Skip to main content

Advertisement

SpringerLink
Log in

Periodontal disease and risk of mortality and kidney function decline in advanced chronic kidney disease: a nationwide population-based cohort study

  • Original Article
  • Published:
Clinical Oral Investigations Aims and scope Submit manuscript

Abstract

Objectives

Periodontal disease is prevalent in patients with chronic kidney disease (CKD) and potentially associated with kidney function decline. However, it is uncertain whether periodontal disease affects the risk of mortality and morbidity in patients with advanced CKD.

Materials and methods

Taiwan’s National Health Insurance Research Database was used to conduct a nationwide population-based cohort study. Propensity score matching procedures were performed to select people with stage 5 CKD and to compare the long-term risk of mortality, end-stage renal disease, and major adverse cardiovascular events (MACE) between people with and without periodontal disease. Multivariable Cox regression analyses were conducted to calculate the adjusted hazard ratio (aHR) with 95% confidence interval (CI) for the outcome of interest.

Results

A total of 8119 subjects with stage 5 CKD were initially included. After matching to demographic and clinical covariates, 1254 subjects with 7099 person-years of follow-up were selected for analyses. Periodontal disease was not associated with long-term risks of all-cause mortality (aHR: 0.77, 95% CI: 0.49–1.22), progression to end-stage renal disease (aHR: 0.91, 95% CI: 0.75–1.10), or MACE (aHR: 1.18, 95% CI: 0.91–1.53). These findings were generally consistent across subgroups of age, sex, comorbid diabetes, uses of systemic antibiotic, and different dental procedures.

Conclusions

Periodontal disease is not a predictor for long-term mortality or morbidity in patients with advanced CKD.

Clinical relevance

These results provide important evidence to elucidate the relationship between periodontitis and critical clinical outcomes of advanced CKD.

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

Similar content being viewed by others

References

  1. GBD 2017 Disease and Injury Incidence and Prevalence Collaborators (2018) Global, regional, and national incidence, prevalence, and years lived with disability for 354 diseases and injuries for 195 countries and territories, 1990-2017: a systematic analysis for the global burden of disease study 2017. Lancet 392:1789–1858. https://doi.org/10.1016/S0140-6736(18)32279-7

    Article  Google Scholar 

  2. O’Sullivan ED, Hughes J, Ferenbach DA (2017) Renal aging: causes and consequences. J Am Soc Nephrol 28:407–420. https://doi.org/10.1681/ASN.2015121308

    Article  PubMed  Google Scholar 

  3. Go AS, Chertow GM, Fan D, McCulloch CE, Hsu CY (2004) Chronic kidney disease and the risks of death, cardiovascular events, and hospitalization. N Engl J Med 351:1296–1305. https://doi.org/10.1056/NEJMoa041031

    Article  PubMed  Google Scholar 

  4. Hung SC, Chang YK, Liu JS, Kuo KL, Chen YH, Hsu CC, Tarng DC (2015) Metformin use and mortality in patients with advanced chronic kidney disease: national, retrospective, observational, cohort study. Lancet Diabetes Endocrinol 3:605–614. https://doi.org/10.1016/S2213-8587(15)00123-0

    Article  PubMed  Google Scholar 

  5. Cody JD, Hodson EM (2016) Recombinant human erythropoietin versus placebo or no treatment for the anaemia of chronic kidney disease in people not requiring dialysis. Cochrane Database Syst Rev 2016:CD003266. https://doi.org/10.1002/14651858.CD003266.pub3

    Article  PubMed Central  Google Scholar 

  6. Campbell KL, Ash S, Bauer JD (2008) The impact of nutrition intervention on quality of life in pre-dialysis chronic kidney disease patients. Clin Nutr 27:537–544. https://doi.org/10.1016/j.clnu.2008.05.002

    Article  PubMed  Google Scholar 

  7. Palmer SC, Ruospo M, Wong G, Craig JC, Petruzzi M, De Benedittis M, Ford P, Johnson DW, Tonelli M, Natale P, Saglimbene V, Pellegrini F, Celia E, Gelfman R, Leal MR, Torok M, Stroumza P, Frantzen L, Bednarek-Skublewska A, Dulawa J, Del Castillo D, Bernat AG, Hegbrant J, Wollheim C, Schon S, Gargano L, Bots CP, Strippoli GF, ORALD Investigators (2016) Patterns of oral disease in adults with chronic kidney disease treated with hemodialysis. Nephrol Dial Transplant 31:1647–1653. https://doi.org/10.1093/ndt/gfv413

