Cognitive decrement in older adults with symptomatic peripheral artery disease.
Brain aging
Cerebrovascular aging
Claudication
Neuropsychological tests
Peripheral artery disease
Vascular cognitive impairment
Journal
GeroScience
ISSN: 2509-2723
Titre abrégé: Geroscience
Pays: Switzerland
ID NLM: 101686284
Informations de publication
Date de publication:
10 2021
10 2021
Historique:
received:
06
05
2021
accepted:
09
08
2021
pubmed:
10
9
2021
medline:
27
1
2022
entrez:
9
9
2021
Statut:
ppublish
Résumé
Peripheral artery disease (PAD) is highly prevalent, affecting up to 20% of people over 70 years of age. To test the hypothesis that PAD promotes the pathogenesis of vascular cognitive impairment (VCI), we compared cognitive function in older adults with symptomatic PAD and in participants without PAD who had a burden of comorbid conditions. Furthermore, we compared the cognitive function of these groups after adjusting for demographic and clinical characteristics, comorbid conditions, and cardiovascular risk factors. Participants with PAD (age: 69 ± 8 years; n = 58) and those without PAD (age: 62 ± 8 years; n = 30) were assessed on a battery of eight neuropsychological tests. The tests assessed attention and working memory, verbal memory, non-verbal memory, perceptuo-motor speed, and executive function. Participants were further characterized on demographic and clinical characteristics, comorbid conditions, cardiovascular risk factors, and ankle-brachial index. The PAD group had significantly lower neuropsychological scores than the non-PAD control group on all eight tests (P < .01). After adjusting for covariates, significantly worse scores in the PAD group persisted for verbal memory, measured by tests on logical memory-immediate recall (P = .022), and logical memory-delayed recall (P < .001), and for attention and working memory, measured by tests on digits forward (P < .001), and digits backward (P = .003). Participants with symptomatic PAD have substantially lower levels of performance on tests of attention, working memory, and verbal memory than participants without PAD independent of demographic characteristics and comorbid health burdens. These findings provide additional evidence in support of the concept that generalized accelerated vascular aging manifesting as symptomatic PAD in the peripheral circulation also affects the brain promoting the pathogenesis of VCI. These cognitive difficulties may also negatively impact symptomatic patient's ability to understand and adhere to behavioral and medical therapies, creating a vicious cycle. We speculate that more intensive follow-up may be needed to promote adherence to therapies and monitor cognitive decline that may affect care.
Identifiants
pubmed: 34498199
doi: 10.1007/s11357-021-00437-8
pii: 10.1007/s11357-021-00437-8
pmc: PMC8599571
doi:
Types de publication
Journal Article
Research Support, N.I.H., Extramural
Research Support, Non-U.S. Gov't
Research Support, U.S. Gov't, Non-P.H.S.
Langues
eng
Sous-ensembles de citation
IM
Pagination
2455-2465Subventions
Organisme : NIA NIH HHS
ID : RF1 AG072295
Pays : United States
Organisme : NIA NIH HHS
ID : P30 AG028747
Pays : United States
Organisme : NIGMS NIH HHS
ID : P20 GM103447
Pays : United States
Organisme : NIA NIH HHS
ID : R01 AG068295
Pays : United States
Organisme : NIA NIH HHS
ID : P60 AG012583
Pays : United States
Organisme : NINDS NIH HHS
ID : R01 NS100782
Pays : United States
Informations de copyright
© 2021. American Aging Association.
Références
Fowkes FG, Rudan D, Rudan I, Aboyans V, Denenberg JO, McDermott MM, et al. Comparison of global estimates of prevalence and risk factors for peripheral artery disease in 2000 and 2010: a systematic review and analysis. Lancet. 2013;382:1329–40.
pubmed: 23915883
Hirsch AT, Hartman L, Town RJ, Virnig BA. National health care costs of peripheral arterial disease in the Medicare population. Vasc Med. 2008;13:209–15.
pubmed: 18687757
Regensteiner JG, Hiatt WR, Coll JR, Criqui MH, Treat-Jacobson D, McDermott MM, et al. The impact of peripheral arterial disease on health-related quality of life in the peripheral arterial disease awareness, risk, and treatment: new resources for survival (PARTNERS) Program. Vasc Med. 2008;13:15–24.
