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Clinical periodontal variables in patients with and without dementia—a systematic review and meta-analysis

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Abstract

Background

Considering the increasing number of elderly people, dementia has gained an important role in today’s society. Although the contributing factors for dementia have not been fully understood, chronic periodontitis (CP) seems to have a possible link to dementia.

Aim

To conduct a systematic review including meta-analysis in order to assess potential differences in clinical periodontal variables between patients with dementia and non-demented individuals.

Methods

The following focused question was evaluated: is periodontitis associated with dementia? Electronic searches in two databases, MEDLINE and EMBASE, were conducted. Meta-analysis was performed with the collected data in order to find a statistically significant difference in clinical periodontal variables between the group of dementia and the cognitive normal controls.

Results

Forty-two articles remained for full text reading. Finally, seven articles met the inclusion criteria and only five studies provided data suitable for meta-analysis. Periodontal probing depth (PPD), bleeding on probing (BOP), gingival bleeding index (GBI), clinical attachment level (CAL), and plaque index (PI) were included as periodontal variables in the meta-analysis. Each variable revealed a statistically significant difference between the groups. In an attempt to reveal an overall difference between the periodontal variables in dementia patients and non-demented individuals, the chosen variables were transformed into units that resulted in a statistically significant overall difference (p < 0.00001).

Conclusion

The current findings indicate that compared to systemically healthy individuals, demented patients show significantly worse clinical periodontal variables. However, further epidemiological studies including a high numbers of participants, the use of exact definitions both for dementia and chronic periodontitis and adjusted for cofounders is warranted.

Clinical relevance

These findings appear to support the putative link between CP and dementia. Consequently, the need for periodontal screening and treatment of elderly demented people should be emphasized.

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References

  1. Van Dyke TE, van Winkelhoff AJ (2013) Infection and inflammatory mechanisms. J Clin Periodontol 40(Suppl 14):S1–S7. https://doi.org/10.1111/jcpe.12088

    PubMed  Google Scholar 

  2. Kassebaum NJ, Bernabe E, Dahiya M, Bhandari B, Murray CJ, Marcenes W (2014) Global burden of severe periodontitis in 1990–2010: a systematic review and meta-regression. J Dent Res 93:1045–1053. https://doi.org/10.1177/0022034514552491

    Article  PubMed  PubMed Central  Google Scholar 

  3. Alzheime’s A (2014) 2014 Alzheimer’s disease facts and figures. Alzheimers Dement 10:e47–e92

    Article  Google Scholar 

  4. Prince M, Bryce R, Albanese E, Wimo A, Ribeiro W, Ferri CP (2013) The global prevalence of dementia: a systematic review and metaanalysis. Alzheimers Dement 9:63–75 e2. https://doi.org/10.1016/j.jalz.2012.11.007

    Article  PubMed  Google Scholar 

  5. Bloom GS (2014) Amyloid-beta and tau: the trigger and bullet in Alzheimer disease pathogenesis. JAMA Neurol 71:505–508. https://doi.org/10.1001/jamaneurol.2013.5847

    Article  PubMed  Google Scholar 

  6. Weiner MW, Veitch DP, Aisen PS, Beckett LA, Cairns NJ, Green RC, Harvey D, Jack CR, Jagust W, Liu E, Morris JC, Petersen RC, Saykin AJ, Schmidt ME, Shaw L, Shen L, Siuciak JA, Soares H, Toga AW, Trojanowski JQ, Alzheimer’s Disease Neuroimaging I (2013) The Alzheimer’s Disease Neuroimaging Initiative: a review of papers published since its inception. Alzheimers Dement 9:e111–e194. https://doi.org/10.1016/j.jalz.2013.05.1769

