Clinicoepidemiological, dermoscopic, and mycological profile of pityriasis versicolor in Northern India

INTRODUCTION

A common superficial fungal disease that affects the stratum corneum, pityriasis versicolor (PV), or tinea versicolor, usually manifests as scaly, unevenly colored macules that are primarily found on the trunk and limbs.^[1] One of the main culprits is identified as the lipid-dependent, dimorphic yeast Malassezia furfur. It is a typical component of the skin’s flora and can turn harmful in specific situations, such as warm and humid settings.^[2] Malassezia globosa, Malassezia obtusa, Malassezia restricta, Malassezia slooffiae, Malassezia dermatitis, M. furfur, Malassezia pachydermatis, Malassezia sympodialis, M. globosa, Malassezia japonica, Malassezia nana, Malassezia yamatoensis, and the unrecognized species Malassezia equi are among the 18 species that have been added to the genus in recent classifications.^[3,4]

Dermoscopy is a valuable technique for differentiating PV from other hypopigmentation-causing disorders, typically manifesting as well-defined white patches with tiny scales frequently seen in the skin’s natural grooves.^[1,2] Diagnostic approaches for PV primarily involve potassium hydroxide (KOH) mount, fungal cultures, and, in some settings, molecular techniques.^[5,6] PV has been diagnosed using contrast stain, such as Calcofluor White and Parker blue black ink. Wood’s light examination may also help to diagnose the condition.^[7,8] At present, systemic antifungal medications are advised for widespread cases of PV, whereas topical antifungals are the first line of treatment.^[9]

The objective of this study was to examine the clinical pattern, epidemiological, dermoscopic, and mycological features of PV patients in the Kashmir Valley.

MATERIALS AND METHODS

A cross-sectional descriptive study was conducted over a year, from October 2020 to September 2021, in a dermatology department tertiary care hospital. A total of 176 patients were enrolled out of whom only 100 PV patients who visited the outpatient department over a year fulfilled the inclusion criteria. Individuals who had taken oral or topical antifungal medication in the previous month were excluded from the study. Every patient provided written informed consent. A comprehensive medical history, demographic information, socioeconomic status using the modified Kuppuswamy scale, questions concerning the disease’s genesis and progression, repeated episodes, related symptoms, personal hygiene status, previous treatments, and similar history in family members were recorded.

During a clinical examination, the location of the lesions, their color and texture, the existence of scales and related seborrheic dermatitis of the scalp, and any additional related dermatological or systemic conditions were noted. Dermoscopy was performed using a hand-held device (DermLite 3Gen, DL3/DL4, USA) at 10x magnification in polarized and non-polarized modes.

Routine laboratory tests and HIV infection screening were carried out if deemed essential. Lesions were examined under a Wood’s lamp to elicit fluorescence, thereby enhancing their visibility and aiding in diagnosis. Scrapings were obtained from the regions exhibiting strong fluorescence under aseptic conditions. The materials were processed in the mycology laboratory after being transported on sterile Whatman filter paper.

Skin scrapings were examined after treatment with a 20% KOH preparation for 20 min to identify fungal elements, typically appearing as hyphae and spores with a characteristic “spaghetti and meatballs” or “banana and grapes” morphology. All cultures were incubated at 32°C following inoculation into Sabouraud’s Dextrose agar (SDA), modified Dixon agar (MDA), plain SDA (for the isolation of nonlipid-dependent M. pachydermatis), and SDA supplemented with sterile olive oil, cycloheximide, and chloramphenicol. The culture plates and slants were examined daily for up to 3 weeks before reporting any negative findings. The colonies showing creamy, wet, and pasty growth were considered indicative of Malassezia growth.

A smear prepared from the colonies was stained using Gram’s stain and examined under an oil immersion microscope (×100 objective) to confirm the presence of Malassezia. Positive findings included short, angular hyphal elements, unipolar budding, and cells that resembled phialide yeast. In addition, the VITEK ID-YST card was used by the VITEK 2 system to validate the results. An ATB 1550 densitometer (bioMerieux) adjusted the culture inocula to a no. 2 McFarland standard by suspending the yeast cells in 0.45% aqueous sodium chloride. Tests were conducted on the subcultures maintained on the aforementioned culture media for 24–55 h.

