Gingival Crevicular Fluid as Biomarker’s Source for Alzheimer’s Disease
DOI:
https://doi.org/10.15517/ijds.2022.49232Keywords:
Periodontitis; Inflammation; Alzheimer’s disease; Elderly; Cytokines.Abstract
Periodontitis is a low-grade inflammatory disease caused by a subgingival dysbiotic microbiota. Multiple studies have determined the higher prevalence of tooth loss and poor oral hygiene in patients with Alzheimer’s disease (AD). However, the periodontal diagnosis, periodontal bacteria or mediators has not been measured to date. Aim: To determine the periodontal status, the pro-inflammatory mediators, Porphyromonas gingivalis load, and Apoliporpotein E (ApoE) in patients with AD. A complete dental examination was performed on 30 patients, and cognitive status was determined by the Montreal Cognitive Assessment (MoCA). Subgingival microbiota and GCF samples were then taken from all patients from the deepest sites. Total DNA was isolated from the microbiota samples for the quantification of the 16S ribosomal subunit. Pro-inflammatory mediators and ApoE were quantified from the gingival crevicular fluid (GCF). Patients with AD had periodontitis stage III-IV in 80%, a higher concentration of pro-inflammatory and ApoE mediators, and a higher P. gingivalis load compared to healthy subjects. The pro-inflammatory mediators, P. gingivalis load had a negative correlation with the MoCA test scores. Finally, a ROC curve was performed to assess the specificity and sensitivity of ApoE levels, detecting an area of 84.9%. In AD patients, we found a more severe periodontitis, a higher levels of pro-inflammatory mediators, and higher bacterial load. In addition, there is an increase in ApoE that allows to clearly determine patients with health, periodontitis and periodontitis and AD.
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Cecoro G., Annunziata M., Iuorio M.T., Nastrii L., Guida L. Periodontitis, Low-Grade inflammation and systemic health: a scoping review. Medicina (Kaunas). 2020; 56 (6): 272. DOI: https://doi.org/10.3390/medicina56060272
Hajishengallis G. Immuno-microbial pathogenesis of periodontitis: Keystones, pathobionts, and the host response. Trends Immunol. 2014; 35 (1): 3-11. DOI: https://doi.org/10.1016/j.it.2013.09.001
Hajishengallis G. Periodontitis: from microbial immune subversion to systemic inflammation. Nature Reviews Immunology. 2015; 15 (1): 30-44. DOI: https://doi.org/10.1038/nri3785
Teixeira F.C.F., Marin-Leon L., Gomes E.P., Pedrao A.M.N., Pereira A.C., Francisco P.M.S.B. Relationship between periodontitis and subclinical risk indicators for chronic non-communicable diseases. Brazilian Oral Research. 2020; 34: 058. DOI: https://doi.org/10.1590/1807-3107bor-2020.vol34.0058
Imamura T., Pike R.N., Potempa J., Travis J. Pathogenesis of periodontitis: a major arginine-specific cysteine proteinase from Porphyromonas gingivalis induces vascular permeability enhancement through activation of the kallikrein/kinin pathway. Journal of Clinical Investigation. 1994; 94 (1): 361-7. DOI: https://doi.org/10.1172/JCI117330
Laine M.L., Applemelk B.J., van Winkelhoff A.J. Prevalence and distribution of six capsular serotypes of Porphyromonas gingivalis in periodontitis patients. Journal for Dental Research. 1997; 76 (12): 1840-4. DOI: https://doi.org/10.1177/00220345970760120601
van Winkelhoff A.J., Loos B.G., van der Reijden W.A., van der Velden U. Porphyromonas gingivalis, Bacteroides forsythus and other putative periodontal pathogens in subjects with and without periodontal destruction. Journal of Clinical Periodontology. 2002; 29 (11): 1023-8. DOI: https://doi.org/10.1034/j.1600-051X.2002.291107.x