pubmed: 18372434
Criqui MH, Langer RD, Fronek A, Feigelson HS, Klauber MR, McCann TJ, et al. Mortality over a period of 10 years in patients with peripheral arterial disease. N Engl J Med. 1992;326:381–6.
pubmed: 1729621
Norgren L, Hiatt WR, Dormandy JA, Nehler MR, Harris KA, Fowkes FG. Inter-society consensus for the management of peripheral arterial disease (TASC II). J Vasc Surg. 2007;45 Suppl S:S5-67.
pubmed: 17223489
Gardner AW, Skinner JS, Cantwell BW, Smith LK. Progressive vs single-stage treadmill tests for evaluation of claudication. Med Sci Sports Exerc. 1991;23:402–8.
pubmed: 2056896
McDermott MM, Greenland P, Liu K, Guralnik JM, Criqui MH, Dolan NC, et al. Leg symptoms in peripheral arterial disease: associated clinical characteristics and functional impairment. JAMA. 2001;286:1599–606.
pubmed: 11585483
McDermott MM, Liu K, Greenland P, Guralnik JM, Criqui MH, Chan C, et al. Functional decline in peripheral arterial disease: associations with the ankle brachial index and leg symptoms. JAMA. 2004;292:453–61.
pubmed: 15280343
Sieminski DJ, Gardner AW. The relationship between free-living daily physical activity and the severity of peripheral arterial occlusive disease. Vasc Med. 1997;2:286–91.
pubmed: 9575600
Guerchet M, Aboyans V, Nubukpo P, Lacroix P, Clement JP, Preux PM. Ankle-brachial index as a marker of cognitive impairment and dementia in general population. A systematic review. Atherosclerosis. 2011;216:251–7.
pubmed: 21497350
Phillips NA, Mate-Kole CC. Cognitive deficits in peripheral vascular disease. A comparison of mild stroke patients and normal control subjects. Stroke. 1997;28:777–84.
pubmed: 9099196
Hofman A, Ott A, Breteler MM, Bots ML, Slooter AJ, van Harskamp F, et al. Atherosclerosis, apolipoprotein E, and prevalence of dementia and Alzheimer’s disease in the Rotterdam Study. Lancet. 1997;349:151–4.
pubmed: 9111537
Newman AB, Fitzpatrick AL, Lopez O, Jackson S, Lyketsos C, Jagust W, et al. Dementia and Alzheimer’s disease incidence in relationship to cardiovascular disease in the Cardiovascular Health Study cohort. J Am Geriatr Soc. 2005;53:1101–7.
pubmed: 16108925
Tasci I, Safer U, Naharci MI, Gezer M, Demir O, Bozoglu E, et al. Undetected peripheral arterial disease among older adults with Alzheimer’s disease and other dementias. Am J Alzheimers Dis Other Demen. 2018;33:5–11.
pubmed: 28786294
Waldstein SR, Tankard CF, Maier KJ, Pelletier JR, Snow J, Gardner AW, et al. Peripheral arterial disease and cognitive function. Psychosom Med. 2003;65:757–63.
pubmed: 14508017
Zimmermann LJ, Ferrucci L, Kiang L, Lu T, Guralnik JM, Criqui MH, et al. Poorer clock draw test scores are associated with greater functional impairment in peripheral artery disease: the Walking and Leg Circulation Study II. Vasc Med. 2011;16:173–81.
pubmed: 21636676
pmcid: 5076886
Virtanen J, Varpela M, Biancari F, Jalkanen J, Hakovirta H. Association between anatomical distribution of symptomatic peripheral artery disease and cerebrovascular disease. Vascular. 2020;28:295–300.
pubmed: 31980011
Rafnsson SB, Deary IJ, Fowkes FG. Peripheral arterial disease and cognitive function. Vasc Med. 2009;14:51–61.
pubmed: 19144780
Beckman JA, Duncan MS, Damrauer SM, Wells QS, Barnett JV, Wasserman DH, et al. Microvascular disease, peripheral artery disease, and amputation. Circulation. 2019;140:449–58.
pubmed: 31280589
pmcid: 6682431
Behroozian A, Beckman JA. Microvascular disease increases amputation in patients with peripheral artery disease. Arterioscler Thromb Vasc Biol. 2020;40:534–40.
