Skip to main content

Advertisement

Log in

Association of pentosidine and homocysteine levels with number of teeth present in Japanese postmenopausal women

  • Original Article
  • Published:
Journal of Bone and Mineral Metabolism Aims and scope Submit manuscript

Abstract

Introduction

Little is known about whether substances inducing tissue protein degeneration in the oral cavity are associated with the number of teeth present in postmenopausal women. We sought to investigate the association of urinary pentosidine and serum homocysteine levels with the number of teeth and subsequent tooth loss in Japanese postmenopausal women.

Materials and methods

Among participants in the Nagano Cohort Study, 785 postmenopausal women (mean age, 68.1 years) participated in the present study. The number of teeth was re-counted at the time of follow-up in 610 women. Poisson regression analysis was used to investigate differences in the number of teeth among quartiles of pentosidine or homocysteine, adjusting for covariates that correlated with the number of teeth. A Cox proportional hazard model was used to evaluate the association of subsequent tooth loss with pentosidine or homocysteine levels.

Results

Pentosidine quartiles were not associated with the number of teeth at baseline. Participants in the highest homocysteine quartile had significantly fewer teeth at baseline than those in the third and lowest quartiles (p < 0.001 for both). Those in the second quartile had fewer teeth than those in the third (p = 0.001) and lowest (p < 0.001) quartiles. An increased risk of tooth loss during follow-up was significantly associated with higher urinary pentosidine (hazard ratio = 1.073 for 10 pmol/mgCre; p = 0.001).

Conclusion

Postmenopausal women with higher homocysteine levels had fewer teeth at baseline. A higher pentosidine concentration increased the risk of subsequent tooth loss. High pentosidine or homocysteine concentrations may be associated with tooth loss in postmenopausal women.

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

Access this article

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

Instant access to the full article PDF.

Similar content being viewed by others

References

  1. Miyazaki H, Motegi E, Yatabe K, Yamaguchi H, Maki Y (2005) A study of occlusion in elderly Japanese over 80 years with at least 20 teeth. Gerodontology 22:206–210

    Article  PubMed  Google Scholar 

  2. Musacchio E, Binotto P, Perissinotto E, Sergi G, Zambon S, Corti MC, Frigo AC, Sartori L (2021) Tooth retention predicts good physical performance in older adults. PLoS ONE 16:e0255741

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Ito W, Komiyama T, Ohi T, Hiratsuka T, Matsuyama S, Sone T, Tsuji I, Watanabe M, Hattori Y (2021) Relationship between oral health and fractures in community-dwelling older Japanese adults. J Am Med Dir Assoc 22:1184–1189

    Article  PubMed  Google Scholar 

  4. Komiyama T, Ohi T, Miyoshi Y, Murakami T, Tsuboi A, Tomata Y, Tsuji I, Watanabe M, Hattori Y (2016) Association between tooth loss, receipt of dental care, and functional disability in an elderly Japanese population: the Tsurugaya Project. J Am Geriatr Soc 64:2495–2502

    Article  PubMed  Google Scholar 

  5. Yu YH, Cheung WS, Steffensen B, Miller DR (2021) Number of teeth is associated with all-cause and disease-specific mortality. BMC Oral Health 21:568

    Article  PubMed  PubMed Central  Google Scholar 

  6. Ishii T (2005) The meaning and problem of the 8020 movement in Japan (in Japanese). Nihon Hotetsu Shika Gakkai Zasshi 49:168–178

    Article  PubMed  Google Scholar 

  7. Krall EA, Dawson-Hughes B, Papas A, Garcia RI (1994) Tooth loss and skeletal bone density in healthy postmenopausal women. Osteoporos Int 4:104–109

    Article  CAS  PubMed  Google Scholar 

  8. Krall EA, Garcia RI, Dawson-Hughes B (1996) Increased risk of tooth loss is related to bone loss at the whole body, hip, and spine. Calcif Tissue Int 59:433–437

    Article  CAS  PubMed  Google Scholar 

  9. Krall EA, Wehler C, Garcia RI, Harris SS, Dawson-Hughes B (2001) Calcium and vitamin D supplements reduce tooth loss in the elderly. Am J Med 111:452–456

