{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,7,30]],"date-time":"2026-07-30T01:38:10Z","timestamp":1785375490107,"version":"3.55.0"},"reference-count":31,"publisher":"American Diabetes Association","issue":"4","content-domain":{"domain":["diabetesjournals.org"],"crossmark-restriction":true},"short-container-title":[],"published-print":{"date-parts":[[2004,4,1]]},"abstract":"<jats:p>OBJECTIVE\u2014Cardiovascular autonomic neuropathy is associated with microalbuminuria in young and middle-aged patients with type 2 diabetes. We examined this relationship and the potential mediating role of blood pressure in older patients.<\/jats:p>\n               <jats:p>RESEARCH DESIGN AND METHODS\u2014At least two of three components of cardiovascular autonomic testing were completed by 132 patients (mean age 70 \u00b1 5.6 years). Relative rankings on each of the components were averaged to create a summary heart rate variability (HRV) measure. The urine microalbumin-to-creatinine ratio (milligrams albumin\/grams creatinine) was calculated. Blood pressure was measured at rest and by 24-h ambulatory recording.<\/jats:p>\n               <jats:p>RESULTS\u2014Urine microalbumin-to-creatinine ratio was higher in those with lower HRV (mean urine microalbumin-to-creatinine ratio 28, 56, and 191 mg\/g from the highest to lowest tertile of HRV; P &amp;lt; 0.0001). Resting and ambulatory blood pressure levels were negatively correlated with HRV and positively correlated with urine microalbumin-to-creatinine ratio. In multivariate analysis adjusting for age, duration of diabetes, HbA1c, and HDL cholesterol, HRV and blood pressure were both independently associated with urine microalbumin-to-creatinine ratio, with no evidence that either mediates the effect of the other.<\/jats:p>\n               <jats:p>CONCLUSIONS\u2014Cardiovascular autonomic neuropathy and blood pressure are independently associated with microalbuminuria in older patients with type 2 diabetes.<\/jats:p>","DOI":"10.2337\/diacare.27.4.972","type":"journal-article","created":{"date-parts":[[2007,3,5]],"date-time":"2007-03-05T22:51:27Z","timestamp":1173135087000},"page":"972-977","update-policy":"https:\/\/doi.org\/10.2337\/ada-journal-policies","source":"Crossref","is-referenced-by-count":42,"title":["Cardiovascular Autonomic Neuropathy Is Associated With Microalbuminuria in Older Patients With Type 2 Diabetes"],"prefix":"10.2337","volume":"27","author":[{"given":"Andrew","family":"Moran","sequence":"first","affiliation":[{"name":"Division of General Medicine, Department of Medicine, Columbia University College of Physicians & Surgeons, New York, New York"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Walter","family":"Palmas","sequence":"additional","affiliation":[{"name":"Division of General Medicine, Department of Medicine, Columbia University College of Physicians & Surgeons, New York, New York"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Lesley","family":"Field","sequence":"additional","affiliation":[{"name":"Division of General Medicine, Department of Medicine, Columbia University College of Physicians & Surgeons, New York, New York"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jyoti","family":"Bhattarai","sequence":"additional","affiliation":[{"name":"Joslin Diabetes Center, SUNY Upstate Medical University, Syracuse, New York"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Joseph E.","family":"Schwartz","sequence":"additional","affiliation":[{"name":"Department of Psychiatry and Behavioral Science, State University of New York at Stony Brook, Stony Brook, New York"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ruth S.","family":"Weinstock","sequence":"additional","affiliation":[{"name":"Joslin Diabetes Center, SUNY Upstate Medical University, Syracuse, New York"},{"name":"Department of Veterans