Epidemiology and Prevalence of Oral Candidiasis in HIV Patients From Chad in the Post-HAART Era

Abstract

Oral candidiasis remains a common problem in HIV-infected individuals, especially in sub-Saharan Africa. Here, we performed the first study in Chad on the prevalence of oral yeasts carriage and oral candidiasis in HIV-positive subjects from southern Chad and analyzed the influence of HAART, CD4⁺ T-cell numbers, and antimycotics in 589 patients. These patients were recruited from a specialized medical center for HIV patients in Sarh and from a rural medical health dispensary in the vicinity, including a total of 384 HIV-positive and 205 HIV-negative individuals. Yeasts obtained from oral specimen were identified by MALDI-TOF MS and their antifungal susceptibility profiles determined. The overall prevalence of yeast colonization and symptomatic oral candidiasis in HIV-infected patients was 25.1%. The prevalence of oral candidiasis was higher in untreated than in HAART-treated HIV-positive patients (16% vs. 2%; p < 0.01). Oral candidiasis was furthermore associated with high fungal burdens of Candida albicans and a CD4⁺ T-cell number <200/μl. A shift toward non-albicans Candida species was observed under nucleoside-based HAART therapy. Azole antifungal drug resistance was only observed for the intrinsically resistant species Candida krusei and Candida glabrata. Prevalence of oral candidiasis in the studied area was very low. The species distribution was similar to other countries around the world, with C. albicans being dominant. Candida dubliniensis was not isolated. Nucleoside-based HAART therapy significantly reduced oral colonization as well as occurrence of oral candidiasis caused by C. albicans and led to a species shift toward non-albicans species. Antifungal resistance was not yet a concern in Chad.

Keywords: AIDS; Chad; HIV; NNRIT-HAART; oral Candida colonization.

Figure 1

Representative samples of oral symptoms of the tongue and palate within the study group: (A,B) mild symptoms with less than 50% coverage of the tongue by whitish plaque, (C) >50% of tongue surface covered with whitish plaque, (D) median rhomboid glossitis with central atrophy, and (E) involvement of palate.

Figure 2

Distribution of the patients according to age, gender, and HIV status. m, male; f, female; and ?, unknown.

Figure 3

Prevalence rates of yeast species among patient groups with different HIV and treatment status. (A) Rates and degree of oral symptoms (* indicates significant differences in prevalence of moderate-to-severe symptoms), (B) rates and degree of oral yeast colonization (* indicates significant differences in prevalence of a high yeast burden), (C) association of oral colonization with disease symptoms (* indicates significant differences in moderately to severely symptomatic yeast carriers), and (D) species distribution derived from yeast-positive swabs. In panels (A–C), numbers above columns indicate size of patient subgroups. a: Y-axis of panel (D) is scaled to total number of isolates, given in parentheses after number of swabs. Due to mixed-species colonization the number of isolates can exceed number of swabs (* indicates significant differences in prevalence rates of Candida albicans).

Figure 4

Influence of Triomune HAART therapy on oral symptoms and yeast colonization in HIV-positive patients. (A) Association of CD4⁺ T-cell numbers with observational parameters investigated, (B) CD4⁺ T-cell numbers, (C) oral symptoms, (D) fungal burden, and (E) colonizing yeast species observed in HIV-positive patients with different lengths of Triomune HAART therapy (up to 0.25, 1, 2, and more than 2 years after initiation). Boxed regions in panel (A) denote CD4⁺ T-cell numbers below 200 cells/μl (dark grey) and 200–350 cells/μl (light grey). Numbers in panel (B) are mean values.

Figure 5

Antifungal drug resistance. Susceptibility distribution to five common antifungals, stratified by species. For color codes see inset, species-specific breakpoints are briefly outlined in the Methods section.