- Email: [email protected]
The Necessity of Culture for the Diagnosis of Tinea Pedis
The Necessity of Culture for the Diagnosis of Tinea Pedis TALAT ECEMIS, MD; KENAN DEGERLI, MD; ERDINC AKTAS, MD; ASLI TEKER, MD; BERIL OZBAKKALOGLU, MD
ABSTRACT: Background: This study examined the consistency between the clinical diagnosis of tinea pedis and the results of direct fungal examination, prepared with 10% potassium hydroxide, and culture. Methods: 2427 patients clinically diagnosed with tinea pedis who presented to the mycology laboratory were reviewed retrospectively for the outcomes of direct fungal examination and culture. Results: Direct examination was positive in 54.3% and culture was positive in 36.6% of the cases. The sensitivity and
specificity of direct microscopy were 95.7% and 69.6%, respectively Conclusions: The clinical diagnosis of tinea pedis can be misleading, since it features lesions that can also be present in some other skin diseases and direct microscopy may be insufficient to confirm the diagnosis. Therefore, we suggest using culture for a definitive diagnosis. KEY INDEXING TERMS: Tinea pedis; Clinical diagnosis; Direct examination; Dermatophyte. [Am J Med Sci 2006;331(2):88–90.]
T
study was to examine, retrospectively, the consistency between the clinical diagnosis of tinea pedis and laboratory results.
inea pedis is a common superficial fungal infection in humans, mainly caused by the anthropophilic dermatophytes, in particular Trichophyton rubrum, Trichophyton mentagrophytes, and Epidermopyhon floccosum. Tinea pedis usually takes one of several forms and in about 5% of cases there is mixed infection.1 The most common clinical manifestation is the intertriginous form, which manifests with maceration, peeling, and fissuring, mainly in the spaces between the fourth and fifth toes. Another common form is the chronic squamous, hyperkeratotic type in which fine silvery scales cover erythematous skin of the soles, heels, and sides of the foot (moccasin foot). An acute inflammatory condition characterized by the formation of vesicles, pustules, and sometimes bullae can also be seen.2 However, these clinical forms, especially the first two, are not always caused by dermatophytes; erythrasma, eczema, psoriasis, dyshydrosis, atopic dermatitis, keratoderma, and soft corns can all cause diagnostic difficulty.3,4 The confusion between tinea pedis and other entities can be experienced by physicians, especially nondermatologists.5 In addition to this confusion, unsuitable treatment not only can delay the initiation of a proper treatment but also can place a financial burden on the patient and/or healthcare system. Therefore, the purpose of this From the Celal Bayar University, Faculty of Medicine, Department of Microbiology and Clinical Microbiology, Manisa, Turkey. Submitted for publication March 3, 2005; accepted for publication August 7, 2005. Correspondence: Talat Ecemis, MD, Celal Bayar Universitesi, Tip Fakultesi Dekanligi, Mikrobiyoloji ve Klinik Mikrobiyoloji, 45030, Uncubozkoy/Manisa, Turkey (E-mail: [email protected]).
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Methods The case reports of 2427 patients, who presented to the Mycology Laboratory at Celal Bayar University Faculty of Medicine, Manisa, Turkey with suspected tinea pedis in 1999 through 2003, were reviewed retrospectively for the outcomes of direct fungal examination and culture. Patients with a clinical diagnosis other than tinea pedis were not included in the study. Age was not an inclusion or exclusion criteria. The standard procedures for skin lesions at the Mycology Laboratory were followed: getting samples from suitable regions by skin scraping, preparing the sample with 10% potassium hydroxide (KOH), and direct microscopic examination of the sample. Patients who used topical antifungal agents within the past 2 weeks or an oral antifungal agent within the past 1 month before the culture were not included. For the isolation of the dermatophytes, Saboraud dextrose agar and potato dextrose agar, with or without chloramphenicol and gentamycin, were used. Cultures were incubated at 26 to 37°C for up to 30 days and checked twice weekly for growth. Negative cultures were confirmed after 4 weeks of no growth. The identification of dermatophyte isolates was on the basis of colonial and microscopic morphology, lactophenol cotton blue stain, tape lift, urease testing, and hair perforation test.6 SPSS v11.0 statistical package was used to analyze the data.