López N., Smith P., Gutierrez J. Periodontal therapy may reduce the risk of preterm low birth weight in women with periodontal disease: A randomized controlled trial. Journal of Periodontology. 2002; 73 (8): 911-24. DOI: https://doi.org/10.1902/jop.2002.73.8.911
López N., Silva I.D., Ipinza J., Gutierrez J. Periodontal therapy reduces the rate of preterm low birth weight women with pregnancy-associates gingivitis. Journal of Periodontology. 2005; 76 (11 Suppl): 2144-53. DOI: https://doi.org/10.1902/jop.2005.76.11-S.2144
Marcelino S.L., Gaetti-Jardim E.J., Nakano V., Canonico L.A.D., Nunes F.D., Lotufo R.F.M., et al. Presence of periodontopathic bacteria in coronary arteries from patients with chronic periodontitis. Anaerobe. 2010; 16 (6): 629-32. DOI: https://doi.org/10.1016/j.anaerobe.2010.08.007
Szulc M., Kustrzycki W., Janczak D., Michalowska D., Baczynska D., Radwan-Oczko M. Presence of periodontopathic bacteria DNA in atheromatous plaques from coronary and carotid arteries. Biomedical Research International. 2015; 2015: 825397. DOI: https://doi.org/10.1155/2015/825397
Udagawa S., Katagiri S., Maekawa S., Takeuchi Y., Komazaki R., Ohtsu A., et al. Effect of Porphyromonas gingivalis infection in the placenta and umbilical cord in pregnant mice with low birth weight. Acta Odontologica Scandinavica. 2018; 76 (6): 433-41. DOI: https://doi.org/10.1080/00016357.2018.1426876
Vanterpool S.F., Been J.V., Houben M.L., Nikkels P.G., De Krijger R.R., Zimmermann L.J., et al. Porphyromonas gingivalis within placental villous mesenchyme and umbilical cord stroma is associated with adverse pregnancy outcome. PLoS One. 2016; 11 (1): e0146157. DOI: https://doi.org/10.1371/journal.pone.0146157
Dominy S.S., Lynch C., Ermini F., Benedyk M., Marczyk A., Konradi A., et al. Porphyromons gingivalis in Alzheimer’s disease brains: Evidence for disease causation and treatment with small-molecule inhibitors. Science Advances. 2019; 5 (1): eaau3333. DOI: https://doi.org/10.1126/sciadv.aau3333
Poole S., Singhrao S.K., Kesavalu L., Curtis M.A., Crean S. Determining the presence of periodontopathic virulence factors in short-term postmortem Alzheimer’s diseas brain tissue. Journal of Alzheimers Disease. 2013; 36 (4): 665-77. DOI: https://doi.org/10.3233/JAD-121918
Selkoe D.J., Hardy J. The amyloid hypothesis of Alzheimer's disease at 25 years. EMBO Molecular Medicine. 2016; 8 (6): 595-608. DOI: https://doi.org/10.15252/emmm.201606210
Bayer T.A., Wirths O. Focusing the amyloid cascade hypothesis on N-truncated Abeta peptides as drug targets against Alzheimer's disease. Acta Neuropathologica. 2014; 127 (6): 787-801. DOI: https://doi.org/10.1007/s00401-014-1287-x
Tse K.H., Herrup K. Re-imagining Alzheimer's disease - the diminishing importance of amyloid and a glimpse of what lies ahead. Journal of Neurochemistry. 2017; 143 (4): 432-44. DOI: https://doi.org/10.1111/jnc.14079
Fulop T., Witkowski J.M., Bourgade K., Khalil A., Zerif E., Larbi A., et al. Can an infection hypothesis explain the Beta amyloid hypothesis of Alzheimer’s disease? Frontiers in Aging Neuroscience. 2018; 10 (224). DOI: https://doi.org/10.3389/fnagi.2018.00224
Pritchard A.B., Crean S, Olsen I., Singhrao S.K. Periodontitis, Microbiomes and their Role in Alzheimer's Disease. Frontiers in Aging Neuroscience. 2017; 24 (9): 336. doi: 10.3389/fnagi.2017.00336 DOI: https://doi.org/10.3389/fnagi.2017.00336
Díaz-Zúñiga J., More J., Melgar-Rodríguez S., Jiménez-Unión M., Villalobos-Orchard F., Muñoz-Manríquez C., et al. Alzheimer’s Disease-Like pathology triggered by Porphyromonas gingivalis in wild type rats is serotype dependent. Frontiers in Immunology. 2020; 11 (588036). DOI: https://doi.org/10.3389/fimmu.2020.588036
Ding Y., Ren J., Yu H., Yu W., Zhou Y. Porphyromonas gingivalis, a periodontitis causing bacterium, induces memory impairment and age-dependent neuroinflammation in mice. Immunity Ageing. 2018; 15 (6).
