Association of moderate alcohol intake with in vivo amyloid-beta deposition in human brain: A cross-sectional study
Autoři:
Jee Wook Kim aff001; Min Soo Byun aff003; Dahyun Yi aff003; Jun Ho Lee aff004; Kang Ko aff005; So Yeon Jeon aff006; Bo Kyung Sohn aff007; Jun-Young Lee aff008; Yu Kyeong Kim aff010; Seong A Shin aff010; Chul-Ho Sohn aff011; Dong Young Lee aff003;
Působiště autorů:
Department of Neuropsychiatry, Hallym University Dongtan Sacred Heart Hospital, Hwaseong, Republic of Korea
aff001; Department of Psychiatry, Hallym University College of Medicine, Chuncheon, Republic of Korea
aff002; Institute of Human Behavioral Medicine, Medical Research Center, Seoul National University, Seoul, Republic of Korea
aff003; Department of Neuropsychiatry, Seoul National University Hospital, Seoul, Republic of Korea
aff004; Department of Geriatric Psychiatry, National Center for Mental Health, Seoul, Republic of Korea
aff005; Department of Psychiatry, Chungnam National University Hospital, Daejeon, Republic of Korea
aff006; Department of Psychiatry, Sanggye Paik Hospital, Inje University College of Medicine, Seoul, Republic of Korea
aff007; Department of Neuropsychiatry, SMG-SNU Boramae Medical Center, Seoul, Republic of Korea
aff008; Department of Psychiatry, Seoul National University College of Medicine, Seoul, Republic of Korea
aff009; Department of Nuclear Medicine, SMG-SNU Boramae Medical Center, Seoul, Republic of Korea
aff010; Department of Radiology, Seoul National University College of Medicine, Seoul, Republic of Korea
aff011
Vyšlo v časopise:
Association of moderate alcohol intake with in vivo amyloid-beta deposition in human brain: A cross-sectional study. PLoS Med 17(2): e32767. doi:10.1371/journal.pmed.1003022
Kategorie:
Research Article
doi:
https://doi.org/10.1371/journal.pmed.1003022
Souhrn
Background
An emerging body of literature has indicated that moderate alcohol intake may be protective against Alzheimer disease (AD) dementia. However, little information is available regarding whether moderate alcohol intake is related to reductions in amyloid-beta (Aβ) deposition, or is protective via amyloid-independent mechanisms in the living human brain. Here we examined the associations of moderate alcohol intake with in vivo AD pathologies, including cerebral Aβ deposition, neurodegeneration of AD-signature regions, and cerebral white matter hyperintensities (WMHs) in the living human brain.
Methods and findings
The present study was part of the Korean Brain Aging Study for Early Diagnosis and Prediction of Alzheimer’s Disease (KBASE), an ongoing prospective cohort study that started in 2014. As of November 2016, 414 community-dwelling individuals with neither dementia nor alcohol-related disorders (280 cognitively normal [CN] individuals and 134 individuals with mild cognitive impairment [MCI]) between 56 and 90 years of age (mean age 70.9 years ± standard deviation 7.8; male, n [%] = 180 [43.5]) were recruited from 4 sites (i.e., 2 university hospitals and 2 public centers for dementia prevention and management) around Seoul, South Korea. All the participants underwent comprehensive clinical assessments comprising lifetime and current histories of alcohol intake and multimodal brain imaging, including [11C] Pittsburgh compound B positron emission tomography (PET), [18F] fluorodeoxyglucose (FDG) PET, and magnetic resonance imaging (MRI) scans. Lifetime and current alcohol intake were categorized as follows: no drinking, <1 standard drink (SD)/week, 1–13 SDs/week, and 14+ SDs/week. A moderate lifetime alcohol intake (1–13 SDs/week) was significantly associated with a lower Aβ positivity rate compared to the no drinking group, even after controlling for potential confounders (odds ratio 0.341, 95% confidence interval 0.163–0.714, p = 0.004). In contrast, current alcohol intake was not associated with amyloid deposition. Additionally, alcohol intake was not related to neurodegeneration of AD-signature regions or cerebral WMH volume. The present study had some limitations in that it had a cross-sectional design and depended on retrospective recall for alcohol drinking history.
Conclusions
In this study, we observed in middle- and old-aged individuals with neither dementia nor alcohol-related disorders that moderate lifetime alcohol intake was associated with lower cerebral Aβ deposition compared to a lifetime history of not drinking. Moderate lifetime alcohol intake may have a beneficial influence on AD by reducing pathological amyloid deposition rather than amyloid-independent neurodegeneration or cerebrovascular injury.
