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Onychomycosis Incidence in Type 2 Diabetes Mellitus Patients Mycopathologia (2008) 166:41–45 DOI 10.1007/s11046-008-9112-5 Onychomycosis Incidence in Type 2 Diabetes Mellitus Patients Patricia Manzano-Gayosso Æ Francisca Herna´ndez-Herna´ndez Æ Luis Javier Me´ndez-Tovar Æ Yanni Palacios-Morales Æ Erika Co´rdova-Martı´nez Æ Elva Baza´n-Mora Æ Rube´nLo´pez-Martinez Received: 26 July 2007 / Accepted: 11 March 2008 / Published online: 29 March 2008 Ó Springer Science+Business Media B.V. 2008 Abstract The onychomycosis incidence was deter- rubrum being the first species (37.1%). All these strains mined in 250 type 2 diabetes mellitus (T2DM) patients corresponded to two morphological varieties: who were registered at the Internal Medicine Service ‘‘yellow’’ and typical downy. From the yeast-like from a Mexico city General Hospital throughout a year isolates, 12 corresponded to Candida spp., firstly (January–December 2006). Out of the total of studied C. albicans and C. parapsilosis; three to Cryptococcus T2DM patients, 93 (37.2%) showed ungual dystrophy spp. (C. albidus, C. uniguttulatus and C. laurentii); two and from these, in 75.3% a fungal etiology was Trichosporon asahii; and only one to Pichia ohmeri. corroborated. Out of 70 patients, 34 were men and 36 Six non-dermatophytic molds were isolated: two women, with an average of 63.5 years. Correlation Chrysosporium keratinophylus, two Scopulariopsis between T2DM evolution time and onychomycosis brevicaulis, one Aspergillus fumigatus, and one was significant (P \ 0.01). Distal-lateral subungual Acremonium sp. The fungal mixture corresponded to and total dystrophic onychomycosis were the most T. mentagrophytes with C. guilliermondii; T. mentag- frequent clinical types (55.1% and 33.7%, respec- rophytes with C. glabrata; T. rubrum with C. glabrata; tively). Fifty-eight fungal isolates were obtained; T. rubrum with P. ohmeri. 48.6% corresponded to dermatophytes, Trichophyton Keywords Candida Á Dermatophytes Á Diabetes mellitus Á Onychomycosis P. Manzano-Gayosso (&) Á F. Herna´ndez-Herna´ndez Á E. Co´rdova-Martı´nez Á E. Baza´n-Mora Á R. Lo´pez-Martinez Laboratorio de Micologı´aMe´dica, Departamento de Introduction Microbiologı´a y Parasitologı´a, Facultad de Medicina, UNAM, Ciudad Universitaria, Mexico, CP 04510, DF, Mexico Onychomycosis are common diseases within the e-mail: [email protected] general population, where these represent from 18% to 40% of nail diseases [1]. However, in adults over L. J. Me´ndez-Tovar 60 years old the disease is 40% more frequent [2] and Unidad de Investigacio´nMe´dica en Dermatologı´ay Micologı´a ‘‘Dr. Ernesto Macotela’’, Hospital de in type 2 diabetes mellitus (T2DM) patients it increases Especialidades, Centro Me´dico Nacional Siglo XXI, 2.5 times [3]. In these patients onychomycosis diag- IMSS, Mexico, DF, Mexico nosis is overestimated since this population commonly presents ungual dystrophy related with the elderly and Y. Palacios-Morales Servicio de Medicina Interna, Hospital General Dr. some diabetes complications such as peripheral vas- ‘‘Darı´o Ferna´ndez Fierro’’, ISSSTE, Mexico, DF, Mexico cular disease and neuropathy [4]. According to Gupta 123 42 Mycopathologia (2008) 166:41–45 et al. [3] 33% of diabetic patients present onychomy- December 2006) were studied. The following data cosis frequently associated with tinea pedis. Lo´pez- were obtained from each patient: gender, age, occu- Gonza´lez and Mayorga [5] found similar data. pation, T2DM evolution time and complications; Among the fungi causing onychomycosis, derma- onychomycosis clinical types and evolution time; tophytes are the most frequent (38–80% of cases), cutaneous lesions suggestive of fungal infection, and followed by yeasts (10–24%) and non-dermatophytic previous antifungal treatment. molds (8–14%) [6–8]. Trichophyton rubrum is the most common isolated species followed by T. ment- Fungal Cultures agrophytes (20%). On the other hand, A´ lvarez et al. [6] found that from 299 onychomycosis patients, Candida In the patients with any kind of ungual dystrophy albicans was the number one etiological agent fol- (onycholysis, paronychia, or pachyonychia), a myco- lowed by T. rubrum. Among the non-dermatophytic logical study was performed. Nail scrapings were molds, Fusarium was the most prevalent. taken in three consecutive days and microscopically Four onychomycosis clinical types have been examined after 15% potassium hydroxide treatment; described: distal-lateral subungual (D-LSO), proxi- samples were inoculated in ten different points on mal subungual (PSO), white superficial (WSO) and Sabouraud dextrose agar plates with and without total dystrophic (TDO) onychomycosis. The first antibiotics (Bioxon). The cultures were incubated at clinical type is the most common and the last one 28°C and examined daily for 