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. 2018 Dec;97(13):1468-1476.
doi: 10.1177/0022034518790941. Epub 2018 Jul 26.

Association between Oral Candida and Bacteriome in Children with Severe ECC

Affiliations

Association between Oral Candida and Bacteriome in Children with Severe ECC

J Xiao et al. J Dent Res. 2018 Dec.

Abstract

Candida albicans is an opportunistic fungal organism frequently detected in the oral cavity of children with severe early childhood caries (S-ECC). Previous studies suggested the cariogenic potential of C. albicans, in vitro and in vivo, and further demonstrated its synergistic interactions with Streptococcus mutans. In combination, the 2 organisms are associated with higher caries severity in a rodent model. However, it remains unknown whether C. albicans influences the composition and diversity of the entire oral bacterial community to promote S-ECC onset. With 16s rRNA amplicon sequencing, this study analyzed the microbiota of saliva and supragingival plaque from 39 children (21 S-ECC and 18 caries-free [CF]) and 33 mothers (17 S-ECC and 16 CF). The results revealed that the presence of oral C. albicans is associated with a highly acidogenic and acid-tolerant bacterial community in S-ECC, with an increased abundance of plaque Streptococcus (particularly S. mutans) and certain Lactobacillus/Scardovia species and salivary/plaque Veillonella and Prevotella, as well as decreased levels of salivary/plaque Actinomyces. Concurrent with this microbial community assembly, the activity of glucosyltransferases (cariogenic virulence factors secreted by S. mutans) in plaque was significantly elevated when C. albicans was present. Moreover, the oral microbial community composition and diversity differed significantly by disease group (CF vs. S-ECC) and sample source (saliva vs. plaque). Children and mothers within the CF and S-ECC groups shared microbiota composition and diversity, suggesting a strong maternal influence on children's oral microbiota. Altogether, this study underscores the importance of C. albicans in association with the oral bacteriome in the context of S-ECC etiopathogenesis. Further longitudinal studies are warranted to examine how fungal-bacterial interactions modulate the onset and severity of S-ECC, potentially leading to novel anticaries treatments that address fungal contributions.

Keywords: Candida species; Streptococcus mutans; early childhood caries; glucosyltransferase; maternal influence; microbiota.

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Conflict of interest statement

The authors declare no potential conflicts of interest with respect to the authorship and/or publication of this article.

Figures

Figure 1.
Figure 1.
Relative abundance of bacterial genera and species in the microbiome of children by caries status and the presence of Candida albicans in saliva and plaque samples. One-way analysis of variance with Tukey-Kramer test was used to compare the proportions of the most populated genus/species relative abundance among 3 groups: CF and S-ECC C. albicans positive and negative. The upper graph reveals that the presence of C. albicans is associated with a distinctive oral microbiota in children with S-ECC, with highly acidogenic and acid-tolerant bacterial genera in addition to an increased abundance of Veillonella and Prevotella in (A) saliva and (B) plaque. (C) The lower graph shows low levels of S. mutans in saliva as compared with other streptococcal species. However, in (D) plaque, S. mutans abundance was dramatically increased in samples from the S-ECC group versus the CF group when C. albicans was present. *P < 0.05 between CF and S-ECC–C. albicans (–). P < 0.05 between CF and S-ECC–C. albicans (+). §P < 0.05 between S-ECC–C. albicans (–) and S-ECC–C. albicans (+). CF, caries free; S-ECC, severe early childhood caries.
Figure 2.
Figure 2.
Relative fold change in abundance of species in (A) saliva and (B) plaque from children with S-ECC in the presence or absence of Candida albicans (Ca). Bars show the fold change for each species, calculated as abundance in the presence of C. albicans divided by the abundance in its absence. The DESeq2-negative binomial Wald test was used to compare the relative abundance of the listed bacterial species; all strains listed have a raw P value <0.05. Strains marked with an asterisk (*) have a significant difference in abundance with an adjusted P value <0.05.
Figure 3.
Figure 3.
Taxa (or operational taxonomic unit) diversity in plaque and saliva samples from CF versus S-ECC and Candida albicans (Ca) positive (+) versus negative (–). (A, B) Mean alpha diversity (measured by Shannon diversity indices with 95% CIs) is shown in the upper graphs. The range of alpha diversity is shown as a dashed line. Means are shown by red lines. (A) Comparisons between sample types (saliva and plaque) were significantly different between S-ECC and CF samples (P < 0.05). Species diversity was higher in plaque samples than in saliva samples. (B) The presence of C. albicans did not alter the microbial alpha diversity in S-ECC salivary or plaque samples when compared within the same sample sources (P > 0.05). (C) This graph depicts 2 main findings. Plaque and saliva samples had dissimilar beta diversity (P < 0.05), which was also different between CF and S-ECC saliva samples (P = 0.005) and plaque samples (P = 0.001). (D) This graph compares saliva and plaque samples in children with S-ECC only, in the presence or absence of C. albicans. Although the cluster pattern looks different in both C. albicans conditions (positive and negative), the differences are not statistically significant. CF, caries free; S-ECC, severe early childhood caries.
Figure 4.
Figure 4.
Species relative abundance and taxa or operational taxonomic unit diversity (Shannon diversity) and dissimilarity (beta diversity) from plaque samples among mother-child dyads. (A) For species relative abundance among mother-child samples, a similar microbial composition was seen between mother and child plaque samples. (B) Beta diversity results indicate the dissimilarity of plaque microbiome in S-ECC samples between children and their mothers (P = 0.703, nonparametric P value) and in CF samples between children and their mothers (P > .99, nonparametric P value). (C) Alpha diversity is shown (mean Shannon diversity indices with 95% CIs). The range of plaque microbiome diversity is shown as a vertical dashed line, and means are shown as red lines. No alpha diversity difference was seen between the children and their mothers in the S-ECC or CF group (P > 0.05). CF, caries free; S-ECC, severe early childhood caries.

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