Report Oxford, UK International IJD Blackwell ?0011-9059 Publishing, Science, Journal 2003 of LtdDermatology
Characteristics of superficial mycoses in Malta
Superficial Vella Zahramycoses et al. in Malta
Loranne Vella Zahra, BPharm (Hons), MPhil, Paul. Gatt, MD, MRCP, Michael J. Boffa, MD, FRCP, FRCP, FAAD, MSc (Derm), DDerm, DGUM, Eileen Borg, MD, Dip Derm Sci, Edwin Mifsud, MD, Dip Derm, L/RAMC, Lawrence Scerri, MD, FRCP, CCST Derm, FAAD, Dino Vella Briffa, MD, PhD, and Joseph L. Pace, MD FRCP, FRCP, FCPP, FAAD
From Medical School, Mycology Laboratory, Department of Pathology, St. Luke’s Hospital, G’Mangia, Department of Dermatology, Sir Paul Boffa Hospital, Floriana, and St. Jude’s Medical Centre, Ta’Xbiex, Malta Correspondence Loranne Vella Zahra, BPharm, MPhil Clinipath Medical Laboratories Mycology Laboratory 217/3 Maring Street Pieta’ MSD 08 Malta E-mail:
[email protected]
Abstract Background A study was conducted to determine the chief agents of superficial mycoses in Malta. Data were collected over a 5-year period from mycologic investigations carried out on all dermatologic specimens sent to the Mycology Laboratory at St. Luke’s Hospital in Malta. Methods In the period between January 1995 and December 1999, a total of 1271 specimens from skin, nails, or hair were collected from 1200 clinically suspected cases of dermatomycoses. Results The fungi cultivated included dermatophytes (n = 371), yeasts (n = 33), and nondermatophyte filamentous fungi (n = 12). Trichophyton rubrum (n = 121) was the most prevalent, followed by Microsporum canis (n = 109), T. mentagrophytes (n = 80), M. gypseum (n = 27), Epidermophyton floccosum (n = 17), T. soudanense (n = 10), T. tonsurans (n = 2), T. verrucosum (n = 2), M. persicolor (n = 1), and T. violaceum (n = 1). Candida species were also cultivated, with C. parapsilosis (n = 14) being the most common, followed by C. albicans (n = 12) and C. tropicalis (n = 6). Nondermatophyte filamentous fungi were isolated from nail specimens only. Conclusions In this study, superficial fungal infections were reported more commonly in female (n = 207) than in male (n = 182) patients. M. canis was the chief agent of tinea capitis and tinea corporis, whilst T. rubrum was the main causative agent of tinea pedis, tinea manuum, and tinea unguium. Onychomycosis due to Candida species was more common in female than in male patients.
Introduction The chief etiologic agents of superficial mycoses are dermatophytes, but yeasts and nondermatophyte saprobic molds may also be involved. Whenever a superficial fungal infection is suspected clinically, mycologic investigations are indicated, especially if there are other differential diagnoses; such investigations will also be useful for the clinician in order to determine appropriate antifungal therapy. This is especially true for chronic infections, such as those caused by Trichophyton rubrum, and infections due to nondermatophyte filamentous fungi, which are increasingly being reported. Moreover, identification to species level is mandatory for epidemiologic purposes. The three small Maltese Islands, Malta, Gozo, and Comino, have a total population of about 400,000.1 Ambient temperatures may vary from 6.0 °C in winter to 41.0 °C in summer and humidity may be as high as 83%. Data on superficial infections are practically nonexistent, and this makes the task of assessing the public health significance of superficial mycoses © 2003 The International Society of Dermatology
quite difficult. We report here the data collected over a 5-year period (1995–99) from mycologic investigations carried out on all dermatologic specimens sent to the Mycology Laboratory at St. Luke’s Hospital in Malta. This is the first and, until recently, the only mycology laboratory in the Maltese Islands. Materials and methods Patients with suspected dermatomycoses, attending the only National Health Service (NHS) dermatology clinic on the Islands (at Sir Paul Boffa Hospital), or directly referred to the Mycology Laboratory at St. Luke’s Hospital, were included in the study. Patients with pityriasis versicolor were excluded from the study because the diagnosis of this condition is usually performed on clinical examination. Specimen collection, culture, and direct microscopy, and the isolation and identification of fungi were carried out using standard procedures.2 Chlamydospore and germ tube formation and assimilation tests were used for yeast identification. The culture medium used was Sabouraud glucose agar supplemented with chloramphenicol (0.05 g / L), with or International Journal of Dermatology 2003, 42, 265–271
