Early life factors and oral microbial signatures define the risk of caries in a Swedish cohort of preschool children.
Journal
Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288
Informations de publication
Date de publication:
11 Apr 2024
11 Apr 2024
Historique:
received:
01
10
2023
accepted:
08
04
2024
medline:
12
4
2024
pubmed:
12
4
2024
entrez:
11
4
2024
Statut:
epublish
Résumé
The oral cavity harbors complex communities comprising bacteria, archaea, fungi, protozoa, and viruses. The oral microbiota is establish at birth and develops further during childhood, with early life factors such as birth mode, feeding practices, and oral hygiene, reported to influence this development and the susceptibility to caries. We here analyzed the oral bacterial composition in saliva of 260 Swedish children at two, three and five years of age using 16S rRNA gene profiling to examine its relation to environmental factors and caries development at five years of age. We were able to assign the salivary bacterial community in each child at each time point to one of seven distinct clusters. We observed an individual dynamic in the development of the oral microbiota related to early life factors, such as being first born, born by C-section, maternal perinatal antibiotics use, with a distinct transition between three and five years of age. Different bacterial signatures depending on age were related to increased caries risk, while Peptococcus consistently linked to reduced risk of caries development.
Identifiants
pubmed: 38605085
doi: 10.1038/s41598-024-59126-z
pii: 10.1038/s41598-024-59126-z
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
8463Subventions
Organisme : Halland Regional Research board
ID : Halland-566481
Organisme : Halland Regional Research board
ID : Halland-665071
Informations de copyright
© 2024. The Author(s).
Références
Dewhirst, F. E. et al. The human oral microbiome. J. Bacteriol. 192, 5002–5017. https://doi.org/10.1128/JB.00542-10 (2010).
doi: 10.1128/JB.00542-10
pubmed: 20656903
pmcid: 2944498
Kennedy, B. et al. Oral microbiota development in early childhood. Sci. Rep. 9, 19025. https://doi.org/10.1038/s41598-019-54702-0 (2019).
doi: 10.1038/s41598-019-54702-0
pubmed: 31836727
pmcid: 6911045
Kahharova, D. et al. Maturation of the oral microbiome in caries-free toddlers: A longitudinal study. J. Dent. Re.s 99, 159–167. https://doi.org/10.1177/0022034519889015 (2020).
doi: 10.1177/0022034519889015
Kaan, A. M. M., Kahharova, D. & Zaura, E. Acquisition and establishment of the oral microbiota. Periodontol 2000(86), 123–141. https://doi.org/10.1111/prd.12366 (2021).
doi: 10.1111/prd.12366
Lif Holgerson, P., Esberg, A., Sjödin, A., West, C. E. & Johansson, I. A longitudinal study of the development of the saliva microbiome in infants 2 days to 5 years compared to the microbiome in adolescents. Sci. Rep. 10, 9629. https://doi.org/10.1038/s41598-020-66658-7 (2020).
doi: 10.1038/s41598-020-66658-7
pubmed: 32541791
pmcid: 7295743
Dashper, S. G. et al. Temporal development of the oral microbiome and prediction of early childhood caries. Sci. Rep. 9, 19732. https://doi.org/10.1038/s41598-019-56233-0 (2019).
doi: 10.1038/s41598-019-56233-0
pubmed: 31874981
pmcid: 6930300
Dzidic, M. et al. Oral microbiome development during childhood: an ecological succession influenced by postnatal factors and associated with tooth decay. ISME J 12, 2292–2306. https://doi.org/10.1038/s41396-018-0204-z (2018).
doi: 10.1038/s41396-018-0204-z
pubmed: 29899505
pmcid: 6092374
Craig, S. J. C. et al. Child weight gain trajectories linked to oral microbiota composition. Sci. Rep. 8, 14030. https://doi.org/10.1038/s41598-018-31866-9 (2018).
doi: 10.1038/s41598-018-31866-9
pubmed: 30232389
pmcid: 6145887
Richards, V. P. et al. Microbiomes of site-specific dental plaques from children with different caries status. Infect Immun. 85, e00106-e117. https://doi.org/10.1128/IAI.00106-17 (2017).
doi: 10.1128/IAI.00106-17
pubmed: 28507066
pmcid: 5520424
Marsh, P. D. In sickness and in health-what does the oral microbiome mean to us? An Ecological Perspective. Adv. Dent. Res. 29, 60–65. https://doi.org/10.1177/0022034517735295 (2018).
doi: 10.1177/0022034517735295
pubmed: 29355410
Pitts, N. B. et al. Dental caries. Nat. Rev. Dis. Primers 3, 17030. https://doi.org/10.1038/nrdp.2017.30 (2017).
doi: 10.1038/nrdp.2017.30
pubmed: 28540937
Tanner, A. C., Kressirer, C. A. & Faller, L. L. Understanding caries from the oral microbiome perspective. J. Calif. Dent. Assoc. 44, 437–446 (2016).