Results Within the 5-year period, the department of dermatology referred 2075 of the 2427 patients (85.4%) for whom direct examination and culture were requested. The remaining 352 patients were referred from different clinics. The ages of the patients ranged from 1 to 95 years, with a mean of 46.5 years. Males comprised 52.5% of the patients and females 47.5%. Samples were taken from the space between February 2006 Volume 331 Number 2
Diagnosis of Tinea Pedis
Table 1. Result of Direct Microscopy and Growth in Culture Growth in Culture
Direct microscopy Negative Positive Total
Negative
Positive
Total
1071 467 1538
38 851 889
1109 1318 2427
the toes, the sole, and the dorsum of the foot in 79.7%, 18.6%, and 1.7% of the cases, respectively. Direct examination, after preparation with 10% KOH, was positive in 1318 cases (54.3%) and culture was positive in 889 (36.6%). Among 2427 samples, the number of both direct examination and culture negative cases was 1071 (44.1%) and that of positive cases was 851 (35.1%). We calculated the ratio of the sum of these numbers to the total number of cases and found a consistency of 79.2% between the culture and direct examination. The sensitivity and specificity of direct microscopy was calculated by using culture as the criterion standard. Eight hundred fifty-one positive direct examinations in 889 culture-positive cases and 1071 negative direct examinations in 1538 culture-negative cases yielded 95.7% sensitivity and 69.6% specificity (Table 1). The most commonly isolated dermatophyte in cultures, found in 822 cases (92.5%), was Trichophyton rubrum. Trichophyton mentagrophytes, Epidermophyton floccosum, and Microsporum canis were responsible in 52 (5.8%), 6 (0.7%), and 5 patients (0.6%), respectively. Discussion The results of this study show that a dermatophyte grew on cultures in only 36.6% of the cases with a clinical diagnosis of tinea pedis. This ratio is quite close to the 32% that was calculated by Fuchs and colleagues.5 Even though the majority of our cases were referred by a dermatologist, in line with the health care system in Turkey, they are usually seen initially by a primary care physician, usually a general practitioner, and tinea pedis tops the list of their differential diagnosis. Many physicians in primary care centers, even in hospitals with a mycology laboratory, do not request a culture and regard direct examination as sufficient. Furthermore, many primary care physicians make a diagnosis just by clinical findings and initiate treatment. Many are in favor of such approach, arguing that culture is expensive and time consuming and therefore it is not needed in day-to-day practice.7,8 We found the ratio of false-positive results for direct examination as 30.4% and false-negative reTHE AMERICAN JOURNAL OF THE MEDICAL SCIENCES
sults as 4.3%. Although it is evident that our negative direct examination results are reliable, as high a false-positive result as 30.4% highlights the need for culture. These results vary among laboratories, and higher false-positive (41%) and false-negative (15%) ratios have been reported.9 The biggest disadvantage of the direct examination is its subjectivity. Various factors (dead or nonviable mycotic organisms, artifacts, or mosaic crystals) contribute to the high false-positive results. In our laboratory, a sample was assessed by an experienced technician and a consultant physician. In the situation of a doubtful case, an opinion from a second consultant was obtained. Assessment of the direct examination by experienced staff has a major contribution in low false-negative