Oral microbiome patterns of dental caries in Kazakhstani adolescents
DOI:
https://doi.org/10.1590/Keywords:
Oral microbiome, DMFT in Kazakhstan, Adolescents’ oral health, Microbiome patternsAbstract
Objective The oral microbiome is one of the most complex microbial ecosystems in the host. This study aimed to investigate and characterize the oral microbiome composition in Kazakhstani adolescents associated with dental caries. Methodology The study included 312 adolescents, with 241 individuals presenting with caries and 71 caries-free, aged 12-15 years. Dental caries assessment was performed using DMFT (Decayed, missed, filled teeth) index. Oral samples were collected, and 16S rRNA (16S ribosomal ribonucleic acid) gene sequencing targeting the V3-V4 hypervariable regions on an Illumina MiSeq platform was performed to profile the microbial communities. Functional metagenomic predictions were generated using PICRUSt2 v2.5.0, using the KEGG database for bacterial pathway abundance estimation. Data analysis was conducted using Python 3.9.16 and R 4.2.2. Results The alpha diversity was insignificant, while beta diversity analysis demonstrated clear distinctions by Bray-Curtis (F=2.5, p=0.003) and weighted UniFrac distances (F=4.4, p=0.002). The Neisseria and Prevotella genera, and Gammaproteobacteria class showed significant associations with dental caries (MaAsLin2 p≤0.05, LDA≥2), stronger predictive power (AUC=0.65, F1=0.83), and higher predicted functional activity through glutathione metabolism, RNA degradation, and unsaturated fatty acid metabolism pathways. Conclusions This study identified specific oral microbiome patterns associated with dental caries in Kazakhstani adolescents, revealing interactions between key bacterial taxa and metabolic pathways.
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References
- Veenman F, van Dijk A, Arredondo A, Medina-Gomez C, Wolvius E, Rivadeneira F, et al. Oral microbiota of adolescents with dental caries: a systematic review. Arch Oral Biol. 2024;161:105933. doi: 10.1016/j.archoralbio.2024.105933
» https://doi.org/10.1016/j.archoralbio.2024.105933
- Kilian M, Chapple IL, Hannig M, Marsh PD, Meuric V, Pedersen AM, et al. The oral microbiome: an update for oral healthcare professionals. Br Dent J. 2016;221(10):657-66. doi: 10.1038/sj.bdj.2016.865
» https://doi.org/10.1038/sj.bdj.2016.865
- Kassebaum NJ, Bernabé E, Dahiya M, Bhandari B, Murray CJ, Marcenes W. Global burden of untreated caries: a systematic review and metaregression. J Dent Res. 2015;94(5):650-8. doi:10.1177/0022034515573272
» https://doi.org/10.1177/0022034515573272
- World Health Organization. Global oral health status report: towards universal health coverage for oral health by 2030. Geneva: WHO; 2022. ISBN: 978-92-4-006148-4.
- Inquimbert C, Bourgeois D, Bravo M, et al. The oral bacterial microbiome of interdental surfaces in adolescents according to carious risk. Microorganisms. 2019;7(9):319. doi:10.3390/microorganisms7090319
» https://doi.org/10.3390/microorganisms7090319
- Burcham ZM, Garneau NL, Comstock SS, et al. Patterns of oral microbiota diversity in adults and children: a crowdsourced population study. Sci Rep. 2020;10(1):2133. doi:10.1038/s41598-020-59016-0
» https://doi.org/10.1038/s41598-020-59016-0
- Xu H, Tian J, Hao W, et al. Oral microbiome shifts from caries-free to caries-affected status in 3-year-old Chinese children: a longitudinal study. Front Microbiol. 2018;9:2009. doi:10.3389/fmicb.2018.02009
» https://doi.org/10.3389/fmicb.2018.02009
- Becker MR, Paster BJ, Leys EJ, et al. Molecular analysis of bacterial species associated with childhood caries. J Clin Microbiol. 2002;40(3):1001-9. doi:10.1128/JCM.40.3.1001-1009.2002
» https://doi.org/10.1128/JCM.40.3.1001-1009.2002
- Xiao C, Ran S, Huang Z, Liang J. Bacterial diversity and community structure of supragingival plaques in adults with dental health or caries revealed by 16S pyrosequencing. Front Microbiol. 2016;7:1145. doi:10.3389/fmicb.2016.01145
» https://doi.org/10.3389/fmicb.2016.01145
- Elyassi M, Babaeekhou L, Ghane M. Streptococcus mutans and Streptococcus sobrinus contributions in dental caries in Iranian and Afghan children: a report from serotype distribution and novel STs. Arch Oral Biol. 2022;139:105431. doi:10.1016/j.archoralbio.2022.105431
» https://doi.org/10.1016/j.archoralbio.2022.105431
- Johansson I, Witkowska E, Kaveh B, Lif Holgerson P, Tanner AC. The microbiome in populations with a low and high prevalence of caries. J Dent Res. 2016;95(1):80-6. doi:10.1177/0022034515609554
» https://doi.org/10.1177/0022034515609554
- Havsed K, Stensson M, Jansson H, et al. Bacterial composition and metabolomics of dental plaque from adolescents. Front Cell Infect Microbiol. 2021;11:716493. doi:10.3389/fcimb.2021.716493
» https://doi.org/10.3389/fcimb.2021.716493
- Vieira AR, Hiller NL, Powell E, et al. Profiling microorganisms in whole saliva of children with and without dental caries. Clin Exp Dent Res. 2019;5(4):438-46. doi:10.1002/cre2.206
» https://doi.org/10.1002/cre2.206
- Zhumadilova A, Supiyev T, Abralina S, Yeslyamgaliyeva A, Kulmirzayeva A, Supiyev A. Determinants of dental caries experience among adolescents in Kazakhstan: a cross-sectional study. Curr Top Nutraceutical Res. 2021;19:388-97. doi:10.37290/ctnr2641-452X.19:388-397
» https://doi.org/10.37290/ctnr2641-452X.19:388-397
- World Health Organization. Oral health surveys: basic methods. 5th ed. Geneva: WHO; 2013. ISBN: 978-92-4-154864-9.