    Article  PubMed  PubMed Central  Google Scholar 

  7. Jawhar S, Wirths O, Schilling S, Graubner S, Demuth HU, Bayer TA (2011) Overexpression of glutaminyl cyclase, the enzyme responsible for pyroglutamate A{beta} formation, induces behavioral deficits, and glutaminyl cyclase knock-out rescues the behavioral phenotype in 5XFAD mice. J Biol Chem 286:4454–4460. https://doi.org/10.1074/jbc.M110.185819

    Article  PubMed  Google Scholar 

  8. Bekris LM, Yu CE, Bird TD, Tsuang DW (2010) Genetics of Alzheimer disease. J Geriatr Psychiatry Neurol 23:213–227. https://doi.org/10.1177/0891988710383571

    Article  PubMed  PubMed Central  Google Scholar 

  9. Pizzo G, Guiglia R, Lo Russo L, Campisi G (2010) Dentistry and internal medicine: from the focal infection theory to the periodontal medicine concept. Eur J Intern Med 21:496–502. https://doi.org/10.1016/j.ejim.2010.07.011

    Article  PubMed  Google Scholar 

  10. Gatz M, Mortimer JA, Fratiglioni L, Johansson B, Berg S, Reynolds CA, Pedersen NL (2006) Potentially modifiable risk factors for dementia in identical twins. Alzheimers Dement 2:110–117. https://doi.org/10.1016/j.jalz.2006.01.002

    Article  PubMed  Google Scholar 

  11. Chen JH, Lin KP, Chen YC (2009) Risk factors for dementia. J Formos Med Assoc 108:754–764. https://doi.org/10.1016/S0929-6646(09)60402-2

    Article  PubMed  Google Scholar 

  12. Hopcraft MS, Morgan MV, Satur JG, Wright FA, Darby IB (2012) Oral hygiene and periodontal disease in Victorian nursing homes. Gerodontology 29:e220–e228. https://doi.org/10.1111/j.1741-2358.2010.00448.x

    Article  PubMed  Google Scholar 

  13. Foley NC, Affoo RH, Martin RE (2015) A systematic review and meta-analysis examining pneumonia-associated mortality in dementia. Dement Geriatr Cogn Disord 39:52–67. https://doi.org/10.1159/000367783

    Article  PubMed  Google Scholar 

  14. Wu B, Fillenbaum GG, Plassman BL, Guo L (2016) Association between oral health and cognitive status: a systematic review. J Am Geriatr Soc 64:1752. https://doi.org/10.1111/jgs.14572

    Article  PubMed  PubMed Central  Google Scholar 

  15. Tonsekar PP, Jiang SS, Yue G (2017) Periodontal disease, tooth loss and dementia: is there a link? A systematic review. Gerodontology 34:151–163. https://doi.org/10.1111/ger.12261

    Article  PubMed  Google Scholar 

  16. 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 86:244–253. https://doi.org/10.1902/jop.2014.140340

    Article  PubMed  Google Scholar 

  17. Rai B, Kaur J, Anand SC (2012) Possible relationship between periodontitis and dementia in a North Indian old age population: a pilot study. Gerodontology 29:e200–e205. https://doi.org/10.1111/j.1741-2358.2010.00441.x

    Article  PubMed  Google Scholar 

  18. Zenthofer A, Baumgart D, Cabrera T, Rammelsberg P, Schroder J, Corcodel N, Hassel AJ (2017) Poor dental hygiene and periodontal health in nursing home residents with dementia: an observational study. Odontology 105:208–213. https://doi.org/10.1007/s10266-016-0246-5

    Article  PubMed  Google Scholar 

  19. Martande SS, Pradeep AR, Singh SP, Kumari M, Suke DK, Raju AP, Naik SB, Singh P, Guruprasad CN, Chatterji A (2014) Periodontal health condition in patients with Alzheimer’s disease. Am J Alzheimers Dis Other Demen 29:498–502. https://doi.org/10.1177/1533317514549650

