Abstract
Mucormycosis (Zygomycosis) is a rare, invasive, opportunistic fungal infection of the paranasal sinuses, caused by a fungus of the order Mucorales. We report a case of rhinoorbital mucormycosis caused by Rhizopus oryzae in an acute lymphoblastic leukemia patient and review the 79 Mucormycosis cases reported in the last decade from Turkey. In our case, the diagnosis was made with endoscopic appearance, computerized tomography of the paranasal sinuses, and culture of the surgical materials. Following aggressive surgical debridement and parenteral amphotericin B therapy, the patient recovered completely. In Turkish literature, rhinocerebral manifestations were the most common form of the mucormycosis (64 cases), followed by pulmonary form (6 cases). The most common risk factor was hematologic malignancies (32 cases) and diabetes mellitus (32 cases), similar to those reported from the rest of the world. The etiologic agents responsible for the review cases were Rhizopus sp., Mucor spp., Rhizomucor spp., Rhizopus oryzae, Mucor circinelloides, and Lichtheimia corymbifera. Although various treatment modalities were used, amphotericin B was the mainstay of therapy. Mortality rate was found to be 49.4% in review cases. It seems that strong clinical suspicion and early diagnosis, along with aggressive antifungal therapy and endoscopic sinus surgery, have great importance for better prognosis in mucormycosis.
References
Kwon-Chung KJ, Bennett JE. Medical mycology. Philadelphia: Lea & Febiger; 1992. p. 524–59.
Ribes JA, Vanover-Sams CL, Baker DJ. Zygomycetes in human disease. Clin Microbiol Rev. 2000;13:236–301.
Romano C, Miracco C, Massai L, et al. Case report. Fatal rhinocerebral zygomycosis due to Rhizopus oryzae. Mycoses. 2002;45:45–9.
Saraçlı MA. Rhizopus, Rhizomucor, Absidia ve Diğer Sistemik ve Subkütanöz Zigomikoz Etkenleri. In: Başustaoğlu AC, editor. Klinik Mikrobiyoloji. Ankara: Atlas Kitapçılık; 2009. p. 1839–56.
Hilal AA, Taj-Aldeen SJ, Mirghani AH. Rhinoorbital mucormycosis secondary to Rhizopus oryzae: a case report and literature review. Ear Nose Throat J. 2004;83:558–62.
Chayakulkeeree M, Ghannoum MA, Perfect JR. Zygomycosis: the re-emerging fungal infection. Eur J Clin Microbiol Infect Dis. 2006;25:215–29.
Ferguson BJ. Mucormycosis of the nose and paranasal sinuses. Otolaryngol Clin North Am. 2000;33:349–65.
Baradkar VP, Mathur M, Panda M, Kumar S. Sino-orbital infection by Syncephalastrum racemosum in chronic hepatorenal disease. J Oral Maxillofac Pathol. 2008;12:45–7.
Nosari A, Oreste P, Montillo M, et al. Mucormycosis in hematologic malignancies: an emerging fungal infection. Haematologica. 2000;85:1068–71.
Yohai RA, Bullock JD, Aziz AA, Markert RJ. Survival factors in rhino-orbital-cerebral mucormycosis. Surv Ophthalmol. 1994;39:3–22.
Baker RD. Mucormycosis. A new disease? JAMA. 1957;163:805–8.
Romano C, Ghilardi A, Massai L, Capecchi PL, Miraccco C, Fimiani M. Primary subcutaneous zygomycosis due to Rhizopus oryzae in a 71-year old man with normal immune status. Mycoses. 2007;50:82–4.
Diwakar A, Dewan RK, Chowdhary A, Randhawa HS, Khanna G, Gaur SN. Zygomycosis–a case report and overview of the disease in India. Mycoses. 2007;50:247–54.
Barr A, Nolan M, Grant W, Costello C, Petrou MA. Rhinoorbital and pulmonary zygomycosis post pulmonary aspergilloma in a patient with chronic lymphocytic leukaemia. Acta Biomed. 2006;77:13–8.
Kara IO, Tasova Y, Uguz A, Sahin B. Mucormycosis-associated fungal infections in patients with haematologic malignancies. Int J Clin Pract. 2009;63:134–9.
Rao SP, Kumar KR, Rokade VR, Khanna V, Pal C. Orbital apex syndrome due to mucormycosis caused by Rhizopus microsporum. Ind J Otolaryng Head Neck Surg. 2006;58:84–7.
Liang KP, Tlevjeh IM, Wilson WR, Roberts GD, Temesgen Z. Rhino-orbitocerebral mucormycosis caused by Apophysomyces elegans. J Clin Microbiol. 2006;44:892–8.
Stark D, Milliken S, Marriott D, Harkness J. Rhizopus microsporus var. rhizopodiformis sinus-orbital zygomycosis in an immunosuppressed patient: successful treatment with posaconazole after a complicated clinical course. J Med Microbiol. 2007;56:699–701.
