Skip to main content

Advertisement

Log in

Association between periodontitis and Alzheimer’s disease and its impact on the self-perceived oral health status: a case-control study

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

Abstract

Purpose

To test the hypothesis that periodontitis is associated with AD and search whether periodontal and other variables would negatively impact the oral health-related quality of life (OHRQoL) perception.

Materials and methods

Oral examinations and interview on self-perceived oral health status (Geriatric Oral Health Assessment Index (GOHAI) questionnaire (higher score corresponds to better perceived oral status)) were carried out and socio-demographic data were collected from outpatients with mild to moderate AD (cases, n = 50) and from their age- and sex-matched family caregivers (controls, n = 52). Full-mouth periodontal examination was performed. Significance of differences between groups was sought by chi-square, Student’s t, or the Mann-Whitney test. The association between the variables periodontitis, probing depth (PD) ≥ 5 mm, and clinical attachment loss (CAL) ≥ 5 mm with the variable group was tested in binary logistic regression models (LRMs). LRMs were used to test the association of oral findings, demographics, and group with GOHAI.

Results

Cases had fewer teeth and greater CAL than controls. Cases had a superior percentage of sites with plaque, calculus, and bleeding on probing than controls. Cases had greater GOHAI scores than controls. Periodontitis was a variable most likely associated with AD (OR = 11.08, p < 0.001). None of the oral findings or demographics, but group, was associated with GOHAI (OR = 14.45, p < 0.001).

Conclusion

Periodontitis is associated with AD, but not with patients’ OHRQoL.

Clinical relevance

Health care professionals must be aware that AD patients should have a periodic thorough oral examination and preventive intervention aiming at their welfare and maintenance of a pain-free functional dentition.

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. Patterson C (2018) World Alzheimer report 2018 - the state of the art of dementia research: new frontiers. Alzheimer’s Disease International, London, pp 1–48

    Google Scholar 

  2. Scheltens P, Blennow K, Breteler MMB, de Strooper B, Frisoni GB, Salloway S, Van der Flier WM (2016) Alzheimer’s disease. Lancet 388(10043):505–517

    PubMed  Google Scholar 

  3. Villemagne VL, Burnham S, Bourgeat P, Brown B, Ellis KA, Salvado O, Szoeke C, Macaulay SL, Martins R, Maruff P, Ames D, Rowe CC, Masters CL, Australian Imaging Biomarkers and Lifestyle (AIBL) Research Group (2013) Amyloid β deposition, neurodegeneration, and cognitive decline in sporadic Alzheimer’s disease: a prospective cohort study. Lancet Neurol 12(4):357–367

    PubMed  Google Scholar 

  4. Masters CL, Bateman R, Blennow K, Rowe CC, Sperling RA, Cummings JL (2015) Alzheimer’s disease. Nat Rev Dis Primers 1(15056):1–18

    Google Scholar 

  5. Voet S, Srinivasan S, Lamkanfi M, van Loo G (2019) Inflammasomes in neuroinflammatory and neurodegenerative diseases. EMBO Mol Med 11(6):e10248

    PubMed  PubMed Central  Google Scholar 

  6. Kinane DF, Stathopoulou PG, Papapanou PN (2017) Periodontal diseases. Nat Rev Dis Primers 3(17038):159–174

    Google Scholar 

  7. Eke PI, Wei L, Borgnakke WS, Thornton-Evans G, Zhang X, Lu H, McGuire LC, Genco RJ (2016) Periodontitis prevalence in adults ≥ 65 years of age, in the USA. Periodontol 2000 72(1):76–95

    PubMed  Google Scholar 

  8. Gross AJ, Paskett KT, Cheever VJ, Lipsky MS (2017) Periodontitis: a global disease and the primary care provider’s role. Postgrad Med J 93(1103):560–565

    PubMed  Google Scholar 

  9. Kamer AR, Craig RG, Dasanayake AP, Brys M, Glodzik-Sobanska L, de Leon MJ (2008) Inflammation and Alzheimer’s disease: possible role of periodontal diseases. Alzheimers Dement 4(4):242–250

