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CUTANEOUS MYCOLOGY 0733-8635/96 $0.00 + .20

DERMATOPHYTOSIS OF THE FEET

Gayle D. Masri-Fridling, MD

Tinea pedis is the most common fungal tive cultures from 11% versus 31% (7.5%- worldwide, affecting 30% to 70% of 61%) of symptomatic cases.5 the population. It is a disease of civilized humans, having evolved in the late nine- teenth and early twentieth centuries, that pre- PREDISPOSING FACTORS dominantly affects adults, with reportedly an equal male to female in~idence.'~Clinical Several factors can predispose patients to practice, however, suggests a predominance contract tinea pedis, including residence in of male patients. warm climates with high humidity that cause The responsible agents are aerobic fungi sweating of the feet and thereby wash away that grow within the layers of the stratum protective surface lipids. Situations in which corneum in the form of branching hyphae, there are external sources of moisture in the and that lack the ability to penetrate through environment are similar. For example, sol- the keratinized layer into the viable epider- diers marching for long periods in cold and mis and internal structures. The host re- damp trenches have persistently wet feet, fa- sponse to the fungal antigens involves cell- cilitating infection. In addition, mediated immunity, which becomes evident the practice of sharing baths, showers, swim- as the disease is resolving. The feet pose ming pools, and even shoes facilitates the a favorable environment for dermatophyte spread of infection. Rugs, linen, and clothing proliferation owing to their lack of sebaceous can act as fomites. Shoes themselves, through glands that produce fungistatic 1i~ids.l~ occlusion, are responsible for the develop- Fungi can be recovered on culture of 9% to ment of tinea pedis because the disease does 21% of clinically normal toe web^.^ Resilient not occur in civilizations where shoes are not spores can survive long periods in unfavor- worn. Plastic shoes especially render the able environments.8 vulnerable because they are conducive to fun- Although occurs primar- gal growth and make infection of the skin ily in the adult population, it has also been more likely. documented, though less frequently, in the Patients with generalized immune defi- pediatric population. The magnitude of the ciency, such as diabetics and those with HIV problem is shown by several large studies disease, are at increased risk for tinea pedis. that revealed positive cultures in 2.9% to 8.2% It is the third most common cutaneous fungal of asymptomatic children and have found infection in HIV.* One possible explanation tinea pedis to account for approximately 50% for the high incidence in HIV is the lack of of symptomatic cases (Fig. 1).6,11Similar stud- CD, lymphocytes to aid in cell-mediated im- ies in asymptomatic adults demonstrate posi- munity. Atopics can also develop chronic

From the Department of , The George Washington University Medical Center, Washington, DC

DERMATOLOGIC CLINICS

VOLUME 14 0 NUMBER 1 *JANUARY 1996 33 34 MASRI-FRIDLING

Figure 1. Tinea pedis in a child.

tinea pedis owing to a lack of cell-mediated erosions beneath and can extend to both the immunity to specific , whereas toes and soles (Fig. 2). Hyperhidrosis is com- the rest of their cell-mediated immunity re- monly found. Pruritus and a foul odor may mains intact. Furthermore, of the be associated features. This compilation of toenails or soles can behave as reservoirs har- findings is referred to as ”dermatophytosis boring spores that can produce numerous re- simplex,” a term coined by Leyden and Klig- currences. man at the University of Pennsylvania. When this uncomplicated form is superinfected by bacteria, specifically lipophilic diphtheroids, CLINICAL FEATURES that are able to gain entry through a defective stratum corneum previously acted on by der- There are three well-accepted clinical pre- matophytes, it is transformed into ”dermato- sentations of tinea pedis, based primarily on phytosis c~mplex.”~ the offending organism, summarized in Table The second or vesicobullous form is gener- 1. The first type is intertriginous/interdigital, ally subacute and often occurs superimposed the chronic form. The fourth to fifth in- on a background of mild simple infection. terspace is most commonly affected, followed With each relapse, there is thickening of the by the third to fourth. The skin involved ap- soles, secondary infection, itch, and macera- pears white and macerated with weepy red tion.13 Vesicles or vesicopustules, in the pres-

