Insulin and sex interactions in older adults with mild cognitive impairment

Journal of Alzheimer's Disease

Volumn 31, Issue 2, 2012, Pages 401-410

  Cholerton, Brenna ^a   Baker, Laura D ^a,b   Trittschuh, Emily H ^a,b   Crane, Paul K ^b   Larson, Eric B ^b,c   Arbuckle, Matthew ^a   Saucedo, Hector Hernandez ^a   McCurry, Susan M ^b   Bowen, James D ^b   McCormick, Wayne C ^b   Craft, Suzanne ^a,b  

^a Veterans Affairs Puget Sound Health Care System   (United States)

^b UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

^c GROUP HEALTH RESEARCH INSTITUTE   (United States)

Author keywords

Age related memory disorders; aging; Alzheimer's disease; cognition; dementia; hyperinsulinemia; insulin; vascular

Indexed keywords

APOLIPOPROTEIN E; INSULIN;

AGED; AMNESIA; ARTICLE; BLOOD SAMPLING; BODY MASS; CARDIOVASCULAR FUNCTION; COHORT ANALYSIS; COMMUNITY CARE; DISEASE ASSOCIATION; DSM-IV; FEMALE; GENOTYPE; HUMAN; INSULIN BLOOD LEVEL; MAJOR CLINICAL STUDY; MALE; MILD COGNITIVE IMPAIRMENT; PRIORITY JOURNAL; SCORING SYSTEM; SEX DIFFERENCE; WAIST HIP RATIO;

EID: 84865607205     PISSN: 13872877     EISSN: 18758908     Source Type: Journal    
DOI: 10.3233/JAD-2012-120202     Document Type: Article

References (67)

