{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,7,24]],"date-time":"2026-07-24T06:33:39Z","timestamp":1784874819154,"version":"3.55.0"},"reference-count":26,"publisher":"Georg Thieme Verlag KG","issue":"04","funder":[{"name":"Swedish research Council","award":["2021-01942"],"award-info":[{"award-number":["2021-01942"]}]},{"DOI":"10.13039\/501100001858","name":"VINNOVA","doi-asserted-by":"crossref","award":["2014-03422"],"award-info":[{"award-number":["2014-03422"]}],"id":[{"id":"10.13039\/501100001858","id-type":"DOI","asserted-by":"crossref"}]},{"DOI":"10.13039\/501100011077","name":"Sk\u00e5ne University Hospital","doi-asserted-by":"crossref","award":["URL N\/ A"],"award-info":[{"award-number":["URL N\/ A"]}],"id":[{"id":"10.13039\/501100011077","id-type":"DOI","asserted-by":"crossref"}]},{"name":"Swedish Diabetes Foundation","award":["DIA 2020-492"],"award-info":[{"award-number":["DIA 2020-492"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Exp Clin Endocrinol Diabetes"],"published-print":{"date-parts":[[2023,4]]},"abstract":"<jats:title>Abstract<\/jats:title><jats:p>\n          Background Diabetes is associated with systemic complications. Prevalence\n                    of diabetic nephropathy, and retinopathy, in type 1 diabetes mellitus (T1DM) is\n                    declining, but it is not known if this is true also for diabetic neuropathy.\n                    Aim: To investigate the relationship between large fibre diabetic neuropathy and\n                    other diabetic complications.<\/jats:p><jats:p>\n          Materials and methods Neuropathy, defined here as large fibre neuropathy,\n                    was assessed by measuring vibration perception thresholds at four different\n                    frequencies on the sole of the foot, using a standard VibroSense Meter\n                    and\/or neuropathic symptoms, in 599 individuals with T1DM. Retinopathy\n                    status was graded using the International Clinical Disease Severity Scale. Grade\n                    of albuminuria and previous history of any macrovascular complications were\n                    registered.<\/jats:p><jats:p>\n          Results Diabetic individuals without retinopathy had similar vibration\n                    thresholds as age- and gender-matched control participants without diabetes,\n                    whereas those without microalbuminuria had higher thresholds than controls. Two\n                    individuals out of 599 (0.3%) had microalbuminuria, but not retinopathy\n                    or neuropathy, and 12\/134 (9%) without retinopathy had signs of\n                    neuropathy. Totally 119\/536 (22%) of the patients without\n                    microalbuminuria had neuropathy. Vibration thresholds increased with the rising\n                    severity of retinopathy and grade of albuminuria. In a multinomial logistic\n                    regression analysis, neuropathy was associated with retinopathy (OR 2.96\n                    [1.35\u20136.49], p=0.007), nephropathy (OR 6.25\n                    [3.21\u201312.15]; p=6.7\u00d710\u20138) and macrovascular\n                    disease (OR 2.72 [1.50\u20134.93], p=0.001).<\/jats:p><jats:p>\n          Conclusions Despite recent changes in the incidence of diabetic\n                    complications, the onset of large fibre neuropathy follows that of retinopathy\n                    but precedes the onset of nephropathy in T1DM.<\/jats:p>","DOI":"10.1055\/a-2010-6987","type":"journal-article","created":{"date-parts":[[2023,1,11]],"date-time":"2023-01-11T00:07:46Z","timestamp":1673395666000},"page":"187-193","source":"Crossref","is-referenced-by-count":4,"title":["Diabetic Neuropathy Assessed with Multifrequency Vibrometry Develops\n                    Earlier than Nephropathy but Later than Retinopathy"],"prefix":"10.1055","volume":"131","author":[{"given":"Eero","family":"Lindholm","sequence":"additional","affiliation":[{"name":"Department of Clinical Sciences, Endocrinology, Lund University,\n                    Malm\u00f6, Sweden"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Linnea","family":"Ekman","sequence":"additional","affiliation":[{"name":"Department of Translational Medicine \u2013 Hand Surgery, Lund\n                    University, Malm\u00f6, Sweden"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Targ","family":"Elgzyri","sequence":"additional","affiliation":[{"name":"Department of Clinical Sciences, Endocrinology, Lund University,\n                    Malm\u00f6, Sweden"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Beata","family":"Lindholm","sequence":"additional","affiliation":[{"name":"Department of Clinical Sciences, Neurology, Lund University,\n                    Malm\u00f6, Sweden"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Magnus","family":"L\u00f6ndahl","sequence":"additional","affiliation":[{"name":"Department of Clinical Sciences, Endocrinology, Lund