A Common Superficial Fungal Infections – A Short Review

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VOL.15 NO.11 NOVEMBER 2010Medical BulletinCommon Superficial Fungal Infections –a Short ReviewDr. King-man HOMBBS (HK), MRCP (UK), FHKCP, FHKAM (Medicine), FRCP (Glasgow, Edin),Dip Derm (London), Dip GUM (LAS)Consultant Dermatologist, Social Hygiene Service, CHPSpecialist in Dermatology and VenereologyDr. Tin-sik CHENGMB, MPhil, MRCP, FHKCP, FHKAM (Medicine)Clinical Assistant Professor (Hon), Dermatology Research Centre,Faculty of Medicine, the Chinese University of Hong KongSpecialist in Dermatology and VenereologyDr. King-man HOIntroductionSuperficial fungal infections of the skin are amongthe most common diseases seen in our daily practice.These infections affect the outer layers of the skin,the nails and hair. In contrary to many of the otherinfections affecting the other organ systems in humans,the fungi may cause dermatological conditions thatdo not involve tissue invasion. On the other hand, theskin surface is the habitat of some of these fungi and isliable to environmental contamination. Therefore, mereisolation of these organisms from clinical specimenstaken from the skin surface is not a sine qua non of theirrole in the disease causation. The main groups of fungicausing superficial fungal infections are dermatophytes,yeasts and moulds.The dermatophytes that usually cause only superficialinfections of the skin are grouped into three genera:Microsporum, Trichophyton, and Epidermophyton. Theycan be classified into three groups according to theirnormal habitats: 1) humans: anthropophilic species2) animals: zoophilic species 3) soil: geophilic species.Dermatophytes grow on keratin and therefore causediseases in body sites wherein keratin is present. Thesesites include the skin surface, hair and nail. Presenceof hyperkeratosis such as palmoplantar keratodermapredisposes to dermatophyte infections. Trichophytonrubrum is the most common cause worldwide forsuperficial dermatophytosis.Yeasts are not inherently pathogenic, but when thehost's cellular defences, skin function, or normal floraare altered, colonisation, infection, and disease canoccur. Candida is a normal inhabitant of the oropharynx,gastrointestinal tract and vagina in some people. Moist,wet conditions favour Candida overgrowth and can leadto superficial infections of the skin. Candida albicans is themost virulent of these organisms, and may cause diseasesof the skin, nails, mucous membranes and viscera.The yeast Malassezia furfur, a skin commensal, can causepityriasis versicolor and pityrosporum folliculitis. Thefungus is also related to seborrhoeic dermatitis thoughtrue infection is not present and its presence on the skinis not a sufficient condition for disease expression. Thepresence of oil facilitates the growth of this organism.Moulds that are also referred as nondermatophytefilamentous fungi are ubiquitous in the environmentbut are not commonly pathogenic in normal hosts. Theyare however not uncommonly isolated from clinicalspecimens for fungal culture. Most of the time, they canDr. Tin-sik CHENGbe regarded as innocent bystanders or contaminants.These organisms sometimes however may have roles indisease causation.Diseases Caused by DermatophytesSpecies from the genera Epidermophyton, Microsporumand Trichophyton are most commonly involved. Speciesfrom the genera Epidermophyton species affect nailsand skin, Microsporum species affect hair and skinwhile Trichophyton species affect hair, nails and skin.Dermatophyte infections are subclassified in Latin namesaccording to the sites of skin involved, e.g. tinea faciei:face; tinea manuum: hands; tinea corporis: glabrousskin, tinea cruris: crural folds; tinea pedis: feet; tineacapitis: scalp; tinea unguium: nails. Infections involvingmore than one site of the integument is not uncommon.It is an axiom to look for infections of other sites whendermatophytosis is found in any one of these sites.Tinea Corporis and VariantsTinea corporis, the classic 'ringworm', is a dermatophyteinfection of the glabrous skin of the trunk and extremities.Common causes are T. rubrum and T. mentagrophytes.The typical lesions are pink-to-red annular or arciformpatches and plaques with scaly or vesicular borders thatexpand peripherally with a tendency for central clearing.Inflammatory follicular papules may be present at theactive border. Sometimes, when the follicular epitheliumis grossly involved resulting in folliculitis, it is known asMajocchi’s granuloma.Topical steroids are often prescribed for skin rash.Sometimes, they are wrongly prescribed for tinea. Thepresentations of the fungal infections are changed asthe inflammatory response is decreased leading to thecondition known as tinea incognito. The well definedmargins and scaling may be absent while diffuseerythema and scales, papules and pustules may be found.When the face is affected, it is called tinea faciei. Thetypical annular lesions with peripheral scaling arefrequently absent. The clinical clue is the presence ofred borders which are faintly demarcated, serpiginousand involving only one side of the face.Tinea PedisTinea pedis occurs in four main patterns: interdigital,moccasin, ulcerative and vesiculobullous. In theinterdigital type, erythema, scaling and maceration with23