1. Luchsinger JA (2010) Type 2 diabetes, related conditions, in relation and dementia: An opportunity for prevention? J Alzheimers Dis 20, 723-736.
2. Craft S (2009) The role of metabolic disorders in Alzheimer disease and vascular dementia: Two roads converged. Arch Neurol 66, 300-305.
3. Strachan MW, Reynolds RM, Marioni RE, Price JF (2011) Cognitive function, dementia and type 2 diabetes mellitus in the elderly. Nat Rev Endocrinol 7, 108-114.
4. Craft S (2007) Insulin resistance and Alzheimer's disease pathogenesis: Potential mechanisms and implications for treatment. Curr Alzheimer Res 4, 147-152. (Pubitemid 46557503)
5. Gasparini L, Gouras GK, Wang R, Gross RS, Beal MF, Greengard P, Xu H (2001) Stimulation of beta-amyloid precursor protein trafficking by insulin reduces intraneuronal beta-amyloid and requires mitogen-activated protein kinase signaling. J Neurosci 21, 2561-2570. (Pubitemid 32298198)
6. Zhao L, Teter B, Morihara T, Lim GP, Ambegaokar SS, Ubeda OJ, Frautschy SA, ColeGM(2004) Insulin-degrading enzyme as a downstream target of insulin receptor signaling cascade: Implications for Alzheimer's disease intervention. J Neurosci 24, 11120-11126. (Pubitemid 40012971)
7. Cook DG, Leverenz JB, McMillan PJ, Kulstad JJ, Ericksen S, Roth RA, Schellenberg GD, Jin LW, Kovacina KS, Craft S (2003) Reduced hippocampal insulin-degrading enzyme in late-onset Alzheimer's disease is associated with the apolipoprotein E-epsilon4 allele. Am J Pathol 162, 313-319. (Pubitemid 36042013)
8. Farris W, Mansourian S, Chang Y, Lindsley L, Eckman EA, Frosch MP, Eckman CB, Tanzi RE, Selkoe DJ, Guenette S (2003) Insulin-degrading enzyme regulates the levels of insulin, amyloid beta-protein, and the beta-amyloid precursor protein intracellular domain in vivo. Proc Natl Acad Sci USA 100, 4162-4167. (Pubitemid 36418174)
9. Perez A, Morelli L, Cresto JC, Castano EM (2000) Degradation of soluble amyloid B-peptides 1-40, 1-42, and the Dutch variant 1-40Q by insulin degrading enzyme from Alzheimer disease and control brains. Neurochem Res 25, 247-255. (Pubitemid 30210091)
10. Haring HU, Mehnert H (1993) Pathogenesis of type 2 (noninsulin-dependent) diabetes mellitus: Candidates for a signal transmitter defect causing insulin resistance of the skeletal muscle. Diabetologia 36, 176-182. (Pubitemid 23067075)
11. Reddy KJ, Singh M, Bangit JR, Batsell RR (2010) The role of insulin resistance in the pathogenesis of atherosclerotic cardiovascular disease: An updated review. J Cardiovasc Med (Hagerstown) 11, 633-647.
12. Zeyda M, Stulnig TM (2009) Obesity, inflammation, and insulin resistance-a mini-review. Gerontology 55, 379-386.
13. Vijayaraghavan K (2010) Treatment of dyslipidemia in patients with type 2 diabetes. Lipids Health Dis 9, 144.
14. Cubeddu LX, Hoffmann IS (2002) Insulin resistance and upper-normal glucose levels in hypertension:Areview. JHum Hypertens 16(Suppl 1), S52-S55. (Pubitemid 34441137)
15. Anstey KJ, Lipnicki DM, Low LF (2008) Cholesterol as a risk factor for dementia and cognitive decline: A systematic review of prospective studies with meta-analysis. Am J Geriatr Psychiatry 16, 343-354.
16. Kivipelto M, Helkala EL, Hanninen T, Laakso MP, Hallikainen M, Alhainen K, Soininen H, Tuomilehto J, Nissinen A (2001) Midlife vascular risk factors and late-life mild cognitive impairment: A population-based study. Neurology 56, 1683-1689. (Pubitemid 32574567)
17. Launer LJ, RossGW, Petrovitch H, Masaki K, FoleyD,White LR, Havlik RJ (2000) Midlife blood pressure and dementia: The Honolulu-Asia aging study. Neurobiol Aging 21, 49-55. (Pubitemid 30224785)