Ibrahim M, Chitnis S, Fallon K, Roberts T. Rhinocerebral mucormycosis in a 12-year-old girl. Arch Neurol. 2009;66:272–3.
Ganesh R, Manikumar S, Vasanthi T. Rhinocerebral mucormycosis in an adolescent with type 1 diabetes mellitus: case report. Ann Trop Paediatr. 2008;28:297–300.
Popa G, Blag C, Sasca F. Rhinocerebral mucormycosis in a child with acute lymphoblastic leukemia: a case report. J Pediatr Hematol Oncol. 2008;30:163–5.
Margo CE, Linden C, Strickland-Marmol LB, Denietolis AL, McCaffrey JC, Kirk N. Rhinocerebral mucormycosis with perineural spread. Ophthal Plast Reconstr Surg. 2007;23:326–7.
Mohindra S, Mohindra S, Gupta R, Bakshi J, Gupta SK. Rhinocerebral mucormycosis: the disease spectrum in 27 patients. Mycoses. 2007;50:290–6.
Ferchichi L, Chadli-Debbiche A, Koubâa W, et al. Rhinocerebral mucormycosis in four diabetics. J Mal Vasc. 2006;31:85–7.
Santos Gorjón P, Blanco Pérez P, Batuecas Caletrío A, Muñoz Herrera AM, Sánchez González F, de la Cañibano R. Rhino-orbito-cerebral mucormycosis, a retrospective study of 7 cases. Acta Otorrinolaringol Esp. 2010;61:48–53.
Elinav H, Zimhony O, Cohen MJ, Marcovich AL, Benenson S. Rhinocerebral mucormycosis in patients without predisposing medical conditions: a review of the literature. Clin Microbiol Infect. 2009;15:693–7.
Turin L, Riva F, Galbiati G, Cainelli T. Fast, simple and highly sensitive double-rounded polymerase chain reaction assay to detect medically relevant fungi in dermatological specimens. Eur J Clin Invest. 2000;30:511–8.
Hall TA. Bioedit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98 NT. Nucl Acids Symp Ser. 1999;41:95–8.
Severo CB, Guazzelli LS, Severo LC. Zygomycosis. J Bras Pneumol. 2010;36:134–41.
Spellberg B, Edwars J, Ibrahim A. Novel perspectives on mucormycosis: pathophysiology, presentation, and management. Clin Microbiol Rev. 2005;18:556–69.
Roden MM, Zaoutis TE, Buchanan WL, et al. Epidemiology and outcome of zygomycosis: a review of 929 reported cases. Clin Infect Dis. 2005;41:634–53.
Eucker J, Sezer O, Graf B, Possinger K. Mucormycoses. Mycoses. 2001;44:253–60.
Koklu E, Akcakus M, Torun YA, Tulpar S, Tasdemir A. Primary gangrenous cutaneous mucormycosis of the scalp in a child: a case report. Pediatr Emerg Care. 2008;24:102–4.
Schwarz P, Bretagne S, Gantier JC, et al. Molecular identification of zygomycetes from culture and experimentally infected tissues. J Clin Microbiol. 2006;44:340–9.
Dannaoui E, Meletiadis J, Mouton JW, Meis JF, Verweij PE. In vitro susceptibilities of zygomycetes to conventional and new antifungals. J Antimicrob Chemother. 2003;51:45–52.
Yıldırım M, Yorgancılar E, Topçu İ, Meriç F. Rino-serebral mukormikozis: palatal nekroz. KBB-Forum. 2009;8:75–8.
Mosquera J, Warn PA, Rodriguez-Tudela JL, Denning DW. Treatment of Absidia corymbifera infection in mice with amphotericin B and itraconazole. J Antimicrob Chemother. 2001;48:583–6.
Mendoza-Ayala R, Tapia R, Salathe M. Spontaneously resolving pulmonary mucormycosis. Clin Infect Dis. 1999;29:1335–6.
Odds FC, Van Gerven F, Espinel-Ingroff A, et al. Evaluation of possible correlations between antifungal susceptibilities of filamentous fungi in vitro and antifungal treatment outcomes in animal infection models. Antimicrob Agents Chemother. 1998;42:282–8.
Van Burik JA, Hare RS, Solomon HF, Corrado ML, Kontoyiannis DP. Posaconazole is effective as salvage therapy in zygomycosis: a retrospective summary of 91 cases. Clin Infect Dis. 2006;42:61–5.
Hendrickson RG, Oldshaker J, Duckett O. Rhinocerebral mucormycosis: a case of a rare, but deadly disease. J Emerg Med. 1999;17:641–5.
