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CLINICAL AND SURGICAL PRACTICE

Received: April 10^th 2014

Accepted: February 4^th 2015

Onychomycosis frequency in psoriatic patients in a tertiary care hospital

Luis Javier Méndez-Tovar,^a Alfredo Arévalo-López,^b Sofía Domínguez-Aguilar,^b Patricia Manzano-Gayosso,^c Francisca Hernández-Hernández,^c Rubén López Martínez,^c Israel Silva González^d

^aLaboratorio de Investigación Médica en Dermatología y Micología

^bServicio de Dermatología y Micología Médica

^cDepartamento de Microbiología y Parasitología, Facultad de Medicina, Universidad Nacional Autónoma de México

^dLaboratorio Central

^a,b,dHospital de Especialidades, Centro Médico Nacional Siglo XXI, Instituto Mexicano del Seguro Social

Distrito Federal, México

Communication with: Luis Javier Méndez-Tovar

Telephone: (55) 5627 6900, extension 21480

Email: ljmt@unam.mx; ljmendez@alestra.net.mx

Background: The changes in psoriatic nails can closely resemble an onychomycosis. Therefore, the fungal infection may be underdiagnosed. It was investigated the frequency of mycosis in fingernails and toenails in 150 patients with psoriasis in a dermatology department.

Methods: The clinical data suggestive of onychomycosis were investigated. Nail scales were obtained and cultured on Sabouraud dextrose agar with and without antibiotic. A direct examination with KOH was also performed.

Results: Out of 150 patients, 67 (45 %) had healthy nails; 42 (28 %) presented onychomycosis and 41 (27 %) showed nail changes without infection. Fingernail changes were more associated with psoriatic onychopathy (82.5 %), unlike toenail changes that were more frequently caused by fungal infection (26.4 % vs. 9.45 % in psoriasis). Out of 20 positive cultures, 22 fungi were isolated, of which 11 belonged to Candida spp. (50 %). As risk factor to develope an onychomycosis, only the psoriasis evolution time showed a significant difference (p = 0.033).

Conclusion: In patients with psoriasis, fingernail disorders are mainly due to the own disease, while toenail disorders changes can be associated with onychomycosis. The main etiological agents were yeasts from the genus Candida. The only factor associated with a higher incidence of onychomycosis in these patients was a long lasting psoriasis.

Keywords: Psoriasis; Onychomycosis

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Psoriasis is an inflammatory skin disease of chronic development that affects 1-3% of the general population. It has a characteristic clinical expression of scaly erythematous lesions of variable extent and severity.¹ In addition to skin lesions, disorders in the nails may occur in up to 55% of patients in both fingernails and toenails;^2,3 the most frequent alterations are punctate depressions ("dimples"), onycholysis, subungual hyperkeratosis, "oil spots" and bleeding in splinters.^2-4 Although usually these nail disorders are recognized as a clinical manifestation of psoriasis, there may also be confusion with other diseases such as fungal infections.

According to Baran et al.,⁵ onychomycosis is classified as: subungual distal and lateral, superficial, subungual proximal, endonyx, and total dystrophic onychomycosis. For many it is difficult to distinguish between damage caused by psoriasis and that caused by fungal infection. The prevalence of onychomycosis in psoriasis patients may vary between 13 and 47%.^6-8 Coexistence of psoriasis and onychomycosis is related with certain factors: prolonged development of psoriasis; greater severity of  psoriasis, as measured by the rate of expansion; severity greater than 10, and, in particular, the presence of psoriatic onychopathy itself.^3,8,9

Onychomycosis in patients with psoriasis (OPP) has special features like frequency variation; reported in different studied groups; the distribution of identified causal agents; and systemic treatment of psoriasis with immunosuppressive drugs (methotrexate, cyclosporine), or with the use of so-called biological agents (anti-TNF, anti-IL-12/23), which may make one prone to the development of invasive fungal infections such as pneumocystosis,¹⁰ or surface infections such as onychomycosis.