18. Ninomiya T, Ohara T, Hirakawa Y, Yoshida D, Doi Y, Hata J, Kanba S, Iwaki T, Kiyohara Y (2011) Midlife and latelife blood pressure and dementia in Japanese elderly: The hisayama study. Hypertension 58, 22-28.
19. Profenno LA, Porsteinsson AP, Faraone SV (2010) Metaanalysis of Alzheimer's disease risk with obesity, diabetes, and related disorders. Biol Psychiatry 67, 505-512.
20. Yang H, Jin X, Wai Kei Lam CW, Yan SK (2011) Oxidative stress and diabetes mellitus. Clin Chem Lab Med 49, 1773-1782.
21. Faerch K, Vaag A, Holst JJ, Hansen T, Jorgensen T, Borch-Johnsen K (2009) Natural history of insulin sensitivity and insulin secretion in the progression from normal glucose tolerance to impaired fasting glycemia and impaired glucose tolerance: The Inter99 study. Diabetes Care 32, 439-444.
22. Albert MS, DeKosky ST, Dickson D, Dubois B, Feldman HH, Fox NC, Gamst A, Holtzman DM, Jagust WJ, Petersen RC, Snyder PJ, Carrillo MC, Thies B, Phelps CH (2011) 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, 270-279.
23. Petersen RC, Doody R, Kurz A, Mohs RC, Morris JC, Rabins PV, Ritchie K, Rossor M, Thal L, Winblad B (2001) Current concepts in mild cognitive impairment. Arch Neurol 58, 1985-1992. (Pubitemid 33143977)
24. Petersen RC, Roberts RO, Knopman DS, Boeve BF, Geda YE, Ivnik RJ, Smith GE, Jack CR Jr (2009) Mild cognitive impairment: Ten years later. Arch Neurol 66, 1447-1455.
25. Kalmijn S, Feskens EJ, Launer LJ, Stijnen T, Kromhout D (1995) Glucose intolerance, hyperinsulinaemia and cognitive function in a general population of elderly men. Diabetologia 38, 1096-1102.
26. Yaffe K, Blackwell T, Kanaya AM, Davidowitz N, Barrett-Connor E, Krueger K (2004) Diabetes, impaired fasting glucose, and development of cognitive impairment in older women. Neurology 63, 658-663. (Pubitemid 39100821)
27. van Oijen M, Okereke OI, Kang JH, Pollak MN, Hu FB, Hankinson SE, Grodstein F (2008) Fasting insulin levels and cognitive decline in older women without diabetes. Neuroepidemiology 30, 174-179. (Pubitemid 351667798)
28. Okereke OI, Kurth T, Pollak MN, Gaziano JM, Grodstein F (2010) Fasting plasma insulin, C-peptide and cognitive change in older men without diabetes: Results from the Physicians' Health Study II. Neuroepidemiology 34, 200-207.
29. Schrijvers EM,Witteman JC, Sijbrands EJ, Hofman A,Koudstaal PJ, BretelerMM(2010) Insulin metabolism and the risk of Alzheimer disease: The Rotterdam Study. Neurology 75, 1982-1987.
30. Peila R, Rodriguez BL, White LR, Launer LJ (2004) Fasting insulin and incident dementia in an elderly population of Japanese-American men. Neurology 63, 228-233. (Pubitemid 38971119)
31. Banos G, Guarner V, Perez-Torres I (2011) Sex steroid hormones, cardiovascular diseases and the metabolic syndrome. Cardiovasc Hematol Agents Med Chem 9, 137-146.
32. Regitz-Zagrosek V, Lehmkuhl E, Weickert MO (2006) Gender differences in the metabolic syndrome and their role for cardiovascular disease. Clin Res Cardiol 95, 136-147.
33. Craft S, Asthana S, Schellenberg G, Cherrier M, Baker LD, Newcomer J, Plymate S, Latendresse S, Petrova A, Raskind M, Peskind E, Lofgreen C, Grimwood K (1999) Insulin metabolism in Alzheimer's disease differs according to apolipoprotein E genotype and gender. Neuroendocrinology 70, 146-152. (Pubitemid 29385395)
34. Risner ME, Saunders AM, Altman JF, Ormandy GC, Craft S, Foley IM, Zvartau-Hind ME, Hosford DA, Roses AD (2006) Efficacy of rosiglitazone in a genetically defined population with mild-to-moderate Alzheimer's disease. Pharmacogenomics J 6, 246-254. (Pubitemid 44137951)
