{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,20]],"date-time":"2026-10-20T21:48:08Z","timestamp":1792532888347,"version":"4.5.0"},"reference-count":36,"publisher":"Springer Science and Business Media LLC","issue":"9","license":[{"start":{"date-parts":[[2018,6,30]],"date-time":"2018-06-30T00:00:00Z","timestamp":1530316800000},"content-version":"tdm","delay-in-days":0,"URL":"http:\/\/www.springer.com\/tdm"}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["Diabetologia"],"published-print":{"date-parts":[[2018,9]]},"DOI":"10.1007\/s00125-018-4668-1","type":"journal-article","created":{"date-parts":[[2018,6,30]],"date-time":"2018-06-30T03:28:08Z","timestamp":1530329288000},"page":"1956-1965","update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":99,"title":["Severe hypoglycaemia, mild cognitive impairment, dementia and brain volumes in older adults with type 2 diabetes: the Atherosclerosis Risk in Communities (ARIC) cohort study"],"prefix":"10.1007","volume":"61","author":[{"given":"Alexandra K.","family":"Lee","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Andreea M.","family":"Rawlings","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Clare J.","family":"Lee","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Alden L.","family":"Gross","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Elbert S.","family":"Huang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"A. Richey","family":"Sharrett","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Josef","family":"Coresh","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Elizabeth","family":"Selvin","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"297","published-online":{"date-parts":[[2018,6,30]]},"reference":[{"key":"4668_CR1","doi-asserted-by":"publisher","first-page":"1384","DOI":"10.2337\/dc12-2480","volume":"36","author":"ER Seaquist","year":"2013","unstructured":"Seaquist ER, Anderson J, Childs B et al (2013) Hypoglycemia and diabetes: a report of a workgroup of the American Diabetes Association and the Endocrine society. Diabetes Care 36:1384\u20131395","journal-title":"Diabetes Care"},{"key":"4668_CR2","doi-asserted-by":"crossref","unstructured":"American Diabetes Association (2017) Standards of Medical Care in Diabetes -- 2017. Diabetes Care 40(Supp 1)","DOI":"10.2337\/dc17-er07d"},{"key":"4668_CR3","doi-asserted-by":"publisher","first-page":"493","DOI":"10.1111\/j.1463-1326.2004.00421.x","volume":"7","author":"RE Warren","year":"2005","unstructured":"Warren RE, Frier BM (2005) Hypoglycemia and cognitive function. Diabetes Obes Metab 7:493\u2013503","journal-title":"Diabetes Obes Metab"},{"key":"4668_CR4","doi-asserted-by":"publisher","first-page":"559","DOI":"10.3174\/ajnr.A1856","volume":"31","author":"E Kang","year":"2010","unstructured":"Kang E, Jeon S, Choi S, Song C, Yu I (2010) Diffusion MR imaging OF hypoglycemic encephalopathy. Am J Neuroradiol 31:559\u2013564","journal-title":"Am J Neuroradiol"},{"key":"4668_CR5","doi-asserted-by":"publisher","first-page":"641","DOI":"10.1007\/s00234-009-0544-5","volume":"51","author":"JH Ma","year":"2009","unstructured":"Ma JH, Kim YJ, Yoo WJ et al (2009) MR imaging of hypoglycemic encephalopathy: lesion distribution and prognosis prediction by diffusion-weighted imaging. Neuroradiology 51:641\u2013649","journal-title":"Neuroradiology"},{"key":"4668_CR6","doi-asserted-by":"publisher","first-page":"1565","DOI":"10.1001\/jama.2009.460","volume":"301","author":"RA Whitmer","year":"2009","unstructured":"Whitmer RA, Karter AJ, Yaffe K, Quesenberry CP Jr, Selby JV (2009) Hypoglycemic episodes and risk of dementia in older patients with type 2 diabetes mellitus. JAMA 301:1565\u20131572","journal-title":"JAMA"},{"key":"4668_CR7","doi-asserted-by":"publisher","first-page":"1300","DOI":"10.1001\/jamainternmed.2013.6176","volume":"173","author":"K Yaffe","year":"2013","unstructured":"Yaffe K, Falvey CM, Hamilton N et al (2013) Association between hypoglycemia and dementia in a biracial cohort of older adults with diabetes mellitus. JAMA Intern Med 173:1300\u20131306","journal-title":"JAMA Intern Med"},{"key":"4668_CR8","doi-asserted-by":"publisher","first-page":"102","DOI":"10.1111\/joim.12000","volume":"273","author":"CH