Skip to main content

Advertisement

Log in

Gingival bleeding as a predictor of handgrip strength—an observational study and a pilot randomized clinical trial

  • Research
  • Published:
Clinical Oral Investigations Aims and scope Submit manuscript

Abstract

Objective

The aim of this study was to (i) assess the association between self-reported periodontal disease and gingival bleeding as predictors of handgrip strength (HGS) in the elderly and (ii) evaluate the impact of baseline periodontal clinical parameters on the improvement of HGS in trained or non-trained treated periodontitis patients.

Methods

For (i), cross-sectional data from the Brazilian Longitudinal Study of Aging were retrieved and association between HGS (dependent variable) and self-reported gingival bleeding, periodontal disease, and missing teeth was analyzed using multiple linear regressions. For (ii), a pilot study was conducted with 17 patients randomly allocated to two groups—physical training or non-training—and followed for 45 days after subgingival instrumentation. Clinical parameters and HGS were recorded before and after treatment.

Results

The observational study showed a significant association between HGS and tooth loss, edentulism and gingival bleeding. The clinical trial showed that baseline bleeding on probing, but not other parameters, was associated with delta HGS.

Conclusion

Taken together, our findings suggest that gingival bleeding could act as a predictor of handgrip strength and its improvement after non-surgical periodontal therapy.

Clinical relevance

Gingival bleeding, either as self-perceived or clinically detected, may impact handgrip strength, an important marker of muscle frailty and mortality.

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.

Fig. 1

Similar content being viewed by others

References

  1. Papapanou PN, Sanz M, Buduneli N, Dietrich T, Feres M, Fine DH et al (2018) Periodontitis: consensus report of workgroup 2 of the 2017 World Workshop on the Classification of Periodontal and Peri-Implant Diseases and Conditions. J Periodontol 89(Suppl 1):S173–S182. https://doi.org/10.1002/JPER.17-0721

    Article  PubMed  Google Scholar 

  2. Kany S, Vollrath JT, Relja B (2019) Cytokines in inflammatory disease. Int J Mol Sci 20(23):6008. https://doi.org/10.3390/ijms20236008

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Franceschi C, Bonafè M, Valensin S, Olivieri F, De Luca M, Ottaviani E et al (2000) Inflamm-aging. An evolutionary perspective on immunosenescence. Ann N Y Acad Sci 908:244–54. https://doi.org/10.1111/j.1749-6632.2000.tb06651.x

    Article  CAS  PubMed  ADS  Google Scholar 

  4. de Pablo P, Chapple IL, Buckley CD, Dietrich T (2009) Periodontitis in systemic rheumatic diseases. Nat Rev Rheumatol 5(4):218–224. https://doi.org/10.1038/nrrheum.2009.28

    Article  PubMed  Google Scholar 

  5. An HR, Choi JS (2022) Association between handgrip strength and periodontitis in Korean adults aged ≥30 years: data from the Korea National Health and Nutrition Examination Survey (2014–2015). Int J Environ Res Public Health 19(17):10598. https://doi.org/10.3390/ijerph191710598

    Article  PubMed  PubMed Central  Google Scholar 

  6. Mihara Y, Matsuda KI, Ikebe K, Hatta K, Fukutake M, Enoki K et al (2018) Association of handgrip strength with various oral functions in 82- to 84-year-old community-dwelling Japanese. Gerodontology. https://doi.org/10.1111/ger.12341

    Article  PubMed  Google Scholar 

  7. Wu D, Gao X, Shi Y, Wang H, Wang W, Li Y et al (2022) Association between handgrip strength and the systemic immune-inflammation index: a nationwide study, NHANES 2011–2014. Int J Environ Res Public Health 19(20):13616. https://doi.org/10.3390/ijerph192013616

    Article  PubMed  PubMed Central  Google Scholar 

  8. Norman K, Stobäus N, Kulka K, Schulzke J (2014) Effect of inflammation on handgrip strength in the non-critically ill is independent from age, gender and body composition. Eur J Clin Nutr 68(2):155–158. https://doi.org/10.1038/ejcn.2013.261

