sign in sign up
<<
Home , Chrysosporium, Tinea capitis, Tinea corporis, Tinea cruris, Trichophyton rubrum, Trichophyton tonsurans

Medical Mycology August 2011, 49, 608–611

Epidemiology of superfi cial fungal diseases in French Guiana: a three-year retrospective analysis

CHRISTINE SIMONNET * , FRANCK BERGER * & JEAN-CHARLES GANTIER † * Institut Pasteur de la Guyane, Cayenne , France, and † Institut Pasteur, Paris , France

A three-year retrospective analysis of fungi isolated from specimens of patients with superfi cial fungal in French Guiana is presented. Clinical samples from 726 Downloaded from https://academic.oup.com/mmy/article/49/6/608/972117 by guest on 27 September 2021 patients with presumptive diagnoses of (28.2% of the patients), (27.8%), superfi cial cutaneous mycoses of the feet (22.0%), and of other areas of the body (21.9%), were assessed by microscopic examination and culture. Dermato- phytes accounted for 59.2% of the isolates, followed by (27.5%) and non-der- matophytic (13.1%). rubrum was the most common recovered from cases of onychomycosis (67.4%), tinea pedis (70.6%) and (52.4%). In contrast, was the predominant species associated with tinea capitis (73.9%). Yeasts were identifi ed as the principal etiologic agents of onychomycosis of the fi ngernails (74.2%), whereas molds were found mainly in cases of onychomycosis of the toenails. In such instances, Neo s cytalidium dimidiatum (70.8%) was the most common recovered in culture. In conclusion, the prevalence of T. rubrum and the occurrence of onychomycosis and fungal infections of the feet in French Guiana are similar to results reported from Europe, whereas the frequency of tinea capi- tis and the importance of T. tonsurans in such infections are similar to the situation in the Americas. Keywords , molds , yeasts , French Guiana, superfi cial fungal infections

Introduction superfi cial mycoses, in order to identify the specifi cities of fungal infections in a subtropical region of Europe. The very high prevalence of superfi cial mycoses and their worldwide distribution make them one of the most com- mon dermatological diseases. Their incidence depends on Materials and methods climatic and geographic conditions and is infl uenced, From January 2006 to December 2009, 726 patients with beyond individual factors such as age and host defences, presumptive diagnoses of fungal infections were referred by individual and social behaviors [1]. Due to their hot and to the medical laboratory of the Pasteur Institute by der- damp climates, these infections are particularly common matologists. Skin scrapings and fl uids were microscopi- in tropical and subtropical areas. French Guiana is an over- cally examined. and nails were predigested with 20% seas region of France located in the rain forest of South Potassium hydroxide (KOH) on a microscopic slide and America, and so combines environmental and cultural fac- staining with water soluble methyl blue was used when tors of subtropical areas with the socioeconomic character- necessary [2]. Portions of the specimens were then inocu- istics of Europe. The epidemiology of fungal diseases in lated onto Sabouraud dextrose agar with chloramphenicol this region has not been previously described and the pur- and Sabouraud dextrose agar with chloramphenicol and pose of this study was to determine the causative agents of cycloheximide. Cultures were incubated at 25 ° C and exam- ined twice a week. Identifi cation of fungi was based on growth rate, macroscopic appearance and color of colo- Received 8 August 2010; Received in fi nal revised form 14 December nies, pigmentation of medium and microscopic morphol- 2010; Accepted 26 January 2011 Correspondence: C. Simonnet, Institut Pasteur de la Guyane, BP 6010, ogy. A Sellotape touch preparation in lactophenol cotton 97306 Cayenne CEDEX, France. Tel.: ϩ 59 45942 95807; fax: ϩ 59 45943 blue was used for observation of microscopic characteris- 09916; E-mail: [email protected] tics of molds recovered in culture. For identifi cation of