    Article  PubMed  Google Scholar 

  8. Borawski J, Wilczyńska-Borawska M, Stokowska W, Myśliwiec M (2007) The periodontal status of pre-dialysis chronic kidney disease and maintenance dialysis patients. Nephrol Dial Transplant 22:457–464. https://doi.org/10.1093/ndt/gfl676

    Article  PubMed  Google Scholar 

  9. Ioannidou E, Swede H, Dongari-Bagtzoglou A (2011) Periodontitis predicts elevated C-reactive protein levels in chronic kidney disease. J Dent Res 90:1411–1415. https://doi.org/10.1177/0022034511423394

    Article  PubMed  PubMed Central  Google Scholar 

  10. Yoshihara A, Iwasaki M, Miyazaki H, Nakamura K (2016) Bidirectional relationship between renal function and periodontal disease in older Japanese women. J Clin Periodontol 43:720–726. https://doi.org/10.1111/jcpe.12576

    Article  PubMed  Google Scholar 

  11. Ioannidou E, Hall Y, Swede H, Himmelfarb J (2013) Periodontitis associated with chronic kidney disease among Mexican Americans. J Public Health Dent 73:112–119. https://doi.org/10.1111/j.1752-7325.2012.00350.x

    Article  PubMed  Google Scholar 

  12. Chen YT, Shih CJ, Ou SM, Hung SC, Lin CH, Tarng DC, Taiwan Geriatric Kidney Disease (TGKD) Research Group (2015) Periodontal disease and risks of kidney function decline and mortality in older people: a community-based cohort study. Am J Kidney Dis 66:223–230. https://doi.org/10.1053/j.ajkd.2015.01.010

    Article  PubMed  Google Scholar 

  13. Grubbs V, Vittinghoff E, Taylor G, Kritz-Silverstein D, Powe N, Bibbins-Domingo K, Ishani A, Cummings SR, Osteoporotic Fractures in Men (MrOS) Study Research Group (2016) The association of periodontal disease with kidney function decline: a longitudinal retrospective analysis of the MrOS dental study. Nephrol Dial Transplant 31:466–472. https://doi.org/10.1093/ndt/gfv312

    Article  PubMed  Google Scholar 

  14. Ausavarungnirun R, Wisetsin S, Rongkiettechakorn N, Chaichalermsak S, Udompol U, Rattanasompattikul M (2016) Association of dental and periodontal disease with chronic kidney disease in patients of a single, tertiary care centre in Thailand. BMJ Open 6:e011836. https://doi.org/10.1136/bmjopen-2016-011836

    Article  PubMed  PubMed Central  Google Scholar 

  15. Chang JF, Yeh JC, Chiu YL, Liou JC, Hsiung JR, Tung TH (2017) Periodontal pocket depth, hyperglycemia, and progression of chronic kidney disease: a population-based longitudinal study. Am J Med 130:61–69. https://doi.org/10.1016/j.amjmed.2016.08.024

    Article  PubMed  Google Scholar 

  16. Yoshihara A, Sugita N, Iwasaki M, Wang Y, Miyazaki H, Yoshie H, Nakamura K (2017) Relationship between renal function and periodontal disease in community-dwelling elderly women with different genotypes. J Clin Periodontol 44:484–489. https://doi.org/10.1111/jcpe.12708

    Article  PubMed  Google Scholar 

  17. Lertpimonchai A, Rattanasiri S, Tamsailom S, Champaiboon C, Ingsathit A, Kitiyakara C, Limpianunchai A, Attia J, Sritara P, Thakkinstian A (2019) Periodontitis as the risk factor of chronic kidney disease: mediation analysis. J Clin Periodontol 46:631–639. https://doi.org/10.1111/jcpe.13114

    Article  PubMed  PubMed Central  Google Scholar 

  18. Sanz M, Marco Del Castillo A, Jepsen S, Gonzalez-Juanatey JR, D’Aiuto F, Bouchard P, Chapple I, Dietrich T, Gotsman I, Graziani F, Herrera D, Loos B, Madianos P, Michel JB, Perel P, Pieske B, Shapira L, Shechter M, Tonetti M, Vlachopoulos C, Wimmer G (2020) Periodontitis and cardiovascular diseases: Consensus report. J Clin Periodontol 47:268–288. https://doi.org/10.1111/jcpe.13189