15 days. seems to be a mixture of all the other onychomycosis types [9, 10]. In diabetic patients another clinical Identification of Dermatophytes and Other form has been described, and is named Candida Keratinophilic Fungi onychomycosis characterized by paronychia [11]. In Mexico, as in other countries, diabetes is a great Identification of isolated fungi was based on morpho- public health problem and according to the national logical characteristics and some physiological tests chronic disease survey reported by Membren˜o et al. depending on genus and species. Dermatophytes and [12], the prevalence of diabetes mellitus is 7.2% in other keratinophilic fungi were grown on bromcresol general population and, T2DM corresponds to 90% of purple milk solids glucose agar, on lactrimel agar, 1% the cases. This disease is the first cause of hospital peptone agar, Christensen-urea agar, 5% NaCl agar; admission. In spite of the fact that other authors have hair perforation test was also performed [13]. not found a significant difference between onychomy- cosis incidence in the general population and diabetic Identification of Yeasts patients, the latter frequently show vascular and sensibility disorders, resulting in small traumatic Yeast species were identified by using germ tube lesions which represent the access for bacteria and production, morphology on cornmeal agar, colonial fungi infections. pigmentation on chromogenic medium (CHROMagar We conducted a descriptive and observational Candida)[14], Christensen-urea agar and Staib agar, study aiming to determine the onychomycosis inci- and the assimilation of carbohydrates by commercial dence, evolution time, clinical forms, and etiological identification systems (API 20C AUX (bioMeriux) and agents in T2DM patients. YBC card (Vitek)). Isolates identified as C. albicans were studied by means of other tests such as chlamydo- conidia production on three media (Staib [15], casein Materials and Methods [16], and tobacco agar [17]) and growth at 45°C[18]to differentiate it from C. dubliniensis. Patients The Pearson Test (SSPS Program, version 12) was applied when it was necessary to establish compar- Two hundred and fifty T2DM patients admitted in isons. Values of P B 0.05 were considered to be the Department of Internal Medicine at the General significant. Percentages of different factors (gender, Hospital ‘‘Dr. Darı´o Ferna´ndez Fierro’’ ISSSTE, clinical types, etiological agents versus T2DM) in in Mexico city, during a 1-year period (January– patients were also obtained. 123 Mycopathologia (2008) 166:41–45 43 Results Table 2 Onychomycosis clinical types observed in 70 T2DM patients From the 250 T2DM patients, 93 (37.2%) presented Clinical type Toenails Fingernails Total Percentage ungual dystrophy. Seventy patients (75.3%) had onychomycosis confirmed by three different positive D-LSO 29 5 34 48.6 samples for direct examination and culture of nail TDO 19 3 22 31.4 scrapings. Among 70 patients, 34 were males and 36 PSO 6 3 9 12.9 females. The average age was 63.5 years. From 70 WSO 2 3 5 7.1 T2DM patients, 28 presented onychomycosis associ- D-LSO, distal-lateral subungual onychomycosis; PSO, ated with other medical conditions, such as peripheral proximal subungual onychomycosis; WSO, white superficial vascular disease (13), diabetic dermatopathy (six), onychomycosis; TDO, total dystrophic onychomycosis cellulitis (five), ‘‘diabetic foot’’ (three), and periph- eral neuropathy (one). Concerning the relationship between the T2DM evolution time and onychomycosis, in most of the cases the last started after the diabetes was diagnosed, and this event was statistically significant (P \ 0.01) (Table 1). The clinical localization of onychomycosis in the 70 patients was in toenails (56) and in fingernails (11). Infections of both fingernails and toenails were observed in three cases. Table 2 shows the observed clinical types of onychomycosis, predominating both D-LSO (48.6%) and TDO (31.4%). Figure 1 shows a case of white superficial onychomycosis. Twenty seven patients had associated tinea pedis, two had tinea mannum, and one tinea corporis. Out of the 70 onychomycosis-T2DM patients, 58 fungal isolates were obtained (82.8%): 34 dermato- phytes (48.6%), 18 yeasts (25.6%), and six other non- Fig. 1 A white superficial onychomycosis case caused by dermatophytic molds (8.6%); in four cases a mixture T. rubrum, in a 68-year-old male patient, with an evolution of of two species was found. 7 years. Lesion consists of transverse leuconychia with a single Table 3 shows the different isolated species corre- band lated with the onychomycosis clinical types previously mentioned. Out of the 34 dermatophyte-positive cul- Other yeast-like isolates corresponded to genera tures, T. rubrum was predominant (37%), corresponding Cryptococcus,
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