35. Craft S, Asthana S, Schellenberg G, Baker L, Cherrier M, Boyt AA, Martins RN, Raskind M, Peskind E, Plymate S (2000) Insulin effects on glucose metabolism, memory, and plasma amyloid precursor protein in Alzheimer's disease differ according to apolipoprotein-E genotype. Ann N Y Acad Sci 903, 222-228. (Pubitemid 30251561)
36. Ronnemaa E, Zethelius B, Sundelof J, Sundstrom J, Degerman-Gunnarsson M, Berne C, Lannfelt L, Kilander L (2008) Impaired insulin secretion increases the risk of Alzheimer disease. Neurology 71, 1065-1071.
37. Kukull WA, Higdon R, Bowen JD, McCormick WC, Teri L, Schellenberg GD, van Belle G, Jolley L, Larson EB (2002) Dementia and Alzheimer disease incidence: A prospective cohort study. Arch Neurol 59, 1737-1746. (Pubitemid 35340484)
38. Larson EB, Wang L, Bowen JD, McCormick WC, Teri L, Crane P,KukullW(2006) Exercise is associated with reduced risk for incident dementia among persons 65 years of age and older. Ann Intern Med 144, 73-81. (Pubitemid 46768225)
39. Teng EL, Hasegawa K, Homma A, Imai Y, Larson E, Graves A, Sugimoto K, Yamaguchi T, Sasaki H, Chiu D, et al. (1994) The Cognitive Abilities Screening Instrument (CASI): A practical test for cross-cultural epidemiological studies of dementia. Int Psychogeriatr 6, 45-58, discussion 62. (Pubitemid 24167129)
40. American Psychiatric Association (1994) Diagnostic and statistical manual of mental disorders, 4th ed.,Washington, DC, pp. 133-143.
41. McKhann G, Drachman D, Folstein M, Katzman R, Price D, Stadlan EM (1984) 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 34, 939-944. (Pubitemid 14076461)
42. Wechsler D (1987) Wechsler Memory Scale-Revised, The Psychological Corporation, San Antonio, TX.
43. Morris JC, Heyman A, Mohs RC, Hughes JP, van Belle G, Fillenbaum G, Mellits ED, Clark C (1989) The Consortium to Establish a Registry for Alzheimer's Disease (CERAD). Part I. Clinical and neuropsychological assessment of Alzheimer's disease. Neurology 39, 1159-1165. (Pubitemid 19239715)
44. Reitan R (1958) Validity of the Trail Making Test as an indicator of organic brain damage. Perceptual Motor Skills 8, 271-276.
45. Kozora E, Cullum CM (1995) Generative naming in normal aging: Total output and qualitative changes using phonemic and semantic constraints. The Clinical Neuropsychologist 9, 313-320.
46. Lucas JA, Ivnik RJ, Smith GE, Bohac DL, Tangalos EG, Graff-Radford NR, Petersen RC (1998) Mayo's older Americans normative studies: Category fluency norms. J Clin Exp Neuropsychol 20, 194-200. (Pubitemid 28451698)
47. Steinberg BA, Bieliauskas LA, Smith GE, Ivnik RJ (2005) Mayo's Older Americans Normative Studies: Age-and IQAdjusted Norms for the Wechsler Memory Scale-Revised. Clin Neuropsychol 19, 378-463. (Pubitemid 41153288)
48. Steinberg BA, Bieliauskas LA, Smith GE, Ivnik RJ (2005) Mayo's Older Americans Normative Studies: Age-and IQAdjusted Norms for the Trail-Making Test, the Stroop Test, and MAE Controlled Oral Word Association Test. Clin Neuropsychol 19, 329-377. (Pubitemid 41153287)
49. Welsh-Bohmer KA, Ostbye T, Sanders L, Pieper CF, Hayden KM, Tschanz JT, Norton MC (2009) Neuropsychological performance in advanced age: Influences of demographic factors and Apolipoprotein E: Findings from the Cache County Memory Study. Clin Neuropsychol 23, 77-99.
50. Galasko D, Bennett DA, Sano M, Marson D, Kaye J, Edland SD (2006) ADCS Prevention Instrument Project: Assessment of instrumental activities of daily living for communitydwelling elderly individuals in dementia prevention clinical trials. Alzheimer Dis Assoc Disord 20, S152-S169. (Pubitemid 44900699)
51. Hixson JE, Vernier DT (1990) Restriction isotyping of human apolipoprotein E by gene amplification and cleavage with HhaI. J Lipid Res 31, 545-548. (Pubitemid 20107994)