VOL.15 NO.11 NOVEMBER 2010Medical Bulletinfissures are found in the web spaces, in particular, theweb space between the 4th and 5th toes. This type isusually associated with T. rubrum or T. mentagrophytes.Diffuse scaling on the soles extending to the sides of thefeet is found in the moccasin type, usually caused by T.rubrum. Genetic predisposition is proposed to explainthe strong family history and recalcitrant nature of thistype of tinea pedis.The ulcerative type, usually caused by T. mentagrophytesvar. interdigitale, typically begins in the two lateralinterdigital spaces and extends to the lateral dorsumand the plantar surface of the arch. The lesions of the toewebs are usually macerated and have scaling borders.Secondary bacterial infection is not uncommon whichmay be referred to as mixed toe web infection.In the vesiculobullous type, usually caused by T.mentagrophytes var. interdigitale, vesicular eruptions onthe arch or side of the feet are found. This type maygive rise to the dermatophytid reaction which is aninflammatory reaction at sites distant from the site ofthe associated dermatophyte infection. Pompholyxlike lesions on the hands are the classic dermatophytidreaction.Tinea ManuumTinea manuum may present as diffuse hyperkeratosiswith predilection to the palmar creases of the palms anddigits. White powdery scales along the palmar creasesare typically seen. It may also present as annular lesionslike the typical tinea corporis but on the dorsum ofthe hands or as pompholyx like lesions on the palmaraspect. Infection of only one hand is common andusually occurs in a patient with concomitant tinea pedis.The term ‘two feet and one hand syndrome’ is coined todescribe this interesting condition. Tinea unguium ofthe involved hand might be observed. The typical fungiresponsible for tinea manuum are the same as those fortinea pedis and tinea cruris.Tinea CrurisFlexural tinea usually only occurs in the groins anddoes not involve the axillae or submammary folds. Theinfection occurs more in males. It begins in the cruralfolds and may extend to the thighs, buttocks and glutealcleft area. Scrotal infection alone is rare. Infection isnearly always from the patient’s own feet and is causedby the same organisms as those causing tinea pedis.Tinea UnguiumBoth dermatophytes and non-dermatophytes cancause onychomycosis. Less than 10% of cases ofonychomycosis are due to yeasts or non-dermatophytemoulds, while dermatophytes account for approximately90% of cases. Toenail infections are more commonthan fingernail infections and are usually found alongwith tinea pedis. The main causative dermatophytesare T. rubrum, T. mentagrophytes and E. floccosum. Theclinical presentations of onychomycosis are as follows:1) distal and lateral subungual onychomycosis (DLSO):it is the most common type, usually caused by T.rubrum. Discolouration, subungual hyperkeratosis and24distal onycholysis start at the hyponychium spreadingproximally. 2) proximal subungual onychomycosis(PSO): the dermatophytes invade the nail unit underthe proximal nail fold and spread distally. It is usuallycaused by T. rubrum and is usually associated withimmunosuppressed conditions, e.g. HIV infection. 3)superficial white onychomycosis (SWO): the fungi,mainly T. mentagrophytes, directly invade the superficiallayers of the nail plate but do not penetrate it leadingto a white, crumbly nail surface. 4) total dystrophiconychomycosis.Tinea CapitisTinea capitis usually occurs predominantly inprepubertal children. It can be acquired from infectedpuppies and kittens and by close contact with infectedchildren. The three most common dermatophytescausing tinea capitis are Trichophyton tonsurans,Microsporum canis and Microsporum audouinii. Thecausative agent varies in different geographical areas.In the USA and in some cities in the UK, T. tonsurans isthe most common cause. In Hong Kong, tinea capitis isusually caused by M. canis. Pet exposure is associatedwith infections caused by M. canis.The dermatophytes can invade hair in three patterns:ectothrix, endothrix and favus. Arthroconidia are foundaround the hair shaft in ectothrix infections and withinthe hair shaft in endothrix infections. Hyphae and airspaces are found within the hair shafts in favus. Manyfungi producing a small spore ectothrix pattern andT. schoenleinii, which causes endothrix infection, willshow fluorescence under Wood’s light because of thepresence of pteridine.Tinea capitis can present in the following patterns:seborrhoeic pattern, black-dot pattern, kerion and favus.In the seborrhoeic pattern, dandruff-like scaling is foundon the scalp. Prepubertal children presenting withsuspected seborrhoeic dermatitis on the scalp should bepresumed to have tinea capitis until proven otherwise.In the black dot pattern, patchy alopecia with blackstumps of broken hair shaft due to breakage of hair nearthe scalp are found. In kerion, boggy masses coveredwith pustular folliculitis are found and scarring mayensue afterwards. In favus, most frequently caused by T.schoenleinii, yellow saucer-shaped adherent crusts madeup of hyphae and spores occur around the hairs.Fungal culture and species identification provideadditional information for patient management.Zoophilic dermatophytes, M. canis, may have an animalsource and therefore the pets should be examinedby veterinary surgeons for the presence of similarinfections. Anthropophilic dermatophytes, T. tonsurans,should prompt the attending physician to look forinfections of the household or institutional contactsor even institutional outbreaks. Mild infections andasymptomatic carriers with positive fungal culture butno clinical signs can be found in tinea capitis, especiallyin T. tonsurans infections. The carriers are consideredinfectious as they shed the fungus. Institutionaloutbreaks are however very uncommon in Hong Kong.