Klíčová slova:
Alcohol consumption – Alzheimer's disease – Cognitive impairment – Dementia – Magnetic resonance imaging – Memory recall – Neuroimaging – Positron emission tomography
Zdroje
1. Harper C. The neuropathology of alcohol-related brain damage. Alcohol Alcohol. 2009;44(2):136–40. doi: 10.1093/alcalc/agn102 19147798
2. Ridley NJ, Draper B, Withall A. Alcohol-related dementia: an update of the evidence. Alzheimers Res Ther. 2013;5(1):3. doi: 10.1186/alzrt157 23347747
3. Kim JW, Lee DY, Lee BC, Jung MH, Kim H, Choi YS, et al. Alcohol and cognition in the elderly: a review. Psychiatry Investig. 2012;9(1):8–16. doi: 10.4306/pi.2012.9.1.8 22396679
4. Oslin DW, Cary MS. Alcohol-related dementia: validation of diagnostic criteria. Am J Geriatr Psychiatry. 2003;11(4):441–7. 12837673
5. Stampfer MJ, Kang JH, Chen J, Cherry R, Grodstein F. Effects of moderate alcohol consumption on cognitive function in women. N Engl J Med. 2005;352(3):245–53. doi: 10.1056/NEJMoa041152 15659724
6. Britton A, Singh-Manoux A, Marmot M. Alcohol consumption and cognitive function in the Whitehall II Study. Am J Epidemiol. 2004;160(3):240–7. doi: 10.1093/aje/kwh206 15257997
7. Ngandu T, Helkala EL, Soininen H, Winblad B, Tuomilehto J, Nissinen A, et al. Alcohol drinking and cognitive functions: findings from the Cardiovascular Risk Factors Aging and Dementia (CAIDE) Study. Dement Geriatr Cogn Disord. 2007;23(3):140–9. doi: 10.1159/000097995 17170526
8. Lang I, Wallace RB, Huppert FA, Melzer D. Moderate alcohol consumption in older adults is associated with better cognition and well-being than abstinence. Age Ageing. 2007;36(3):256–61. doi: 10.1093/ageing/afm001 17353234
9. Panza F, Capurso C, D’Introno A, Colacicco AM, Frisardi V, Lorusso M, et al. Alcohol drinking, cognitive functions in older age, predementia, and dementia syndromes. J Alzheimers Dis. 2009;17(1):7–31. doi: 10.3233/JAD-2009-1009 19494429
10. Ruitenberg A, van Swieten JC, Witteman JC, Mehta KM, van Duijn CM, Hofman A, et al. Alcohol consumption and risk of dementia: the Rotterdam Study. Lancet. 2002;359(9303):281–6. doi: 10.1016/S0140-6736(02)07493-7 11830193
11. Mukamal KJ, Kuller LH, Fitzpatrick AL, Longstreth WT Jr, Mittleman MA, Siscovick DS. Prospective study of alcohol consumption and risk of dementia in older adults. JAMA. 2003;289(11):1405–13. doi: 10.1001/jama.289.11.1405 12636463
12. Weyerer S, Schaufele M, Wiese B, Maier W, Tebarth F, van den Bussche H, et al. Current alcohol consumption and its relationship to incident dementia: results from a 3-year follow-up study among primary care attenders aged 75 years and older. Age Ageing. 2011;40(4):456–63. doi: 10.1093/ageing/afr007 21367764
13. Peters R, Peters J, Warner J, Beckett N, Bulpitt C. Alcohol, dementia and cognitive decline in the elderly: a systematic review. Age Ageing. 2008;37(5):505–12. doi: 10.1093/ageing/afn095 18487267
14. McGuire LC, Ajani UA, Ford ES. Cognitive functioning in late life: the impact of moderate alcohol consumption. Ann Epidemiol. 2007;17(2):93–9. doi: 10.1016/j.annepidem.2006.06.005 17027288
15. Huang W, Qiu C, Winblad B, Fratiglioni L. Alcohol consumption and incidence of dementia in a community sample aged 75 years and older. J Clin Epidemiol. 2002;55(10):959–64. doi: 10.1016/s0895-4356(02)00462-6 12464371
16. Xu W, Wang H, Wan Y, Tan C, Li J, Tan L, et al. Alcohol consumption and dementia risk: a dose-response meta-analysis of prospective studies. Eur J Epidemiol. 2017;32(1):31–42. doi: 10.1007/s10654-017-0225-3 28097521
17. Wang J, Ho L, Zhao Z, Seror I, Humala N, Dickstein DL, et al. Moderate consumption of Cabernet Sauvignon attenuates Abeta neuropathology in a mouse model of Alzheimer’s disease. FASEB J. 2006;20(13):2313–20. doi: 10.1096/fj.06-6281com 17077308
