Clinicat and Experimentat Dermatotogy 1992; 17 (Suppl. 1): 37-40.
Clinical and mycological diagnostic aspects of onychomycoses and dermatomycoses Y.M.CLAYTON, Institute of Dermatology, St Thomas' Hospital, London, UK the nail plate and then spreads proximally up the nail. As the infection becomes established, the nail plate becomes friable and thickened and may eventually completely crumble away due to the accumulation of subungual debris. In developed countries, this type of nail invasion is nearly always caused by Trichophyton rubrum. During 1990, 462 of 539 (85%) dermatophytes isolated from nails investigated in a routine diagnostic mycological laboratory were T. rubrum. Trichophyton interdigitale was grown from 13% of infected nails and Epidermophyton floccosum from only three cases (Table 1). In parts ofthe world where T. violaceum, T. soudanense and T. schoenleinii are endemic, these fungi may produce similar infections. However, it has been reported that nail changes caused by infection with T. soudanense may be different from the usual type of
The most common fungal disease of man is tinea pedis, and it has been estimated that 10-15% of the adult population in developed countries are affected at any one time. This prevalence may be even higher among at-risk groups such as swimmers and coal miners. There is no published data on the extent of onychomycoses in the general population but, extrapolating from the above figures and assuming that one-third of subjects will have some form of nail involvement, Evans' postulated that about 5% of the general population could have fungal disease. In view of the dimensions of these clinical conditions and because of their relatively poor response to treatment, it is important to summarize the natural history and diagnosis of nail and foot infections. Onychomycosis
Onychomycosis may be caused by dermatophytes or nondermatophyte filamentous fungi and yeasts. Dermatophytes are the principal organisms causing primary disease of toe and finger nails, and the term tinea unguium is used to describe the infection. Non-dermatophytes such as Scopulariopsis brevicaulis, Aspergillus and Acremo-Table 1. Results from 2113 nails examined during 1990 nium species are nearly always associated with toe-nail dystrophy and are usually secondary invaders of diseased Toe or traumatized nails. In temperate regions they may nails account for only 2-3% of fungal-nail infections. Two other non-dermatophytes, Hendersonula toruloidea {Scy- Total examined 1430 talidium dimidiatum) and S. hyalinum, can invade nails Negative for fungi 671 (47)t and thickly keratinized skin.^ The vast majority of these Microscopy positive \ 275 (19) infections have been recorded in subjects from subtropi- Culture negative J cal and tropical parts ofthe world. Nail infection caused by yeasts is almost exclusively seen in finger nails, and Fungi isolated Candida albicans is the organism most commonly Dermatophytes involved. T. rubrum 389 (27) T. interdigitale 71(5) Onychomycoses are rare in children but frequency E. floccosum 3 increases with age, and it has been suggested that a T. erinaceijT. violaceum 1 prevalence of 15-20% ofthe population aged between 40 Non-dermatophytes and 60 years could be an underestimation.^ Hendersonula toruloidea 4 Clinical aspects (a) Tinea unguium Two main types of infection are seen.
Others* Yeasts Candida atbicans Candida species
11 4 1
Finger nails 683 424 (62) 74(11)
73(11) 1 0 1 2
•
0 71 (10) 37(5)
(i) Distal and lateral subungual onychomycosis. Invasion starts at the distal or lateral edges of * Scop, brevicautis, eight; Aspergittus fumigatus, one; A. nidulans, Correspondence: Dr Y.M.Clayton, Institute of Dermatology, St Thomas' Hospital, London SEI 7EH, UK.
one; Acremonium sp., one. t Numbers in parentheses are percentages.