    Article  PubMed  PubMed Central  Google Scholar 

  19. Palmer SC, Ruospo M, Wong G, Craig JC, Petruzzi M, De Benedittis M, Ford P, Johnson DW, Tonelli M, Natale P, Saglimbene V, Pellegrini F, Celia E, Gelfman R, Leal MR, Torok M, Stroumza P, Bednarek-Skublewska A, Dulawa J, Frantzen L, Ferrari JN, Del Castillo D, Bernat AG, Hegbrant J, Wollheim C, Gargano L, Bots CP, Strippoli GF, ORAL-D Study Investigators (2015) Dental health and mortality in people with end-stage kidney disease treated with hemodialysis: a multinational cohort study. Am J Kidney Dis 66:666–676. https://doi.org/10.1053/j.ajkd.2015.04.051

    Article  PubMed  Google Scholar 

  20. Sharma P, Dietrich T, Ferro CJ, Cockwell P, Chapple IL (2016) Association between periodontitis and mortality in stages 3-5 chronic kidney disease: NHANES III and linked mortality study. J Clin Periodontol 43:104–113. https://doi.org/10.1111/jcpe.12502

    Article  PubMed  PubMed Central  Google Scholar 

  21. Dai YX, Tai YH, Chen CC, Chang YT, Chen TJ, Chen MH (2020) Bidirectional association between alopecia areata and major depressive disorder among probands and unaffected siblings: a nationwide population-based study. J Am Acad Dermatol 82:1131–1137. https://doi.org/10.1016/j.jaad.2019.11.064

    Article  PubMed  Google Scholar 

  22. Dai YX, Tai YH, Chang YT, Chen TJ, Chen MH (2020) Association between major depressive disorder and subsequent autoimmune skin diseases: a nationwide population-based cohort study. J Affect Disord 274:334–338. https://doi.org/10.1016/j.jad.2020.05.070

    Article  PubMed  Google Scholar 

  23. Tai YH, Chang CC, Yeh CC, Sung LC, Hu CJ, Cherng YG, Chen TL, Liao CC (2020) Long-term risk of stroke and poststroke outcomes in patients with heart failure: two nationwide studies. Clin Epidemiol 12:1235–1244. https://doi.org/10.2147/CLEP.S261179

    Article  PubMed  PubMed Central  Google Scholar 

  24. Wu YM, Kuo HC, Li CC, Wu HL, Chen JT, Cherng YG, Chen TJ, Dai YX, Liu HY, Tai YH (2020) Preexisting dementia is associated with increased risks of mortality and morbidity following major surgery: a nationwide propensity score matching study. Int J Environ Res Public Health 17:8431. https://doi.org/10.3390/ijerph17228431

    Article  PubMed Central  Google Scholar 

  25. National Health Insurance Research Database. Data subsets. Available from: https://nhird.nhri.org.tw/en/Data_Subsets.html. Accessed January 6, 2021.

  26. Lee CY, Chang CC, Lin CS, Yeh CC, Hu CJ, Wu CZ, Chen TL, Liao CC (2020) Risk of dementia in patients with periodontitis and related protective factors: a nationwide retrospective cohort study. J Clin Periodontol 47:1428–1436. https://doi.org/10.1111/jcpe.13372

    Article  PubMed  Google Scholar 

  27. Lin HW, Chen CM, Yeh YC, Chen YY, Guo RY, Lin YP, Li YC (2019) Dental treatment procedures for periodontal disease and the subsequent risk of ischaemic stroke: a retrospective population-based cohort study. J Clin Periodontol 46:642–649. https://doi.org/10.1111/jcpe.13113

    Article  PubMed  Google Scholar 

  28. Lee YL, Hu HY, Chou P, Chu D (2015) Dental prophylaxis decreases the risk of acute myocardial infarction: a nationwide population-based study in Taiwan. Clin Interv Aging 10:175–182. https://doi.org/10.2147/CIA.S67854

