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1 Medical Mycology Case Reports 1 (2012) Contents lists available at SciVerse ScienceDirect Medical Mycology Case Reports journal homepage: Granulomatous invasive fungal rhinosinusitis extending into the pterygopalatine fossa and orbital floor: A case report Tae Hoon Kim, Hyun Uk Jang, Yun Young Jung, Jung Soo Kim n Department of Otorhinolaryngology Head and Neck Surgery, School of Medicine, Kyungpook National University, Daegu, Korea article info Article history: Received 1 September 2012 Received in revised form 5 October 2012 Accepted 12 October 2012 Keywords: Fungi Sinusitis Aspergillosis abstract Invasive fungal rhinosinusitis is a rare and life-threatening disease. Granulomatous invasive fungal rhinosinusitis has a time course exceeding 12 weeks, and the destruction of bone progresses slowly. This disease has been reported primarily in Sudan, India, Pakistan, and the USA; however, it is very rare in Korea. In this study, we present the case of a 69-year-old man with granulomatous invasive fungal rhinosinusitis. He was successfully treated with a combination of surgery and itraconazole. & 2012 International Society for Human and Animal Mycology. Published by Elsevier B.V. All rights reserved. 1. Introduction 2. Case Invasive fungal rhinosinusitis is rare; however, there has recently been an increase in the prevalence of invasive fungal rhinosinusitis due to the development of diagnostic techniques and an increase in the prevalence of diabetes and immunosuppressive conditions. Invasive fungal rhinosinusitis is a potentially life-threatening disease that has high mortality and morbidity rates. Several organisms are known to cause fungal rhinosinusitis, of which Aspergillus is the most common [1]. Fungal rhinosinusitis can be classified as invasive and noninvasive on the basis of the histopathological findings of the invaded tissue. Invasive fungal rhinosinusitis is further classified into 3 groups: (1) acute invasive (fulminant) fungal rhinosinusitis, (2) granulomatous invasive fungal rhinosinusitis, and (3) chronic invasive fungal rhinosinusitis [2,3]. Of these, granulomatous invasive fungal rhinosinusitis has been primarily reported in Sudan, but it is also prevalent in India, Pakistan, and the United States [2,3]. Invasive fungal rhinosinusitis, excluding granulomatous invasive fungal rhinosinusitis, mostly occurs in diabetics and other immunosuppressed patients. In Korea and Japan, several cases of invasive fungal rhinosinusitis have been reported [4,5]; however, no case of granulomatous invasive fungal rhinosinusitis has been reported. In this study, we report the clinical case of a patient with granulomatous invasive fungal rhinosinusitis involving the pterygopalatine fossa and orbital floor and review the associated literature. n Corresponding author. Tel.: þ ; fax: þ address: sookim@knu.ac.kr (J.S. Kim). A 69-year-old man with a history of hypertension and HBV carriage was referred to our hospital (Day 0) because of headache, which had persisted for 6 months (Day 180), and left cheek numbness and pain, which had persisted for 2 months (Day 60). Brain magnetic resonance imaging (MRI) was performed at a local medical center 3 months (Day 90) before he visited our hospital; however, the MRI findings were nonspecific. Afterward, he remained under observation without any specific treatment. His headache persisted, and he developed left cheek numbness and pain. He visited our hospital and underwent MRI and computed tomography (CT) serially (Day 0). T2-weighted MR images revealed hypointense signal opacity that extended into the posterior wall of the left maxillary sinus. T1-weighted MR images with gadolinium-enhancement revealed enhanced signal opacity in the left maxillary sinus that extended into the posterior wall (Fig. 1). CT showed opacity of the left maxillary sinus that extended into the pterygopalatine fossa, orbital floor, and lateral maxillary sinus wall (Figs. 2a and b). We performed endoscopic biopsy and partial debridement under local anesthesia to rule out malignant disease or mucocele (Day 43). Histological examination confirmed tissue invasion by Aspergillus with the formation of granuloma and fibrosis (Fig. 3). Granulomatous invasive fungal rhinosinusitis was diagnosed on the basis of clinical and histopathologic findings. Follow-up CT (Day 83) revealed exacerbation of the disease condition in comparison to the previous CT (Figs. 2c and d). We performed left partial maxillectomy without orbital exenteration under general anesthesia because of the relative ease of separating pathologic tissues from the periorbitum (Day 88). The maxillary sinus was filled with granulation and /$ - see front matter & 2012 International Society for Human and Animal Mycology. Published by Elsevier B.V. All rights reserved.
