The Association between HbA1c Levels, Olfactory Memory and Cognition in Normal, Pre-Diabetic and Diabetic Persons

Burak	      Yulug; Ozlem	      Saatci; Aysun       Işıklar; Lutfu	      Hanoglu; Ulkan	      Kilic; Mehmet	      Ozansoy; Seyda	      Cankaya; Baris	      Cankaya; Ertugrul	      Kilic
doi:10.2174/1871530319666190614121738
Abstract

Background and Aim: Recent data have shown that olfactory dysfunction is strongly related to Alzheimer’s Disease (AD) that is often preceded by olfactory deficits suggesting that olfactory dysfunction might represent an early indicator of future cognitive in prediabetes.
Methods: We have applied to a group of normal (n=15), prediabetic (n=16) and type 2 diabetic outpatients (n=15) olfactory testing, 1.5-T MRI scanner and detailed cognitive evaluation including the standard Mini-Mental State Examination (MMSE) form, Short Blessed Test (SBT), Letter Fluency Test (LFT) and the category fluency test with animal, Fruit and Vegetable Naming (CFT).
Results: We have shown that Odour Threshold (OT), Discrimination (OD), and Identification (OI) scores and most cognitive test results were significantly different in the prediabetes and diabetes group compared to those in the control group. OD and OT were significantly different between the prediabetes and diabetes group, although the cognitive test results were only significantly different in the prediabetes and diabetes group compared to those in the control group. In evaluating the association between OI, OT, OD scores and specific cognitive tests, we have found, that impaired olfactory identification was the only parameter that correlated significantly with the SBT both in the pre-diabetes and diabetes group. Although spot glucose values were only correlated with OT, HbA1c levels were correlated with OT, OD, and OI, as well as results of the letter fluency test suggesting that HbA1c levels rather than the spot glucose values play a critical role in specific cognitive dysfunction.
Conclusion: To the best of our knowledge, this is the first prospective study to demonstrate a strong association between olfactory dysfunction and specific memory impairment in a population with prediabetes and diabetes suggesting that impaired olfactory identification might play an important role as a specific predictor of memory decline.
Keywords: Olfaction, cognition, prediabetes, diabetes, olfactory memory, memory dysfunction.
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Graphical Abstract

[1] 
Marseglia, A.; Fratiglioni, L.; Laukka, E.J.; Santoni, G.; Pedersen, N.L.; Bäckman, L.; Xu, W. Early Cognitive Deficits in Type 2 Diabetes: A Population-Based Study. J. Alzheimers Dis.,  2016, 53(3), 1069-1078.
[http://dx.doi.org/10.3233/JAD-160266] [PMID:  27314527] 
[2] 
Biessels, G.J.; Strachan, M.W.; Visseren, F.L.; Kappelle, L.J.; Whitmer, R.A. Dementia and cognitive decline in type 2 diabetes and prediabetic stages: towards targeted interventions. Lancet Diabetes Endocrinol.,  2014, 2(3), 246-255.
[http://dx.doi.org/10.1016/S2213-8587(13)70088-3] [PMID:  24622755] 
[3] 
Lietzau, G.; Davidsson, W.; Östenson, C.G.; Chiazza, F.; Nathanson, D.; Pintana, H.; Skogsberg, J.; Klein, T.; Nyström, T.; Darsalia, V.; Patrone, C. Type 2 diabetes impairs odour detection, olfactory memory and olfactory neuroplasticity; effects partly reversed by the DPP-4 inhibitor Linagliptin. Acta Neuropathol. Commun.,  2018, 6(1), 14.
[http://dx.doi.org/10.1186/s40478-018-0517-1] [PMID:  29471869] 
[4] 
Abbatecola, A.M.; Paolisso, G.; Lamponi, M.; Bandinelli, S.; Lauretani, F.; Launer, L.; Ferrucci, L. Insulin resistance and executive dysfunction in older persons. J. Am. Geriatr. Soc.,  2004, 52(10), 1713-1718.
[http://dx.doi.org/10.1111/j.1532-5415.2004.52466.x] [PMID:  15450050] 
[5] 
Kalmijn, S.; Feskens, E.J.; Launer, L.J.; Stijnen, T.; Kromhout, D. Glucose intolerance, hyperinsulinaemia and cognitive function in a general population of elderly men. Diabetologia,  1995, 38(9), 1096-1102.
[http://dx.doi.org/10.1007/BF00402181] [PMID:  8591825] 
[6] 
Neergaard, J.S.; Dragsbæk, K.; Christiansen, C.; Nielsen, H.B.; Brix, S.; Karsdal, M.A.; Henriksen, K. Metabolic Syndrome, Insulin Resistance, and Cognitive Dysfunction: Does Your Metabolic Profile Affect Your Brain? Diabetes,  2017, 66(7), 1957-1963.
[http://dx.doi.org/10.2337/db16-1444] [PMID:  28389469 ] 
[7] 
Avadhani, R.; Fowler, K.; Barbato, C.; Thomas, S.; Wong, W.; Paul, C.; Aksakal, M.; Hauser, T.H.; Weinger, K.; Goldfine, A.B. Glycemia and cognitive function in metabolic syndrome and coronary heart disease. Am. J. Med.,  2015, 128(1), 46-55.
