Microbial Indicators of Dental Health, Dysbiosis, and Early Childhood Caries

D. Kahharova; V. Y. Pappalardo; M. J. Buijs; R. X. de Menezes; M. Peters; R. Jackson; A. T. Hara; G. Eckert; B. Katz; M. A. Keels; S. M. Levy; E. Zaura; B. W. Brandt; M. Fontana

doi:10.1177/00220345231160756

Microbial Indicators of Dental Health, Dysbiosis, and Early Childhood Caries

D. Kahharova^*
, V. Y. Pappalardo
, M. J. Buijs
, R. X. de Menezes
, M. Peters
, R. Jackson
, A. T. Hara
, G. Eckert
, B. Katz
, M. A. Keels
, S. M. Levy
, E. Zaura
, B. W. Brandt
, M. Fontana

^*Corresponding author for this work

Preventive Dentistry

Research output: Contribution to Journal › Article › Academic › peer-review

Abstract

Dental caries lesions are a clinical manifestation of disease, preceded by microbial dysbiosis, which is poorly characterized and thought to be associated with saccharolytic taxa. Here, we assessed the associations between the oral microbiome of children and various caries risk factors such as demographics and behavioral and clinical data across early childhood and characterized over time the salivary and dental plaque microbiome of children before clinical diagnosis of caries lesions. Children (N = 266) were examined clinically at ~1, 2.5, 4, and 6.5 y of age. The microbiome samples were collected at 1, 2.5, and 4 y. Caries groups consisted of children who remained caries free (International Caries Detection and Assessment System [ICDAS] = 0) at all time points (CFAT) (n = 50); children diagnosed with caries (ICDAS ≥ 1) at 6.5 y (C6.5), 4 y (C4), or 2.5 y of age (C2.5); and children with early caries or advanced caries lesions at specific time points. Microbial community analyses were performed on zero-radius operational taxonomic units (zOTUs) obtained from V4 of 16S ribosomal RNA gene amplicon sequences. The oral microbiome of the children was affected by various factors, including antibiotic use, demographics, and dietary habits of the children and their caregivers. At all time points, various risk factors explained more of the variation in the dental plaque microbiome than in saliva. At 1 y, composition of saliva of the C4 group differed from that of the CFAT group, while at 2.5 y, this difference was observed only in plaque. At 4 y, multiple salivary and plaque zOTUs of genera Prevotella and Leptotrichia were significantly higher in samples of the C6.5 group than those of the CFAT group. In conclusion, up to 3 y prior to clinical caries detection, the oral microbial communities were already in a state of dysbiosis that was dominated by proteolytic taxa. Plaque discriminated dysbiotic oral ecosystems from healthy ones better than saliva.

Original language	English
Pages (from-to)	759-766
Number of pages	8
Journal	Journal of Dental Research
Volume	102
Issue number	7
Early online date	11 Apr 2023
DOIs	https://doi.org/10.1177/00220345231160756
Publication status	Published - Jul 2023

Bibliographical note

Funding Information:
The authors disclosed receipt of the following financial support for the research, authorship, and/or publication of this article: This study was supported by National Institutes of Health (NIH) grant 5U01DE021412; NIH CTSA grants (UL1-TR000442, University of Iowa; 2UL1-TR000433, University of Michigan; and UL1-TR000006, Indiana University); Colgate-Palmolive, the University of Michigan, School of Dentistry; and a Consortium of Delta Dental Plans (Delta Dental of Iowa, Delta Dental of Wisconsin, the Renaissance Health Service Corporation for Delta Dental of Michigan). D. Kahharova was supported by Stichting Bevordering Tandheelkundige Kennis with NTvT Onderzoeksbeurs 2017 and by the ACTA Research Institute. V.Y. Pappalardo was funded by ACTA Research Institute, with ACTA 2019 Lustrum grant.

Publisher Copyright:
© International Association for Dental Research and American Association for Dental, Oral, and Craniofacial Research 2023.

Funding

The authors disclosed receipt of the following financial support for the research, authorship, and/or publication of this article: This study was supported by National Institutes of Health (NIH) grant 5U01DE021412; NIH CTSA grants (UL1-TR000442, University of Iowa; 2UL1-TR000433, University of Michigan; and UL1-TR000006, Indiana University); Colgate-Palmolive, the University of Michigan, School of Dentistry; and a Consortium of Delta Dental Plans (Delta Dental of Iowa, Delta Dental of Wisconsin, the Renaissance Health Service Corporation for Delta Dental of Michigan). D. Kahharova was supported by Stichting Bevordering Tandheelkundige Kennis with NTvT Onderzoeksbeurs 2017 and by the ACTA Research Institute. V.Y. Pappalardo was funded by ACTA Research Institute, with ACTA 2019 Lustrum grant.

