Skip to main content
Top
Published in: BMC Neurology 1/2014

Open Access 01-12-2014 | Research article

The brain structural and cognitive basis of odor identification deficits in mild cognitive impairment and Alzheimer's disease

Authors: Grete Kjelvik, Ingvild Saltvedt, Linda R White, Pål Stenumgård, Olav Sletvold, Knut Engedal, Kristina Skåtun, Ann Kristin Lyngvær, Hill Aina Steffenach, Asta K Håberg

Published in: BMC Neurology | Issue 1/2014

Login to get access

Abstract

Background

The objectives of this study were to explore the relationship between olfactory impairment, cognitive measures, and brain structure volumes in healthy elderly individuals, compared to patients with amnestic mild cognitive impairment (aMCI) or early Alzheimer's disease (AD). The primary aim was to elucidate possible differences in cognitive scores and brain structure volumes between aMCI/AD patients with relatively intact odor identification (OI) ability and those with reduced ability.

Methods

Twelve patients with aMCI, six with early AD, and 30 control subjects were included. OI abilities were assessed with the Brief Smell Identification Test (B-SIT) and Sniffin Sticks Identification Test (SSIT). Neuropsychological tests of executive functions and memory were performed. Brain structural volumes were obtained from T1 weighted 3D MRI at 3 Tesla. Statistical comparisons between the patients with aMCI and AD indicated no significant differences in performance on most tests. Since the groups were small and AD patients were in an early phase of disease, all patients were subsequently considered together as a single group for studying OI. Patients were subdivided into relatively intact (scores >50%) and reduced OI (≤ 50% score) on the olfactory tests.

Results

The aMCI/AD group with reduced OI ability, as measured by both B-SIT and SSIT, had significantly smaller hippocampal volume as compared to the patient group with OI scores > 50%. There was a significant association between OI scores and hippocampal volume in the patient (not the control) group. Similar changes with tests of executive function and memory were not found. Low OI scores on B-SIT were associated with conversion from aMCI to AD in patients. The reduced OI patient group was significantly faster on Rey complex figure copying than the fairly intact OI group.

