I
MYCOSES
ACCEPTED: JULY 3, 1990
34, 125-128 (1991)
Candida cXerrii: clinical and microbiological features of an emerging pathogen
Candida ciferrii: Klinische und mikrobiologische Charakteristika eines Erregers zunehmender Bedeutung L. de Gentile, J. P. Bouchara, B. Cimon and D. Chabasse Key words. Candida ciferrii, onychomycosis. Schliisselworter. Candida ufirrii, Onychomykose.
Summary. The authors report six cases of toenail onyxis due to an unusual yeast species,Candida cifirrii. For half of these cases, direct microscopical examination showed the presence of blastospores and pseudo-to-true mycelium, demonstrating the parasitic transition of the fungus. In light of the literature and of their own experience, the authors suggest that C.ciferriicould be an etiological agent of onychomycosis, particularly for elderly patients with extensive trophic disorders. Zusammenfassung. Die Autoren berichten uber sechs Falle von FuBnagel-Onychomykose durch eine ungewohnliche Hefeart, Candida cifirrii. In drei dieser Falle zeigten sich Blastosporen und Obergange von Pseudomyzel zu echtem Myzel als Ausdruck parasitarer Aktivitat des Pilzes. Unter Beriicksichtigung der Literatur und eigener Erfahrungen vermuten die Autoren, daB C.cifirrii als atiologisches Agens fur Onychomykosen insbesondere bei alteren Menschen mit umfassenden trophischen Storungen in Frage kommt.
Introduction During the past decade, the incidence of yeast infections in humans has increased dramatically, probably in relation with the development of immunosuppressive therapy, and to a lesser extent with the improvement of diagnostic and identification methods. Similarly, apart from species usually encountered in human mycology such as Candida albicans, C. tropicalis and C. parapsilosis, or Candida (Torulopsis) glabra ta and Cryptococcus neoformans, other species are increasingly being noted as pathogens: for example C.guilliermondii [l], C.pulcherrima [2], Hansenula anomala [3] or Trichosporon beigelii [4]. Likewise, species of the genera Saccharomyces, Rhodotorula or Malassezia (Pityrosporum) have been described as etiological agents of mycoses in cancer patients [5]. Here, we report six cases of tinea pedis or onychomycosis due to C. cifirrii. For three of them, direct examination revealed numerous blastospores associated with hyphae, demonstrating the pathogenic potential of this unusual yeast. Moreover, this paper outlines the circumstances associated with the development of the infection.
Material and methods Laboratoire de Parasitologie - Mycologie, CHRU, Angers, France. Correspondence: Dr Ludovic de Gentile, Laboratoire de Parasitologie, CHRU, 4, rue Larrey, F-49033 Angers Cedex, France.
All clinical specimens were examined using a Leitz phase-contrast microscope after mounting in chloral lactophenol. Mycological cultures were also performed on Sabouraud dextrose agar (SDA) containing 0.5 mg ml-' choramphenicol and supplemented or not with 0.5 mg ml-' cycloheximide (Sig-
126
L.
DE
GENTILE ET
AL.
ma). Agar plates were incubated at 22" or 37"C, respectively. The yeasts were identified using standard biochemical tests: carbohydrate assimilation and fermentation as well as the assimilation of potassium nitrate were studied according to the methods described by van der Walt & Yarrow [6];identification of the last isolate was also realized with a microcupule carbohydrate assimilation system (ATB 32 C; API System). Susceptibility studies performed by two different commercially available diffusion methods (Eurobio and Diagnostics Pasteur) and resistance to 5-fluorocytosine (5FC) was confirmed by the determination of minimum inhibitory concentration (MIC) using the API 10 M - 5FC (API System). Diagnostics were confirmed, for yeasts by the Centraalbureau voor Schimmelcultures (CBS) at Delft (Netherlands) and for filamentous fungi, by the mycology unit of the Institut Pasteur of Paris.
Case 6. Since 1970, a 75-year-old man with a noninsulin-dependent diabetes mellitus and a rheumatismal valvulopathy consulted bimonthly for ulcerous lesions of the legs. On mid-November 1989, this patient was examined in our laboratory for an extensive and bilateral tinea pedis accompanied by toe-nail onyxis and tinea cruris. The skin was erythematous and chapped; the nails were distorted, discolored and friable. Direct examination of all samples of tinea pedis and onyxis showed numerous blastospores with pseudohyphae and true hyphae. Cultures of these materials yielded profuse growth of yeast-like colonies which were identified as C. cifirrii, associated with colonies of Aspergillus sydowi. In contrast, mycological examination of the scales scraped in the lesions of the crural and submammary folds were negative. In the absence of treatment, lesions persisted and the patient was again examined on mid-February 1990. At this time, results of direct examination and cultures of new samples were similar to those previously observed.
