Case Reports
Pseudomycetoma for Microsporum canis Report of a Case Diagnosed by Fine Needle Aspiration Biopsy
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Keywords: Microsporum; aspiration biopsy, fine-needle; pseudomycetoma; Microsporum canis.
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We report a case of pseudomycetoma caused by Microsporum canis, with the diagnosis made by FNAB. This case appears to be the first one diagnosed by this method in a human. (Acta Cytol 2007;51:424–428)
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A 17-year-old male with an 8-year history of tinea capitis and multiple kerion lesions in the occipital region, left foot and right elbow resistant to conventional treatment was diagnosed by KOH tests and cultures as Microsporum canis. Two months before consultation he noticed the slow growth of a subcutaneous nodule in the base of the neck. FNAB of the neck nodule was performed. The diagnosis of pseudomycetoma by Microsporum canis was made.
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This...is the first reported case of pseudomycetoma in a human diagnosed by fine needle aspiration biopsy.
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n 1986, Slater and Reilly1 demonstrated, in 60 patients, that the main application of fine needle aspiration biopsy (FNAB) was neoplastic lesions and that it was less effective in the exact classification of lymphoproliferative lesions, in which the effectiveness was nearly 50%. Other studies reported specificity rates close to 89% in differentiating benign from malignant lesions.2 With regard to the effectiveness of FNAB in the diagnosis of mycosis, this has been reported by Das and colleagues3 to have an accuracy of 80%, including superficial and deep mycosis. The fungi diagnosed in that study were Aspergillus spp, Cryptococcus neoformans, mucoral fungi, Candida spp, Phialophora parasiticus, Sporothrix schenkii and Cladosporium spp. The clinical diagnosis had not been suspected in 70% of cases. Specifically in scalp lesions, Garcia-Rojo and colleagues4 reported a cytohistologic correlation for malignant tumors near 100%; nevertheless, they emphasized the fact that it is indispensable to have experience in skin cytopathology to obtain these results. Bhambhani and colleagues5 found that FNAB was more effective for tumorlike lesions, skin and inflammatory mucosal diseases than in scrapes of injuries in which generally only necrotic material was obtained. Other infectious processes that appear in skin as subcutaneous nodules have been diagnosed successfully by FNAB, such as leishmaniasis,6 leprosy,7 histoplasmosis,8 blastomycosis,9 tuberculosis,10 sporotrichosis11 and atypical mycobacteriosis.12 Examples of subcutaneous lesions approached by this method are amyloidosis,13 amyloid tumor,14 calcinosis cutis15,16 and gouty tophus.17-19 Dermatophytes constitute 70–80% of mycoses and 5% of dermatologic consultations.20 Endemic to Latin America, they constitute a health problem all over the world. They are almost exclusively superficial cutaneous mycosis, the diagnosis of which is usually made with direct microscopic examination and 20% KOH test alone or
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Fine needle aspiration biopsy (FNAB) of the skin is useful in subcutaneous lesions. Dermatophytes are almost exclusively superficial cutaneous mycoses and constitute 70–80% of all mycoses and 5% of dermatologic consultations. Inflammatory and invasive forms, as well as infections that remain in chronic forms or persist in spite of treatment, are more frequent in immunocompromised individuals. The clinical presentations of these invasive cases are dermatophytic granulomas (granuloma of Wilson-Majocchi and pseudomycetoma) or Hadida’s disease.
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Oralia Barboza-Quintana, M.D., F.I.A.C., Raquel Garza-Guajardo, M.D., F.I.A.C., Carlos Assad-Morel, M.D., and Nora Méndez-Olvera, M.D.
