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Clinical, bacteriological, and dermoscopic study of pitted keratolysis

Hodeib, Abeera; Khalil, Haidyb; Hammad, Gehana

Journal of the Egyptian Women's Dermatologic Society: May 2017 - Volume 14 - Issue 2 - p 85–91
doi: 10.1097/01.EWX.0000499600.30709.c2
Original articles
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Background Pitted keratolysis is an acquired superficial infection of the skin. It is characterized by crateriform pitting of the pressure-bearing aspects of the plantar surface of the feet and occasionally in the palms of the hand as a collarette of scales.

Objective To evaluate the role of a dermoscope in the diagnosis of pitted keratolysis and to correlate the dermoscopic diagnosis with bacterial diagnosis.

Patients and methods The current cross-sectional study included 90 patients with pitted keratolysis. They were recruited from Outpatient Clinics of Dermatology and Venereology Department, Tanta University Hospitals. Clinical examination, bacteriological examination, and dermoscopic examination of the feet of the patients were performed.

Results The clinical features of pitted keratolysis were still the gold standard for diagnosis. Crater-like pits by dermoscopic examination as well as Micrococcus sedentarius and Corynebacterium spp. were observed in patients with pitted keratolysis. The Corynebacterium spp. was more prone to develop a crater-like/punched out/pigmented and crater-like/smooth/not pigmented pattern on desmoscopy, whereas the Micrococcus spp. was more prone to develop a crater-like/punched out/pigmented pattern on dermoscopy. There was no statistically significant relation between the dermoscopic criteria and bacteriological results. The dermoscope revealed 100% sensitivity in the diagnosis of pitted keratolysis, whereas the bacterial isolate was detected only from 90% of the clinically diagnosed cases of pitted keratolysis.

Conclusion Dermoscopy is useful in the diagnosis of pitted keratolysis. Bacteriological examination helps to identify the type of organism in the lesion but does not confirm that the lesion in the foot is pitted keratolysis. The type of organism does not correlate with the dermoscopic criteria. Larger-scale studies correlating dermoscopic findings with bacteriological and histopathological results are recommended to improve the understanding of the dermoscopic criteria.

Departments of aDermatology and Venereology

bMicrobiology and Immunology, Tanta University, Tanta, Egypt

Correspondence to Abeer Hodeib, MD, Department of Dermatology and Venereology, Tanta University, Tanta 31527, Egypt Tel: +20 128 216 9139; e-mail: abeerhodeib@hotmail.com

Received May 15, 2017

Accepted August 25, 2017

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Introduction

Pitted keratolysis (also known as keratolysis plantare sulcatum, keratoma plantare sulcatum, and ringed keratolysis) is a noncontagious skin infection caused by wearing tight or restricting footwear and by excessive sweating; it is seen in, for example, army personnel, farmers, and athletes. It is characterized by itching, soreness, pain, and crater-like pits on the surface of the feet and toes, particularly in weight-bearing areas 1,2.

Pitted keratolysis is caused by cutaneous infection with Micrococcus sedentarius (known as Kytococcus sedentarious), Dermatophilus congolensis, or species of Corynebacterium, Actinomyces, or Streptomyces. Under appropriate conditions such as prolonged occlusion hyperhidrosis and increased skin surface pH, these bacteria proliferate and produce proteinases that destroy the stratum corneum, creating pits. The malodor of pitted keratolysis might be due to production of sulfur-compound by-products such as thiols, sulfides, and thioesters 3.

Pitted keratolysis can be diagnosed easily from its unique clinical presentation and characteristic odor. Wood’s ultraviolet light examination is not consistently helpful but the affected area displays a characteristic coral red fluorescence. The organisms may be obtained from the pitted lesions and cultured on brain heart infusion agar nitrogen and carbon dioxide at 37°C. The dermoscopic features of typical pits can confirm its diagnosis 4.

The aim of this study was to evaluate the role of the dermoscope in the diagnosis of pitted keratolysis and to correlate the dermoscopic diagnosis with the bacterial diagnosis.

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Patients and methods

The present cross-sectional study included 90 patients with pitted keratolysis. They were recruited from the Outpatient Clinic of Dermatology and Venereology Department, Tanta University Hospitals. The bacteriological diagnosis was made in the Microbiology and Immunology Department, Faculty of Medicine, Tanta University. Informed consent was obtained from all participants in this study. The study was approved by the research ethics committee of the Faculty. The inclusion criterion was the presence of pitted keratolysis in the patients. Patients who received any systemic or topical treatment for pitted keratolysis not earlier than 6 weeks before the study as well as patients who had other dermatological or systemic diseases were excluded from the study.

