Increased Prevalence of Vestibular Loss in Mild Cognitive Impairment and Alzheimer’s Disease

Page: [1143 - 1150] Pages: 8

  • * (Excluding Mailing and Handling)

Abstract

Background/Aims: Recent evidence has shown that Alzheimer’s Disease (AD) patients have reduced vestibular function relative to healthy controls. In this study, we evaluated whether patients with Mild Cognitive Impairment (MCI) also have reduced vestibular function relative to controls, and compared the level of vestibular impairment between MCI and AD patients.

Methods: Vestibular physiologic function was assessed in 77 patients (26 MCI, 51 AD) and 295 matched controls using 3 clinical vestibular tests. The association between vestibular loss and cognitive impairment was evaluated using conditional logistic regression models.

Results: Individuals with vestibular impairment had a 3 to 4-fold increased odds of being in the MCI vs. control group (p-values < 0.05). MCI patients had a level of vestibular impairment that was intermediate between controls and AD.

Conclusion: These findings suggest a dose-response relationship between vestibular loss and cognitive status, and support the hypothesis that vestibular loss contributes to cognitive decline.

Keywords: Alzheimer's disease, mild cognitive impairment, vestibular system, vestibular function tests, aging.

[1]
Bigelow RT, Semenov YR, Trevino C, Ferrucci L, Resnick SM, Simonsick EM, et al. Association between visuospatial ability and vestibular function in the Baltimore Longitudinal Study of Aging. J Am Geriatr Soc 63(9): 1837-44. (2015).
[http://dx.doi.org/10.1111/jgs.13609] [PMID: 26311169]
[2]
Popp P, Wulff M, Finke K, Rühl M, Brandt T, Dieterich M. Cognitive deficits in patients with a chronic vestibular failure. J Neurol 264(3): 554-63. (2017).
[http://dx.doi.org/10.1007/s00415-016-8386-7] [PMID: 28074268]
[3]
Kremmyda O, Hüfner K, Flanagin VL, Hamilton DA, Linn J, Strupp M, et al. Beyond dizziness: virtual navigation, spatial anxiety and hippocampal volume in bilateral vestibulopathy. Front Hum Neurosci 10: 139. (2016).
[http://dx.doi.org/10.3389/fnhum.2016.00139] [PMID: 27065838]
[4]
Xie Y, Bigelow RT, Frankenthaler SF, Studenski SA, Moffat SD, Agrawal Y. Vestibular loss in older adults is associated with impaired spatial navigation: data from the triangle completion task. Front Neurol 8: 173. (2017).
[http://dx.doi.org/10.3389/fneur.2017.00173] [PMID: 28496432]
[5]
Glasauer S, Amorim M-A, Viaud-Delmon I, Berthoz A. Differential effects of labyrinthine dysfunction on distance and direction during blindfolded walking of a triangular path. Exp Brain Res 145(4): 489-97. (2002).
[http://dx.doi.org/10.1007/s00221-002-1146-1] [PMID: 12172660]
[6]
Smith PF. The vestibular system and cognition. Curr Opin Neurol 30(1): 84-9. (2017).
[http://dx.doi.org/10.1097/WCO.0000000000000403] [PMID: 27845944]
[7]
Hitier M, Besnard S, Smith PF. Vestibular pathways involved in cognition. Front Integr Nuerosci 8: 59. (2014).
[http://dx.doi.org/10.3389/fnint.2014.00059] [PMID: 25100954]
[8]
Aitken P, Benoit A, Zheng Y, Philoxene B, Le Gall A, Denise P, et al. Hippocampal and striatal M1 -muscarinic acetylcholine receptors are down-regulated following bilateral vestibular loss in rats. Hippocampus 26(12): 1509-14. (2016).
[http://dx.doi.org/10.1002/hipo.22651] [PMID: 27569857]
[9]
Stackman RW, Clark AS, Taube JS. Hippocampal spatial representations require vestibular input. Hippocampus 12(3): 291-303. (2002).
[http://dx.doi.org/10.1002/hipo.1112] [PMID: 12099481]
[10]