- Elamin A, Garemo M, Gardner A. Dental caries and their association with socioeconomic characteristics, oral hygiene practices and eating habits among preschool children in Abu Dhabi, United Arab Emirates: the NOPLAS project. BMC Oral Health. 2018;18(1):104. doi:10.1186/s12903-018-0557-8
» https://doi.org/10.1186/s12903-018-0557-8
- Vernazza CR, Rolland SL, Chadwick B, Pitts N. Caries experience, the caries burden and associated factors in children in England, Wales and Northern Ireland 2013. Br Dent J. 2016;221(6):315-20. doi:10.1038/sj.bdj.2016.682
» https://doi.org/10.1038/sj.bdj.2016.682
- Versalovic J, Baylor P, Keitel W, Watson M, Dunne M. HMP Initiative 1: core microbiome sampling protocol A. Human Microbiome Project; Protocol No. HMP-07-001 [Internet]. Bethesda (MD): National Institutes of Health; 2008 [cited 2025 Feb 22]. Available from: https://www.ncbi.nlm.nih.gov/projects/gap/cgi-bin/document.cgi?study_id=phs000228.v3.p1&phd=2844
» https://www.ncbi.nlm.nih.gov/projects/gap/cgi-bin/document.cgi?study_id=phs000228.v3.p1&phd=2844
- GBD 2017 Disease and Injury Incidence and Prevalence Collaborators. Global, regional, and national incidence, prevalence, and years lived with disability for 354 diseases and injuries for 195 countries and territories, 1990-2017: a systematic analysis for the Global Burden of Disease Study 2017. Lancet. 2018;392(10159):1789-858. doi:10.1016/S0140-6736(18)32279-7
» https://doi.org/10.1016/S0140-6736(18)32279-7
- Rebelo MB, Oliveira CS, Tavaria FK. Novel strategies for preventing dysbiosis in the oral cavity. Front Biosci (Elite Ed). 2023;15(4):23. doi:10.31083/j.fbe1504023
» https://doi.org/10.31083/j.fbe1504023
- Gupta A, Shivachandran A, Saleena LM. Oral microbiome insights: tracing acidic culprits in dental caries with functional metagenomics. Arch Oral Biol. 2024;168:106064. doi:10.1016/j.archoralbio.2024.106064
» https://doi.org/10.1016/j.archoralbio.2024.106064
- Butcher MC, Short B, Veena CLR, et al. Meta-analysis of caries microbiome studies can improve upon disease prediction outcomes. APMIS. 2022;130(12):763-77. doi:10.1111/apm.13272
» https://doi.org/10.1111/apm.13272
- Marsh PD. Dental plaque as a biofilm and a microbial community: implications for health and disease. BMC Oral Health. 2006;6 Suppl 1:S14. doi:10.1186/1472-6831-6-S1-S14
» https://doi.org/10.1186/1472-6831-6-S1-S14
- Agnello M, Marques J, Cen L, et al. Microbiome associated with severe caries in Canadian First Nations children. J Dent Res. 2017;96(12):1378-85. doi:10.1177/0022034517718819
» https://doi.org/10.1177/0022034517718819
- Xu H, Hao W, Zhou Q, et al. Plaque bacterial microbiome diversity in children younger than 30 months with or without caries prior to eruption of second primary molars. PLoS One. 2014;9(2):e89269. doi:10.1371/journal.pone.0089269
» https://doi.org/10.1371/journal.pone.0089269
- Zheng Y, Zhang M, Li J, et al. Comparative analysis of the microbial profiles in supragingival plaque samples obtained from twins with discordant caries phenotypes and their mothers. Front Cell Infect Microbiol. 2018;8:361. doi:10.3389/fcimb.2018.00361
» https://doi.org/10.3389/fcimb.2018.00361
- Baker JL, Morton JT, Dinis M, et al. Deep metagenomics examines the oral microbiome during dental caries, revealing novel taxa and co-occurrences with host molecules. Genome Res. 2021;31(1):64-74. doi:10.1101/gr.265645.120