    PubMed  Google Scholar 

  10. Noble JM, Scarmeas N, Celenti RS, Elkind MSV, Wright CB, Schupf N, Papapanou PN (2014) Serum IgG antibody levels to periodontal microbiota are associated with incident Alzheimer disease. PLoS ONE 9(12):1–14

    Google Scholar 

  11. Feres M, Teles F, Teles R, Figueiredo LC, Faveri M (2016) The subgingival periodontal microbiota of the aging mouth. Periodontol 2000 72(1):30–53

    PubMed  PubMed Central  Google Scholar 

  12. Dominy SS, Lynch C, Ermini F, Benedyk M, Marczyk A, Konradi A, Nguyen M, Haditsch U, Raha D, Griffin C, Holsinger LJ, Arastu-Kapur S, Kaba S, Lee A, Ryder MI, Potempa B, Mydel P, Hellvard A, Adamowicz K, Hasturk H, Walker GD, Reynolds EC, Faull RLM, Curtis MA, Dragunow M, Potempa J (2019) Porphyromonas gingivalis in Alzheimer’s disease brains: evidence for disease causation and treatment with small-molecule inhibitors. Sci Adv 5(1):eaau3333

    PubMed  PubMed Central  Google Scholar 

  13. Kamer AR, Craig RG, Niederman R, Fortea J, de Leon MJ (2020) Periodontal disease as a possible cause for Alzheimer’s disease. Periodontol 2000 83(1):242–271

    PubMed  Google Scholar 

  14. Miklossy J (2011) Emerging roles of pathogens in Alzheimer disease. Exp Rev Mol Med 13(e30):1–34

    Google Scholar 

  15. Stein PS, Steffen MJ, Smith C, Jicha G, Ebersole JL, Abner E, Dawson D 3rd (2012) Serum antibodies to periodontal pathogens are a risk factor for Alzheimer’s disease. Alzheimers Dement 8(3):196–203

    PubMed Central  Google Scholar 

  16. Singhrao SK, Harding A, Poole S, Kesavalu L, Crean SJ (2015) Porphyromonas gingivalis periodontal infection and its putative links with Alzheimer’s disease. Mediat Inflamm 2015(137357):1–10

    Google Scholar 

  17. Sochocka M, Sobczyński M, Sender-Janeczek A, Zwolińska K, Błachowicz O, Tomczyk T, Ziętek M, Leszek J (2017) Association between periodontal health status and cognitive abilities. The role of cytokine profile and systemic inflammation. Curr Alzheimer Res 14(9):978–990

    PubMed  PubMed Central  Google Scholar 

  18. Poole S, Singhrao SK, Kesavalu L, Curtis MA, Crean SJ (2013) Determining the presence of periodontopathic virulence factors in short-term postmortem Alzheimer’s disease brain tissue. J Alzheimers Dis 36(4):665–677

    PubMed  Google Scholar 

  19. Beydoun MA, Beydoun HA, Hossain S, El-Hajj ZW, Weiss J, Zonderman AB (2020) Clinical and bacterial markers of periodontitis and their association with incident all-cause and Alzheimer’s disease dementia in a large national survey. J Alzheimers Dis 75(1):157–172

    PubMed  Google Scholar 

  20. Laugisch O, Johnen A, Maldonado A, Ehmke B, Bürgin W, Olsen I, Potempa J, Sculean A, Duning T, Eick S (2018) Periodontal pathogens and associated intrathecal antibodies in early stages of Alzheimer’s disease. J Alzheimers Dis 66(1):105–114

    PubMed  Google Scholar 

  21. Gil-Montoya JA, Sanchez-Lara I, Carnero-Pardo C, Fornieles F, Montes J, Vilchez R, Burgos JS, Gonzalez-Moles MA, Barrios R, Bravo M (2015) Is periodontitis a risk factor for cognitive impairment and dementia? A case-control study. J Periodontol 86(2):244–253

    PubMed  Google Scholar 

  22. Ide M, Harris M, Stevens A, Sussams R, Hopkins V, Culliford D, Fuller J, Ibbett P, Raybould R, Thomas R, Puenter U, Teeling J, Perry VH, Holmes C (2016) Periodontitis and cognitive decline in Alzheimer’s disease. PLoS One 11(3):e0151081