    Article  CAS  PubMed  Google Scholar 

  10. Penoni DC, Fidalgo TK, Torres SR, Varela VM, Masterson D, Leão AT, Maia LC (2017) Bone density and clinical periodontal attachment in postmenopausal women: a systematic review and meta-analysis. J Dent Res 96:261–269

    Article  CAS  PubMed  Google Scholar 

  11. Xu S, Zhang G, Guo JF, Tan YH (2021) Associations between osteoporosis and risk of periodontitis: a pooled analysis of observational studies. Oral Dis 27:357–369

    Article  PubMed  Google Scholar 

  12. Wang CJ, McCauley LK (2016) Osteoporosis and periodontitis. Curr Osteoporos Rep 14:284–291

    Article  PubMed  PubMed Central  Google Scholar 

  13. Stöhr J, Barbaresko J, Neuenschwander M, Schlesinger S (2021) Bidirectional association between periodontal disease and diabetes mellitus: a systematic review and meta-analysis of cohort studies. Sci Rep 11:13686

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  14. Lalla E, Papapanou PN (2011) Diabetes mellitus and periodontitis: a tale of two common interrelated diseases. Nat Rev Endocrinol 7:738–748

    Article  CAS  PubMed  Google Scholar 

  15. Saito M, Kida Y, Kato S, Marumo K (2014) Diabetes, collagen, and bone quality. Curr Osteoporos Rep 12:181–188

    Article  PubMed  Google Scholar 

  16. Schwartz AV, Garnero P, Hillier TA, Sellmeyer DE, Strotmeyer ES, Feingold KR, Resnick HE, Tylavsky FA, Black DM, Cummings SR, Harris TB, Bauer DC, Health, Aging, and Body Composition Study (2009) Pentosidine and increased fracture risk in older adults with type diabetes. J Clin Endocrinol Metab 94:2380–2386

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Tanaka S, Kuroda T, Saito M, Shiraki M (2011) Urinary pentosidine improves risk classification using fracture risk assessment tools for postmenopausal women. J Bone Miner Res 26:2778–2784

    Article  CAS  PubMed  Google Scholar 

  18. Saito M, Marumo K (2018) The effects of homocysteine on the skeleton. Curr Osteoporos Rep 16:554–560

    Article  PubMed  Google Scholar 

  19. He T, Jin X, Koh YS, Zhang Q, Zhang C, Liu F (2021) The association of homocysteine, folate, vitamin B12, and vitamin B6 with fracture incidence in older adults: a systematic review and meta-analysis. Ann Transl Med 9:1143

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Husseini B, Nehme E, Senni K, Ghorra CS, Younes K, Roffino S, Ghorra P, Changotade S, Younes R (2022) Oral manifestations associated with inherited hyperhomocysteinemia: a first case description. Oral Surg Oral Med Oral Pathol Oral Radiol 133:e105–e112

    Article  PubMed  Google Scholar 

  21. Joseph R, Nath SG, Joseraj MG (2011) Elevated plasma homocysteine levels in chronic periodontitis: a hospital-based case-control study. J Periodontol 82:439–444

    Article  PubMed  Google Scholar 

  22. Botelho J, Machado V, Leira Y, Proença L, Mendes JJ (2021) Periodontal inflamed surface area mediates the link between homocysteine and blood pressure. Biomolecules 11:875

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Taguchi A, Fujiwara S, Masunari N, Suzuki G (2004) Self-reported number of remaining teeth is associated with bone mineral density of the femoral neck, but not of the spine, in Japanese men and women. Osteoporos Int 15:842–846

    Article  PubMed  Google Scholar 

  24. Nicopoulou-Karayianni K, Tzoutzoukos P, Mitsea A, Karayiannis A, Tsiklakis K, Jacobs R, Lindh C, van der Stelt P, Allen P, Graham J, Horner K, Devlin H, Pavitt S, Yuan J (2009) Tooth loss and osteoporosis: the OSTEODENT Study. J Clin Periodontol 36:190–197