» https://doi.org/10.1101/gr.265645.120
- Qudeimat MA, Alyahya A, Karched M, Behbehani J, Salako NO. Dental plaque microbiota profiles of children with caries-free and caries-active dentition. J Dent. 2021;104:103539. doi:10.1016/j.jdent.2020.103539
» https://doi.org/10.1016/j.jdent.2020.103539
- Könönen E, Fteita D, Gursoy UK, Gursoy M. Prevotella species as oral residents and infectious agents with potential impact on systemic conditions. J Oral Microbiol. 2022;14(1):2079814. doi:10.1080/20002297.2022.2079814
» https://doi.org/10.1080/20002297.2022.2079814
- Zhang Y, Zhen M, Zhan Y, Song Y, Zhang Q, Wang J. Population-genomic insights into variation in Prevotella intermedia and Prevotella nigrescens isolates and its association with periodontal disease. Front Cell Infect Microbiol. 2017;7:409. doi:10.3389/fcimb.2017.00409
» https://doi.org/10.3389/fcimb.2017.00409
- Monteiro MF, Altabtbaei K, Kumar PS, et al. Parents with periodontitis impact the subgingival colonization of their offspring. Sci Rep. 2021;11(1):1357. doi:10.1038/s41598-020-80372-4
» https://doi.org/10.1038/s41598-020-80372-4
- Chanda W, Joseph TP, Padhiar AA, et al. Combined effect of linolenic acid and tobramycin on Pseudomonas aeruginosa biofilm formation and quorum sensing. Exp Ther Med. 2017;14(5):4328-38. doi:10.3892/etm.2017.5110
» https://doi.org/10.3892/etm.2017.5110
- Osawa K, Miyazaki K, Shimura S, Okuda J, Matsumoto M, Ooshima T. Identification of cariostatic substances in the cacao bean husk: their anti-glucosyltransferase and antibacterial activities. J Dent Res. 2001;80(11):2000-4. doi:10.1177/00220345010800111001
» https://doi.org/10.1177/00220345010800111001
- Lee K, Pi K, Kim EB, et al. Glutathione-mediated response to acid stress in the probiotic bacterium, Lactobacillus salivarius. Biotechnol Lett. 2010;32(7):969-72. doi:10.1007/s10529-010-0244-6
» https://doi.org/10.1007/s10529-010-0244-6
- Han DH, Kim MJ, Jun EJ, Kim JB. The role of glutathione metabolism in cariogenic bacterial growth and caries in Korean children. Arch Oral Biol. 2013;58(5):493-9. doi:10.1016/j.archoralbio.2012.09.021
» https://doi.org/10.1016/j.archoralbio.2012.09.021
- de Carvalho CCCR, Caramujo MJ. The various roles of fatty acids. Molecules. 2018;23(10):2583. doi:10.3390/molecules23102583
» https://doi.org/10.3390/molecules23102583
- Stenz L, François P, Fischer A, et al. Impact of oleic acid (cis-9-octadecenoic acid) on bacterial viability and biofilm production in Staphylococcus aureus FEMS Microbiol Lett. 2008;287(2):149-55. doi:10.1111/j.1574-6968.2008.01316.x
» https://doi.org/10.1111/j.1574-6968.2008.01316.x
- Carpousis AJ. The RNA degradosome of Escherichia coli: an mRNA-degrading machine assembled on RNase E. Annu Rev Microbiol. 2007;61:71-87. doi:10.1146/annurev.micro.61.080706.093440
» https://doi.org/10.1146/annurev.micro.61.080706.093440
- Marcaida MJ, DePristo MA, Chandran V, Carpousis AJ, Luisi BF. The RNA degradosome: life in the fast lane of adaptive molecular evolution. Trends Biochem Sci. 2006;31(7):359-65. doi:10.1016/j.tibs.2006.05.005
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Copyright (c) 2025 Argul Issilbayeva, Zharkyn Jarmukhanov, Samat Kozhakhmetov, Yermekbayeva Bakytgul, Laura Chulenbayeva, Graciela Muniz-Terrera, Masae Furukawa, Hiroki Nikawa, Adil Supiyev, Almagul kushugulova, Anara Zhumadilova

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