University, Lund,\n                    Sweden"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Lars","family":"Dahlin","sequence":"additional","affiliation":[{"name":"Department of Translational Medicine \u2013 Hand Surgery, Lund\n                    University, Malm\u00f6, Sweden"},{"name":"Department of Hand Surgery, Sk\u00e5ne University Hospital,\n                    Malm\u00f6, Sweden"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"194","published-online":{"date-parts":[[2023,2,16]]},"reference":[{"key":"ref1","doi-asserted-by":"publisher","first-page":"51","DOI":"10.1016\/j.dsx.2014.09.011","article-title":"Diabetic retinopathy \u2013 biomolecules and multiple pathophysiology","volume":"9","author":"H Ahsan","year":"2015","journal-title":"Diabetes Metab Syndr"},{"key":"ref2","doi-asserted-by":"publisher","first-page":"1425","DOI":"10.1007\/s12013-014-0365-y","article-title":"The role of oxidative stress in diabetic neuropathy: Generation of free radical\n                    species in the glycation reaction and gene polymorphisms encoding antioxidant\n                    enzymes to genetic susceptibility to diabetic neuropathy in population of type I\n                    diabetic patients","volume":"71","author":"M A Babizhayev","year":"2015","journal-title":"Cell Biochem Biophys"},{"key":"ref3","doi-asserted-by":"publisher","first-page":"1615","DOI":"10.2337\/diabetes.54.6.1615","article-title":"The pathobiology of diabetic complications: A unifying mechanism","volume":"54","author":"M Brownlee","year":"2005","journal-title":"Diabetes"},{"key":"ref4","doi-asserted-by":"publisher","first-page":"18","DOI":"10.1111\/j.2040-1124.2010.00070.x","article-title":"Mechanism of diabetic neuropathy: Where are we now and where to go?","volume":"2","author":"S Yagihashi","year":"2011","journal-title":"J Diabetes Investig"},{"key":"ref5","doi-asserted-by":"publisher","first-page":"146","DOI":"10.1046\/j.1464-5491.2000.00222.x","article-title":"The prevalence of multiple diabetes-related complications","volume":"17","author":"C L Morgan","year":"2000","journal-title":"Diabet Med"},{"key":"ref6","doi-asserted-by":"publisher","first-page":"1456","DOI":"10.2337\/diab.38.11.1456","article-title":"Epidemiological correlates of diabetic neuropathy. Report from Pittsburgh\n                    Epidemiology of Diabetes Complications Study. Diabetes","volume":"38","author":"R E Maser","year":"1989"},{"key":"ref7","doi-asserted-by":"publisher","first-page":"1677","DOI":"10.1016\/S0161-6420(03)00475-5","article-title":"Proposed international clinical diabetic retinopathy and diabetic macular edema\n                    disease severity scales","volume":"110","author":"C P Wilkinson","year":"2003","journal-title":"Ophthalmology"},{"key":"ref8","doi-asserted-by":"publisher","first-page":"2","DOI":"10.1111\/j.1524-6175.2004.4064.x","article-title":"Microalbuminuria: Definition, detection, and clinical significance","volume":"6","author":"R D Toto","year":"2004","journal-title":"J Clin Hypertens (Greenwich)"},{"key":"ref9","doi-asserted-by":"publisher","first-page":"136","DOI":"10.2337\/dc16-2042","article-title":"Diabetic neuropathy: A position statement by the American Diabetes\n                    Association","volume":"40","author":"R Pop-Busui","year":"2017","journal-title":"Diabetes Care"},{"key":"ref10","doi-asserted-by":"publisher","first-page":"1000","DOI":"10.2337\/db19-1046","article-title":"Risk factors for diabetic peripheral neuropathy and cardiovascular autonomic\n                    neuropathy in the Diabetes Control and Complications Trial\/Epidemiology\n                    of Diabetes Interventions and Complications (DCCT\/EDIC) Study","volume":"69","author":"B H Braffett","year":"2020","journal-title":"Diabetes"},{"key":"ref11","doi-asserted-by":"publisher","first-page":"38","DOI":"10.1111\/ane.13171","article-title":"Evaluation of small nerve fiber dysfunction in type 2 diabetes","volume":"141","author":"L Ekman","year":"2020","journal-title":"Acta Neurol Scand"},{"key":"ref12","doi-asserted-by":"publisher","first-page":"e0212921","DOI":"10.1371\/journal.pone.0212921","article-title":"Strong association between vibration perception thresholds at low frequencies (4\n                    and 8 Hz), neuropathic symptoms and diabetic foot ulcers","volume":"14","author":"E Lindholm","year":"2019","journal-title":"PLoS One"},{"key":"ref13","doi-asserted-by":"publisher","first-page":"e0196243","DOI":"10.1371\/journal.pone.0196243","article-title":"Impaired vibrotactile sense in children and adolescents with type 1 diabetes\n                    \u2013 Signs of peripheral neuropathy","volume":"13","author":"E Ising","year":"2018","journal-title":"PLoS One"},{"key":"ref14","doi-asserted-by":"publisher","DOI":"10.1007\/s00592-019-01450-2","article-title":"Improved metabolic control using glucose monitoring systems leads to improvement\n                    in vibration perception thresholds in type 1 diabetes