Ishida N., Ishihara Y., Ishida K., Tada H., Funaki-Kato Y., Hagiwara M., et al. Periodontitis induced by bacterial infection exacerbates features of Alzheimer’s disease in transgenic mice. NPJ Aging and Mechanisms of Disease. 2017; 3 (15). DOI: https://doi.org/10.1038/s41514-017-0015-x
Leira Y., Iglesias-Rey R., Gómez-Lado N., Aguiar P., Campos F., d’Aiuto F., et al. Porphyromonas gingivalis lipopolysaccharide-induced periodontitis and serum amyloid-neta peptides. Archives in Oral Biology. 2019; 99: 120-5. DOI: https://doi.org/10.1016/j.archoralbio.2019.01.008
Poole S., Singhrao S.K., Chukkapalli S., Rivera M., Velsko I., Kesavalu L., et al. Active invasion of Porphyromonas gingivalis and infection-induced complement activation in ApoE-/- mice brains. Journal of Alzheimers Disease. 2015; 43 (1): 67-80. DOI: https://doi.org/10.3233/JAD-140315
Wu Z., Ni J., Liu Y., Teeling J.L., Takayama F., Collcutt A., et al. Cathepsin B plays a critical role in inducing Alzheimer's disease-like phenotypes following chronic systemic exposure to lipopolysaccharide from Porphyromonas gingivalis in mice. Brain, Behaviour, and Immunity. 2017; 65: 350-61. DOI: https://doi.org/10.1016/j.bbi.2017.06.002
Zhang J., Yu C., Zhang X., Chen H., Dong J., Lu W., et al. Porphyromonas gingivalis lipopolysaccharide induces cognitive dysfunction, mediated by neuronal inflammation via activation of the TLR4 signaling pathway in C57BL/6 mice. Journal of Neuroinflammation. 2018; 15 (1): 37-52. DOI: https://doi.org/10.1186/s12974-017-1052-x
Lane C.A., Hardy J., Scott J.M. Alzheimer’s disease. European Journal of Neurology. 2017; 25 (1): 59-70. DOI: https://doi.org/10.1111/ene.13439
Frost G.R., Li Y.M. The role of astrocytes in amyloid production and Alzheimer’s disease. Open Biology. 2017; 7: 170228. DOI: https://doi.org/10.1098/rsob.170228
Ritchie C., Smailagic N., Noel-Storr A.H., Ukuomunne O., Ladds E.C., Martin S. CSF tau and the CSF tau/ABeta ratio for the diagnosis of Alzheimer’s disease dementia and other dementias in people with mild cognitive impairment (MCI). Cochrane Database Systematic Review. 2017; 3 (3): CD10803. DOI: https://doi.org/10.1002/14651858.CD010803.pub2
Limon-Sztencel A., Lipska-Zietkiewicz B.S., Chmara M., Wasag B., Bidzan L., Godlewska B.R., et al. The algorithm for Alzheimer risk assessment based on APOE promoter polymorphisms. Alzheimers Research & Therapy. 2016; 8 (1): 19. DOI: https://doi.org/10.1186/s13195-016-0187-9
Liu C.C., Zhao N., Fu Y., Wang N., Linares C., Tsai C.W., et al. ApoE4 accelerates early seeding of amyloid pathology. Neuron Reports. 2017; 96 (5): 1024-32. DOI: https://doi.org/10.1016/j.neuron.2017.11.013
Singhrao S.K., Harding A., Chukkapalli S., Olsen I., Kesavalu L., Crean S. Apolipoprotein E related co-morbidities and Alzheimer’s Disease. Journal of Alzheimer’s Disease. 2016; 51 (4): 935-48. DOI: https://doi.org/10.3233/JAD150690
McKhann G.M., Knopman D.S., Chertkow H., Hyman B.T., Jack Jr. C.R., Kawas C.H., et al. The diagnosis of dementia due to Alzheimer’s disease: recommendations from the National Institute on Aging-Alzheimer’s Association workgroups on diagnostic guidelines for Alzheimer’s disease. Alzheimer’s & Dementia. 2011; 7 (3): 263-9. DOI: https://doi.org/10.1016/j.jalz.2011.03.005