Case reports
Cases 1 and 2. Yeasts isolated from toe-nail onyxis (age: 52 and 69 years) were identified as C. cifirrii. No other etiological agent was isolated. Moreover, direct microscopical examination of the nail samples in case 1 revealed numerous blastospores and pseudohyphae.
Results Direct microscopical examination of the skin scales or nail fragments showed, for three of the reported
Case 3. An 88-year-old man was admitted to hospital for extensive cutaneous ulceration of the legs due to a vascular disease, probably in relation with an auricular fibrillation. He presented extensive ingrowing toe-nails. Mycological cultures of the nail fragments isolated C. ciferrii. Case 4. An alcoholic and tabagic 70-year-old man was admitted to hospital in April 1978. Because of a severe bilateral arteriopathy of the pelvic limbs, his second left toe was amputated four months before. Clinical examination revealed a venous insufficiency with large perforatic ulcers and an onychopathy. A white powdery material was observed under the distorted nails. Direct examination of this material showed numerous blastospores and hyphae. Yeasts isolated from the clinical specimens were identified as C. ciferrii. Case 5. A 84-year-old farmer, treated one year before for cardiac arrythmia, was admitted to hospital for various dermatologic problems. The patient presented a numular eczematosis on the legs associated with trophic disorders which rapidly disappeared with local treatment. Clinical examination revealed a toe-nail onyxis from which C. ciferrii was isolated.
Figure 1. Toe-nail scraping (in chloral lactophenol) showing thin branched septate hyphae and blastospores ( x 400).
rnycoses 34, 125-128 (1991)
CANDIDA CIFERRII: AN
cases, numerous blastospores associated with hyphae (Fig. 1). Moreover, cultures yielded many colonies of yeasts identified as C.ciferriiand associated, for the toe-nail samples of the last case, with colonies of Aspergillus sydowi. This yeast, C. ciferrii, has a slow growth at 22°C or 37°C after one week, the colonies are small, cream coloured, tough, raised and wrinkled. Microscopical examination of the culture revealed an abundant and branched septate mycelium with small ramified chains of oval blastospores, variable in size, and arranged alongside the hyphae (Fig. 2). Susceptibility studies showed that the last isolate of C. ciferriiwas sensitive to amphotericin B, oxiconazole, econazole, clotrimazole, tioconazole and ketoconazole. In contrast, the yeast presented a total resistance to itraconazole, isoconazole, bifonazole, miconazole, fluconazole and 5FC. The API 10M - 5FC microcupule test proved the resistance of this isolate with a MIC > 64 mg ml-’. Finally, this isolate did mate with one of the mating type of Stephanoascus ciferrii and so can be identified as this teleomorph yeast.
Figure 2. Microscopical examination of culture of C. ciferrii showing short ramified chains of oval blastospores arranged alongside the hyphae ( x 1000).