    Article  PubMed  Google Scholar 

  20. Cestari JA, Fabri GM, Kalil J, Nitrini R, Jacob-Filho W, Tesseroli de Siqueira JT, Siqueira SR (2016) Oral infections and cytokine levels in patients with Alzheimer’s disease and mild cognitive impairment compared with controls. J Alzheimers Dis 54:845. https://doi.org/10.3233/JAD-169006

    Article  PubMed  Google Scholar 

  21. Zenthofer A, Schroder J, Cabrera T, Rammelsberg P, Hassel AJ (2014) Comparison of oral health among older people with and without dementia. Community Dent Health 31:27–31

    PubMed  Google Scholar 

  22. Syrjala AM, Ylostalo P, Ruoppi P, Komulainen K, Hartikainen S, Sulkava R, Knuuttila M (2012) Dementia and oral health among subjects aged 75 years or older. Gerodontology 29:36–42. https://doi.org/10.1111/j.1741-2358.2010.00396.x

    Article  PubMed  Google Scholar 

  23. Lewis S, Jagger RG, Treasure E (2001) The oral health of psychiatric in-patients in South Wales. Spec Care Dentist 21:182–186

    Article  PubMed  Google Scholar 

  24. Wu B, Plassman BL, Liang J, Wei L (2007) Cognitive function and dental care utilization among community-dwelling older adults. Am J Public Health 97:2216–2221. https://doi.org/10.2105/AJPH.2007.109934

    Article  PubMed  PubMed Central  Google Scholar 

  25. Noble JM, Borrell LN, Papapanou PN, Elkind MS, Scarmeas N, Wright CB (2009) Periodontitis is associated with cognitive impairment among older adults: analysis of NHANES-III. J Neurol Neurosurg Psychiatry 80:1206–1211. https://doi.org/10.1136/jnnp.2009.174029

    Article  PubMed  PubMed Central  Google Scholar 

  26. Philip P, Rogers C, Kruger E, Tennant M (2012) Oral hygiene care status of elderly with dementia and in residential aged care facilities. Gerodontology 29:e306–e311. https://doi.org/10.1111/j.1741-2358.2011.00472.x

    Article  PubMed  Google Scholar 

  27. 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 28:613–624. https://doi.org/10.3233/JAD-2011-102004

    Article  PubMed  Google Scholar 

  28. Naorungroj S, Slade GD, Beck JD, Mosley TH, Gottesman RF, Alonso A, Heiss G (2013) Cognitive decline and oral health in middle-aged adults in the ARIC study. J Dent Res 92:795–801. https://doi.org/10.1177/0022034513497960

    Article  PubMed  PubMed Central  Google Scholar 

  29. Cicciu M, Matacena G, Signorino F, Brugaletta A, Cicciu 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 6:766–772

    PubMed  PubMed Central  Google Scholar 

  30. Farhad SZ, Amini S, Khalilian A, Barekatain M, Mafi M, Barekatain M, Rafei E (2014) The effect of chronic periodontitis on serum levels of tumor necrosis factor-alpha in Alzheimer disease. Dent Res J (Isfahan) 11:549–552

    Google Scholar 

  31. Naorungroj S, Schoenbach VJ, Wruck L, Mosley TH, Gottesman RF, Alonso A, Heiss G, Beck J, Slade GD (2015) Tooth loss, periodontal disease, and cognitive decline in the Atherosclerosis Risk in Communities (ARIC) study. Community Dent Oral Epidemiol 43:47–57. https://doi.org/10.1111/cdoe.12128

    Article  PubMed  Google Scholar 

  32. Kamer AR, Pirraglia E, Tsui W, Rusinek H, Vallabhajosula S, Mosconi L, Yi L, McHugh P, Craig RG, Svetcov S, Linker R, Shi C, Glodzik L, Williams S, Corby P, Saxena D, de Leon MJ (2015) Periodontal disease associates with higher brain amyloid load in normal elderly. Neurobiol Aging 36:627–633. https://doi.org/10.1016/j.neurobiolaging.2014.10.038