2 108 T. Hoon Kim et al. / Medical Mycology Case Reports 1 (2012) site (Fig. 4). To date (Day 530), the patient has successfully managed postsurgery with amphotericin B followed by itraconazole, without clinical symptoms or recurrence. 3. Discussion Fig. 1. (a) Gadolinium-enhanced T1-weighted magnetic resonance (MR) image showing enhanced opacity with extension into the posterior wall of the left maxillary sinus. (b) T2-weighted MR image showing hypointensity signal opacity with extension into the posterior wall of the left maxillary sinus along with the findings of (a). necrotic tissue. A biopsy specimen confirmed invasion of the surrounding tissue by Aspergillus. Systemic amphotericin B (50 mg/day) was intravenously administered for 10 days after the operation. The patient experienced intermittent fever (maximum body temperature: C) and chilling sensations during the amphotericin B therapy. Therefore, the antifungal agent was changed to itraconazole. The patient received intravenous itraconazole (250 mg/day) for 10 days and oral itraconazole (400 mg/day) for 70 days. Administration of the antifungal agent was stopped after 3 months (Day 180). At the 6-month follow-up visit (Day 250), endoscopic findings revealed no recurrence and confirmed the healing of the surgical Three types of fungal rhinosinusitis were identified by McGill in 1980: indolent aspergillosis, aspergilloma, and fulminant aspergillosis [6]. Since the late 1990s, a new type of fungal rhinosinusitis has been reported [2,3]. Fungal rhinosinusitis is classified as noninvasive and invasive. Invasive fungal rhinosinusitis is further classified into 3 types: acute invasive (fulminant) fungal rhinosinusitis, chronic invasive fungal rhinosinusitis, and granulomatous invasive fungal rhinosinusitis. Acute invasive (fulminant) fungal rhinosinusitis occurs predominantly in immunocompromised and rarely in immunocompetent patients, and it has a time course of less than 4 weeks. Its histopathology includes vascular invasion, inclusion of the carotid arteries and cavernous sinus, vasculitis with thrombosis, hemorrhage, and tissue infarction [2,3]. Aspergillus fumigatus and saprophytic fungi of the order Mucorales are the most common causative agents. Chronic invasive fungal rhinosinusitis and granulomatous invasive fungal rhinosinusitis have a time course exceeding 12 weeks. The most important differences between chronic and granulomatous invasive fungal rhinosinusitis are the histopathological characteristics. Chronic invasive fungal rhinosinusitis is characterized by the dense accumulation of the hyphae, occasional invasion of the blood vessels, and the involvement of adjacent tissues, whereas granulomatous invasive fungal rhinosinusitis is characterized by noncaseating granuloma with foreign bodies or Langhans-type giant cells, occasional vasculitis, vascular proliferation, and perivascular fibrosis [2,3]. The former usually develops in immunocompromised patients who are infected with A. fumigatus, whereas the latter develops in immunocompetent patients, most commonly in association with Aspergillus flavus infection. Radiological findings associated with fungal rhinosinusitis generally include hyperattenuating soft-tissue collection and calcifications in the paranasal sinus on CT scans. Iso or hypointense signals are observed on T1-weighted MR images, and marked hypointense signals are observed on T2-weighted MR images. It is known that CT is superior to MRI for evaluating the sinonasal anatomy and identifying the surgical landmark. The imaging findings of chronic invasive fungal rhinosinusitis are similar to those of granulomatous invasive fungal rhinosinusitis. These findings are analogous to those of malignant lesions and include bony destruction and extension beyond the sinus. By contrast, acute invasive fungal rhinosinusitis is occasionally associated with very subtle and nonsignificant bone destruction and mucosal thickening compared to the other types of invasive fungal rhinosinusitis [7]. In our case, the patient complained of a headache for 6 months and left cheek numbness and pain that had persisted for 2 months. Although 3 months elapsed before a diagnosis of granulomatous invasive fungal rhinosinusitis was made, this was not considered consequential for a chronic disease. The patient was in an immunocompetent state and histological examination with Gomori methenamine silver staining revealed tissue invasion by narrow septate hyphae and 451 dichotomous branching hyphae, which are consistent with Aspergillus; moreover, histological examination with hematoxylin and eosin staining (H&E stain) revealed granuloma and giant cells (Fig. 3). Hence, granulomatous invasive fungal rhinosinusitis was diagnosed because these findings were consistent with its diagnostic criteria. The standard management of invasive fungal rhinosinusitis involves a combination of surgical debridement and antifungal
3 T. Hoon Kim et al. / Medical Mycology Case Reports 1 (2012) Fig. 2. (a and b) Initial coronal computed tomography (CT) scans showing opacification of the left maxillary sinus extending into the orbital floor and pterygopalatine fossa. (c and d) After 2 months, coronal CT scans revealed progressed lesions in comparison to the initial CT findings. agent administration with the treatment of underlying diseases such as immunosuppression and diabetes. Unlike other types of invasive fungal rhinosinusitis, granulomatous invasive fungal rhinosinusitis can be treated by surgery alone without the use of antifungal agents [8]. However, DeShazo et al. [3] suggested debridement, aeration, and itraconazole as the best treatments for granulomatous invasive fungal rhinosinusitis. Invasive fungal rhinosinusitis is primarily treated using antifungal agents such as amphotericin B and itraconazole, which are administered after surgery. It is known that amphotericin B is effective against species of Aspergillus, which belong to the order Mucorales, and Candida, whereas itraconazole is effective against Aspergillus spp. Itraconazole has relatively fewer side effects than amphotericin B. Recently, voriconazole has been introduced clinically as a new antifungal agent. This is a new broad-spectrum triazole with efficacy against fungi such as Candida and Aspergillus spp. Moreover, it is superior to amphotericin B for the treatment of invasive aspergillosis with respect to its therapeutic effects [9]. Thus, voriconazole has been widely used for the treatment of invasive aspergillus rhinosinusitis since its approval by the Food and Drug Administration. However, we did not use voriconazole in our case because the patient did not satisfy the application standard of Korean health insurance. Although the duration of antifungal agent administration for the treatment of granulomatous invasive fungal rhinosinusitis is disputable, Stringer et al. [10] recommended that patients should receive amphotericin B for 6 weeks and should additionally receive amphotericin B or itraconazole for a little longer to control the disease. In our case, the patient received antifungal agents for 3 months and displayed no clinical symptoms or recurrence 18 months after the surgery.