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From the Anatomic Pathology and Cytopathology Service, University Hospital “Dr. José Eleuterio González"; Universidad Autónoma de Nuevo León; and Dermassad, Monterrey, Nuevo Leon, Mexico. Dr. Barboza-Quintana is Professor and Chief of Cytopathology, Anatomic Pathology and Cytopathology Service, University Hospital “Dr. José Eleuterio González”; Universidad Autónoma de Nuevo León. Dr. Garza-Guajardo is Professor of Cytopathology, Anatomic Pathology and Cytopathology Service, University Hospital “Dr. José Eleuterio González”; Universidad Autónoma de Nuevo León. Dr. Assad-Morel is Dermatologist, Dermassad. Dr. Méndez-Olvera is Professor of Dermatopathology, Anatomic Pathology and Cytopathology Service, University Hospital “Dr. José Eleuterio González”; Universidad Autónoma de Nuevo León. Address correspondence to: Oralia Barboza-Quintana, M.D., F.I.A.C., Servicio de Anatomía Patológica y Citopatología, Sótano, Hospital Universitario “Dr. José Eleuterio González”; Universidad Autónoma de Nuevo León, Gonzalitos y Madero s/n, Colonia Mitras Centro, C.P. 64460, Monterrey, Nuevo León, México (
[email protected]). Financial Disclosure: The authors have no connection to any companies or products mentioned in this article. Received for publication June 23, 2005. Accepted for publication October 11, 2005.
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Pseudomycetoma from Microsporum canis
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with ultraviolet light. The diagnosis is made definitively by culture in agar-Sabouraud medium; the sensitivity of KOH is 89.2% and of agar-Sabouraud, 98.2%.21 In the last 2 decades the number of serious and invasive infections caused by dermatophytes has increased, principally in immunosuppressed patients, although immunocompetent patients can also be affected.22 The clinical presentations of these invasive cases are dermatophytic granulomas (granuloma of Wilson-Majocchi and pseudomycetoma) or Hadida’s disease.23-28 All the reported cases of invasive dermatophytosis have been diagnosed by routine methods, such as KOH tests, cultures and biopsies. Below we report a case of pseudomycetoma caused by Microsporum canis the diagnosis of which was made by FNAB. This was the first case diagnosed by this method in a human; since the only other case describing the cytologic diagnosis of pseudomicetoma occurred in a Persian cat.29 Case Report
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The epidermis showed hyperkeratosis, and in the stratum corneum and hair follicles numerous hyphae and arthrospores were observed. In the dermis and the subcutaneous tissue we identified granulomas with abundant multinucleated giant cells that contained empty hyphae measuring 50–100 μm in length by 10–20 μm in width. Inter-
Dermatophytes have been known since ancient times. Romans termed this condition tinea, or “moth eaten.” In the fifth century, Cassius talked about tinea of the head.30 The dermatophytes are parasite fungi of the keratin, hair and nails and belong to 3 genera: Microsporum, Trichophyton and Epidermophyton. Diverse infections of specific body regions caused by dermatophytes are recognized: tinea capitis, tinea faciei, tinea barbae, tinea corporis, tinea cruris, tinea pedis and onicomicosis.31 Tinea capitis is a disease that affects mainly children between 4 and 14 years of age.32 Although numerous pathogenic fungi can produce the disease, Trichophyton tonsurans is responsible for > 90% of cases reported in North America and Britain; for 20 years the re-
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Histopathologic Findings
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The smears showed an inflammatory background with abundant polymorphonuclear leukocytes and cellular detritus and between them many round, empty bodies, 0.5–1 μm in diameter, surrounded by clear halos that corresponded to hyphae. There also were macrophages, multinucleated giant cells and rests of proteinaceous material (Figures 2–4). Gomori-Grocott staining was positive for fungi (Figure 5). The diagnosis of pseudomycetoma from M canis was made.
mingled were large, empty spores with pear shapes, 3–5 μm in diameter (Figure 6), shrunk in amorphous, eosinophilic, periodic acid-Schiff–positive material (Figure 7). That was similar to the Splendore-Hoeppli phenomenon, and reminiscent of true micetomas. The diagnosis made was pseudomycetoma from M canis.
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Figure 2 Round, empty bodies, 0.5-1 μm in diameter, surrounded by clear halos, which corresponded to hyphae.
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A 17-year-old male had an 8-year case of tinea capitis and multiple kerion lesions in the occipital region, left foot and right elbow resistant to conventional treatment and diagnosed by KOH tests and cultures as M canis. Two months before consultation he experienced the slow growth of a subcutaneous nodule at the base of the neck (Figure 1). FNAB of the neck nodule was performed, and subsequent to the cytologic diagnosis, an incisional biopsy was performed. Immunologic tests done throughout the 8-year period were normal.