mycoses 34, 125-128 (1991)
EMERGING PATHOGEN
127
Comments
Candida ciferrii Kreger-van Rij 1965 [71 is the anamorph of Stephanoascus ciferri Smith, van der Walt et Johanssen 1976 [8]. This yeast assimilates a large variety of carbohydrates and derivatives: glucose, galactose, saccharose, maltose, rafinose, Dxylose, cellobiose, trehalose, L-arabinose, D-ribose, inositol, erythritol, ribitol, D-mannitol, citric acid and succinic acid. In contrast, C. ciferrii does not assimilate lactose or potassium nitrate and does not ferment any carbohydrate. Using the ATB 32C identification system, we found that carbohydrate assimilation pattern of this yeast may resemble that of Trichosporon cutaneum. However, contrary to Tr. cutaneum, C. cifernY never assimilates melezitose and a-methyl-D-glucopyranoside. Finally, C. ciferrii seems to be the sole yeast able to utilize allantoin as source of carbon [9]. The natural habitat of this recently described yeast is poorly documented. C. ciferrii may be isolated from soil using enrichment culture medium with adenine [9]. So, this species has been described in soils of different origins: uncultivated soil in South Africa (strain CBS 6699) [8], dune sand contaminated with buffalo dung in Italy (strain BOA-304) [9], and soil taken from a goose breeder’s farm in France (strain GOA-302) [9]. The pathogenicity of this yeast is not really proved. Three strains have been described from animals: so, the strain CBS 4856 has been isolated from the neck of a cow in the Netherlands [7]; likewise, strains CBS 5295 and CBS 5646 have been isolated from the throat of a pig [7], and from bovine placenta [6], respectively. I n humans, only six isolates have been reported previously from clinical specimens. In light of the literature and of our experience, C. ciferriiseems to present a dual clinical spectrum. So, Furman & Ahearn [ 101 reported the case of a 25-year-old man examined in Kansas for pressure in the ears; a white powdery material was observed in the patient’s ear canals and culture of this material yielded on two occasions a profuse growth of C. cifernY. Likewise, this yeast has been isolated from the ear canals of young men in Oregon [ 101 and in Gabon [ l l ] , but associated in the last case with Aspergillus flavus, a well known agent of otomycosis. On the other hand, C. ciferrii may be involved in onychomycosis and tinea pedis. This species has been isolated from a human toe-web in Florida [ 101 and from the gangrenous foot of a 68-year-old female in Georgia [ 101. Moreover, a case of toe-nail onyxis caused by C. ciferriiin an elderly woman has been reported in Haway [lo] and in this case, the fungus was cultured on five occasions over a 1.5 year period. The presence of blastospores associated with pseudo-to-true mycelium at the direct microscopical
128
L. DE GENTILE ET AL.
examination of the clinical specimens which shows the parasitic transition of this yeast, and its repeated isolation from some of the reported cases lead us to consider C. ciferrii as an etiological agent of mycoses, especially onychomycosis. Our findings are insufficient to prove some clinical predispositions. Nevertheless, they suggest the association of these toe-nail or toe-web infections with extensive trophic disorders in elderly patients.
References Nagy, B., Sutka, P., Ziwe-el-Aldine, M., KovPcs, I., ForgPcs, V., Pulay, T., Gimes, R., Paulin, F., Lindeisz, F., Cstapli, J. & Csomor, S. ( 1 989) Candida guilliermondii var. guilliermondii infection in infertile women. mycoses 32, 183-186. PospiSil, L. ( 1 989) The significance of Candida pulcherrima findings in human clinical specimens. mycoses 32, 581-583. Klein, A. S., Tortora, G. T., Malowitz, R. & Greene, W. H. (1988) Hansenula anomala: a new fungal pathogen. Arch. Intern. Med. 148, 1210-1213.
4 Payne, A. L. & Teall, A. J. (1989) Trichosporon beigelii infection in an immunocompromised host. mycoses 32, 581583. 5 Kiehn, T. E., Edwards, F. F. & Armstrong, D. (1980) The prevalence of yeasts in clinical specimens from cancer patients. Am. J. Clin. Pathol. 73, 518-521. 6 van der Walt, J. P. & Yarrow, D. (1984) Methods for the isolation, maintenance, classification and identification of yeasts. In: Kreger-van Rij, N. J. W. (ed) The yeasts. A taxonomic study. Third revised and enlarged edition. Amsterdam: Elsevier, pp. 45-104. 7 Kreger-van Rij, N. J. W. (1965) Candida ufirnY, a new yeast species. Mycopath. Mycol. Appl. 26, 49-52. 8 Smith, M. T., van der Walt, J. P. & Johannsen, E. (1976) The genus Srephanoacus gen. nov. (Ascoideaceae). Antonie van LeeuwenhoekJ. Microbiol. Serol. 42, 119-127. 9 Middelhoven, W. J., de Kievit, H. & Biesbrock, A. L. (1985) Yeast species utilizing uric acid, adenine n-alkylamines or diamines as sole source of carbon and energy. Antonie van LeeuwenhoekJ. MicrobioI. Serol. 51, 289-301. 10 Furman, R. M. & Ahearn, D. G. (1983) Candida ciferriiand Candida chiropterum isolated from clinical specimens. J. Clin. Microbiol. 18, 1252-1255. 1 1 Kombila, M., Gomez de Diaz, M., de Bievre, C., Grepet, G., Debrie, J. C., Belembaogo, E. & Richard-Lenoble, D. (1989) Les otites mycosiques a Libreville; ttude de 83 cas. Bull. Soc. Path. Ex. 82, 201-207.
mycoses 34, 125-128 (1991)
MYCOSES
ACCEPTED: JULY 3, 1990
34, 125-128 (1991)
Candida cXerrii: clinical and microbiological features of an emerging pathogen
Candida ciferrii: Klinische und mikrobiologische Charakteristika eines Erregers zunehmender Bedeutung L. de Gentile, J. P. Bouchara, B. Cimon and D. Chabasse Key words. Candida ciferrii, onychomycosis. Schliisselworter. Candida ufirrii, Onychomykose.