Table 1. CLINICAL PRESENTATIONS OF TINEA PEDIS Clinical Type Agent Presentation Symptoms Associated Features Intertriginous, T. rubrum Chronic Hyperhidrosis, Maceration, erosions, 4th interdigital T. mentagrophytes pruritus, to 5th toe web E. floccosum odoriferous Vesicobullous T. mentagrophyfes Subacute on Secondary Vesicles and pustules k background of infection, itch fissures, extend out chronic mild from web space infection Moccasin T. rubrum Chronic Branny scale over sole E. floccosum possible and sides of feet DERMATOPHYTOSIS OF THE FEET 35

Additional etiologic agents in order of de- creasing frequency include men- tagrophytes and jloccosum. One study yielded positive cultures for T. rubrum in 76%, T. mentagrophytes in 17%, and E. jloc- cosum in 1%;Candida was responsible for 6% of infections.12 Elewski has reported Tricho- phyton tonsurans as another possible given its presence in the epidemic number of cases of . Because each of these pathogenic dermatophytes is anthropophilic (T. mentagrophytes var mentagrophytes is zoo- philic but var interdigitale is anthropophilic), they can be spread easily among people. The moccasin form, though predominantly attributed to T. rubrum, can also be caused by E. j7occosum. It is the most common tinea infection in the HIV-positive population, owing almost exclusively to T. rubrum.* The interdigital presentation can result from infec- tion with any of the three common dermato- Figure 2. Intertriginoushnterdigitaltinea. phytes and can involve Candidu albicuns as well, whereas the vesicular type is typically induced by T. mentagrophytes. A virulent form ence or absence of fissures, extend from the manifesting itself with ulcers, pustules, and web space to the dorsum of the foot and rapid extension is due to Trichophyton menta- soles, and especially the arches and lateral grophytes var rnent~grophytes.'~As alluded to aspect of the feet (Fig. 3). The vesicular fluid previously, infections can also be mixed and is initially clear but can change in the pres- include Cundida and bacteria, especially noted ence of such complications as lymphangitis, in the interdigital type. lymphadenitis, or cellulitis. The final presentation is the squamous or hyperkeratotic form, also referred to as the moccasin type. It presents as branny, furfura- ceous scale, with silvery white flakes on a red thickened base distributed over the sole, heel, and sides of the feet, and tends to be chronic (Fig. 4). It can appear patchy and discrete or confluent and can affect the nails as well. Symptoms may or may not be apparent. The moccasin type of tinea pedis can be seen in patients with atopic who also have a negative trichophyton test result to the fun- gus. The chronic forms of tinea can also be man- ifested as "two foot one ," involving the palm of one hand in addition to the soles of both feet (Fig. 5).

ETIOLOGY

Trichophyton rubrum is the most commonly isolated dermatophyte involved in tinea pe- dis, although any dermatophyte can be re- sponsible. T. rubrum can give rise to all types of infection, except for the vesiculous type. Figure 3. Vesicobullous form. 36 MASRI-FRIDLING

Figure 4. Moccasin type of tinea.

Infections that closely resemble those ~ion.~Scytalidium dimidiatum (formerly Hen- caused by the dermatophytes can be caused dersonula torloidea) and Scytalidium hyalinum by nondermatophyte saprophytic can result in both tinea pedis and onycho- found in soil, air, water, and on fomites. They . Interdigital and moccasin type infec- are referred to as dermatomycoses because tions occur, as can ”two foot one hand” they mimic dermatophyte infections. These tinea.4,l2 These saprophytic molds can also agents rarely affect skin and and are coexist with the dermatophytes and both can most likely contracted by direct transmis- be pathogenic. S. dimidiatum is endemic in