[http://dx.doi.org/10.1016/j.amjmed.2014.08.025] [PMID:  25220612 ] 
[8] 
Cukierman-Yaffe, T.; Gerstein, H.C.; Williamson, J.D.; Lazar, R.M.; Lovato, L.; Miller, M.E.; Coker, L.H.; Murray, A.; Sullivan, M.D.; Marcovina, S.M.; Launer, L.J. Action to Control Cardiovascular Risk in Diabetes-Memory in Diabetes (ACCORD-MIND) Investigators. Relationship between baseline glycemic control and cognitive function in individuals with type 2 diabetes and other cardiovascular risk factors: the action to control cardiovascular risk in diabetes-memory in diabetes (ACCORD-MIND) trial. Diabetes Care,  2009, 32(2), 221-226.
[http://dx.doi.org/10.2337/dc08-1153] [PMID:  19171735 ] 
[9] 
Exalto, L.G.; Whitmer, R.A.; Kappele, L.J.; Biessels, G.J. An update on type 2 diabetes, vascular dementia and Alzheimer’s disease. Exp. Gerontol.,  2012, 47(11), 858-864.
[http://dx.doi.org/10.1016/j.exger.2012.07.014] [PMID:  22884853 ] 
[10] 
Gorelick, P.B.; Scuteri, A.; Black, S.E.; Decarli, C.; Greenberg, S.M.; Iadecola, C.; Launer, L.J.; Laurent, S.; Lopez, O.L.; Nyenhuis, D.; Petersen, R.C.; Schneider, J.A.; Tzourio, C.; Arnett, D.K.; Bennett, D.A.; Chui, H.C.; Higashida, R.T.; Lindquist, R.; Nilsson, P.M.; Roman, G.C.; Sellke, F.W.; Seshadri, S. American Heart Association Stroke Council, Council on Epidemiology and Prevention, Council on Cardiovascular Nursing, Council on Cardiovascular Radiology and Intervention, and Council on Cardiovascular Surgery and Anesthesia. Vascular contributions to cognitive impairment and dementia: a statement for healthcare professionals from the american heart association/american stroke association. Stroke,  2011, 42(9), 2672-2713.
[http://dx.doi.org/10.1161/STR.0b013e3182299496] [PMID:  21778438 ] 
[11] 
Craft, S. The role of metabolic disorders in Alzheimer disease and vascular dementia: two roads converged. Arch. Neurol.,  2009, 66(3), 300-305.
[http://dx.doi.org/10.1001/archneurol.2009.27] [PMID:  19273747 ] 
[12] 
Ohara, T.; Doi, Y.; Ninomiya, T.; Hirakawa, Y.; Hata, J.; Iwaki, T.; Kanba, S.; Kiyohara, Y. Glucose tolerance status and risk of dementia in the community: the Hisayama study. Neurology,  2011, 77(12), 1126-1134.
[http://dx.doi.org/10.1212/WNL.0b013e31822f0435] [PMID:  21931106 ] 
[13] 
van den Berg, E.; de Craen, A.J.; Biessels, G.J.; Gussekloo, J.; Westendorp, R.G. The impact of diabetes mellitus on cognitive decline in the oldest of the old: a prospective population-based study. Diabetologia,  2006, 49(9), 2015-2023.
[http://dx.doi.org/10.1007/s00125-006-0333-1] [PMID:  16804671 ] 
[14] 
Rönnemaa, E.; Zethelius, B.; Sundelöf, J.; Sundström, J.; Degerman-Gunnarsson, M.; Lannfelt, L.; Berne, C.; Kilander, L. Glucose metabolism and the risk of Alzheimer’s disease and dementia: a population-based 12 year follow-up study in 71-year-old men. Diabetologia,  2009, 52(8), 1504-1510.
[http://dx.doi.org/10.1007/s00125-009-1393-9] [PMID:  19455303 ] 
[15] 
Pandini, G.; Pace, V.; Copani, A.; Squatrito, S.; Milardi, D.; Vigneri, R. Insulin has multiple antiamyloidogenic effects on human neuronal cells. Endocrinology,  2013, 154(1), 375-387.
[http://dx.doi.org/10.1210/en.2012-1661] [PMID:  23239816 ] 
[16] 
Bartl, J.; Meyer, A.; Brendler, S.; Riederer, P.; Grunblatt, E. Different
effects of soluble and aggregated amyloid beta42 on
gene/protein expression and enzyme activity involved in insulin and
APP pathways, Journal of neural transmission (Vienna, Austria :
1996),  2013, 120(1), 113-20.
[17] 
Nalivaeva, N.N.; Beckett, C.; Belyaev, N.D.; Turner, A.J. Are amyloid-degrading enzymes viable therapeutic targets in Alzheimer’s disease? J. Neurochem.,  2012, 120(Suppl. 1), 167-185.
[http://dx.doi.org/10.1111/j.1471-4159.2011.07510.x] [PMID:  22122230 ] 
[18] 
Candeias, E.; Duarte, A.I.; Carvalho, C.; Correia, S.C.; Cardoso, S.; Santos, R.X.; Plácido, A.I.; Perry, G.; Moreira, P.I. The impairment of insulin signaling in Alzheimer’s disease. IUBMB Life,  2012, 64(12), 951-957.
[http://dx.doi.org/10.1002/iub.1098] [PMID:  23129399 ] 
[19] 
Correia, S.C.; Santos, R.X.; Carvalho, C.; Cardoso, S.; Candeias, E.; Santos, M.S.; Oliveira, C.R.; Moreira, P.I. Insulin signaling, glucose metabolism and mitochondria: major players in Alzheimer’s disease and diabetes interrelation. Brain Res.,  2012, 1441, 64-78.
