Collateral consequences of agricultural fungicides on pathogenic yeasts: A One Health perspective to tackle azole resistance

Abstract

Candida and Cryptococcus affect millions of people yearly, being responsible for a wide array of clinical presentations, including life‐threatening diseases. Interestingly, most human pathogenic yeasts are not restricted to the clinical setting, as they are also ubiquitous in the environment. Recent studies raise concern regarding the potential impact of agricultural use of azoles on resistance to medical antifungals in yeasts, as previously outlined with Aspergillus fumigatus. Thus, we undertook a narrative review of the literature and provide lines of evidence suggesting that an alternative, environmental route of azole resistance, may develop in pathogenic yeasts, in addition to patient route. However, it warrants sound evidence to support that pathogenic yeasts cross border between plants, animals and humans and that environmental reservoirs may contribute to azole resistance in Candida or other yeasts for humans. As these possibilities could concern public health, we propose a road map for future studies under the One Health perspective.

Environmental reservoirs of the drug-resistant pathogenic yeast Candida auris

“…In contrast to pathogenic moulds and non-Candida human pathogenic yeast (such as Cryptococcus neoformans), which are known to inhabit diverse environmental niches, pathogenic Candida species primarily exist as human commensals or as contaminants in clinical environments from where they can cause opportunistic infections. However, several species of pathogenic Candida have been isolated from nonhuman or nonclinical environmental samples [26,27], which could provide novel exposure routes for human infection [26,[28][29][30]. Candida albicans was previously thought to exist mainly as a human commensal [30], but has now been widely isolated from nonclinical environmental samples, e.g., soil, wetlands, and plants (Table 1).…”

The importance of antimicrobial resistance in medical mycology

“…This can be a consequence of the response to patient antifungal treatment, but many human pathogenic fungi also have an environmental phase where resistance can emerge 12 . For example, antifungal resistance in Aspergillus fumigatus is clearly associated with environmental selection of resistance as a consequence of exposure to agricultural azoles used in crop protection 13 . Indeed, estimates suggest that one in 20 culturable isolates of this fungus isolated from the air are tebuconazole resistant 14 .…”

Short Tandem Repeat Genotyping and Antifungal Susceptibility Testing of Latin American Candida tropicalis Isolates

“…The absence of this mutation in other isolates suggests that spontaneous development of this mutation is unlikely and that this mutation may have originated from a common single ancestor C. tropicalis strain in Brazil. Widespread use of agricultural azoles is known to have driven the emergence of environmental resistance mechanisms in fungi, which could hypothetically be a contributing factor in this setting [ 57 , 58 , 59 , 60 , 61 ]. However, although 11 out of 23 of these isolates originated from the environment, a non-environmental source cannot be excluded, as these samples were acquired from a public beach.…”