petrikkos G, et al. Efficiency and safety of caspofungin for treatment of invasive aspergillosis in patients refractory to or intolerant of conventional antifungal therapy. Clin Infect Dis 2004; 39: This paper was first published online on ifirst on 24 July 2008.
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