[http://dx.doi.org/10.1016/j.brainres.2011.12.063] [PMID:  22290178 ] 
[20] 
Luchsinger, J.A.; Cabral, R.; Eimicke, J.P.; Manly, J.J.; Teresi, J. Glycemia, Diabetes Status, and Cognition in Hispanic Adults Aged 55-64 Years. Psychosom. Med.,  2015, 77(6), 653-663.
[http://dx.doi.org/10.1097/PSY.0000000000000208] [PMID:  26163818 ] 
[21] 
Rhee, M.K.; Herrick, K.; Ziemer, D.C.; Vaccarino, V.; Weintraub, W.S.; Narayan, K.M.; Kolm, P.; Twombly, J.G.; Phillips, L.S. Many Americans have pre-diabetes and should be considered for metformin therapy. Diabetes Care,  2010, 33(1), 49-54.
[http://dx.doi.org/10.2337/dc09-0341] [PMID:  19808929 ] 
[22] 
Akbaraly, T.N.; Kivimaki, M.; Shipley, M.J.; Tabak, A.G.; Jokela, M.; Virtanen, M.; Marmot, M.G.; Ferrie, J.E.; Singh-Manoux, A. Metabolic syndrome over 10 years and cognitive functioning in late midlife: the Whitehall II study. Diabetes Care,  2010, 33(1), 84-89.
[http://dx.doi.org/10.2337/dc09-1218] [PMID:  19837794 ] 
[23] 
Gatto, N.M.; Henderson, V.W.; St John, J.A.; McCleary, C.; Hodis, H.N.; Mack, W.J. Metabolic syndrome and cognitive function in healthy middle-aged and older adults without diabetes. Neuropsychol. Dev. Cogn. B. Aging Neuropsychol. Cogn.,  2008, 15(5), 627-641.
[http://dx.doi.org/10.1080/13825580802036936] [PMID:  18608045 ] 
[24] 
Kalmijn, S.; Foley, D.; White, L.; Burchfiel, C.M.; Curb, J.D.; Petrovitch, H.; Ross, G.W.; Havlik, R.J.; Launer, L.J. Metabolic cardiovascular syndrome and risk of dementia in Japanese-American elderly men. The Honolulu-Asia aging study. Arterioscler. Thromb. Vasc. Biol.,  2000, 20(10), 2255-2260.
[http://dx.doi.org/10.1161/01.ATV.20.10.2255] [PMID:  11031212 ] 
[25] 
O’Bryant, S.E.; Humphreys, J.D.; Smith, G.E.; Ivnik, R.J.; Graff-Radford, N.R.; Petersen, R.C.; Lucas, J.A. Detecting dementia with the mini-mental state examination in highly educated individuals. Arch. Neurol.,  2008, 65(7), 963-967.
[http://dx.doi.org/10.1001/archneur.65.7.963] [PMID:  18625866 ] 
[26] 
Grut, M.; Fratiglioni, L.; Viitanen, M.; Winblad, B. Accuracy of the Mini-Mental Status Examination as a screening test for dementia in a Swedish elderly population. Acta Neurol. Scand.,  1993, 87(4), 312-317.
[http://dx.doi.org/10.1111/j.1600-0404.1993.tb05514.x] [PMID:  8503262] 
[27] 
Harvan, J.R.; Cotter, V. An evaluation of dementia screening in the primary care setting. J. Am. Acad. Nurse Pract.,  2006, 18(8), 351-360.
[http://dx.doi.org/10.1111/j.1745-7599.2006.00137.x] [PMID:  16907696 ] 
[28] 
Mungas, D.; Marshall, S.C.; Weldon, M.; Haan, M.; Reed, B.R. Age and education correction of Mini-Mental State Examination for English and Spanish-speaking elderly. Neurology,  1996, 46(3), 700-706.
[http://dx.doi.org/10.1212/WNL.46.3.700] [PMID:  8618670 ] 
[29] 
Benedict, R.H.; Brandt, J. Limitation of the Mini-Mental State Examination for the detection of amnesia. J. Geriatr. Psychiatry Neurol.,  1992, 5(4), 233-237.
[PMID:  1418369  ] 
[30] 
Nys, G.M.; van Zandvoort, M.J.; de Kort, P.L.; Jansen, B.P.; Kappelle, L.J.; de Haan, E.H. Restrictions of the Mini-Mental State Examination in acute stroke, Archives of clinical neuropsychology: the official journal of the National Academy of Neuropsychologists,  2005, 20(5), 623-9.
[31] 
Tombaugh, T.N.; McIntyre, N.J. The mini-mental state examination: a comprehensive review. J. Am. Geriatr. Soc.,  1992, 40(9), 922-935.
[http://dx.doi.org/10.1111/j.1532-5415.1992.tb01992.x] [PMID:  1512391 ] 
[32] 
Doty, R.L. Olfactory dysfunction in neurodegenerative diseases: is there a common pathological substrate? Lancet Neurol.,  2017, 16(6), 478-488.
[http://dx.doi.org/10.1016/S1474-4422(17)30123-0] [PMID:  28504111 ] 
[33] 
Daulatzai, M.A. Olfactory dysfunction: its early temporal relationship
and neural correlates in the pathogenesis of Alzheimer's disease, Journal of neural transmission (Vienna, Austria : 1996) ,,  2015, 122(10), 1475-97.
[34] 
Mesholam, R.I.; Moberg, P.J.; Mahr, R.N.; Doty, R.L. Olfaction in neurodegenerative disease: a meta-analysis of olfactory functioning in Alzheimer’s and Parkinson’s diseases. Arch. Neurol.,  1998, 55(1), 84-90.