Songu M, Unlu HH, Gunhan K, Ilker SS, Nese N. Orbital exenteration: a dilemma in mucormycosis presented with orbital apex syndrome. Am J Rhinol. 2008;22:98–103.
Dizbay M, Adisen E, Kustimur S, et al. Fungemia and cutaneous zygomycosis due to Mucor circinelloides in an intensive care unit patient: case report and review of literature. Jpn J Infect Dis. 2009;62:146–8.
Tök ÖY, Kocaoğlu FA, Acar U, Demir MN, Örnek F. Rino-orbito-serebral mukormikozis. T Oft Gaz. 2009;39:409–14.
Türkel Y, Terzi M, Yazıcı T, Cengiz N. Santral sinir sistemi tutulumu olan ve bilateral oftalmopleji kliniği ile prezente olan mukormikoz olgusu: olgu sunumu. Turk Norol Derg. 2009;15:89–93.
Koc Z, Koc F, Yerdelen D, Ozdogu H. Rhino-orbital-cerebral mucormycosis with different cerebral involvements: infarct, hemorrhage, and ophthalmoplegia. Int J Neurosci. 2007;117:1677–90.
Oktay MF, Yıldırım M. İki olgu nedeniyle mukormikozis. Dicle Tıp Derg. 2007;34:211–5.
Tuzcu A, Bahceci M, Celen MK, Kilinc N, Ozmen S. Necrotizing (malignant) otitis externa: an unusual localization of mucormycosis. Indian J Med Microbiol. 2006;24:289–91.
Aslan IK, Yazar T, Altın Ü, Kırbaş D. Rino-orbitoserebral mukormikoz. Türkiye Klinikleri J Med Sci. 2005;25:745–8.
Bilazer M, Taş E, Şahin E, et al. Rinorbital mukormikoz: olgu sunumu. Vakif Gur Egit Araşt Hast Derg. 2005;3:37–40.
Orguc S, Yücetürk AV, Demir MA, Goktan C. Rhinocerebral mucormycosis: perineural spread via the trigeminal nerve. J Clin Neurosci. 2005;12:484–6.
Tugsel Z, Sezer B, Akalin T. Facial swelling and palatal ulceration in a diabetic patient. Oral Surg Oral Med Oral Pathol Oral Radiol Endod. 2004;98:630–6.
Turhan Ö, İnan D, Saba R, Günseren F, Mamıkoglu L. Rinoserebral mukormikoz: bir olgu sunumu. ANKEM Derg. 2004;18:228–30.
Dökmetaş HS, Canbay E, Yilmaz S, et al. Diabetic ketoacidosis and rhino-orbital mucormycosis. Diabetes Res Clin Pract. 2002;57:139–42.
Cagatay AA, Oncü SS, Calangu SS, Yildirmak TT, Ozsüt HH, Eraksoy HH. Rhinocerebral mucormycosis treated with 32 gram liposomal amphotericin B and incomplete surgery: a case report. BMC Infect Dis. 2001;1:22.
Kebapci N, Efe B, Alataş F, Açikalin M, Kiraz N. Pulmonary multinodular mucormycosis in type 1 diabetic patient with diabetic ketoacidosis. J Endocrinol Invest. 2007;30:247–52.
Karakurum B, Karatas M, Cagici AC, et al. Mucormycosis presenting with painful ophthalmoplegia. Acta Neurol Belg. 2005;105:201–5.
Haliloglu NU, Yesilirmak Z, Erden A, Erden I. Rhino-orbito-cerebral mucormycosis: report of two cases and review of the literature. Dentomaxillofac Radiol. 2008;37:161–6.
Oktay MF, Askar I, Kilinç N, Tuzcu A, Topçu I. Auricular mucormycosis: a case report. Kulak Burun Bogaz Ihtis Derg. 2007;17:228–30.
Toygar O, Pelit A, Bolat F, Akova YA. Diyabetik ketoasidoz ile birlikte olmayan orbital mukormikozis olgusu. T Oft Gaz. 2007;37:51–5.
Özay S, Veyseller B, Önder F. Rino-orbito-serebral mukormikozisli iki olgunun klinik özellikleri. T Oft Gaz. 2007;37:299–304.
Coşkun H, Heper Y, Hızalan İ, Erişen L, Basut O, Akalın H. Rino-serebral mukormikozis: üç olgu sunumu. Türk Otolarengoloji Arşv. 2004;42:41–50.
Taşbakan MS, Çeviker Y, Sipahi OR, et al. Pansitopenik bir olguda rinoserebral ve akciğer mukormikozu ve aspergillozu. ANKEM Derg. 2010;24:42–5.
Erkaleli M, Alacacıoğlu İ, Payzın B, Ermete M, Arslan SL. Kraniofasiyal mukormikoz: bir olgu sunumu. Fırat Tıp Derg. 2009;14:210–2.
