Ann Lab Med.  2012 Sep;32(5):375-379. 10.3343/alm.2012.32.5.375.

Molecular Identification of Schizophyllum commune as a Cause of Allergic Fungal Sinusitis

• Won EJ
• Shin JH
• Lim SC
• Shin MG
• Suh SP
• Ryang DW

• KMID: 1387355
• DOI: http://doi.org/10.3343/alm.2012.32.5.375

Abstract

Schizophyllum commune, a basidiomycetous fungus, rarely causes disease in humans. We report a rare case of allergic fungal sinusitis caused by S. commune in a 14-yr-old girl. The patient presented with nasal obstruction and a purulent nasal discharge. Materials obtained during endoscopic surgery of the frontal recess revealed allergic mucin and a few fungal hyphae. A potato dextrose agar (PDA) culture from the allergic mucin yielded a rapidly growing white woolly mold. Although no distinctive features including hyphae bearing spicules or a clamp connection were present, the case isolate disclosed compatible mycological features including growth at 37degrees C, susceptibility to cycloheximide, and production of a tart and disagreeable smell. S. commune was confirmed by sequence analysis of the internal transcribed spacer region and D1/D2 regions of the 26S ribosomal DNA. We believe this is the first report of allergic fungal sinusitis caused by S. commune in Korea. Moreover, this report highlights the value of gene sequencing as an identification tool for non-sporulating isolates of S. commune.

Keyword

Schizophyllum commune; Sinusitis; Sequencing

MeSH Terms

Adolescent
Antifungal Agents/pharmacology
Cycloheximide/pharmacology
DNA, Ribosomal/chemistry/genetics
Female
Humans
Hypersensitivity/*diagnosis
Schizophyllum/drug effects/genetics/*isolation & purification
Sequence Analysis, DNA
Sinusitis/*diagnosis/microbiology
Tomography, X-Ray Computed

Figure

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  Fig. 1 Diagnosis of allergic fungal sinusitis in the patient. (A) A non-enhanced computed tomography scan of the ostiomeatal unit (coronal view) reveals soft-tissue opacification in the right frontal, ethmoid, and maxillary sinuses. Arrow indicates allergic mucin, which filled the sinuses. (B) Staining of the allergic mucin with methenamine silver shows a few scattered fungal hyphae within the allergic mucin (methenamine silver stain,×400).

• 

  Fig. 2 Macroscopic and microscopic appearance of the isolates. (A) Rapid growing, white and densely woolly fungus with a yellow-brown reverse. (B) Microscopic examination of the mold shows hyaline, septate, branched hyphae of 2 widths. Arrow (→) indicates wider hyphae and arrowhead (▴) indicates the narrower width hyphae. No evidence of clamp connections or spicules is found (lacto-phenol cotton blue stain, ×400).

Reference

1. Deanna AS, Mary EB. James V, editor. Fusarium and other opportunistic hyaline fungi. Manual of Clinical Microbiology. 2011. 10th ed. Washington, DC: ASM press;1866.

2. Buzina W, Lang-Loidolt D, Braun H, Freudenschuss K, Stammberger H. Development of molecular methods for identification of Schizophyllum commune from clinical samples. J Clin Microbiol. 2001. 39:2391–2396.

3. Amitani R, Nishimura K, Niimi A, Kobayashi H, Nawada R, Murayama T, et al. Bronchial mucoid impaction due to the monokaryotic mycelium of Schizophyllum commune. Clin Infect Dis. 1996. 22:146–148.

4. Kamei K, Unno H, Nagao K, Kuriyama T, Nishimura K, Miyaji M. Allergic bronchopulmonary mycosis caused by the basidiomycetous fungus Schizophyllum commune. Clin Infect Dis. 1994. 18:305–309.

5. Ogawa H, Fujimura M, Takeuchi Y, Makimura K. Two cases of Schizophyllum asthma: is this a new clinical entity or a precursor of ABPM? Pulm Pharmacol Ther. 2011. 24:559–562.

6. Clark S, Campbell CK, Sandison A, Choa DI. Schizophyllum commune: an unusual isolate from a patient with allergic fungal sinusitis. J Infect. 1996. 32:147–150.

7. Sigler L, de la Maza LM, Tan G, Egger KN, Sherburne RK. Diagnostic difficulties caused by a nonclamped Schizophyllum commune isolate in a case of fungus ball of the lung. J Clin Microbiol. 1995. 33:1979–1983.

8. Bulajic N, Cvijanovic V, Vukojevic J, Tomic D, Johnson E. Schizophyllum commune associated with bronchogenous cyst. Mycoses. 2006. 49:343–345.