[http://dx.doi.org/10.1001/archneur.55.1.84] [PMID:  9443714 ] 
[35] 
Sanke, H.; Mita, T.; Yoshii, H.; Yokota, A.; Yamashiro, K.; Ingaki, N.; Onuma, T.; Someya, Y.; Komiya, K.; Tamura, Y.; Shimizu, T.; Ohmura, C.; Kanazawa, A.; Fujitani, Y.; Watada, H. Relationship between olfactory dysfunction and cognitive impairment in elderly patients with type 2 diabetes mellitus. Diabetes Res. Clin. Pract.,  2014, 106(3), 465-473.
[http://dx.doi.org/10.1016/j.diabres.2014.09.039] [PMID:  25451914 ] 
[36] 
Serby, M.; Larson, P.; Kalkstein, D. The nature and course of olfactory deficits in Alzheimer’s disease. Am. J. Psychiatry,  1991, 148(3), 357-360.
[http://dx.doi.org/10.1176/ajp.148.3.357] [PMID:  1992839 ] 
[37] 
Deacon, C.F.; Holst, J.J. Dipeptidyl peptidase-4 inhibitors for the treatment of type 2 diabetes: comparison, efficacy and safety. Expert Opin. Pharmacother.,  2013, 14(15), 2047-2058.
[http://dx.doi.org/10.1517/14656566.2013.824966] [PMID:  23919507 ] 
[38] 
Cassano, T.; Romano, A.; Macheda, T.; Colangeli, R.; Cimmino, C.S.; Petrella, A.; LaFerla, F.M.; Cuomo, V.; Gaetani, S. Olfactory memory is impaired in a triple transgenic model of Alzheimer disease. Behav. Brain Res.,  2011, 224(2), 408-412.
[http://dx.doi.org/10.1016/j.bbr.2011.06.029] [PMID:  21741995] 
[39] 
Coronas-Samano, G.; Baker, K.L.; Tan, W.J.; Ivanova, A.V.; Verhagen, J.V. Fus1 KO Mouse As a Model of Oxidative Stress-Mediated Sporadic Alzheimer’s Disease: Circadian Disruption and Long-Term Spatial and Olfactory Memory Impairments. Front. Aging Neurosci.,  2016, 8, 268.
[http://dx.doi.org/10.3389/fnagi.2016.00268] [PMID:  27895577 ] 
[40] 
Larsson, M.; Hedner, M.; Papenberg, G.; Seubert, J.; Bäckman, L.; Laukka, E.J. Olfactory memory in the old and very old: relations to episodic and semantic memory and APOE genotype. Neurobiol. Aging,  2016, 38, 118-126.
[http://dx.doi.org/10.1016/j.neurobiolaging.2015.11.012] [PMID:  26827650] 
[41] 
Roman, F.S.; Alescio-Lautier, B.; Soumireu-Mourat, B. Age-related learning and memory deficits in odor-reward association in rats. Neurobiol. Aging,  1996, 17(1), 31-40.
[http://dx.doi.org/10.1016/0197-4580(95)02030-6] [PMID:  8786800 ] 
[42] 
Seubert, J.; Laukka, E.J.; Rizzuto, D.; Hummel, T.; Fratiglioni, L.; Bäckman, L.; Larsson, M. Prevalence and Correlates of Olfactory Dysfunction in Old Age: A Population-Based Study. J. Gerontol. A Biol. Sci. Med. Sci.,  2017, 72(8), 1072-1079.
[http://dx.doi.org/10.1093/gerona/glx054] [PMID:  28444135 ] 
[43] 
Young, J.W.; Sharkey, J.; Finlayson, K. Progressive impairment in olfactory working memory in a mouse model of Mild Cognitive Impairment. Neurobiol. Aging,  2009, 30(9), 1430-1443.
[http://dx.doi.org/10.1016/j.neurobiolaging.2007.11.018] [PMID:  18242780 ] 
[44] 
Xu, Z.P.; Yang, S.L.; Zhao, S.; Zheng, C.H.; Li, H.H.; Zhang, Y.; Huang, R.X.; Li, M.Z.; Gao, Y.; Zhang, S.J.; Zhan, P.Y.; Zhang, L.F.; Deng, L.; Wei, S.; Liu, Y.C.; Ye, J.W.; Ren, H.J.; Li, N.; Kong, C.X.; Wang, X.; Fang, L.; Zhou, Q.Z.; Jiang, H.W.; Li, J.R.; Wang, Q.; Ke, D.; Liu, G.P.; Wang, J.Z. Biomarkers for Early Diagnostic of Mild Cognitive Impairment in Type-2 Diabetes Patients: A Multicentre, Retrospective, Nested Case-Control Study. EBioMedicine,  2016, 5, 105-113.
[http://dx.doi.org/10.1016/j.ebiom.2016.02.014] [PMID:  27077117 ] 
[45] 
Havrankova, J.; Brownstein, M.; Roth, J. Insulin and insulin receptors in rodent brain. Diabetologia,  1981, 20(Suppl.), 268-273.
[http://dx.doi.org/10.1007/BF00254492] 
[46] 
Zhang, Z.; Zhang, B.; Wang, X.; Zhang, X.; Yang, Q.X.; Qing, Z.; Lu, J.; Bi, Y.; Zhu, D. Altered Odor-Induced Brain Activity as an Early Manifestation of Cognitive Decline in Patients With Type 2 Diabetes. Diabetes,  2018, 67(5), 994-1006.
