The emergence of Trichophyton tonsurans in Port-au-Prince, Haiti.

The occurrence of the anthropophilic dermatophyte Trichophyton tonsurans as a frequent causative agent of tinea capitis in several developed countries has been associated with a global rise in its isolation during recent years. While T. tonsurans was never found in Haiti before 1988, a sharp increase in the number of isolates of this species from scalp lesions began to be observed in 2005 in Port-au-Prince, Haiti. A prospective study was conducted in Port-au-Prince from May to November 2006 of 64 children presenting with tinea capitis at the dermatological outpatient clinic of the university hospital. Forty-five (70%) were male and 19 female (30%), with an average age at presentation of 6.1 years (age range 1-16 years). Direct microscopic examination of scalp hair using 10% potassium hydroxide was positive in 93.8% and culture confirmation was established in 55 cases (85.9%). Five species of dermatophytes were identified, with the anthropophilic dermatophyte T. tonsurans, accounting for the majority or 35 (63.6%) of all cases of tinea capitis. Other dermatophyte species identified included T. mentagrophytes (14.5%), Microsporum audouinii (12.7%), T. rubrum (7.3%) and in one case, the geophilic M. gypseum (1.8%). In two cases caused by T. tonsurans skin involvement on other areas of the body was recorded. The most frequent pathogen in tinea capitis is now T. tonsurans in Port-au-Prince. We speculate that the recent emergence of T. tonsurans in Haiti is linked to the dramatically increasing mobility of Haitian Diaspora.


Introduction
Skin, hair and nails infections by dermatophytic fungi are common in developed and developing countries alike. However, the species involved and the clinical presentations may vary both geographically and with time. Tinea capitis remains a common infection in paediatric populations and has become an increasingly and important public health issue around the world. The emergence or re-emergence of Trichophyton tonsurans has been pointed out in several countries in the past decade and asymptomatic carriers of dermatophytes have been shown to have a role in inter-human transmission [1Á3].
In developed countries, the pattern of infection is changing with a dramatic increase in infections caused by anthropophilic dermatophytes, particularly T. tonsurans. This strongly contagious dermatophyte has been the cause of health problems among children in the United States since the 1950s [4]. T. tonsurans-related tinea capitis has been increasing in importance in childhood tinea for the past decades in the US [5Á10], and more recently in Canada [11], Australia [12], and Europe [13Á16]. In the US, T. tonsurans infection is more prevalent among African American children [17,18], with the percentage of the recorded cases of T. tonsurans correlating significantly with the percentage of blacks in large cities (100,000 people or more) [8]. Similar results have been found with Afro Caribbean and African descent children in the UK [19] and Ireland [15]. In Australia, strains of T. tonsurans cause infections almost exclusively in aboriginal patients [20]. In France, an increase of T. tonsurans-related tinea capitis has been recently observed [3,21], particularly in adopted children from Haiti (N. Contet-Audonneau, personal communication).
From this data it became obvious that an evaluation of the frequency of T. tonsurans scalp infections in the paediatric population in Haiti was needed. A prospective study was conducted in 2006 in the dermatologic clinic at the university hospital in Port-au-Prince.

Material and methods
The present prospective study took place from 24 May to 30 November 2006 at the dermatology outpatient clinic of the university hospital in Port-au-Prince. Children who came with scalp lesions resembling tinea capitis, and for whom a parental consent was obtained, were enrolled in the study. Samples were taken at the time of initial examination and were sent to the referral laboratory located in Port-au-Prince (Laboratoire Boncy-Pereira) on the same day for direct microscopic examination and culture.
Hair specimens and scaling were taken using forceps and scalpel. Direct microscopic examination in 10% potassium hydroxide (KOH) was conducted. Culture on Sabouraud dextrose agar with chloramphenicol without cycloheximide were incubated at room temperature (about 258C) and examined for the appearance of typical colonies for 30 days.
Species were identified according to the macroscopic and microscopic phenotypic features of the cultures [22,23].

Results
Sixty-four children have been included during the 6-month study period. The age/sex distribution is shown in Table 1. The average age at presentation was 6.1 years (age range 1Á16 years). Boys are more frequently infected than girls (sex ration 01.4) with 50% of cases found in the 5Á7 age group and with 98.5% being aged 1Á12 years.
Direct examination of hair or scaling after addition of a drop of 10% KOH was positive for 60 cases (94%). Hair morphology showed endothrix invasion in 41 cases (64%), ectothrix in 15 cases (23%), and ectoendothrix fungus in three cases (5%). Four cases were negative and one was questionable. Positive culture of dermatophytes was obtained from specimens of 55 patients (85%). The repartition of species is shown in Table 2.