    PubMed  PubMed Central  Google Scholar 

  23. Olsen I, Singhrao SK (2015) Can oral infection be a risk factor for Alzheimer’s disease? J Oral Microbiol 7(1):29143

    PubMed  Google Scholar 

  24. Pongan E, Tillmann B, Leveque Y, Trombert B, Getenet JC, Auguste N, Dauphinot V, El Haouari H, Navez M, Dorey J-M, Krolak-Salmon P, Auguste N, Bachelet R, Brunon L, Dayot J, Dorey J-M, El Haouari H, Fatisson M, Ferrer M, Gaillat C, Gentil C, Getenet JC, Goldet K, Krolak-Salmon P, Laurent B, Leroyer M, Leveque Y, Michon A, Mortreux A, Navez M, Neagu A, Perrot C, Pongan E, Rouch I, Solimeo M, Tillmann B, Touzet du Vigier A, Vulliez E, Laurent B, Rouch I (2017) Can musical or painting interventions improve chronic pain, mood, quality of life, and cognition in patients with mild Alzheimer’s disease? Evidence from a randomized controlled trial. J Alzheimers Dis 60(2):663–677

    PubMed  Google Scholar 

  25. Lima S, Garrett C, Machado JC, Vilaça M, Pereira MG (2019) Quality of life in patients with mild Alzheimer disease: the mediator role of mindfulness and spirituality. Aging Ment Health in press:1–8. https://doi.org/10.1080/13607863.2019.1650891

  26. Kishita N, Backhouse T, Mioshi E (2020) Nonpharmacological interventions to improve depression, anxiety, and quality of life (QoL) in people with dementia: an overview of systematic reviews. J Geriatr Psychiatry Neurol 33(1):28–41

    PubMed  Google Scholar 

  27. Campos JADB, Carrascosa AC, Zucoloto ML, Maroco J (2014) Validation of a measuring instrument for the perception of oral health in women. Braz Oral Res 28(1):1–7

    Google Scholar 

  28. Ming Y, Hsu S-W, Yen Y-Y, Lan S-J (2019) Association of oral health–related quality of life and Alzheimer disease: a systematic review. J Prosth Dent in press 124:168–175. https://doi.org/10.1016/j.prosdent.2019.08.015

    Article  Google Scholar 

  29. Lee KH, Wu B, Plassman BL (2013) Cognitive function and oral health-related quality of life in older adults. J Am Geriatr Soc 61(9):1602–1607

    PubMed  PubMed Central  Google Scholar 

  30. Papapanou PN, Sanz M, Buduneli N, Dietrich T, Feres M, Fine DH, Flemmig TF, Garcia R, Giannobile WV, Graziani F, Greenwell H, Herrera D, Kao RT, Kebschull M, Kinane DF, Kirkwood KL, Kocher T, Kornman KS, Kumar PS, Loos BG, Machtei E, Meng H, Mombelli A, Needleman I, Offenbacher S, Seymour GJ, Teles R, Tonetti MS (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

    PubMed  Google Scholar 

  31. Page RC, Eke PI (2007) Case definitions for use in population-based surveillance of periodontitis. J Periodontol 78(7s):1387–1399

    PubMed  Google Scholar 

  32. Atchison KA, Dolan TA (1990) Development of the geriatric oral health assessment index. J Dent Educ 54(11):680–687

    PubMed  Google Scholar 

  33. Aragón F, Zea-Sevilla MA, Montero J, Sancho P, Corral R, Tejedor C, Frades-Payo B, Paredes-Gallardo V, Albaladejo A (2018) Oral health in Alzheimer’s disease: a multicenter case-control study. Clin Oral Investig 22(9):3061–3070

    PubMed  Google Scholar 

  34. Holmer J, Eriksdotter M, Schultzberg M, Pirkko J, Pussinen PJ, Buhlin K (2018) Association between periodontitis and risk of Alzheimer’s disease, mild cognitive impairment and subjective cognitive decline: a case–control study. J Clin Periodontol 45(11):1287–1298

    PubMed  Google Scholar 

  35. Elsig F, Schimmel M, Duvernay E, Giannelli SV, Graf CE, Carlier S, Herrmann FR, Michel JP, Gold G, Zekry D, Müller F (2015) Tooth loss, chewing efficiency and cognitive impairment in geriatric patients. Gerodontology 32(2):149–156