Figure 1 Patient with a subcutaneous nodule at the base of the neck.
Figure 3 Macrophages, multinucleated giant cells and rests of proteinaceous material.
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Figure 4 Inflammatory background with abundant polymorphonuclear leukocytes and cellular detritus.
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hair follicles; subsequently alopecia appears, with hair that is broken just right above the level of the hairy skin. The hair is opaque and gray because it is covered by arthrospores. The inflammatory types are diffuse and pustular, which is a pruritic, pustular folliculitis associated with lymphadenopathy and fever; 2–3% can have humid nodules with broken hair and purulent material. Later, cicatricial alopecia (kerion) develops. Another form is called the “black point,” and a variety of infections by endothrix occur in which hair becomes fragile at the hairy skin level; the rest of the infected follicles look like black points.34,41 There exist more invasive forms, such as dermatophytic granuloma, (granuloma of Wilson-Majocchi and pseudomycetoma) and Hadida’s disease.23-28 Inflammatory and invasive forms, as well as infections that remain in chronic forms or persist in spite of treatment, are more frequent in immunocompromised individuals.42 Pseudomycetoma, the morphology of which has been described, has been reported mainly in transplant patients and those with autoimmune disease, although they have also been seen in exceptional cases in immunocompetent patients.43-45 Dermatophytes are 1 of the 10 top reasons for dermatologic con-
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sponsible fungus was M canis due to exposure to contaminated cats and dogs. The reason for this change in pathogen is not clear.33 Urban cases are acquired through epidemics in schools or between members of a family; in addition, poor hygiene and malnourishment are contributing factors.34 Simple contact of the fungi with the skin and adnexa can produce the disease, although a genetic or immunologic predisposition has been suggested. In Mexico, 86% of dermatophytes are caused by Tinea rubrum, which produces onychomycosis in 37% and tinea of the feet in 25–30%.35-37 Living in humid and tropical places, diabetes, poor hygiene, use of closed shoes, synthetic clothes and not drying the skin adequately37 predispose to the infection. Topical steroid abuse can predispose to infection by dermatophytes.38,39 The clinical appearance is greatly variable and depends on numerous factors, including the type of fungal species, site of infection, immunologic state of the patient and previous use of steroids. Clinically, infections by dermatophytes can be noninflammatory and inflammatory types.34,40 The noninflammatory ones produce diffuse desquamation and erythematous, grayish papules around
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Figure 6 Granulomas with multinucleated giant cells that contain empty hyphae.
Figure 5 Gomori-Grocott stain positive for fungi.
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Figure 7 Periodic acid–Schiff-positive material.
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cutaneous sporotrichosis: A case report. Diagn Cytopathol 1999;20:74– 77 12. Thompson KS, Donzelli J, Jensen J, Pachucki C, Eng AM, Reyes CV: Breast and cutaneous mycobacteriosis: Diagnosis by fine-needle aspiration biopsy. Diagn Cytopathol 1997;17:45–49 13. Klemi PJ, Sorsa S, Happonen RP: Fine-needle aspiration biopsy from subcutaneous fat: An easy way to diagnose secondary amyloidosis. Scand J Rheumatol 1987;16:429–431 14. Sahoo S, Reeves W, DeMay RM: Amyloid tumor: A clinical and cytomorphologic study. Diagn Cytopathol 2003;28:325–328
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15. Deshpande A, Munshi M: Calcinosis cutis: Diagnosis by aspiration cytology: A case report. Diagn Cytopathol 1999;21:200–202 16. Reed MA, de Luna AM, Holaysan JS, Gerardo LT: Calcinosis cutis in chronic renal failure diagnosed by fine needle aspiration: A case report. Acta Cytol 2002;46:738–740