Summary. The authors report six cases of toenail onyxis due to an unusual yeast species,Candida cifirrii. For half of these cases, direct microscopical examination showed the presence of blastospores and pseudo-to-true mycelium, demonstrating the parasitic transition of the fungus. In light of the literature and of their own experience, the authors suggest that C.ciferriicould be an etiological agent of onychomycosis, particularly for elderly patients with extensive trophic disorders. Zusammenfassung. Die Autoren berichten uber sechs Falle von FuBnagel-Onychomykose durch eine ungewohnliche Hefeart, Candida cifirrii. In drei dieser Falle zeigten sich Blastosporen und Obergange von Pseudomyzel zu echtem Myzel als Ausdruck parasitarer Aktivitat des Pilzes. Unter Beriicksichtigung der Literatur und eigener Erfahrungen vermuten die Autoren, daB C.cifirrii als atiologisches Agens fur Onychomykosen insbesondere bei alteren Menschen mit umfassenden trophischen Storungen in Frage kommt.
Introduction During the past decade, the incidence of yeast infections in humans has increased dramatically, probably in relation with the development of immunosuppressive therapy, and to a lesser extent with the improvement of diagnostic and identification methods. Similarly, apart from species usually encountered in human mycology such as Candida albicans, C. tropicalis and C. parapsilosis, or Candida (Torulopsis) glabra ta and Cryptococcus neoformans, other species are increasingly being noted as pathogens: for example C.guilliermondii [l], C.pulcherrima [2], Hansenula anomala [3] or Trichosporon beigelii [4]. Likewise, species of the genera Saccharomyces, Rhodotorula or Malassezia (Pityrosporum) have been described as etiological agents of mycoses in cancer patients [5]. Here, we report six cases of tinea pedis or onychomycosis due to C. cifirrii. For three of them, direct examination revealed numerous blastospores associated with hyphae, demonstrating the pathogenic potential of this unusual yeast. Moreover, this paper outlines the circumstances associated with the development of the infection.
Material and methods Laboratoire de Parasitologie - Mycologie, CHRU, Angers, France. Correspondence: Dr Ludovic de Gentile, Laboratoire de Parasitologie, CHRU, 4, rue Larrey, F-49033 Angers Cedex, France.
All clinical specimens were examined using a Leitz phase-contrast microscope after mounting in chloral lactophenol. Mycological cultures were also performed on Sabouraud dextrose agar (SDA) containing 0.5 mg ml-' choramphenicol and supplemented or not with 0.5 mg ml-' cycloheximide (Sig-
126
L.
DE
GENTILE ET
AL.
ma). Agar plates were incubated at 22" or 37"C, respectively. The yeasts were identified using standard biochemical tests: carbohydrate assimilation and fermentation as well as the assimilation of potassium nitrate were studied according to the methods described by van der Walt & Yarrow [6];identification of the last isolate was also realized with a microcupule carbohydrate assimilation system (ATB 32 C; API System). Susceptibility studies performed by two different commercially available diffusion methods (Eurobio and Diagnostics Pasteur) and resistance to 5-fluorocytosine (5FC) was confirmed by the determination of minimum inhibitory concentration (MIC) using the API 10 M - 5FC (API System). Diagnostics were confirmed, for yeasts by the Centraalbureau voor Schimmelcultures (CBS) at Delft (Netherlands) and for filamentous fungi, by the mycology unit of the Institut Pasteur of Paris.
Case 6. Since 1970, a 75-year-old man with a noninsulin-dependent diabetes mellitus and a rheumatismal valvulopathy consulted bimonthly for ulcerous lesions of the legs. On mid-November 1989, this patient was examined in our laboratory for an extensive and bilateral tinea pedis accompanied by toe-nail onyxis and tinea cruris. The skin was erythematous and chapped; the nails were distorted, discolored and friable. Direct examination of all samples of tinea pedis and onyxis showed numerous blastospores with pseudohyphae and true hyphae. Cultures of these materials yielded profuse growth of yeast-like colonies which were identified as C. cifirrii, associated with colonies of Aspergillus sydowi. In contrast, mycological examination of the scales scraped in the lesions of the crural and submammary folds were negative. In the absence of treatment, lesions persisted and the patient was again examined on mid-February 1990. At this time, results of direct examination and cultures of new samples were similar to those previously observed.