results. However, an experienced person is not always available in the primary care centers in which a patient presents with tinea-pedislike clinical symptoms and entails the use of an objective diagnostic method, culture. Since an agent grew on culture from only 36.6% of the patients referred with a clinical diagnosis of tinea pedis, and there was a consistency between direct examination and culture in 79.2% of the cases, there would be an overall 20.8% margin of error if the assessment of the patient were based on direct examination of the specimen in KOH only. Clinical symptoms of tinea pedis can be a deceptive and insufficient diagnostic value of the direct examination in KOH compared to culture necessitates employing culture in tinea pedis patients. The major disadvantage of the culture is the time it takes to get the results, which is at least 3 weeks. Treatment can be initiated in patients with positive direct examination but culture is necessary for the follow-up and outcome. The cost of the culture should not be taken as a financial burden, since the cost of an inappropriate treatment far exceeds the cost of the culture and results in loss of time. Acknowledgments The authors thank Enis Cezayirli, Shannon Rose Mavi, and Hasan Mavi for linguistic consultations and contributions. References 1. Lacroix C, Baspeyras M, de La Salmoniere P, et al. Tinea pedis in European marathon runners. J Eur Acad Dermatol Venereol 2002;16:139–42. 2. Weitzman I, Summerbell RC. The dermatophytes. Clin Microbiol Rev 1995;8:240–59. 3. Smith AG. Skin infections of the foot. Foot 1999;9:56–9. 4. Gupta AK. Uncommon localization or presentation of tinea infection. J Eur Acad Dermatol Venereol 2001;15:7–8. 5. Fuchs A, Fiedler J, Lebwohl M, et al. Frequency of cultureproven dermatophyte infection in patients with suspected tinea pedis. Am J Med Sci 2004;327:77–8.
89
Ecemis et al
6. Foster KW, Ghannoum MA, Elewski BE. Epidemiologic surveillance of cutaneous fungal infection in the United States from 1999 to 2002. J Am Acad Dermatol 2004;50: 748–52. 7. Noble SL, Forbes RC, Stamm PL. Diagnosis and management of common tinea infections. Am Fam Physician 1998;58:163-78.
90
8. Weinstein A, Berman B. Topical treatment of common superficial tinea infections. Am Fam Physician 2002;65:2095– 102. 9. Porres J. Natural history of tinea pedis. Available at http:// www.fda.gov/ohrms/dockets/ac/04/slides/4036S1_01_ A-FDA-Porres.ppt. Accessed January 6, 2005.
February 2006 Volume 331 Number 2
ABSTRACT: Background: This study examined the consistency between the clinical diagnosis of tinea pedis and the results of direct fungal examination, prepared with 10% potassium hydroxide, and culture. Methods: 2427 patients clinically diagnosed with tinea pedis who presented to the mycology laboratory were reviewed retrospectively for the outcomes of direct fungal examination and culture. Results: Direct examination was positive in 54.3% and culture was positive in 36.6% of the cases. The sensitivity and
specificity of direct microscopy were 95.7% and 69.6%, respectively Conclusions: The clinical diagnosis of tinea pedis can be misleading, since it features lesions that can also be present in some other skin diseases and direct microscopy may be insufficient to confirm the diagnosis. Therefore, we suggest using culture for a definitive diagnosis. KEY INDEXING TERMS: Tinea pedis; Clinical diagnosis; Direct examination; Dermatophyte. [Am J Med Sci 2006;331(2):88–90.]
T
study was to examine, retrospectively, the consistency between the clinical diagnosis of tinea pedis and laboratory results.