Conclusion

The results from this pilot study suggest that the reduction in the size of hippocampus in connection with early AD is associated more with loss of OI ability rather than loss of memory, thus demonstrating that impaired OI is an early marker of medial temporal lobe degeneration.
Appendix
Available only for authorised users
Literature
1.
go back to reference Rahayel S, Frasnelli J, Joubert S: The effect of Alzheimer's disease and Parkinson's disease on olfaction: a meta-analysis. Behav Brain Res. 2012, 231 (1): 60-74. 10.1016/j.bbr.2012.02.047.CrossRefPubMed Rahayel S, Frasnelli J, Joubert S: The effect of Alzheimer's disease and Parkinson's disease on olfaction: a meta-analysis. Behav Brain Res. 2012, 231 (1): 60-74. 10.1016/j.bbr.2012.02.047.CrossRefPubMed
2.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
3.
go back to reference Hedner M, Larsson M, Arnold N, Zucco GM, Hummel T: Cognitive factors in odor detection, odor discrimination, and odor identification tasks. J Clin Exp Neuropsychol. 2010, 32 (10): 1062-1067. 10.1080/13803391003683070.CrossRefPubMed Hedner M, Larsson M, Arnold N, Zucco GM, Hummel T: Cognitive factors in odor detection, odor discrimination, and odor identification tasks. J Clin Exp Neuropsychol. 2010, 32 (10): 1062-1067. 10.1080/13803391003683070.CrossRefPubMed
4.
go back to reference Larsson M, Finkel D, Pedersen NL: Odor identification: Influences of age, gender, cognition, and personality. J Gerontol B-Psychol. 2000, 55 (5): 304-P310. 10.1093/geronb/55.5.P304.CrossRef Larsson M, Finkel D, Pedersen NL: Odor identification: Influences of age, gender, cognition, and personality. J Gerontol B-Psychol. 2000, 55 (5): 304-P310. 10.1093/geronb/55.5.P304.CrossRef
5.
go back to reference Devanand DP, Michaels-Marston KS, Liu X, Pelton GH, Padilla M, Marder K, Bell K, Stern Y, Mayeux R: Olfactory deficits in patients with mild cognitive impairment predict Alzheimer's disease at follow-up. Am J Psychiatry. 2000, 157 (9): 1399-1405. 10.1176/appi.ajp.157.9.1399.CrossRefPubMed Devanand DP, Michaels-Marston KS, Liu X, Pelton GH, Padilla M, Marder K, Bell K, Stern Y, Mayeux R: Olfactory deficits in patients with mild cognitive impairment predict Alzheimer's disease at follow-up. Am J Psychiatry. 2000, 157 (9): 1399-1405. 10.1176/appi.ajp.157.9.1399.CrossRefPubMed
6.
go back to reference Westervelt HJ, Bruce JM, Coon WG, Tremont G: Odor identification in mild cognitive impairment subtypes. J Clin Exp Neuropsychol. 2008, 30 (2): 151-156. 10.1080/13803390701287408.CrossRefPubMed Westervelt HJ, Bruce JM, Coon WG, Tremont G: Odor identification in mild cognitive impairment subtypes. J Clin Exp Neuropsychol. 2008, 30 (2): 151-156. 10.1080/13803390701287408.CrossRefPubMed
7.
go back to reference Kjelvik G, Sando SB, Aasly J, Engedal KA, White LR: Use of the brief smell identification test for olfactory deficit in a Norwegian population with Alzheimer's disease. Int J Geriatr Psychiatry. 2007, 22 (10): 1020-1024. 10.1002/gps.1783.CrossRefPubMed Kjelvik G, Sando SB, Aasly J, Engedal KA, White LR: Use of the brief smell identification test for olfactory deficit in a Norwegian population with Alzheimer's disease. Int J Geriatr Psychiatry. 2007, 22 (10): 1020-1024. 10.1002/gps.1783.CrossRefPubMed
8.
go back to reference Gray AJ, Staples V, Murren K, Dhariwal A, Bentham P: Olfactory identification is impaired in clinic-based patients with vascular dementia and senile dementia of Alzheimer type. Int J Geriatr Psychiatry. 2001, 16 (5): 513-517. 10.1002/gps.383.CrossRefPubMed Gray AJ, Staples V, Murren K, Dhariwal A, Bentham P: Olfactory identification is impaired in clinic-based patients with vascular dementia and senile dementia of Alzheimer type. Int J Geriatr Psychiatry. 2001, 16 (5): 513-517. 10.1002/gps.383.CrossRefPubMed
9.
