Rapid eye movement sleep disruption and sleep fragmentation are associated with increased orexin-A cerebrospinal-fluid levels in mild cognitive impairment due to Alzheimer's disease

Neurobiology of Aging

Volumn 40, Issue , 2016, Pages 120-126

  Liguori, Claudio ^a   Nuccetelli, Marzia ^a   Izzi, Francesca ^a   Sancesario, Giuseppe ^a,b   Romigi, Andrea ^a   Martorana, Alessandro ^a   Amoroso, Chiara ^a   Bernardini, Sergio ^a   Marciani, Maria Grazia ^a   Mercuri, Nicola Biagio ^a,b   Placidi, Fabio ^a  

^a UNIVERSITY OF ROME TOR VERGATA   (Italy)

^b IRCCS FONDAZIONE SANTA LUCIA   (Italy)

Author keywords

Mild cognitive impairment due to Alzheimer's disease; Orexin; Polysomnography; REM sleep disruption; Subjective sleep disturbances

Indexed keywords

OREXIN A; BIOLOGICAL MARKER; OREXIN;

AGED; ALZHEIMER DISEASE; ARTICLE; CLINICAL ARTICLE; CONTROLLED STUDY; DISEASE ASSOCIATION; FEMALE; HUMAN; LATENT PERIOD; MALE; MILD COGNITIVE IMPAIRMENT; OREXIN A CEREBROSPINAL FLUID LEVEL; PARASOMNIA; PITTSBURGH SLEEP QUALITY INDEX; POLYSOMNOGRAPHY; PRIORITY JOURNAL; PROTEIN CEREBROSPINAL FLUID LEVEL; PROTEIN DETERMINATION; QUESTIONNAIRE; SCORING SYSTEM; SLEEP PARAMETERS; SLEEP PATTERN; SLEEP TIME; SLEEP WAKING CYCLE; CEREBROSPINAL FLUID; COGNITIVE DYSFUNCTION; COMPLICATION; REM SLEEP; SLEEP DEPRIVATION; SLEEP WAKE DISORDERS;

AGED; ALZHEIMER DISEASE; BIOMARKERS; COGNITIVE DYSFUNCTION; FEMALE; HUMANS; MALE; OREXINS; POLYSOMNOGRAPHY; SLEEP DEPRIVATION; SLEEP WAKE DISORDERS; SLEEP, REM;

EID: 84960408192     PISSN: 01974580     EISSN: 15581497     Source Type: Journal    
DOI: 10.1016/j.neurobiolaging.2016.01.007     Document Type: Article

References (56)

