Candida spp. are yeasts of the normal mucocutaneous flora of humans. They cause a wide range of diseases from superficial lesions of mucous membranes to life-threatening deep tissue infections in humans [1]. The treatment of these candidiasis involves the use of antifungal drugs, the choice of which depends on the sensitivity of the Candida species [2,3]. Resistance of Candida spp. to antifungal drugs has been observed in Ouagadougou with human clinical strains isolated from oral, vaginal, urine and stool samples [4]. Among the possible sources of human contamination by these yeasts, the telluric source is described. Their presence in the soil can promote their spread and constitute a source of contamination, particularly in areas with high human concentration such as markets, sports and play areas, and recreational facilities [4]. These yeast strains could have several origins: clinical, animal, or environmental. Several studies in Asia and in Latin America have shown that several species of the genus Candida are regularly isolated from the soil. Among these species, some are commonly isolated in human pathology. These include C. albicans, C. tropicalis, and C. parapsilosis [5,6]. Although most Candida species isolated from soil are recognized in human pathology, some authors report species still poorly understood in human pathology, also isolated from soil. Indeed, strains representing a new ascomycete yeast species, Candida sanyaensis, have been isolated from soil samples collected on the islands of Hainan and Taiwan, in China, and in Ireland. Analysis of the D1/D2 domains of the large subunit (LUS) rRNA gene and the internal transcribed spacer (ITS) regions of these strains showed that this species is related to C. tropicalis [5,6]. This is also the case for Candida kantuleensis, a d-xylose-fermenting yeast species isolated from peat in a tropical swamp forest in Thailand [7]. However, the virulence of this soilborne species in humans remains to be established.

In Africa, studies on soil fungal diversity are rare or even non-existent according to the literature. The few data that do exist on the subject report new species whose relevance to human pathology is completely unknown. These are Candida mokoenaii, Candida lyxosophila, and Candida amidevorans [6,7,8].

Although the literature indicates that the soil diversity of pathogenic yeasts of the genus Candida is poorly understood, these yeasts are nonetheless common in soil within human environments [9,10]. This constitutes a significant source of contamination for humans. Furthermore, the likely contact of these soil strains with antifungal pesticides could lead to cross-resistance with antifungal molecules used in human medicine [11,12]. Indeed, some authors have reported cross-resistance of soil-dwelling Candida strains to azole fungicides used in agriculture and to azole antifungals used in therapy [12]. It is thus also important to study their sensitivity to antifungals used in humans, as understanding this sensitivity will contribute to the fight against antimicrobial resistance within the context of One Health, an integrated approach to disease management.

Thus, the present study aimed to explore the diversity and antifungal susceptibility profile of Candida species isolated from soil samples in the city of Ouagadougou.

To our knowledge, this study is the first to explore the yeast species present in soils in Burkina Faso. In addition to inoculation on chromogenic medium (CAN ID2), we used MALDI-TOF (Matrix-Assisted Laser Desorption/Ionization Time-of-Flight) mass spectrometry to increase the sensitivity and specificity of mycological analyses. MALDI-TOF is a technique widely used in medical microbiology, but which remains inaccessible in our context in Burkina Faso. Six (6) yeast species were isolated (Candida tropicalis, C. glabrata, C. lusitaniae, C. krusei, C. kefyr, and C. orthosilopsis).

This study therefore provides epidemiological data indicating that the soil of the city of Ouagadougou constitutes a reservoir for several Candida species, primarily C. tropicalis [16]. The presence of Candida species frequently isolated from humans in the soil provides an idea of the diversity of these yeasts’ habitats and indicates a significant telluric reservoir [16]. In Burkina Faso, prior to this study, no data on the soil reservoir of Candida fungi were available, although the importance of this reservoir has already been described elsewhere. Indeed, according to the literature, C. tropicalis is one of the most frequently isolated pathogenic species of the Candida genus from soil in Asia and South America [17].