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17. Nicol KK, Ward WG, Pike EJ, Geisinger KR, Cappellari JO, Kilpatrick SE: Fine-needle aspiration biopsy of gouty tophi: Lessons in cost-effective patient management. Diagn Cytopathol 1997;17:30–35
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18. Liu K, Moffatt EJ, Hudson ER, Layfield LJ: Gouty tophus presenting as a soft-tissue mass diagnosed by fine-needle aspiration: A case report. Diagn Cytopathol 1996;15:246–249 19. Paik SS, Park MH: Fine needle aspiration cytology of gouty tophus in a patient with rheumatoid arthritis. Acta Cytol 2002;46:1024–1025
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20. King D, Hood WCH, Horn TD, Rinaldi MG, Merz1 WG: Primary invasive cutaneous Microsporum canis infections in immunocompromised patients. J Clin Microbiol 1996;34:460–462
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22. Arenas R: Dermatophytoses in Mexico. Rev Iberoam Micol 2002;19: 63–67 23. Erbagci Z: Mycopathologia: Deep dermatophytoses in association with atrophy and diabetes mellitus: Majocchi’s granuloma tricophyticum or dermatophytic pseudomycetoma? Mycopathologia 2002;154:163–169
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2. Dey P, Das A, Radhika S, Nijhawan R: Cytology of primary skin tumors. Acta Cytol 1996;40:708–713
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25. Zaror L, Moreno MI, Hering M, Siegmund I, Norambuena L: Mycetomas caused by Microsporum canis: Report of one case. Rev Med Chil 1997;125:922–626 26. West BC, Kwon-Chung KJ: Mycetoma caused by Microsporum audouinii: First reported case. Am J Clin Pathol 1980;73:447–454
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1. Slater DN, Reilly G: Fine needle aspiration cytology in dermatology: A clinicopathological appraisal. Br J Dermatol 1986;115:317–327
24. Akiba H, Motoki Y, Satoh M, Iwatsuki K, Kaneko F: Recalcitrant trichophytic granuloma associated with NK-cell deficiency in a SLE patient treated with corticosteroid. Eur J Dermatol 2001;11:58–62
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References
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sultation. As much as their ecology and epidemiology have changed over the last 20 years, their persistence can be attributed to the constant migration of populations and hygiene habits.34,46 Tinea capitis constitutes a worldwide problem because of its high frequency and easy transmission.47 The most frequent causal agents are T tonsurans and M canis, with worldwide distribution.33,46,48 Clinically the dermatophyte appears as a pseudoalopecic plate with a scale on its surface from which hairs approximately 5 mm long grow. The dermatophyte’s inflammatory forms as granulomas or pseudomycetomas had been reported mainly in immunocompromised patients, related to the physiopathology of the infection. Dermatophytes affect the corneal layer and generally do not invade underlying layers because the immune system uses several mechanisms to eliminate the fungus, including specific T-cell immunity and other nonspecific mechanisms. The adaptive response is preceded by innate immunity from circulating neutrophils, natural killer cells and proteins as antimicrobial peptides and components of the complement. In patients with localized or systemic immune defects, the development of invasive lesions can occur.24 In pseudomycetomas on very rare occasions the fungi organize in loose or compact aggregates of variable size that simulate eumycetes grains embedded in an amorphous periodic acid–Schiff-positive substance, resembling Splendore-Hoeppli material. The microscopic image is not dependent on the type of dermatophyte that causes it, but most reported cases have been caused by M canis.43-45 Unlike in human beings, in Persian cats this lesion is very common, and probably a hereditary factor in the development of these injuries exists.29 Tinea capitis must be treated with oral agents, such as grisofulvine and ketoconazole. In addition, other drugs can be used: terbinafine, itraconazole and fuconazole.49,50 The significance of this case resides in the fact that the pseudomycetoma caused by M canis developed in an immunocompetent child and that it is the first reported case of pseudomycetoma in a human diagnosed by fine needle aspiration biopsy.