[http://dx.doi.org/10.2337/db17-1274] [PMID:  29500313 ] 
[47] 
Dintica, C.S.; Marseglia, A.; Rizzuto, D.; Wang, R.; Seubert, J.; Arfanakis, K.; Bennett, D.A.; Xu, W. Impaired olfaction is associated with cognitive decline and neurodegeneration in the brain. Neurology,  2019, 92(7), e700-e709.
[http://dx.doi.org/10.1212/WNL.0000000000006919] [PMID:  30651382 ] 
[48] 
Alencar, R.C.; Cobas, R.A.; Gomes, M.B. Assessment of cognitive status in patients with type 2 diabetes through the Mini-Mental Status Examination: a cross-sectional study. Diabetol. Metab. Syndr.,  2010, 2, 10.
[http://dx.doi.org/10.1186/1758-5996-2-10] [PMID:  20205826 ] 
[49] 
Chobanian, A.V.; Bakris, G.L.; Black, H.R.; Cushman, W.C.; Green, L.A.; Izzo, J.L., Jr; Jones, D.W.; Materson, B.J.; Oparil, S.; Wright, J.T., Jr; Roccella, E.J. National Heart, Lung, and Blood Institute Joint National Committee on Prevention, Detection, Evaluation, and Treatment of High Blood Pressure; National High Blood Pressure Education Program Coordinating Committee. The Seventh Report of the Joint National Committee on Prevention, Detection, Evaluation, and Treatment of High Blood Pressure: the JNC 7 report. JAMA,  2003, 289(19), 2560-2572.
[http://dx.doi.org/10.1001/jama.289.19.2560] [PMID:  12748199] 
[50] 
Messier, C. Impact of impaired glucose tolerance and type 2 diabetes on cognitive aging. Neurobiol. Aging,  2005, 26(Suppl. 1), 26-30.
[http://dx.doi.org/10.1016/j.neurobiolaging.2005.09.014] [PMID:  16236384 ] 
[51] 
Hummel, T.; Sekinger, B.; Wolf, S.R.; Pauli, E.; Kobal, G. ‘Sniffin’ sticks’: olfactory performance assessed by the combined testing of odor identification, odor discrimination and olfactory threshold. Chem. Senses,  1997, 22(1), 39-52.
[http://dx.doi.org/10.1093/chemse/22.1.39] [PMID:  9056084 ] 
[52] 
Tekeli, H.; Altundağ, A.; Salihoğlu, M.; Cayönü, M.; Kendirli, M.T. The applicability of the “Sniffin’ Sticks” olfactory test in a Turkish population. Med. Sci. Monit.,  2013, 19, 1221-1226.
[http://dx.doi.org/10.12659/MSM.889838] [PMID:  24382345 ] 
[53] 
Kronenbuerger, M.; Belenghi, P.; Ilgner, J.; Freiherr, J.; Hummel, T.; Neuner, I. Olfactory functioning in adults with Tourette syndrome. PLoS One,  2018, 13(6) e0197598
[http://dx.doi.org/10.1371/journal.pone.0197598] [PMID:  29874283 ] 
[54] 
Hummel, T.; Jahnke, U.; Sommer, U.; Reichmann, H.; Muller, A. Olfactory function in patients with idiopathic Parkinson's dis-ease:
effects of deep brain stimulation in the subthalamic nu-cleus, Journal
of neural transmission (Vienna, Austria : 1996),,  2005, 112(5) 669-76
[55] 
Altundag, A.; Cayonu, M.; Salihoglu, M.; Yazıcı, H.; Kurt, O.; Yalcınkaya, E.; Saglam, O. Laryngopharyngeal Reflux Has Negative Effects on Taste and Smell Functions. Otolaryngol. Head Neck Surg.,  2016, 155(1), 117-121.
[http://dx.doi.org/10.1177/0194599816640249] [PMID:  27048678 ] 
[56] 
Whitcroft, K.L.; Cuevas, M.; Andrews, P.; Hummel, T. Monitoring olfactory function in chronic rhinosinusitis and the effect of disease duration on outcome. Int. Forum Allergy Rhinol.,  2018, 8(7), 769-776.
[http://dx.doi.org/10.1002/alr.22104] [PMID:  29480955 ] 
[57] 
Folstein, M.F.; Folstein, S.E.; McHugh, P.R. “Mini-mental state”. A practical method for grading the cognitive state of patients for the clinician. J. Psychiatr. Res.,  1975, 12(3), 189-198.
[http://dx.doi.org/10.1016/0022-3956(75)90026-6] [PMID:  1202204 ] 
[58] 
Gungen, C.; Ertan, T.; Eker, E.; Yasar, R.; Engin, F. [Reliability
and validity of the standardized Mini Mental State Examination in
the diagnosis of mild dementia in Turk-ish population], Turk psikiyatri
dergisi = Turkish journal of psychiatry,  2002, 13(4), 273-81.
[59] 
Ö.Ö. Kalem ŞA. Emre M, Determination of the Descpriptive Statisitcs for Short Blessed Orientation-Memory-Concentration Test (BOMC) and Standardized mini Mental State Examination Test (SMMSE) in an Normal Adult Turkish Sample. Noro Psikiyatri Arsivi,  2002, 39(2-4), 95-102.
[60] 
Katzman, R.; Brown, T.; Fuld, P.; Peck, A.; Schechter, R.; Schimmel, H. Validation of a short Orientation-Memory-Concentration Test of cognitive impairment. Am. J. Psychiatry,  1983, 140(6), 734-739.
[http://dx.doi.org/10.1176/ajp.140.6.734] [PMID:  6846631] 
[61] 
Isaacs, B.; Kennie, A.T. The Set test as an aid to the detection of dementia in old people. Br. J. Psychiatry,  1973, 123(575), 467-470.