4 110 T. Hoon Kim et al. / Medical Mycology Case Reports 1 (2012) Fig. 3. (a) Fibrosis demonstrated by hematoxylin and eosin (H&E) staining ( 100). (b) Granuloma and giant cells as identified by H&E staining ( 200). (c) Periodic acid- Schiff staining showing fungal hyphae in the giant cells ( 200). (d) Narrow septate hyphae and 41 dichotomous branching hyphae consistent with Aspergillus, as identified by Gomori methenamine silver staining ( 100). the high relapse rate of granulomatous invasive fungal rhinosinusitis after surgery. Because granulomatous invasive fungal rhinosinusitis is extremely rare in Korea, its diagnosis is delayed due to the lack of knowledge about the disease. Despite the increasing lesion size in the orbital area on follow-up CT scans, we treated this disease successfully with surgery and antifungal agents (amphotericin B followed by itraconazole), preserving the vision of the patient. Therefore, based on our experience and other studies, we suggest that a combination of surgery and antifungal agents (amphotericin B or itraconazole) is essential for the treatment of granulomatous invasive fungal rhinosinusitis rather than surgery alone to achieve optimal outcomes. Author s contribution Fig. 4. Endoscopic findings. We observed healthy mucosa and no recurrence in the nasal cavity sinus after 6 months of follow-up (Day 250). Therefore, we agree that antifungal agents should be administered to patients with granulomatous invasive fungal rhinosinusitis for more than 6 weeks. The prognosis of invasive fungal rhinosinusitis is generally poor. Although granulomatous invasive fungal rhinosinusitis has a good prognosis in comparison to the other types of invasive fungal rhinosinusitis, it tends to have a high relapse rate [3]. Gumaa et al. [11] reported that itraconazole effectively reduces TH Kim: Manuscript writing and data collection; HU Jang and YY Jung: data collection and proofreading of the manuscript; JS Kim: study design and responsibility for the integrity of the content of the paper. All the authors have read and approved the final version of the manuscript. Conflict of interest None.
5 T. Hoon Kim et al. / Medical Mycology Case Reports 1 (2012) Acknowledgment There are no acknowledgment for this paper. References [1] Stammberger H, Jakse R, Beaufort F. Aspergillosis of the paranasal sinuses x-ray diagnosis, histopathology, and clinical aspects. Annals of Otology Rhinology and Laryngology 1984;93(3 Pt 1): [2] Chakrabarti A, Denning DW, Ferguson BJ, Ponikau J, Buzina W, Kita H, et al. Fungal rhinosinusitis: a categorization and definitional schema addressing current controversies. Laryngoscope 2009;119(9): [3] deshazo RD, Chapin K, Swain RE. Fungal sinusitis. New England Journal of Medicine 1997;337(4): [4] Nakaya K, Oshima T, Kudo T, Aoyagi I, Katori Y, Ota J, et al. New treatment for invasive fungal sinusitis: three cases of chronic invasive fungal sinusitis treated with surgery and voriconazole. Auris, Nasus, Larynx 2010;37(2): [5] Kim DK, Nam SK, Lee KA, Cho JHA. Case of chronic invasive fungal sinusitis invading pterygopalatine fossa. Korean Journal of Otorhinolaryngology Head and Neck Surgery 2010;53(5): [6] McGill TJ, Simpson G, Healy GB. Fulminant aspergillosis of the nose and paranasal sinuses: a new clinical entity. Laryngoscope 1980;90(5 Pt 1): [7] Aribandi M, McCoy VA, Bazan III C. Imaging features of invasive and noninvasive fungal sinusitis: a review. Radiographics 2007;27(5): [8] Milosev B, el-mahgoub S, Aal OA, el-hassan AM. Primary aspergilloma of paranasal sinuses in the Sudan. A review of seventeen cases. British Journal of Surgery 1969;56(2): [9] Herbrecht R, Denning DW, Patterson TF, Bennett JE, Greene RE, Oestmann JW, et al. Voriconazole versus amphotericin B for primary therapy of invasive aspergillosis. New England Journal of Medicine 2002;347(6): [10] Stringer SP, Ryan MW. Chronic invasive fungal rhinosinusitis. Otolaryngologic Clinics of North America 2000;33(2): [11] Gumaa SA, Mahgoub ES, Hay RJ. Post-operative responses of paranasal Aspergillus granuloma to itraconazole. Transactions of the Royal Society of Tropical Medicine and Hygiene 1992;86(1):93 94.
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