37
38
Y.M.CLAYTON
distal subunguai onychomycosis. Differences Candida albicans although other Candida species, include a diffuse, mild thickening ofthe nail in particular C. parapsilosis., may be implicated. plate, often with hyperpigmentation, lamellar There is no evidence that yeasts are keratinolytic peeling, transverse ridging and pitting.^ but they may possibly possess some proteolytic (ii) Superjtcial white onychomycosis. This is a activity which can destroy the integrity of keratin. minor type of nail damage produced by a Finger nails are far more commonly involved than fungus invading the superficial surface ofthe toe nails. nail plate with minimal penetration ofthe nail. Candida species may affect nails in the following White patches are produced in the nail which ways: may be easily removed by scraping. This (i) Total dystrophtc onychomycosis. There is gross condition occurs mainly on toe nails and the hyperkeratosis ofthe nail plate with distortion dermatophyte most frequently associated with ot the normal curvature and distal erosion. this form of invasion is T. interdigitale. This type of nail invasion is seen in patients (b) Non-dermatophyte infections with chronic mucocutaneous candidosis. Nail infections caused by non-keratinolytic (ii) Chronic proximal paronychia. Nail invasion moulds such as Scopulariopsis brevicaulis^ Aspergilfollows a chronic paronychial infection. The lus, Acremonium and Fusarium species are of nail plate may be affected centrally or at one or necessity secondary invaders of damaged or disboth lateral edges. The nail may show irregueased nails, and have most frequently been lar transverse grooves and ridges with discoreported from elderly patients whose nails are louration ofthe lateral margin. often affected by age-related changes.-^'' Toe nails (iii) Primary distal and lateral onycholysis without are more likely to be infected than finger nails. paronychia. These changes have been Hendersonula toruloidea and S. hyalinum are reported mainly from patients with underprimary invaders of the nail plate and infected lying vascular disease or Cushing's synnails are often severely abnormal. Toe nails drome.'" frequently show distal or lateral subungual hyperChronic paronychia, the commonest keratosis with onycholysis and thickening and predisposing factor to nail invasion by Canopacification ofthe nail plate. dida species., is seen three times more freA brownish-black discoloration may occur. quently in women than in men. It is not Some features of finger-nail invasion by these surprising, therefore, that finger-nail fungi are pathognomonic. Onycholysis of the infections occur more commonly in women. lateral nail plate alone is the predominant form of Table 2 shows the number of isolations of invasion leading lo involvement ofthe whole nailplate without significant thickening, followed by transverse fracture and shedding of the major Table 2. Dermatophytes and yeasts isokted from linger nails during portion ofthe nail. Paronychia may also be present 1990 so that onychomycosis of the finger nail may be more suggestive of candidosis than dermatophytoMales Females sis.' Superficial white onychomycosis may be pro- Dermatophytes T. rubrum 50(17) 23(6) duced by non-dermatophytes, particularly AcreT. interdigitate 1 0 monttim species.-^ T. violaceum 0 1 C>>mparcd to dermatophytosis ofthe nails, these Yeasts infections are relatively rare. Jn one series of over Candida albicans 15(5) 56* (14) 2500 cases of onychomycosis.. filamentous nonC. parapsilosis 2 24 (6) Candida sp. dermatophytes were isolated from 83 cases (3 3'^'(,) 2 9 with S. brevicaulis, II.toruloidea and Aspergillus Non-dermatophytes species being the commonest species.^ However, it Hendersonula toruloidea 1 1 has been suggested thar these infections may be Microscopv positive 1 34(11) 40(10) more common in the general population than Culture negative J reported results from dermatological clinics.'^ Negative for fungi 191 (65) 23.^> (f)0) They may cause little discomfort to the patient so that only a small proportion may present to the Total 296 387 dermatologist. (c) Yeast infections * Six with C. parapsilosis. The majority of these infections arc caused by t Numbers in parentheses are percentages.
ONYCIIOMYCOSES AND DKRMATOMYCOSES C.albicans and other Candida species from fmger nails compared to dermatophytes during a 1-year period. Of 183 finger nails which were positive on microscopy for either dermatophyte hyphae, yeasts and hyphae or yeasts alone, 108 (59",',) grew C. alhicans or other Candida species. Whilst male finger nails were more likely to be infected by dermatophytes (73'>Q), Candida species were the cause of 79**o of female finger-nail infections. During the same period, there were only five isolations of Candida species from toe-nail infections (C. albicans—two males and two females and one (.. parapsilosis |malej). Dermatomycoses of the feet
infection of the skin of the feet. Hendersonula toruloidea and S. hyalinum., on the other hand, can produce lesions between the toes and on the soles that are clinically indistinguishable from those of T. rubrum.' Infections caused by these two fungi have occurred mainly among patients from tropical and subtropical parts of the world. Hendersonula toruloidea has heen recorded in patients from the Caribbean, Africa, the Middle East, the Indian Ocean, Thailand, Hong Kong and Fiji. Scytaltdiiim hyalinum infections have so far been only in patients from the Caribbean and West Africa. The majority of cases of H. toruloidea infection recorded in Europe- and Canada^ have been in immigrants from areas where the fungus is endemic and account for only approximately 2-3"o of isolates from cases of fungal foot infections. However, in endemic areas where H. loruloidea infections have been studied, the incidence has been found to be high. In Thailand, for example, 68 cases of tinea pedis found in a survey of 145 soldiers showed that dermatophytes accounted for only S-S^)Q of the infections while H. toruloidea was grown from 39"',,.''' In Nigeria,'i^'-^'oof 250 coal miners had //. toruloidea infection of the toe spaces indicating a 47"{, prevalence.'*' Mixed infections of H. toruloidea with a dermatophyte are not uncommon." (c) Yeast infections Candida albicans and other Candida species may occasionally cause maceration and erosion ot the skin of the toe spaces.