Papapanou P.N., Sanz M., Buduneli N., Dietrich T., Feres M., Fine D.H., et al. Periodontitis: Consensus report of workgroup 2 of the 2017 World Workshop on the Classification of Periodontal and Peri-Implant Diseases and Conditions. Journal of Clinical Periodontology. 2018; 45: S162-S70. DOI: https://doi.org/10.1111/jcpe.12946
Tonetti M.S., Greenwell H., Kornman K.S. Staging and grading of periodontitis: framework and proposal of a new classification and case definition. Journal of Periodontology. 2018; 89:159-72. DOI: https://doi.org/10.1002/JPER.18-0006
Abusleme L., Dupuy A.K., Dutzan N., Silva N., Burleson J.A., Strausbaugh L.D., et al. The subgingival microbiome in health and periodontitis and its relationship with community biomass and inflammation. International Society for Microbiological Ecology Journal. 2013; 7: 1016-25. DOI: https://doi.org/10.1038/ismej.2012.174
Ovalle A., Gamonal J., Martínez M.A., Silva N., Kakarieka E., Fuentes A., et al. Relationship between periodontal diseases and ascending bacterial infection with preterm delivery. Revista Médica de Chile. 2009; 137: 504-14. DOI: https://doi.org/10.4067/S0034-98872009000400008
Vernal R., Dutzan N., Chaparro A., Puente J., Valenzuela M., Gamonal J. Levels of interleukin-17 in gingival crevicular fluid and in supernatants of cellular cultures of gingival tissue from patients with chronic periodontitis. Journal of Clinical Periodontology. 2005; 32 (4): 383-9. DOI: https://doi.org/10.1111/j.1600-051X.2005.00684.x
Aragón F., Zea-Sevilla M.A., Montero J., Sancho P., Corral R., Tejedor C., et al. Oral health in Alzheimer’s disease: a multicenter case-control study. Clinical Oral Investigations. 2018; 22: 3061-70. DOI: https://doi.org/10.1007/s00784-018-2396-z
Chen X., Shuman S.K., Hodges J.S., Gatewood L.C., Xu J. Patterns of tooth loss in older adults with and without dementia: a retrospective study based on a Minnesota Cohort. Journal of the American Geriatrics Society. 2010; 58 (12): 2300-7. DOI: https://doi.org/10.1111/j.1532-5415.2010.03192.x
Chen X., Clark J.J.J., Naorungroj S. Oral health in nursing home residents with different cognitive statuses. Gerodontology. 2012; 30 (1): 49-60. DOI: https://doi.org/10.1111/j.1741-2358.2012.00644.x
Chen C.K., Wu Y.T., Chang Y.C. Association between chronic periodontitis and the risk of Alzheimer’s disease: a retrospective, population-based, matched-cohort study. Alzheimer’s Research Therapy. 2017; 9 (1): 56-62. DOI: https://doi.org/10.1186/s13195-017-0282-6
Gil Montoya J.A., Barrios R., Sanchez-Lara I., Ramos P., Carnero C., Fornieles F., et al. Systemic inflammatory impact of periodontitis on cognitive impairment. Gerodontology. 2019; 37 (1): 11-8. DOI: https://doi.org/10.1111/ger.12431
Hatipoglu M.G., Kabay S.C., Güven G. The clinical evaluation of the oral status in Alzheimer-type dementia patients. Gerodontology. 2011; 28 (4): 302-6. DOI: https://doi.org/10.1111/j.1741-2358.2010.00401.x
Laugisch O., Johnen A., Buergin W., Eick S., Ehmke B., Duning T., et al. Oral and periodontal health in patients with Alzhiemer’s disease and other forms of dementia - A cross-sectional pilot study. Oral Health and Preventie Dentistry. 2021; 19 (1): 255-61.