VOL.15 NO.11 NOVEMBER 2010Diseases Caused by YeastsCandidiasisCandida species are capable of producing skin andmucous membrane infections. However, cutaneouscandidosis is less common than dermatophytosis. Thereare about two hundred species in the genus Candidaand about twenty of them are associated with human oranimal infections, e.g. C. albicans, C. tropicalis, C. glabrata,C. parapsilosis, C. krusei, C. guilliermondii, with C. albicansaccounting for most of the infections.1 A decrease inthe prevalence of C. albicans as a cause of infection andan increase in non-albicans Candida (NAC) such as C.glabrata, C. krusei, and C. parapsilosis was found in thelast decade. It could possibly be due to the extensiveuse of azole drugs, such as fluconazole, which led tothe emergence of those non-albicans species such as C.glabrata or C. krusei, with inherent lower sensitivity toazoles.The organisms can exist as commensal flora but becomepathogenic in various predisposed conditions e.g.infancy, pregnancy, moist and occluded sites, diabetes,Cushing’s syndrome, immunosuppression, imbalancein the normal microbial flora, etc. The yeast infectsonly the outer layers of skin and mucous membrane inmucocutaneous candidosis.Skin and Intertriginous InfectionsIn the skin, pustules are formed which dissect underthe stratum corneum peeling it away resulting in a red,denuded, glistening surface with a long, cigarette paperlike, scaling and advancing border. Pustules rupture toform a superficial collarette of scales. The infection isusually found in the intertriginous skin folds and othermoist, occluded sites, e.g. webspaces, genital area andarea covered by diaper. Intertriginal candidal infectionsaffect all flexures, e.g. the groins, axillae, finger and toewebs. The rash is red, macerated and well demarcatedand surrounded by satellite papules and pustules. Afringe of moist scale might be found at the border.The rash may be sore rather than itchy. In diaperdermatitis caused by Candida, bright red plaques in theinguinal and gluteal folds and satellite pustules may befound. Candidal infection is a frequent cause of chronicparonychia, manifesting as painful periungual erythemaand swellings associated with secondary nail thickening,ridging and discolouration.Infections of the Mucosae and MucocutaneousJunctionOropharyngeal candidiasis causes white plaques andpustules on the oral mucosal surface that leave a raw,bleeding base when removed mechanically. Medianrhomboid glossitis is associated with Candida infection.Candida sp may cause angular cheilitis which ispredisposed in drooling and edentulous elderly patients.Candidal balanitis is more commonly found in theuncircumcised and usually presents with red patches,swelling and tiny pustules. In candidal vulvovaginitis,usually causing itchiness and soreness, a curd-likedischarge, pustules, erythema and oedema of the vaginaand vulva are found. Pruritus ani and macerations areusually found in perianal candidiasis.Chronic Mucocutaneous CandidiasisMedical BulletinChronic mucocutaneous candidiasis is a clinical entityassociated with a heterogeneous group of autoimmune,immunologic and endocrinologic diseases which ischaracterised by recurrent or persistent superficialcandidal infections due to an impaired cell-mediatedimmunity against Candida species. This is a clinicalsituation wherein true candidal infection of the nail ispresent.Malassezia InfectionsThe genus Malassezia comprises a group of lipophilicyeasts that have their natural habitat on the skin ofhumans and different warm-blooded animals. Thegeographic distribution of Malassezia species isworldwide. Since the taxonomic revision in 1996,the genus Malassezia was enlarged to comprise sevendifferent species. They are part of the normal floraof human skin and M. sympodialis is the predominantspecies. Pityriasis versicolor is the only human disease inwhich the causative role of the lipophilic yeast Malasseziais fully established. Malassezia has been implicatedin several other skin diseases, including seborrhoeicdermatitis, atopic dermatitis and folliculitis. However,the role of these yeasts in these entities is controversial.Pityriasis VersicolorPityriasis versicolor occurs most frequently in hot andhumid tropical climates. However, it is also prevalent intemperate climates. The fact that Malassezia has an oilrequirement for growth explains the increased incidencein adolescents and the predilection for sebum-rich areasof the skin. Pityriasis versicolor occurs when the buddingyeast form transforms to the mycelial form. Variousfactors have been implicated, including