Lin","year":"2013","unstructured":"Lin CH, Sheu WHH (2013) Hypoglycaemic episodes and risk of dementia in diabetes mellitus: 7-year follow-up study. J Intern Med 273:102\u2013110","journal-title":"J Intern Med"},{"key":"4668_CR9","doi-asserted-by":"publisher","first-page":"1808","DOI":"10.1007\/s00125-009-1437-1","volume":"52","author":"DG Bruce","year":"2009","unstructured":"Bruce DG, Davis WA, Casey GP et al (2009) Severe hypoglycaemia and cognitive impairment in older patients with diabetes: the Fremantle Diabetes Study. Diabetologia 52:1808\u20131815","journal-title":"Diabetologia"},{"key":"4668_CR10","doi-asserted-by":"publisher","first-page":"507","DOI":"10.2337\/dc13-1384","volume":"37","author":"I Feinkohl","year":"2014","unstructured":"Feinkohl I, Aung PP, Keller M et al (2014) Severe hypoglycemia and cognitive decline in older people with type 2 diabetes: the Edinburgh type 2 diabetes study. Diabetes Care 37:507\u2013515","journal-title":"Diabetes Care"},{"key":"4668_CR11","doi-asserted-by":"publisher","first-page":"1842","DOI":"10.1056\/NEJMoa066397","volume":"356","author":"Diabetes Control and Complications Trial\/Epidemiology of Diabetes Interventions and Complications (DCCT\/EDIC) Study Research Group","year":"2007","unstructured":"Diabetes Control and Complications Trial\/Epidemiology of Diabetes Interventions and Complications (DCCT\/EDIC) Study Research Group (2007) Long-term effect of diabetes and its treatment on cognitive function. N Engl J Med 356:1842\u20131852","journal-title":"N Engl J Med"},{"key":"4668_CR12","unstructured":"National Institute of Neurological Disorders and Stroke. Dementia information page. Available from \n                    www.ninds.nih.gov\/disorders\/all-disorders\/dementia-information-page#disorders-r1\n                    \n                  ? Accessed 7 Apr 2018"},{"key":"4668_CR13","doi-asserted-by":"publisher","first-page":"135","DOI":"10.1111\/dom.12587","volume":"18","author":"K Mattishent","year":"2016","unstructured":"Mattishent K, Loke YK (2016) Bi-directional interaction between hypoglycaemia and cognitive impairment in elderly patients treated with glucose-lowering agents: a systematic review and meta-analysis. Diabetes Obes Metab 18:135\u2013141","journal-title":"Diabetes Obes Metab"},{"key":"4668_CR14","doi-asserted-by":"publisher","first-page":"787","DOI":"10.2337\/dc11-1855","volume":"35","author":"Z Punthakee","year":"2012","unstructured":"Punthakee Z, Miller ME, Launer LJ et al (2012) Poor cognitive function and risk of severe hypoglycemia in type 2 diabetes: post hoc epidemiologic analysis of the ACCORD trial. Diabetes Care 35:787\u2013793","journal-title":"Diabetes Care"},{"key":"4668_CR15","doi-asserted-by":"publisher","first-page":"2328","DOI":"10.1007\/s00125-009-1484-7","volume":"52","author":"BE Galan De","year":"2009","unstructured":"De Galan BE, Zoungas S, Chalmers J et al (2009) Cognitive function and risks of cardiovascular disease and hypoglycaemia in patients with type 2 diabetes: the action in diabetes and vascular disease: preterax and diamicron modified release controlled evaluation (ADVANCE) trial. Diabetologia 52:2328\u20132336","journal-title":"Diabetologia"},{"key":"4668_CR16","doi-asserted-by":"publisher","first-page":"1661","DOI":"10.2337\/dc17-0819","volume":"40","author":"AK Lee","year":"2017","unstructured":"Lee AK, Lee CJ, Huang ES, Sharrett AR (2017) Risk factors for severe hypoglycemia in black and white adults with diabetes: the Atherosclerosis Risk in Communities (ARIC) Study. Diabetes Care 40:1661\u20131667","journal-title":"Diabetes Care"},{"key":"4668_CR17","doi-asserted-by":"publisher","first-page":"73","DOI":"10.1016\/j.diabres.2015.10.026","volume":"112","author":"N Prinz","year":"2015","unstructured":"Prinz N, Stingl J, Dapp A et al (2015) High rate of hypoglycemia in 6770 type 2 diabetes patients with comorbid dementia: a multicenter cohort study on 215,932 patients from the German\/Austrian diabetes registry. Diabetes Res Clin Pract 112:73\u201381","journal-title":"Diabetes Res Clin Pract"},{"key":"4668_CR18","doi-asserted-by":"publisher","first-page":"785","DOI":"10.7326\/M14-0737","volume":"161","author":"AM Rawlings","year":"2014","unstructured":"Rawlings AM, Sharrett