Mexico has limited knowledge on the epidemiology of OPP, as research in this area is scarce. Orellana-Arauco et al.,¹¹ in a review published in 2012 of 50 psoriasis patients, found 17 cases (34%) with onychomycosis; 80% of the cultures were dermatophytes and 20% Candida albicans. A study published in 1999 reports a frequency of onychomycosis of 28.7% in 101 patients with psoriasis.¹²

The objectives of this study were to determine the frequency of onychomycosis in a series of patients with psoriasis treated at a highly specialized IMSS hospital, to find the main causative agents, and to evaluate the influence of comorbidity and the type of psoriasis treatment.

Methods

A prospective transversal and analytical study was performed that included all patients with psoriasis who came to the Servicio de Dermatología of the Hospital de Especialidades del Centro Médico Nacional Siglo XXI of the Instituto Mexicano del Seguro Social for a period of six months.

Each patient's age, sex, type of psoriasis, severity of illness, and treatment used were registered. Fingernails and toenails were studied; with any nail disorder hyponychium flakes were taken. With this material direct examination was performed with potassium hydroxide 15% to find hyphae, yeasts or both; they were also seeded in Sabouraud dextrose agar (SDA) media and SDA with added cycloheximide and chloramphenicol. Cultures were incubated at 25 ° C for 15 days. When they had developed, a direct examination of the colonies was performed with cotton blue. In cultures with growth of fungal contaminants the study was repeated twice more. The yeasts were identified by physiological tests on Vytec® equipment.

The results were analyzed with SPSS, version 17. The frequency was determined by sex, age, and chi-squared test was used to establish the statistical correlation of onychomycosis with the following parameters: clinical presentation and development time of psoriasis, percentage of body surface area affected, associated comorbidity, and type of treatment for psoriasis. In the analysis of both groups, a p-value < 0.05 was considered statistically significant,

Results

Of a total of 150 psoriasis patients, 83 (55%) had nail disorders; of these, 42 had onychomycosis (32 men and 10 women). Most infections occurred in people over 40 years of age (Table I).

The most common clinical disorders in both groups were dyschromia, subungual hyperkeratosis, and onycholysis. The disorders present in the fingernails were mainly associated with psoriasis (82.5%), while the disorders of the toenails were most often associated with onychomycosis (Table II).

Of the 42 patients with onychomycosis, the diagnosis was established only with direct examination with KOH in 20 cases, by cultivation in four cases, and with both methods in 18 patients. 22 fungal agents were isolated, of which 11 (50%) were yeasts, 7 (32%) dermatophytes, and in four cases (18%) by repeated subculturing, non-dermatophyte filamentous fungi (Curvularia sp., Fusarium sp., Fonsecaea sp., and Penicillium sp.), was isolated, all from toenails (Table III).

All yeasts were genus Candida and C. albicans was the most common species. The only dermatophyte that was isolated was Trichophyton rubrum. According to the classification proposed by Kaminski,¹³ two of the seven isolates corresponded to the hairy variety with red pigment typical of the species, while the other five belonged to the variety Y, which forms white, hairy colonies, with few microconidia and yellowish or orange pigment on the back (Figure 1). 

Regarding comorbidity in patients with psoriasis and onychomycosis, other associated diseases were found: 12 patients with metabolic disorders (diabetes mellitus, metabolic syndrome, and dyslipidemia), seven with psoriatic arthritis, and two with AIDS. In psoriasis patients without onychomycosis, 13 patients had metabolic disorders, four psoriatic arthritis, one hepatitis C, and four cancer (gastric carcinoma, colon adenocarcinoma, squamous cell carcinoma, and Merkel carcinoma). No type of comorbidity showed any significant difference between the groups of psoriasis patients with and without onychomycosis.

The most common clinical form of psoriasis in patients with onychomycosis was plaque psoriasis (88%). Of the 42 patients with onychomycosis, 27 had affected body surface below 5% at the time of the study.