hot and humidenvironment, oily skin and excessive sweating. Becausethis yeast is lipophilic, use of bath oils and skin lubricantsmay enhance disease development.The lesions consist of multiple white, pink to brown,oval to round coalescing macules and patches withmild and fine scaling mainly found on the seborrhoeicareas, in particular, the upper trunk and shoulders.Lesions can also be found on the face, scalp, antecubitalfossae, submammary regions and groins. The lesionsoften become confluent and quite extensive. Whenpityriasis versicolor involves the flexural areas, it issometimes referred to as ‘inverse’ pityriasis versicolor.Demonstration of the associated scale may requirescratching of the skin surface. The fungus producesdicarboxylic acids, notably azelaic acid, that interfere withmelanin synthesis leading to decreased pigmentation.Decreased tanning, due to the ability of the fungus tofilter sunlight and the screening effect of tryptophandependent metabolites are other factors that explain theabsence of pigmentation in exposed areas.Malassezia (Pityrosporum) FolliculitisThis is characterised by inflammatory follicular papuleslocalised predominantly on the back, chest and upperarms. These inflammatory papules are not uncommonlyquite monomorphic and frank pustule formation is notcommon. Pruritus and the absence of comedones andfacial lesions distinguish it from acne. This conditionis more frequent in tropical countries and in summerin temperate regions and has been associated with25

VOL.15 NO.11 NOVEMBER 2010Medical Bulletinantibiotic treatment e.g. tetracyclines, corticosteroidsand immunosuppression associated with organtransplantation. Scrapings or biopsy specimens showabundant Malassezia yeasts occluding the opening of theinfected follicles. However, as the colonisation of hairfollicles by Malassezia is not abnormal, the diagnosis ofMalassezia folliculitis has to be confirmed by the responseto antifungal therapy: topical treatment is effective inmost cases, whereas others need systemic therapy withazole or triazole.Mould InfectionsMould is ubiquitous in the environment, but pure mouldinfection of the skin is very uncommon. Superficialskin infection may mimic moccasin tinea pedis, tineamanuum, and tinea unguium.Principles of Laboratory Diagnosis ofSuperficial Fungal InfectionsClinical diagnosis is usually good enough for the routinemanagement of patients. If laboratory confirmation isdeemed required, the following principles should beborne in mind. As cutaneous diseases associated withthese fungi may or may not have genuine tissue invasion,and skin surface is the habitat of some of these fungi andthe skin surface is liable to environmental contamination,mere isolation of some of these fungi from clinicalspecimens taken from the skin surface is not a sine qua nonof their role in disease causation. The laboratory approachto these cutaneous conditions may involve answeringthe following 3 questions: 1) what is the purpose ofperforming the laboratory tests under consideration? 2)which is the most appropriate laboratory test? 3) how tointerpret the laboratory results in the concerned clinicalcontext? To better inform the laboratory microbiologists,it is prudent to provide the essential clinical informationand specify the organisms of interest on the requestform. The laboratory diagnostic approach will involve1) wet mount KOH examination that can be performedrapidly at the “bed-side” with or without staining (e.g. byParker’s blue black ink, chlorazole black), 2) culture forproper species identification.The scales from active lesions produced by skin scrapingcan be collected and wrapped in colour paper (and put ina properly sealed container) and sent to the supportinglaboratory by mail. Cleansing of the site may be requiredin those grossly contaminated sites such as from a “dirty”foot before performing skin scraping.Diseased hairs should be plucked (not cut) in those casesof suspected tinea capitis. Scraping of diseased scalpskin for fungal study is the recommended approach ofthe British Association of Dermatologists.2 Specimencollection by cytobrush or toothbrush are alternativemethods of sample collection especially in the contextof outbreak investigation.2, 3 As aforementioned, speciesidentification in tinea capit

a Short Review Dr. King-man HO Dr. Tin-sik CHENG Dr. King-man HO Dr. Tin-sik CHENG Introduction Superficial fungal infections of the skin are among the most common diseases seen in our daily practice. These infections affect the outer layers of the s

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