Russell NA, Horii A, Smith PF, Darlington CL, Bilkey DK. Long-term effects of permanent vestibular lesions on hippocampal spatial firing. J Neurosci 23: 6490-8. (2003).
[11]
Russell NA, Horii A, Smith PF, Darlington CL, Bilkey DK. Lesions of the vestibular system disrupt hippocampal theta rhythm in the rat. J Neurophysiol 96(1): 4-14. (2006).
[http://dx.doi.org/10.1152/jn.00953.2005] [PMID: 16772515]
[12]
Harun A, Oh ES, Bigelow RT, Studenski S, Agrawal Y. Vestibular impairment in dementia. Otol Neurotol 37(8): 1137-42. (2016).
[http://dx.doi.org/10.1097/MAO.0000000000001157] [PMID: 27466890]
[13]
Cummings JL. Cognitive and behavioral heterogeneity in Alzheimer’s disease: seeking the neurobiological basis. Neurobiol Aging 21(6): 845-61. (2000).
[http://dx.doi.org/10.1016/S0197-4580(00)00183-4] [PMID: 11124429]
[14]
Grady CL, Haxby JV, Horwitz B, Sundaram M, Berg G, Schapiro M, et al. Longitudinal study of the early neuropsychological and cerebral metabolic changes in dementia of the Alzheimer type. J Clin Exp Neuropsychol 10(5): 576-96. (1988).
[http://dx.doi.org/10.1080/01688638808402796] [PMID: 3265710]
[15]
Chase TN, Fedio P, Foster NL, Brooks R, Di Chiro G, Mansi L. Wechsler adult intelligence scale performance. cortical localization by fluorodeoxyglucose F 18-positron emission tomography. Arch Neurol 41(12): 1244-7. (1984).
[http://dx.doi.org/10.1001/archneur.1984.04050230026012] [PMID: 6333862]
[16]
Wei EX, Oh ES, Harun A, Ehrenburg M, Agrawal Y. Vestibular loss predicts poorer spatial cognition in patients with Alzheimer’s disease. J Alzheimers Dis 61(3): 995-1003. (2018).
[http://dx.doi.org/10.3233/JAD-170751] [PMID: 29254098]
[17]
Roberts R, Knopman DS. Classification and epidemiology of MCI. Clin Geriatr Med 29(4): 753-72. (2013).
[http://dx.doi.org/10.1016/j.cger.2013.07.003] [PMID: 24094295]
[18]
Winblad B, Palmer K, Kivipelto M, Jelic V, Fratiglioni L, Wahlund LO, et al. Mild cognitive impairment--beyond controversies, towards a consensus: report of the International Working Group on Mild Cognitive Impairment. J Intern Med 256(3): 240-6. (2004).
[http://dx.doi.org/10.1111/j.1365-2796.2004.01380.x] [PMID: 15324367]
[19]
2017 Alzheimer’s Disease Facts and Figures. Alzheimers Dement 13: 325-73. (2017).
[http://dx.doi.org/10.1016/j.jalz.2017.02.001]
[20]
Ward A, Tardiff S, Dye C, Arrighi HM. Rate of conversion from prodromal Alzheimer’s disease to Alzheimer’s dementia: a systematic review of the literature. Dement Geriatr Cogn Disord Extra 3(1): 320-32. (2013).
[http://dx.doi.org/10.1159/000354370] [PMID: 24174927]
[21]
Langa KM, Levine DA. The diagnosis and management of mild cognitive impairment: a clinical review. JAMA 312(23): 2551-61. (2014).
[http://dx.doi.org/10.1001/jama.2014.13806] [PMID: 25514304]
[22]
Mukherjee B, Liu I, Sinha S. Analysis of matched case-control data with multiple ordered disease states: possible choices and comparisons. Stat Med 26(17): 3240-57. (2007).
[http://dx.doi.org/10.1002/sim.2790] [PMID: 17206600]
[23]
McKhann GM, Knopman DS, Chertkow H, Hyman BT, Jack CR Jr, Kawas CH, 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. Alzheimers Dement 7(3): 263-9. (2011).
[http://dx.doi.org/10.1016/j.jalz.2011.03.005] [PMID: 21514250]
[24]
Albert MS, DeKosky ST, Dickson D, Dubois B, Feldman HH, Fox NC, et al. The diagnosis of mild cognitive impairment 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 7(3): 270-9. (2011).
[http://dx.doi.org/10.1016/j.jalz.2011.03.008] [PMID: 21514249]
[25]
Li C, Layman AJ, Carey JP, Agrawal Y. Epidemiology of vestibular evoked myogenic potentials: data from the baltimore longitudinal study of aging. Clin Neurophysiol 126(11): 2207-15. (2015).