AR, Schneider ALC et al (2014) Diabetes in midlife and cognitive change over 20 years: a cohort study. Ann Intern Med 161:785\u2013793","journal-title":"Ann Intern Med"},{"key":"4668_CR19","doi-asserted-by":"publisher","first-page":"687","DOI":"10.1093\/oxfordjournals.aje.a115184","volume":"129","author":"ARIC Investigators","year":"1989","unstructured":"ARIC Investigators (1989) The Atherosclerosis Risk In Communities (ARIC) Study: design and objectives. Am J Epidemiol 129:687\u2013702","journal-title":"Am J Epidemiol"},{"key":"4668_CR20","doi-asserted-by":"publisher","first-page":"4","DOI":"10.1186\/1472-6823-8-4","volume":"8","author":"AA Ginde","year":"2008","unstructured":"Ginde AA, Blanc PG, Lieberman RM, Camargo CA (2008) Validation of ICD-9-CM coding algorithm for improved identification of hypoglycemia visits. BMC Endocr Disord 8:4","journal-title":"BMC Endocr Disord"},{"key":"4668_CR21","first-page":"1","volume":"2","author":"DS Knopman","year":"2016","unstructured":"Knopman DS, Gottesman RF, Sharrett AR et al (2016) Mild cognitive impairment and dementia prevalence: the Atherosclerosis Risk in Communities Neurocognitive Study (ARIC-NCS). Alzheimers Dement 2:1\u201311","journal-title":"Alzheimers Dement"},{"key":"4668_CR22","doi-asserted-by":"publisher","first-page":"1246","DOI":"10.1001\/jamaneurol.2017.1658","volume":"74","author":"RF Gottesman","year":"2017","unstructured":"Gottesman RF, Albert MS, Alonso A et al (2017) Associations between midlife vascular risk factors and 25-year incident dementia in the Atherosclerosis Risk in Communities (ARIC) Cohort. JAMA Neurol 74:1246\u20131254","journal-title":"JAMA Neurol"},{"key":"4668_CR23","doi-asserted-by":"publisher","first-page":"433","DOI":"10.1161\/STROKEAHA.114.007847","volume":"46","author":"DS Knopman","year":"2015","unstructured":"Knopman DS, Griswold ME, Lirette ST et al (2015) Vascular imaging abnormalities and cognition: mediation by cortical volume in nondemented individuals: Atherosclerosis risk in Communities-Neurocognitive Study. Stroke 46:433\u2013440","journal-title":"Stroke"},{"key":"4668_CR24","unstructured":"ARIC Investigators. ARIC Visit 5\/NCS Analysis Manual. Available from \n                    www2.cscc.unc.edu\/aric\/sites\/default\/files\/public\/listings\/V5%20NCS%20Analysis%20Manual_150901%20v1.pdf\n                    \n                  . Accessed 3 June 2017"},{"key":"4668_CR25","doi-asserted-by":"publisher","first-page":"878","DOI":"10.1097\/EDE.0000000000000379","volume":"26","author":"AL Gross","year":"2015","unstructured":"Gross AL, Power MC, Albert MS et al (2015) Application of latent variable methods to the study of cognitive decline when tests change over time. Epidemiology 26:878\u2013887","journal-title":"Epidemiology"},{"key":"4668_CR26","doi-asserted-by":"publisher","first-page":"1190","DOI":"10.1111\/jgs.14750","volume":"65","author":"MK Georgakis","year":"2017","unstructured":"Georgakis MK, Dimitriou NG, Karalexi MA (2017) Albuminuria in association with cognitive function and dementia: a systematic review and meta-analysis. J Am Geriatr Soc 65:1190\u20131198","journal-title":"J Am Geriatr Soc"},{"key":"4668_CR27","doi-asserted-by":"publisher","first-page":"2043","DOI":"10.1212\/WNL.0b013e31823b4765","volume":"77","author":"C Helmer","year":"2011","unstructured":"Helmer C, Stengel B, Metzger M et al (2011) Chronic kidney disease, cognitive decline, and incident dementia: the 3C Study. Neurology 77:2043\u20132051","journal-title":"Neurology"},{"key":"4668_CR28","doi-asserted-by":"publisher","first-page":"3279","DOI":"10.2337\/dc14-0973","volume":"37","author":"Z Zhang","year":"2014","unstructured":"Zhang Z, Lovato J, Battapady H et al (2014) Effect of hypoglycemia on brain structure in people with type 2 diabetes: epidemiological analysis of the ACCORD-MIND MRI Trial. Diabetes Care 37:3279\u20133285","journal-title":"Diabetes Care"},{"key":"4668_CR29","doi-asserted-by":"publisher","first-page":"611","DOI":"10.1016\/S0950-351X(05)80210-1","volume":"7","author":"RN Auer","year":"1993","unstructured":"Auer RN, Siesjo BK (1993) Hypoglycaemia: brain neurochemistry and neuropathology. Bailliere Clin Endocrinol Metab 7:611\u2013625","journal-title":"Bailliere Clin