pubmed: 32075418
Frisbee JC, Butcher JT, Frisbee SJ, Olfert IM, Chantler PD, Tabone LE, et al. Increased peripheral vascular disease risk progressively constrains perfusion adaptability in the skeletal muscle microcirculation. Am J Physiol Heart Circ Physiol. 2016;310:H488-504.
pubmed: 26702145
Igari K, Kudo T, Toyofuku T, Inoue Y. Endothelial dysfunction of patients with peripheral arterial disease measured by peripheral arterial tonometry. Int J Vasc Med. 2016;2016:3805380.
pubmed: 27853624
pmcid: 5088270
Yang C, Kwak L, Ballew SH, Jaar BG, Deal JA, Folsom AR, et al. Retinal microvascular findings and risk of incident peripheral artery disease: an analysis from the atherosclerosis risk in communities (ARIC) Study. Atherosclerosis. 2020;294:62–71.
pubmed: 31812251
Wintergerst MWM, Falahat P, Holz FG, Schaefer C, Schahab N, Finger R. Retinal vasculature assessed by OCTA in peripheral arterial disease. Invest Ophthalmol Vis Sci. 2020;61:3203.
Gardner AW, Montgomery PS, Parker DE. Metabolic syndrome impairs physical function, health-related quality of life, and peripheral circulation in patients with intermittent claudication. J Vasc Surg. 2006;43:1191–6.
pubmed: 16765237
Gardner AW, Montgomery PS. The effect of metabolic syndrome components on exercise performance in patients with intermittent claudication. J Vasc Surg. 2008;47:1251–8.
pubmed: 18407453
pmcid: 2453503
Waldstein SR, Manuck SB, Ryan CM, Muldoon MF. Neuropsychological correlates of hypertension: review and methodologic considerations. Psychol Bull. 1991;110:451–68.
pubmed: 1758919
Elias MF, Wolf PA, D’Agostino RB, Cobb J, White LR. Untreated blood pressure level is inversely related to cognitive functioning: the Framingham Study. Am J Epidemiol. 1993;138:353–64.
pubmed: 8213741
Toth P, Tarantini S, Csiszar A, Ungvari Z. Functional vascular contributions to cognitive impairment and dementia: mechanisms and consequences of cerebral autoregulatory dysfunction, endothelial impairment, and neurovascular uncoupling in aging. Am J Physiol Heart Circ Physiol. 2017;312:H1–20.
pubmed: 27793855
Ungvari Z, Toth P, Tarantini S, Prodan CI, Sorond F, Merkely B, et al. Hypertension-induced cognitive impairment: from pathophysiology to public health. Nat Rev Nephrol. 2021;1–16. https://doi.org/10.1038/s41581-021-00430-6 .
Desmond DW, Tatemichi TK, Paik M, Stern Y. Risk factors for cerebrovascular disease as correlates of cognitive function in a stroke-free cohort. Arch Neurol. 1993;50:162–6.
pubmed: 8431135
Elias PK, Elias MF, D’Agostino RB, Cupples LA, Wilson PW, Silbershatz H, et al. NIDDM and blood pressure as risk factors for poor cognitive performance. The Framingham Study. Diabetes Care. 1997;20:1388–95.
pubmed: 9283785
van Sloten TT, Sedaghat S, Carnethon MR, Launer LJ, Stehouwer CDA. Cerebral microvascular complications of type 2 diabetes: stroke, cognitive dysfunction, and depression. Lancet Diabetes Endocrinol. 2020;8:325–36.
pubmed: 32135131
Muldoon MF, Ryan CM, Matthews KA, Manuck SB. Serum cholesterol and intellectual performance. Psychosom Med. 1997;59:382–7.
pubmed: 9251158
Balasubramanian P, Kiss T, Tarantini S, Nyul-Toth A, Ahire C, Yabluchanskiy A, et al. Obesity-induced cognitive impairment in older adults: a microvascular perspective. Am J Physiol Heart Circ Physiol. 2021;320:H740–61.
pubmed: 33337961
Naderali EK, Ratcliffe SH, Dale MC. Obesity and Alzheimer’s disease: a link between body weight and cognitive function in old age. Am J Alzheimers Dis Other Demen. 2009;24:445–9.
pubmed: 19801534
Farmer ME, White LR, Abbott RD, Kittner SJ, Kaplan E, Wolz MM, et al. Blood pressure and cognitive performance. The Framingham Study. Am J Epidemiol. 1987;126:1103–14.