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without cycloheximide (0.5 g/ L). A considerable number of specimens (n = 661) were sent to the laboratory already inoculated on Dermatoslide™ (BBL), which is a dipstick consisting of malt agar on one side and dermatophyte test medium on the other. For such specimens, it was not possible to carry out direct microscopy with 10% KOH. Statistical analysis was carried out using the chi-squared test with Yates’ correction.3
Results The total number of patients included in this study was 1200, 48% (n = 575) of whom were males and 52% (n = 625) were females. Positive cultures were obtained from 415 specimens collected from 32.0% (n = 389) of these patients. Table 1 summarizes the number and types of specimens processed for mycologic investigations. Direct microscopy and culture results are summarized in Table 2. The fungi cultivated included dermatophytes (n = 371), yeasts (n = 33), and nondermatophyte filamentous fungi (n = 12). Dermatophyte isolates
Patients with dermatophytoses (n = 353) were predominantly young, with a mean age of 29 years (range, 9 months to 77 years). There were slightly more female (n = 182) than male (n = 171) patients. Patients with tinea unguium in this study were also young adults, with a mean age of 38 years; there were no children with tinea unguium, the youngest patient being a 15-year-old girl. The dermatophytes cultivated were T. rubrum (n = 122), Microsporum canis (n = 109), T. mentagrophytes (n = 80), M. gypseum (n = 27), Epidermophyton floccosum (n = 17), T. soudanense (n = 10), T. tonsurans (n = 2), T. verrucosum (n = 2), M. persicolor (n = 1), and T. violaceum (n = 1). One of the isolates of T. tonsurans was T. tonsurans var. sulfureum. In the case of T. mentagrophytes isolates, there were 23 isolates identified as T. mentagrophytes var. interdigitale and 54 isolates identified as T. mentagrophytes var. mentagrophytes. The variety of the remaining three isolates could not be determined with certainty on observation of the colonies on the Table 1 Analysis of specimens
Specimen type Skin Nail debris, nail pieces Hair Genital smears Pus Total
Number of specimens
Specimens with a positive culture
903 228 127 4 9
275 73 66 0 1
1271
415
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primary Sabouraud plate, and hence they were identified as T. mentagrophytes. Both M. canis and T. rubrum were primarily isolated from young patients (Table 3). No definite pattern was obtained for other dermatophytes, such as T. mentagrophytes, which was isolated from all age groups. The majority of patients had tinea corporis (n = 143), mostly due to M. canis, which was also the chief agent causing nearly all cases of tinea capitis (Table 4). All patients with tinea capitis were children, except for two elderly women (Table 5). One of these patients was a 66-year-old woman who had five Persian cats at home; she had multiple ringworm lesions on her torso and abdomen, in addition to tinea capitis (caused by M. canis), which was noted only at the time of specimen collection. The other elderly female was 64 years of age and had tinea capitis due to T. soudanense. The single isolate of T. tonsurans var. sulfureum was responsible for tinea capitis in an 11-year-old boy. The only isolate of T. violaceum was cultivated from hair stubs collected from a 2-year-old girl from Pakistan who had been adopted by a Maltese family. Of the children with tinea capitis, 33 were males; there were also more male (n = 28) than female (n = 22) patients with tinea capitis caused by M. canis. The mean age of the patients with tinea capitis was 8 years, but when the two adult females were omitted, the mean age dropped to 6 years. T. rubrum was the principal dermatophyte causing tinea pedis, tinea manuum, and tinea unguium. Nearly all T. rubrum