Endocrinol Metab"},{"key":"4668_CR30","doi-asserted-by":"publisher","first-page":"1514","DOI":"10.2337\/dc17-1185","volume":"40","author":"ALC Schneider","year":"2017","unstructured":"Schneider ALC, Selvin E, Sharrett AR et al (2017) Diabetes, prediabetes, and brain volumes and subclinical cerebrovascular disease on MRI: the Atherosclerosis Risk in Communities Neurocognitive Study (ARIC-NCS). Diabetes Care 40:1514\u20131521","journal-title":"Diabetes Care"},{"key":"4668_CR31","doi-asserted-by":"publisher","first-page":"246","DOI":"10.1016\/S2213-8587(13)70088-3","volume":"2","author":"GJ Biessels","year":"2014","unstructured":"Biessels GJ, Strachan MWJ, Visseren FLJ, Kappelle LJ, Whitmer RA (2014) Dementia and cognitive decline in type 2 diabetes and prediabetic stages: towards targeted interventions. Lancet Diabetes Endocrinol 2:246\u2013255","journal-title":"Lancet Diabetes Endocrinol"},{"key":"4668_CR32","doi-asserted-by":"publisher","first-page":"1154","DOI":"10.1001\/archneur.59.7.1154","volume":"59","author":"RS Wilson","year":"2002","unstructured":"Wilson RS, Schneider JA, Barnes LL et al (2002) The apolipoprotein E epsilon 4 allele and decline in different cognitive systems during a 6-year period. Arch Neurol 59:1154\u20131160","journal-title":"Arch Neurol"},{"key":"4668_CR33","doi-asserted-by":"publisher","first-page":"868","DOI":"10.1172\/JCI31669","volume":"117","author":"PE Cryer","year":"2007","unstructured":"Cryer PE (2007) Hypoglycemia, functional brain failure, and brain death. J Clin Invest 117:868\u2013870","journal-title":"J Clin Invest"},{"key":"4668_CR34","first-page":"3535","volume":"36","author":"AJ Karter","year":"2017","unstructured":"Karter AJ, Warton EM, Lipska KJ et al (2017) Development and validation of a tool to identify patients with type 2 diabetes at high risk of hypoglycemia-related emergency department or hospital use. JAMA Intern Med 36:3535\u20133542","journal-title":"JAMA Intern Med"},{"key":"4668_CR35","doi-asserted-by":"publisher","first-page":"1023","DOI":"10.1001\/jamainternmed.2016.2288","volume":"176","author":"MN Munshi","year":"2016","unstructured":"Munshi MN, Slyne C, Segal AR, Saul N, Lyons C, Weinger K (2016) Simplification of insulin regimen in older adults and risk of hypoglycemia. JAMA Intern Med 176:1023\u20131025","journal-title":"JAMA Intern Med"},{"key":"4668_CR36","doi-asserted-by":"publisher","first-page":"211","DOI":"10.2337\/ds16-0006","volume":"30","author":"VG Vimalananda","year":"2017","unstructured":"Vimalananda VG, DeSotto K, Chen T et al (2017) A quality improvement program to reduce potential overtreatment of diabetes among veterans at high risk of hypoglycemia. Diabetes Spectr 30:211\u2013216","journal-title":"Diabetes Spectr"}],"container-title":["Diabetologia"],"original-title":[],"language":"en","link":[{"URL":"http:\/\/link.springer.com\/article\/10.1007\/s00125-018-4668-1\/fulltext.html","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"http:\/\/link.springer.com\/content\/pdf\/10.1007\/s00125-018-4668-1.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"http:\/\/link.springer.com\/content\/pdf\/10.1007\/s00125-018-4668-1.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2019,6,30]],"date-time":"2019-06-30T00:02:32Z","timestamp":1561852952000},"score":1,"resource":{"primary":{"URL":"http:\/\/link.springer.com\/10.1007\/s00125-018-4668-1"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2018,6,30]]},"references-count":36,"journal-issue":{"issue":"9","published-print":{"date-parts":[[2018,9]]}},"alternative-id":["4668"],"URL":"https:\/\/doi.org\/10.1007\/s00125-018-4668-1","relation":{},"ISSN":["0012-186X","1432-0428"],"issn-type":[{"value":"0012-186X","type":"print"},{"value":"1432-0428","type":"electronic"}],"subject":[],"published":{"date-parts":[[2018,6,30]]},"assertion":[{"value":"16 February 2018","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"21 May 2018","order":2,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"30 June 2018","order":3,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"The authors declare that there is no duality of interest associated with this manuscript.","order":1,"name":"Ethics","group":{"name":"EthicsHeading","label":"Duality of interest"}}]}}