    Article  PubMed  PubMed Central  Google Scholar 

  29. Chan CL, You HJ, Lian HJ, Huang CH (2016) Patients receiving comprehensive periodontal treatment have better clinical outcomes than patients receiving conventional periodontal treatment. J Formos Med Assoc 115:152–162. https://doi.org/10.1016/j.jfma.2015.10.017

    Article  PubMed  Google Scholar 

  30. Lockhart PB, Tampi MP, Abt E, Aminoshariae A, Durkin MJ, Fouad AF, Gopal P, Hatten BW, Kennedy E, Lang MS, Patton LL, Paumier T, Suda KJ, Pilcher L, Urquhart O, O’Brien KK, Carrasco-Labra A (2019) Evidence-based clinical practice guideline on antibiotic use for the urgent management of pulpal- and periapical-related dental pain and intraoral swelling: a report from the American Dental Association. J Am Dent Assoc 150:906–921. https://doi.org/10.1016/j.adaj.2019.08.020

    Article  PubMed  PubMed Central  Google Scholar 

  31. Schoenfeld DA (1983) Sample-size formula for the proportional-hazards regression model. Biometrics 39:499–503

    Article  PubMed  Google Scholar 

  32. Austin PC (2011) An introduction to propensity score methods for reducing the effects of confounding in observational studies. Multivar Behav Res 46:399–424. https://doi.org/10.1080/00273171.2011.568786

    Article  Google Scholar 

  33. Austin PC (2009) Balance diagnostics for comparing the distribution of baseline covariates between treatment groups in propensity-score matched samples. Stat Med 28:3083–3107. https://doi.org/10.1002/sim.3697

    Article  PubMed  PubMed Central  Google Scholar 

  34. Wangerin C, Pink C, Endlich K, Rettig R, Stracke S, Nauck M, Völzke H, Kocher T, Holtfreter B (2019) Long-term association of periodontitis with decreased kidney function. Am J Kidney Dis 73:513–524. https://doi.org/10.1053/j.ajkd.2018.10.013

    Article  PubMed  Google Scholar 

  35. Reichel H, Zee J, Tu C, Young E, Pisoni RL, Stengel B, Duttlinger J, Lonnemann G, Robinson BM, Pecoits-Filho R, Fliser D (2020) Chronic kidney disease progression and mortality risk profiles in Germany: results from the Chronic Kidney Disease Outcomes and Practice Patterns Study. Nephrol Dial Transplant 35:803–810. https://doi.org/10.1093/ndt/gfz260

    Article  PubMed  PubMed Central  Google Scholar 

  36. Lin CM, Yang MC, Hwang SJ, Sung JM (2013) Progression of stages 3b-5 chronic kidney disease--preliminary results of Taiwan national pre-ESRD disease management program in Southern Taiwan. J Formos Med Assoc 112:773–782. https://doi.org/10.1016/j.jfma.2013.10.021

    Article  PubMed  Google Scholar 

  37. Fang F, Wu B, Qu Q, Gao J, Yan W, Huang X, Ma D, Yue J, Chen T, Liu F, Liu Y (2015) The clinical response and systemic effects of non-surgical periodontal therapy in end-stage renal disease patients: a 6-month randomized controlled clinical trial. J Clin Periodontol 42:537–546. https://doi.org/10.1111/jcpe.12411

    Article  PubMed  Google Scholar 

  38. Wehmeyer MM, Kshirsagar AV, Barros SP, Beck JD, Moss KL, Preisser JS, Offenbacher S (2013) A randomized controlled trial of intensive periodontal therapy on metabolic and inflammatory markers in patients with ESRD: results of an exploratory study. Am J Kidney Dis 61:450–458. https://doi.org/10.1053/j.ajkd.2012.10.021

    Article  PubMed  Google Scholar 

  39. Graziani F, Cei S, La Ferla F, Vano M, Gabriele M, Tonetti M (2010) Effects of non-surgical periodontal therapy on the glomerular filtration rate of the kidney: an exploratory trial. J Clin Periodontol 37:638–643. https://doi.org/10.1111/j.1600-051X.2010.01578.x

    Article  PubMed  Google Scholar 

  40. Holmlund A, Holm G, Lind L (2006) Severity of periodontal disease and number of remaining teeth are related to the prevalence of myocardial infarction and hypertension in a study based on 4,254 subjects. J Periodontol 77:1173–1178. https://doi.org/10.1902/jop.2006.050233