Table 2 Direct microscopy and culture results Results
Number of specimens
M+ C+
183 (14.4%)
M– C+
23 (1.8%)
M+ C–
74 (5.8%)
M– C–
308 (24.2%)
Culture only (+) Culture only (–)
244 (19.2%)* 439 (34.5%)†
Total
1271
M, direct microscopy; C, culture. *There were 231 specimens that were sent already inoculated onto Dermatoslide™. The rest of the specimens were insufficient in quantity to be examined by both methods and hence only culture was performed. †There were 430 specimens that were sent already inoculated onto Dermatoslide™. The remaining specimens were insufficient in quantity to be examined by both methods and hence only culture was performed. © 2003 The International Society of Dermatology
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Table 3 Age distribution of patients with
dermatophytosis
Dermatophyte
0 –20 years
T. rubrum M. canis T. mentagrophytes M. gypseum E. floccosum T. soudanense T. verrucosum M. persicolor T. tonsurans T. tonsurans var. sulfureum T. violaceum Total
21– 40 years
41– 60 years
> 60 years
Total
23 77 18 6 4 4 2 1 – 1 1
51 20 35 4 7 3 – – – – –
33 8 18 12 6 1 – – 1 – –
6 1 4 5 – 1 – – – – –
113 106 75 27 17 9 2 1 1 1 1
137
120
79
17
353
Table 4 Distribution of dermatophytes by clinical condition Tinea barbae
Organism T. rubrum M. canis T. mentagrophytes M. gypseum E. floccosum T. soudanense T. tonsurans T. verrucosum T. violaceum M. persicolor
Tinea capitis
6 3 4 6
50 2
1 1
Total patients
Tinea faciei
2
4 1 1 1 1
2
60
22
Tinea unguium
Tinea manuum
25
1
16 2 7 2 2
31
29
5
Tinea corporis
Tinea pedis
Site unknown
Total patients
28 51 36 18 6 3 1
34
4
19
1
113 106 75 27 17 9 2 2 1
143
61
8
1
Table 5 Tinea capitis in patients according to age and sex Age (years)
Boys
Girls
Adults
Total
0–1 1–5 6–10 11–15 16–20 > 20
– 18 13 2 – –
1 9 14 – 1 –
– – – – – 2
1 27 27 2 1 2
Total
33
25
2
60
5
353
Some patients (n = 47) could link their clinical lesions to contact with an animal, with cats (n = 26 cases) being the most commonly mentioned animal. Rabbits (n = 12 cases) also featured prominently, and this was to be expected given the fact that there are many rabbit breeders in Malta who rear rabbits for food, as a hobby, or for competition purposes. Other animals included dogs (n = 7) and hamsters (n = 1). No relevant history of animal contact could be obtained with regard to the source of the single case of tinea capitis caused by T. verrucosum. Yeast isolates
strains belonged to the downy type, which is one regularly isolated from the European population. In the case of tinea unguium, toenails (n = 17) were more frequently infected with dermatophytes than fingernails (n = 1) (no information was supplied on the request form as to the type of the nail specimen in thirteen cases). E. floccosum was responsible for a single case of tinea unguium in a 37-year-old woman, who had onychomycosis of the right big toenail. © 2003 The International Society of Dermatology
Various yeasts were cultivated from 31 specimens (30 nail specimens and one skin specimen) from 30 patients; there were two nail specimens from the same female patient on separate occasions. The age ranged from 8 to 76 years, with a mean age of 41 years. The number of female patients (n = 22) who reported nail problems was much higher than male patients (n = 7) in this group (the mean age of patients with onychomycosis caused by yeasts was 40 years). Of the nail specimens submitted, there were four toenail specimens and 13 fingernail specimens; unfortunately, no data were given about the nature of the nail in the remaining 12 cases. International Journal of Dermatology 2003, 42, 265 –271
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Table 6 Patients with isolates of nondermatophyte filamentous fungi Patient
Sex
Age (years)
Clinical details
10% KOH
Culture
1
M
29
Big toenail dystrophy; nail debris sent twice on different dates and S. brevicaulis cultured twice
Septate hyphae and spherical, thick-walled conidia seen (in both instances)
Scopulariopsis brevicaulis
2
M
48
Onychomycosis of toenails; whole toenail sent
Septate hyphae and round, thick-walled conidia seen