Martande S.S., Pradeep A.R., Singh S.P., Kumari M., Suke D.K., Raju A.P., et al. Periodontal health condition in patients with Alzheimer's disease. American Journal of Alzheimer's Disease and Other Dementias. 2014; 29 (6): 498-502. DOI: https://doi.org/10.1177/1533317514549650
Noble J.M., Borrell L.N., Papapnou P.N., Elkind M.S.V., Scarmeas N., Wright C.B. Periodontitis is associated with cognitive impairment among older adults: Analysis of NHANES-III. Journal of Neurology, Neurosurgery, and Psychiatry. 2009; 80 (11): 1206-11. DOI: https://doi.org/10.1136/jnnp.2009.174029
Noble J.M., Scarmeas N., Celenti R.S., Elkind M.S., Wright C.B., Schupf N., et al. Serum IgG antibody levels to periodontal microbiota are associated with incident Alzheimer disease. PLoS One. 2014; 9 (12): e114959. DOI: https://doi.org/10.1371/journal.pone.0114959
Ribeiro G.R., Costa J.L.C., Ambrosano G.M.B., Garcia R.C.M.R. Oral health of the elderly with Alzheimer’s disease. Oral Surgery, Oral Medicine, Oral Pathology and Oral Radiology. 2012; 114( 3): 338-43. DOI: https://doi.org/10.1016/j.oooo.2012.03.028
Rong X., Xiang L., Li Y., Yang H., Chen W., Li L., et al. Chronic periodontitis and Alzheimer disease: a putative link of serum proteins identification by 2S-DIGE proteomics. Frontiers in Aging Neuroscience. 2020; 12: 248. DOI: https://doi.org/10.3389/fnagi.2020.00248
Srisilapanan P., Jai-ua C. Oral health status of dementia patients in Chiang Mai Neurological Hospital. Journal of the Medical Association of Thailand. 2013; 96 (3): 351-7.
Syrjälä A.M.H., Ylöstalo P., Ruoppi P., Komulainen K., Hartikainen S., Sulkava R., et al. Dementia and oral health among subjects aged 75 years or older. Gerodontology. 2012; 29 (1): 36-42. DOI: https://doi.org/10.1111/j.1741-2358.2010.00396.x
Tiisanoja A., Syrjälä A.M.H., Tertsonen M., Komulainen K., Pesonen P., Knuuttila M., et al. Oral diseases and inflammatory burden and Alzheimer’s disease among subjectsaged 75 years or older. Special Care in Dentistry. 2019; 39 (2): 158-65. DOI: https://doi.org/10.1111/scd.12357
Heneka M.T., Carson M.J., El Khoury J., Landreth G.E., Brosseron F., Feinstein D.L., et al. Neuroinflammation in Alzheimer’s disease. Lancet Neurology. 2015; 14 (4): 388-405. DOI: https://doi.org/10.1016/S1474-4422(15)70016-5
Bowman G.L., Dayon L., Kirkland R., Wojcik J., Peyratout G., Severin I.C., et al. Blood-brain barrier breakdown, neuroinflammation, and cognitive decline in older adults. Alzheimer’s Dementia. 2018. DOI: https://doi.org/10.1016/j.jalz.2018.06.2857
Kebir H., Krymborg K., Ifergan I., Dodelet-Devillers A., Cayrol R., Bernard M., et al. Human Th17 lymphocytes promote blood-brain barrier disruption and central nervous system inflammation. Nature Medicine. 2007;1 3 (10): 1173-5. DOI: https://doi.org/10.1038/nm1651
Tao Q., Ang T.F.A., DeCarli C., Auerbach S.H., Devine S., Stein T.D., et al. Association of chronic low-grade inflammation with risk of Alzheimer’s disease in ApoE4 carriers. Journal of American Medical Association Network Open. 2018; 1 (6): 183597. DOI: https://doi.org/10.1001/jamanetworkopen.2018.3597
Ueno M., Chiba Y., Murakami R., Matsumoto K., WKawauchi M., Fujihara R. Blood-brain barrier and blood-cerebrospinal fluid barrier in normal and pathological conditions. Brain Tumor Pathology. 2016; 33 (2): 89-96. DOI: https://doi.org/10.1007/s10014-016-0255-7
Walker K.A., Ficek B.N., Westbrook R. Understanding the role of systemic inflammation in Alzheimer’s Disease. ACS Chemical Neuroscience. 2019; 10 (8): 3340-2. DOI: https://doi.org/10.1021/acschemneuro.9b00333
Hawkins B.T., Davis T.P. The blood-brain barrier/neurovascular unit in health and disease. Pharmacological Reviews. 2005; 57: 173-85. DOI: https://doi.org/10.1124/pr.57.2.4