© 2011 ISHAM DOI: 10.3109/13693786.2011.558929 Fungal diseases in French Guiana 609 yeasts, 19 biochemical tests were carried out using the API into the following four categories; onychomycosis – 28.2% 20C AUX (bioMerieux, France) [3]. When required for (205/726 patients), superfi cial involvement of the feet – species identifi cation of dermatophytes, auxiliary tech- 22.0% (160/726), suspected tinea capitis – 27.8% (202/726), niques were performed such as subculture on Borelli and superfi cial mycoses of the body – 21.9% (159/726). lactrimel agar (SR2 B, France) for strains in The rate of recovery of the fungi in culture and the identity order to promote production of conidia and the perfor- of these fungi varied with the disease. mance of in vitro hair perforation test [4]. Finally, the From the 205 patients (M/F ratio, 47%; median age, 34) results of direct microscopic examination, colony growth with onychodystrophy, toenail samples were collected characteristics, clinical relevance and epidemiologic back- from 159 of the patients (77.6%) and fi ngernail specimens, ground of the isolates were evaluated to support their role the second most common site, were obtained as the etiologic agents. Growth in at least three of the fi ve from 46 patients (22.4%). Thickened nails, color changes points of inoculation in culture, pure cultures of the recov- and less commonly onycholysis, were observed. The con- Downloaded from https://academic.oup.com/mmy/article/49/6/608/972117 by guest on 27 September 2021 ered molds or yeasts, presence of hyphae or yeasts and ditions often went untreated for several months. The results their abundance noted in the direct preparation of the spec- (Table 1) showed the role played by dermatophytes as imens, were required to conclude the pathogenic roles of agents of onychomycosis of the toenails in that 44.4% yeasts and molds. In addition, the type of lesions, the clin- (52/117) of isolates recovered were fungi in this group, ical symptoms, the existence of predisposing factors, the with non-dermatophyte molds comprising 35% (41/117) of patient’ s history, were compared with the identifi cation of isolates. was the principal etiologic the fungi and contributed to the interpretation of their agent of toenail onychomycosis followed by the non-der- clinical relevance. When required by the dermatologists, matophyte Neoscytalidium dimidiatum . In contrast, yeasts repeated mycological evaluations were performed. Speci- were responsible for 74.2% of onychomycosis of the fi n- mens were declared negative if the isolates did not meet gernails (23/31) and accounted for 54.8% these criteria or if there was no fungal growth after six (17/31) of the fungi isolated in culture (Table 1). weeks of incubation. Superfi cial mycoses of the feet were suspected in 160 patients (M/F ratio, 85%; median age, 40). The lesions were interdigital for 64 patients (40%) and plantar for 73 Results patients (45.6%). Scaly plaques were the most common During the study period, 726 patients were tested whose clinical feature (43%) followed by fi ssures, hyperkeratosis mean age was 34 years (range, Ͻ 1 – 87 years) and 54% and vesicles. A majority of patients complained of pruritus. (392/726) were women. The clinical diagnoses were classifi ed Dermatophytes accounted for 52.6% of isolates (51/97),

Table 1 Fungal isolated in onychomycosis.

Toenails n % Fingernailsn %

Dermatophytes Dermatophytes Trichophyton rubrum 35 67.4 Trichophyton rubrum 360 Trichophyton mentagrophytes 12 23.2 Trichophyton mentagrophytes 240 3 5.7 Molds Trichopyton tonsurans 1 1.9 Scopulariopsis brevicaulis 1 33.3 1 1.9 Onychocola canadensis 1 33.3 Molds niger 1 33.3 Neoscytalidium dimidiatum 29 70.8 Yeasts oxysporum 5 12.3 Candida albicans 17 73.9 Scytalidium hyalinum 3 7.3 2 8.7 Aspergillus sp. 1 2.4 Candida parapsilosis 2 8.7 sp . 1 2.4 Candida guilliermondii 1 4.3 Penicillium sp. 1 2.4 Candida famata 1 4.3 Scopulariopsis brevicaulis 1 2.4 Yeasts Candida parapsilosis 10 41.7 Candida albicans 7 29.2 inkin 2 8.3 Candida tropicalis 2 8.3 Rhodotorula mucilaginosa 2 8.3 Trichosporon asahii 1 4.2

n , number of isolates; %, percentage of the different species.