1. Albert M.S., DeKosky S.T., Dickson D., Dubois B., Feldman H.H., Fox N.C., Gamst A., Holtzman D.M., Jagust W.J., Petersen R.C., Snyder P.J., Carrillo M.C., Thies B., Phelps C.H. 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. 2011, 7:270-279.
2. Beaulieu-Bonneau S., Hudon C. Sleep disturbances in older adults with mild cognitive impairment. Int. Psychogeriatr. 2009, 21:654-666.
3. Boeve B.F. Mild cognitive impairment associated with underlying Alzheimer's disease versus Lewy body disease. Parkinsonism Relat. Disord. 2012, 18(Suppl 1):S41-S44.
4. Bonanni E., Maestri M., Tognoni G., Fabbrini M., Nucciarone B., Manca M.L., Gori S., Iudice A., Murri L. Daytime sleepiness in mild and moderate Alzheimer's disease and its relationship with cognitive impairment. J. Sleep Res. 2005, 14:311-317.
5. Busse A., Angermeyer M.C., Riedel-Heller S.G. Progression of mild cognitive impairment to dementia: a challenge to current thinking. Br. J. Psychiatry 2006, 189:399-404.
6. Buysse D.J., Reynolds C.F., Monk T.H., Berman S.R., Kupfer D.J. The Pittsburgh Sleep Quality Index: a new instrument for psychiatric practice and research. Psychiatry Res. 1989, 28:193-213.
7. Carlesimo G.A., Caltagirone C., Gainotti G. The Mental Deterioration Battery: normative data, diagnostic reliability and qualitative analyses of cognitive impairment. The Group for the Standardization of the Mental Deterioration Battery. Eur. Neurol. 1996, 36:378-384.
8. Christos G.A. Is Alzheimer's disease related to a deficit or malfunction of rapid eye movement (REM) sleep?. Med. Hypotheses 1993, 41:435-439.
9. Dauvilliers Y.A., Lehmann S., Jaussent I., Gabelle A. Hypocretin and brain β-amyloid peptide interactions in cognitive disorders and narcolepsy. Front Aging Neurosci. 2014, 6:119.
10. Deuschle M., Schilling C., Leweke F.M., Enning F., Pollmächer T., Esselmann H., Wiltfang J., Frölich L., Heuser I. Hypocretin in cerebrospinal fluid is positively correlated with Tau and pTau. Neurosci. Lett. 2014, 561:41-45.
11. De Vos A., Jacobs D., Struyfs H., Fransen E., Andersson K., Portelius E., Andreasson U., De Surgeloose D., Hernalsteen D., Sleegers K., Robberecht C., VanBroeckhoven C., Zetterberg H., Blennow K., Engelborghs S., Vanmechelen E. C-terminal neurogranin is increased in cerebrospinal fluid but unchanged in plasma in Alzheimer's disease. Alzheimers Dement 2015, 11:1461-1469.
12. Dubois B., Feldman H.H., Jacova C., Hampel H., Molinuevo J.L., Blennow K., DeKosky S.T., Gauthier S., Selkoe D., Bateman R., Cappa S., Crutch S., Engelborghs S., Frisoni G.B., Fox N.C., Galasko D., Habert M.O., Jicha G.A., Nordberg A., Pasquier F., Rabinovici G., Robert P., Rowe C., Salloway S., Sarazin M., Epelbaum S., de Souza L.C., Vellas B., Visser P.J., Schneider L., Stern Y., Scheltens P., Cummings J.L. Advancing research diagnostic criteria for Alzheimer's disease: the IWG-2 criteria. Lancet Neurol. 2014, 13:614-629.
13. Ferman T.J., Boeve B.F., Smith G.E., Lin S.C., Silber M.H., Pedraza O., Wszolek Z., Graff-Radford N.R., Uitti R., Van Gerpen J., Pao W., Knopman D., Pankratz V.S., Kantarci K., Boot B., Parisi J.E., Dugger B.N., Fujishiro H., Petersen R.C., Dickson D.W. Inclusion of RBD improves the diagnostic classification of dementia with Lewy bodies. Neurology 2011, 77:875-882.