Affairs Medical Center, Syracuse, New York"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Steven","family":"Shea","sequence":"additional","affiliation":[{"name":"Division of General Medicine, Department of Medicine, Columbia University College of Physicians & Surgeons, New York, New York"},{"name":"Department of Epidemiology, Mailman School of Public Health, Columbia University, New York, New York"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1167","reference":[{"key":"2022031216032234500_R1","doi-asserted-by":"crossref","unstructured":"Neil HAW, Thompson AV, John S, McCarthy ST, Mann JI: Diabetic autonomic neuropathy: the prevalence of impaired heart rate variability in a geographically defined population. Diabet Med\u20086:20\u201324, 1989","DOI":"10.1111\/j.1464-5491.1989.tb01133.x"},{"key":"2022031216032234500_R2","doi-asserted-by":"crossref","unstructured":"Zeigler D: The epidemiology of diabetic neuropathy. J Diabetes Complications\u20086:49\u201357, 1992","DOI":"10.1016\/1056-8727(92)90049-Q"},{"key":"2022031216032234500_R3","doi-asserted-by":"crossref","unstructured":"Gerritsen J, Dekker JM, TenVoorde BJ, Kostense PJ, Heine RJ, Bouter LM, Heethaar RM, Stehouwer CD: Impaired autonomic function is associated with increased mortality, especially in subjects with diabetes, hypertension, or a history of cardiovascular disease. Diabetes Care\u200824:1793\u20131798, 2001","DOI":"10.2337\/diacare.24.10.1793"},{"key":"2022031216032234500_R4","doi-asserted-by":"crossref","unstructured":"Haffner SM, Lehto S, Ronnemaa T, Pyorala K, Laakso M: Mortality from coronary heart disease in subjects with type 2 diabetes and without prior myocardial infarction. N Engl J Med\u2008339:229\u2013234, 1998","DOI":"10.1056\/NEJM199807233390404"},{"key":"2022031216032234500_R5","doi-asserted-by":"crossref","unstructured":"Chen HS, Hwu CM, Kuo BI, Chiang SC, Kwok CF, Lee SH, Lee YS, Weih MJ, Hsiao LC, Lin SH, Ho LT: Abnormal cardiovascular reflex tests are predictors of mortality in type 2 diabetes mellitus. Diabet Med\u200818:268\u2013273, 2001","DOI":"10.1046\/j.1464-5491.2001.00442.x"},{"key":"2022031216032234500_R6","doi-asserted-by":"crossref","unstructured":"Ewing D, Martyn C, Young R, Clarke BF: The value of cardiovascular autonomic function tests: 10 years of experience in diabetes. Diabetes Care\u20088:491\u2013498, 1985","DOI":"10.2337\/diacare.8.5.491"},{"key":"2022031216032234500_R7","doi-asserted-by":"crossref","unstructured":"Kahn R: Proceedings of a consensus development conference on standardized measures in diabetic neuropathy: autonomic nervous system testing. Diabetes Care\u200815:1095\u20131103, 1992","DOI":"10.2337\/diacare.15.8.1095"},{"key":"2022031216032234500_R8","doi-asserted-by":"crossref","unstructured":"Smulders Y, Jager A, Gerritsen J, Dekker JM, Nijpels G, Heine RJ, Bouter LM, Stehouwer C: Cardiovascular autonomic function is associated with (micro-)albuminuria in elderly Caucasion subjects with impaired glucose tolerance or type 2 diabetes: the Hoorn Study. Diabetes Care\u200823:1368\u20131375, 2000","DOI":"10.2337\/diacare.23.9.1369"},{"key":"2022031216032234500_R9","doi-asserted-by":"crossref","unstructured":"Zander E, Schulz B, Heinke P, Grimmberger E, Zander G: Importance of cardiovascular autonomic dysfunction in IDDM subjects with diabetic nephropathy. Diabetes Care\u200812:259\u2013264, 1989","DOI":"10.2337\/diacare.12.4.259"},{"key":"2022031216032234500_R10","doi-asserted-by":"crossref","unstructured":"Spallone V, Gambardella S, Maiello MR, Barini A, Frontoni S, Menzinger G: Relationship between autonomic neuropathy, 24-hour blood pressure profile, and nephropathy in normotensive IDDM patients. Diabetes Care\u200817:578\u2013584, 1994","DOI":"10.2337\/diacare.17.6.578"},{"key":"2022031216032234500_R11","doi-asserted-by":"crossref","unstructured":"Sundvist