© 2011 ISHAM, Medical Mycology, 49, 608–611 610 Simonnet et al . yeasts 30.9% (30/97) and non-dermatophyte molds made Discussion up 16.5% (16/97) of the fungi recovered. Trichophyton Distribution of superfi cial mycoses varies among countries rubrum accounted for 70.6% (36/51) of the dermatophytes, in relation to the ecology of the fungi. Climatic, socioeco- C. albicans for 36.7% (11/30) of the yeasts and N. dimid- nomic and even historical factors can explain the variations iatum for 62.5% (10/16) of the molds (Table 2). in the frequency of the infected anatomic sites [5]. In our While tinea capitis was not observed in adults, it was study, a nearly equal distribution of cases among four clinically suspected in 202 patients (M/F ratio, 120%) of clinical presumptive diagnoses – onychomycosis, tinea whom 168 (83%) were prepubertal children. The promi- capitis, superfi cial cutaneous mycoses of the feet and der- nent clinical fi ndings in confi rmed cases were alopecia for matomycoses of other areas of the body – was observed. 65% of the patients, scaly patches of the for 13%, Dermatophytes accounted for 59.2% of the agents identi- and both clinical features for 22%. Follicular pustules were fi ed. Trichophyton rubrum was the most common causative Downloaded from https://academic.oup.com/mmy/article/49/6/608/972117 by guest on 27 September 2021 observed in 15 patients and celsi in three. Dermato- agent of superfi cial fungal infections being involved in 97 phytes were recovered from samples of 119 patients cases and representing 21% of isolates. These results are (58.9%) and were the sole potential pathogens associated far from the 70 – 80% prevalence found in some studies with these patients. Trichophyton tonsurans was the most carried out in Europe or in subtropical America [6,7]. Con- common dermatophyte isolated (73.9%; 88/119) in this sidering specifi c locations, it can be noted that in onycho- pathology (Table 2). of the toenails, most cases were caused by Several lesions affecting the limbs, face, thorax, abdo- T. rubrum , followed by T. mentagrophytes . The same obser- men, groin, , buttocks, gluteal cleft, palms, neck, vations are found in European and South American reports chest, submammary folds, shoulders and back, were [8,9]. The non-dermatophyte mold N. dimidiatum , found observed in 159 patients (M/F ratio, 100%; median age, mainly in tropical and subtropical areas, was the second 37). The clinical features varied according to the body most common agent of toenail onychomycosis in our prac- area and the fungal agent involved, but dry, scaly ery- tice. In Europe, few cases are described and these usually thematous plaques were the prominent finding. Der- are found as a result of tourism and immigration [10]. matophytes comprised 46.7% of the isolates (42/90) and Whereas dermatophytes were predominant in fungal infec- yeasts 53.3% (48/90), including two cases where tions of the toenails, yeasts were the main causative agent spp. was diagnosed on clinical signs and of infections of the fi ngernails. The signifi cant role played microscopic examination but was not isolated in culture. by yeasts in tropical onychomycosis is highlighted by According to the criteria set for relevance, no non-der- Brazilian studies [11,12]. matophyte molds were considered to be the causative In fungal infections of the feet, the species involved agents of the lesions (Table 2). Candida albicans (28.9%; were the same as in onychomycosis – T. rubrum , T. men- 26/90) and T. rubrum (24.4%; 22/90) were the most fre- tagrophytes , C. albicans and N. dimidiatum – suggesting quent pathogens identifi ed. possibly identical routes of infection and risk factors.

Table 2 Fungal pathogens isolated in tinea pedis, tinea corporis and tinea capitis.