    Article  CAS  PubMed  Google Scholar 

  9. Soysal P, Hurst C, Demurtas J, Firth J, Howden R, Yang L et al (2021) Handgrip strength and health outcomes: umbrella review of systematic reviews with meta-analyses of observational studies. J Sport Health Sci 10(3):290–295. https://doi.org/10.1016/j.jshs.2020.06.009

    Article  PubMed  Google Scholar 

  10. Yun J, Lee Y (2020) Association between oral health status and handgrip strength in older Korean adults. Eur Geriatr Med 11(3):459–464. https://doi.org/10.1007/s41999-020-00318-x

    Article  PubMed  Google Scholar 

  11. Sadjapong U, Yodkeeree S, Sungkarat S, Siviroj P. Multicomponent exercise program reduces frailty and inflammatory biomarkers and improves physical performance in community-dwelling older adults: a randomized controlled trial. Int J Environ Res Public Health. 2020;17(11). https://doi.org/10.3390/ijerph17113760

  12. Okamoto T, Hashimoto Y, Kobayashi R (2020) Isometric handgrip training reduces blood pressure and wave reflections in East Asian, non-medicated, middle-aged and older adults: a randomized control trial. Aging Clin Exp Res 32(8):1485–1491. https://doi.org/10.1007/s40520-019-01330-3

    Article  PubMed  Google Scholar 

  13. Herrod PJJ, Lund JN, Phillips BE (2021) Time-efficient physical activity interventions to reduce blood pressure in older adults: a randomised controlled trial. Age Ageing 50(3):980–984. https://doi.org/10.1093/ageing/afaa211

    Article  PubMed  Google Scholar 

  14. Zhuo C, Zhao J, Wang Q, Lin Z, Cai H, Pan H et al (2022) Assessment of causal associations between handgrip strength and cardiovascular diseases: a two sample mendelian randomization study. Front Cardiovasc Med 9:930077. https://doi.org/10.3389/fcvm.2022.930077

    Article  PubMed  PubMed Central  Google Scholar 

  15. Lima-Costa MF, de Andrade FB, Souza PR, Neri AL, Duarte YA, Castro-Costa E et al (2018) The Brazilian longitudinal study of aging (ELSI-Brazil): objectives and design. Am J Epidemiol 187(7):1345–53. https://doi.org/10.1093/aje/kwx387

    Article  PubMed  PubMed Central  Google Scholar 

  16. von Elm E, Altman DG, Egger M, Pocock SJ, Gøtzsche PC, Vandenbroucke JP (2008) The Strengthening the Reporting of Observational Studies in Epidemiology (STROBE) statement: guidelines for reporting observational studies. J Clin Epidemiol 61(4):344–349. https://doi.org/10.1016/j.jclinepi.2007.11.008

    Article  Google Scholar 

  17. Application of logistic regression with different sampling models. Applied Logistic Regression2000;203–22. https://doi.org/10.1002/0471722146.ch6

  18. Schulz KF, Altman DG, Moher D (2010) CONSORT 2010 statement: updated guidelines for reporting parallel group randomised trials. PLoS Med 7(3):e1000251. https://doi.org/10.1371/journal.pmed.1000251

    Article  PubMed  PubMed Central  Google Scholar 

  19. Klika B, Jordan C (2013) High-intensity circuit training using body weight: maximum results with minimal investment. ACSMs Health Fit J 17(3):8–13. https://doi.org/10.1249/FIT.0b013e31828cb1e8

    Article  Google Scholar 

  20. Schmidt D, Anderson K, Graff M, Strutz V (2016) The effect of high-intensity circuit training on physical fitness. J Sports Med Phys Fitness 56(5):534–540