inea pedis is a common superficial fungal infection in humans, mainly caused by the anthropophilic dermatophytes, in particular Trichophyton rubrum, Trichophyton mentagrophytes, and Epidermopyhon floccosum. Tinea pedis usually takes one of several forms and in about 5% of cases there is mixed infection.1 The most common clinical manifestation is the intertriginous form, which manifests with maceration, peeling, and fissuring, mainly in the spaces between the fourth and fifth toes. Another common form is the chronic squamous, hyperkeratotic type in which fine silvery scales cover erythematous skin of the soles, heels, and sides of the foot (moccasin foot). An acute inflammatory condition characterized by the formation of vesicles, pustules, and sometimes bullae can also be seen.2 However, these clinical forms, especially the first two, are not always caused by dermatophytes; erythrasma, eczema, psoriasis, dyshydrosis, atopic dermatitis, keratoderma, and soft corns can all cause diagnostic difficulty.3,4 The confusion between tinea pedis and other entities can be experienced by physicians, especially nondermatologists.5 In addition to this confusion, unsuitable treatment not only can delay the initiation of a proper treatment but also can place a financial burden on the patient and/or healthcare system. Therefore, the purpose of this From the Celal Bayar University, Faculty of Medicine, Department of Microbiology and Clinical Microbiology, Manisa, Turkey. Submitted for publication March 3, 2005; accepted for publication August 7, 2005. Correspondence: Talat Ecemis, MD, Celal Bayar Universitesi, Tip Fakultesi Dekanligi, Mikrobiyoloji ve Klinik Mikrobiyoloji, 45030, Uncubozkoy/Manisa, Turkey (E-mail: [email protected]).
88
Methods The case reports of 2427 patients, who presented to the Mycology Laboratory at Celal Bayar University Faculty of Medicine, Manisa, Turkey with suspected tinea pedis in 1999 through 2003, were reviewed retrospectively for the outcomes of direct fungal examination and culture. Patients with a clinical diagnosis other than tinea pedis were not included in the study. Age was not an inclusion or exclusion criteria. The standard procedures for skin lesions at the Mycology Laboratory were followed: getting samples from suitable regions by skin scraping, preparing the sample with 10% potassium hydroxide (KOH), and direct microscopic examination of the sample. Patients who used topical antifungal agents within the past 2 weeks or an oral antifungal agent within the past 1 month before the culture were not included. For the isolation of the dermatophytes, Saboraud dextrose agar and potato dextrose agar, with or without chloramphenicol and gentamycin, were used. Cultures were incubated at 26 to 37°C for up to 30 days and checked twice weekly for growth. Negative cultures were confirmed after 4 weeks of no growth. The identification of dermatophyte isolates was on the basis of colonial and microscopic morphology, lactophenol cotton blue stain, tape lift, urease testing, and hair perforation test.6 SPSS v11.0 statistical package was used to analyze the data.
Results Within the 5-year period, the department of dermatology referred 2075 of the 2427 patients (85.4%) for whom direct examination and culture were requested. The remaining 352 patients were referred from different clinics. The ages of the patients ranged from 1 to 95 years, with a mean of 46.5 years. Males comprised 52.5% of the patients and females 47.5%. Samples were taken from the space between February 2006 Volume 331 Number 2
Diagnosis of Tinea Pedis
Table 1. Result of Direct Microscopy and Growth in Culture Growth in Culture
Direct microscopy Negative Positive Total
Negative
Positive
Total
1071 467 1538
38 851 889
1109 1318 2427
the toes, the sole, and the dorsum of the foot in 79.7%, 18.6%, and 1.7% of the cases, respectively. Direct examination, after preparation with 10% KOH, was positive in 1318 cases (54.3%) and culture was positive in 889 (36.6%). Among 2427 samples, the number of both direct examination and culture negative cases was 1071 (44.1%) and that of positive cases was 851 (35.1%). We calculated the ratio of the sum of these numbers to the total number of cases and found a consistency of 79.2% between the culture and direct examination. The sensitivity and specificity of direct microscopy was calculated by using culture as the criterion standard. Eight hundred fifty-one positive direct examinations in 889 culture-positive cases and 1071 negative direct examinations in 1538 culture-negative cases yielded 95.7% sensitivity and 69.6% specificity (Table 1). The most commonly isolated dermatophyte in cultures, found in 822 cases (92.5%), was Trichophyton rubrum. Trichophyton mentagrophytes, Epidermophyton floccosum, and Microsporum canis were responsible in 52 (5.8%), 6 (0.7%), and 5 patients (0.6%), respectively. Discussion The results of this study show that a dermatophyte grew on cultures in only 36.6% of the cases with a clinical diagnosis of tinea pedis. This ratio is quite close to the 32% that was calculated by Fuchs and colleagues.5 Even though the majority of our cases were referred by a dermatologist, in line with the health care system in Turkey, they are usually seen initially by a primary care physician, usually a general practitioner, and tinea pedis tops the list of their differential diagnosis. Many physicians in primary care centers, even in hospitals with a mycology laboratory, do not request a culture and regard direct examination as sufficient. Furthermore, many primary care physicians make a diagnosis just by clinical findings and initiate treatment. Many are in favor of such approach, arguing that culture is expensive and time consuming and therefore it is not needed in day-to-day practice.7,8 We found the ratio of false-positive results for direct examination as 30.4% and false-negative reTHE AMERICAN JOURNAL OF THE MEDICAL SCIENCES
sults as 4.3%. Although it is evident that our negative direct examination results are reliable, as high a false-positive result as 30.4% highlights the need for culture. These results vary among laboratories, and higher false-positive (41%) and false-negative (15%) ratios have been reported.9 The biggest disadvantage of the direct examination is its subjectivity. Various factors (dead or nonviable mycotic organisms, artifacts, or mosaic crystals) contribute to the high false-positive results. In our laboratory, a sample was assessed by an experienced technician and a consultant physician. In the situation of a doubtful case, an opinion from a second consultant was obtained. Assessment of the direct examination by experienced staff has a major contribution in low false-negative results. However, an experienced person is not always available in the primary care centers in which a patient presents with tinea-pedislike clinical symptoms and entails the use of an objective diagnostic method, culture. Since an agent grew on culture from only 36.6% of the patients referred with a clinical diagnosis of tinea pedis, and there was a consistency between direct examination and culture in 79.2% of the cases, there would be an overall 20.8% margin of error if the assessment of the patient were based on direct examination of the specimen in KOH only. Clinical symptoms of tinea pedis can be a deceptive and insufficient diagnostic value of the direct examination in KOH compared to culture necessitates employing culture in tinea pedis patients. The major disadvantage of the culture is the time it takes to get the results, which is at least 3 weeks. Treatment can be initiated in patients with positive direct examination but culture is necessary for the follow-up and outcome. The cost of the culture should not be taken as a financial burden, since the cost of an inappropriate treatment far exceeds the cost of the culture and results in loss of time. Acknowledgments The authors thank Enis Cezayirli, Shannon Rose Mavi, and Hasan Mavi for linguistic consultations and contributions. References 1. Lacroix C, Baspeyras M, de La Salmoniere P, et al. Tinea pedis in European marathon runners. J Eur Acad Dermatol Venereol 2002;16:139–42. 2. Weitzman I, Summerbell RC. The dermatophytes. Clin Microbiol Rev 1995;8:240–59. 3. Smith AG. Skin infections of the foot. Foot 1999;9:56–9. 4. Gupta AK. Uncommon localization or presentation of tinea infection. J Eur Acad Dermatol Venereol 2001;15:7–8. 5. Fuchs A, Fiedler J, Lebwohl M, et al. Frequency of cultureproven dermatophyte infection in patients with suspected tinea pedis. Am J Med Sci 2004;327:77–8.
89
Ecemis et al
6. Foster KW, Ghannoum MA, Elewski BE. Epidemiologic surveillance of cutaneous fungal infection in the United States from 1999 to 2002. J Am Acad Dermatol 2004;50: 748–52. 7. Noble SL, Forbes RC, Stamm PL. Diagnosis and management of common tinea infections. Am Fam Physician 1998;58:163-78.
90
8. Weinstein A, Berman B. Topical treatment of common superficial tinea infections. Am Fam Physician 2002;65:2095– 102. 9. Porres J. Natural history of tinea pedis. Available at http:// www.fda.gov/ohrms/dockets/ac/04/slides/4036S1_01_ A-FDA-Porres.ppt. Accessed January 6, 2005.
February 2006 Volume 331 Number 2