9. Kim MN, Shin JH, Sung H, Lee K, Kim EC, Ryoo N, et al. Candida haemulonii and closely related species at 5 university hospitals in Korea: identification, antifungal susceptibility, and clinical features. Clin Infect Dis. 2009. 48:e57–e61.

10. Schubert MS. Allergic fungal sinusitis. Clin Rev Allergy Immunol. 2006. 30:205–216.

11. Bent JP 3rd, Kuhn FA. Diagnosis of allergic fungal sinusitis. Otolaryngol Head Neck Surg. 1994. 111:580–588.

12. Ponikau JU, Sherris DA, Kern EB, Homburger HA, Frigas E, Gaffey TA, et al. The diagnosis and incidence of allergic fungal sinusitis. Mayo Clin Proc. 1999. 74:877–884.

13. Montone KT, Livolsi VA, Feldman MD, Palmer J, Chiu AG, Lanza DC, et al. Fungal rhinosinusitis: a retrospective microbiologic and pathologic review of 400 patients at a single university medical center. Int J Otolaryngol. 2012. in press.

14. Baron O, Cassaing S, Percodani J, Berry A, Linas MD, Fabre R, et al. Nucleotide sequencing for diagnosis of sinusal infection by Schizophyllum commune, an uncommon pathogenic fungus. J Clin Microbiol. 2006. 44:3042–3043.

15. Catalano P, Lawson W, Bottone E, Lebenger J. Basidiomycetous (mushroom) infection of the maxillary sinus. Otolaryngol Head Neck Surg. 1990. 102:183–185.

16. Rosenthal J, Katz R, DuBois DB, Morrissey A, Machicao A. Chronic maxillary sinusitis associated with the mushroom Schizophyllum commune in a patient with AIDS. Clin Infect Dis. 1992. 14:46–48.

17. Marlier S, De Jaureguiberry JP, Aguilon P, Carloz E, Duval JL, Jaubert D. Chronic sinusitis caused by Schizophyllum commune in AIDS. Presse Med. 1993. 22:1107.

18. Sigler L, Estrada S, Montealegre NA, Jaramillo E, Arango M, De Bedout C, et al. Maxillary sinusitis caused by Schizophyllum commune and experience with treatment. J Med Vet Mycol. 1997. 35:365–370.

19. Sigler L, Bartley JR, Parr DH, Morris AJ. Maxillary sinusitis caused by medusoid form of Schizophyllum commune. J Clin Microbiol. 1999. 37:3395–3398.

20. Ahmed MK, Ishino T, Takeno S, Hirakawa K. Bilateral allergic fungal rhinosinusitis caused by Schizophyllum commune and Aspergillus niger. A case report. Rhinology. 2009. 47:217–221.

21. Perić A, Vojvodić D, Zolotarevski L, Perić A. Nasal polyposis and fungal Schizophyllum commune infection: a case report. Acta Medica (Hradec Kralove). 2011. 54:83–86.

22. Swain B, Panigrahy R, Panigrahi D. Schizophyllum commune sinusitis in an immunocompetent host. Indian J Med Microbiol. 2011. 29:439–442.

23. Lorentz C, Rivier A, Debourgogne A, Sokolowska-Gillois J, Vignaud JM, Jankowski R, et al. Ethmoido-maxillary sinusitis caused by the basidiomycetous fungus Schizophyllum commune. Mycoses. 2012. 55:e8–e12.

24. Mabry RL, Marple BF, Folker RJ, Mabry CS. Immunotherapy for allergic fungal sinusitis: three years' experience. Otolaryngol Head Neck Surg. 1998. 119:648–651.

25. Chowdhary A, Randhawa HS, Gaur SN, Agarwal K, Kathuria S, Roy P, et al. Schizophyllum commune as an emerging fungal pathogen: a review and report of two cases. Mycoses. 2012. in press.

26. Balajee SA, Sigler L, Brandt ME. DNA and the classical way: identification of medically important molds in the 21st century. Med Mycol. 2007. 45:475–490.

27. Premamalini T, Ambujavalli BT, Anitha S, Somu L, Kindo AJ. Schizophyllum commune a causative agent of fungal sinusitis: a case report. Case Rep Infect Dis. 2011. 2011:821259.

28. Kim YH, Kim KS. Diagnosis and treatment of allergic rhinitis. J Korean Med Assoc. 2010. 53:780–790.

29. Jang YJ, Kim JS. Non-surgical management of fungal sinusitis. J Rhinol. 2007. 14:76–81.