[http://dx.doi.org/10.1192/bjp.123.4.467] [PMID:  4748864 ] 
[62] 
Tumaç. Normal deneklerde, frontal hasara duyarlı bazı testlerde
per-formansa yaş ve eğitimin etkisi Institute of Social Sciences, Istanbul
University,Istanbul,Psychology Master Thesis, 1997, 76.
[63] 
Lezak, M.D. Neuropsychological assessment, 4th ed; Ox-ford University Press: Oxford, New York, 2004. 
[64] 
Lezak, M.D. Neuropsychological assessment, 3rd ed; Ox-ford University Press: Oxford, New York, 1995. 
[65] 
Malek-Ahmadi, M.; Small, B.J.; Raj, A. The diagnostic value of controlled oral word association test-FAS and category fluency in single-domain amnestic mild cognitive impairment. Dement. Geriatr. Cogn. Disord.,  2011, 32(4), 235-240.
[http://dx.doi.org/10.1159/000334525] [PMID:  22156335 ] 
[66] 
Ringman, J.M.; Pope, W.; Salamon, N. Insensitivity of visual assessment of hippocampal atrophy in familial Alzheimer’s disease. J. Neurol.,  2010, 257(5), 839-842.
[http://dx.doi.org/10.1007/s00415-009-5436-4] [PMID:  20047059 ] 
[67] 
Bangen, K.J.; Gu, Y.; Gross, A.L.; Schneider, B.C.; Skinner, J.C.; Benitez, A.; Sachs, B.C.; Shih, R.; Sisco, S.; Schupf, N.; Mayeux, R.; Manly, J.J.; Luchsinger, J.A. Relationship Between Type 2 Diabetes Mellitus and Cognitive Change in a Multiethnic Elderly Cohort. J. Am. Geriatr. Soc.,  2015, 63(6), 1075-1083.
[http://dx.doi.org/10.1111/jgs.13441] [PMID:  26096383 ] 
[68] 
Schneider, B.C.; Gross, A.L.; Bangen, K.J.; Skinner, J.C.; Benitez, A.; Glymour, M.M.; Sachs, B.C.; Shih, R.A.; Sisco, S.; Manly, J.J.; Luchsinger, J.A. Association of vascular risk factors with cognition in a multiethnic sample. J. Gerontol. B Psychol. Sci. Soc. Sci.,  2015, 70(4), 532-544.
[http://dx.doi.org/10.1093/geronb/gbu040] [PMID:  24821298 ] 
[69] 
van den Berg, E.; Reijmer, Y.D.; de Bresser, J.; Kessels, R.P.; Kappelle, L.J.; Biessels, G.J. Utrecht Diabetic Encephalopathy Study Group. A 4 year follow-up study of cognitive functioning in patients with type 2 diabetes mellitus. Diabetologia,  2010, 53(1), 58-65.
[http://dx.doi.org/10.1007/s00125-009-1571-9] [PMID:  19882137 ] 
[70] 
Euser, S.M.; Sattar, N.; Witteman, J.C.; Bollen, E.L.; Sijbrands, E.J.; Hofman, A.; Perry, I.J.; Breteler, M.M.; Westendorp, R.G. PROSPER and Rotterdam Study. A prospective analysis of elevated fasting glucose levels and cognitive function in older people: results from PROSPER and the Rotterdam Study. Diabetes,  2010, 59(7), 1601-1607.
[http://dx.doi.org/10.2337/db09-0568] [PMID:  20393152 ] 
[71] 
Reijmer, Y.D.; van den Berg, E.; Ruis, C.; Kappelle, L.J.; Biessels, G.J. Cognitive dysfunction in patients with type 2 diabetes. Diabetes Metab. Res. Rev.,  2010, 26(7), 507-519.
[http://dx.doi.org/10.1002/dmrr.1112] [PMID:  20799243 ] 
[72] 
Knopman, D.; Boland, L.L.; Mosley, T.; Howard, G.; Liao, D.; Szklo, M.; McGovern, P.; Folsom, A.R. Atherosclerosis Risk in Communities (ARIC) Study Investigators. Cardiovascular risk factors and cognitive decline in middle-aged adults. Neurology,  2001, 56(1), 42-48.
[http://dx.doi.org/10.1212/WNL.56.1.42] [PMID:  11148234 ] 
[73] 
Kuhl, D.E.; Metter, E.J.; Riege, W.H.; Hawkins, R.A. The effect of normal aging on patterns of local cerebral glucose utilization. Ann. Neurol.,  1984, 15(Suppl.), S133-S137.
[http://dx.doi.org/10.1002/ana.410150726] [PMID:  6611114 ] 
[74] 
De Santi, S.; de Leon, M.J.; Convit, A.; Tarshish, C.; Rusinek, H.; Tsui, W.H.; Sinaiko, E.; Wang, G.J.; Bartlet, E.; Volkow, N. Age-related changes in brain: II. Positron emission tomography of frontal and temporal lobe glucose metabolism in normal subjects. Psychiatr. Q.,  1995, 66(4), 357-370.
[http://dx.doi.org/10.1007/BF02238755] [PMID:  8584591 ] 
[75] 
Ratcliff, G.; Dodge, H.; Birzescu, M.; Ganguli, M. Tracking cognitive functioning over time: ten-year longitudinal data from a community-based study. Appl. Neuropsychol.,  2003, 10(2), 76-88.