    Article  PubMed  Google Scholar 

  33. 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:e0151081. https://doi.org/10.1371/journal.pone.0151081

    Article  PubMed  PubMed Central  Google Scholar 

  34. Iwasaki M, Yoshihara A, Kimura Y, Sato M, Wada T, Sakamoto R, Ishimoto Y, Fukutomi E, Chen W, Imai H, Fujisawa M, Okumiya K, Taylor GW, Ansai T, Miyazaki H, Matsubayashi K (2016) Longitudinal relationship of severe periodontitis with cognitive decline in older Japanese. J Periodontal Res 51:681–688. https://doi.org/10.1111/jre.12348

    Article  PubMed  Google Scholar 

  35. Ship JA, Puckett SA (1994) Longitudinal study on oral health in subjects with Alzheimer’s disease. J Am Geriatr Soc 42:57–63

    Article  PubMed  Google Scholar 

  36. Chalmers JM, Carter KD, Spencer AJ (2003) Oral diseases and conditions in community-living older adults with and without dementia. Spec Care Dentist 23:7–17

    Article  PubMed  Google Scholar 

  37. Kim JM, Stewart R, Prince M, Kim SW, Yang SJ, Shin IS, Yoon JS (2007) Dental health, nutritional status and recent-onset dementia in a Korean community population. Int J Geriatr Psychiatry 22:850–855. https://doi.org/10.1002/gps.1750

    Article  PubMed  Google Scholar 

  38. Kamer AR, Craig RG, Pirraglia E, Dasanayake AP, Norman RG, Boylan RJ, Nehorayoff A, Glodzik L, Brys M, de Leon MJ (2009) TNF-alpha and antibodies to periodontal bacteria discriminate between Alzheimer’s disease patients and normal subjects. J Neuroimmunol 216:92–97. https://doi.org/10.1016/j.jneuroim.2009.08.013

    Article  PubMed  PubMed Central  Google Scholar 

  39. Kaye EK, Valencia A, Baba N, Spiro A 3rd, Dietrich T, Garcia RI (2010) Tooth loss and periodontal disease predict poor cognitive function in older men. J Am Geriatr Soc 58:713–718. https://doi.org/10.1111/j.1532-5415.2010.02788.x

    Article  PubMed  PubMed Central  Google Scholar 

  40. Hatipoglu MG, Kabay SC, Guven G (2011) The clinical evaluation of the oral status in Alzheimer-type dementia patients. Gerodontology 28:302–306. https://doi.org/10.1111/j.1741-2358.2010.00401.x

    Article  PubMed  Google Scholar 

  41. Arrive E, Letenneur L, Matharan F, Laporte C, Helmer C, Barberger-Gateau P, Miquel JL, Dartigues JF (2012) Oral health condition of French elderly and risk of dementia: a longitudinal cohort study. Community Dent Oral Epidemiol 40:230–238. https://doi.org/10.1111/j.1600-0528.2011.00650.x

    Article  PubMed  Google Scholar 

  42. Miranda Lde P, Silveira MF, Oliveira TL, Alves SF, Junior HM, Batista AU, Bonan PR (2012) Cognitive impairment, the Mini-Mental State Examination and socio-demographic and dental variables in the elderly in Brazil. Gerodontology 29:e34–e40. https://doi.org/10.1111/j.1741-2358.2011.00541.x

    Article  PubMed  Google Scholar 

  43. Sparks Stein P, Steffen MJ, Smith C, Jicha G, Ebersole JL, Abner E and Dawson D, 3rd (2012) Serum antibodies to periodontal pathogens are a risk factor for Alzheimer’s disease. Alzheimers Dement 8:196–203. doi: https://doi.org/10.1016/j.jalz.2011.04.006