Scopulariopsis brevicaulis
3
M
70
Onychomycosis affecting left little fingernail; whole nail sent
Abundant septate hyphae seen
Fusarium solani
4
M
13
Dystrophy and discoloration affecting left middle fingernail; nail debris sent twice on separate dates; A. flavus cultured twice
Abundant septate hyphae seen in both instances, and abundant green conidia and two deformed Aspergillus conidiophores seen in the preparation from the second specimen
Aspergillus flavus
5
F
22
Onychomycosis of the right little fingernail; nail debris sent twice on different dates and, finally, the whole fingernail was sent on the third occasion; F. oxysporum cultured in all three instances
Abundant hyphae and chlamydospores seen on all three occasions
Fusarium oxysporum
6
F
21
Whitish discoloration of both right and left big toenails. Nail debris sent twice from right toenail on different dates and finally, the right big toenail was also sent. F. solani was cultured in all three instances
Septate hyphae and chlamydospores seen in 1st and 3rd instances; there was insufficient material to perform KOH in the 2nd instance
Fusarium solani
M, male; F, female.
A total of 33 yeasts, all Candida species, were isolated. C. parapsilosis was the most frequently isolated species from the nail (n = 14), accounting for 42.4% of the isolates. C. albicans was the second most common (n = 12, 36.4%); one of the C. albicans isolates was cultured from the single skin specimen submitted. The third most commonly isolated species was C. tropicalis (n = 6, 18.2%) and, finally, there was a single isolate of C. guilliermondii (n = 1, 3.0%), all strains having been isolated from nail specimens. C. tropicalis was isolated once together with C. parapsilosis from the same specimen. In this study, for yeast infections, we report only the culture results for those specimens for which direct microscopy with 10% KOH showed budding yeasts and pseudohyphae and/or true hyphae. These isolates were reported as significant after carefully relating the direct microscopy results with the culture and the patient’s history. Nondermatophyte filamentous fungi
Only 12 nondermatophyte filamentous fungi were isolated from 12 specimens (Table 6). There were two female and four male patients, with an age range of 13–70 years and a mean age of 34 years. International Journal of Dermatology 2003, 42, 265 –271
Of the 12 specimens submitted, direct microscopy with 10% KOH was carried out for 11 specimens only. As in the case of the yeast isolates, the direct microscopy and culture results were cautiously interpreted before reporting the final results. Discussion There were more female than male patients, which is similar to the results of other studies.4–6 This could be due to the fact that females may more readily seek advice at the dermatology clinic, because they may be more conscious of their physical well-being than males. Other studies, however, have shown a higher male prevalence of dermatophytosis.7–10 It is worth noting that up to 6% (n = 74) of specimens were positive on direct microscopy (septate hyphae and arthrospores), but failed to yield a culture, sometimes even with consecutive specimens. There are various reasons for this: patients might have already been treated for a few days before specimen collection, or the specimens may have consisted mainly of skin or nail tissue with dead and hence nonviable fungal hyphae. © 2003 The International Society of Dermatology
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This study confirms previous reports that dermatophytosis is most prevalent in the younger age group, which is probably due to the heightened physical activities common in this group.4,7 The results obtained are in agreement with other studies, which show that, worldwide, T. rubrum heads the list of isolated dermatophytes as the most frequent isolate reported.5,7,10–16 The patients with tinea unguium in this study were young. This result is consistent with some reports,5,10,11,13–15 but differs from others, which show an increased prevalence of this infection in patients who are more than 50 years of age.17–19 Children were the least affected by tinea unguium, as reported in other