Figure 5. Two foot, one hand tinea DERMATOPHYTOSIS OF THE FEET 37 the western and southeastern United States, With progression of symptomatology and California, Washington, Canada, South Amer- infection, it becomes more and more difficult ica, the Caribbean, Africa, India, and the Far to isolate the offending dermatophyte source East.4 S. hyalinum has not yet been cultured on culture. A study performed in 1978 by from the environment but may be endemic in Leyden and Kligman revealed that in derma- the southeastern United States given the case tophytosis simplex cultures were positive for reports from patients originating in those ar- dermatophyte in 84.6% for T. rubrum and T. eas. Scopulariopsis, , and mentagrophytes. Moderate dermatophytosis are additional fungal that are able to complex showed dermatophytes present in produce infections that mimic classic tinea 56%, decreasing further to a low 36% in se- pedis. vere dermatophytosis complex. At the same Organisms that can be cultured from nor- time, cultures for Proteus and other gram- mal toe webs include such microflora as Mi- negative bacteria increased respectively from crococcae (staph), aerobic coryneforms, and a 12% to 35% and 18% to 65%. The incidence few gram-negative bacteria. The interspaces of Staphylococcus aureus increased as well can also be colonized by dermatophytes and from 8% to 11%.9 such as Candida. Once the stratum cor- The dermatophytes produce penicillin and neum barrier is disrupted by dermatophytes, streptomycin-like antibiotics that then select producing maceration and inflammation, bac- for growth of more resistant bacteria. The teria are able to pr~liferate.~ bacteria in turn elaborate proteolytic en- Other pathogenic dermatophytes include zymes, which increase tissue destruction.* Trichophyton violaceum in the Near East, east- One possible explanation for the elimination ern Europe, the countries of the former Soviet of fungi as disease progresses is the produc- Union, north Africa, and Latin America and tion of compounds that possess anti- much more rarely persicolor, Mi- fungal properties, for example, methanethiol, crosporum canis, and Trichophyton megninii. ethanethiol, and dimethyl sulfide by Micrococ- cus sedentarius and Brevibacterium epidermidis.*

PATHOGENESIS COMPLICATIONS

The dermatophyte functioning as the incit- Gram-negative toe web infections are at the ing agent in these infections is responsible for extreme end of the spectrum of dermato- the destruction of the normal barrier role of phytosis complex. The clinical presentation the stratum corneum. The host response to is one of white macerated interspaces with proliferation of the is to increase painful erosions. These lesions are exudative growth of the basal cell layer of the epider- and odoriferous and can be inflammatory to mis, resulting in scaling and thickening of the point of disability. In these patients cul- the skin.13 Under appropriate environmental tures are most likely to reveal Pseudomonas or circumstances such as occlusion and humid- Proteus (Fig. 6). Antibacterial agents are able ity, local conditions favor overgrowth of to halt progression to symptomatic disease opportunistic bacteria at the expense of the via inhibition of large colony diphtheroid dermatophyte. Initially large colony diph- gr~wth.~ theroids proliferate but increasing severity The (autoeczematization) is a leads to a dominance of gram-negative organ- vesicular, eczematous, or anhidrotic eruption isms. Without the initial invasion of the der- on the fingers, palms, and toes. Tense pruritic matophyte, gram-negative bacteria grow min- vesicles containing clear or cloudy fluid, imally. These changes are manifested as which may or may not be tender, develop progression from an uncomplicated superfi- after a flare of tinea pedis.'O The reaction is cial fungal infection to a much more aggres- due to allergic sensitization from hematoge- sive picture with erosions and maceration of nous spread of fungi or fungal antigens from the web space^.^ Bacterial organisms isolated the primary focus. By definition, fungi can be include Staphylococcus aureus, gram-negative demonstrated at the primary focus on the bacteria such as Pseudomonas and Proteus, feet and not in the secondary focus or ID. Corynebacterium minutissimum, Coynebacterium Although the ID usually occurs on the fingers jeikeium, Brevibacterium epidermidis, and Micro- and , it can be seen on the legs and feet coccus sedent~rius.~, as well. 38 MASRI-FRIDLING