Discussion and conclusion
This six-month prevalence study of the dermatophytes causing tinea capitis in children in Haiti demonstrated for the first time the spectrum of species circulating in the urban middle class population in Haiti's capital, Port-au-Prince. Three anthropophilic species were identified (T. tonsurans 063.6%; M. audouinii 012.7%; T. rubrum 07.3%), one zoophilic species (T. mentagrophytes 014.5%), and one geophilic species (M. gypseum 01.8%). The lack of M. canis in this survey is remarkable. Indeed, this dermatophyte is frequently found in other Caribbean countries such as Trinidad (20%) [24], Martinique (56.6%) [25], and in Brazil (respectively 38.97% and 70.5%) [26,27]. However for the majority of the Haitian population there is limited association with pets and therefore dogs and cats are usually kept at a distance. This is probably one of the reasons that M. canis is rarely found as a causative agent of tinea capitis or tinea corporis in children in Haiti, except for those in the upper class.  As usually observed among the paediatric population, lesions of the scalp in Haiti occurred from the age of one year until before the age of puberty. In this study, all children seen for dermatophytic scalp lesions were aged between 1 and 12 years, except one 16-year male infected by M. audouinii. More males were affected than females in all age groups. Children younger than 8 years old accounted for more than 75% of the cases (76.5%). The epidemiologic profile of tinea capitis in children in Haiti is very similar to those found in Trinidad [24], Martinique [25], Brazil [27] in children under 16 years, or in Ireland [15], and in France [21] in children of African descent.
Increased incidence of T. tonsurans tinea capitis has been recently observed in developed countries, particularly in North America [5Á11] and Europe [13Á16]. Before 1988, no case of T. tonsurans was found in Port-au-Prince. Between 1960 and 1987, six species were reported as causative agents of tinea capitis or tinea corporis among patients attending private clinics in Port-au-Prince, i.e., M. audouinii, M. canis, M. gypseum, T. mentagrophytes, T. rubrum and T. verrucosum. The first case of T. tonsurans identified by the mycology section of the Laboratoire Boncy-Pereira in Port-au-Prince was found on 9 October 1988. No further cases were noted in the following three years (1989Á1991). Since 1992, T. tonsurans was found associated with infections from time to time. The prevalence of T. tonsurans increased dramatically during the two last years with 74 cases found with 158 scalp examinations (47%) in 2006 and (40%) in 2007. Our prospective study confirms the recent emergence of this dermatophyte in the capital city of Port-au-Prince with a rate of 63.6% of T. tonsurans. Today in Haiti tinea capitis in children is due mostly to this very contagious anthropophilic dermatophyte.
The youngest case was 1 year old and the majority of diagnosed and confirmed cases were in children less than 5 years of age, with a clear male predominance. Two boys aged respectively 18 months and 2 years displayed both tinea capitis and tinea corporis. The same observation was made in Martinique where T. tonsurans has been isolated with increased frequency since 1998; the rate of tinea capitis-related to T. tonsurans was 31% for the period 1997Á2001 [25].
In Port-au-Prince, the majority of cases of T. tonsurans tinea capitis presented the clinical aspect of small circular bald patches with short hair stubs or broken hair within hair follicles (91% of the cases). In three cases, we observed large bald patchy spots, as reported in Martinique [25]. The number of lesions observed that had the aspect of small patchy spots with central scaling ranged from 1Á36; multiple baldish and scaly patches were not well-defined in six cases. However, some dermatophyte isolates may present very atypical features, particularly T. tonsurans and can be confused with atypical T. soudanense or T. mentagrophytes. Therefore, it would be of interest, in the future, to employ physiological, biochemical, and even molecular methods to more specifically determine the dermatophytes circulating in the Haitian population.
The increase of tinea capitis cases caused by T. tonsurans in children in Port-au-Prince during recent years is the principal and the most significant data uncovered by this survey. A recent review of worldwide dermatophytes isolations over the past three decades, with emphasis on the causal agents of tinea capitis, has shown changing patterns of dermatophytes species, underlining the rise of T. tonsurans in the world [16]. However, it is difficult to be sure that the high incidence of T. tonsurans noted in this prospective Haitian study represents a true recent increase rather than an unmasking of a chronic problem. According to the mycology laboratory data accumulated by one of us (MB) during the last 48 years in Port-au-Prince, it is absolutely clear that the recent rise of T. tonsurans in Haiti is an emergent problem versus better detection. In reality, the same culture techniques and the same phenotypic features of the cultures were used for mycologic diagnosis during this long period of time as described in two available reference manuals [22,23].
This emergence could be linked to the gradual increase of the Haitian Diaspora in North America, especially in big cities such as Miami, New York, Boston, Chicago, Montreal and Toronto, where T. tonsurans has been prevalent for a number of years especially in black populations [6Á8,18]. Indeed, many Haitian immigrants living in North America began returning to their own country for vacations or to resettle following the end of dictatorship in 1986. It is noteworthy that in the US, children developing lesions in day care centres have to stay home. In the case of Haitians parents, who have busy working schedules, they may have no choice but to send their children to their grandparents who are still living in Haiti. Elsewhere flight connections between Haiti and North America are extensive with 3Á4 daily flights from Miami or Fort Lauderdale and one from New York plus two direct weekly flights from Montreal, creating an influx of 1500Á2000 travelling passengers per day despite the fact that Haiti is not a tourist Caribbean destination! These social phenomena could explain the emergence of T. tonsurans in Port-au-Prince at the end of the 1980s decade and the high prevalence observed in Haiti today. Recent studies underline the fact that T. tonsurans is highly contagiousness and the role of children scalp asymptomatic carriers in the rise of incidence of infections due to anthropophilc fungi [1Á3].
A second hypothesis concerning a 'local' transfer from other Caribbean countries to Haiti is also conceivable. As Haiti has borders with Dominican Republic, T. tonsurans could be easily transported from this country to Haiti, but no published data exist on Dominican Republic dermatophytoses. In Martinique, T. tonsurans also recently appeared beginning in 1998 [25], and it is also the most prevalent dermatophyte in Trinidad [24]. Although this study did not permit us to determine how many children acquired T. tonsurans infection indigenously and how many were already infected when they returned to Haiti from other countries, we speculate that the recent emergence of T. tonsurans in Haiti is strongly linked to dramatic increases in Haitians travelling from and to North America as in the Caribbean. It would be of interest to develop studies on genetic diversities of dermatophytes strains occurring in Haiti and to compare their phenotypical and genotypical characteristics with those of Caribbean, Latin and North American most prevalent strains.

Declaration of interest:
The authors report no conflicts of interest. The authors alone are responsible for the content and writing of the paper.