pubmed: 3687920
Scherr PA, Albert MS, Funkenstein HH, Cook NR, Hennekens CH, Branch LG, et al. Correlates of cognitive function in an elderly community population. Am J Epidemiol. 1988;128:1084–101.
pubmed: 3189282
Mangiafico RA, Sarnataro F, Mangiafico M, Fiore CE. Impaired cognitive performance in asymptomatic peripheral arterial disease: relation to C-reactive protein and D-dimer levels. Age Ageing. 2006;35:60–5.
pubmed: 16364935
Gardner AW, Parker DE, Montgomery PS, Blevins SM. Step-monitored home exercise improves ambulation, vascular function, and inflammation in symptomatic patients with peripheral artery disease: a randomized controlled trial. J Am Heart Assoc. 2014;3:e001107.
pubmed: 25237048
pmcid: 4323792
Folstein MF, Folstein SE, McHugh PR. Mini-mental state. A practical method for grading the cognitive state of patients for the clinician. J Psychiatr Res. 1975;12:189–98.
pubmed: 1202204
pmcid: 1202204
Aboyans V, Criqui MH, Abraham P, Allison MA, Creager MA, Diehm C, et al. Measurement and interpretation of the ankle-brachial index: a scientific statement from the American Heart Association. Circulation. 2012;126:2890–909.
pubmed: 23159553
Lohman TC, Roche AF, Marubini E. Anthropometric standardization reference manual. Champaign: Human Kinetics Books; 1988. p. 39–70.
Farah BQ, Ritti-Dias RM, Cucato GG, Montgomery PS, Gardner AW. Factors associated with sedentary behavior in patients with intermittent claudication. Eur J Vasc Endovasc Surg. 2016;52:809–14.
pubmed: 27769867
pmcid: 5136501
Expert panel on detection evaluation and treatment of high blood cholesterol in adults. Executive summary of the third report of The National Cholesterol Education Program (NCEP) Expert Panel on Detection, Evaluation, and Treatment of High Blood Cholesterol In Adults (Adult Treatment Panel III). JAMA. 2001;285:2486–97.
Gardner AW, Montgomery PS, Casanegra AI, Silva-Palacios F, Ungvari Z, Csiszar A. Association between gait characteristics and endothelial oxidative stress and inflammation in patients with symptomatic peripheral artery disease. Age. 2016;38:64.
pubmed: 27273077
pmcid: 5005916
Hirsch AT, Haskal ZJ, Hertzer NR, Bakal CW, Creager MA, Halperin JL, et al. ACC/AHA 2005 Practice Guidelines for the management of patients with peripheral arterial disease (lower extremity, renal, mesenteric, and abdominal aortic): a collaborative report from the American Association for Vascular Surgery/Society for Vascular Surgery, Society for Cardiovascular Angiography and Interventions, Society for Vascular Medicine and Biology, Society of Interventional Radiology, and the ACC/AHA Task Force on Practice Guidelines (Writing Committee to Develop Guidelines for the Management of Patients With Peripheral Arterial Disease): endorsed by the American Association of Cardiovascular and Pulmonary Rehabilitation; National Heart, Lung, and Blood Institute; Society for Vascular Nursing; TransAtlantic Inter-Society Consensus; and Vascular Disease Foundation. Circulation. 2006;113:e463–654.
pubmed: 16549646
National Kidney Foundation. K/DOQI clinical practice guidelines for chronic kidney disease: evaluation, classification, and stratification. Am J Kidney Dis. 2002;39:S1-266.
Montgomery PS, Gardner AW. The clinical utility of a six-minute walk test in peripheral arterial occlusive disease patients. J Am Geriatr Soc. 1998;46:706–11.
pubmed: 9625185
Singh-Manoux A, Britton AR, Marmot M. Vascular disease and cognitive function: evidence from the Whitehall II Study. J Am Geriatr Soc. 2003;51:1445–50.
pubmed: 14511166
Breteler MM, Claus JJ, Grobbee DE, Hofman A. Cardiovascular disease and distribution of cognitive function in elderly people: the Rotterdam Study. BMJ. 1994;308:1604–8.
pubmed: 8025427
pmcid: 2540432
Elwood PC, Pickering J, Bayer A, Gallacher JE. Vascular disease and cognitive function in older men in the Caerphilly cohort. Age Ageing. 2002;31:43–8.
