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A Case of Rhinoorbital Mucormycosis in a Leukemic Patient with a Literature Review from Turkey

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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.

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References

  1. Kwon-Chung KJ, Bennett JE. Medical mycology. Philadelphia: Lea & Febiger; 1992. p. 524–59.

    Google Scholar 

  2. Ribes JA, Vanover-Sams CL, Baker DJ. Zygomycetes in human disease. Clin Microbiol Rev. 2000;13:236–301.

    Article  PubMed  CAS  Google Scholar 

  3. Romano C, Miracco C, Massai L, et al. Case report. Fatal rhinocerebral zygomycosis due to Rhizopus oryzae. Mycoses. 2002;45:45–9.

    Article  PubMed  CAS  Google Scholar 

  4. 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.

    Google Scholar 

  5. 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.

    Google Scholar 

  6. Chayakulkeeree M, Ghannoum MA, Perfect JR. Zygomycosis: the re-emerging fungal infection. Eur J Clin Microbiol Infect Dis. 2006;25:215–29.

    Article  PubMed  CAS  Google Scholar 

  7. Ferguson BJ. Mucormycosis of the nose and paranasal sinuses. Otolaryngol Clin North Am. 2000;33:349–65.

    Article  PubMed  CAS  Google Scholar 

  8. 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.

    Article  Google Scholar 

  9. Nosari A, Oreste P, Montillo M, et al. Mucormycosis in hematologic malignancies: an emerging fungal infection. Haematologica. 2000;85:1068–71.

    PubMed  CAS  Google Scholar 

  10. Yohai RA, Bullock JD, Aziz AA, Markert RJ. Survival factors in rhino-orbital-cerebral mucormycosis. Surv Ophthalmol. 1994;39:3–22.

    Article  PubMed  CAS  Google Scholar 

  11. Baker RD. Mucormycosis. A new disease? JAMA. 1957;163:805–8.

    CAS  Google Scholar 

  12. 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.

    Article  PubMed  CAS  Google Scholar 

  13. 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.

    Article  PubMed  Google Scholar 

  14. 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.

    PubMed  Google Scholar 

  15. 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.

    Article  PubMed  CAS  Google Scholar 

  16. 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.

    Google Scholar 

  17. Liang KP, Tlevjeh IM, Wilson WR, Roberts GD, Temesgen Z. Rhino-orbitocerebral mucormycosis caused by Apophysomyces elegans. J Clin Microbiol. 2006;44:892–8.

    Article  PubMed  Google Scholar 

  18. 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.

    Article  PubMed  CAS  Google Scholar 

  19. Ibrahim M, Chitnis S, Fallon K, Roberts T. Rhinocerebral mucormycosis in a 12-year-old girl. Arch Neurol. 2009;66:272–3.

    Article  PubMed  Google Scholar 

  20. 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.

    Article  PubMed  CAS  Google Scholar 

  21. 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.

    Article  PubMed  Google Scholar 

  22. 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.

    Article  PubMed  Google Scholar 

  23. Mohindra S, Mohindra S, Gupta R, Bakshi J, Gupta SK. Rhinocerebral mucormycosis: the disease spectrum in 27 patients. Mycoses. 2007;50:290–6.

    Article  PubMed  Google Scholar 

  24. Ferchichi L, Chadli-Debbiche A, Koubâa W, et al. Rhinocerebral mucormycosis in four diabetics. J Mal Vasc. 2006;31:85–7.

    Article  PubMed  CAS  Google Scholar 

  25. 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.

    Article  PubMed  Google Scholar 

  26. 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.

    Article  PubMed  CAS  Google Scholar 

  27. 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.

    Article  PubMed  CAS  Google Scholar 

  28. 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.

    CAS  Google Scholar 

  29. Severo CB, Guazzelli LS, Severo LC. Zygomycosis. J Bras Pneumol. 2010;36:134–41.

    Article  PubMed  Google Scholar 

  30. Spellberg B, Edwars J, Ibrahim A. Novel perspectives on mucormycosis: pathophysiology, presentation, and management. Clin Microbiol Rev. 2005;18:556–69.

    Article  PubMed  CAS  Google Scholar 

  31. 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.

    Article  PubMed  Google Scholar 

  32. Eucker J, Sezer O, Graf B, Possinger K. Mucormycoses. Mycoses. 2001;44:253–60.

    Article  PubMed  CAS  Google Scholar 

  33. 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.

    Article  PubMed  Google Scholar 

  34. 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.

    Article  PubMed  CAS  Google Scholar 

  35. 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.

    Article  PubMed  CAS  Google Scholar 

  36. Yıldırım M, Yorgancılar E, Topçu İ, Meriç F. Rino-serebral mukormikozis: palatal nekroz. KBB-Forum. 2009;8:75–8.

    Google Scholar 

  37. 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.

    Article  PubMed  CAS  Google Scholar 

  38. Mendoza-Ayala R, Tapia R, Salathe M. Spontaneously resolving pulmonary mucormycosis. Clin Infect Dis. 1999;29:1335–6.

    Article  PubMed  CAS  Google Scholar 

  39. 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.

    PubMed  CAS  Google Scholar 

  40. 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.

    Article  Google Scholar 

  41. Hendrickson RG, Oldshaker J, Duckett O. Rhinocerebral mucormycosis: a case of a rare, but deadly disease. J Emerg Med. 1999;17:641–5.

    Article  PubMed  CAS  Google Scholar 

  42. 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.

    Article  PubMed  Google Scholar 

  43. 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.

    PubMed  Google Scholar 

  44. Tök ÖY, Kocaoğlu FA, Acar U, Demir MN, Örnek F. Rino-orbito-serebral mukormikozis. T Oft Gaz. 2009;39:409–14.

    Google Scholar 

  45. 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.

