Skip to main content

Advertisement

SpringerLink
Log in

Oral Health and the Altered Colonic Mucosa-Associated Gut Microbiota

  • Original Article
  • Published:
Digestive Diseases and Sciences Aims and scope Submit manuscript

Abstract

Background

Systemic diseases have been associated with oral health and gut microbiota. We examined the association between oral health and the community composition and structure of the adherent colonic gut microbiota.

Methods

We obtained 197 snap-frozen colonic biopsies from 62 colonoscopy-confirmed polyp-free individuals. Microbial DNA was sequenced for the 16S rRNA V4 region using the Illumina MiSeq, and the sequences were assigned to the operational taxonomic unit based on SILVA. We used a questionnaire to ascertain tooth loss, gum disease, and lifestyle factors. We compared biodiversity and relative abundance of bacterial taxa based on the amount of tooth loss and the presence of gum disease. The multivariable negative binomial regression model for panel data was used to estimate the association between the bacterial count and oral health. False discovery rate-adjusted P value (q value) < .05 indicated statistical significance.

Results

More tooth loss and gum disease were associated with lower bacterial alpha diversity. The relative abundance of Faecalibacterium was lower (q values < .05) with more tooth loss. The association was significant after adjusting for age, ethnicity, obesity, smoking, alcohol use, hypertension, diabetes, and the colon segment. The relative abundance of Bacteroides was higher in those with gum disease.

Conclusions

Oral health was associated with alteration in the community composition and structure of the adherent gut bacteria in the colon. The reduced anti-inflammatory Faecalibacterium in participants with more tooth loss may indicate systemic inflammation. Future studies are warranted to confirm our findings and investigate the systemic role of Faecalibacterium.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  1. Kane SF. The effects of oral health on systemic health. Gen Dent. 2017;6:30–34.

    Google Scholar 

  2. Tavares M, Calabi KA, San Martin L. Systemic diseases and oral health. Dent Clin. 2014;4:797–814.

    Google Scholar 

  3. Momen Heravi F, Babic A, Tworoger SS, et al. Periodontal disease, tooth loss and colorectal cancer risk: results from the Nurses’ Health Study. Int J Cancer. 2017;3:646–652.

    Article  CAS  Google Scholar 

  4. Maisonneuve P, Amar S, Lowenfels AB. Periodontal disease, edentulism, and pancreatic cancer: a meta-analysis. Ann Oncol. 2017;5:985–995.

    Article  Google Scholar 

  5. Oliveira FA, Fernandes Forte CP, Silva PG, et al. Relationship of Streptococcus mutans with valvar cardiac tissue: a molecular and immunohistochemical study. J Oral Pathol Med. 2019;48:745–753.

    Article  CAS  PubMed  Google Scholar 

  6. Rajendran M, Looney S, Singh N, et al. Systemic antibiotic therapy reduces circulating inflammatory dendritic cells and Treg–Th17 plasticity in periodontitis. J Immunol. 2019;202:2690–2699.

    Article  CAS  PubMed  Google Scholar 

  7. D’Aiuto F, Parkar M, Andreou G, et al. Periodontitis and systemic inflammation: control of the local infection is associated with a reduction in serum inflammatory markers. J Dent Res. 2004;83:156–160.

    Article  PubMed  Google Scholar 

  8. Roca-Millan E, González-Navarro B, del Mar Sabater-Recolons M, Marí-Roig A, Jané-Salas E, López-López J. Periodontal treatment on patients with cardiovascular disease: systematic review and meta-analysis. Med Oral Patol Oral Cirugia Bucal. 2018;23:e681.

    CAS  Google Scholar 

  9. Ide M, Harris M, Stevens A, et al. Periodontitis and cognitive decline in Alzheimer’s disease. PloS One. 2016;11:e0151081.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  10. West CE, Renz H, Jenmalm MC, et al. The gut microbiota and inflammatory noncommunicable diseases: associations and potentials for gut microbiota therapies. J Allergy Clin Immunol. 2015;1:3–13.

    Article  Google Scholar 

  11. Meyer TA, Noguchi Y, Ogle CK, et al. Endotoxin stimulates interleukin-6 production in intestinal epithelial cells: a synergistic effect with prostaglandin E2. Arch Surg. 1994;12:1290–1295.