pubmed: 27514155
Fakhruddin, K. S., Ngo, H. C. & Samaranayake, L. P. Cariogenic microbiome and microbiota of the early primary dentition: A contemporary overview. Oral Dis 25, 982–995. https://doi.org/10.1111/odi.12932 (2019).
doi: 10.1111/odi.12932
pubmed: 29969843
Grier, A. et al. Oral microbiota composition predicts early childhood caries onset. J. Dent. Res. 100, 599–607. https://doi.org/10.1177/0022034520979926 (2021).
doi: 10.1177/0022034520979926
pubmed: 33356775
Xu, L. et al. Dynamic alterations in salivary microbiota related to dental caries and age in preschool children with deciduous dentition: A 2-year follow-up study. Front. Physiol. 9, 342. https://doi.org/10.3389/fphys.2018.00342 (2018).
doi: 10.3389/fphys.2018.00342
pubmed: 29670544
pmcid: 5893825
Boustedt, K., Roswall, J., Twetman, S. & Dahlgren, J. Influence of mode of delivery, family and nursing determinants on early childhood caries development: A prospective cohort study. Acta Odontol. Scand. 76, 595–599. https://doi.org/10.1080/00016357.2018.1490965 (2018).
doi: 10.1080/00016357.2018.1490965
pubmed: 30264628
Boustedt, K., Roswall, J., Kjellberg, E., Twetman, S. & Dahlgren, J. A prospective study of perinatal and metabolic risk factors for early childhood caries. Acta Paediatr https://doi.org/10.1111/apa.15231 (2020).
doi: 10.1111/apa.15231
pubmed: 32559323
Roswall, J. et al. Developmental trajectory of the healthy human gut microbiota during the first 5 years of life. Cell Host Microbe. https://doi.org/10.1016/j.chom.2021.02.021 (2021).
doi: 10.1016/j.chom.2021.02.021
pubmed: 33794185
Peres, K. G. et al. Scoping review of oral health-related birth cohort studies: Toward a global consortium. J. Dent. Res. 101, 632–646. https://doi.org/10.1177/00220345211062475 (2022).
doi: 10.1177/00220345211062475
pubmed: 35012400
Kilian, M. et al. The oral microbiome: An update for oral healthcare professionals. Br. Dent. J. 221, 657–666. https://doi.org/10.1038/sj.bdj.2016.865 (2016).
doi: 10.1038/sj.bdj.2016.865
pubmed: 27857087
de Jesus, V. C. et al. Characterization of supragingival plaque and oral swab microbiomes in children with severe early childhood caries. Front. Microbiol. 12, 683685. https://doi.org/10.3389/fmicb.2021.683685 (2021).
doi: 10.3389/fmicb.2021.683685
pubmed: 34248903
pmcid: 8267818
Kim, D. et al. Spatial mapping of polymicrobial communities reveals a precise biogeography associated with human dental caries. Proc. Natl. Acad. Sci. U S A 117, 12375–12386. https://doi.org/10.1073/pnas.1919099117 (2020).
doi: 10.1073/pnas.1919099117
pubmed: 32424080
pmcid: 7275741
Burcham, Z. M. et al. Patterns of oral microbiota diversity in adults and children: A crowdsourced population study. Sci. Rep. 10, 2133. https://doi.org/10.1038/s41598-020-59016-0 (2020).
doi: 10.1038/s41598-020-59016-0
pubmed: 32034250
pmcid: 7005749
Borewicz, K. et al. The association between breastmilk oligosaccharides and faecal microbiota in healthy breastfed infants at two, six, and twelve weeks of age. Sci. Rep. 10, 4270. https://doi.org/10.1038/s41598-020-61024-z (2020).
doi: 10.1038/s41598-020-61024-z
pubmed: 32144305
pmcid: 7060319
Holgerson, P. L. et al. Oral microbial profile discriminates breast-fed from formula-fed infants. J. Pediatr. Gastroenterol. Nutr. 56, 127–136. https://doi.org/10.1097/MPG.0b013e31826f2bc6 (2013).
doi: 10.1097/MPG.0b013e31826f2bc6
pubmed: 22955450
pmcid: 3548038
Kumar, S., Tadakamadla, J. & Johnson, N. W. Effect of toothbrushing frequency on incidence and increment of dental caries: A systematic review and meta-analysis. J. Dent. Res. 95, 1230–1236. https://doi.org/10.1177/0022034516655315 (2016).
doi: 10.1177/0022034516655315
pubmed: 27334438
Uchida-Fukuhara, Y. et al. Caries increment and salivary microbiome during university life: A prospective cohort study. Int. J. Environ. Res. Public Health 17, 3713. https://doi.org/10.3390/ijerph17103713 (2020).