G, Lilja B: Autonomic neuropathy predicts deterioration in glomerular filtration rate in patients with IDDM. Diabetes Care\u200816:773\u2013779, 1993","DOI":"10.2337\/diacare.16.5.773"},{"key":"2022031216032234500_R12","doi-asserted-by":"crossref","unstructured":"Weinrauch LA, Kennedy FP, Gleason RE, Keogh J, D\u2019Elia JA: Relationship between autonomic function and progression of renal disease in diabetic proteinuria: clinical correlations and implications for blood pressure control. Am J Hypertens\u200811:302\u2013308, 1998","DOI":"10.1016\/S0895-7061(97)00472-X"},{"key":"2022031216032234500_R13","doi-asserted-by":"crossref","unstructured":"Forsblom CM, Groop PH, Ekstrand A, Totterman KJ, Sane T, Saloranta C, Groop L: Predictors of progression from normoalbuminuria to microalbuminuria in NIDDM. Diabetes Care\u200821:1932\u20131938, 1998","DOI":"10.2337\/diacare.21.11.1932"},{"key":"2022031216032234500_R14","doi-asserted-by":"crossref","unstructured":"Gerstein HC, Mann JFE, Yi Q, Zinman B, Dinneen SF, Hoogwerf B, Halle JP, Young J, Rashkow A, Joyce C, Nawaz S, Yusuf S, HOPE Study Investigators: Albuminuria and risk of cardiovascular events, death, and heart failure in diabetic and nondiabetic individuals. JAMA\u2008286:421\u2013426, 2001","DOI":"10.1001\/jama.286.4.421"},{"key":"2022031216032234500_R15","doi-asserted-by":"crossref","unstructured":"Nakano S, Uchida K, Kigoshi T, Azukizawa S, Iwasaki R, Kaneko M, Morimoto S: Circadian rhythm of blood pressure in normotensive NIDDM subjects: its relationship to microvascular complications. Diabetes Care\u200814:707\u2013711, 1991","DOI":"10.2337\/diacare.14.8.707"},{"key":"2022031216032234500_R16","doi-asserted-by":"crossref","unstructured":"Lurbe E, Redon J, Kesani A, Pascual JM, Tacons J, Alvarez V, Batlle D: Increase in nocturnal blood pressure and progression to microalbuminuria in type 1 diabetes. N Engl J Med\u2008347:797\u2013805, 2002","DOI":"10.1056\/NEJMoa013410"},{"key":"2022031216032234500_R17","doi-asserted-by":"crossref","unstructured":"Shea S, Starren J, Weinstock RS, Knudson PE, Teresi J, Holmes D, Palmas W, Field L, Goland R, Tuck C, Hripcsak G, Capps L, Liss D: Columbia University\u2019s Informatics for Diabetes Education and Telemedicine (IDEATel) Project: rationale and design. J Am Med Informat Assoc\u20089:49\u201362, 2002","DOI":"10.1136\/jamia.2002.0090049"},{"key":"2022031216032234500_R18","doi-asserted-by":"crossref","unstructured":"Pickering TG: Ambulatory Blood Pressure. Redmond, WA, Spacelabs Medical, 1994","DOI":"10.1097\/00004872-199412001-00007"},{"key":"2022031216032234500_R19","doi-asserted-by":"crossref","unstructured":"Roman MJ, Pickering TG, Schwartz JE, Cavallini MC, Pini R, Devereux RB: Is the absence of normal nocturnal fall in blood pressure (nondipping) associated with cardiovascular target organ damage? J Hypertens\u200815:969\u2013978, 1997","DOI":"10.1097\/00004872-199715090-00007"},{"key":"2022031216032234500_R20","doi-asserted-by":"crossref","unstructured":"Kario K, Eguchi K, Nakagawa Y, Motai K, Shimada K: Relationship between extreme dippers and orthostatic hypotension in elderly hypertensive patients. Hypertension\u200831:77\u201392, 1998","DOI":"10.1161\/01.HYP.31.1.77"},{"key":"2022031216032234500_R21","doi-asserted-by":"crossref","unstructured":"Risk M, Bril V, Broadbridge C, Cohen A: Heart rate variability measurement in diabetic neuropathy: review of methods. Diabetes Technol Ther\u20083:63\u201376, 2001","DOI":"10.1089\/152091501750220028"},{"key":"2022031216032234500_R22","doi-asserted-by":"crossref","unstructured":"Consensus Statement: Report and recommendations of the San Antonio Conference on Diabetic Neuropathy. Diabetes\u200837:1000\u20131004, 1988","DOI":"10.2337\/diab.37.7.1000"},{"key":"2022031216032234500_R23","doi-asserted-by":"crossref","unstructured":"American