go back to reference McShane RH, Nagy Z, Esiri MM, King E, Joachim C, Sullivan N, Smith AD: Anosmia in dementia is associated with Lewy bodies rather than Alzheimer's pathology. J Neurol Neurosurg Psychiatry. 2001, 70 (6): 739-743. 10.1136/jnnp.70.6.739.CrossRefPubMedPubMedCentral McShane RH, Nagy Z, Esiri MM, King E, Joachim C, Sullivan N, Smith AD: Anosmia in dementia is associated with Lewy bodies rather than Alzheimer's pathology. J Neurol Neurosurg Psychiatry. 2001, 70 (6): 739-743. 10.1136/jnnp.70.6.739.CrossRefPubMedPubMedCentral
10.
go back to reference Peters JM, Hummel T, Kratzsch T, Lotsch J, Skarke C, Frolich L: Olfactory function in mild cognitive impairment and Alzheimer's disease: an investigation using psychophysical and electrophysiological techniques. Am J Psychiatry. 2003, 160 (11): 1995-2002. 10.1176/appi.ajp.160.11.1995.CrossRefPubMed Peters JM, Hummel T, Kratzsch T, Lotsch J, Skarke C, Frolich L: Olfactory function in mild cognitive impairment and Alzheimer's disease: an investigation using psychophysical and electrophysiological techniques. Am J Psychiatry. 2003, 160 (11): 1995-2002. 10.1176/appi.ajp.160.11.1995.CrossRefPubMed
11.
go back to reference Kjelvik G, Evensmoen HR, Brezova V, Haberg AK: The human brain representation of odor identification. J Neurophysiol. 2012, 108 (2): 645-57. 10.1152/jn.01036.2010.CrossRefPubMed Kjelvik G, Evensmoen HR, Brezova V, Haberg AK: The human brain representation of odor identification. J Neurophysiol. 2012, 108 (2): 645-57. 10.1152/jn.01036.2010.CrossRefPubMed
12.
go back to reference Poellinger A, Thomas R, Lio P, Lee A, Makris N, Rosen BR, Kwong KK: Activation and habituation in olfaction-an fMRI study. Neuroimage. 2001, 13 (4): 547-560. 10.1006/nimg.2000.0713.CrossRefPubMed Poellinger A, Thomas R, Lio P, Lee A, Makris N, Rosen BR, Kwong KK: Activation and habituation in olfaction-an fMRI study. Neuroimage. 2001, 13 (4): 547-560. 10.1006/nimg.2000.0713.CrossRefPubMed
13.
go back to reference Savic I, Gulyas B, Larsson M, Roland P: Olfactory functions are mediated by parallel and hierarchical processing. Neuron. 2000, 26 (3): 735-745. 10.1016/S0896-6273(00)81209-X.CrossRefPubMed Savic I, Gulyas B, Larsson M, Roland P: Olfactory functions are mediated by parallel and hierarchical processing. Neuron. 2000, 26 (3): 735-745. 10.1016/S0896-6273(00)81209-X.CrossRefPubMed
14.
go back to reference Suzuki Y, Critchley HD, Suckling J, Fukuda R, Williams SC, Andrew C, Howard R, Ouldred E, Bryant C, Swift CG, Jackson SH: Functional magnetic resonance imaging of odor identification: the effect of aging. J Gerontol A Biol Sci Med Sci. 2001, 56 (12): M756-M760. 10.1093/gerona/56.12.M756.CrossRefPubMed Suzuki Y, Critchley HD, Suckling J, Fukuda R, Williams SC, Andrew C, Howard R, Ouldred E, Bryant C, Swift CG, Jackson SH: Functional magnetic resonance imaging of odor identification: the effect of aging. J Gerontol A Biol Sci Med Sci. 2001, 56 (12): M756-M760. 10.1093/gerona/56.12.M756.CrossRefPubMed
15.
go back to reference Wang J, Eslinger PJ, Smith MB, Yang QX: Functional magnetic resonance imaging study of human olfaction and normal aging. J Gerontol A Biol Sci Med Sci. 2005, 60 (4): 510-514. 10.1093/gerona/60.4.510.CrossRefPubMed Wang J, Eslinger PJ, Smith MB, Yang QX: Functional magnetic resonance imaging study of human olfaction and normal aging. J Gerontol A Biol Sci Med Sci. 2005, 60 (4): 510-514. 10.1093/gerona/60.4.510.CrossRefPubMed
16.
go back to reference Wilson RS, Arnold SE, Schneider JA, Tang Y, Bennett DA: The relationship between cerebral Alzheimer's disease pathology and odour identification in old age. J Neurol Neurosurg Psychiatry. 2007, 78 (1): 30-35. 10.1136/jnnp.2006.099721.CrossRefPubMed Wilson RS, Arnold SE, Schneider JA, Tang Y, Bennett DA: The relationship between cerebral Alzheimer's disease pathology and odour identification in old age. J Neurol Neurosurg Psychiatry. 2007, 78 (1): 30-35. 10.1136/jnnp.2006.099721.CrossRefPubMed