    Google Scholar 

  46. 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.

    Article  PubMed  Google Scholar 

  47. Oktay MF, Yıldırım M. İki olgu nedeniyle mukormikozis. Dicle Tıp Derg. 2007;34:211–5.

    Google Scholar 

  48. 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.

    Article  PubMed  CAS  Google Scholar 

  49. Aslan IK, Yazar T, Altın Ü, Kırbaş D. Rino-orbitoserebral mukormikoz. Türkiye Klinikleri J Med Sci. 2005;25:745–8.

    Google Scholar 

  50. Bilazer M, Taş E, Şahin E, et al. Rinorbital mukormikoz: olgu sunumu. Vakif Gur Egit Araşt Hast Derg. 2005;3:37–40.

    Google Scholar 

  51. Orguc S, Yücetürk AV, Demir MA, Goktan C. Rhinocerebral mucormycosis: perineural spread via the trigeminal nerve. J Clin Neurosci. 2005;12:484–6.

    Article  PubMed  Google Scholar 

  52. 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.

    Article  PubMed  Google Scholar 

  53. Turhan Ö, İnan D, Saba R, Günseren F, Mamıkoglu L. Rinoserebral mukormikoz: bir olgu sunumu. ANKEM Derg. 2004;18:228–30.

    Google Scholar 

  54. Dökmetaş HS, Canbay E, Yilmaz S, et al. Diabetic ketoacidosis and rhino-orbital mucormycosis. Diabetes Res Clin Pract. 2002;57:139–42.

    Article  PubMed  Google Scholar 

  55. 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.

    Article  PubMed  CAS  Google Scholar 

  56. 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.

    PubMed  CAS  Google Scholar 

  57. Karakurum B, Karatas M, Cagici AC, et al. Mucormycosis presenting with painful ophthalmoplegia. Acta Neurol Belg. 2005;105:201–5.

    PubMed  CAS  Google Scholar 

  58. 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.

    Article  PubMed  CAS  Google Scholar 

  59. Oktay MF, Askar I, Kilinç N, Tuzcu A, Topçu I. Auricular mucormycosis: a case report. Kulak Burun Bogaz Ihtis Derg. 2007;17:228–30.

    PubMed  Google Scholar 

  60. Toygar O, Pelit A, Bolat F, Akova YA. Diyabetik ketoasidoz ile birlikte olmayan orbital mukormikozis olgusu. T Oft Gaz. 2007;37:51–5.

    Google Scholar 

  61. Özay S, Veyseller B, Önder F. Rino-orbito-serebral mukormikozisli iki olgunun klinik özellikleri. T Oft Gaz. 2007;37:299–304.

    Google Scholar 

  62. 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.

    Google Scholar 

  63. Taşbakan MS, Çeviker Y, Sipahi OR, et al. Pansitopenik bir olguda rinoserebral ve akciğer mukormikozu ve aspergillozu. ANKEM Derg. 2010;24:42–5.

    Google Scholar 

  64. Erkaleli M, Alacacıoğlu İ, Payzın B, Ermete M, Arslan SL. Kraniofasiyal mukormikoz: bir olgu sunumu. Fırat Tıp Derg. 2009;14:210–2.

    Google Scholar 

  65. Başak PY, Çetin ES, Yetkin H, Akkaya B. Oral ülserlerle seyreden bir mukormikozis olgusu. Turkderm. 2009;43:70–2.

    Google Scholar 

  66. 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.

    Article  PubMed  Google Scholar 

  67. Aydogdu I, Sari R, Mizrak B. Case report. Rhinocerebral zygomycosis. Mycoses. 2001;44:59–60.

    Article  PubMed  CAS  Google Scholar 

  68. 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.

    PubMed  Google Scholar 

  69. 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.

    Article  PubMed  Google Scholar 

  70. 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.

    Google Scholar 

  71. 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.

    Google Scholar 

  72. 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.

    PubMed  Google Scholar 

  73. 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.

    PubMed  Google Scholar 

  74. Taşbakan MI, Arda B, Soyer NA, Sipahi OR, Kandiloğlu G, Tombuloğlu M. Aplastik anemili bir olguda mukormikoz. Ege Tıp Derg. 2007;46:57–60.

    Google Scholar 

  75. Telhan L, Erdem E, Taşdemir M, Sakız D, Arapoglu M, Palanduz A. Ölümcül seyreden mukormikoz olgusu. Cocuk Enf Derg. 2007;1:118–20.

    Google Scholar 

  76. 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.

    Article  PubMed  Google Scholar 

  77. 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.

    Article  PubMed  Google Scholar 

  78. Atilla MH, İleri F, Köybaşıoğlu A, et al. Steroid induced rhinocerebral mucormycosis: report of a case. Gazi Med J. 2001;12:29–32.

    Google Scholar 

  79. 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.

    Article  PubMed  Google Scholar 

  80. Akçay A, Altun B, Usalan C, et al. Rhinocerebral mucormycosis in a patient with membranous glomerulonephritis. Nephron. 2000;86:352–3.

    Article  PubMed  Google Scholar 

  81. 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.

    Article  Google Scholar 

  82. Yetkin G, Bayraktar MR, Kılıç S. Mucormycosis in a case of fever with nephrolithiasis. İnönü Üni Tıp Fak Derg. 2006;13:103–4.

    Google Scholar 

  83. Ketenci I, Unlü Y, Sentürk M, Tuncer E. Indolent mucormycosis of the sphenoid sinus. Otolaryngol Head Neck Surg. 2005;132:341–2.

    Article  PubMed  Google Scholar 

  84. 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.

    Google Scholar 

  85. 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.

    Article  PubMed  Google Scholar 

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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

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