All patients were subjected to the following:

  • Full history taking, including age, sex, occupation, progress of the lesions, previous medication or intervention.
  • Dermatological examination of the feet for clinical diagnosis of the lesions.
  • Clinical photographs using a digital camera (DSC_WX300; Sony, Beijing, China).
  • Derrmoscopic examination of the patients’ feet. Dermlite II Pro HR (3 Gen LLC, San Juan Capistrano, California, USA) is a pocket epiluminescence microscopy device designed to view skin lesions with magnification and clarity.
  • Bacteriological diagnosis: specimens were taken from the lesion. Culturing was done before smearing on nutrient agar, blood agar, bile esculin agar, and MacConkey’s agar. Incubation was carried out for 24 h at 37°C. Smearing was done using a swab and the specimens were stained with gram stain for examination under a microscope.
  • Identification of the bacterial isolate, as follows:
    • Determination of colonial morphology including size, shape, color, consistency, surface edge, and odor of the colony on the culture media.
    • Gram-stained film examination under the microscope.
    • Biochemical reactions to differentiate different members of the family Micrococcacae, which includes Staphylococcus aureus, coagulase-negative Staphylococcus (CONs), Micrococcus, and Stomatococcus spp.
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Catalase test

The catalase test was conducted to differentiate the bacteria that produce catalase, such as Staphylococci and Micrococci spp., which are capable of decomposing hydrogen peroxide into water and oxygen from noncatalase-producing bacteria such as Streptococci spp.

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Coagulase test

Slide test (detect bound coagulase)

If fine grains of sand or small clumps are seen, the coagulase test is positive. If the mixture remains smooth ‘milky’ looking, the coagulase test is negative.

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Tube test

A positive result was considered if any degree of clotting of the tube contents was noted, whereas a negative result was considered when neither clotting nor fiber clot was formed.

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Sensitivity to bacitracin and polymyxin

This test was used to differentiate members of the family Micrococcacae (which includes Staphylococci, Micrococci, and Stomatococci spp.). Micrococci and Stomatococci spp. were sensitive to bacitracin, whereas Staphylococci spp. were resistant. Micrococci and Stomatococci spp. were further differentiated by polymyxin as Micrococci spp. were sensitive, whereas Stomatococci spp. were resistant.

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Statistical analysis

Data were a statistically analyzed using the Statistical Package for Social Science (SPSS, version 21; SPSS Inc., Chicago, Illinois, USA). The mean value, SD, the χ2, and Fisher’s exact test were calculated. Correlation studies were conducted using Pearson’s correlation coefficient. P values were considered significant if ≤ 0.05.

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Results

Clinical results

The present study included 90 male military patients with pitted keratolysis. Their ages ranged between 20 and 23 years. Complaints, the duration of the disease, and the anatomical distribution of the lesions among the studied patients are shown in Table 1.

Table 1

Table 1

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Dermoscopic results

The lesions showed numerous black circles in a parallel pattern on the ridges of the skin markings, which were crater-like/punched out/pigmented in 48 (53.34%) patients, crater-like/smooth/not pigmented lesions in 21 (23.33%) patients, crater-like/smooth/pigmented in 12 (13.33%) patients, and crater-like/punched out/not pigmented in nine (10%) patients (Table 2 and Figs 1 and 2).

Table 2

Table 2

Figure 1

Figure 1

Figure 2

Figure 2

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Bacteriological results

Corynebacterium spp. was reported in 42 (46.67%) patients. Micrococcus spp. growth was reported in 39 (43.33%) patients. Nine (10%) patients revealed no growth. The duration of illness did not have a significant effect upon bacterial growth (P=1) (Tables 2 and 3 and Figs 3 and 4).

Table 3

Table 3

Figure 3

Figure 3

Figure 4

Figure 4

Different dermoscopic patterns were detected on bacteriological examination and dermoscopic examination. It was observed that the Corynebacterium spp. was more prone to develop a crater-like/punched out/pigmented and crater-like/smooth/not pigmented pattern, whereas the Micrococcus spp. was more prone to develop a crater-like/punched out/pigmented pattern on dermoscopy. However, there was no statistically significant relation between the dermoscopic criteria and bacteriological results. The dermoscope revealed 100% sensitivity in the diagnosis, whereas the bacterial isolates were detected only from 90% of the clinically diagnosed cases of pitted keratolysis (Table 4).

Table 4

Table 4

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Discussion

Pitted keratolysis is a skin disorder that is characterized by crateriform pits that primarily affect the pressure-bearing parts of the plantar surfaces of the feet and occasionally the palms of the hands. Diagnosis of pitted keratolysis can easily be made by means of visual examination and recognition of the characteristic odor 4.

Pitted keratolysis occurs in people engaged in certain occupations, such as in barefooted laborers/farmers, marine workers, soldiers, and industrial workers wearing occluded shoes for prolonged periods 1. In this study, all cases were military people who wore occluded shoes for prolonged periods.

This study was similar to another conducted by Sasmaz and Celik 5, which reported pitted keratolysis as a primary dermatological disease in 34.5% of the soldiers.

Pitted keratolysis is characterized by many discrete, superficial crater-like pits and superficial erosion in the thickly keratinized skin of the plantar aspect of the feet. Although most cases are asymptomatic, some patients may complain of itching, tenderness, malodor (due to production of sulfur-compound by-products such as thiol, sulfides, and thioesters), hyperhidrosis, burning sensation, and sliminess of the skin of the feet, which can cause socks to stick to the skin 3. Some cases involve painful plaque-like lesions. The cause of pain is unknown 1. In this study, more than half of the cases suffered from malodor. Singh and Nail 1 found that malodor was the most common symptom of pitted keratolysis. Although hyperhidrosis was reported in 16.67% of the cases in this study, Singh and Nail 1 reported it in 70% of their cases.