doi: 10.3390/ijerph17103713
pubmed: 32466124
pmcid: 7277743
Ten Cate, J. M. & Buzalaf, M. A. R. Fluoride mode of action: Once there was an observant dentist. J. Dent. Res. 98, 725–730. https://doi.org/10.1177/0022034519831604 (2019).
doi: 10.1177/0022034519831604
pubmed: 31219410
Pitts, N. B., Twetman, S., Fisher, J. & Marsh, P. D. Understanding dental caries as a non-communicable disease. Br. Dent. J. 231, 749–753. https://doi.org/10.1038/s41415-021-3775-4 (2021).
doi: 10.1038/s41415-021-3775-4
pubmed: 34921271
pmcid: 8683371
Simón-Soro, A. & Mira, A. Solving the etiology of dental caries. Trends Microbiol. 23, 76–82. https://doi.org/10.1016/j.tim.2014.10.010 (2015).
doi: 10.1016/j.tim.2014.10.010
pubmed: 25435135
Zhu, C. et al. The predictive potentiality of salivary microbiome for the recurrence of early childhood caries. Front. Cell Infect. Microbiol. 8, 423. https://doi.org/10.3389/fcimb.2018.00423 (2018).
doi: 10.3389/fcimb.2018.00423
pubmed: 30619773
pmcid: 6302014
Belstrøm, D. et al. Influence of periodontal treatment on subgingival and salivary microbiotas. J. Periodontol. 89, 531–539. https://doi.org/10.1002/JPER.17-0377 (2018).
doi: 10.1002/JPER.17-0377
pubmed: 29520798
Roswall, J. et al. Overweight at four years of age in a Swedish birth cohort: influence of neighbourhood-level purchasing power. BMC Public Health 16, 546. https://doi.org/10.1186/s12889-016-3252-1 (2016).
doi: 10.1186/s12889-016-3252-1
pubmed: 27400741
pmcid: 4940903
Organization, W. H. Oral Health Surveys: Basic Methods (World Health Organization, 2013).
Boustedt, K., Dahlgren, J., Twetman, S. & Roswall, J. Tooth brushing habits and prevalence of early childhood caries: A prospective cohort study. Eur. Arch. Paediatr. Dent. 21, 155–159. https://doi.org/10.1007/s40368-019-00463-3 (2020).
doi: 10.1007/s40368-019-00463-3
pubmed: 31338770
Callahan, B. J. et al. DADA2: High-resolution sample inference from Illumina amplicon data. Nat. Methods 13, 581–583. https://doi.org/10.1038/nmeth.3869 (2016).
doi: 10.1038/nmeth.3869
pubmed: 27214047
pmcid: 4927377
Quast, C. et al. The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res. 41, D590–D596. https://doi.org/10.1093/nar/gks1219 (2013).
doi: 10.1093/nar/gks1219
pubmed: 23193283
Davis, N. M., Proctor, D. M., Holmes, S. P., Relman, D. A. & Callahan, B. J. Simple statistical identification and removal of contaminant sequences in marker-gene and metagenomics data. Microbiome 6, 226. https://doi.org/10.1186/s40168-018-0605-2 (2018).
doi: 10.1186/s40168-018-0605-2
pubmed: 30558668
pmcid: 6298009
Team, R. C. R: A language and environment for statistical computing. (2020). DOI:
Oksanen, J. et al. vegan: Community Ecology Package 2022).
Holmes, I., Harris, K. & Quince, C. Dirichlet multinomial mixtures: generative models for microbial metagenomics. PLoS One 7, e30126. https://doi.org/10.1371/journal.pone.0030126 (2012).
doi: 10.1371/journal.pone.0030126
pubmed: 22319561
pmcid: 3272020
Stewart, C. J. et al. Temporal development of the gut microbiome in early childhood from the TEDDY study. Nature 562, 583–588. https://doi.org/10.1038/s41586-018-0617-x (2018).
doi: 10.1038/s41586-018-0617-x
pubmed: 30356187
pmcid: 6415775
Rohart, F., Gautier, B., Singh, A. & Lê Cao, K. A. mixOmics: An R package for ‘omics feature selection and multiple data integration. PLoS Comput. Biol. 13, e1005752. https://doi.org/10.1371/journal.pcbi.1005752 (2017).
doi: 10.1371/journal.pcbi.1005752
pubmed: 29099853
pmcid: 5687754
Lubbe, S., Filzmoser, P. & Templ, M. Comparison of zero replacement strategies for compositional data with large numbers of zeros. Chemom. Intell. Lab. Syst. 210, 104248. https://doi.org/10.1016/j.chemolab.2021.104248 (2021).
doi: 10.1016/j.chemolab.2021.104248
Vinod, H. D. (ed.) Causal Mediation Analysis Using R (Springer, New York, 2010).