    Article  PubMed  Google Scholar 

  41. Naorungroj S, Slade GD, Divaris K, Heiss G, Offenbacher S, Beck JD (2017) Racial differences in periodontal disease and 10-year self-reported tooth loss among late middle-aged and older adults: the dental ARIC study. J Public Health Dent 77:372–382. https://doi.org/10.1111/jphd.12226

    Article  PubMed  PubMed Central  Google Scholar 

  42. Ekart R, Ferjuc A, Furman B, Gerjevič Š, Bevc S, Hojs R (2013) Chronic kidney disease progression to end stage renal disease: a single center experience of the role of the underlying kidney disease. Ther Apher Dial 17:363–367. https://doi.org/10.1111/1744-9987.12079

    Article  PubMed  Google Scholar 

Download references

Funding

This work was supported by the grants from Shuang Ho Hospital (109IIT-02), Taipei Medical University, New Taipei City, Taiwan, and Ministry of Science and Technology (MOST109-2314-B-038-024), Taipei, Taiwan.

Author information

Authors and Affiliations

  1. Department of Anesthesiology, Shuang Ho Hospital, Taipei Medical University, No. 291, Zhongzheng Rd., Zhonghe District, New Taipei City, 23561, Taiwan

    Ying-Hsuan Tai, Jui-Tai Chen, Hsien-Cheng Kuo, Wan-Chi Liu & Yih-Giun Cherng

  2. Department of Anesthesiology, School of Medicine, College of Medicine, Taipei Medical University, Taipei, Taiwan

    Ying-Hsuan Tai, Jui-Tai Chen, Hsien-Cheng Kuo, Wan-Chi Liu & Yih-Giun Cherng

  3. Department of Dentistry, Shuang Ho Hospital, Taipei Medical University, New Taipei City, Taiwan

    Wei-Jen Chang

  4. School of Dentistry, College of Oral Medicine, Taipei Medical University, Taipei, Taiwan

    Wei-Jen Chang

  5. Division of Nephrology, Department of Internal Medicine, Shuang Ho Hospital, Taipei Medical University, New Taipei City, Taiwan

    Mei-Yi Wu

  6. Division of Nephrology, Department of Internal Medicine, Taipei Medical University, Taipei, Taiwan

    Mei-Yi Wu

  7. TMU Research Center of Urology and Kidney, Taipei Medical University, Taipei, Taiwan

    Mei-Yi Wu

  8. Department of Dermatology, Taipei Veterans General Hospital, Taipei, Taiwan

    Ying-Xiu Dai

  9. School of Medicine, National Yang Ming Chiao Tung University, Taipei, Taiwan

    Ying-Xiu Dai, Tzeng-Ji Chen & Hsiang-Ling Wu

  10. Department of Family Medicine, Taipei Veterans General Hospital, Taipei, Taiwan

    Tzeng-Ji Chen

  11. Department of Anesthesiology, Taipei Veterans General Hospital, Taipei, Taiwan

    Hsiang-Ling Wu

Authors
  1. Ying-Hsuan Tai
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jui-Tai Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Hsien-Cheng Kuo
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Wei-Jen Chang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Mei-Yi Wu
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Ying-Xiu Dai
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Wan-Chi Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Tzeng-Ji Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Hsiang-Ling Wu
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Yih-Giun Cherng
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Yih-Giun Cherng.

Ethics declarations

Ethics approval

This study was reviewed and approved by the Institutional Review Board of Taipei Medical University and Taipei Veterans General Hospital in Taiwan (TMU-JIRB-N202010040; IRB-TPEVGH-2013-04-005E).

Consent to participate

Written informed consent was waived by the Institutional Review Board (chair: Professor Chung-Ming Chen of Taipei Medical University and Professor Shung-Tai Ho of Taipei Veterans General Hospital).

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.

Supplementary information

ESM 1

(DOCX 41 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Tai, YH., Chen, JT., Kuo, HC. et al. Periodontal disease and risk of mortality and kidney function decline in advanced chronic kidney disease: a nationwide population-based cohort study. Clin Oral Invest 25, 6259–6268 (2021). https://doi.org/10.1007/s00784-021-03924-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00784-021-03924-6

Keywords

Search

Navigation