(a) Tinea pedis The dermatophytes causing tinea pedis are all anthropophilic and i . rubrum is now the commonest species isolated in temperate climates accounting for apprtjximately 85'*,) of isolates. 7'. interdigitale is next in prevalence (12-15",,) whilst R. floccosuni is isolated mueh less frequently (2-5"()). Infection usually starts in the toe spaces, often between the fourth and fifth toe, and is characterized by peeling, maceration and fissures. In the acute phase the lesions are usually itchy. Spread of infection ma\ occur to the toes and soles where the clinical features are dependent on the fungus responsible. When 7'. inlerdigitale is the causative organism, a vesicular, eczema-like appearance may occur, whereas vcr\ persistent, non-inflammatory Mycological diagnosis lesions v\ith tine, dry scaling are characteristic of T. rubrum infections. The variety of organisms that cause naii and foot infection Few studies have been carried out on the has already been indicated. As the clinical features prevalence of tinea pedis among the general produced may be identical, for example as in 7'. ruhrum population. A survey of 296 shop and office and //. toruloidea infections of the toe spaces and toe nails, workers in London showed that 15'*,) had a and as they may not respond to the same antifungal dermatophyte infection of the toe spaces.'^ treatment, it is always important to confirm the diagnosis As these subjects were volunteers the results by microscopy of skin scrapings and nail clippings and by could be slightly biased as some may have been culture. It is also essential to confirm that the infection is seeking advice for known symptoms. Surveys have fungal. In a study t)f 113 patients with primary onycholvshown that among at-ri,sk groups such as swim- sis of big-toe nails, Baran and Badillet'' found that the mers and those using communal bathing facilities main aetiological factor was not a fungal infection, only the incidence may be as high as 22",,.'-''' A survey 23'!,, of the nails being positi\e on microscopy. In an of coal miners, where an incidence of 27",'> analysis of over 2000 nails with suspected fungal disease dermatophvte infections of the toe spaces was examined in a diagnostie myeological laboratory, 47'*,, of found, also showed a high prevalence of mixed toe nails and 62'^,, of finger nails were negative on infection with dermatophytes and Gram-negative microscopy and on culture (Table 1). bacteria such as Pseudomonas and Proteus species. '"* Initial damage to the toe space by a dermatophyte Microscopy may predispose ir to a secondary bacterial infection. Direct microscopy provides a rapid test for the diagnosis (b) Non~dermatophyte Jilamenlous injections of fungal infection of the skin and nail. Dermatophytes Moulds such as S. brevicaulis rarely, il ever, cause can readily be distinguished from yeasts and it is possible
40
Y.M.CLAYTON
for a trained observer to differentiate a non-dermatophyte fungus from a dermatophyte. This is particularly helpful in the case of infected nails which often fail to produce a positive culture due to the fact that the fungus in the accessible, distal part of the nail is no longer viable. As can be seen from Table 1, 19 and 11% of toe and finger nails respectively positive on microscopy failed to produce a positive culture. Microscopy is usually performed by softening and clearing the skin or nail specimen in 20-30% potassium hydroxide (KOH). For suspected mould infections, the addition of Parker's blue-black ink (1 part KOH: 1 part blue-black ink) may be helpful. The use of a fluorescent brightener sueb as Calcofluor or Blankophor B, which are retained by chitin of the cell wall and seen under a fluorescent microscope, is also helpful, particularly when only scanty fungal elements are present.