Tinea pedisn % Tinea corporisn % Tinea capitis n %

Dermatophytes Dermatophytes Dermatophytes T. rubrum 36 70.6 T. rubrum 22 52.4 T. tonsurans 88 73.9 T. mentagrophytes 11 21.5 M. canis 7 16.6 T. mentagrophytes 10 8.4 E. fl occosum 2 3.9 T. tonsurans 5 11.9 M. canis 9 7.5 M. canis 1 1.9 E. fl occosum 3 7.1 M.audouinii 6 5.0 T. schoenleinii 1 1.9 T. mentagrophytes 3 7.1 M. gypseum 2 1.7 Molds M. audouinii 1 2.4 M. langeronii a 1 0.8 N. dimidiatum 10 62.5 M. praecox 1 2.4 T. rubrum 1 0.8 Fusarium sp. 2 12.5 T. verrucosum 1 0.8 Yeasts Yeasts C. albicans 11 36.7 C. albicans 26 54.2 C. parapsilosis 6 20.0 C. parapsilosis 15 31.2 C. famata 3 10.0 C. famata 2 4.2 R. mucilaginosa 2 6.6 R. mucilaginosa 2 4.2 C. glabrata, krusei, guilliermondii, tropicalis 4 13.3 Malassezia sp. 2 4.2 Trichosporon sp. , asahii, inkin 3 10.0 T. inkin 1 2.1 Cryptococcus laurentii 1 3.3

n , number of isolates; %, percentage of the different species; a Patient coming back from holidays in sub-Saharan Africa.