Funders	Funder number
Renaissance Health Service
Stichting bevordering tandheelkundige kennis
National Institutes of Health	5U01DE021412, UL1-TR000442
National Institutes of Health
Indiana University
University of Michigan	UL1-TR000006
University of Michigan
School of Dentistry, University of Michigan
University of Iowa	2UL1-TR000433
University of Iowa
Asia Research Institute

Keywords

16S rRNA
antibiotics
child
dental caries
dental plaque
saliva

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10.1177/00220345231160756

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title = "Microbial Indicators of Dental Health, Dysbiosis, and Early Childhood Caries",

abstract = "Dental caries lesions are a clinical manifestation of disease, preceded by microbial dysbiosis, which is poorly characterized and thought to be associated with saccharolytic taxa. Here, we assessed the associations between the oral microbiome of children and various caries risk factors such as demographics and behavioral and clinical data across early childhood and characterized over time the salivary and dental plaque microbiome of children before clinical diagnosis of caries lesions. Children (N = 266) were examined clinically at \textasciitilde{}1, 2.5, 4, and 6.5 y of age. The microbiome samples were collected at 1, 2.5, and 4 y. Caries groups consisted of children who remained caries free (International Caries Detection and Assessment System [ICDAS] = 0) at all time points (CFAT) (n = 50); children diagnosed with caries (ICDAS ≥ 1) at 6.5 y (C6.5), 4 y (C4), or 2.5 y of age (C2.5); and children with early caries or advanced caries lesions at specific time points. Microbial community analyses were performed on zero-radius operational taxonomic units (zOTUs) obtained from V4 of 16S ribosomal RNA gene amplicon sequences. The oral microbiome of the children was affected by various factors, including antibiotic use, demographics, and dietary habits of the children and their caregivers. At all time points, various risk factors explained more of the variation in the dental plaque microbiome than in saliva. At 1 y, composition of saliva of the C4 group differed from that of the CFAT group, while at 2.5 y, this difference was observed only in plaque. At 4 y, multiple salivary and plaque zOTUs of genera Prevotella and Leptotrichia were significantly higher in samples of the C6.5 group than those of the CFAT group. In conclusion, up to 3 y prior to clinical caries detection, the oral microbial communities were already in a state of dysbiosis that was dominated by proteolytic taxa. Plaque discriminated dysbiotic oral ecosystems from healthy ones better than saliva.",

keywords = "16S rRNA, antibiotics, child, dental caries, dental plaque, saliva",

author = "D. Kahharova and Pappalardo, \{V. Y.\} and Buijs, \{M. J.\} and \{de Menezes\}, \{R. X.\} and M. Peters and R. Jackson and Hara, \{A. T.\} and G. Eckert and B. Katz and Keels, \{M. A.\} and Levy, \{S. M.\} and E. Zaura and Brandt, \{B. W.\} and M. Fontana",

note = "Funding Information: The authors disclosed receipt of the following financial support for the research, authorship, and/or publication of this article: This study was supported by National Institutes of Health (NIH) grant 5U01DE021412; NIH CTSA grants (UL1-TR000442, University of Iowa; 2UL1-TR000433, University of Michigan; and UL1-TR000006, Indiana University); Colgate-Palmolive, the University of Michigan, School of Dentistry; and a Consortium of Delta Dental Plans (Delta Dental of Iowa, Delta Dental of Wisconsin, the Renaissance Health Service Corporation for Delta Dental of Michigan). D. Kahharova was supported by Stichting Bevordering Tandheelkundige Kennis with NTvT Onderzoeksbeurs 2017 and by the ACTA Research Institute. V.Y. Pappalardo was funded by ACTA Research Institute, with ACTA 2019 Lustrum grant. Publisher Copyright: {\textcopyright} International Association for Dental Research and American Association for Dental, Oral, and Craniofacial Research 2023.",

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doi = "10.1177/00220345231160756",

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AU - de Menezes, R. X.

AU - Peters, M.

AU - Jackson, R.

AU - Hara, A. T.

AU - Eckert, G.

AU - Katz, B.

AU - Keels, M. A.

AU - Levy, S. M.

AU - Zaura, E.

AU - Brandt, B. W.

AU - Fontana, M.