medium. As many of these moulds are common in the environment, it is important whenever possible to repeat culture studies on any microscopically positive nail that grows these fungi.'' This is in order to ensure that the fungus isolated is the cause of the infection and not masking a more slowly growing dermatophyte. As H. toruloidea and S. hyalinum infections are sometimes difficult to distinguish from dermatophytosis both clinically and on microscopy, material from cases suspected of being of non-dermatophyte origin should always be cultured on medium with and without cycloheximide. Referenees
1, Evans EGV, Nail dermatophytosis: the nature and scale of the prohXtm. Journal of Dermatological Treatment 1990; l(Suppl, 2) 47-48. 2, Moore MK, Hendersonula toruloidea and Scytalidium hyalinum Microscopical features infections in London, Enghnd. Journal of Medical and Veterinary Mycology 1986; 24: 219-230. (a) Dermatophytes. 3, Zaias N, Onychomycosis, Dermatological Clinics 1985; 3:445-460, Hyphae and arthroconidia (arthrospores). 4, Kalter DC, Hay RJ, Onychomycosis due to Trichophyton (b) Scopulariopsis brevicaulis. soudanense. Clinical and Experimental Dermatology 1988; 12: 221227, Scanty hyphal elements but numerous lemon5, English MP, Atkinson R, Onychomycosis in elderly chiropody shaped and thick-walled spores. These readily take patients, British Journal of Dermatology 1974; 91: bl-ll. up Parker's stain. 6, Schonborn C, Schmoranzer H, Untersuchungen iiber Schimmel(c) Other moulds such as Aspergillius and Acremonium pilzinfektionen der Zehennagel, Mykosen 1970; 13: 253-272. species. 7, Hay RJ, Moore MK, Clinical features of superficial fungal infections caused by Hendersonula toruloidea and Scytalidium Hyphae often have a fronded appearance'^ and hyalinum. British Journal of Dermatology 1984; 110: 677-683, may stain more quickly in Parker's stain than 8, Summerbell RC, Kane J, Krajden S, Onychomycosis, tinea pedis dermatophyte hyphae. and tinea manuum caused by non-dermatophyte filamentous (d) Hendersonula toruloidea and S. hyalinum. fungi. Mycoses 1989; 32: 609-619, Hyphae of these two fungi are indistinguishable 9, Walshe MM, English MP. Fungi in nails. British Journal of from one another but differ from dermatophyte Dermatology 1966; 78: 198-207, hyphae in being much more variable in width, with 10, Hay, RJ, Baran R, Moore MK, Wilkinson JD. Candida onychomycosis—an evaluation of the role of Candida species in nail a smooth, sinuous appearance. They often appear dkease. Journal of Dermatology 1988; 118: 47-58, double-contoured due to retraction of cytoplasm 11, Howell SA, Clayton YM, Phan QC, Noble WC, Tinea pedis: The from the hyphal cell wall.^ relationship between symptoms, organisms and host characteristics, Microbial Ecology in Health and Disease 1988; 1: 131-135, (e) Yeasts. Oval, budding yeast cells which may be dis- 12, Gentles JC, Evans EGV, Foot infections in swimming baths. British Medical Journal 1973; 3: 260-262, tinguished from Pityrosporum yeasts by Parker's 13, English MP, Gibson MD, Warin RP, Studies in the epidemiology stain. The latter take up the blue dye immediately of tinea pedis VI Tinea Pedis in a boys' boarding school, British whilst Candida yeasts will take much longer to Medical Journal 1961; 1: 1083-1086, stain. When C. albicans is the infective agent, both 14, Hope YM, Clayton YM, Hay RJ, Noble WC, Elder-Smith JG, Foot infection in coal-miners: a reassessment, British Journal of hyphae and yeasts are present. Dermatology 1985; 112: 405-413, 15, Kotrajaras R, Chongsathien S, Rojanavanich V, Buddhavudhikrai Culture P, Viriyayudhakorn, S. Hendersonula toruloidea infection in Thailand, Internationaljournal ofDermatology 1988; 27:391-395, A glucose/peptone agar (Sabouraud medium) is satis16, Gugnani HC, Nzelibe FK, Osunkwo IC, Onychomycosis due to factory for the isolation of the majority of fungal Hendersonula toruloidea in Nigeria, Journal of Medical and pathogens of the skin and nail. Veterinary Mycology 1986; 24: 239-241. 17, Baran R, Badillet G. Primary onycholysis of the big toe nails: a (a) Dermatophytes. review of 113 cases, British Journal ofDermatology 1982; 106: 529Cycloheximide (Actidione) should be added to cut 534, down contaminating fungi. 18, Zaias N, Onychomycosis, Archives ofDermatology 1972; 105: 263(b) Non-dermatophytefilamentousfungi. 274, All these fungi are sensitive to cycloheximide so 19, Englis.hM?.Nai\s!ind{ungi. British Journal ofDermatotogy 1976; 94: 697-701, this antibiotic must be omitted from culture