(ScytuIidium dimidiutum and hyulinurn) demon- strates atypical long septate branching hy- phae and mycelia with walls of varying thick- ness and can be confused with typical dermatophytes.’ Standard cultures are performed on Sab- ouraud dextrose agar, which is the standard for judging colony color and morphology. Lactophenol cotton blue tease preparations are used to study morphology after growth of the organism on culture. Saprophytic molds can also be grown on this medium. If chloramphenicol and cycloheximide are added to the media for the inhibition of bacte- ria and molds, respectively, Mycosel agar is produced. The disadvantage of this medium is that growth of pathogenic nondermato- phytes and molds would be inhibited. Pathogenic molds should be suspected in the case of failure of the usual Figure 6. Pseudomoms (gram negative) toe-web infec- tion. treatments and failure of growth on standard cultures in the presence of a positive KOH preparation. Another possible complication is secondary infection by saprophytic molds, which in this case are not primary . The differential diagnosis includes other common entities that can produce scaling, DIAGNOSIS vesicles, or pustules on the feet such as con- tact dermatitis, , , and Direct microscopy is performed with 10% dyshidrosis. Other disorders to consider in- to 20% potassium hydroxide from the scaly clude pustular , acrodermatitis con- advancing border of the lesion. It should be tinua, pustular bacterids, , and lightly heated prior to viewing to enhance secondary syphilis. penetration of the potassium hydroxide The hands should be examined for condi- (KOH). Best viewing conditions occur with tions such as “two foot one hand” tinea, the microscope at a low light intensity and pits or onycholysis for a diagnosis of psoria- the condenser down. Ten or 40 power can be sis, or keratotic copper colored papules on used, looking for septate branching hyphae. the palms for syphilis. A thorough history In the case of vesicular lesions, the top of the should be obtained of exacerbating factors, vesicle should be sliced off and placed on the hyperhidrosis, or family members with simi- glass slide for testing. The KOH preparation lar symptoms. The distribution of the erup- has a sensitivity of 77% and a specificity of tion may be suggestive of a diagnosis such as 62% according to one study on 333 speci- contact dermatitis, with a history of worsen- mens.I2 A negative result does not rule out ing with certain shoes, socks, or medications. the diagnosis, and a positive result, although Additional studies, for example, Wood‘s suggestive, does not completely prove the di- lamp, can be used to diagnose Corynebucte- agnosis either. It will not distinguish der- rium minutissimum by its distinctive coral red matophytes from nondermatophytes (such as fluorescence and Pseudomonas, which fluo- pathogenic saprophytic molds) and Cundida. resces green. Candidu albicuns can exhibit a Chlorozol black E is specific for chitin in fun- Swiss cheese-like punched out appearance to gal cell walls and stains hyphae blue-black. the web space.5 This stain contains DMSO (dimethyl sulfox- ide) and therefore will not require heating. TREATMENT A culture should follow the potassium hy- droxide examination even if it is positive. A General guidelines for the management of KOH preparation of the saprophytic molds tinea pedis begin with maintaining a dry local DERMATOPHYTOSIS OF THE FEET 39 environment and avoiding occlusive footwear iting, abdominal pain, headache, gynecomas- to the extent possible. Socks should be 100% tia, and impotence. These will reportedly re- cotton and changed frequently to prevent solve with discontinuation of the medicine. dampness. Shoes should be alternated so that Newer oral imidazoles show promise, in- they may air dry over 2 to 3 days. Antifungal cluding itraconazole and , and the powder can be used in shoes daily and new oral allylamine . Fixed treat- shower sandals worn at health clubs and ment schedules for these medications are be- other communal bathing facilities or swim- ing reported. Itraconazole has certain advan- ming pools. tages, such as a broad spectrum covering For chronic or recurrent infections patients Cundidu, dermatophyte, and some molds, and may be treated with long-term topical anti- is 10-fold more active than ow- fungal agents on an every other day or twice ing to its increased affinity for fungal cyto- weekly basis. Mild keratolytic agents such as chrome P450.It also demonstrates an affinity Whitfield’s ointment can be substituted for for keratinized tissues, resulting in much noninflammatory asymptomatic infections. higher skin levels than sebum. Side effects, Antibacterial soaps can be recommended in reported in up to 7% include pruritus, , cases of interdigital maceration due to mixed dizziness, sleepiness, nausea and vomiting, bacterial and fungal infection. Finally, abdominal pain, and headache. Reported Burow’s compresses or vinegar soaks can aid treatment schedules have included 100 mg/d in bullous disease or hyperhidrosis with mac- for 2 to 4 weeks, 400 mg/d for 7 days, and eration to dry out toe webs and decrease the 200 mg/d for 1 week per month for 3 to 4 bacterial load. month^.'