14. Fronczek R., Overeem S., Lee S.Y., Hegeman I.M., van Pelt J., van Duinen S.G., Lammers G.J., Swaab D.F. Hypocretin (orexin) loss and sleep disturbances in Parkinson's disease. Brain 2008, 131(Pt 1):e88.
15. Fronczek R., van Geest S., Frölich M., Overeem S., Roelandse F.W., Lammers G.J., Swaab D.F. Hypocretin (orexin) loss in Alzheimer's disease. Neurobiol. Aging 2012, 33:1642-1650.
16. Gerashchenko D., Murillo-Rodriguez E., Lin L., Xu M., Hallett L., Nishino S., Mignot E., Shiromani P.J. Relationship between CSF hypocretin levels and hypocretin neuronal loss. Exp. Neurol. 2003, 184:1010-1016.
17. Grothe M., Zaborszky L., Atienza M., Gil-Neciga E., Rodriguez-Romero R., Teipel S.J., Amunts K., Suarez-Gonzalez A., Cantero J.L. Reduction of basal forebrain cholinergic system parallels cognitive impairment in patients at high risk of developing Alzheimer's disease. Cereb. Cortex 2010, 20:1685-1695.
18. Guillozet A.L., Weintraub S., Mash D.C., Mesulam M.M. Neurofibrillary tangles, amyloid, and memory in aging and mild cognitive impairment. Arch. Neurol. 2003, 60:729-736.
19. Heister D., Brewer J.B., Magda S., Blennow K., McEvoy L.K. Alzheimer's Disease Neuroimaging Initiative, Predicting MCI outcome with clinically available MRI and CSF biomarkers. Neurology 2011, 77:1619-1628.
20. Hita-Yañez E., Atienza M., Cantero J.L. Polysomnographic and subjective sleep markers of mild cognitive impairment. Sleep 2013, 36:1327-1334.
21. Iber C., Ancoli-Israel S., Chesson A., Quan S. The AASM Manual for the Scoring of Sleep and Associated Events; Rules, Terminology and Technical Specifications 2007, for the American Academy of Sleep Medicine, American Academy of Sleep Medicine, Westchester, IL. first ed.
22. Jack C.R., Shiung M.M., Weigand S.D., O'Brien P.C., Gunter J.L., Boeve B.F., Knopman D.S., Smith G.E., Ivnik R.J., Tangalos E.G., Petersen R.C. Brain atrophy rates predict subsequent clinical conversion in normal elderly and amnestic MCI. Neurology 2005, 65:1227-1231.
23. Jack C.R., Weigand S.D., Shiung M.M., Przybelski S.A., O'Brien P.C., Gunter J.L., Knopman D.S., Boeve B.F., Smith G.E., Petersen R.C. Atrophy rates accelerate in amnestic mild cognitive impairment. Neurology 2008, 70(19 Pt 2):1740-1752.
24. Johansson P., Almqvist E.G., Wallin A., Johansson J.O., Andreasson U., Blennow K., Zetterberg H., Svensson J. Cerebrospinal fluid substance P concentrations are elevated in patients with Alzheimer's disease. Neurosci. Lett. 2015, 609:58-62.
25. Johnson K.A., Sperling R.A., Gidicsin C.M., Carmasin J.S., Maye J.E., Coleman R.E., Reiman E.M., Sabbagh M.N., Sadowsky C.H., Fleisher A.S., Murali Doraiswamy P., Carpenter A.P., Clark C.M., Joshi A.D., Lu M., Grundman M., Mintun M.A., Pontecorvo M.J., Skovronsky D.M. AV45-A11 study group, Florbetapir (F18-AV-45) PET to assess amyloid burden in Alzheimer's disease dementia, mild cognitive impairment, and normal aging. Alzheimers Dement. 2013, 9(5 Suppl):S72-S83.
26. Ju Y.E., McLeland J.S., Toedebusch C.D., Xiong C., Fagan A.M., Duntley S.P., Morris J.C., Holtzman D.M. Sleep quality and preclinical Alzheimer disease. JAMA Neurol. 2013, 70:587-593.
27. Kang J.E., Lim M.M., Bateman R.J., Lee J.J., Smyth L.P., Cirrito J.R., Fujiki N., Nishino S., Holtzman D.M. Amyloid-beta dynamics are regulated by orexin and the sleep-wake cycle. Science 2009, 326:1005-1007.