    PubMed  Google Scholar 

  21. Zhou Z, Gu Y, Zhang Q, Liu L, Wu H, Meng G et al (2020) Association between tooth loss and handgrip strength in a general adult population. PLoS ONE 15(7):e0236010. https://doi.org/10.1371/journal.pone.0236010

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Hämäläinen P, Rantanen T, Keskinen M, Meurman JH (2004) Oral health status and change in handgrip strength over a 5-year period in 80-year-old people. Gerodontology 21(3):155–160. https://doi.org/10.1111/j.1741-2358.2004.00022.x

    Article  PubMed  Google Scholar 

  23. Lee JH, Lee SY, Han K, Han JS (2020) Relationship between oral health behaviour and handgrip strength: a cross-sectional study with 7589 Korean adults. Acta Odontol Scand 78(6):438–444. https://doi.org/10.1080/00016357.2020.1735516

    Article  PubMed  Google Scholar 

  24. Kim JE, Kim NY, Choi CH, Chung KH (2021) Association between oral health status and relative handgrip strength in 11,337 Korean. J Clin Med 10(22):5425. https://doi.org/10.3390/jcm10225425

    Article  PubMed  PubMed Central  Google Scholar 

  25. Eremenko M, Pink C, Biffar R, Schmidt CO, Ittermann T, Kocher T et al (2016) Cross-sectional association between physical strength, obesity, periodontitis and number of teeth in a general population. J Clin Periodontol 43(5):401–407. https://doi.org/10.1111/jcpe.12531

    Article  CAS  PubMed  Google Scholar 

  26. Aravindakshan V, Hakeem FF, Sabbah W (2020) Periodontal disease and grip strength among older adults. Geriatrics 5(3):46. https://doi.org/10.3390/geriatrics5030046

    Article  PubMed  PubMed Central  Google Scholar 

  27. Kang MG, Jung HW (2022) Association between oral health and frailty in older Korean population: a cross-sectional study. Clin Interv Aging 17:1863–1872. https://doi.org/10.2147/CIA.S384417

    Article  PubMed  PubMed Central  Google Scholar 

  28. Solemdal K, Sandvik L, Møinichen-Berstad C, Skog K, Willumsen T, Mowe M (2012) Association between oral health and body cell mass in hospitalised elderly. Gerodontology 29(2):e1038–e1044. https://doi.org/10.1111/j.1741-2358.2011.00607.x

    Article  PubMed  Google Scholar 

  29. Bunte K, Wiessner C, Bahat G, Erdogan T, Cruz-Jentoft AJ, Zapf A (2023) Association of periodontitis with handgrip strength and skeletal muscle mass in middle-aged US adults from NHANES 2013–2014. Aging Clin Exp Res 35(9):1909–1916. https://doi.org/10.1007/s40520-023-02471-2

    Article  PubMed  PubMed Central  Google Scholar 

  30. Eberhard J, Grote K, Luchtefeld M, Heuer W, Schuett H, Divchev D et al (2013) Experimental gingivitis induces systemic inflammatory markers in young healthy individuals: a single-subject interventional study. PLoS ONE 8(2):e55265. https://doi.org/10.1371/journal.pone.0055265

    Article  CAS  PubMed  PubMed Central  ADS  Google Scholar 

  31. Tuttle CSL, Thang LAN, Maier AB (2020) Markers of inflammation and their association with muscle strength and mass: a systematic review and meta-analysis. Ageing Res Rev 64:101185. https://doi.org/10.1016/j.arr.2020.101185

    Article  CAS  PubMed  Google Scholar 

  32. Li X, Moody MR, Engel D, Walker S, Clubb FJ Jr, Sivasubramanian N et al (2000) Cardiac-specific overexpression of tumor necrosis factor-alpha causes oxidative stress and contractile dysfunction in mouse diaphragm. Circulation 102(14):1690–1696. https://doi.org/10.1161/01.cir.102.14.1690

