Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Original Article
  • Published:

Clinical Studies and Practice

Tannerella forsythia and coating color on the tongue dorsum, and fatty food liking associate with fat accumulation and insulin resistance in adult catch-up fat

Abstract

Background/Objectives:

We aimed to determine the alteration of Tannerella forsythia and coating color on the dorsal tongue, and fatty food liking in catch-up fat in adult (CUFA), as well as the probable associations between fat accumulation, insulin resistance (IR) and these changes.

Subjects/Methods:

T. forsythia on the tongue dorsum, fatty food liking, fat accumulation and insulin sensitivity were investigated in CUFA humans and rats, and tongue-coating color was observed in CUFA individuals. We further determined the changes of fatty food liking, fat accumulation and IR in T. forsythia-infected rodents by oral lavage.

Results:

Increases in fat accumulation, IR, percentage of subjects with yellow tongue coating and that with T. forsythia detected were observed in CUFA individuals. Additionally, the fat ranking scores were significantly lower and the hedonic ratings of low-fat options of sampled food were lower, while the ratings of high-fat options were remarkably higher in CUFA subjects. Additionally, T. forsythia level elevated in CUFA rats, and fatty food liking, fat accumulation and IR increased in CUFA and T. forsythia-infected animals, with the increases in T. forsythia infection and fatty food liking preceding the occurrence of fat accumulation and IR.

Conclusions:

T. forsythia and yellow coating on the dorsal tongue and fatty food liking associate fat accumulation and IR in CUFA. Moreover, we tentatively put forward that T. forsythia, which is very important in yellow tongue-coating microbiota, and its consequent increases in fatty food liking, might be crucial in the development of fat accumulation and IR in CUFA.

This is a preview of subscription content, access via your institution

Access options

Buy this article

Prices may be subject to local taxes which are calculated during checkout

Figure 1
Figure 2
Figure 3

Similar content being viewed by others

References

  1. Marcelino H, Veyrat-Durebex C, Summermatter S, Sarafian D, Miles-Chan J, Arsenijevic D et al. A role for adipose tissue de novo lipogenesis in glucose homeostasis during catch-up growth: a Randle cycle favoring fat storage. Diabetes 2013; 62: 362–372.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Hu X, Chen LL, Zheng J, Kong W, Zhang HH, Zeng TS et al. Increases in systemic and local stress: a probable mechanism of visceral fat accumulation and insulin resistance in adult catch-up growth rats? Exp Biol Med 2013; 238: 57–65.

    Article  CAS  Google Scholar 

  3. Hu X, Zhang Q, Zheng J, Kong W, Zhang HH, Zeng TS et al. Alteration of FXR phosphorylation and sumoylation in liver in the development of adult catch-up growth. Exp Biol Med 2016; 242: 297–304.

    Article  Google Scholar 

  4. Tao F, Lu H, Oppert JM, Basdevant A . ZHENG may contribute to obesity phenotypes based on body composition: a pilot study on the traditional chinese medicine approach. Evid Based Complement Alternat Med 2014; 2014: 580803.

    PubMed  PubMed Central  Google Scholar 

  5. Sui Y, Zhao HL, Wong VC, Brown N, Li XL, Kwan AK et al. A systematic review on use of Chinese medicine and acupuncture for treatment of obesity. Obes Rev 2012; 13: 409–430.

    Article  CAS  PubMed  Google Scholar 

  6. Lee TC, Lo LC, Wu FC . Traditional chinese medicine for metabolic syndrome via TCM pattern differentiation: tongue diagnosis for predictor. Evid Based Complement Alternat Med 2016; 2016: 1971295.

    PubMed  PubMed Central  Google Scholar 

  7. Tseng SH, Chien TY, Chen JR, Lin IH, Wang CC . Hypolipidemic effects of three purgative decoctions. Evid Based Complement Alternat Med 2011; 2011: 249254.

    Article  PubMed  PubMed Central  Google Scholar 

  8. Han S, Chen Y, Hu J, Ji Z . Tongue images and tongue coating microbiome in patients with colorectal cancer. Microb Pathog 2014; 77: 1–6.

    Article  PubMed  Google Scholar 

  9. Ye J, Cai X, Yang J, Sun X, Hu C, Xia J et al. Bacillus as a potential diagnostic marker for yellow tongue coating. Sci Rep 2016; 6: 32496.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Haffajee AD, Socransky SS . Relation of body mass index, periodontitis and Tannerella forsythia. J Clin Periodontol 2009; 36: 89–99.

    Article  PubMed  Google Scholar 

  11. Ardila CM, Perez-Valencia AY, Rendon-Osorio WL . Tannerella forsythia is associated with increased levels of atherogenic low density lipoprotein and total cholesterol in chronic periodontitis. J Clin Exp Dent 2015; 7: e254–e260.

    Article  PubMed  PubMed Central  Google Scholar 

  12. Besnard P, Passilly-Degrace P, Khan NA . Taste of fat: a sixth taste modality? Physiol Rev 2016; 96: 151–176.

    Article  CAS  PubMed  Google Scholar 

  13. Tucker RM, Edlinger C, Craig BA, Mattes RD . Associations between BMI and fat taste sensitivity in humans. Chem Senses 2014; 39: 349–357.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Ulven T, Christiansen E . Dietary fatty acids and their potential for controlling metabolic diseases through activation of FFA4/GPR120. Annu Rev Nutr 2015; 35: 239–263.

    Article  CAS  Google Scholar 

  15. Crescenzo R, Lionetti L, Mollica MP, Ferraro M, D'Andrea E, Mainieri D et al. Altered skeletal muscle subsarcolemmal mitochondrial compartment during catch-up fat after caloric restriction. Diabetes 2006; 55: 2286–2293.