    Article  Google Scholar 

  12. Koch A, Meesters MI, Scheller B, Boer C, Zacharowski K. Systemic endotoxin activity correlates with clot formation: an observational study in patients with early systemic inflammation and sepsis. Crit Care. 2013;5:R198.

    Article  Google Scholar 

  13. Sokol H, Pigneur B, Watterlot L, et al. Faecalibacterium prausnitzii is an anti-inflammatory commensal bacterium identified by gut microbiota analysis of Crohn disease patients. Proc Natl Acad Sci USA. 2008;43:16731–16736.

    Article  CAS  Google Scholar 

  14. Gurwara S, Ajami NJ, Jang A, et al. Dietary nutrients involved in one-carbon metabolism and colonic mucosa-associated gut microbiome in individuals with an endoscopically normal colon. Nutrients. 2019;3:613.

    Article  CAS  Google Scholar 

  15. Subar AF, Thompson FE, Kipnis V, et al. Comparative validation of the Block, Willett, and National Cancer Institute food frequency questionnaires: the Eating at America’s Table Study. Am J Epidemiol. 2001;12:1089–1099.

    Article  Google Scholar 

  16. Guenther PM, Reedy J, Krebs-Smith SM. Development of the healthy eating index-2005. J Am Dietetic Assoc. 2008;108:1896–1901.

    Article  Google Scholar 

  17. Caporaso JG, Lauber CL, Walters WA, et al. Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms. ISME J. 2012;8:1621–1624.

    Article  CAS  Google Scholar 

  18. Methé BA, Nelson KE, Pop M, et al. A framework for human microbiome research. Nature. 2012;7402:215.

    Google Scholar 

  19. Huttenhower C, Gevers D, Knight R, et al. Structure, function and diversity of the healthy human microbiome. Nature. 2012;7402:207.

    Google Scholar 

  20. Edgar RC. Search and clustering orders of magnitude faster than BLAST. Bioinformatics. 2010;19:2460–2461.

    Article  CAS  Google Scholar 

  21. Edgar RC. UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat Methods. 2013;10:996.

    Article  CAS  Google Scholar 

  22. Quast C, Pruesse E, Yilmaz P, et al. The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res. 2012;D1:D590–D596.

    Article  CAS  Google Scholar 

  23. Paradis E, Claude J, Strimmer K. APE: analyses of phylogenetics and evolution in R language. Bioinformatics. 2004;2:289–290.

    Article  Google Scholar 

  24. Lozupone C, Lladser ME, Knights D, Stombaugh J, Knight R. UniFrac: an effective distance metric for microbial community comparison. ISME J. 2011;2:169–172.

    Article  Google Scholar 

  25. Gloor GB, Macklaim JM, Pawlowsky-Glahn V, Egozcue JJ. Microbiome datasets are compositional: and this is not optional. Front Microbiol. 2017;15:2224.

    Article  Google Scholar 

  26. Benjamini Y, Yekutieli D. Quantitative trait loci analysis using the false discovery rate. Genetics. 2005;2:783–790.

    Article  CAS  Google Scholar 

  27. Lourenςo TG, Spencer SJ, Alm EJ, Colombo AP. Defining the gut microbiota in individuals with periodontal diseases: an exploratory study. J Oral Microbiol. 2018;1:1487741.

    Article  CAS  Google Scholar 

  28. Ai D, Huang R, Wen J, Li C, Zhu J, Xia LC. Integrated metagenomic data analysis demonstrates that a loss of diversity in oral microbiota is associated with periodontitis. BMC Genomics. 2017;1:1041.

    Article  Google Scholar 

  29. Meuric V, Le Gall-David S, Boyer E, et al. Signature of microbial dysbiosis in periodontitis. Appl Environ Microbiol. 2017;14:e00462-17.

    Google Scholar 

  30. Schulz S, Porsch M, Grosse I, Hoffmann K, Schaller HG, Reichert S. Comparison of the oral microbiome of patients with generalized aggressive periodontitis and periodontitis-free subjects. Arch Oral Biol. 2019;99:169–176.

    Article  CAS  PubMed  Google Scholar 

  31. Ohira H, Tsutsui W, Fujioka Y. Are short chain fatty acids in gut microbiota defensive players for inflammation and atherosclerosis? J Atheroscler Thromb. 2017;7:660–672.