28. Kundermann B., Thum A., Rocamora R., Haag A., Krieg J.C., Hemmeter U. Comparison of polysomnographic variables and their relationship to cognitive impairment in patients with Alzheimer's disease and frontotemporal dementia. J. Psychiatr. Res. 2011, 45:1585-1592.
29. Liguori C., Placidi F., Albanese M., Nuccetelli M., Izzi F., Marciani M.G., Mercuri N.B., Bernardini S., Romigi A. CSF beta-amyloid levels are altered in narcolepsy: a link with the inflammatory hypothesis?. J. Sleep Res. 2014, 23:420-424.
30. Liguori C., Romigi A., Mercuri N.B., Nuccetelli M., Izzi F., Albanese M., Sancesario G., Martorana A., Sancesario G.M., Bernardini S., Marciani M.G., Placidi F. Cerebrospinal-fluid orexin levels and daytime somnolence in frontotemporal dementia. J. Neurol. 2014, 261:1832-1836.
31. Liguori C., Romigi A., Nuccetelli M., Zannino S., Sancesario G., Martorana A., Albanese M., Mercuri N.B., Izzi F., Bernardini S., Nitti A., Sancesario G.M., Sica F., Marciani M.G., Placidi F. Orexinergic system dysregulation, sleep impairment, and cognitive decline in alzheimer disease. JAMA Neurol. 2014, 71:1498-1505.
32. Maestri M., Carnicelli L., Tognoni G., Di Coscio E., Giorgi F.S., Volpi L., Economou N.T., Ktonas P., Ferri R., Bonuccelli U., Bonanni E. Non-rapid eye movement sleep instability in mild cognitive impairment: a pilot study. Sleep Med. 2015, 16:1139-1145.
33. Mallick B.N., Joseph M.M. Role of cholinergic inputs to the medial preoptic area in regulation of sleep-wakefulness and body temperature in freely moving rats. Brain Res. 1997, 750:311-317.
34. Mander B.A., Marks S.M., Vogel J.W., Rao V., Lu B., Saletin J.M., Ancoli-Israel S., Jagust W.J., Walker M.P. β-amyloid disrupts human NREM slow waves and related hippocampus-dependent memory consolidation. Nat. Neurosci. 2015, 18:1051-1057.
35. McKeith I.G., Dickson D.W., Lowe J., Emre M., O'Brien J.T., Feldman H., Cummings J., Duda J.E., Lippa C., Perry E.K., Aarsland D., Arai H., Ballard C.G., Boeve B., Burn D.J., Costa D., Del Ser T., Dubois B., Galasko D., Gauthier S., Goetz C.G., Gomez-Tortosa E., Halliday G., Hansen L.A., Hardy J., Iwatsubo T., Kalaria R.N., Kaufer D., Kenny R.A., Korczyn A., Kosaka K., Lee V.M., Lees A., Litvan I., Londos E., Lopez O.L., Minoshima S., Mizuno Y., Molina J.A., Mukaetova-Ladinska E.B., Pasquier F., Perry R.H., Schulz J.B., Trojanowski J.Q., Yamada M. Consortium on DLB., Diagnosis and management of dementia with Lewy bodies: third report of the DLB consortium. Neurology 2005, 65:1863-1872.
36. Mieda M., Willie J.T., Hara J., Sinton C.M., Sakurai T., Yanagisawa M. Orexin peptides prevent cataplexy and improve wakefulness in an orexin neuron-ablated model of narcolepsy in mice. Proc. Natl. Acad. Sci. U. S. A. 2004, 101:4649-4654.
37. Montplaisir J., Petit D., Gauthier S., Gaudreau H., Décary A. Sleep disturbances and eeg slowing in alzheimer's disease. Sleep Res. Online 1998, 1:147-151.
38. Montplaisir J., Petit D., Lorrain D., Gauthier S., Nielsen T. Sleep in Alzheimer's disease: further considerations on the role of brainstem and forebrain cholinergic populations in sleep-wake mechanisms. Sleep 1995, 18:145-148.
39. Musiek E.S., Xiong D.D., Holtzman D.M. Sleep, circadian rhythms, and the pathogenesis of Alzheimer disease. Exp. Mol. Med. 2015, 47:e148.
40. Naismith S.L., Hickie I.B., Terpening Z., Rajaratnam S.M., Hodges J.R., Bolitho S., Rogers N.L., Lewis S.J. Circadian misalignment and sleep disruption in mild cognitive impairment. J. Alzheimers Dis. 2014, 38:857-866.