Clinical and mycological diagnostic aspects of onychomycoses and dermatomycoses Y.M.CLAYTON, Institute of Dermatology, St Thomas' Hospital, London, UK the nail plate and then spreads proximally up the nail. As the infection becomes established, the nail plate becomes friable and thickened and may eventually completely crumble away due to the accumulation of subungual debris. In developed countries, this type of nail invasion is nearly always caused by Trichophyton rubrum. During 1990, 462 of 539 (85%) dermatophytes isolated from nails investigated in a routine diagnostic mycological laboratory were T. rubrum. Trichophyton interdigitale was grown from 13% of infected nails and Epidermophyton floccosum from only three cases (Table 1). In parts ofthe world where T. violaceum, T. soudanense and T. schoenleinii are endemic, these fungi may produce similar infections. However, it has been reported that nail changes caused by infection with T. soudanense may be different from the usual type of
The most common fungal disease of man is tinea pedis, and it has been estimated that 10-15% of the adult population in developed countries are affected at any one time. This prevalence may be even higher among at-risk groups such as swimmers and coal miners. There is no published data on the extent of onychomycoses in the general population but, extrapolating from the above figures and assuming that one-third of subjects will have some form of nail involvement, Evans' postulated that about 5% of the general population could have fungal disease. In view of the dimensions of these clinical conditions and because of their relatively poor response to treatment, it is important to summarize the natural history and diagnosis of nail and foot infections. Onychomycosis
Onychomycosis may be caused by dermatophytes or nondermatophyte filamentous fungi and yeasts. Dermatophytes are the principal organisms causing primary disease of toe and finger nails, and the term tinea unguium is used to describe the infection. Non-dermatophytes such as Scopulariopsis brevicaulis, Aspergillus and Acremo-Table 1. Results from 2113 nails examined during 1990 nium species are nearly always associated with toe-nail dystrophy and are usually secondary invaders of diseased Toe or traumatized nails. In temperate regions they may nails account for only 2-3% of fungal-nail infections. Two other non-dermatophytes, Hendersonula toruloidea {Scy- Total examined 1430 talidium dimidiatum) and S. hyalinum, can invade nails Negative for fungi 671 (47)t and thickly keratinized skin.^ The vast majority of these Microscopy positive \ 275 (19) infections have been recorded in subjects from subtropi- Culture negative J cal and tropical parts ofthe world. Nail infection caused by yeasts is almost exclusively seen in finger nails, and Fungi isolated Candida albicans is the organism most commonly Dermatophytes involved. T. rubrum 389 (27) T. interdigitale 71(5) Onychomycoses are rare in children but frequency E. floccosum 3 increases with age, and it has been suggested that a T. erinaceijT. violaceum 1 prevalence of 15-20% ofthe population aged between 40 Non-dermatophytes and 60 years could be an underestimation.^ Hendersonula toruloidea 4 Clinical aspects (a) Tinea unguium Two main types of infection are seen.
Others* Yeasts Candida atbicans Candida species
11 4 1
Finger nails 683 424 (62) 74(11)
73(11) 1 0 1 2
•
0 71 (10) 37(5)
(i) Distal and lateral subungual onychomycosis. Invasion starts at the distal or lateral edges of * Scop, brevicautis, eight; Aspergittus fumigatus, one; A. nidulans, Correspondence: Dr Y.M.Clayton, Institute of Dermatology, St Thomas' Hospital, London SEI 7EH, UK.
one; Acremonium sp., one. t Numbers in parentheses are percentages.