    Article  Google Scholar 

  32. Martín R, Miquel S, Benevides L, et al. Functional characterization of novel Faecalibacterium prausnitzii strains isolated from healthy volunteers: a step forward in the use of F. prausnitzii as a next-generation probiotic. Front Microbiol. 2017;8:1226.

  33. Breyner NM, Michon C, de Sousa CS, et al. Microbial anti-inflammatory molecule (MAM) from Faecalibacterium prausnitzii shows a protective effect on DNBS and DSS-induced colitis model in mice through inhibition of NF-κB pathway. Front Microbiol. 2017;8:114.

    Article  PubMed  PubMed Central  Google Scholar 

  34. Quévrain E, Maubert MA, Michon C, et al. Identification of an anti-inflammatory protein from Faecalibacterium prausnitzii, a commensal bacterium deficient in Crohn’s disease. Gut. 2016;3:415–425.

    Article  CAS  Google Scholar 

  35. Balamurugan R, Rajendiran E, George S, Samuel GV, Ramakrishna BS. Real-time polymerase chain reaction quantification of specific butyrate-producing bacteria, Desulfovibrio and Enterococcus faecalis in the feces of patients with colorectal cancer. J Gastroenterol Hepatol. 2008;8pt1:1298–1303.

  36. Shin NR, Whon TW, Bae JW. Proteobacteria: microbial signature of dysbiosis in gut microbiota. Trends Biotechnol. 2015;9:496–503.

    Article  CAS  Google Scholar 

  37. Distrutti E, Monaldi L, Ricci P, Fiorucci S. Gut microbiota role in irritable bowel syndrome: new therapeutic strategies. World J Gastroenterol. 2016;21:2219.

    Article  CAS  Google Scholar 

  38. Kim JM, Oh YK, Kim YJ, Youn J, Ahn MJ. Escherichia coli up-regulates proinflammatory cytokine expression in granulocyte/macrophage lineages of CD34 + stem cells via p50 homodimeric NF-κB. Clin Exp Immunol. 2004;2:341–350.

    Article  CAS  Google Scholar 

  39. Van Winkelhoff AJ, Loos BG, Van Der Reijden WA, Van Der Velden U. Porphyromonas gingivalis, Bacteroides forsythus and other putative periodontal pathogens in subjects with and without periodontal destruction. J Clin Periodontol. 2002;11:1023–1028.

    Article  Google Scholar 

  40. Wexler HM. Bacteroides: the good, the bad, and the nitty-gritty. Clin Microbiol Rev. 2007;20:593–621.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. O’Donnell LE, Robertson D, Nile CJ, et al. The oral microbiome of denture wearers is influenced by levels of natural dentition. PLoS One. 2015;9:e0137717.

    Article  CAS  Google Scholar 

  42. Savoca MR, Arcury TA, Leng X, et al. Impact of denture usage patterns on dietary quality and food avoidance among older adults. J Nutr Gerontol Geriatr. 2011;1:86–102.

    Article  Google Scholar 

  43. Olsen I, Yamazaki K. Can oral bacteria affect the microbiome of the gut? J Oral Microbiol. 2019;1:1586422.

    Article  CAS  Google Scholar 

  44. Duncan SH, Hold GL, Harmsen HJ, Stewart CS, Flint HJ. Growth requirements and fermentation products of Fusobacterium prausnitzii, and a proposal to reclassify it as Faecalibacterium prausnitzii gen. nov., comb. nov. Int J Syst Evol Microbiol. 2002;6:2141–2146.

  45. Mal X, Wactawski Wende J, Hovey KM, et al. Associations between smoking and tooth loss according to the reason for tooth loss: the Buffalo OsteoPerio Study. J Am Dent Assoc. 2013;3:252–265.

    Google Scholar 

  46. Huang C, Shi G. Smoking and microbiome in oral, airway, gut and some systemic diseases. J Transl Med. 2019;1:225.

    Article  Google Scholar 

  47. Iwasaki M, Borgnakke WS, Ogawa H, et al. Effect of lifestyle on 6-year periodontitis incidence or progression and tooth loss in older adults. J Clin Periodontol. 2018;8:896–908.

    Article  Google Scholar 

  48. La Ferla K, Seegert D, Schreiber S. Activation of NF-κB in intestinal epithelial cells by E. coli strains isolated from the colonic mucosa of IBD patients. Int J Colorectal Dis. 2004;4:334–342.