studies.15,18 There were more females (n = 17) than males (n = 14) with tinea unguium (Although this was not found to be statistically significant at P < 0.05), which differs from other reports.8,15 From the results of this study, toenails were more commonly infected with dermatophytes than fingernails, which is similar to some reports,18,19 but differs from others.15 Although infected fingernails may give rise to more cosmetic concern, infected toenails may also affect the psychologic and physical well-being of patients, particularly in the hot summer months which, in Malta, last from early May until late November. Various studies, as well as this investigation, have reported M. canis as the most common agent of tinea capitis and tinea corporis.4,20–28 Children are more commonly affected with tinea capitis than adults, probably because of the increased fungistatic action of triglycerides in the sebum produced at puberty.29 It is worth noting that a reduction in triglycerides in sebum may predispose postmenopausal women to the development of tinea capitis more often than other adults,29 as in the case of the two elderly female patients with tinea capitis. The higher male preponderance of tinea capitis in this study is similar to that reported by other workers.7,8,20,21,30,31 Tinea capitis due to Trichophyton species may affect males and females equally, but, in tinea capitis due to M. canis, males are more likely to be affected than females.28,32 Comparable results were also obtained in the present study, although the difference was not found to be statistically significant (P < 0.05). The predominance of M. canis is probably due to the contact of children and adults with pets, particularly long-haired cats and dogs. The frequent contact of adults with children may result in adults becoming asymptomatic carriers of the condition, and thereby contributing to its wider spread. Hence, it is important to treat children with active disease and screen for and treat any adult carriers with whom children with tinea capitis might have had contact.33 Other studies have reported different dermatophytes as the main agents responsible for tinea capitis; the epidemiology changes significantly with population movements and a change in customs: T. violaceum in Tripoli, Libya,30 the Transvaal, South Africa,12 and Basrah, Iraq;31 M. audouinii in eastern Nigeria;34 T. schoenleinii in Borno State, Nigeria;35 and, until © 2003 The International Society of Dermatology
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1984, T. mentagrophytes in Alberta, Canada.8 In Ontario, Canada, different regions of the USA, and, more recently, in the UK, however, there has been a shift favoring T. tonsurans as the major etiologic agent of tinea capitis in these countries.36–40 We have not yet observed such a preferential change to T. tonsurans in the Maltese Islands. We also report here the first isolations of several dermatophytes as human pathogens in the Maltese Islands (mycologic investigations of clinical specimens were first performed in 1995): M. persicolor, T. violaceum, and T. tonsurans var. sulfureum. The single case of imported T. violaceum may reflect the common occurrence of this dermatophyte as an agent of tinea capitis in Pakistan.41 With regard to yeast isolates, this study showed that 2.5% of patients had nail or skin infections due to Candida species. C. parapsilosis was the main yeast isolated from nail specimens; other studies have reported C. albicans as the principal yeast isolated from nail and skin specimens.42,43 C. albicans is not a normal commensal of the skin and nails (although it can occasionally be found on the skin).44–46 Cutaneous candidosis is generally caused by C. albicans, but other Candida species may be involved; it often occurs in warm, moist conditions, such as in skin folds, particularly in tropical climates or during the summer months.43–46 On the other hand, C. parapsilosis is a common inhabitant of normal skin, and this presumably serves as a reservoir of infection for the nails. The prevalence of skin mycoses and onychomycoses caused by yeasts is steadily increasing.25,47,48 The results of this study concur with previous