37
38
Y.M.CLAYTON
distal subunguai onychomycosis. Differences Candida albicans although other Candida species, include a diffuse, mild thickening ofthe nail in particular C. parapsilosis., may be implicated. plate, often with hyperpigmentation, lamellar There is no evidence that yeasts are keratinolytic peeling, transverse ridging and pitting.^ but they may possibly possess some proteolytic (ii) Superjtcial white onychomycosis. This is a activity which can destroy the integrity of keratin. minor type of nail damage produced by a Finger nails are far more commonly involved than fungus invading the superficial surface ofthe toe nails. nail plate with minimal penetration ofthe nail. Candida species may affect nails in the following White patches are produced in the nail which ways: may be easily removed by scraping. This (i) Total dystrophtc onychomycosis. There is gross condition occurs mainly on toe nails and the hyperkeratosis ofthe nail plate with distortion dermatophyte most frequently associated with ot the normal curvature and distal erosion. this form of invasion is T. interdigitale. This type of nail invasion is seen in patients (b) Non-dermatophyte infections with chronic mucocutaneous candidosis. Nail infections caused by non-keratinolytic (ii) Chronic proximal paronychia. Nail invasion moulds such as Scopulariopsis brevicaulis^ Aspergilfollows a chronic paronychial infection. The lus, Acremonium and Fusarium species are of nail plate may be affected centrally or at one or necessity secondary invaders of damaged or disboth lateral edges. The nail may show irregueased nails, and have most frequently been lar transverse grooves and ridges with discoreported from elderly patients whose nails are louration ofthe lateral margin. often affected by age-related changes.-^'' Toe nails (iii) Primary distal and lateral onycholysis without are more likely to be infected than finger nails. paronychia. These changes have been Hendersonula toruloidea and S. hyalinum are reported mainly from patients with underprimary invaders of the nail plate and infected lying vascular disease or Cushing's synnails are often severely abnormal. Toe nails drome.'" frequently show distal or lateral subungual hyperChronic paronychia, the commonest keratosis with onycholysis and thickening and predisposing factor to nail invasion by Canopacification ofthe nail plate. dida species., is seen three times more freA brownish-black discoloration may occur. quently in women than in men. It is not Some features of finger-nail invasion by these surprising, therefore, that finger-nail fungi are pathognomonic. Onycholysis of the infections occur more commonly in women. lateral nail plate alone is the predominant form of Table 2 shows the number of isolations of invasion leading lo involvement ofthe whole nailplate without significant thickening, followed by transverse fracture and shedding of the major Table 2. Dermatophytes and yeasts isokted from linger nails during portion ofthe nail. Paronychia may also be present 1990 so that onychomycosis of the finger nail may be more suggestive of candidosis than dermatophytoMales Females sis.' Superficial white onychomycosis may be pro- Dermatophytes T. rubrum 50(17) 23(6) duced by non-dermatophytes, particularly AcreT. interdigitate 1 0 monttim species.-^ T. violaceum 0 1 C>>mparcd to dermatophytosis ofthe nails, these Yeasts infections are relatively rare. Jn one series of over Candida albicans 15(5) 56* (14) 2500 cases of onychomycosis.. filamentous nonC. parapsilosis 2 24 (6) Candida sp. dermatophytes were isolated from 83 cases (3 3'^'(,) 2 9 with S. brevicaulis, II.toruloidea and Aspergillus Non-dermatophytes species being the commonest species.^ However, it Hendersonula toruloidea 1 1 has been suggested thar these infections may be Microscopv positive 1 34(11) 40(10) more common in the general population than Culture negative J reported results from dermatological clinics.'^ Negative for fungi 191 (65) 23.^> (f)0) They may cause little discomfort to the patient so that only a small proportion may present to the Total 296 387 dermatologist. (c) Yeast infections * Six with C. parapsilosis. The majority of these infections arc caused by t Numbers in parentheses are percentages.
ONYCIIOMYCOSES AND DKRMATOMYCOSES C.albicans and other Candida species from fmger nails compared to dermatophytes during a 1-year period. Of 183 finger nails which were positive on microscopy for either dermatophyte hyphae, yeasts and hyphae or yeasts alone, 108 (59",',) grew C. alhicans or other Candida species. Whilst male finger nails were more likely to be infected by dermatophytes (73'>Q), Candida species were the cause of 79**o of female finger-nail infections. During the same period, there were only five isolations of Candida species from toe-nail infections (C. albicans—two males and two females and one (.. parapsilosis |malej). Dermatomycoses of the feet
infection of the skin of the feet. Hendersonula toruloidea and S. hyalinum., on the other hand, can produce lesions between the toes and on the soles that are clinically indistinguishable from those of T. rubrum.' Infections caused by these two fungi have occurred mainly among patients from tropical and subtropical parts of the world. Hendersonula toruloidea has heen recorded in patients from the Caribbean, Africa, the Middle East, the Indian Ocean, Thailand, Hong Kong and Fiji. Scytaltdiiim hyalinum infections have so far been only in patients from the Caribbean and West Africa. The majority of cases of H. toruloidea infection recorded in Europe- and Canada^ have been in immigrants from areas where the fungus is endemic and account for only approximately 2-3"o of isolates from cases of fungal foot infections. However, in endemic areas where H. loruloidea infections have been studied, the incidence has been found to be high. In Thailand, for example, 68 cases of tinea pedis found in a survey of 145 soldiers showed that dermatophytes accounted for only S-S^)Q of the infections while H. toruloidea was grown from 39"',,.''' In Nigeria,'i^'-^'oof 250 coal miners had //. toruloidea infection of the toe spaces indicating a 47"{, prevalence.'*' Mixed infections of H. toruloidea with a dermatophyte are not uncommon." (c) Yeast infections Candida albicans and other Candida species may occasionally cause maceration and erosion ot the skin of the toe spaces.