Regarding the time of development of psoriasis, it was found that when it was ≥ 10 years, patients had a higher frequency of onychomycosis (69%), whereas this was only 30.9% in patients with less than 10 years. This difference was statistically significant with a p-value = 0.03 (Table IV).

Of the 150 patients with psoriasis, 33 (22%) received topical therapy (corticosteroids, coal tar, salicylic acid); the rest (78%) were under some type of systemic treatment distributed as follows: monotherapy with immunosuppressants (methotrexate, cyclosporine), 46 patients (31%); treatment with biological agents (infliximab, adalimumab, etanercept), 18 patients (12%); or combined management, 53 patients (35%). Statistical analysis of the different types of treatment showed no significant difference in the frequency of onychomycosis (Table V).

Discussion

OPP frequency found in this study (28%) is similar to that reported in two previous Mexican works that report 29 and 34%, respectively.^11,12 Although Mexico has published numerous studies of cases of onychomycosis, such as Arenas et al.,¹⁴ the overall prevalence of onychomycosis in the general population has not been established with precision and therefore comparisons cannot be made. However, the results of these percentages are higher than those reported in the general population from other places like Ohio, USA (2-3%)¹⁵ and Finland (13%).¹⁶

OPP frequency can show a wide variation in published studies; so for example, Solovăstru¹⁷ reports a single case of onychomycosis in 60 patients; however, in most reports OPP frequency has been found greater than that observed in the general population; Gupta reports a prevalence of 56%,⁸ in Spain a frequency of 30% is reported,¹⁸ while in a study of patients in Bulgaria and Greece, OPP frequency reached 62%.¹⁹ The large variation in the OPP frequency probably reflects social and ecological differences, in addition to factors related to diagnostic methods themselves. 

OPP frequency may increase by the influence of other factors such as lower resistance to infection in the hyponychium due to distal condition of the nail bed. It is also possible that treatment with immunosuppressive drugs such as methotrexate and cyclosporin, or so-called biological agents, facilitate and increase the infection rate, as demonstrated in other fungal infections.¹⁰ Al-Mutairi et al.²⁰ in a study of 315 patients with psoriasis treated with biological agents found onychomycosis in 33% of those receiving infliximab, 15.45% in patients treated with etanercept, and only 13.33% in those receiving adalimumab. These researchers concluded that treatment with infliximab in psoriasis patients predisposed them to the development of onychomycosis; however, in this study the statistical analysis of the treatment type against frequency of onychomycosis showed no difference; even patients receiving biological agents had a lower frequency of infection.    

Regarding the etiologic agents for OPP, the species reported in different cases also show variation. In a study conducted in Turkey the main agent was T. rubrum,⁷ while in another study reported in Denmark⁶ yeasts were isolated more frequently, including Candida spp. and Trichosporon sp. However, all studies agree that non-dermatophyte filamentous fungi (molds) are the least common causative agents with indices ranging from 2.7 to 5%.^7,9,19 In the present study Candida yeasts predominated (50 %), followed by T. rubrum (32%) and molds had a frequency of 18%, which is higher than that reported in other investigations. It was notable that two cases of infection by rare filamentous nail fungus (Penicillium and Fonsecaea) were seen; however, in both patients repeated isolation of the same agent was performed.

The prevalence of infections caused by yeast was probably because 25 of the 83 patients with nail disorders (30.12%) had type 2 diabetes mellitus, and as has been shown in other studies, this endocrine disorder favors the development of candidosis in all locations, including nails,²¹ plus the nails of patients with psoriasis are more easily colonized by yeasts.⁷

Conclusion

Fingernail disorders in patients with psoriasis are caused in most cases by the psoriasis itself (82.5 versus 23.3%), while in the toenails the presence of dyschromia, deformity, onycholysis or subungual hyperkeratosis fungal infection may be associated with more than twice as many cases. Yeasts are the major cause of infection in the patients studied and of the predisposing factors analyzed, only the development time of psoriasis has an influence, significantly increasing the frequency of onicomicosisis.

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