  44. Chen X, Clark JJ, Naorungroj S (2013) Oral health in nursing home residents with different cognitive statuses. Gerodontology 30:49–60. https://doi.org/10.1111/j.1741-2358.2012.00644.x

    Article  PubMed  Google Scholar 

  45. Stewart R, Weyant RJ, Garcia ME, Harris T, Launer LJ, Satterfield S, Simonsick EM, Yaffe K, Newman AB (2013) Adverse oral health and cognitive decline: the health, aging and body composition study. J Am Geriatr Soc 61:177–184. https://doi.org/10.1111/jgs.12094

    Article  PubMed  PubMed Central  Google Scholar 

  46. Noble JM, Scarmeas N, Celenti RS, Elkind MS, Wright CB, Schupf N, Papapanou PN (2014) Serum IgG antibody levels to periodontal microbiota are associated with incident Alzheimer disease. PLoS One 9:e114959. https://doi.org/10.1371/journal.pone.0114959

    Article  PubMed  PubMed Central  Google Scholar 

  47. de Souza Rolim T, Fabri GM, Nitrini R, Anghinah R, Teixeira MJ, de Siqueira JT, Cestari JA, de Siqueira SR (2014) Oral infections and orofacial pain in Alzheimer’s disease: a case-control study. J Alzheimers Dis 38:823–829. https://doi.org/10.3233/JAD-131283

    Article  PubMed  Google Scholar 

  48. Bramanti E, Bramanti A, Matacena G, Bramanti P, Rizzi A, Cicciu M (2015) Clinical evaluation of the oral health status in vascular-type dementia patients. A case-control study. Minerva Stomatol 64:167–175

    PubMed  Google Scholar 

  49. Stewart R, Stenman U, Hakeberg M, Hagglin C, Gustafson D, Skoog I (2015) Associations between oral health and risk of dementia in a 37-year follow-up study: the prospective population study of women in Gothenburg. J Am Geriatr Soc 63:100–105. https://doi.org/10.1111/jgs.13194

    Article  PubMed  Google Scholar 

  50. Chu CH, Ng A, Chau AM and Lo EC (2015) Oral health status of elderly Chinese with dementia in Hong Kong Oral health Prev Dent 13:51–57. doi: https://doi.org/10.3290/j.ohpd.a32343

  51. Lee YT, Lee HC, Hu CJ, Huang LK, Chao SP, Lin CP, Su EC, Lee YC, Chen CC (2017) Periodontitis as a modifiable risk factor for dementia: a nationwide population-based cohort study. J Am Geriatr Soc 65:301–305. https://doi.org/10.1111/jgs.14449

    Article  PubMed  Google Scholar 

  52. Tzeng NS, Chung CH, Yeh CB, Huang RY, Yuh DY, Huang SY, Lu RB, Chang HA, Kao YC, Chiang WS, Chou YC, Chien WC (2016) Are chronic periodontitis and gingivitis associated with dementia? A nationwide, retrospective, matched-cohort study in Taiwan. Neuroepidemiology 47:82–93. https://doi.org/10.1159/000449166

    Article  PubMed  Google Scholar 

  53. Shin HS, Shin MS, Ahn YB, Choi BY, Nam JH, Kim HD (2016) Periodontitis is associated with cognitive impairment in elderly Koreans: results from the Yangpyeong cohort study. J Am Geriatr Soc 64:162–167. https://doi.org/10.1111/jgs.13781

    Article  PubMed  Google Scholar 

  54. Stang A (2010) Critical evaluation of the Newcastle-Ottawa scale for the assessment of the quality of nonrandomized studies in meta-analyses. Eur J Epidemiol 25:603–605. https://doi.org/10.1007/s10654-010-9491-z

    Article  PubMed  Google Scholar 

  55. Israel H, Richter RR (2011) A guide to understanding meta-analysis. J Orthop Sports Phys Ther 41:496–504. https://doi.org/10.2519/jospt.2011.3333