41. Pedrazzoli M., D'Almeida V., Martins P.J., Machado R.B., Ling L., Nishino S., Tufik S., Mignot E. Increased hypocretin-1 levels in cerebrospinal fluid after REM sleep deprivation. Brain Res. 2004, 995:1-6.
42. Perry E., Walker M., Grace J., Perry R. Acetylcholine in mind: a neurotransmitter correlate of consciousness?. Trends Neurosci. 1999, 22:273-280.
43. Peter-Derex L., Yammine P., Bastuji H., Croisile B. Sleep and Alzheimer's disease. Sleep Med. Rev. 2015, 19:29-38.
44. Petersen R.C., Aisen P., Boeve B.F., Geda Y.E., Ivnik R.J., Knopman D.S., Mielke M., Pankratz V.S., Roberts R., Rocca W.A., Weigand S., Weiner M., Wiste H., Jack C.R. Mild cognitive impairment due to Alzheimer disease in the community. Ann. Neurol. 2013, 74:199-208.
45. Power A.E. Slow-wave sleep, acetylcholine, and memory consolidation. Proc. Natl. Acad. Sci. U. S. A. 2004, 101:1795-1796.
46. Romigi A., Albanese M., Placidi F., Izzi F., Liguori C., Marciani M.G., Mercuri N.B., Terracciano C., Vitrani G., Petrucci A., Di Gioia B., Massa R. Sleep disorders in myotonic dystrophy type 2: a controlled polysomnographic study and self-reported questionnaires. Eur. J. Neurol. 2014, 21:929-934.
47. Sancesario G.M., Esposito Z., Nuccetelli M., Bernardini S., Sorge R., Martorana A., Federici G., Bernardi G., Sancesario G. Abeta1-42 Detection in CSF of Alzheimer's disease is influenced by temperature: indication of reversible Abeta1-42 aggregation?. Exp. Neurol. 2010, 223:371-376.
48. Saper C.B., Scammell T.E., Lu J. Hypothalamic regulation of sleep and circadian rhythms. Nature 2005, 437:1257-1263.
49. Scheltens P., Leys D., Barkhof F., Huglo D., Weinstein H.C., Vermersch P., Kuiper M., Steinling M., Wolters E.C., Valk J. Atrophy of medial temporal lobes on MRI in "probable" Alzheimer's disease and normal ageing: diagnostic value and neuropsychological correlates. J. Neurol. Neurosurg. Psychiatry 1992, 55:967-972.
50. Schmidt F.M., Kratzsch J., Gertz H.J., Tittmann M., Jahn I., Pietsch U.C., Kaisers U.X., Thiery J., Hegerl U., Schönknecht P. Cerebrospinal fluid melanin-concentrating hormone (MCH) and hypocretin-1 (HCRT-1, orexin-A) in Alzheimer's disease. PLoS One 2013, 8:e63136.
51. Slats D., Claassen J.A., Lammers G.J., Melis R.J., Verbeek M.M., Overeem S. Association between hypocretin-1 and amyloid-β42 cerebrospinal fluid levels in Alzheimer's disease and healthy controls. Curr. Alzheimer Res. 2012, 9:1119-1125.
52. Tononi G., Cirelli C. Sleep function and synaptic homeostasis. Sleep Med. Rev. 2006, 10:49-62.
53. Villa C., Ferini-Strambi L., Combi R. The synergistic relationship between Alzheimer's disease and sleep disorders: an update. J. Alzheimers Dis. 2015, 46:571-580.
54. Wennström M., Londos E., Minthon L., Nielsen H.M. Altered CSF orexin and α-synuclein levels in dementia patients. J. Alzheimers Dis. 2012, 29:125-132.
55. Xie L., Kang H., Xu Q., Chen M.J., Liao Y., Thiyagarajan M., O'Donnell J., Christensen D.J., Nicholson C., Iliff J.J., Takano T., Deane R., Nedergaard M. Sleep drives metabolite clearance from the adult brain. Science 2013, 342:373-377.
56. Yoon J.H., Kim M., Moon S.Y., Yong S.W., Hong J.M. Olfactory function and neuropsychological profile to differentiate dementia with Lewy bodies from Alzheimer's disease in patients with mild cognitive impairment: a 5-year follow-up study. J. Neurol. Sci. 2015, 355:174-179.