Diabetes Association: Consensus development conference on the diagnosis and management of nephropathy in patients with diabetes mellitus (Consensus Statement). Diabetes Care\u200817:1357\u20131361, 1994","DOI":"10.2337\/diacare.17.11.1357"},{"key":"2022031216032234500_R24","doi-asserted-by":"crossref","unstructured":"Hilsted J: Pathophysiology in diabetic autonomic neuropathy: cardiovascular, hormonal, and metabolic studies. Diabetes\u200831:730\u2013737, 1982","DOI":"10.2337\/diab.31.8.730"},{"key":"2022031216032234500_R25","doi-asserted-by":"crossref","unstructured":"Winocour PH, Dhar H, Anderson DC: The relationship between autonomic neuropathy and urinary sodium and albumin excretion in insulin-treated diabetics. Diabet Med\u20083:436\u2013440, 1986","DOI":"10.1111\/j.1464-5491.1986.tb00786.x"},{"key":"2022031216032234500_R26","doi-asserted-by":"crossref","unstructured":"Strojek K, Grzeszczak W, Gorska J, Leschinger MI, Ritz E: Lowering of microalbuminuria in diabetic patients by a sympathicoplegic agent: novel approach to prevent diabetic nephropathy? J Am Soc Nephrol\u200812:602\u2013605, 2001","DOI":"10.1681\/ASN.V123602"},{"key":"2022031216032234500_R27","doi-asserted-by":"crossref","unstructured":"Niskansen LK, Penttila I, Parviainen M, Uusitupa MIJ: Evolution, risk factors, and prognostic implications of albuminuria in NIDDM. Diabetes Care\u200819:486\u2013493, 1996","DOI":"10.2337\/diacare.19.5.486"},{"key":"2022031216032234500_R28","unstructured":"Gerstein HC, Mann JFE, Pogue J, Dinneen SF, Halle JP, Hoogwerf B, Joyce C, Rashkow A, Young J, Zinman B, Yusuf S: Prevalence and determinants of microalbuminuria in high-risk diabetic and nondiabetic patients in the Heart Outcomes Prevention Evaluation study. Diabetes Care\u200823(Suppl. 2):B35\u2013B39, 2000"},{"key":"2022031216032234500_R29","doi-asserted-by":"crossref","unstructured":"Torbjornsdotter TB, Jaremko GA, Berg UB: Ambulatory blood pressure and heart rate in relation to kidney structure and metabolic control in adolescents with type 1 diabetes. Diabetologia\u200844:865\u2013873, 2001","DOI":"10.1007\/s001250100528"},{"key":"2022031216032234500_R30","doi-asserted-by":"crossref","unstructured":"Nielsen S, Schmitz A, Poulsen PL, Hansen KW, Mogensen CE: Albuminuria and 24-hour ambulatory blood pressure in normoalbuminuric and microalbuminuric NIDDM patients: a longitudinal study. Diabetes Care\u200818:1434\u20131441, 1995","DOI":"10.2337\/diacare.18.11.1434"},{"key":"2022031216032234500_R31","doi-asserted-by":"crossref","unstructured":"Zelmanovitz T, Gross JL, Oliveira JR, Paggi A, Tatsch M, Azevedo MJ: The receiver operating characteristics curve in the evaluation of a random urine specimen as a screening test for diabetic nephropathy. Diabetes Care\u200820:516\u2013519, 1997","DOI":"10.2337\/diacare.20.4.516"}],"container-title":["Diabetes Care"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/diabetesjournals.org\/care\/article-pdf\/27\/4\/972\/562117\/zdc00404000972.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"syndication"},{"URL":"https:\/\/diabetesjournals.org\/care\/article-pdf\/27\/4\/972\/562117\/zdc00404000972.pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2022,3,12]],"date-time":"2022-03-12T16:21:05Z","timestamp":1647102065000},"score":1,"resource":{"primary":{"URL":"https:\/\/diabetesjournals.org\/care\/article\/27\/4\/972\/23259\/Cardiovascular-Autonomic-Neuropathy-Is-Associated"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2004,4,1]]},"references-count":31,"journal-issue":{"issue":"4","published-print":{"date-parts":[[2004,4,1]]}},"URL":"https:\/\/doi.org\/10.2337\/diacare.27.4.972","relation":{},"ISSN":["0149-5992","1935-5548"],"issn-type":[{"value":"0149-5992","type":"print"},{"value":"1935-5548","type":"electronic"}],"subject":[],"published":{"date-parts":[[2004,4,1]]}}}