    Article  CAS  PubMed  Google Scholar 

  33. Belizário JE, Fontes-Oliveira CC, Borges JP, Kashiabara JA, Vannier E (2016) Skeletal muscle wasting and renewal: a pivotal role of myokine IL-6. Springerplus 5:619. https://doi.org/10.1186/s40064-016-2197-2

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Haddad F, Zaldivar F, Cooper DM, Adams GR (2005) IL-6-induced skeletal muscle atrophy. J Appl Physiol 98(3):911–7. https://doi.org/10.1152/japplphysiol.01026.2004

    Article  CAS  PubMed  Google Scholar 

  35. Shah SA, Safian N, Mohammad Z, Nurumal SR, Wan Ibadullah WAH, Mansor J et al (2022) Factors associated with handgrip strength among older adults in Malaysia. J Multidiscip Healthc 15:1023–1034. https://doi.org/10.2147/JMDH.S363421

    Article  PubMed  PubMed Central  Google Scholar 

  36. Martins R, Loureiro N (2023) The effects of low-volume combined training on health-related physical fitness outcomes in active young adults: a controlled clinical trial. Sports Med Health Sci 5(1):74–80. https://doi.org/10.1016/j.smhs.2022.12.004

    Article  PubMed  PubMed Central  Google Scholar 

  37. Pan PJ, Hsu NW, Lee MJ, Lin YY, Tsai CC, Lin WS (2022) Physical fitness and its correlation with handgrip strength in active community-dwelling older adults. Sci Rep 12(1):17227. https://doi.org/10.1038/s41598-022-21736-w

    Article  CAS  PubMed  PubMed Central  ADS  Google Scholar 

  38. Rojer AGM, Reijnierse EM, Trappenburg MC, van Lummel RC, Niessen M, van Schooten KS et al (2018) Instrumented assessment of physical activity is associated with muscle function but not with muscle mass in a general population. J Aging Health 30(9):1462–1481. https://doi.org/10.1177/0898264317721554

    Article  PubMed  Google Scholar 

  39. Lera L, Albala C, Leyton B, Márquez C, Angel B, Saguez R et al (2018) Reference values of hand-grip dynamometry and the relationship between low strength and mortality in older Chileans. Clin Interv Aging 13:317–324. https://doi.org/10.2147/CIA.S152946

    Article  PubMed  PubMed Central  Google Scholar 

  40. Concha-Cisternas Y, Petermann-Rocha F, Castro-Piñero J, Parra S, Albala C, Wyngard VV et al (2022) Handgrip strength as a predictor of adverse health outcomes. Rev Med Chil 150(8):1075–1086. https://doi.org/10.4067/S0034-98872022000801075

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

The authors would like to thank Dr. Tacito Pessoa de Souza Junior's team, from the Department of Physical Education of UFPR,for their assistance in preparing the training protocol.

Funding

The Paraná State Research Foundation (Fundação Araucária, Curitiba, PR, Brazil) and the National Council for Research and Technological Development (CNPq, Brasília, DF, Brazil) partially funded this study (No. 70/2021).

Author information

Authors and Affiliations

Authors

Contributions

All authors have made substantial contributions to the conception and design of the study. JR was involved in data interpretation and drafting the manuscript. GG, RF, and HM were involved in data collection and data analysis of the pilot study. AH and RP were involved in the observational study data collection and analysis. JS guided the entire work. All authors agreed on the final version of the manuscript.

Corresponding author

Correspondence to Joao Paulo Steffens.

Ethics declarations

Competing interests

The authors declare no competing interests.

Ethical approval

This study was approved by the Institutional Ethics Committee under No. 02621018.4.0000.0102.

Informed consent

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

Conflict of interest

The authors declare no competing interests.

Additional information

Publisher's Note

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

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Roth, J.V.S., Guarenghi, G.G., Ferro, R.M. et al. Gingival bleeding as a predictor of handgrip strength—an observational study and a pilot randomized clinical trial. Clin Oral Invest 28, 109 (2024). https://doi.org/10.1007/s00784-024-05507-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s00784-024-05507-7

Keywords

Navigation