    Article  PubMed  Google Scholar 

  56. McKhann G, Drachman D, Folstein M, Katzman R, Price D, Stadlan EM (1984) Clinical diagnosis of Alzheimer’s disease: report of the NINCDS-ADRDA Work Group under the auspices of Department of Health and Human Services Task Force on Alzheimer’s Disease. Neurology 34:939–944

    Article  PubMed  Google Scholar 

  57. Folstein MF, Folstein SE, McHugh PR (1975) “Mini-mental state”. A practical method for grading the cognitive state of patients for the clinician. J Psychiatr Res 12:189–198

    Article  PubMed  Google Scholar 

  58. Mungas D (1991) In-office mental status testing: a practical guide. Geriatrics 46 63(66):54–58

    Google Scholar 

  59. Yamamoto T, Kondo K, Hirai H, Nakade M, Aida J, Hirata Y (2012) Association between self-reported dental health status and onset of dementia: a 4-year prospective cohort study of older Japanese adults from the Aichi Gerontological Evaluation Study (AGES) Project. Psychosom Med 74:241–248. https://doi.org/10.1097/PSY.0b013e318246dffb

    Article  PubMed  Google Scholar 

  60. Ebersole JL, Steffen MJ, Thomas MV, Al-Sabbagh M (2014) Smoking-related cotinine levels and host responses in chronic periodontitis. J Periodontal Res 49:642–651. https://doi.org/10.1111/jre.12146

    Article  PubMed  Google Scholar 

  61. Li X, Kolltveit KM, Tronstad L, Olsen I (2000) Systemic diseases caused by oral infection. Clin Microbiol Rev 13:547–558

    Article  PubMed  PubMed Central  Google Scholar 

  62. Olsen I, Singhrao SK (2015) Can oral infection be a risk factor for Alzheimer’s disease? J Oral Microbiol 7:29143. https://doi.org/10.3402/jom.v7.29143

    Article  PubMed  Google Scholar 

  63. Singhrao SK, Harding A, Poole S, Kesavalu L, Crean S (2015) Porphyromonas gingivalis periodontal infection and its putative links with Alzheimer’s disease. Mediat Inflamm 2015:137357–137310. https://doi.org/10.1155/2015/137357

    Article  Google Scholar 

  64. Poole S, Singhrao SK, Kesavalu L, Curtis MA, Crean S (2013) Determining the presence of periodontopathic virulence factors in short-term postmortem Alzheimer’s disease brain tissue. J Alzheimers Dis 36:665–677. https://doi.org/10.3233/JAD-121918

    Article  PubMed  Google Scholar 

  65. Yoneyama T, Yoshida M, Ohrui T, Mukaiyama H, Okamoto H, Hoshiba K, Ihara S, Yanagisawa S, Ariumi S, Morita T, Mizuno Y, Ohsawa T, Akagawa Y, Hashimoto K, Sasaki H, Oral Care Working G (2002) Oral care reduces pneumonia in older patients in nursing homes. J Am Geriatr Soc 50:430–433

    Article  PubMed  Google Scholar 

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Funding

This study was supported by the European Commission (FP7-Health 2012-306029 “TRIGGER”).

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Authors and Affiliations

  1. Department of Periodontology, School of Dental Medicine, University of Bern, Bern, Switzerland

    Alejandra Maldonado, Oliver Laugisch, Anton Sculean & Sigrun Eick

  2. Research Section, School of Dental Medicine, University of Bern, Bern, Switzerland

    Walter Bürgin

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  1. Alejandra Maldonado
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  2. Oliver Laugisch
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  5. Sigrun Eick
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Correspondence to Alejandra Maldonado.

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Maldonado, A., Laugisch, O., Bürgin, W. et al. Clinical periodontal variables in patients with and without dementia—a systematic review and meta-analysis. Clin Oral Invest 22, 2463–2474 (2018). https://doi.org/10.1007/s00784-018-2523-x

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