[http://dx.doi.org/10.1016/j.clinph.2015.01.008] [PMID: 25703943]
[26]
Li C, Zuniga MG, Nguyen KD, Carey JP, Agrawal Y. How to interpret latencies of cervical and ocular vestibular-evoked myogenic potentials: our experience in fifty-three participants. Clin Otolaryngol 39(5): 297-301. (2014).
[http://dx.doi.org/10.1111/coa.12277] [PMID: 24962335]
[27]
Nguyen KD, Welgampola MS, Carey JP. Test-retest reliability and age-related characteristics of the ocular and cervical vestibular evoked myogenic potential tests. Otol Neurotol 31(5): 793-802. (2010).
[http://dx.doi.org/10.1097/MAO.0b013e3181e3d60e] [PMID: 20517167]
[28]
Bartl K, Lehnen N, Kohlbecher S, Schneider E. Head impulse testing using video-oculography Ann NY Acad Sci 1164, Blackwell Publishing Inc; 331-3 (2009).
[http://dx.doi.org/10.1111/j.1749-6632.2009.03850.x]
[29]
MacDougall HG, Weber KP, McGarvie LA, Halmagyi GM, Curthoys IS. The video head impulse test: diagnostic accuracy in peripheral vestibulopathy. Neurology 73(14): 1134-41. (2009).
[http://dx.doi.org/10.1212/WNL.0b013e3181bacf85] [PMID: 19805730]
[30]
Agrawal Y, Schubert MC, Migliaccio AA, Zee DS, Schneider E, Lehnen N, et al. Evaluation of quantitative head impulse testing using search coils versus video-oculography in older individuals. Otol Neurotol 35(2): 283-8. (2014).
[http://dx.doi.org/10.1097/MAO.0b013e3182995227] [PMID: 24080977]
[31]
Schneider E, Villgrattner T, Vockeroth J, Bartl K, Kohlbecher S, Bardins S, et al. Eyeseecam: an eye movement-driven head camera for the examination of natural visual exploration Ann N Y Acad Sci, vol 1164, Blackwell Publishing Inc 461-7 (2009).
[32]
Alzheimer’s Association. Alzheimer’s disease facts and figures includes a special report on Alzheimer’s detection in the primary care setting: connecting patients and physicians (2019).
[33]
Kelley BJ, Petersen RC. Alzheimer’s disease and mild cognitive impairment. Neurol Clin 25: 577-609. (2007).
[http://dx.doi.org/10.1016/j.ncl.2007.03.008]
[34]
Petersen RC, Stevens JC, Ganguli M, Tangalos EG, Cummings JL, DeKosky ST. Practice parameter: early detection of dementia: mild cognitive impairment (an evidence-based review). Report of the Quality Standards Subcommittee of the American Academy of Neurology. Neurology 56(9): 1133-42. (2001).
[http://dx.doi.org/10.1212/WNL.56.9.1133] [PMID: 11342677]
[35]
Leandri M, Cammisuli S, Cammarata S, Baratto L, Campbell J, Simonini M, et al. Balance features in Alzheimer’s disease and amnestic mild cognitive impairment. J Alzheimers Dis 16(1): 113-20. (2009).
[http://dx.doi.org/10.3233/JAD-2009-0928] [PMID: 19158427]
[36]
Franssen EH, Souren LE, Torossian CL, Reisberg B. Equilibrium and limb coordination in mild cognitive impairment and mild Alzheimer’s disease. J Am Geriatr Soc 47(4): 463-9. (1999). [In Process Citation]
[http://dx.doi.org/10.1111/j.1532-5415.1999.tb07240.x] [PMID: 10203123]
[37]
Semenov YR, Bigelow RT, Xue Q-L, du Lac S, Agrawal Y. Association between vestibular and cognitive function in U.S. adults: data from the National Health and Nutrition Examination Survey. J Gerontol A Biol Sci Med Sci 71(2): 243-50. (2016).
[http://dx.doi.org/10.1093/gerona/glv069] [PMID: 26219850]
[38]
Vitte E, Derosier C, Caritu Y, Berthoz A, Hasboun D, Soulié D. Activation of the hippocampal formation by vestibular stimulation: a functional magnetic resonance imaging study. Exp Brain Res 112(3): 523-6. (1996).
[http://dx.doi.org/10.1007/BF00227958] [PMID: 9007554]
[39]