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4. Garcia-Rojo B, Garcia-Solano J, Sanchez-Sanchez C, MontalbanRomero S, Martinez-Parra D, Perez-Guillermo M: On the utility of fineneedle aspiration in the diagnosis of primary scalp lesions. Diagn Cytopathol 2001;24:104–111
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27. Moraes MA, Machado AA, Medeiros, Filho P, Reis CM: Dermatophytic pseudomycetoma: Report of a case caused by Trichophyton tonsurans. Rev Soc Bras Med Trop 2001;34:291–294 28. Botterel F, Romand S, Cornet M, Recanati G, Dupont B, Bouree P: Dermatophyte pseudomycetoma of the scalp: Case report and review. Br J Dermatol 2001;145:151–153 29. Zimmerman K, Feldman B, Robertson J, Herring ES, Manning T: Dermal mass aspirate from a Persian cat. Vet Clin Pathol 2003;32:213–217 30. Arenas GR: Dermatofitosis. In Micología. Second edition. Mexico City, McGraw Hill, 2003, pp 61–83 31. Weedon D: Mycoses and algal inections.Dermatofitosis. In Skin Pathology. Second edition. London, Churchill Livingstone, 2000, pp 659–666 32. Bronson DM, Desai DR, Barsky S, Foley SM: An epidemic of infection with Trichophyton tonsurans revealed in a 20-year survey of fungal infections in Chicago. J Am Acad Dermatol 1983;8:322–330 33. Seebacher C: The change of dermatophyte spectrum in dermatomycoses Mycoses (suppl 1) 2003;46:42–46 34. Elewski BE: Tinea capitis: A current perspective. J Am Acad Dermatol 2000;42:1–20, quiz 21–24
9. Mamikunian C, Gatti WM, Reyes CV: Subcutaneous blastomycosis: Diagnosis by fine-needle aspiration cytology. Otolaryngol Head Neck Surg 1989;101:607–610
35. Martin AG, Kobayashi GS: Fungal diseases with cutaneous involvement. In Dermatology in General Medicine. Second volume. Edited by TB Fitzpatrick. New York, McGraw-Hill, 1993, pp 2421–2451
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37. Ruiz-Esmenjaud J, Arenas R, Rodriguez-Alvarez M, Monroy E, Felipe Fernandez R: Tinea pedis and Onychomycosis in children of the Mazahua Indian community in Mexico. Gac Med Mex 2003;139:215–220
Dermatophytic granuloma caused by Microsporum canis in a heart-lung recipient. Dermatology 1999;198:317–319 45. Barson WJ: Granuloma and pseudogranuloma of the skin due to Microsporum canis: Successful management with local injections of miconazole. Arch Dermatol 1985;121:895–897
38. Bicer A, Tursen U, Cimen OB, Kaya TI, Ozisik S, Ikizoglu G, Erdogan C: Prevalence of dermatophytosis in patients with rheumatoid arthritis. Rheumatol Int 2003;23:37–40
46. Aly R: Ecology and epidemiology of dermatophyte infections. J Am Acad Dermatol 1994;31:S21–S25
39. Alston SJ, Cohen BA, Braun M: Persistent and recurrent tinea corporis in children treated with combination antifungal/corticosteroid agents. Pediatrics 2003;111:201–203
47. Ceburkovas O, Schwartz RA, Janniger CK: Tinea capitis: Current concepts. J Dermatol 2000;27:144–148 48. Fernandez NC, Akiti T, Barreiros MGC: Dermatophytoses in children: Study of 137 cases. Rev Inst Med Trop S Paulo 2001;43:83–85
41. Aste N, Pau M, Biggio P: Kerion celsi: A clinical epidemiological study. Mycoses 1998;41:169–173
49. Drake LA, Dinehart SM, Farmer ER, Goltz RW, Graham GF, Hordinsky MK, Lewis CW, Pariser DM, Skouge JW: Guidelines of care for superficial mycotic infections of the skin: Tinea capitis and tinea barbae: Guidelines/Outcomes Committee, American Academy of Dermatology. J Am Acad Dermatol 1996;34:290–294
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42. Nir-Paz R, Elinav H, Pierard GE, Walker D, Maly A, Shapiro M, Barton RC, Polacheck I: Deep infection by Trichophyton rubrum in an immunocompromised patient. J Clin Microbiol 2003;41:5298–5301 43. Fernandez-Torres B, Mayayo E, Boronat J, Guarro J: Subcutaneous infection by Microsporum gypseum. Br J Dermatol 2002;146:311–313
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