    Article  PubMed  Google Scholar 

  25. Iwasaki M, Nakamura K, Yoshihara A, Miyazaki H (2012) Change in bone mineral density and tooth loss in Japanese community-dwelling postmenopausal women: a 5-year cohort study. J Bone Miner Metab 30:447–453

    Article  PubMed  Google Scholar 

  26. Jang KM, Cho KH, Lee SH, Han SB, Han KD, Kim YH (2015) Tooth loss and bone mineral density in postmenopausal South Korean women: the 2008–2010 Korea National Health and Nutrition Examination Survey. Maturitas 82:360–364

    Article  PubMed  Google Scholar 

  27. Ji S, Tak YJ, Han DH, Kim YJ, Lee SY, Lee JG, Jeong DW, Kim MJ (2016) Low bone mineral density is associated with tooth loss in postmenopausal women: a nationwide representative study in Korea. J Womens Health (Larchmt) 25:1159–1165

    Article  Google Scholar 

  28. Savić Pavičin I, Dumančić J, Jukić T, Badel T (2017) The relationship between periodontal disease, tooth loss and decreased skeletal bone mineral density in ageing women. Gerodontology 34:441–445

    Article  PubMed  Google Scholar 

  29. Kawamura M, Masaki C, Shibata Y, Kondo Y, Mukaibo T, Miyazaki T, Hosokawa R (2019) Pentosidine correlates with nanomechanical properties of human jaw bone. J Mech Behav Biomed Mater 98:20–25

    Article  CAS  PubMed  Google Scholar 

  30. LaMonte MJ, Hovey KM, Genco RJ, Millen AE, Trevisan M, Wactawski-Wende J (2013) Five-year changes in periodontal disease measures among postmenopausal females: the Buffalo OsteoPerio study. J Periodontol 84:572–584

    Article  PubMed  Google Scholar 

  31. Mai X, Wactawski-Wende J, Hovey KM, LaMonte MJ, Chen C, Tezal M, Genco RJ (2013) Associations between smoking and tooth loss according to the reason for tooth loss: the Buffalo OsteoPerio Study. J Am Dent Assoc 144:252–265

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Grodstein F, Colditz GA, Stampfer MJ (1996) Post-menopausal hormone use and tooth loss: a prospective study. J Am Dent Assoc 127:370–377

    Article  CAS  PubMed  Google Scholar 

  33. Penoni DC, Leão ATT, Torres SR, Farias MLF, Fernandes TM, Crivelli M, Vettore MV (2018) Effects of bone fragility and antiresorptive drugs on periodontal disease and tooth loss: a longitudinal study. JDR Clin Trans Res 3:378–387

    CAS  PubMed  Google Scholar 

  34. Taguchi A, Shiraki M, Tanaka S, Ohshige H, Nakamura T (2019) Improved periodontal disease and prevention of tooth loss in osteoporosis patients receiving once-yearly zoledronic acid: a randomized clinical trial. Menopause 26:1277–1283

    Article  PubMed  Google Scholar 

  35. Shiraki M, Kuroda T, Tanaka S, Saito M, Fukunaga M, Nakamura T (2008) Nonenzymatic collagen cross-links induced by glycoxidation (pentosidine) predicts vertebral fractures. J Bone Miner Metab 26:93–100

    Article  CAS  PubMed  Google Scholar 

  36. Shiraki M, Kuroda T, Shiraki Y, Tanaka S, Higuchi T, Saito M (2011) Urinary pentosidine and plasma homocysteine levels at baseline predict future fractures in osteoporosis patients under bisphosphonate treatment. J Bone Miner Metab 29:62–70

    Article  CAS  PubMed  Google Scholar 

  37. Hefti AF, Preshaw PM (2012) Examiner alignment and assessment in clinical periodontal research. Periodontol 2000 59:41–60

    Article  PubMed  Google Scholar 

  38. Kato T, Fujiwara N, Ogawa T, Numabe Y (2021) Risk factors for tooth loss with a mean follow-up period of 139 years in supportive periodontal therapy patients. BMC Oral Health 21:202