Dieterich M, Bense S, Stephan T, Yousry TA, Brandt T. fMRI signal increases and decreases in cortical areas during small-field optokinetic stimulation and central fixation. Exp Brain Res 148(1): 117-27. (2003).
[http://dx.doi.org/10.1007/s00221-002-1267-6] [PMID: 12478402]
[40]
Brandt T, Schautzer F, Hamilton DA, Brüning R, Markowitsch HJ, Kalla R, et al. Vestibular loss causes hippocampal atrophy and impaired spatial memory in humans. Brain 128(Pt 11): 2732-41. (2005).
[http://dx.doi.org/10.1093/brain/awh617] [PMID: 16141283]
[41]
Seo YJ, Kim J, Kim SH. The change of hippocampal volume and its relevance with inner ear function in Meniere’s disease patients. Auris Nasus Larynx 43(6): 620-5. (2016).
[http://dx.doi.org/10.1016/j.anl.2016.01.006] [PMID: 26856304]
[42]
Rüb U, Stratmann K, Heinsen H, Turco DD, Seidel K. Dunnen Wd, et al. The brainstem tau cytoskeletal pathology of Alzheimer’s disease: a brief historical overview and description of its anatomical distribution pattern, evolutional features, pathogenetic and clinical relevance. Curr Alzheimer Res 13(10): 1178-97. (2016).
[http://dx.doi.org/10.2174/1567205013666160606100509] [PMID: 27264543]
[43]
Hashimoto M, Ho G, Shimizu Y, Sugama S, Takenouchi T, Waragai M, et al. Potential application of centrifuges to protect the cns in space and on earth. Curr Alzheimer Res 15(6): 544-51. (2018).
[http://dx.doi.org/10.2174/1567205015666171229225501] [PMID: 29298650]
[44]
Wei EX, Oh ES, Harun A, Ehrenburg M, Agrawal Y. Saccular impairment in Azheimer’s disease is associated with driving difficulty. Dement Geriatr Cogn Disord 44(5-6): 294-302. (2017).
[http://dx.doi.org/10.1159/000485123] [PMID: 29393172]
[45]
Previc FH. Vestibular loss as a contributor to Alzheimer’s disease. Med Hypotheses 80(4): 360-7. (2013).
[http://dx.doi.org/10.1016/j.mehy.2012.12.023] [PMID: 23375669]
[46]
Johnson DK, Storandt M, Morris JC, Galvin JE. Longitudinal study of the transition from healthy aging to Alzheimer disease. Arch Neurol 66(10): 1254-9. (2009).
[http://dx.doi.org/10.1001/archneurol.2009.158] [PMID: 19822781]
[47]
Walther LE, Blödow A. Ocular vestibular evoked myogenic potential to air conducted sound stimulation and video head impulse test in acute vestibular neuritis. Otol Neurotol 34(6): 1084-9. (2013).
[http://dx.doi.org/10.1097/MAO.0b013e318280da47] [PMID: 23370570]
[48]
Taylor RL, Kong J, Flanagan S, Pogson J, Croxson G, Pohl D, et al. Prevalence of vestibular dysfunction in patients with vestibular schwannoma using video head-impulses and vestibular-evoked potentials. J Neurol 262(5): 1228-37. (2015).
[http://dx.doi.org/10.1007/s00415-015-7697-4] [PMID: 25794859]
[49]
Manzari L, Burgess AM, MacDougall HG, Curthoys IS. Superior canal dehiscence reveals concomitant unilateral utricular loss (UUL). Acta Otolaryngol 135(6): 557-64. (2015).
[http://dx.doi.org/10.3109/00016489.2014.999877] [PMID: 25719967]
[50]
Manzari L, Macdougall HG, Burgess AM, Curthoys IS. Selective otolith dysfunctions objectively verified J Vestib Res Equilib Orientat vol 24, IOS Press. 365-73. (2014).
[51]
Skorić MK, Adamec I, Pavičić T, Pavlović I, Ruška B, Crnošija L, et al. Vestibular evoked myogenic potentials and video head impulse test in patients with vertigo, dizziness and imbalance. J Clin Neurosci 39: 216-20. (2017).
[http://dx.doi.org/10.1016/j.jocn.2017.02.009] [PMID: 28242131]
[52]
Kalkan M, Bayram A, Gökay F, Cura HS, Mutlu C. Assessment of vestibular-evoked myogenic potentials and video head impulse test in type 2 diabetes mellitus patients with or without polyneuropathy. Eur Arch Otorhinolaryngol 275(3): 719-24. (2018).
[http://dx.doi.org/10.1007/s00405-018-4873-z] [PMID: 29330601]