RESULTS

Out of 100 patients of PV, 67 (67%) were male and 33 (33%) were female with a male-to-female ratio of 2.03:1. Most of the patients were young adults, with 40% belonging to the age group of 21–30 years, with only two patients below 10 years and 6 patients above 50 years. Duration of the disease ranged from 2 weeks to 1 year.

Majority of our patients (65%) were students, followed by farmers (10%) and housewives (8%). Most (38%) of our patients were from lower socioeconomic classes, and 62% were from rural areas. The incidence of PV in our patients was highest during August–September (34%), followed by October–November (23%). Forty-five (45%) patients had a history of PV, and 18 (18%) had a positive family history. Most patients (72%) were asymptomatic, whereas 21% had mild and 7% had moderate pruritus. Twenty-one (21%) patients had lesions predisposed by sweating, and 8 (8%) had lesions due to vigorous physical activity. There was no clear correlation between PV and the use of cosmetics, talcum powder, oil, soap, shampoo, or synthetic garments. About 85% of patients reported practicing good personal hygiene.

The most frequent sites of involvement were chest (55%), followed by back (14%) and neck (12%) [Figure 1]. Flexural lesions were seen only in 5 (5%) patients. In terms of morphology, 80% of the varieties were hypopigmented, 8% were hyperpigmented, and 12% were mixed. In 72% of cases, branny scaling was found. Twenty-four percentages of patients had coexisting seborrheic dermatitis. The associated dermatological disorders seen included dermatophytosis (6%) of the patients, acne vulgaris (10%), vitiligo (2%), melasma (3%), eczemas (2%), polymorphous light eruption (2%), and alopecia areata (2%). HIV positivity was not seen in any of our patients. Among the associated systemic conditions, diabetes mellitus was the most common association, seen in 3 (3%) patients, while 4 (4%) patients were on immunosuppressant drugs or systemic corticosteroids and were referred to the dermatology department for the treatment of PV.

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Figure 1a:

Hyperpigmented scaly lesions in pityriasis versicolor, (b): Yellowish green fluorescence seen on Wood’s lamp examination; (c): Perifollicular hypopigmentation (green arrows) and perilesional hyperpigmentation with no scales (blue arrows) (DermLite 3Gen, DL3/DL4, USA, polarized mode, 10x).

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A total of 85 (85%) of the 100 patients analyzed under a Wood’s lamp showed yellow-green fluorescence. While 15 (15%) of them had no fluorescence, the remaining ones were Wood’s lamp positive [Figure 1b].

The dermoscopic findings in most of our patients showed fine whitish scales adhered to the skin furrows in both hyper- and hypopigmented types. In the former, the hyperpigmented areas appeared as homogenous brownish stripes separated by the scaly furrows [Figures 1c and 2]. In the latter, fairly demarcated white areas with whitish scales were seen in most cases. Furthermore, reduction in perifollicular pigment (folliculotropism) and perilesional hyperpigmentation were seen in some patients who had no scaling [Table 1 and Figure 3].

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Figure 2:

Homogeneous brown stripes (black arrow) separated by skin furrows with adherent fine scales (red arrow) (DermLite 3Gen, DL3/DL4, USA, polarized mode, 10x).

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Figure 3:

Fine whitish scales adhered to the skin furrows seen in the inset image (DermLite 3Gen, DL3/DL4, USA, polarized mode, 20x) on a homogenous brown background image ( DermLite 3Gen, DL3/DL4, USA, polarized mode, 10x).

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Mounts of KOH were found in 80 (80%) of the patients. Sixty-seven (83.75%) of the 80 positives were Malassezia isolates that developed in culture. M. globosa was the most common isolate which grew in 39 (58.20%) of the 67 samples that produced Malassezia growth, followed by M. sympodialis 17 (25.3%) and M. furfur 11 (16.41%). Compared to other species, M. globosa has a considerably greater isolation rate (P < 0.001) [Table 2 and Figures 4 and 5].

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Figure 4:

Creamy white, moist colonies of Malassezia globosa on Sabouraud’s dextrose agar culture (black circles).