Rochfort K.D., Collins L.E., Murphy R.P., Cummins P.M. Downregulation of blood-brain barrier phenotype by proinflammatory cytokines involves NADPH oxidase dependent ROS generation: consequences for interendothelial adherens and tight junctions. PLoS One. 2014; 9 (7): e101815. DOI: https://doi.org/10.1371/journal.pone.0101815
Chen J., Ren C.J., Wu L., Xia L.Y., Shao J., Leng W.D., et al. Tooth loss is associated with increased risk of dementia and with a dose-response relationship. Frontiers in Aging Neuroscience. 2018; 10: 415. DOI: https://doi.org/10.3389/fnagi.2018.00415
Emami E., Freitas de Souza R., Kabawat M., Feine J.S. The impact of edentulism on oral and general health. International Journal of Dentistry. 2013; 2013: 498305. DOI: https://doi.org/10.1155/2013/498305
Okamoto N., Morikawa M., Tomioka K., Yanagi M., Amano N., Kurumatani N. Association between tooth loss and the development of mild memory impairment in the elderly: the Fujiwara-kyo Study. Journal of Alzheimer’s Disease. 2015; 44: 777-86. DOI: https://doi.org/10.3233/JAD-141665
Paganini-Hill A., White S.C., Atchison K.A. Dentition, dental health habits, and dementia: the Leisure World cohort study. Journal of the American Geriatrics Society. 2012; 60 (8): 1556-63. DOI: https://doi.org/10.1111/j.1532-5415.2012.04064.x
Singhrao S.K., Harding A., Simmons T., Robinson S., Kesavalu L., Crean S. Oral inflammation, tooth loss, risk factors, and association with progression of Alzheimer’s disease. Journal of Alzheimer’s Disease. 2014; 42 (3): 723-37. DOI: https://doi.org/10.3233/JAD-140387
Stein P.S., Desrosiers M., Donegan S.J., Yepes J.F., Kryscio R.J. Tooth loss, dementia and neuropathy in the Nun study. Journal of the American Dental Association. 2007; 138 (10): 1214-22. DOI: https://doi.org/10.14219/jada.archive.2007.0046
Kobayashi R., Ogawa Y., Hashizume-Takizawa T., Kurita-Ochiai T. Oral bacteria affect the gut microbiome and intestinal immunity. Pathology Disease. 2020; 78 (3): 024. DOI: https://doi.org/10.1093/femspd/ftaa024
Ding Y., Ren J., Yu H., Yu W., Zhou Y. Porphyromonas gingivalis, a periodontitis causing bacterium, induces memory impairment and age-dependent neuroinflammation in mice. Immunity & Ageing. 2018; 15 (6). DOI: https://doi.org/10.1186/s12979-017-0110-7
Gaur S, Agnihotri R. Alzheimer’s disease and chronic periodontitis: Is there an association? Geriatrics Gerontology. 2015;15:391-404. DOI: https://doi.org/10.1111/ggi.12425
Kamer A.P., Craig R.G., Dasanayake A.P., Brys M., Glodzik-Sobanska L., de Leon M.J. Inflammation and Alzheimer’s disease: Possible role of periodontal diseases. Alzheimer’s Dementia. 2008; 4: 242-50. DOI: https://doi.org/10.1016/j.jalz.2007.08.004
Kamer A.R., Craig R.G., Pirraglia E., Dasanayake A.P., Norman R.G., Boylan R.J., et al. TNF-alpha and antibodies to periodontal bacteria discriminate between Alzheimer’s disease patients and normal subjects. Journal of Neuroimmunology. 2009; 216 (1-2): 92-7. DOI: https://doi.org/10.1016/j.jneuroim.2009.08.013
Sparks Stein P., Steffen M.J., Smith C., Jicha G., Ebersole J.L., Abner E., et al. Serum antibodies to periodontal pathogens are a risk factor for Alzheimer's disease. Alzheimer’s Dementia. 2012; 8 (3): 196-203. DOI: https://doi.org/10.1016/j.jalz.2011.04.006
Laugisch O., Johnen A., Maldonado A., Ehmke B., Bürgin W., Olsen I., et al. Periodontal Pathogens and Associated Intrathecal Antibodies in Early Stages of Alzheimer's Disease. Journal of Alzheimer’s Disease. 2018; 66 (1): 105-14. DOI: https://doi.org/10.3233/JAD-180620
Creavin S.T., Wisniewski S., Noel-Storr A.H., Trevelyan C.M., Hampton T., Rayment D., et al. Mini-Mental State Examination (MMSE) for the detection of dementia in clinically unevaluated people aged 65 and over in community and primary care populations. Cochrane Database Systematic Review. 2016; 1: CD011145. DOI: https://doi.org/10.1002/14651858.CD011145.pub2