^ The palms and soles present a unique treat- Oral terbinafine is also a potentially useful ment problem because of the thick horny agent because of its primary fungicidal ef- layer of skin without sebum excretion and fects. It has been used at doses of 250 mg/d minimal sweating. Topical imidazoles such for 2 weeks and symptoms continue to im- as , isoconazole, , and prove off the medication.16 Side effects are ketoconazole inhibit ergosterol biosynthesis, reported in approximately 10% and include which is necessary for fungal cell membranes. gastrointestinal upset, urticaria, pruritus, loss A lack of ergosterol results in a defective and of taste, and elevated liver functions. Both permeable cell membrane. These agents are agents appear to produce results superior to fungistatic only and can be used for chronic ketoconazole, but oral terbinafine is still in infections and to treat mild pruritus or ery- clinical trials in the United States at the time thema. The allylamines such as naftifine and of this writing. terbinafine inhibit fungal squalene epoxidase and are fungicidal. Severe infection requires more than topical SUMMARY antifungal agents. An oral antibiotic may be used with the topical antifungal agent for Tinea pedis is the most common fungal recurrent interdigital infection with bacterial infection. Positive culture results can be ob- involvement, especially Stuphylococcus or tained from both symptomatic and asymp- Pseudornonas superinfection. A more acute tomatic toe webs. Although infection is much presentation of tinea, extensive chronic dis- more likely in adults, it can occur in prepu- ease, or even one that appears resistant to bertal children as well. Predisposition to the topical agents possibly through an inability development of tinea pedis occurs with gen- to penetrate the thick stratum comeum will eralized and in atopic der- require systemic antifungal therapy. The matitis. Cell-mediated immunity is necessary mainstay of therapy had been for to mount a response to the dermatophytes. extensive dermatophyte infection. It does not Most cases are caused by T. rubrurn but have activity against nondermatophytes. can also occur with T. rnentugrophytes and E. Griseofulvin acts on the cell nucleus, an un- j7occosurn. Three general presentations are common site. Problems, however, have devel- noted: interdigital, moccasin, and vesicobul- oped with emerging antifungal resistance lous. Bacterial superinfection can occur once both to this and to ketoconazole, which had the stratum corneum barrier is disrupted. been the second choice owing to reported Complications such as gram-negative toe web idiosyncratic hepatotoxicity. Other potential infections and ID reactions can occur. reported side effects include nausea, vom- Diagnosis should be made through a KOH 40 MASRI-FRIDLING preparation followed by culture. Treatment is dren: Does it occur? J Am Acad Dermatol 19:619- based on the severity of symptoms. General 622, 1988 7. Leyden JJ: Progression of interdigital infections from guidelines for foot care should be followed in simplex to complex. J Am Acad Dermatol 28:S7-11, all cases, and topical antifungal agents can be 1993 applied to chronic forms. More widespread 8. Leyden JL: Tinea pedis pathophysiology and treat- or inflammatory cases may require the addi- ment. J Am Acad Dermatol 31:S31-33, 1994 tion of an oral antifungal and antibiotic. 9. Leyden JJ, Kligman AM: Interdigital athlete’s foot. Arch Dermatol 114:1466-1472, 1978 10. Macura A: Dermatophyte infections. Int J Dermatol 32~313-23, 1993 References 11. Maroon MS, Miller OF bullous tinea pedis in a child. Arch Dermatol 125:1716, 1989 1. Abramson C: Athlete’s foot and onychomycosis 12. Miller MA: Sensitivity and specificity of potassium caused by Hendersonula torloidea. Cutis 46:128-132, hydroxide smears of skin scrapings for the diagnosis 1990 of tinea pedis. Arch Dermatol 129:510-511, 1993 2. Conant MA: The AIDS epidemic. J Am Acad Derma- 13. Odom R: Pathophysiology of dermatophyte infec- to1 31:S47-50, 1994 tions. J Am Acad Dermatol 28:S2-7, 1993 3. Dahl MV: Suppression of immunity and inflamma- 14. Rippon JW: Cutaneous infections: Dermatophytosis tion by products produced by dermatophytes. J Am and . In Medical Mycology. Philadel- Acad Dermatol 28:S19-23, 1993 phia, W.B. Saunders, 1988, pp 218-223 4. Elewski B, Greer D Hendersonula torloidea and Scytali- 15. Saul A, Bonifaz A: Itraconazole in common dermato- dium hyalinum. Arch Dermatol 1271041-1044, 1991 phyte infections of the skin: Fixed treatment sched- 5. Kates SG, Nordstrom KM, McGinley KJ, et al: Micro- ules. J Am Acad Dermatol 23:554-558, 1990 bial ecology of interdigital infections of toe web 16. White JE, Perkins PJ, Evans EGV: Successful 2-week spaces. J Am Acad Dermatol 22:578-582, 1990 treatment with terbinafine for moccasin tinea pedis 6. Kearse H, Miller F: Tinea pedis in prepubertal chil- and tinea manum. Br J Dermatol 125:260-262, 1991

Address reprint requests to Gayle D. Masri-Fridling, MD Department of Dermatology The George Washington University Medical Center 2150 Pennsylvania Avenue, NW Suite 6A406 Washington, DC 20037