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Figure 5:

Pie chart showing different species of Malassezia isolated on culture.

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DISCUSSION

PV, the most prevalent Malassezia-caused illness, has also been linked to seborrheic dermatitis. Adults are typically infected due to increasing sebum secretions following puberty.^[1,2] Although PV is frequently asymptomatic, some individuals may experience mild pruritus. The primary concern prompting patients to seek treatment is the unsightly appearance of the skin.^[2]

It can occasionally mimic diseases such as vitiligo (early lesions), progressive macular hypomelanosis, pityriasis alba, and, infrequently, mycosis fungoides (early patch stage). Dermoscopy is a valuable technique for differentiating PV from other hypopigmented lesions, typically manifesting as well-defined white patches with tiny scales frequently seen in the skin’s natural grooves. On the other hand, fine whitish scales in the furrows are linked to a pigment network made up of focal or diffuse, uniform brownish pigmentation, similar to hyperpigmented macules.^[1,2,10,11]

In a KOH mount, PV fungi typically exhibit the characteristic spaghetti and meatball pattern featuring short hyphae and numerous spores, which is diagnostic of PV. By exhibiting yellowish fluorescence Wood’s light examination may also help diagnose.^[3,4]

This research aimed to evaluate the epidemiological and clinical features of PV among patients in Kashmir’s temperate environment. The study was conducted at a tertiary care hospital and included patients from both rural and urban areas. Our study revealed several observations that were consistent with those reported in previous studies. The highest prevalence of PV in the age group 21–30 years is attributed to increased sebum production during this stage of life. Tschen and Ghosh et al. observed similar findings.^[12,13]

In the present study, we found a predominance of male patients (M:F=2.08:1). The male predominance observed could be due to greater exposure to environmental factors such as heat and humidity through outdoor activities. Rao et al., Krishnan and Thapa, and Maheswari observed similar findings.^[5,14,15]

A family history of PV was seen in 18% of the individuals in this study. Studies by Ghosh et al.^[13] (25%) and Rao et al.^[5] (38.30%) also reported similar findings. However, Tschen did not find any such history.^[12]

In the present study, sweating was identified as a contributing factor in 21% of the patients, 8 (8%) patients attributed physical activity, while in 4% of patients, medications such as oral steroids and oral contraceptives. Stein discovered a number of risk factors in his study, such as corticosteroid usage, cancer, pregnancy, poor general health, and genetic vulnerability.^[16] Faergemann and Bernander identified hyperhidrosis, malnutrition, and oral contraceptive use as risk factors.^[17]

Forty-eight (48%) of the patients in our study had a history of recurrences. According to Ghosh et al., 48.18% of patients had a history of recurrences.^[13] According to Rao et al., 3.3% of the patients who were not receiving treatment experienced recurrence.^[5]

In the present study, we noted a seasonal trend with most patients presenting between August and September, followed by October and November. The reasons for this seasonal variation may be an increase in the humidity during these months and the fact that lesions are more visible to the patients due to less clothing, thus making them seek medical attention. In their research, Ghosh et al. reported that most cases were presented in August and September.^[13] A similar seasonal trend was observed in the studies by Rao et al.^[5] and Dutta et al.^[18]

Gupta et al.^[19] reported that PV is known to be asymptomatic and is mainly a cosmetic concern. Most (72%) of our study population were asymptomatic, while 28% of our patients experienced mild-to-moderate pruritus, as also reported by Ghosh et al.,^[13] Abdul Razack et al.,^[20] and Ingordo et al.^[21]

In the present study, fine branny scaling over the lesions was present in 72 (72%) patients, which was almost in agreement with the observations made by Assaf and Weil, who noted scaling in all the patients in their study.^[22] The most common sites of involvement were chest, neck, and back, while flexural involvement was uncommon, seen in only five patients This finding was also in accordance to other studies.^[12,13] In contrast to our observation, Aljabre, in their study, showed that flexural lesions of PV were not uncommon.^[23] The distribution of affected skin lesions reflects the lipophilic nature of the fungus since the seborrheic areas are predominantly involved. These species lack fatty acid synthase genes, except M. pachydermatis, and thus depend on exogenous lipids.