  49. Rabiei N, Badi SA, Marvasti FE, Sattari TN, Vaziri F, Siadat SD. Induction effects of Faecalibacterium prausnitzii and its extracellular vesicles on toll-like receptor signaling pathway gene expression and cytokine level in human intestinal epithelial cells. Cytokine. 2019;121:154718.

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

We thank David Ramsey, Diane Hutchinson, and Nadim Ajami at Baylor College of Medicine for project management. We thank Ashely Johnson, Sarah Plew, Ava Smith, Liang Chen, and Jocelyn Uriostegui for collecting and processing samples. We thank Dr. David Y. Graham for patient recruitment and manuscript review. We thank Annie Dai for manuscript preparation.

Funding

This study is funded by Cancer Prevention and Research Institute of Texas (RP#140767, PI: Jiao, L; Petrosino, JF), Gillson Longenbaugh Foundation, Golfers Against Cancer organization (PI: Jiao, L), and partly supported by the use of resources and facilities at the Houston VA HSR&D Center for Innovations in Quality, Effectiveness and Safety (CIN13-413) and The Texas Medical Center Digestive Disease Center (P30 DK56338, PI: El-Serag, HB). Jiao received the salary support from the NIH R01CA172880 (PI: Jiao, L). White received the grant support from the U.S. Department of Veterans Affairs (CX001430, PI: White, D). The opinions expressed are those of the authors and not necessarily those of the Department of Veterans Affairs, the US government, or Baylor College of Medicine.

Author information

Authors and Affiliations

  1. Department of Medicine, Baylor College of Medicine, 2002 Holcombe Blvd, MS152, Houston, 77030, TX, USA

    Anthony A. Xu, Shawn Gurwara, Donna L. White, Fasiha Kanwal, Hashem B. El-Serag & Li Jiao

  2. Department of Molecular Virology and Microbiology, The Alkek Center for Metagenomics and Microbiome Research, Baylor College of Medicine, 2002 Holcombe Blvd, MS152, Houston, 77030, TX, USA

    Kristi Hoffman & Joseph F. Petrosino

  3. Section of Gastroenterology, Michael E. DeBakey VA Medical Center, 2002 Holcombe Blvd, MS152, Houston, 77030, TX, USA

    Fasiha Kanwal, Hashem B. El-Serag & Li Jiao

  4. Texas Medical Center Digestive Disease Center, 2002 Holcombe Blvd, MS152, Houston, 77030, TX, USA

    Donna L. White, Fasiha Kanwal, Hashem B. El-Serag, Joseph F. Petrosino & Li Jiao

  5. Dan L Duncan Comprehensive Cancer Center, Baylor College of Medicine, 2002 Holcombe Blvd, MS152, Houston, 77030, TX, USA

    Donna L. White, Fasiha Kanwal, Hashem B. El-Serag, Joseph F. Petrosino & Li Jiao

  6. Center for Innovations in Quality, Effectiveness and Safety, Michael E. DeBakey VA Medical Center, 2002 Holcombe Blvd, MS152, Houston, 77030, TX, USA

    Donna L. White, Fasiha Kanwal, Hashem B. El-Serag & Li Jiao

  7. Center for Translational Research on Inflammatory Diseases (CTRID), Michael E. DeBakey VA Medical Center, 2002 Holcombe Blvd, MS152, Houston, 77030, TX, USA

    Donna L. White & Li Jiao

Authors
  1. Anthony A. Xu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Kristi Hoffman
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Shawn Gurwara
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Donna L. White
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Fasiha Kanwal
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Hashem B. El-Serag
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Joseph F. Petrosino
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Li Jiao
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Li Jiao.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional research committee and with the 1964 Helsinki declaration and its later amendments.

Informed consent

Informed consent was obtained from all participants included in the study.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PPTX 210 kb)

Supplementary material 2 (DOCX 16 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Xu, A.A., Hoffman, K., Gurwara, S. et al. Oral Health and the Altered Colonic Mucosa-Associated Gut Microbiota. Dig Dis Sci 66, 2981–2991 (2021). https://doi.org/10.1007/s10620-020-06612-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10620-020-06612-9

Keywords

Search

Navigation