Başak PY, Çetin ES, Yetkin H, Akkaya B. Oral ülserlerle seyreden bir mukormikozis olgusu. Turkderm. 2009;43:70–2.
Alacacioglu I, Kargi A, Ozcan MA, et al. Fatal disseminated mucormycosis in a patient with mantle cell non-Hodgkin’s lymphoma: an autopsy case. Braz J Infect Dis. 2009;13:238–41.
Aydogdu I, Sari R, Mizrak B. Case report. Rhinocerebral zygomycosis. Mycoses. 2001;44:59–60.
Dogan MC, Leblebisatan G, Haytac MC, Antmen B, Surmegozler O. Oral mucormycosis in children with leukemia: report of 2 cases. Quintessence Int. 2007;38:515–20.
Paydas S, Yavuz S, Disel U, et al. Mucormycosis of the tongue in a patient with acute lymphoblastic leukemia: a possible relation with use of a tongue depressor. Am J Med. 2003;114:618–20.
Kandemir Ö, Görür K, Şahin E, Özcan C. Düşmez apa D: the probable role of desferrioxamine for rhinocerebral mucormycosis in a diabetic patient. ANKEM Derg. 2007;21:237–41.
Kuzdan C, Poplata B, Soysal A, Çerikçioğlu N, Bakır M. Rino-orbital-serebral mukormikoz tedavisinde posakonazol kullanımı: olgu sunumu. J Pediatr Inf. 2009;3:131–52.
Hatipoglu HG, Gurbuz MO, Yuksel E. Restricted diffusion in the optic nerve and retina demonstrated by MRI in rhino-orbital mucormycosis. J Neuroophthalmol. 2009;29:13–5.
Yetgin S, Kuşkonmaz B, Aytaç S, Çetin M. The evaluation of acquired aplastic anemia in children and unexpected frequency of varicella-zoster virus association: a single-center study. Turk J Pediatr. 2008;50:342–8.
Taşbakan MI, Arda B, Soyer NA, Sipahi OR, Kandiloğlu G, Tombuloğlu M. Aplastik anemili bir olguda mukormikoz. Ege Tıp Derg. 2007;46:57–60.
Telhan L, Erdem E, Taşdemir M, Sakız D, Arapoglu M, Palanduz A. Ölümcül seyreden mukormikoz olgusu. Cocuk Enf Derg. 2007;1:118–20.
Ergene U, Ozbalci D, Baykal B, Metin Ciris I, Yariktas M. Aplastic anemia, mucormycosis and aspergillosis in infectious mononucleosis: success is possible. Transfus Apher Sci. 2007;37:125–9.
Saşmaz I, Leblebisatan G, Antmen B, Binokay F, Tunali N, Kilinç Y. Cardiac mucormycosis in a child with severe aplastic anemia: a case report. Pediatr Hematol Oncol. 2006;23:433–7.
Atilla MH, İleri F, Köybaşıoğlu A, et al. Steroid induced rhinocerebral mucormycosis: report of a case. Gazi Med J. 2001;12:29–32.
Kantarcioglu AS, Yucel A, Nagao K, et al. Rhizopus oryzae strain isolated from resected bone and soft tissue specimens from a sinonasal and palatal mucormycosis case. Report of a case and in vitro experiments of yeastlike cell development. Med Mycol. 2006;44:515–21.
Akçay A, Altun B, Usalan C, et al. Rhinocerebral mucormycosis in a patient with membranous glomerulonephritis. Nephron. 2000;86:352–3.
Poyrazoglu H, Paydas S, Uguz A, et al. Dramatic improvement of pulmonary mucormycosis after surgery in a case without immunodeficiency. Infect Dis Clin Pract. 2006;14:403–5.
Yetkin G, Bayraktar MR, Kılıç S. Mucormycosis in a case of fever with nephrolithiasis. İnönü Üni Tıp Fak Derg. 2006;13:103–4.
Ketenci I, Unlü Y, Sentürk M, Tuncer E. Indolent mucormycosis of the sphenoid sinus. Otolaryngol Head Neck Surg. 2005;132:341–2.
Dağlı M, Akmansu H, Göçer C, Boynueğri S, Eryılmaz A. Immunolojik olarak normal bir hastada sfenoid sinüs mukormikozisi. KBB ve BBC Derg. 2001;9:48–51.
Chamilos G, Lewis RE, Kontoyiannis DP. Delaying amphotericin B-based frontline therapy significantly increases mortality among patients with hematologic malignancy who have zygomycosis. Clin Infect Dis. 2008;47:503–9.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Gumral, R., Yıldızoglu, U., Saracli, M.A. et al. A Case of Rhinoorbital Mucormycosis in a Leukemic Patient with a Literature Review from Turkey. Mycopathologia 172, 397–405 (2011). https://doi.org/10.1007/s11046-011-9449-z
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11046-011-9449-z