N1 - Funding Information: The authors disclosed receipt of the following financial support for the research, authorship, and/or publication of this article: This study was supported by National Institutes of Health (NIH) grant 5U01DE021412; NIH CTSA grants (UL1-TR000442, University of Iowa; 2UL1-TR000433, University of Michigan; and UL1-TR000006, Indiana University); Colgate-Palmolive, the University of Michigan, School of Dentistry; and a Consortium of Delta Dental Plans (Delta Dental of Iowa, Delta Dental of Wisconsin, the Renaissance Health Service Corporation for Delta Dental of Michigan). D. Kahharova was supported by Stichting Bevordering Tandheelkundige Kennis with NTvT Onderzoeksbeurs 2017 and by the ACTA Research Institute. V.Y. Pappalardo was funded by ACTA Research Institute, with ACTA 2019 Lustrum grant. Publisher Copyright: © International Association for Dental Research and American Association for Dental, Oral, and Craniofacial Research 2023.

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N2 - Dental caries lesions are a clinical manifestation of disease, preceded by microbial dysbiosis, which is poorly characterized and thought to be associated with saccharolytic taxa. Here, we assessed the associations between the oral microbiome of children and various caries risk factors such as demographics and behavioral and clinical data across early childhood and characterized over time the salivary and dental plaque microbiome of children before clinical diagnosis of caries lesions. Children (N = 266) were examined clinically at ~1, 2.5, 4, and 6.5 y of age. The microbiome samples were collected at 1, 2.5, and 4 y. Caries groups consisted of children who remained caries free (International Caries Detection and Assessment System [ICDAS] = 0) at all time points (CFAT) (n = 50); children diagnosed with caries (ICDAS ≥ 1) at 6.5 y (C6.5), 4 y (C4), or 2.5 y of age (C2.5); and children with early caries or advanced caries lesions at specific time points. Microbial community analyses were performed on zero-radius operational taxonomic units (zOTUs) obtained from V4 of 16S ribosomal RNA gene amplicon sequences. The oral microbiome of the children was affected by various factors, including antibiotic use, demographics, and dietary habits of the children and their caregivers. At all time points, various risk factors explained more of the variation in the dental plaque microbiome than in saliva. At 1 y, composition of saliva of the C4 group differed from that of the CFAT group, while at 2.5 y, this difference was observed only in plaque. At 4 y, multiple salivary and plaque zOTUs of genera Prevotella and Leptotrichia were significantly higher in samples of the C6.5 group than those of the CFAT group. In conclusion, up to 3 y prior to clinical caries detection, the oral microbial communities were already in a state of dysbiosis that was dominated by proteolytic taxa. Plaque discriminated dysbiotic oral ecosystems from healthy ones better than saliva.

AB - Dental caries lesions are a clinical manifestation of disease, preceded by microbial dysbiosis, which is poorly characterized and thought to be associated with saccharolytic taxa. Here, we assessed the associations between the oral microbiome of children and various caries risk factors such as demographics and behavioral and clinical data across early childhood and characterized over time the salivary and dental plaque microbiome of children before clinical diagnosis of caries lesions. Children (N = 266) were examined clinically at ~1, 2.5, 4, and 6.5 y of age. The microbiome samples were collected at 1, 2.5, and 4 y. Caries groups consisted of children who remained caries free (International Caries Detection and Assessment System [ICDAS] = 0) at all time points (CFAT) (n = 50); children diagnosed with caries (ICDAS ≥ 1) at 6.5 y (C6.5), 4 y (C4), or 2.5 y of age (C2.5); and children with early caries or advanced caries lesions at specific time points. Microbial community analyses were performed on zero-radius operational taxonomic units (zOTUs) obtained from V4 of 16S ribosomal RNA gene amplicon sequences. The oral microbiome of the children was affected by various factors, including antibiotic use, demographics, and dietary habits of the children and their caregivers. At all time points, various risk factors explained more of the variation in the dental plaque microbiome than in saliva. At 1 y, composition of saliva of the C4 group differed from that of the CFAT group, while at 2.5 y, this difference was observed only in plaque. At 4 y, multiple salivary and plaque zOTUs of genera Prevotella and Leptotrichia were significantly higher in samples of the C6.5 group than those of the CFAT group. In conclusion, up to 3 y prior to clinical caries detection, the oral microbial communities were already in a state of dysbiosis that was dominated by proteolytic taxa. Plaque discriminated dysbiotic oral ecosystems from healthy ones better than saliva.

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JF - Journal of Dental Research

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Microbial Indicators of Dental Health, Dysbiosis, and Early Childhood Caries

Abstract

Bibliographical note

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Keywords

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