    PubMed  Google Scholar 

  36. Hirano Y, Obata T, Kashikura K, Nonaka H, Tachibana A, Ikehira H, Onozuka M (2008) Effects of chewing in working memory processing. Neurosci Lett 436(2):189–192

    PubMed  Google Scholar 

  37. Kamer AR, Morse DE, Holm-Pedersen P, Mortensen EL, Avlund K (2012) Periodontal inflammation in relation to cognitive function in an older adult Danish population. J Alzheimers Dis 28(3):613–624

    PubMed  Google Scholar 

  38. Lee Y-T, Lee H-C, Hu C-J, Huang L-K, Chao S-P, Lin C-P, Su EC-Y, Lee Y-C, Chen C-C (2016) Periodontitis as a modifiable risk factor for dementia: a nationwide population based cohort study. J Am Geriatr Soc 65(2):301–305

    PubMed  Google Scholar 

  39. Nilsson H, Berglund SM, Renvert S (2019) Longitudinal evaluation of periodontitis and development of cognitive decline among older adults. J Clin Periodontol 46(10):1141–1149

    Google Scholar 

  40. Livingston G, Sommerlad A, Orgeta V, Costafreda SG, Huntley J, Ames D, Ballard C, Banerjee S, Burns A, Cohen-Mansfield J, Cooper C, Fox N, Gitlin LN, Howard R, Kales CK, Larson EB, Ritchie K, Rockwood K, Sampson EL, Samus Q, Lon S, Schneider LS, Selbæk G, Teri L, Mukadam N (2017) Dementia prevention, intervention, and care. Lancet 390(10113):2673–2734

    PubMed  Google Scholar 

  41. Oliveira D, Otuyama LJ, Mabunda D, Mandlate F, Gonçalves-Pereira M, Xavier M, Laks J, Ferri CP (2019) Reducing the number of people with dementia through primary prevention in Mozambique, Brazil, and Portugal: an analysis of population-based data. J Alzheimers Dis 70(s1):S283–S291

    PubMed  PubMed Central  Google Scholar 

  42. Ribeiro GR, Costa JLR, Ambrosano GMB, Garcia RCMR (2012) Oral health of the elderly with Alzheimer’s disease. Oral Surg Oral Med Oral Pathol Oral Radiol 114(3):338–343

    PubMed  Google Scholar 

  43. Campos CH, Ribeiro GR, Matheus RC, Garcia R (2016) Oral health-related quality of life in mild Alzheimer: patient versus caregiver perceptions. Spec Care Dentist 36(5):271–276

    PubMed  Google Scholar 

  44. Marín Zuluaga DJ, Gil Montoya JA, Contreras CI, Herrera RR (2012) Association between oral health, cognitive impairment and oral health–related quality of life. Gerontology 29(2):e667–e673

    Google Scholar 

  45. Thorgrimsen L, Selwood A, Spector A, Royan L, Madariaga Lopez M, Woods RT, Orrell M (2003) Whose quality of life is it anyway? The validity and reliability of the quality of life-Alzheimer’s disease (QoL-AD) scale. Alzheimer Dis Assoc Disord 17(4):201–208

    PubMed  Google Scholar 

  46. Cicciù M, Matacena G, Signorino F, Brugaletta A, Cicciù A, Bramanti E (2013) Relationship between oral health and its impact on the quality life of Alzheimer’s disease patients: a supportive care trial. Int J Clin Exp Med 6(9):766–772

    PubMed  PubMed Central  Google Scholar 

  47. Chen C-K, Wu Y-T, Chang Y-C (2017) Association between chronic periodontitis and the risk of Alzheimer’s disease: a retrospective, population-based, matched-cohort study. Alzheimers Res Ther 9(1):56

    PubMed  PubMed Central  Google Scholar 

  48. Teixeira FB, Saito MT, Matheus FC, Prediger RD, Yamada ES, Maia CSF, Lima RR (2017) Periodontitis and Alzheimer’s disease: a possible comorbidity between oral chronic inflammatory condition and neuroinflammation. Front Aging Neurosci 9:327. https://doi.org/10.3389/fnagi.2017.00327