(a) Tinea pedis The dermatophytes causing tinea pedis are all anthropophilic and i . rubrum is now the commonest species isolated in temperate climates accounting for apprtjximately 85'*,) of isolates. 7'. interdigitale is next in prevalence (12-15",,) whilst R. floccosuni is isolated mueh less frequently (2-5"()). Infection usually starts in the toe spaces, often between the fourth and fifth toe, and is characterized by peeling, maceration and fissures. In the acute phase the lesions are usually itchy. Spread of infection ma\ occur to the toes and soles where the clinical features are dependent on the fungus responsible. When 7'. inlerdigitale is the causative organism, a vesicular, eczema-like appearance may occur, whereas vcr\ persistent, non-inflammatory Mycological diagnosis lesions v\ith tine, dry scaling are characteristic of T. rubrum infections. The variety of organisms that cause naii and foot infection Few studies have been carried out on the has already been indicated. As the clinical features prevalence of tinea pedis among the general produced may be identical, for example as in 7'. ruhrum population. A survey of 296 shop and office and //. toruloidea infections of the toe spaces and toe nails, workers in London showed that 15'*,) had a and as they may not respond to the same antifungal dermatophyte infection of the toe spaces.'^ treatment, it is always important to confirm the diagnosis As these subjects were volunteers the results by microscopy of skin scrapings and nail clippings and by could be slightly biased as some may have been culture. It is also essential to confirm that the infection is seeking advice for known symptoms. Surveys have fungal. In a study t)f 113 patients with primary onycholvshown that among at-ri,sk groups such as swim- sis of big-toe nails, Baran and Badillet'' found that the mers and those using communal bathing facilities main aetiological factor was not a fungal infection, only the incidence may be as high as 22",,.'-''' A survey 23'!,, of the nails being positi\e on microscopy. In an of coal miners, where an incidence of 27",'> analysis of over 2000 nails with suspected fungal disease dermatophvte infections of the toe spaces was examined in a diagnostie myeological laboratory, 47'*,, of found, also showed a high prevalence of mixed toe nails and 62'^,, of finger nails were negative on infection with dermatophytes and Gram-negative microscopy and on culture (Table 1). bacteria such as Pseudomonas and Proteus species. '"* Initial damage to the toe space by a dermatophyte Microscopy may predispose ir to a secondary bacterial infection. Direct microscopy provides a rapid test for the diagnosis (b) Non~dermatophyte Jilamenlous injections of fungal infection of the skin and nail. Dermatophytes Moulds such as S. brevicaulis rarely, il ever, cause can readily be distinguished from yeasts and it is possible
40
Y.M.CLAYTON
for a trained observer to differentiate a non-dermatophyte fungus from a dermatophyte. This is particularly helpful in the case of infected nails which often fail to produce a positive culture due to the fact that the fungus in the accessible, distal part of the nail is no longer viable. As can be seen from Table 1, 19 and 11% of toe and finger nails respectively positive on microscopy failed to produce a positive culture. Microscopy is usually performed by softening and clearing the skin or nail specimen in 20-30% potassium hydroxide (KOH). For suspected mould infections, the addition of Parker's blue-black ink (1 part KOH: 1 part blue-black ink) may be helpful. The use of a fluorescent brightener sueb as Calcofluor or Blankophor B, which are retained by chitin of the cell wall and seen under a fluorescent microscope, is also helpful, particularly when only scanty fungal elements are present.