Ciesielska N., Sokolowski R., Mazur E., Podhorecka M., Polak-Szabela A., Kedziora-Kornatowska K. Is the Montreal Cognitive Assessment (MoCA) test better suited than the Mini-Mental State Examination (MMSE) in mild cognitive impairment (MCI) detection amon people aged over 60? Meta-analysis. Psychiatria Polska. 2016; 50 (5): 1039-52. DOI: https://doi.org/10.12740/PP/45368
Nasreddine Z., Phillips N., Bédirian V., Charbonneau S., Whitehead V., Collin I., et al. The Montreal Cognitive Assessment (MoCA): a brief screening tool for mild cognitive impairment. Journal of the American Geriatrics Society. 2005; 53 (4): 695-9. DOI: https://doi.org/10.1111/j.1532-5415.2005.53221.x
Aggarwal A., Kean E. Comparison of the Folstein Mini Mental State Examination (MMSE) to the Montreal Cognitive Assessment (MoCA) as a cognitive screening tool in an inpatient rehabilitation setting. Neuroscience Medicine. 2010; 1 (39-42). DOI: https://doi.org/10.4236/nm.2010.12006
Dong Y.H., Sharma V.K., Chan B.P.L., Venketasubramanian N., Teoh H.L., Seet R.C.S., et al. The Montreal Cognitive Assessment (MoCA) is superior to the Mini-Mental State Examination (MMSE) for the detection of vascular cognitive impairment after acute stroke. Journal of the Neurological Sciences. 2010; 299 (1-2): 15-8. DOI: https://doi.org/10.1016/j.jns.2010.08.051
Dong Y.H., Lee W.Y., Basri N.A., Collinson S.L., Merchant R.A., Venkataraman A., et al. The Montreal Cognitive Assessment is superior to the Mini-Mental State Examination in detecting patients at higher rosk of dementia. International Psychogeriatrics. 2012; 24 (1): 1749-55. DOI: https://doi.org/10.1017/S1041610212001068
Godefroy O., Fickl A., Roussel M., Auribault C., Bugnicourt J.M., Lamy C., et al. Is the Montreal Cognitive Assessment superior to the Mini-Mental State Examination to detect poststroke cognitive impairment? A study with neurophychological evaluation. Stroke. 2011; 42 (6): 1712-6. DOI: https://doi.org/10.1161/STROKEAHA.110.606277
Pendlebury S.T., Cuthbertson F.C., Weich S.J.V., Mehta Z., Rothwell P.M. Underestimation of cognitive impairment by Mini-Mental State Examination versus the Montreal Cognitive Assessment in patients with transient ischemic attack and stroke. Stroke. 2010; 41(6): 1290-3. DOI: https://doi.org/10.1161/STROKEAHA.110.579888
Morris J.C., Roe C.M., Xiong C., Fagan A.M., Goate A.M., Holtzman D.M., et al. APOE predicts amyloid-beta but not tau Alzheimer pathology in cognitively normal aging. Annals in Neurology. 2010; 67 (1):122-31. DOI: https://doi.org/10.1002/ana.21843
Gao H., Tian Y., Menhg H., Hou J., Xu L., Zhang L., et al. Associations of apolipoprotein E and low-density lipoprotein receptor-related protein 5 polymorphisms with dyslipidemia and generalized aggressive periodontitis in a Chinese population. Journal of Periodontal Research. 2015; 50 (4): 509-18. DOI: https://doi.org/10.1111/jre.12237
Linhartova P.B., Bartova J., Poskerova H., Machal J., Vokurka J., Fassmann A., et al. Apolipoprotein E gene polymorphisms in relation to chronic periodontitis, periodontopathic bacteria, and lipid levels. Archives in Oral Biology. 2015; 60 (3): 456-62. DOI: https://doi.org/10.1016/j.archoralbio.2014.10.003
Kok E., Haikonen S., Luoto T., Huhtala H., Goebeler S., Haapasalo H., et al. Apolipoprotein E-dependent accumulation of Alzheimer disease-related lesions begins in middle age. Annals in Neurology. 2009; 65 (6): 650-7. DOI: https://doi.org/10.1002/ana.21696
Reiman E.M., Chen K., Liu X., Bandy D., Yu M., Lee W.Y., et al. Fibrillar amyloid-beta burden in cognitively normal people at 3 levels of genetic risk for Alzheimer’s disease. Proceedings of the National Academy of Sciences. 2009; 106 (16): 6820-5. DOI: https://doi.org/10.1073/pnas.0900345106
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