18. Bate C, Williams A. Ethanol protects cultured neurons against amyloid-beta and alpha-synuclein-induced synapse damage. Neuropharmacology. 2011;61(8):1406–12. doi: 10.1016/j.neuropharm.2011.08.030 21903110
19. Munoz G, Urrutia JC, Burgos CF, Silva V, Aguilar F, Sama M, et al. Low concentrations of ethanol protect against synaptotoxicity induced by Abeta in hippocampal neurons. Neurobiol Aging. 2015;36(2):845–56. doi: 10.1016/j.neurobiolaging.2014.10.017 25433458
20. Ormeno D, Romero F, Lopez-Fenner J, Avila A, Martinez-Torres A, Parodi J. Ethanol reduces amyloid aggregation in vitro and prevents toxicity in cell lines. Arch Med Res. 2013;44(1):1–7. doi: 10.1016/j.arcmed.2012.12.004 23291379
21. den Heijer T, Vermeer SE, van Dijk EJ, Prins ND, Koudstaal PJ, van Duijn CM, et al. Alcohol intake in relation to brain magnetic resonance imaging findings in older persons without dementia. Am J Clin Nutr. 2004;80(4):992–7. doi: 10.1093/ajcn/80.4.992 15447910
22. Mukamal KJ, Longstreth WT Jr, Mittleman MA, Crum RM, Siscovick DS. Alcohol consumption and subclinical findings on magnetic resonance imaging of the brain in older adults: the cardiovascular health study. Stroke. 2001;32(9):1939–46. doi: 10.1161/hs0901.095723 11546878
23. Anstey KJ, Jorm AF, Reglade-Meslin C, Maller J, Kumar R, von Sanden C, et al. Weekly alcohol consumption, brain atrophy, and white matter hyperintensities in a community-based sample aged 60 to 64 years. Psychosom Med. 2006;68(5):778–85. doi: 10.1097/01.psy.0000237779.56500.af 17012533
24. Wang Q, Sun AY, Simonyi A, Kalogeris TJ, Miller DK, Sun GY, et al. Ethanol preconditioning protects against ischemia/reperfusion-induced brain damage: role of NADPH oxidase-derived ROS. Free Radic Biol Med. 2007;43(7):1048–60. doi: 10.1016/j.freeradbiomed.2007.06.018 17761301
25. Ray PS, Maulik G, Cordis GA, Bertelli AA, Bertelli A, Das DK. The red wine antioxidant resveratrol protects isolated rat hearts from ischemia reperfusion injury. Free Radic Biol Med. 1999;27(1–2):160–9. doi: 10.1016/s0891-5849(99)00063-5 10443932
26. Guiraud A, de Lorgeril M, Boucher F, Berthonneche C, Rakotovao A, de Leiris J. Cardioprotective effect of chronic low dose ethanol drinking: insights into the concept of ethanol preconditioning. J Mol Cell Cardiol. 2004;36(4):561–6. doi: 10.1016/j.yjmcc.2004.02.003 15081315
27. Wang Q, Xu J, Rottinghaus GE, Simonyi A, Lubahn D, Sun GY, et al. Resveratrol protects against global cerebral ischemic injury in gerbils. Brain Res. 2002;958(2):439–47. doi: 10.1016/s0006-8993(02)03543-6 12470882
28. Shigematsu S, Ishida S, Hara M, Takahashi N, Yoshimatsu H, Sakata T, et al. Resveratrol, a red wine constituent polyphenol, prevents superoxide-dependent inflammatory responses induced by ischemia/reperfusion, platelet-activating factor, or oxidants. Free Radic Biol Med. 2003;34(7):810–7. doi: 10.1016/s0891-5849(02)01430-2 12654468
29. Taki Y, Kinomura S, Sato K, Goto R, Inoue K, Okada K, et al. Both global gray matter volume and regional gray matter volume negatively correlate with lifetime alcohol intake in non-alcohol-dependent Japanese men: a volumetric analysis and a voxel-based morphometry. Alcohol Clin Exp Res. 2006;30(6):1045–50. doi: 10.1111/j.1530-0277.2006.00118.x 16737464
30. Paul CA, Au R, Fredman L, Massaro JM, Seshadri S, Decarli C, et al. Association of alcohol consumption with brain volume in the Framingham study. Arch Neurol. 2008;65(10):1363–7. doi: 10.1001/archneur.65.10.1363 18852353
31. Aho L, Karkola K, Juusela J, Alafuzoff I. Heavy alcohol consumption and neuropathological lesions: a post-mortem human study. J Neurosci Res. 2009;87(12):2786–92. doi: 10.1002/jnr.22091 19382227
32. American Psychiatric Association. Diagnostic and statistical manual of mental disorders, 5th edition: DSM-5. Arlington (VA): American Psychiatric Association; 2013.
