Ecology of Candida albicans gut colonization: inhibition of Candida adhesion, colonization, and dissemination from the gastrointestinal tract by bacterial antagonism

Abstract

Antibiotic-treated and untreated Syrian hamsters were inoculated intragastrically with Candida albicans to determine whether C. albicans could opportunistically colonize the gastrointestinal tract and disseminate to visceral organs. Antibiotic treatment decreased the total population levels of the indigenous bacterial flora and predisposed hamsters to gastrointestinal overgrowth and subsequent systemic dissemination by C. albicans in 86% of the animals. Both control hamsters not given antibiotics and antibiotic-treated animals reconventionalized with an indigenous microflora showed significantly lower gut populations of C. albicans, and C. albicans organisms were cultured from the visceral organs of 0 and 10% of the animals, respectively. Conversely, non-antibiotic-treated hamsters inoculated repeatedly with C. albicans had high numbers of C. albicans in the gut, and viable C. albicans was recovered from the visceral organs of 53% of the animals. Examination of the mucosal surfaces from test and control animals indicated further that animals which contained a complex indigenous microflora had significantly lower numbers of C. albicans associated with their gut walls than did antibiotic-treated animals. The ability of C. albicans to associate with intestinal mucosal surfaces also was tested by an in vitro adhesion assay. The results indicate that the indigenous microflora reduced the mucosal association of C. albicans by forming a dense layer of bacteria in the mucus gel, out-competing yeast cells for adhesion sites, and producing inhibitor substances (possibly volatile fatty acids, secondary bile acids, or both) that reduced C. albicans adhesion. It is suggested, therefore, that the indigenous intestinal microflora suppresses C. albicans colonization and dissemination from the gut by inhibiting Candida-mucosal association and reducing C. albicans population levels in the gut. Systemic Candida infections are important causes of morbidity and mortality among patients who are compromised immunologically or who are undergoing prolonged antibiotic therapy (41, 52, 69). The passage of viable Candida albicans through the gastrointestinal (GI) mucosa into the host bloodstream is believed to be an important mechanism leading to systemic candidosis (38, 61, 62), particularly in patients with acute leukemia (43). Patient and animal studies support this hypothesis and indicate that a number of opportunistic fungal pathogens can spread systemically from the intestinal lumen to invade visceral organs (28, 29, 67, 68). We recently reported, for instance, that C. albicans, Candida parapsilosis, Candida pseudotropicalis, Candida tropicalis, and Torulopsis glabrata could opportunistically colonize the gut and disseminate to visceral organs after intragastic challenge of antibiotic-treated mice (37). The feeding of C. albicans to animals not given antibiotics, in contrast, does not lead to Candida dissemination from the

Interactions of Candida albicans with other Candida spp. and bacteria in the biofilms*

“…However, this effect was not observed with C. parapsilosis or T. glabrata. Competition between two micro-organisms for adhesion sites has been reported (Kennedy and Volz 1985). Taking that into consideration, it would mean that the highly adherent isolates of Candida spp.…”

“…Competition for the adhesion sites is another form of interaction that may take place between bacteria and yeast cells. Indigenous intestinal microflora reduced the mucosal adhesion of C. albicans to the gastrointestinal tract of Syrian hamsters by forming a dense layer of bacteria in the mucus gel, outcompeting yeast cells for adhesion sites, and producing substances inhibitory to the adhesion of C. albicans (Kennedy and Volz 1985).…”

Factors affecting the adherence of Candida albicans to human buccal epithelial cells in human immunodeficiency virus infection

“…Similar effects of antibacterials have been reported in a number of previous studies, where increased attachment of yeasts to epithelial cells was noted after the administration of antibiotics. 18,19 One reason for this is thought to be the elimination of bacterial species which competitively inhibit candidal adhesion to the buccal mucosa. Liljemark and Gibbons, 20 using gnotobiotic rats, demonstrated that the presence of oral bacterial species on epithelial surfaces reduces the subsequent adherence of C. albicans.…”

Potential role of probiotic bacteria in the treatment and prevention of localised candidosis

“…29 It has been suggested that most systemic candidal infections are endogenously acquired from the gastrointestinal tract. 30 Most studies addressing the use of probiotics for the treatment of intestinal disorders are related to inflammatory bowel diseases such as Crohn disease and ulcerative colitis or antibiotic-associated diarrhoea where probiotics are already used as therapeutics.…”