    Article  PubMed  PubMed Central  Google Scholar 

  49. Fülöp T, Witkowski JM, Bourgade K, Khalil A, Zerif E, Larbi A, Hirokawa K, Pawelec G, Bocti C, Lacombe G, Dupuis G, Frost EH (2018) Can an infection hypothesis explain the beta amyloid hypothesis of Alzheimer’s disease? Front Aging Neurosci 10:224. https://doi.org/10.3389/fnagi.2018.00224

    Article  PubMed  PubMed Central  Google Scholar 

  50. Fülöp T, Itzhaki RF, Balin BJ, Miklossy J, Barron AE (2018) Role of microbes in the development of Alzheimer’s disease: state of the art - an international symposium presented at the 2017 IAGG Congress in San Francisco. Front Genet 9:362. https://doi.org/10.3389/fgene.2018.00362

    Article  PubMed  PubMed Central  Google Scholar 

  51. Schnaider L, Arnon Z, Gazit E (2020) Reevaluating the microbial infection link to Alzheimer’s disease. J Alzheimers Dis 73(1):59–62

    PubMed  Google Scholar 

  52. Eggink E, Moll van Charante EP, van Gool WA, Richard E (2019) A population perspective on prevention of dementia. J Clin Med 8(6):834

    PubMed Central  Google Scholar 

  53. Montgomery W, Goren A, Kahle-Wrobleski K, Nakamura T, Ueda K (2018) Alzheimer’s disease severity and its association with patient and caregiver quality of life in Japan: results of a community-based survey. BMC Geriatr 18(1):141

    PubMed  PubMed Central  Google Scholar 

  54. Cerhan JR, Fredericksen ZS, Wang AW, Habermann TM, Kay NE, Macon WR, Cunningham JM, Shanafelt TD, Ansell SM, Call TG, Witzig TE, Slager SL, Liebow M (2011) Design and validity of a clinic-based case-control study on the molecular epidemiology of lymphoma. Int J Mol Epidemiol Genet 2(2):95–113

    PubMed  PubMed Central  Google Scholar 

  55. Heßmann P, Seeberg G, Reese JP, Dams J, Baum E, Müller MJ, Dodel R, Balzer-Geldsetzer M (2016) Health-related quality of life in patients with Alzheimer’s disease in different German health care settings. J Alzheimers Dis 51(2):545–561

    PubMed  Google Scholar 

Download references

Acknowledgments

The authors wish to thank the IPUB UFRJ staff and, particularly, Dr. Valeska Marinho Rodrigues and Dr. Marcia Cristina Nascimento Dourado whose professionalism and willingness to collaborate have made this work possible.

Funding

This study was financially supported, in part, by the Coordination for the Improvement of Higher Education Personnel (CAPES), Ministry of Education, Brasilia, Brazil.

Author information

Authors and Affiliations

Authors

Contributions

All authors contributed to the study conception and design. Raquel de Oliveira Araújo and German Eduardo M. Villoria were involved in patient screening and data collection. Ronir Raggio Luiz, Anna Thereza Thomé Leão, and Raquel de Oliveira Araújo performed the statistical analysis. Eduardo Jorge Feres Filho and Anna Thereza Thomé Leão drafted the manuscript. All authors revised de manuscript and approved its final version.

Corresponding author

Correspondence to Eduardo Jorge Feres-Filho.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

The study protocol was approved by the Ethics Committees of Clementino Fraga Filho University Hospital (protocol # 2.494.598) and of Psychiatric Institute (protocol # 2.496.753) of the Federal University of Rio de Janeiro. Furthermore, this study was conducted in accordance with the Helsinki Declaration of 1975.

Informed consent

To participate, each subject signed an informed consent form.

Additional information

Publisher’s note

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

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

de Oliveira Araújo, R., Villoria, G.E.M., Luiz, R.R. et al. Association between periodontitis and Alzheimer’s disease and its impact on the self-perceived oral health status: a case-control study. Clin Oral Invest 25, 555–562 (2021). https://doi.org/10.1007/s00784-020-03489-w

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00784-020-03489-w

Keywords

Navigation