pubmed: 11850307
Rejeski WJ, Tian L, Liao Y, McDermott MM. Social cognitive constructs and the promotion of physical activity in patients with peripheral artery disease. J Cardiopulm Rehabil Prev. 2008;28:65–72.
pubmed: 18277834
Thomas RJ, Beatty AL, Beckie TM, Brewer LC, Brown TM, Forman DE, et al. Home-based cardiac rehabilitation: a scientific statement from the American Association of Cardiovascular and Pulmonary Rehabilitation, the American Heart Association, and the American College of Cardiology. J Cardiopulm Rehabil Prev. 2019;39:208–25.
pubmed: 31082934
pmcid: 7530797
Rao R, Jackson S, Howard R. Neuropsychological impairment in stroke, carotid stenosis, and peripheral vascular disease, a comparison with healthy community residents. Stroke. 1999;30:2167–73.
pubmed: 10512923
Gardner AW, Parker DE, Webb N, Montgomery PS, Scott KJ, Blevins SM. Calf muscle hemoglobin oxygen saturation characteristics and exercise performance in patients with intermittent claudication. J Vasc Surg. 2008;48:644–9.
pubmed: 18572363
pmcid: 2759322
Gardner AW, Parker DE, Montgomery PS, Blevins SM, Nael R, Afaq A. Sex differences in calf muscle hemoglobin oxygen saturation in patients with intermittent claudication. J Vasc Surg. 2009;50:77–82.
pubmed: 19223136
pmcid: 2765784
Gardner AW, Parker DE, Montgomery PS, Khurana A, Ritti-Dias RM, Blevins SM. Calf muscle hemoglobin oxygen saturation in patients with peripheral artery disease who have different types of exertional leg pain. J Vasc Surg. 2012;55:1654–61.
pubmed: 22341835
pmcid: 3358574
Gardner AW, Parker DE, Montgomery PS, Sosnowska D, Casanegra AI, Esponda OL, et al. Impaired vascular endothelial growth factor A and inflammation in patients with peripheral artery disease. Angiology. 2014;65:683–90.
pubmed: 24006146
Gardner AW, Parker DE, Montgomery PS, Sosnowska D, Casanegra AI, Ungvari Z, et al. Greater endothelial apoptosis and oxidative stress in patients with peripheral artery disease. Int J Vasc Med. 2014;2014:160534.
pubmed: 24963409
pmcid: 4054861
Sorond FA, Hurwitz S, Salat DH, Greve DN, Fisher NDL. Neurovascular coupling, cerebral white matter integrity, and response to cocoa in older people. Neurology. 2013;81(10):904–9. https://doi.org/10.1212/WNL.0b013e3182a351aa .
doi: 10.1212/WNL.0b013e3182a351aa
pubmed: 23925758
pmcid: 3885215
Tarantini S, Hertelendy P, Tucsek Z, Valcarcel-Ares MN, Smith N, Menyhart A, et al. Pharmacologically-induced neurovascular uncoupling is associated with cognitive impairment in mice. J Cereb Blood Flow Metab. 2015;35:1871–81.
pubmed: 26174328
pmcid: 4635246
van der Veen PH, Muller M, Vincken KL, Witkamp TD, Mali WP, van der Graaf Y, et al. Longitudinal changes in brain volumes and cerebrovascular lesions on MRI in patients with manifest arterial disease: the SMART-MR study. J Neurol Sci. 2014;337:112–8.
pubmed: 24314719
Wang C, Fu K, Liu H, Xing F, Zhang S. Brain structural changes and their correlation with vascular disease in type 2 diabetes mellitus patients: a voxel-based morphometric study. Neural Regen Res. 2014;9:1548–56.
pubmed: 25317173
pmcid: 4192973
Bots ML, van Swieten JC, Breteler MM, de Jong PT, van Gijn J, Hofman A, et al. Cerebral white matter lesions and atherosclerosis in the Rotterdam Study. Lancet. 1993;341:1232–7.
pubmed: 8098390
Amar K, Lewis T, Wilcock G, Scott M, Bucks R. The relationship between white matter low attenuation on brain CT and vascular risk factors: a memory clinic study. Age Ageing. 1995;24:411–5.
pubmed: 8669345