17.
go back to reference 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 function, and volume loss of medial temporal lobe structures in patients with mild cognitive impairment. Curr Alzheimer Res. 2011, 8 (6): 689-98. 10.2174/156720511796717212.CrossRefPubMed 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 function, and volume loss of medial temporal lobe structures in patients with mild cognitive impairment. Curr Alzheimer Res. 2011, 8 (6): 689-98. 10.2174/156720511796717212.CrossRefPubMed
18.
go back to reference Murphy C, Jernigan TL, Fennema-Notestine C: Left hippocampal volume loss in Alzheimer's disease is reflected in performance on odor identification: a structural MRI study. J Int Neuropsychol Soc. 2003, 9 (3): 459-471. 10.1017/S1355617703930116.CrossRefPubMed Murphy C, Jernigan TL, Fennema-Notestine C: Left hippocampal volume loss in Alzheimer's disease is reflected in performance on odor identification: a structural MRI study. J Int Neuropsychol Soc. 2003, 9 (3): 459-471. 10.1017/S1355617703930116.CrossRefPubMed
19.
go back to reference Velayudhan L, Proitsi P, Westman E, Muehlboeck JS, Mecocci P, Vellas B, Tsolaki M, Kłoszewska I, Soininen H, Spenger C, Hodges A, Powell J, Lovestone S, Simmons A: Entorhinal cortex thickness predicts cognitive decline in Alzheimer's disease. J Alzheimers Dis. 2013, 33 (3): 755-766.PubMed Velayudhan L, Proitsi P, Westman E, Muehlboeck JS, Mecocci P, Vellas B, Tsolaki M, Kłoszewska I, Soininen H, Spenger C, Hodges A, Powell J, Lovestone S, Simmons A: Entorhinal cortex thickness predicts cognitive decline in Alzheimer's disease. J Alzheimers Dis. 2013, 33 (3): 755-766.PubMed
20.
go back to reference Struble RG, Clark HB: Olfactory bulb lesions in Alzheimer's disease. Neurobiol Aging. 1992, 13 (4): 469-473. 10.1016/0197-4580(92)90074-8.CrossRefPubMed Struble RG, Clark HB: Olfactory bulb lesions in Alzheimer's disease. Neurobiol Aging. 1992, 13 (4): 469-473. 10.1016/0197-4580(92)90074-8.CrossRefPubMed
21.
go back to reference Larsson M, Nilsson LG, Olofsson JK, Nordin S: Demographic and cognitive predictors of cued odor identification: evidence from a population-based study. Chem Senses. 2004, 29 (6): 547-554. 10.1093/chemse/bjh059.CrossRefPubMed Larsson M, Nilsson LG, Olofsson JK, Nordin S: Demographic and cognitive predictors of cued odor identification: evidence from a population-based study. Chem Senses. 2004, 29 (6): 547-554. 10.1093/chemse/bjh059.CrossRefPubMed
22.
go back to reference Wilson RS, Arnold SE, Tang Y, Bennett DA: Odor identification and decline in different cognitive domains in old age. Neuroepidemiology. 2006, 26 (2): 61-67. 10.1159/000090250.CrossRefPubMed Wilson RS, Arnold SE, Tang Y, Bennett DA: Odor identification and decline in different cognitive domains in old age. Neuroepidemiology. 2006, 26 (2): 61-67. 10.1159/000090250.CrossRefPubMed
23.
go back to reference Westervelt HJ, Ruffolo JS, Tremont G: Assessing olfaction in the neuropsychological exam: the relationship between odor identification and cognition in older adults. Arch Clin Neuropsychol. 2005, 20 (6): 761-769. 10.1016/j.acn.2005.04.010.CrossRefPubMed Westervelt HJ, Ruffolo JS, Tremont G: Assessing olfaction in the neuropsychological exam: the relationship between odor identification and cognition in older adults. Arch Clin Neuropsychol. 2005, 20 (6): 761-769. 10.1016/j.acn.2005.04.010.CrossRefPubMed
24.
go back to reference Conti MZ, Vicini-Chilovi B, Riva M, Zanetti M, Liberini P, Padovani A, Rozzini L: Odor identification deficit predicts clinical conversion from mild cognitive impairment to dementia due to Alzheimer's disease. Arch Clin Neuropsychol. 2013, 28 (5): 391-399. 10.1093/arclin/act032.CrossRefPubMed Conti MZ, Vicini-Chilovi B, Riva M, Zanetti M, Liberini P, Padovani A, Rozzini L: Odor identification deficit predicts clinical conversion from mild cognitive impairment to dementia due to Alzheimer's disease. Arch Clin Neuropsychol. 2013, 28 (5): 391-399. 10.1093/arclin/act032.CrossRefPubMed