33. Williamson W, Lewandowski AJ, Forkert ND, Griffanti L, Okell TW, Betts J, et al. Association of cardiovascular risk factors with MRI indices of cerebrovascular structure and function and white matter hyperintensities in young adults. JAMA. 2018;320(7):665–73. doi: 10.1001/jama.2018.11498 30140877
34. Debette S, Markus HS. The clinical importance of white matter hyperintensities on brain magnetic resonance imaging: systematic review and meta-analysis. BMJ. 2010;341:c3666. doi: 10.1136/bmj.c3666 20660506
35. Byun MS, Yi D, Lee JH, Choe YM, Sohn BK, Lee JY, et al. Korean Brain Aging Study for the Early Diagnosis and Prediction of Alzheimer’s Disease: methodology and baseline sample characteristics. Psychiatry Investig. 2017;14(6):851–63. doi: 10.4306/pi.2017.14.6.851 29209391
36. Morris JC. The Clinical Dementia Rating (CDR): current version and scoring rules. Neurology. 1993;43(11):2412–4.
37. Lee DY, Lee KU, Lee JH, Kim KW, Jhoo JH, Kim SY, et al. A normative study of the CERAD neuropsychological assessment battery in the Korean elderly. J Int Neuropsychol Soc. 2004;10(1):72–81. doi: 10.1017/S1355617704101094 14751009
38. Morris JC, Heyman A, Mohs RC, Hughes JP, van Belle G, Fillenbaum G, et al. The Consortium to Establish a Registry for Alzheimer’s Disease (CERAD). Part I. Clinical and neuropsychological assessment of Alzheimer’s disease. Neurology. 1989;39(9):1159–65. doi: 10.1212/wnl.39.9.1159 2771064
39. Lee JH, Lee KU, Lee DY, Kim KW, Jhoo JH, Kim JH, et al. Development of the Korean version of the Consortium to Establish a Registry for Alzheimer’s Disease Assessment Packet (CERAD-K): clinical and neuropsychological assessment batteries. J Gerontol B Psychol Sci Soc Sci. 2002;57(1):47–53.
40. Babor TF, Higgins-Biddle JC. Brief intervention: for hazardous drinking—a manual for use in primary care. Geneva: World Health Organization; 2001 [cited 2020 Jan 24]. Available from: https://www.who.int/substance_abuse/publications/audit_sbi/en/.
41. Topiwala A, Allan CL, Valkanova V, Zsoldos E, Filippini N, Sexton C, et al. Moderate alcohol consumption as risk factor for adverse brain outcomes and cognitive decline: longitudinal cohort study. BMJ. 2017;357:j2353. doi: 10.1136/bmj.j2353 28588063
42. UK Department of Health. New alcohol guidelines launched. UK Department of Health; 2016 [cited 2020 Jan 24]. Available from: https://www.health-ni.gov.uk/news/new-alcohol-guidelines-launched.
43. Kim JY, Park JH, Lee JJ, Huh Y, Lee SB, Han SK, et al. Standardization of the Korean version of the Geriatric Depression Scale: reliability, validity, and factor structure. Psychiatry Investig. 2008;5(4):232–8. doi: 10.4306/pi.2008.5.4.232 20046343
44. DeCarli C, Mungas D, Harvey D, Reed B, Weiner M, Chui H, et al. Memory impairment, but not cerebrovascular disease, predicts progression of MCI to dementia. Neurology. 2004;63(2):220–7. doi: 10.1212/01.wnl.0000130531.90205.ef 15277612
45. International Labour Office. International standard classification of occupations: ISCO-08. Volume 1: structure, group definitions and correspondence tables. Geneva: International Labour Office; 2012 [cited 2020 Jan 24]. Available from: https://www.ilo.org/wcmsp5/groups/public/—dgreports/—dcomm/—publ/documents/publication/wcms_172572.pdf.
46. Wenham PR, Price WH, Blandell G. Apolipoprotein E genotyping by one-stage PCR. Lancet. 1991;337(8750):1158–9.
47. Reiman EM, Chen K, Liu X, Bandy D, Yu M, Lee W, et al. Fibrillar amyloid-beta burden in cognitively normal people at 3 levels of genetic risk for Alzheimer’s disease. Proc Nati Acad Sci U S A. 2009;106(16):6820–5.