[http://dx.doi.org/10.1207/S15324826AN1002_03] [PMID:  12788682 ] 
[76] 
Arevalo-Rodriguez, I.; Smailagic, N.; Roqué, I. Figuls, M.; Ciapponi, A.; Sanchez-Perez, E.; Giannakou, A.; Pedraza, O.L.; Bonfill Cosp, X.; Cullum, S. Mini-Mental State Examination (MMSE) for the detection of Alzheimer’s disease and other dementias in people with mild cognitive impairment (MCI). Cochrane Database Syst. Rev., 2015, (3) CD010783
[PMID:  25740785  ] 
[77] 
Carpenter, C.R.; Bassett, E.R.; Fischer, G.M.; Shirshekan, J.; Galvin, J.E.; Morris, J.C. Four sensitive screening tools to detect cognitive dysfunction in geriatric emergency department patients: brief Alzheimer's Screen, Short Blessed Test, Ottawa 3DY, and the caregiver-completed AD8, Academic emergency medicine: official journal of the Society for Academic Emergency Medicine,  2011, 18(4), 374-84.
[78] 
Shao, Z.; Janse, E.; Visser, K.; Meyer, A.S. What do verbal fluency tasks measure? Predictors of verbal fluency performance in older adults. Front. Psychol.,  2014, 5, 772.
[http://dx.doi.org/10.3389/fpsyg.2014.00772] [PMID:  25101034 ] 
[79] 
Zhao, Q.; Guo, Q.; Hong, Z. Clustering and switching during a semantic verbal fluency test contribute to differential diagnosis of cognitive impairment. Neurosci. Bull.,  2013, 29(1), 75-82.
[http://dx.doi.org/10.1007/s12264-013-1301-7] [PMID:  23322003 ] 
[80] 
Andreou, G.; Trott, K. Verbal fluency in adults diagnosed with attention-deficit hyperactivity disorder (ADHD) in childhood. Atten. Defic. Hyperact. Disord.,  2013, 5(4), 343-351.
[http://dx.doi.org/10.1007/s12402-013-0112-z] [PMID:  23749309] 
[81] 
Ettenhofer, M.L.; Hambrick, D.Z.; Abeles, N. Reliability and stability of executive functioning in older adults. Neuropsychology,  2006, 20(5), 607-613.
[http://dx.doi.org/10.1037/0894-4105.20.5.607] [PMID:  16938023 ] 
[82] 
Costafreda, S.G.; Fu, C.H.; Lee, L.; Everitt, B.; Brammer, M.J.; David, A.S. A systematic review and quantitative appraisal of fMRI studies of verbal fluency: role of the left inferior frontal gyrus. Hum. Brain Mapp.,  2006, 27(10), 799-810.
[http://dx.doi.org/10.1002/hbm.20221] [PMID:  16511886 ] 
[83] 
Robinson, G.; Shallice, T.; Bozzali, M.; Cipolotti, L. The differing roles of the frontal cortex in fluency tests. Brain,  2012, 135(Pt 7), 2202-2214.
[http://dx.doi.org/10.1093/brain/aws142] [PMID:  22669082 ] 
[84] 
Grogan, A.; Green, D.W.; Ali, N.; Crinion, J.T.; Price, C.J. Structural
correlates of semantic and phonemic fluency ability in first
and second languages, Cerebral cortex,  (New York, N.Y. : 1991). 2009, 19, pp. (11)2690-8.
[85] 
Katzev, M.; Tüscher, O.; Hennig, J.; Weiller, C.; Kaller, C.P. Revisiting the functional specialization of left inferior frontal gyrus in phonological and semantic fluency: the crucial role of task demands and individual ability. J. Neurosci.,  2013, 33(18), 7837-7845.
[http://dx.doi.org/10.1523/JNEUROSCI.3147-12.2013] [PMID:  23637175 ] 
[86] 
Baldo, J.V.; Shimamura, A.P. Letter and category fluency in patients with frontal lobe lesions. Neuropsychology,  1998, 12(2), 259-267.
[http://dx.doi.org/10.1037/0894-4105.12.2.259] [PMID:  9556772 ] 
[87] 
Schwartz, S.; Baldo, J. Distinct patterns of word retrieval in right and left frontal lobe patients: a multidimensional perspective. Neuropsychologia,  2001, 39(11), 1209-1217.
[http://dx.doi.org/10.1016/S0028-3932(01)00053-7] [PMID:  11527558 ] 
[88] 
Klunk, W.E.; Engler, H.; Nordberg, A.; Wang, Y.; Blomqvist, G.; Holt, D.P.; Bergström, M.; Savitcheva, I.; Huang, G.F.; Estrada, S.; Ausén, B.; Debnath, M.L.; Barletta, J.; Price, J.C.; Sandell, J.; Lopresti, B.J.; Wall, A.; Koivisto, P.; Antoni, G.; Mathis, C.A.; Långström, B. Imaging brain amyloid in Alzheimer’s disease with Pittsburgh Compound-B. Ann. Neurol.,  2004, 55(3), 306-319.
[http://dx.doi.org/10.1002/ana.20009] [PMID:  14991808 ] 
[89] 
Stamps, J.J.; Bartoshuk, L.M.; Heilman, K.M. A brief olfactory test for Alzheimer’s disease. J. Neurol. Sci.,  2013, 333(1-2), 19-24.
[http://dx.doi.org/10.1016/j.jns.2013.06.033] [PMID:  23927938 ] 
[90] 
Blennow, K. Cerebrospinal fluid protein biomarkers for Alzheimer's dis-ease, NeuroRx: the journal of the American Society for Ex-perimental NeuroTherapeutics,  2004, 1(2), 213-25.