patients","author":"L B Dahlin","year":"2019","journal-title":"Acta Diabetol"},{"key":"ref15","doi-asserted-by":"publisher","first-page":"3","DOI":"10.1007\/s00125-018-4711-2","article-title":"Global trends in diabetes complications: A review of current evidence","volume":"62","author":"J L Harding","year":"2019","journal-title":"Diabetologia"},{"key":"ref16","doi-asserted-by":"publisher","first-page":"496","DOI":"10.1007\/bf00284458","article-title":"Diabetic nephropathy in type 1 (insulin-dependent) diabetes: An epidemiological\n                    study","volume":"25","author":"A R Andersen","year":"1983","journal-title":"Diabetologia"},{"key":"ref17","doi-asserted-by":"publisher","first-page":"209","DOI":"10.1080\/09286586.2016.1193618","article-title":"Ten emerging trends in the epidemiology of diabetic retinopathy","volume":"23","author":"C Sabanayagam","year":"2016","journal-title":"Ophthalmic Epidemiol"},{"key":"ref18","doi-asserted-by":"publisher","first-page":"1266","DOI":"10.1007\/s00125-004-1431-6","article-title":"Declining incidence of severe retinopathy and persisting decrease of nephropathy\n                    in an unselected population of Type 1 diabetes-the Linkoping Diabetes\n                    Complications Study","volume":"47","author":"M Nordwall","year":"2004","journal-title":"Diabetologia"},{"key":"ref19","doi-asserted-by":"publisher","first-page":"e0249461","DOI":"10.1371\/journal.pone.0249461","article-title":"Normative values of the vibration perception thresholds at finger pulps and\n                    metatarsal heads in healthy adults","volume":"16","author":"L Ekman","year":"2021","journal-title":"PLoS One"},{"key":"ref20","doi-asserted-by":"publisher","first-page":"240","DOI":"10.1111\/j.1464-5491.2009.02667.x","article-title":"Reliability and validity of the modified Toronto Clinical Neuropathy Score in\n                    diabetic sensorimotor polyneuropathy","volume":"26","author":"V Bril","year":"2009","journal-title":"Diabet Med"},{"key":"ref21","doi-asserted-by":"publisher","first-page":"S471","DOI":"10.1007\/s00125-019-4946-6","article-title":"55(th) EASD Annual Meeting of the European Association for the Study of Diabetes\n                    : Barcelona, Spain, 16 \u2013 20 September 2019","volume":"62","author":"E Lindholm","year":"2019","journal-title":"Diabetologia"},{"key":"ref22","doi-asserted-by":"publisher","first-page":"149","DOI":"10.1016\/j.kint.2016.01.023","article-title":"An autopsy study suggests that diabetic nephropathy is underdiagnosed","volume":"90","author":"C Q Klessens","year":"2016","journal-title":"Kidney Int"},{"key":"ref23","doi-asserted-by":"publisher","first-page":"15","DOI":"10.1056\/NEJM199401063300103","article-title":"Declining incidence of nephropathy in insulin-dependent diabetes mellitus","volume":"330","author":"M Bojestig","year":"1994","journal-title":"N Engl J Med"},{"key":"ref24","doi-asserted-by":"publisher","first-page":"898","DOI":"10.3109\/02713683.2012.683507","article-title":"Correlation of diabetic retinopathy and corneal neuropathy using confocal\n                    microscopy","volume":"37","author":"E Nitoda","year":"2012","journal-title":"Curr Eye Res"},{"key":"ref25","doi-asserted-by":"publisher","first-page":"38","DOI":"10.1186\/s12995-014-0038-1","article-title":"Test-retest reliability of neurophysiological tests of hand-arm vibration\n                    syndrome in vibration exposed workers and unexposed referents","volume":"9","author":"L Gerhardsson","year":"2014","journal-title":"J Occup Med Toxicol"},{"key":"ref26","doi-asserted-by":"publisher","first-page":"e0226371","DOI":"10.1371\/journal.pone.0226371","article-title":"Examining practice effects in repeated measurements of vibration perception\n                    thresholds on finger pulps of healthy individuals \u2013 Is it possible to\n                    improve your results over a clinically relevant test interval?","volume":"14","author":"L Ekman","year":"2019","journal-title":"PLoS One"}],"container-title":["Experimental and Clinical Endocrinology &amp; Diabetes"],"original-title":[],"language":"en","link":[{"URL":"http:\/\/www.thieme-connect.de\/products\/ejournals\/pdf\/10.1055\/a-2010-6987.pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2023,4,13]],"date-time":"2023-04-13T23:32:25Z","timestamp":1681428745000},"score":1,"resource":{"primary":{"URL":"http:\/\/www.thieme-connect.de\/DOI\/DOI?10.1055\/a-2010-6987"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2023,1,10]]},"references-count":26,"journal-issue":{"issue":"04","published-online":{"date-parts":[[2023,4,13]]},"published-print":{"date-parts":[[2023,4]]}},"URL":"https:\/\/doi.org\/10.1055\/a-2010-6987","archive":["Portico","CLOCKSS"],"relation":{},"ISSN":["0947-7349","1439-3646"],"issn-type":[{"value":"0947-7349","type":"print"},{"value":"1439-3646","type":"electronic"}],"subject":[],"published-other":{"date-parts":[[2023,1,10]]},"published":{"date-parts":[[2023,1,10]]}}}