Case reports
Cases 1 and 2. Yeasts isolated from toe-nail onyxis (age: 52 and 69 years) were identified as C. cifirrii. No other etiological agent was isolated. Moreover, direct microscopical examination of the nail samples in case 1 revealed numerous blastospores and pseudohyphae.
Results Direct microscopical examination of the skin scales or nail fragments showed, for three of the reported
Case 3. An 88-year-old man was admitted to hospital for extensive cutaneous ulceration of the legs due to a vascular disease, probably in relation with an auricular fibrillation. He presented extensive ingrowing toe-nails. Mycological cultures of the nail fragments isolated C. ciferrii. Case 4. An alcoholic and tabagic 70-year-old man was admitted to hospital in April 1978. Because of a severe bilateral arteriopathy of the pelvic limbs, his second left toe was amputated four months before. Clinical examination revealed a venous insufficiency with large perforatic ulcers and an onychopathy. A white powdery material was observed under the distorted nails. Direct examination of this material showed numerous blastospores and hyphae. Yeasts isolated from the clinical specimens were identified as C. ciferrii. Case 5. A 84-year-old farmer, treated one year before for cardiac arrythmia, was admitted to hospital for various dermatologic problems. The patient presented a numular eczematosis on the legs associated with trophic disorders which rapidly disappeared with local treatment. Clinical examination revealed a toe-nail onyxis from which C. ciferrii was isolated.
Figure 1. Toe-nail scraping (in chloral lactophenol) showing thin branched septate hyphae and blastospores ( x 400).
rnycoses 34, 125-128 (1991)
CANDIDA CIFERRII: AN
cases, numerous blastospores associated with hyphae (Fig. 1). Moreover, cultures yielded many colonies of yeasts identified as C.ciferriiand associated, for the toe-nail samples of the last case, with colonies of Aspergillus sydowi. This yeast, C. ciferrii, has a slow growth at 22°C or 37°C after one week, the colonies are small, cream coloured, tough, raised and wrinkled. Microscopical examination of the culture revealed an abundant and branched septate mycelium with small ramified chains of oval blastospores, variable in size, and arranged alongside the hyphae (Fig. 2). Susceptibility studies showed that the last isolate of C. ciferriiwas sensitive to amphotericin B, oxiconazole, econazole, clotrimazole, tioconazole and ketoconazole. In contrast, the yeast presented a total resistance to itraconazole, isoconazole, bifonazole, miconazole, fluconazole and 5FC. The API 10M - 5FC microcupule test proved the resistance of this isolate with a MIC > 64 mg ml-’. Finally, this isolate did mate with one of the mating type of Stephanoascus ciferrii and so can be identified as this teleomorph yeast.
Figure 2. Microscopical examination of culture of C. ciferrii showing short ramified chains of oval blastospores arranged alongside the hyphae ( x 1000).