reports that Candida onychomycosis occurs more frequently in females than in males,6,10,42 (in this study, such a gender difference was not found to be statistically significant at P < 0.1). Local factors that were found to promote nail infections in the study patients included occlusion, trauma during manicure, and prolonged contact with water and detergents, similar to those reported by other workers.18,49 Nondermatophyte filamentous fungi were isolated from relatively young patients. This observation contrasts with the reports of others, which show that onychomycosis due to these molds generally tends to occur later in life, usually in patients over 50 years of age.50 Fusarium species (n = 7) were the most common nondermatophyte molds to be isolated in this study, followed by Scopulariopsis brevicaulis (n = 3) and Aspergillus species (n = 2). This is similar to the results reported by Lim et al.,10 but contrasts with those reported by Seneckzo et al.,42 where Aspergillus species were the most common molds to be isolated in a 10-year period. The pathogenic role of nondermatophyte filamentous fungi is debatable in patients who submit only one specimen and in whom direct microscopy reveals no additional information; however, in cases in which direct microscopy can be related to culture results, the isolated fungi may be responsible for onychomycoses. Indeed, we observed two patients who submitted only one specimen consisting of a whole nail, but in whom the KOH International Journal of Dermatology 2003, 42, 265 –271
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examination was consistent with the nondermatophyte mold grown as a pure culture. Ideally, positive direct microscopy and isolation of the same fungus from successive specimens of the infected nail (three in total), without isolation of dermatophytes (although dual infections can occur), are necessary to establish the significance of nondermatophyte filamentous fungi. Acknowledgments Dr Rinaldo Mercantini, Laboratorio di Microbiologia, Sezione di Micologia, Istituto Dermatologico S. Gallicano, Rome, Italy, confirmed the identity of M. persicolor, and Dr Dag Harmsen, Institut für Hygiene und Mikrobiologie, Bayerische Julius-Maximilians-Universität, Wurzburg, Germany, confirmed the identity of T. tonsurans var. sulfureum. Mr Stephen Decelis provided technical assistance and Dr Michael Camilleri, Dr Stephanie Lateo, Dr Godfrey Baldacchino, and Dr Antoine Ellul contributed to specimen collection. References 1 Demographic Review of the Maltese Islands – 1996. Malta: Central Office of Statistics, 1997. 2 Clayton YM, Midgley G. Identification of agents of superficial mycoses. In: Evans EGV, Richardson MD, eds. Medical Mycology, A Practical Approach. Oxford: IRL Press at Oxford University Press, 1989: 65– 95. 3 Spiegel MR. The chi-squared test. Theory and Problems of Statistics. Singapore: McGraw-Hill, 1981: 201–216. 4 Casal M, Linares MJ, Fernandez JC, Solis F. Dermatófitos y dermatofitosis en Córdoba (España). Enferm Infecc Microbiol Clin 1991; 9 (8): 491–494. 5 Macura AB, Laskownicka Z, Macura C. Fungi causing superficial cutaneous mycoses in the district of Cracow – Part one: the incidence of dermatophytes. Mykosen 1984; 27 (1): 36 –42. 6 Macura AB, Laskownicka Z, Macura C. Fungi causing superficial cutaneous mycoses in the district of Cracow – Part two: the incidence of yeast-like fungi and moulds. Mykosen 1984; 27 (2): 102–106. 7 Lim JTE, Goh CL, Chua HC. Pattern of dermatophyte infection in Singapore. Ann Acad Med 1992; 21 (6): 781–784. 8 Sekhon AS, Garg AK. A 13-year (1972–1984) study of dermatophytic infections in Alberta, Canada. Mykosen 1986; 29 (6): 255–262. 9 Badillet G. Dermatophytes et immigration. Ann Biol Clin 1988; 46: 37–43. 10 Lim JTE, Chua HC, Goh CL. Dermatophyte and non-dermatophyte onychomycosis in Singapore. Australas J Dermatol 1992; 33: 159–163. 11 Devliotou-Panagiotidou D, Koussidou-Eremondi T, Karakatsanis G, et al. Dermatophytosis due to Trichophyton rubrum in northern Greece during the decade 1981–1990. Mycoses 1992; 35: 375–380. International Journal of Dermatology 2003, 42, 265 –271
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