52. Luchsinger JA (2008) Adiposity, hyperinsulinemia, diabetes and Alzheimer's disease: An epidemiological perspective. Eur J Pharmacol 585, 119-129.
53. StrachanMW, Reynolds RM, Frier BM, Mitchell RJ, Price JF (2008) The relationship between type 2 diabetes and dementia. Br Med Bull 88, 131-146.
54. Euser SM, Sattar N, Witteman JC, Bollen EL, Sijbrands EJ, Hofman A, Perry IJ, Breteler MM, Westendorp RG (2010) A prospective analysis of elevated fasting glucose levels and cognitive function in older people: Results from PROSPER and the Rotterdam Study. Diabetes 59, 1601-1607.
55. Ronnemaa E, Zethelius B, Sundelof J, Sundstrom J, Degerman-Gunnarsson M, Lannfelt L, Berne C, Kilander L (2009) 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 52, 1504-1510.
56. Okereke OI, Selkoe DJ, Pollak MN, Stampfer MJ, Hu FB, Hankinson SE, Grodstein F (2009) A profile of impaired insulin degradation in relation to late-life cognitive decline: A preliminary investigation. Int J Geriatr Psychiatry 24, 177-182.
57. Okereke OI, Pollak MN, Hu FB, Hankinson SE, Selkoe DJ, Grodstein F (2008) Plasma C-peptide levels and rates of cognitive decline in older, community-dwelling women without diabetes. Psychoneuroendocrinology 33, 455-461.
58. Burns JM, Donnelly JE, Anderson HS, Mayo MS, Spencer-Gardner L, Thomas G, Cronk BB, Haddad Z, Klima D, Hansen D, Brooks WM (2007) Peripheral insulin and brain structure in early Alzheimer disease. Neurology 69, 1094-1104. (Pubitemid 47517554)
59. Burns JM, Honea RA, Vidoni ED, Hutfles L, Brooks WM, Swerdlow RH (2012) Insulin is differentially related to cognitive decline and atrophy in Alzheimer's disease and aging. Biochim Biophys Acta 1822, 333-339.
60. Gil-Bea FJ, Solas M, Solomon A, Mugueta C, Winblad B, Kivipelto M, Ramirez MJ, Cedazo-Minguez A (2010) Insulin levels are decreased in the cerebrospinal fluid of women with prodomal Alzheimer's disease. J Alzheimers Dis 22, 405-413.
61. He J, Farias S, Martinez O, Reed B, Mungas D, Decarli C (2009) Differences in brain volume, hippocampal volume, cerebrovascular risk factors, and apolipoprotein E4 among mild cognitive impairment subtypes. Arch Neurol 66, 1393-1399.
62. Reaven GM (2005) Compensatory hyperinsulinemia and the development of an atherogenic lipoprotein profile: The price paid to maintain glucose homeostasis in insulin-resistant individuals. Endocrinol Metab Clin North Am 34, 49-62. (Pubitemid 40332502)
63. Reaven GM (2011) Relationships among insulin resistance, type 2 diabetes, essential hypertension, and cardiovascular disease: Similarities and differences. J Clin Hypertens (Greenwich) 13, 238-243.
64. Ronnemaa T, Laakso M, Puukka P, Kallio V, Pyorala K (1988) Atherosclerotic vascular disease in middle-aged, insulin-treated, diabetic patients. Association with endogenous insulin secretion capacity. Arteriosclerosis 8, 237-244.
65. Burchfiel CM, Curb JD, Arakaki R, Abbott RD, Sharp DS, Rodriguez BL, Yano K (1996) Cardiovascular risk factors and hyperinsulinemia in elderly men: The Honolulu Heart Program. Ann Epidemiol 6, 490-497. (Pubitemid 27016918)
66. Burchfiel CM, Sharp DS, Curb JD, Rodriguez BL, Abbott RD, Arakaki R, Yano K (1998) Hyperinsulinemia and cardiovascular disease in elderly men: The Honolulu Heart Program. Arterioscler Thromb Vasc Biol 18, 450-457. (Pubitemid 28125640)
67. Schianca GP, Castello L, Rapetti R, Limoncini A, Bartoli E (2006) Insulin sensitivity: Gender-related differences in subjects with normal glucose tolerance. Nutr Metab Cardiovasc Dis 16, 339-344. (Pubitemid 43996986)