25.
go back to reference Devanand DP, Liu X, Tabert MH, Pradhaban G, Cuasay K, Bell K, de Leon MJ, Doty RL, Stern Y, Pelton GH: Combining early markers strongly predicts conversion from mild cognitive impairment to Alzheimer's disease. Biol Psychiatry. 2008, 64 (10): 871-879. 10.1016/j.biopsych.2008.06.020.CrossRefPubMedPubMedCentral Devanand DP, Liu X, Tabert MH, Pradhaban G, Cuasay K, Bell K, de Leon MJ, Doty RL, Stern Y, Pelton GH: Combining early markers strongly predicts conversion from mild cognitive impairment to Alzheimer's disease. Biol Psychiatry. 2008, 64 (10): 871-879. 10.1016/j.biopsych.2008.06.020.CrossRefPubMedPubMedCentral
26.
go back to reference Waldemar G, Dubois B, Emre M, Georges J, McKeith IG, Rossor M, Scheltens P, Tariska P, Winblad B: Recommendations for the diagnosis and management of Alzheimer's disease and other disorders associated with dementia: EFNS guideline. Eur J Neurol. 2007, 14 (1): E1-E26. 10.1111/j.1468-1331.2006.01605.x.CrossRefPubMed Waldemar G, Dubois B, Emre M, Georges J, McKeith IG, Rossor M, Scheltens P, Tariska P, Winblad B: Recommendations for the diagnosis and management of Alzheimer's disease and other disorders associated with dementia: EFNS guideline. Eur J Neurol. 2007, 14 (1): E1-E26. 10.1111/j.1468-1331.2006.01605.x.CrossRefPubMed
27.
go back to reference McKhann G, Drachman D, Folstein M, Katzman R, Price D, Stadlan EM: 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. 10.1212/WNL.34.7.939.CrossRefPubMed McKhann G, Drachman D, Folstein M, Katzman R, Price D, Stadlan EM: 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. 10.1212/WNL.34.7.939.CrossRefPubMed
28.
go back to reference Winblad B, Palmer K, Kivipelto M, Jelic V, Fratiglioni L, Wahlund LO, Nordberg A, Bäckman L, Albert M, Almkvist O, Arai H, Basun H, Blennow K, de Leon M, DeCarli C, Erkinjuntti T, Giacobini E, Graff C, Hardy J, Jack C, Jorm A, Ritchie K, van Duijn C, Visser P, Petersen RC: Mild cognitive impairment-beyond controversies, towards a consensus: report of the International Working Group on Mild Cognitive Impairment. J Intern Med. 2004, 256 (3): 240-246. 10.1111/j.1365-2796.2004.01380.x.CrossRefPubMed Winblad B, Palmer K, Kivipelto M, Jelic V, Fratiglioni L, Wahlund LO, Nordberg A, Bäckman L, Albert M, Almkvist O, Arai H, Basun H, Blennow K, de Leon M, DeCarli C, Erkinjuntti T, Giacobini E, Graff C, Hardy J, Jack C, Jorm A, Ritchie K, van Duijn C, Visser P, Petersen RC: Mild cognitive impairment-beyond controversies, towards a consensus: report of the International Working Group on Mild Cognitive Impairment. J Intern Med. 2004, 256 (3): 240-246. 10.1111/j.1365-2796.2004.01380.x.CrossRefPubMed
29.
go back to reference Reitan RM: Validity of the Trail Making Test as an indication of organic brain damage. Percept Mot Skills. 1958, 8: 271-276. 10.2466/pms.1958.8.3.271.CrossRef Reitan RM: Validity of the Trail Making Test as an indication of organic brain damage. Percept Mot Skills. 1958, 8: 271-276. 10.2466/pms.1958.8.3.271.CrossRef
30.
go back to reference Watanabe K, Ogino T, Nakano K, Hattori J, Kado Y, Sanada S, Ohtsuka Y: The Rey-Osterrieth Complex Figure as a measure of executive function in childhood. Brain Dev. 2005, 27 (8): 564-569. 10.1016/j.braindev.2005.02.007.CrossRefPubMed Watanabe K, Ogino T, Nakano K, Hattori J, Kado Y, Sanada S, Ohtsuka Y: The Rey-Osterrieth Complex Figure as a measure of executive function in childhood. Brain Dev. 2005, 27 (8): 564-569. 10.1016/j.braindev.2005.02.007.CrossRefPubMed
31.
go back to reference Brewer JB: Fully-automated volumetric MRI with normative ranges: translation to clinical practice. Behav Neurol. 2009, 21 (1): 21-28. 10.1155/2009/616581.CrossRefPubMed Brewer JB: Fully-automated volumetric MRI with normative ranges: translation to clinical practice. Behav Neurol. 2009, 21 (1): 21-28. 10.1155/2009/616581.CrossRefPubMed