48. Choe YM, Sohn BK, Choi HJ, Byun MS, Seo EH, Han JY, et al. Association of homocysteine with hippocampal volume independent of cerebral amyloid and vascular burden. Neurobiol Aging. 2014;35(7):1519–25. doi: 10.1016/j.neurobiolaging.2014.01.013 24524964
49. Villeneuve S, Rabinovici GD, Cohn-Sheehy BI, Madison C, Ayakta N, Ghosh PM, et al. Existing Pittsburgh Compound-B positron emission tomography thresholds are too high: statistical and pathological evaluation. Brain. 2015;138(Pt 7):2020–33. doi: 10.1093/brain/awv112 25953778
50. Jack CR Jr, Wiste HJ, Weigand SD, Rocca WA, Knopman DS, Mielke MM, et al. Age-specific population frequencies of cerebral beta-amyloidosis and neurodegeneration among people with normal cognitive function aged 50–89 years: a cross-sectional study. Lancet Neurol. 2014;13(10):997–1005. doi: 10.1016/S1474-4422(14)70194-2 25201514
51. Hsu DC, Mormino EC, Schultz AP, Amariglio RE, Donovan NJ, Rentz DM, et al. Lower late-life body-mass index is associated with higher cortical amyloid burden in clinically normal elderly. J Alzheimers Dis. 2016;53(3):1097–105. doi: 10.3233/JAD-150987 27340843
52. Zizza CA, Ellison KJ, Wernette CM. Total water intakes of community-living middle-old and oldest-old adults. J Gerontol A Biol Sci Med Sci. 2009;64(4):481–6. doi: 10.1093/gerona/gln045 19213852
53. Verbaten MN. Chronic effects of low to moderate alcohol consumption on structural and functional properties of the brain: beneficial or not? Hum Psychopharmacol. 2009;24(3):199–205. doi: 10.1002/hup.1022 19330800
54. Rao R, Draper B. Alcohol-related brain damage in older people. Lancet Psychiatry. 2015;2(8):674–5. doi: 10.1016/S2215-0366(15)00215-1 26249282
55. Moselhy HF, Georgiou G, Kahn A. Frontal lobe changes in alcoholism: a review of the literature. Alcohol Alcohol. 2001;36(5):357–68. doi: 10.1093/alcalc/36.5.357 11524299
56. Jansen WJ, Ossenkoppele R, Knol DL, Tijms BM, Scheltens P, Verhey FR, et al. Prevalence of cerebral amyloid pathology in persons without dementia: a meta-analysis. JAMA. 2015;313(19):1924–38. doi: 10.1001/jama.2015.4668 25988462
57. Herzog AR. Methodological issues in survey research with older Americans. In: Linsansky Gomberg ES, Hegedus AM, Zucker RA, editors. Alcohol problems and ageing. Bethesda (MD): National Institute on Alcohol Abuse and Alcoholism; 1998. pp. 25–39.
58. Leyhe T, Muller S, Milian M, Eschweiler GW, Saur R. Impairment of episodic and semantic autobiographical memory in patients with mild cognitive impairment and early Alzheimer’s disease. Neuropsychologia. 2009;47(12):2464–9. doi: 10.1016/j.neuropsychologia.2009.04.018 19409401
Článek vyšel v časopise
PLOS Medicine
2020 Číslo 2
- Distribuce a lokalizace speciálně upravených exosomů může zefektivnit léčbu svalových dystrofií
- O krok blíže k pochopení efektu placeba při léčbě bolesti
- Prof. Jan Škrha: Metformin je bezpečný, ale je třeba jej bezpečně užívat a léčbu kontrolovat
- FDA varuje před selfmonitoringem cukru pomocí chytrých hodinek. Jak je to v Česku?
- Vánoční dárky s přidanou hodnotou pro zdraví – nechte se inspirovat a poraďte svým pacientům
Nejčtenější v tomto čísle
- Virological suppression and clinical management in response to viremia in South African HIV treatment program: A multicenter cohort study
- Digitally enabled aged care and neurological rehabilitation to enhance outcomes with Activity and MObility UsiNg Technology (AMOUNT) in Australia: A randomised controlled trial
- The effect of assessing genetic risk of prostate cancer on the use of PSA tests in primary care: A cluster randomized controlled trial
- An evaluation of Chile’s Law of Food Labeling and Advertising on sugar-sweetened beverage purchases from 2015 to 2017: A before-and-after study