mycoses 34, 125-128 (1991)
EMERGING PATHOGEN
127
Comments
Candida ciferrii Kreger-van Rij 1965 [71 is the anamorph of Stephanoascus ciferri Smith, van der Walt et Johanssen 1976 [8]. This yeast assimilates a large variety of carbohydrates and derivatives: glucose, galactose, saccharose, maltose, rafinose, Dxylose, cellobiose, trehalose, L-arabinose, D-ribose, inositol, erythritol, ribitol, D-mannitol, citric acid and succinic acid. In contrast, C. ciferrii does not assimilate lactose or potassium nitrate and does not ferment any carbohydrate. Using the ATB 32C identification system, we found that carbohydrate assimilation pattern of this yeast may resemble that of Trichosporon cutaneum. However, contrary to Tr. cutaneum, C. cifernY never assimilates melezitose and a-methyl-D-glucopyranoside. Finally, C. ciferrii seems to be the sole yeast able to utilize allantoin as source of carbon [9]. The natural habitat of this recently described yeast is poorly documented. C. ciferrii may be isolated from soil using enrichment culture medium with adenine [9]. So, this species has been described in soils of different origins: uncultivated soil in South Africa (strain CBS 6699) [8], dune sand contaminated with buffalo dung in Italy (strain BOA-304) [9], and soil taken from a goose breeder’s farm in France (strain GOA-302) [9]. The pathogenicity of this yeast is not really proved. Three strains have been described from animals: so, the strain CBS 4856 has been isolated from the neck of a cow in the Netherlands [7]; likewise, strains CBS 5295 and CBS 5646 have been isolated from the throat of a pig [7], and from bovine placenta [6], respectively. I n humans, only six isolates have been reported previously from clinical specimens. In light of the literature and of our experience, C. ciferriiseems to present a dual clinical spectrum. So, Furman & Ahearn [ 101 reported the case of a 25-year-old man examined in Kansas for pressure in the ears; a white powdery material was observed in the patient’s ear canals and culture of this material yielded on two occasions a profuse growth of C. cifernY. Likewise, this yeast has been isolated from the ear canals of young men in Oregon [ 101 and in Gabon [ l l ] , but associated in the last case with Aspergillus flavus, a well known agent of otomycosis. On the other hand, C. ciferrii may be involved in onychomycosis and tinea pedis. This species has been isolated from a human toe-web in Florida [ 101 and from the gangrenous foot of a 68-year-old female in Georgia [ 101. Moreover, a case of toe-nail onyxis caused by C. ciferriiin an elderly woman has been reported in Haway [lo] and in this case, the fungus was cultured on five occasions over a 1.5 year period. The presence of blastospores associated with pseudo-to-true mycelium at the direct microscopical
128
L. DE GENTILE ET AL.
examination of the clinical specimens which shows the parasitic transition of this yeast, and its repeated isolation from some of the reported cases lead us to consider C. ciferrii as an etiological agent of mycoses, especially onychomycosis. Our findings are insufficient to prove some clinical predispositions. Nevertheless, they suggest the association of these toe-nail or toe-web infections with extensive trophic disorders in elderly patients.
References Nagy, B., Sutka, P., Ziwe-el-Aldine, M., KovPcs, I., ForgPcs, V., Pulay, T., Gimes, R., Paulin, F., Lindeisz, F., Cstapli, J. & Csomor, S. ( 1 989) Candida guilliermondii var. guilliermondii infection in infertile women. mycoses 32, 183-186. PospiSil, L. ( 1 989) The significance of Candida pulcherrima findings in human clinical specimens. mycoses 32, 581-583. Klein, A. S., Tortora, G. T., Malowitz, R. & Greene, W. H. (1988) Hansenula anomala: a new fungal pathogen. Arch. Intern. Med. 148, 1210-1213.
4 Payne, A. L. & Teall, A. J. (1989) Trichosporon beigelii infection in an immunocompromised host. mycoses 32, 581583. 5 Kiehn, T. E., Edwards, F. F. & Armstrong, D. (1980) The prevalence of yeasts in clinical specimens from cancer patients. Am. J. Clin. Pathol. 73, 518-521. 6 van der Walt, J. P. & Yarrow, D. (1984) Methods for the isolation, maintenance, classification and identification of yeasts. In: Kreger-van Rij, N. J. W. (ed) The yeasts. A taxonomic study. Third revised and enlarged edition. Amsterdam: Elsevier, pp. 45-104. 7 Kreger-van Rij, N. J. W. (1965) Candida ufirnY, a new yeast species. Mycopath. Mycol. Appl. 26, 49-52. 8 Smith, M. T., van der Walt, J. P. & Johannsen, E. (1976) The genus Srephanoacus gen. nov. (Ascoideaceae). Antonie van LeeuwenhoekJ. Microbiol. Serol. 42, 119-127. 9 Middelhoven, W. J., de Kievit, H. & Biesbrock, A. L. (1985) Yeast species utilizing uric acid, adenine n-alkylamines or diamines as sole source of carbon and energy. Antonie van LeeuwenhoekJ. MicrobioI. Serol. 51, 289-301. 10 Furman, R. M. & Ahearn, D. G. (1983) Candida ciferriiand Candida chiropterum isolated from clinical specimens. J. Clin. Microbiol. 18, 1252-1255. 1 1 Kombila, M., Gomez de Diaz, M., de Bievre, C., Grepet, G., Debrie, J. C., Belembaogo, E. & Richard-Lenoble, D. (1989) Les otites mycosiques a Libreville; ttude de 83 cas. Bull. Soc. Path. Ex. 82, 201-207.
mycoses 34, 125-128 (1991)