Some of these species of yeast in the soil in this study conducted in Ouagadougou, Burkina Faso, and in other countries are frequently implicated in human infections. Indeed, C. tropicalis, C. glabrata and C. krusei have been isolated in studies conducted in Burkina Faso on vaginal candidiasis and digestive candidiasis [18,19]. Their involvement in human pathology is well known. In humans, C. tropicalis, C. glabrata and C. krusei are found in the gastrointestinal tract and genitourinary tract. They cause superficial candidiasis, deep candidiasis and candidemia [20]. Candida lusitaniae, C. kefyr and C. orthopsilosis are rarer in human pathology. In humans, in addition to colonizing the skin and digestive and genitourinary mucosa, several species of Candida found in the soil can cause more serious illnesses. For example, C. tropicalis, the most isolated species in the soil of the city of Ouagadougou, causes superficial and systemic candidiasis. In Asia and in certain Latin American countries, this species is one of the species most frequently associated with candidemia, and mortality rates are generally higher than 40% [16]. It is therefore important to take into consideration the telluric reservoir of these species in the fight against candidiasis, particularly systemic candidiasis in people at risk. C. albicans, the species most frequently found in human pathology, was not isolated in the present study. Indeed, according to the literature, C. albicans is almost exclusively found in humans, to whom it is well adapted. And its presence in the soil indicates contamination of human origin, particularly through feces [16]. The distribution of candida species according to site did not show any statistically significant difference. The isolated species were therefore distributed in the soil independently of their specific characteristics, whether the sites were regularly frequented by humans or animals.

Considering the susceptibility of the candida strains isolated in this study, we found that it was variable depending on the species and the antifungal tested. Indeed, resistance to fluconazole was encountered in C. tropicalis (53.8%), the predominant species in our isolates, and absent in C. glabrata, the 2nd most frequent species. In a recent study conducted in Cameroon, the resistance rate of C. tropicalis to fluconazole was slightly lower (50%), while C. glabrata showed low resistance (3%) [21]. Besides fluconazole, azole resistance concerned itraconazole with several species involved (C. glabrata, C. lusitaniae, C. orthopsilosis and C. krusei) [21]. The azole resistance profile of our soil-borne isolates is thus similar to the resistance profile of human clinical strains that were previously tested in Ouagadougou [4]. These observations show a probable circulation of isolated strains between the environment and humans and raises concern in the management of candidiasis in Burkina Faso. Indeed, C. tropicalis is part of the Candida genus, along with C. albicans, species frequently isolated during candidiasis in humans, and fluconazole is the main molecule used in the treatment of deep candidiasis [4]. Several authors report that selection pressure from the widespread use of fluconazole could be responsible for the cross-resistance to other azoles such as itraconazole observed in the present study [22,23,24]. Furthermore, fluconazole is established as a first-line treatment for esophageal candidiasis and is administered free of charge to immunocompromised patients by the Ministry of Health of Burkina Faso [25]. In addition to having relative safety and high oral bioavailability, this triazole also remains a less expensive antifungal (around 500 FCFA for the generic tablet form in pharmacies in Ouagadougou) in Burkina Faso and is then mostly prescribed for the management of candidiasis. Another source that could explain this high rate of resistance to azoles, in the context of a One Health approach, is the animal origin of Candida strains isolated from the soil [26]. Some authors have reported multi-resistant strains of Candida isolated from some animals. According to a study conducted in sheep in China, some isolated species of the genus Candida, including Candida tropicalis, showed a high level of resistance to antifungals, particularly to azoles such as itraconazole and fluconazole [27].

Regarding polyenes, while all our isolates were sensitive to nystatin (100%), the majority of strains were resistant to amphotericin B (89.7%). The absence of resistance to nystatin in our study confirms the observations of several authors who note that this resistance is still rare. In fact, the genetic mutations conferring resistance to nystatin in yeasts of the genus Candida are lethal, thus slowing down the selection of resistant strains [28]. Thus, the few studies that have found it report low rates of strains resistant to nystatin: 3% in Brazil with clinical strains of oral origin and 0.61% in Uganda with strains of vulvovaginal origin [29,30]. Resistance to amphotericin B, which was also considered rare, is increasingly found in studies. Zarei et al. (2014) found a rate of 42.5% with clinical isolates [31]. Just as with the distribution of Candida species according to the site, there was no statistically significant link between their sensitivity to antifungals, particularly that of C. tropicalis, the species predominantly isolated in the present study, and the site.

This study allowed us to isolate six species of Candida from the soils of the city of Ouagadougou. Some of these species are sometimes found in human diseases. The antifungal susceptibility profile of these soil-based isolates is quite similar to the profiles regularly obtained with human isolates. Because yeasts isolated from soil can be a source of contamination and colonization for humans, it is useful to monitor their susceptibility to common antifungal agents.