[91] 
McKhann, G.; Drachman, D.; Folstein, M.; Katzman, R.; Price, D.; Stadlan, E.M. 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,  1984, 34(7), 939-944.
[http://dx.doi.org/10.1212/WNL.34.7.939] [PMID:  6610841 ] 
[92] 
McKhann, G.M.; Knopman, D.S.; Chertkow, H.; Hyman, B.T.; Jack, C.R., Jr; Kawas, C.H.; Klunk, W.E.; Koroshetz, W.J.; Manly, J.J.; Mayeux, R.; Mohs, R.C.; Morris, J.C.; Rossor, M.N.; Scheltens, P.; Carrillo, M.C.; Thies, B.; Weintraub, S.; Phelps, C.H. 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. Alzheimers Dement.,  2011, 7(3), 263-269.
[http://dx.doi.org/10.1016/j.jalz.2011.03.005] [PMID:  21514250 ] 
[93] 
Rowe, C.C.; Villemagne, V.L. Brain amyloid imaging, Journal of nuclear medicine: official publication, Society of Nuclear Medicine,  2011, 52(11), 1733-40.
[94] 
Irwin, D.J.; McMillan, C.T.; Toledo, J.B.; Arnold, S.E.; Shaw, L.M.; Wang, L.S.; Van Deerlin, V.; Lee, V.M.; Trojanowski, J.Q.; Grossman, M. Comparison of cerebrospinal fluid levels of tau and Aβ 1-42 in Alzheimer disease and frontotemporal degeneration using 2 analytical platforms. Arch. Neurol.,  2012, 69(8), 1018-1025.
[http://dx.doi.org/10.1001/archneurol.2012.26] [PMID:  22490326 ] 
[95] 
Swan, G.E.; Carmelli, D. Impaired olfaction predicts cognitive decline in nondemented older adults. Neuroepidemiology,  2002, 21(2), 58-67.
[http://dx.doi.org/10.1159/000048618] [PMID:  11901274 ] 
[96] 
Lojkowska, W.; Sawicka, B.; Gugala, M.; Sienkiewicz-Jarosz, H.; Bochynska, A.; Scinska, A.; Korkosz, A.; Lojek, E.; Ryglewicz, D. Follow-up study of olfactory deficits, cognitive functions, and volume loss of medial temporal lobe structures in patients with mild cognitive impairment. Curr. Alzheimer Res.,  2011, 8(6), 689-698.
[http://dx.doi.org/10.2174/156720511796717212] [PMID:  21592056 ] 
[97] 
Cerf-Ducastel, B.; Murphy, C. Neural substrates of cross-modal olfactory recognition memory: an fMRI study. Neuroimage,  2006, 31(1), 386-396.
[http://dx.doi.org/10.1016/j.neuroimage.2005.11.009] [PMID:  16414279 ] 
[98] 
Hedner, M.; Larsson, M.; Arnold, N.; Zucco, G.M.; Hummel, T. Cognitive factors in odor detection, odor discrimination, and odor identification tasks. J. Clin. Exp. Neuropsychol.,  2010, 32(10), 1062-1067.
[http://dx.doi.org/10.1080/13803391003683070] [PMID:  20437286 ] 
[99] 
Schubert, C.R.; Carmichael, L.L.; Murphy, C.; Klein, B.E.; Klein, R.; Cruickshanks, K.J. Olfaction and the 5-year incidence of cognitive impairment in an epidemiological study of older adults. J. Am. Geriatr. Soc.,  2008, 56(8), 1517-1521.
[http://dx.doi.org/10.1111/j.1532-5415.2008.01826.x] [PMID:  18662205 ] 
[100] 
Wilson, R.S.; Arnold, S.E.; Schneider, J.A.; Tang, Y.; Bennett, D.A. The relationship between cerebral Alzheimer’s disease pathology and odour identification in old age. J. Neurol. Neurosurg. Psychiatry,  2007, 78(1), 30-35.
[http://dx.doi.org/10.1136/jnnp.2006.099721] [PMID:  17012338 ] 
[101] 
Sohrabi, H.R.; Bates, K.A.; Rodrigues, M.; Taddei, K.; Laws, S.M.; Lautenschlager, N.T.; Dhaliwal, S.S.; Johnston, A.N.; Mackay-Sim, A.; Gandy, S.; Foster, J.K.; Martins, R.N. Olfactory dysfunction is associated with subjective memory complaints in community-dwelling elderly individuals. J. Alzheimers Dis.,  2009, 17(1), 135-142.
[http://dx.doi.org/10.3233/JAD-2009-1020] [PMID:  19494438 ] 
[102] 
Aqrabawi, A.J.; Kim, J.C. Hippocampal projections to the anterior olfactory nucleus differentially convey spatiotemporal information during episodic odour memory. Nat. Commun.,  2018, 9(1), 2735.
[http://dx.doi.org/10.1038/s41467-018-05131-6] [PMID:  30013078 ] 
[103] 
Olofsson, J.K.; Rönnlund, M.; Nordin, S.; Nyberg, L.; Nilsson, L.G.; Larsson, M. Odor identification deficit as a predictor of five-year global cognitive change: interactive effects with age and ApoE-epsilon4. Behav. Genet.,  2009, 39(5), 496-503.
[http://dx.doi.org/10.1007/s10519-009-9289-5] [PMID:  19633944] 
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DOI https://dx.doi.org/10.2174/1871530319666190614121738	Print ISSN 1871-5303
Publisher Name Bentham Science Publisher	Online ISSN 2212-3873
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