medium. As many of these moulds are common in the environment, it is important whenever possible to repeat culture studies on any microscopically positive nail that grows these fungi.'' This is in order to ensure that the fungus isolated is the cause of the infection and not masking a more slowly growing dermatophyte. As H. toruloidea and S. hyalinum infections are sometimes difficult to distinguish from dermatophytosis both clinically and on microscopy, material from cases suspected of being of non-dermatophyte origin should always be cultured on medium with and without cycloheximide. Referenees
1, Evans EGV, Nail dermatophytosis: the nature and scale of the prohXtm. Journal of Dermatological Treatment 1990; l(Suppl, 2) 47-48. 2, Moore MK, Hendersonula toruloidea and Scytalidium hyalinum Microscopical features infections in London, Enghnd. Journal of Medical and Veterinary Mycology 1986; 24: 219-230. (a) Dermatophytes. 3, Zaias N, Onychomycosis, Dermatological Clinics 1985; 3:445-460, Hyphae and arthroconidia (arthrospores). 4, Kalter DC, Hay RJ, Onychomycosis due to Trichophyton (b) Scopulariopsis brevicaulis. soudanense. Clinical and Experimental Dermatology 1988; 12: 221227, Scanty hyphal elements but numerous lemon5, English MP, Atkinson R, Onychomycosis in elderly chiropody shaped and thick-walled spores. These readily take patients, British Journal of Dermatology 1974; 91: bl-ll. up Parker's stain. 6, Schonborn C, Schmoranzer H, Untersuchungen iiber Schimmel(c) Other moulds such as Aspergillius and Acremonium pilzinfektionen der Zehennagel, Mykosen 1970; 13: 253-272. species. 7, Hay RJ, Moore MK, Clinical features of superficial fungal infections caused by Hendersonula toruloidea and Scytalidium Hyphae often have a fronded appearance'^ and hyalinum. British Journal of Dermatology 1984; 110: 677-683, may stain more quickly in Parker's stain than 8, Summerbell RC, Kane J, Krajden S, Onychomycosis, tinea pedis dermatophyte hyphae. and tinea manuum caused by non-dermatophyte filamentous (d) Hendersonula toruloidea and S. hyalinum. fungi. Mycoses 1989; 32: 609-619, Hyphae of these two fungi are indistinguishable 9, Walshe MM, English MP. Fungi in nails. British Journal of from one another but differ from dermatophyte Dermatology 1966; 78: 198-207, hyphae in being much more variable in width, with 10, Hay, RJ, Baran R, Moore MK, Wilkinson JD. Candida onychomycosis—an evaluation of the role of Candida species in nail a smooth, sinuous appearance. They often appear dkease. Journal of Dermatology 1988; 118: 47-58, double-contoured due to retraction of cytoplasm 11, Howell SA, Clayton YM, Phan QC, Noble WC, Tinea pedis: The from the hyphal cell wall.^ relationship between symptoms, organisms and host characteristics, Microbial Ecology in Health and Disease 1988; 1: 131-135, (e) Yeasts. Oval, budding yeast cells which may be dis- 12, Gentles JC, Evans EGV, Foot infections in swimming baths. British Medical Journal 1973; 3: 260-262, tinguished from Pityrosporum yeasts by Parker's 13, English MP, Gibson MD, Warin RP, Studies in the epidemiology stain. The latter take up the blue dye immediately of tinea pedis VI Tinea Pedis in a boys' boarding school, British whilst Candida yeasts will take much longer to Medical Journal 1961; 1: 1083-1086, stain. When C. albicans is the infective agent, both 14, Hope YM, Clayton YM, Hay RJ, Noble WC, Elder-Smith JG, Foot infection in coal-miners: a reassessment, British Journal of hyphae and yeasts are present. Dermatology 1985; 112: 405-413, 15, Kotrajaras R, Chongsathien S, Rojanavanich V, Buddhavudhikrai Culture P, Viriyayudhakorn, S. Hendersonula toruloidea infection in Thailand, Internationaljournal ofDermatology 1988; 27:391-395, A glucose/peptone agar (Sabouraud medium) is satis16, Gugnani HC, Nzelibe FK, Osunkwo IC, Onychomycosis due to factory for the isolation of the majority of fungal Hendersonula toruloidea in Nigeria, Journal of Medical and pathogens of the skin and nail. Veterinary Mycology 1986; 24: 239-241. 17, Baran R, Badillet G. Primary onycholysis of the big toe nails: a (a) Dermatophytes. review of 113 cases, British Journal ofDermatology 1982; 106: 529Cycloheximide (Actidione) should be added to cut 534, down contaminating fungi. 18, Zaias N, Onychomycosis, Archives ofDermatology 1972; 105: 263(b) Non-dermatophytefilamentousfungi. 274, All these fungi are sensitive to cycloheximide so 19, Englis.hM?.Nai\s!ind{ungi. British Journal ofDermatotogy 1976; 94: 697-701, this antibiotic must be omitted from culture