Pitted keratolysis is a superficial cutaneous bacterial infection. The causative agents are Corynebacterium, M. sedentarius, D. congolensis, and Actinomyces spp. 3. In this study, most cases were caused by Corynebacterium and Micrococcus spp., and only nine patients showed no growth.

Different results have emerged from different parts of the world. Some of them concurred with the results of this study and some did not. Longshaw et al.6 had suggested that the causal agent of pitted keratolysis is M. sedentarius, from strains isolated from the feet. They are proteolytic and can cause pitting if inoculated into the skin surface under occlusion. M. sedentarius is capable of degrading callus in vitro, and evidence from continuous culture studies indicated that two extracellular protease enzymes are likely to be responsible and have callus-degrading activity.

It has been reported that Corynebacterium spp. is the main cause of pitted keratolysis. Increase in skin surface pH, hyperhidrosis, and prolonged occlusion allow these bacteria to proliferate and produce two keratin-degrading enzymes, which create pits by locally dissolving the stratum corneum’s corneodesmosomes and keratohyaline granules 7. In contrast, Rho and Kim 8 reported that pitted keratolysis can be found in association with other factors.

Corynebacterium infections can cause erythrasma and tricomycosis axillaris but in this study only pitted keratolysis was observed.

Amor et al.9 reported a case of pitted keratolysis caused by D. congolensis, which had been isolated from the lesion and had been identified by its morphological, cultural, and biochemical characteristics.

Dermoscopic examination of the lesions showed black circles in a parallel pattern on the ridges of the skin markings. Crater-like/punched out/pigmented pits, crater-like/smooth/not pigmented pits, crater-like/smooth/pigmented pits, and crater-like/punched out/not pigmented pits were reported in a descending manner at incidence rates of 53.34, 23.33, 13.33, and 10%, respectively. This correlates with the results of other dermoscopic studies on pitted keratolysis that revealed numerous black circles in a parallel pattern. Craters that were limited to the stratum corneum explained the circle seen on dermoscopy. Some bacteria produce pigments that can be seen after they grow into colonies. Here the pigment seen as black circles on dermoscopy may correspond to the pigment produced by the coccoid organisms 4.

The clinical features of pitted keratolysis continued to be the gold standard for its diagnosis. The Corynebacterium spp. was more prone to develop a crater-like/punched out/pigmented and crater-like/smooth/not pigmented pattern, whereas the Micrococcus spp. was more prone to develop a crater-like/punched out/pigmented pattern of dermoscopy. However, there was no statistically significant relation between the dermoscopic criteria and bacteriological results. The dermoscope revealed 100% sensitivity in the diagnosis of pitted keratolysis, whereas the bacterial isolate was detected only in 90% of the clinically diagnosed patients.

It is recommended to use dermoscopy in every practise to diagnose various foot disorders.

Bacteriological examination helps to identify the type of isolated microorganism, which may guide the prescription of the correct antibiotic according to culture and sensitivity results. Larger-scale studies correlating dermoscopic findings with bacteriological and histopathological results are recommended to improve the understanding of the dermoscopic criteria.

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Conflicts of interest

There are no conflicts of interest.

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References

1. Singh G, Naik CL. Pitted keratolysis. Indian J Dermatol Venereol Leprol 2005; 71:213–215.
2. Van der Snoek EM, Ekkelenkamp MB, Suykerbuyk JC. Pitted keratolysis; physicians’ treatment and their perceptions in Dutch army personnel. J Eur Acad Dermatol Venereol 2013; 27:1120–1126.
3. Fernández-Crehuet P, Ruiz-Villaverde R. Pitted keratolysis: an infective cause of foot odour. CMAJ 2015; 187:519.
4. Lockwood LL, Gehrke S, Navarini AA. Dermoscopy of pitted keratolysis. Case Rep Dermatol 2010; 2:146–148.
5. Sasmaz S, Celik M. Skin disease in Turkish soldiers. Dermatologica Sinica 2011; 29:44–46.
6. Longshaw CM, Wright JD, Farrell AM, Holland KT. Kytococcus sedentarius, the organism associated with pitted keratolysis, produces two keratin-degrading enzymes. J Appl Microbiol 2002; 93:810–816.
7. Hermanns-Le T, Garcia R, Arrese JE, Pierard GE. Pitted keratolysis: new ultrastructural insight in keratohyalin granule and corneodesmosome alterations. Exog Dermatol 2004; 3:107–111.
8. Rho NK, Kim BJ. A corynebacterial triad: prevalence of erythrasma and trichomycosis axillaris in soldiers with pitted keratolysis. J Am Acad Dermatol 2008; 58 (Suppl):S57–S58.
9. Amor A, Enríquez A, Corcuera MT, Toro C, Herrero D, Baquero M. Is infection by Dermatophilus congolensis underdiagnosed? J Clin Microbiol 2011; 49:449–451.
Keywords:

bacteriological examination; dermoscopy; pitted keratolysis

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