In the present study, in complete agreement with the findings of Ghosh et al., the majority of PV lesions were hypopigmented, followed by mixed (hypopigmented and hyperpigmented) and exclusively hyperpigmented lesions.^[13] In addition to having a direct lethal effect on hyperactive melanocytes, the formation of dicarboxylic acids, the primary component of which is azelaic acid, a known competitive inhibitor of DOPA tyrosinase, can be used to explain the hypopigmentation caused by this fungus. According to Gupta et al., a single patient may have both types of lesions, either hypopigmented or hyperpigmented.^[19] In their study, Rao et al., Krishnan and Thapa, and Assaf and Weil reported similar findings, which showed that PV lesions usually start as reddish macules before gradually becoming hypopigmented. The occasional hyperpigmentation could be caused by variations in each person’s inflammatory response.^[5,14,22] In contrast to our findings, according to Aljabre, dark-skinned people do not typically have PV that is noticeably hypopigmented.^[23]

In our study, we found 12% of patients had coexisting seborrheic dermatitis, which conformed to the observation made by other workers.^[14] Rao et al. discovered 11.60% of their tinea versicolor patients had seborrheic dermatitis.^[5] Approximately 4% of patients with PV were using immunosuppressive medications or systemic corticosteroids, and 3% of patients had concurrent systemic illnesses such as diabetes mellitus. Krishnan and Thapa found no correlation with diabetic mellitus, corticosteroids, or other immunosuppressive treatments, contrasting our findings.^[14] Clinical examination, Wood’s lamp examination, microscopic inspection of the lesions, and cultural identification are used to diagnose PV. Of the 100 individuals analyzed in this study under a Wood’s lamp, 85 (85%) showed yellow-green fluorescence and were classified as Wood’s lamp positive, while 15 (15%) did not. In their study, Shah et al. found that 88.48% of patients had positive Wood’s lamp results.^[7]

According to reports, dermoscopy revealed hypopigmented patches in the hyperpigmented type and small whitish scales attached to the skin furrows around the uniform brownish stripes in a net-like pattern in the hypopigmented type. A study carried out by Lekkas et al. revealed similar results.^[24] Vishwanath et al reported pigmentation and scaling to be universal findings on dermoscopy. Similar findings were observed by Manickam et al.^[10,11]

All 100 patients with PV underwent microscopic examination with 20% KOH; 80 samples tested positive for KOH, and 63 (63%) showed the traits – the look of meatballs with spaghetti. Of 80 KOH-positive samples, 67 (83.75%) had Malassezia isolated on MDA and SDA. Malassezia was recovered in 61.40% of the samples with KOH positivity, whereas Shah et al. showed an 82.01% KOH positivity in their samples.^[7] Kindo et al.,^[25] Kannan et al.,^[26] and Chaudhary et al.^[27] reported similar findings.

Out of the 67 samples that produced Malassezia growth in the current investigation, 39 patients (58.20%) had growth of M. globosa, followed by M. sympodialis (17 [25.3%]) and M. furfur (11 [16.41%]). M. globosa was isolated at a significantly higher frequency compared to other species (P < 0.001). The predominance of M. globosa as an isolate has been reported by Shah et al., Dutta et al., Chaudhary et al., and Nakabayashi et al.^[7,18,27,28] In contrast to our investigation, M. sympodialis was the most common isolate in the studies conducted by Gupta et al. and Archana et al.^[29,30]

Kindo et al., from South India, found that M. sympodialis was the most prevalent species.^[25] The most prevalent species in Asia are M. globosa and M. restricta, but the most prevalent species in Europe is M. sympodialis.^[31] According to our research, there was no discernible difference in the distribution of Malassezia species between people who presented with hyperpigmented and hypopigmented lesions. Table 3 compares the clinicoepidemiological and mycological findings in our study with those of other studies.

CONCLUSION

The clinicoepidemiological, dermoscopic, and mycological parameters observed in our study were largely consistent with those reported by other researchers. However, long-term epidemiological studies are warranted in the Kashmir Valley to monitor the trends and burden of this condition more comprehensively.