© 2011 ISHAM, Medical Mycology, 49, 608–611 Fungal diseases in French Guiana 611

In the fourth clinical category, we included different 5 Seebacher C, Bouchara JP, Mignon B. Updates on the epidemiology dermatomycoses, i.e., , , fungal of dermatophytes infections. Mycopathologia 2008; 166 : 335 – 352. infections of the arms and legs, and . The latter 6 Kemna ME, Boni EE. A US epidemiological survey of superfi cial fun- gal diseases. J Am Acad Dermatol 1996; 35 : 539 – 542. accounts for only a few cases, although it is a common 7 Lopez-Martinez R, Manzano-Gayosso P, Hernandez-Hernandez F, observation noted in several reports from tropical countries et al. Dynamics of frequency in Mexico: an analysis [13,14]. Candidosis was the prominent disease followed by of 2084 cases. Med Mycol 2010; 48 : 476 – 479. T. rubrum infections. Only a few cases were related to the 8 Perea S, Ramos MJ, Garau M, et al . Prevalence and risk factors of zoophilic dermatophyte Microsporum canis, in contrast tinea unguium and tinea pedis in the general population in Spain. J Clin Microbiol 2000; 38 : 3226 – 3230. with its prevalence in Europe [15,16]. 9 Flores JM, Castillo VB, Franco FC, et al . Superfi cial fungal infec- Similarly, whereas M. canis remains the most common tions: clinical and epidemiological study in adolescents from mar- causative agent of tinea capitis in Europe [17– 19], it was ginal districts of Lima and Callao, Peru. J Infect Dev Ctries 2009; 3 : the agent of only a few cases of tinea capitis in French 313 – 317. Downloaded from https://academic.oup.com/mmy/article/49/6/608/972117 by guest on 27 September 2021 Guiana. The anthropophilic T. tonsurans, uncommon in 10 Soler CP, Gerome P, Leguyadec T, et al . Scytalidium dimidiatum pseudodermatophyte, agent of superfi cial mycoses and phaehypho- Metropolitan France outside of the description of a few mycosis. Med Trop 1999; 59 : 375 – 377. sporadic cases [20], was the predominant species recov- 11 Godoy-Martinez P, Nunes FG, Tomimori-Yamashita J, et al . Onycho- ered from cases as described in US [6,21], Brazilian and mycosis in Sao Paulo, Brazil. Mycopathologia 2009; 168 : 111 – 116. Haitian surveys [22,23]. 12 Souza LKH, Fernandes OFL, Passos XS, et al . Epidemiological and In conclusion, whereas the epidemiology of fungal infec- mycological data of onychomycosis in Goiania, Brazil. Mycoses 2009; 53 : 68 – 71. tions in French Guiana shows some of the hallmarks found 13 Brilhante RS, Paixao GC, Salvino LK, et al . Epidemiology and ecol- in European studies – chiefl y the prevalence of T. rubrum ogy of dermatophytosis in Fortaleza city: Trichophyton tonsurans as and the place of onychomycosis and fungal infections of the an important emergent of tinea capitis. Rev Soc Bras Med feet – many features seem close to those observed in Amer- Trop 2000; 33 : 417 – 425. ica, particularly in the neighboring country, Brazil, as for 14 Kamalam A, Thambia AS. A study of 3891 cases of mycoses in the tropics. Sabouraudia 1976; 14 : 129 – 148. example the importance of T. tonsurans in tinea capitis, the 15 Asticcioli S, Di Silverio A, Sacco L, et al . Dermatophyte infections in frequency of tinea capitis, nearly completely eradicated in patients attending a tertiary care hospital in northern Italy. New Micro- Europe [5], and the role of yeasts in onychomycosis. biol 2008; 31 : 543 – 548. Finally, the occurrence of molds other than dermato- 16 Maraki S, Nioti E, Mantadakis E, et al. A 7-year survey of dermato- phytes, above all the large number of infections caused by phytoses in Crete, Greece. Mycoses 2007; 50 : 481 – 484. 17 Ginter-Hanselmayer G, Weger W, Ilkit M, et al. Epidemiology of tinea N. dimidiatum , seems a distinctive and specifi c aspect of capitis in Europe: current state and changing patterns. Mycoses 2007; dermatomycoses in French Guiana. 50 : 6 – 13. 18 Hay RJ, Robles W, Midgley G, et al. Tinea capitis in Europe: new perspectives on an old problem. J Eur Acad Dermatol Venereol 2001; Declaration of interest : The authors report no confl icts of 15 : 229 – 233. interest. The authors alone are responsible for the content 19 Cremer G, Bousseloua N, Roudot-Thoraval F, et al . Tinea capitis and writing of the paper. in Creteil: trends over ten years. Ann Dermatol Venereol 1998; 125 : 171 – 173. 20 Vigui é -Vallanet C, Serre M, Masliah L, et al . Epidemic of Trichophy- References ton tonsurans tinea capitis in a nursery school in the Southern suburbs of Paris. Ann Dermatol Venereol 2005; 132 : 432 – 438. 1 Havlickova B, Czaika VA, Friedrich M. Epidemiological trends in 21 Wilmington M, Aly R, Frieden IJ. Trichophyton tonsurans tinea capi- skin mycoses worldwide. Mycoses 2008; 51 : 2 – 15. tis in San Francisco Bay area: increased infection demonstrated in 20- 2 Ellis DH. Diagnosis of onychomycosis made simple. J Am Acad year survey of fungal infections from 1974 to 1994. J Med Vet Mycol Dermatol 1999; 40 : 3 – 8. 1996; 34 : 285 – 287. 3 Roberts GD, Wang HS, Hollick GE. Evaluation of the API 20C micro- 22 Brilhante RS, Cordeiro RA, Rocha MF, et al. Tinea capitis in a derma- tube system for the identifi cation of clinically important yeasts. J Clin tology center in the city of Fortaleza, Brazil: the role of Trichophyton Microbiol 1976; 3 : 302 – 305. tonsurans . Int J Dermatol 2004; 43 : 575 – 579. 4 Sinski JT, Van Avermaete D, Kelley LM. Analysis of tests used to dif- 23 Raccurt CP, Dorsainvil D, Boncy M, et al. The emergence of ferentiate Trichophyton rubrum from Trichophyton mentagrophytes . J Trichophyton tonsurans in Port-au-Prince, Haiti. Med Mycol 2009; Clin Microbiol 1981; 13 : 62 – 65. 47 : 197 – 200.

This paper was fi rst published online on Early Online on 17 February 2011.

© 2011 ISHAM, Medical Mycology, 49, 608–611