32.
go back to reference Brewer JB, Magda S, Airriess C, Smith ME: Fully-automated quantification of regional brain volumes for improved detection of focal atrophy in Alzheimer disease. AJNR Am J Neuroradiol. 2009, 30 (3): 578-580. 10.3174/ajnr.A1402.CrossRefPubMed Brewer JB, Magda S, Airriess C, Smith ME: Fully-automated quantification of regional brain volumes for improved detection of focal atrophy in Alzheimer disease. AJNR Am J Neuroradiol. 2009, 30 (3): 578-580. 10.3174/ajnr.A1402.CrossRefPubMed
33.
go back to reference Ross DE, Ochs AL, Seabaugh J, Henshaw T: NeuroQuant(R) revealed hippocampal atrophy in a patient with traumatic brain injury. J Neuropsychiatry Clin Neurosci. 2012, 24 (1): E33-10.1176/appi.neuropsych.11020044.CrossRefPubMed Ross DE, Ochs AL, Seabaugh J, Henshaw T: NeuroQuant(R) revealed hippocampal atrophy in a patient with traumatic brain injury. J Neuropsychiatry Clin Neurosci. 2012, 24 (1): E33-10.1176/appi.neuropsych.11020044.CrossRefPubMed
34.
go back to reference Braak H, Braak E: The human entorhinal cortex: normal morphology and lamina-specific pathology in various diseases. Neurosci Res. 1992, 15 (1-2): 6-31. 10.1016/0168-0102(92)90014-4.CrossRefPubMed Braak H, Braak E: The human entorhinal cortex: normal morphology and lamina-specific pathology in various diseases. Neurosci Res. 1992, 15 (1-2): 6-31. 10.1016/0168-0102(92)90014-4.CrossRefPubMed
35.
go back to reference Velayudhan L, Pritchard M, Powell JF, Proitsi P, Lovestone S: Smell identification function as a severity and progression marker in Alzheimer's disease. Int Psychogeriatr. 2013, 25 (7): 1157-1166. 10.1017/S1041610213000446.CrossRefPubMed Velayudhan L, Pritchard M, Powell JF, Proitsi P, Lovestone S: Smell identification function as a severity and progression marker in Alzheimer's disease. Int Psychogeriatr. 2013, 25 (7): 1157-1166. 10.1017/S1041610213000446.CrossRefPubMed
36.
go back to reference Doty RL, Shaman P, Applebaum SL, Giberson R, Skisorski L, Rosenberg L: Smell identification ability: changes with age. Science. 1984, 226 (4681): 1441-1443. 10.1126/science.6505700.CrossRefPubMed Doty RL, Shaman P, Applebaum SL, Giberson R, Skisorski L, Rosenberg L: Smell identification ability: changes with age. Science. 1984, 226 (4681): 1441-1443. 10.1126/science.6505700.CrossRefPubMed
37.
go back to reference Murphy C, Schubert CR, Cruickshanks KJ, Klein BE, Klein R, Nondahl DM: Prevalence of olfactory impairment in older adults. JAMA. 2002, 288 (18): 2307-2312. 10.1001/jama.288.18.2307.CrossRefPubMed Murphy C, Schubert CR, Cruickshanks KJ, Klein BE, Klein R, Nondahl DM: Prevalence of olfactory impairment in older adults. JAMA. 2002, 288 (18): 2307-2312. 10.1001/jama.288.18.2307.CrossRefPubMed
38.
go back to reference Morris JC, Blennow K, Froelich L, Nordberg A, Soininen H, Waldemar G, Wahlund LO, Dubois B: Harmonized diagnostic criteria for Alzheimer's disease: recommendations. J Intern Med. 2014, 275 (3): 204-213. 10.1111/joim.12199.CrossRefPubMed Morris JC, Blennow K, Froelich L, Nordberg A, Soininen H, Waldemar G, Wahlund LO, Dubois B: Harmonized diagnostic criteria for Alzheimer's disease: recommendations. J Intern Med. 2014, 275 (3): 204-213. 10.1111/joim.12199.CrossRefPubMed
Metadata
Title
The brain structural and cognitive basis of odor identification deficits in mild cognitive impairment and Alzheimer's disease
Authors
Grete Kjelvik
Ingvild Saltvedt
Linda R White
Pål Stenumgård
Olav Sletvold
Knut Engedal
Kristina Skåtun
Ann Kristin Lyngvær
Hill Aina Steffenach
Asta K Håberg
Publication date
01-12-2014
Publisher
BioMed Central
Published in
BMC Neurology / Issue 1/2014
Electronic ISSN: 1471-2377
DOI
https://doi.org/10.1186/s12883-014-0168-1

Other articles of this Issue 1/2014

BMC Neurology 1/2014 Go to the issue