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Changes in oral health during aging in a novel non-human primate model

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Abstract

Oral health plays a significant role in the quality of life and overall well-being of the aging population. However, age-related changes in oral health are not well understood due to challenges with current animal models. In this study, we analyzed the oral health and microbiota of a short-lived non-human primate (i.e., marmoset), as a step towards establishing a surrogate for studying the changes that occur in oral health during human aging. We investigated the oral health of marmosets using cadaveric tissues in three different cohorts: young (aged ≤6 years), middle-aged, and older (>10 years) and assessed the gingival bacterial community using analyses of the V3–V4 variable region of 16S rRNA gene. The oldest cohort had a significantly higher number of dental caries, increased dental attrition/erosion, and deeper periodontal pocket depth scores. Oral microbiome analyses showed that older marmosets had a significantly greater abundance of Escherichia-Shigella and Propionibacterium, and a lower abundance of Agrobacterium/Rhizobium at the genus level. Alpha diversity of the microbiome between the three groups showed no significant differences; however, principal coordinate analysis and non-metric multidimensional scaling analysis revealed that samples from middle-aged and older marmosets were more closely clustered than the youngest cohort. In addition, linear discriminant analysis effect size (LEFSe) identified a higher abundance of Esherichia-Shigella as a potential pathogenic biomarker in older animals. Our findings confirm that changes in the oral microbiome are associated with a decline in oral health in aging marmosets. The current study suggests that the marmoset model recapitulates some of the changes in oral health associated with human aging and may provide opportunities for developing new preventive strategies or interventions which target these disease conditions.

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Funding

This research was supported by the NIH grants from the NIDCR (R21-DE028271A and R01-DE025286) and NIA (R01-AG050797, U34-AG068482, P30-AG013319, and P30-AG044271).

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Author notes

  1. Parveez Ahamed Abdul-Azees and Hanzhou Wang contributed equally to this study as first authors.

Authors and Affiliations

  1. Department of Comprehensive Dentistry, University of Texas Health Science Center at San Antonio, San Antonio, TX, USA

    Parveez Ahamed Abdul-Azees, Hanzhou Wang, Jason Pizzini, David D. Dean, Milos Marinkovic, Xiao-Dong Chen & Chih-Ko Yeh

  2. Department of Periodontics, Department of Cell Systems and Anatomy, Department of Molecular Medicine, University of Texas Health Science Center at San Antonio, San Antonio, TX, USA

    Yong-Hee P. Chun

  3. Barshop Institute for Longevity and Aging Studies, University of Texas Health Science Center at San Antonio, San Antonio, TX, USA

    Kelly R. Reveles, Xiao-Dong Chen, Adam B. Salmon & Chih-Ko Yeh

  4. Pharmacotherapy Division, College of Pharmacy, The University of Texas at Austin, Austin, TX, USA

    Kelly R. Reveles

  5. Research Service, South Texas Veterans Health Care System, San Antonio, TX, USA

    Milos Marinkovic & Xiao-Dong Chen

  6. Geriatric Research Education and Clinical Center, South Texas Veterans Health Care System, San Antonio, TX, USA

    Adam B. Salmon & Chih-Ko Yeh

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Contributions

PAAA and HW carried out the experiments, processed the experimental data and performed the analyses, drafted the manuscript, and designed the figures. YPC, JP, KRR, and MM processed the experimental data, verified the analytical method, validated the data curation, interpreted the results, and performed a critical review of the manuscript. DDD and XDC aided in interpretation of the results, validated the data curation, provided administrative support, and reviewed/edited the manuscript. CKY and ABS conceived the concept and design the study, supervised the project, obtained financial support, performed the data analysis and interpretation, manuscript writing, and final approval of the manuscript. All authors provided critical feedback, helped shape the research, conducted the analysis, and reviewed and approved the final version of the manuscript.

Corresponding author

Correspondence to Chih-Ko Yeh.

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Procedures in this study were conducted in compliance with the approval of UTHSCSA Institutional Animal Care and Use Committee (IACUC), US Public Health Service’s Policy on Humane Care and Use of Laboratory Animals, and American Society of Primatologists (ASP) regarding the use of experimental animals.

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The authors declare no competing interests.

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Abdul-Azees, P.A., Wang, H., Chun, YH.P. et al. Changes in oral health during aging in a novel non-human primate model. GeroScience 46, 1909–1926 (2024). https://doi.org/10.1007/s11357-023-00939-7

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