    Article  CAS  PubMed  Google Scholar 

  16. Chen LL, Hu X, Zheng J, Kong W, Zhang HH, Yang WH et al. Lipid overaccumulation and drastic insulin resistance in adult catch-up growth rats induced by nutrition promotion after undernutrition. Metabolism 2011; 60: 569–578.

    Article  CAS  PubMed  Google Scholar 

  17. Wu HY, Xu SY, Chen LL, Zhang HF . Waist to height ratio as a predictor of abdominal fat distribution in men. Chin J Physiol 2009; 52: 441–445.

    Article  PubMed  Google Scholar 

  18. Huang H, Peng M, Zhang J, Hu X, Chen L . Relocation potentiates obesity and cardiovascular risk: A case-control study on relocatees from the Three Gorges area. J Diabetes 2016; 8: 732–735.

    Article  PubMed  Google Scholar 

  19. Zhang WJ, Chen LL, Zheng J, Lin L, Zhang JY, Hu X . Association of adult weight gain and nonalcoholic fatty liver in a cross-sectional study in Wan Song Community, China. Braz J Med Biol Res 2014; 47: 151–156.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Stewart JE, Feinle-Bisset C, Golding M, Delahunty C, Clifton PM, Keast RS . Oral sensitivity to fatty acids, food consumption and BMI in human subjects. Br J Nutr 2010; 104: 145–152.

    Article  CAS  PubMed  Google Scholar 

  21. Haryono RY, Sprajcer MA, Keast RS . Measuring oral fatty acid thresholds, fat perception, fatty food liking, and papillae density in humans. J Vis Exp 2014; 88: 51236.

  22. Duffy VB, Hayes JE, Sullivan BS, Faghri P . Surveying food and beverage liking: a tool for epidemiological studies to connect chemosensation with health outcomes. Ann NY Acad Sci 2009; 1170: 558–568.

    Article  PubMed  Google Scholar 

  23. Huang Y, Zeng J, Chen G, Xie X, Guo W, Tian W . Periodontitis contributes to adipose tissue inflammation through the NF-κB, JNK and ERK pathways to promote insulin resistance in a rat model. Microbes Infect 2016; 18: 804–812.

    Article  CAS  PubMed  Google Scholar 

  24. Oktay S, Chukkapalli SS, Rivera-Kweh MF, Velsko IM, Holliday LS, Kesavalu L . Periodontitis in rats induces systemic oxidative stress that is controlled by bone-targeted antiresorptives. J Periodontol 2015; 86: 137–145.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Chen LL, Hu X, Zheng J, Zhang HH, Kong W, Yang WH et al. Increases in energy intake, insulin resistance and stress in rats before Wenchuan earthquake far from the epicenter. Exp Biol Med 2010; 235: 1216–1223.

    Article  CAS  Google Scholar 

  26. Shin AC, Townsend RL, Patterson LM, Berthoud HR . ‘Liking’ and ‘wanting’ of sweet and oily food stimuli as affected by high-fat diet-induced obesity, weight loss, leptin, and genetic predisposition. Am J Physiol Regul Integr Comp Physiol 2011; 301: R1267–R1280.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Feurte S, Nicolaidis S, Berridge KC . Conditioned taste aversion in rats for a threonine-deficient diet: demonstration by the taste reactivity test. Physiol Behav 2000; 68: 423–429.

    Article  CAS  PubMed  Google Scholar 

  28. Pataro AL, Cortelli SC, Abreu MH, Cortelli JR, Franco GC, Aquino DR et al. Frequency of periodontal pathogens and Helicobacter pylori in the mouths and stomachs of obese individuals submitted to bariatric surgery: a cross-sectional study. J Applied Oral Sci 2016; 24: 229–238.

    Article  Google Scholar 

  29. Sales-Peres SH, de Moura-Grec PG, Yamashita JM, Torres EA, Dionisio TJ, Leite CV et al. Periodontal status and pathogenic bacteria after gastric bypass: a cohort study. J Clin Periodontol 2015; 42: 530–536.

    Article  CAS  PubMed  Google Scholar 

  30. Tanaka TH . Tongue diagnosis: relationship between sublingual tongue morphology in three tongue protrusion angles and menstrual clinical symptoms. J Integrative Med 2015; 13: 248–256.

    Article  Google Scholar 

  31. Besnard P . Lipids and obesity: also a matter of taste? Rev Endocr Metab Disord 2016; 17: 159–170.

    Article  CAS  PubMed  Google Scholar 

  32. Cecil JD, O'Brien-Simpson NM, Lenzo JC, Holden JA, Chen YY, Singleton W et al. Differential responses of pattern recognition receptors to outer membrane vesicles of three periodontal pathogens. PLoS ONE 2016; 11: e0151967.

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

We thank all those involved in this work, with particular gratitude to Drs. Li Yuan, Yu-Ming Li, Hui Sun, Feng Gao, Wen-Fang Xia, Hui-Qing Li, Xiu-Ling Deng and Yun-Fei Liao for their generous advice and fruitful discussions. This work was supported by National Natural Science Foundation of China (81471069, 81170737, 81400820 and 81100562).

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to X Hu or L-L Chen.

Ethics declarations

Competing interests

The authors declare no conflict of interest.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Hu, X., Zhang, Q., Zhang, M. et al. Tannerella forsythia and coating color on the tongue dorsum, and fatty food liking associate with fat accumulation and insulin resistance in adult catch-up fat. Int J Obes 42, 121–128 (2018). https://doi.org/10.1038/ijo.2017.191

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/ijo.2017.191

This article is cited by

Search

Quick links