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  39. Nascimento GG, Leite FR, Conceição DA, Ferrúa CP, Singh A, Demarco FF (2016) Is there a relationship between obesity and tooth loss and edentulism? A systematic review and meta-analysis. Obes Rev 17:587–598

    Article  CAS  PubMed  Google Scholar 

  40. Suzuki S, Noda T, Nishioka Y, Imamura T, Kamijo H, Sugihara N (2020) Evaluation of tooth loss among patients with diabetes mellitus using the National Database of Health Insurance Claims and Specific Health Checkups of Japan. Int Dent J 70:308–315

    Article  PubMed  PubMed Central  Google Scholar 

  41. Taguchi A, Sanada M, Suei Y, Ohtsuka M, Lee K, Tanimoto K, Tsuda M, Ohama K, Yoshizumi M, Higashi Y (2004) Tooth loss is associated with an increased risk of hypertension in postmenopausal women. Hypertension 43:1297–1300

    Article  CAS  PubMed  Google Scholar 

  42. Saito S, Ohi T, Murakami T, Komiyama T, Miyoshi Y, Endo K, Satoh M, Asayama K, Inoue R, Kikuya M, Metoki H, Imai Y, Ohkubo T, Hattori Y (2018) Association between tooth loss and cognitive impairment in community-dwelling older Japanese adults: a 4-year prospective cohort study from the Ohasama study. BMC Oral Health 18:142

    Article  PubMed  PubMed Central  Google Scholar 

  43. Nakahori N, Sekine M, Yamada M, Tatsuse T, Kido H, Suzuki M (2019) Socioeconomic status and remaining teeth in Japan: results from the Toyama dementia survey. BMC Public Health 19:691

    Article  PubMed  PubMed Central  Google Scholar 

  44. Ishikawa S, Konta T, Susa S, Kitabatake K, Ishizawa K, Togashi H, Tsuya A, Ueno Y, Kubota I, Yamashita H, Kayama T, Iino M (2019) Risk factors for tooth loss in community-dwelling Japanese aged 40 years and older: the Yamagata (Takahata) study. Clin Oral Investig 23:1753–1760

    Article  PubMed  Google Scholar 

  45. Ishikawa S, Konta T, Susa S, Edamatsu K, Ishizawa K, Togashi H, Nagase S, Ueno Y, Kubota I, Yamashita H, Kayama T, Iino M (2021) High parity is an independent risk factor for tooth loss in women: a community-based Takahata study in Japan. Tohoku J Exp Med 253:77–84

    Article  PubMed  Google Scholar 

  46. Taguchi A, Nagai K, Ideno Y, Kurabayashi T, Hayashi K (2020) Parity and number of teeth in Japanese women: results from the Japan Nurses’ Health Study. Womens Health Rep (New Rochelle) 15:366–374

    Google Scholar 

Download references

Acknowledgements

The Nagano Cohort Study was funded by the Budget of Research Institute and Practice for Involutional Diseases, Japan. We thank Analisa Avila, MPH, ELS, of Edanz (https://jp.edanz.com/ac) for editing a draft of this manuscript.

Author information

Authors and Affiliations

Authors

Contributions

Conception and design: AT, MS, and MS. Analysis and interpretation of the data: AT and MS. Drafting of the article: AT, MS, and MS. Critical revision of the article for important intellectual content: MS and MS. Final approval of the article: all the authors.

Corresponding author

Correspondence to Akira Taguchi.

Ethics declarations

Conflict of interest

A Taguchi, M Saito, and M Shiraki declare that they have no conflicts of interest.

Human and animal rights

All the procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki Declaration and its later amendments or comparable ethical standards. The study protocol of this investigation was approved by the ethics committee of the Research Institute and Practice for Involutional Diseases, Japan.

Informed consent

Informed consent was obtained from all the individual 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.

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Taguchi, A., Saito, M. & Shiraki, M. Association of pentosidine and homocysteine levels with number of teeth present in Japanese postmenopausal women. J Bone Miner Metab 40, 773–781 (2022). https://doi.org/10.1007/s00774-022-01343-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00774-022-01343-5

Keywords

Navigation