{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,5,7]],"date-time":"2026-05-07T16:21:58Z","timestamp":1778170918502,"version":"3.51.4"},"reference-count":31,"publisher":"MDPI AG","issue":"1","license":[{"start":{"date-parts":[[2024,12,24]],"date-time":"2024-12-24T00:00:00Z","timestamp":1734998400000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"CNRS","award":["EDP163403"],"award-info":[{"award-number":["EDP163403"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Medicina"],"abstract":"<jats:p>Background and Objectives: According to the International Working Group on Diabetic Foot (IWGDF) risk classification, the estimated risk of developing a diabetic foot ulcer (DFU) is much higher in patients with a history of DFUs (Grade 3) compared to those with a peripheral neuropathy but without a history of DFUs (Grades 1 and 2). It has been suggested that microcirculation impairment is involved in DFU genesis and could be taken into account to refine the existing risk classification. The aim of this study was to evaluate microcirculation parameters in patients with diabetes according to their estimated DFU risk. Materials and Methods: A total of 172 patients with type 2 diabetes associated with a peripheral neuropathy and\/or a history of DFUs were included and classified into two groups (Grade 1\u20132 and Grade 3) according to the IWGDF classification. All patients underwent an evaluation of peripheral neuropathy, plantar sudomotor function, and skin microcirculation parameters. These different parameters were compared between both groups. Results: There was no significant difference between the two groups in terms of age, diabetes duration, transcutaneous oxygen pressure level, skin microcirculatory reactivity, neuropathy disability score, neuropathy symptom score, or thermal sensitivity. Patients in Grade 3 were more likely to present with retinopathy (OR 3.15, 95%CI [1.53; 6.49]) and severe sudomotor dysfunction (OR 2.73 95%CI [1.29; 5.80] but less likely to have abnormal VPT (OR 0.20 95%CI [0.05; 0.80]). Conclusions: The present study found more retinopathy and a more pronounced alteration to sudomotor function in Grade 3 patients, suggesting that these parameters could be considered to better identify patients at high risk of DFUs.<\/jats:p>","DOI":"10.3390\/medicina61010002","type":"journal-article","created":{"date-parts":[[2024,12,24]],"date-time":"2024-12-24T09:00:57Z","timestamp":1735030857000},"page":"2","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":2,"title":["Impairment of Microcirculation Parameters in Patients with a History of Diabetic Foot Ulcers"],"prefix":"10.3390","volume":"61","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-4136-4383","authenticated-orcid":false,"given":"Julien","family":"Vouillarmet","sequence":"first","affiliation":[{"name":"Service d\u2019Endocrinologie, Diab\u00e8te et Nutrition, Centre Hospitalier Lyon-Sud, Hospices Civils de Lyon, 69310 Pierre B\u00e9nite, France"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Audrey","family":"Josset-Lamaugarny","sequence":"additional","affiliation":[{"name":"Laboratoire de Biologie Tissulaire et Ing\u00e9nierie Th\u00e9rapeutique, CNRS UMR 5305, 69367 Lyon, France"},{"name":"UFR Biosciences, Universit\u00e9 Claude Bernard, Villeurbanne, 69100 Lyon, France"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Myriam","family":"Moret","sequence":"additional","affiliation":[{"name":"Service d\u2019Endocrinologie, Diab\u00e8te et M\u00e9tabolisme, Groupement Hospitalier Est, Hospices Civils de Lyon, 69677 Bron, France"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Christine","family":"Cugnet-Anceau","sequence":"additional","affiliation":[{"name":"Service d\u2019Endocrinologie, Diab\u00e8te et Nutrition, Centre Hospitalier Lyon-Sud, Hospices Civils de Lyon, 69310 Pierre B\u00e9nite, France"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Paul","family":"Michon","sequence":"additional","affiliation":[{"name":"Service d\u2019Endocrinologie, Diab\u00e8te et Nutrition, Centre Hospitalier Lyon-Sud, Hospices Civils de Lyon, 69310 Pierre B\u00e9nite, France"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Emmanuel","family":"Disse","sequence":"additional","affiliation":[{"name":"Service d\u2019Endocrinologie, Diab\u00e8te et Nutrition, Centre Hospitalier Lyon-Sud, Hospices Civils de Lyon, 69310 Pierre B\u00e9nite, France"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Dominique","family":"Sigaudo-Roussel","sequence":"additional","affiliation":[{"name":"Laboratoire de Biologie Tissulaire et Ing\u00e9nierie Th\u00e9rapeutique, CNRS UMR 5305, 69367 Lyon, France"},{"name":"UFR Biosciences, Universit\u00e9 Claude Bernard, Villeurbanne, 69100 Lyon, France"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"1968","published-online":{"date-parts":[[2024,12,24]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"62","DOI":"10.1001\/jama.2023.10578","article-title":"Diabetic Foot Ulcers: A Review","volume":"330","author":"Armstrong","year":"2023","journal-title":"JAMA"},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"186","DOI":"10.12968\/jowc.2018.27.3.186","article-title":"Delayed referral of patients with diabetic foot ulcers across Europe: Patterns between primary care and specialised units","volume":"27","author":"Manu","year":"2018","journal-title":"J. Wound Care"},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"S84","DOI":"10.1002\/1520-7560(200009\/10)16:1+<::AID-DMRR113>3.0.CO;2-S","article-title":"International consensus and practical guidelines on the management and the prevention of the diabetic foot. International Working Group on the Diabetic Foot","volume":"16","author":"Apelqvist","year":"2000","journal-title":"Diabetes Metab. Res. Rev."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"1442","DOI":"10.2337\/diacare.24.8.1442","article-title":"Effectiveness of the diabetic foot risk classification system of the International Working Group on the Diabetic Foot","volume":"24","author":"Peters","year":"2001","journal-title":"Diabetes Care"},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"960","DOI":"10.2337\/diacare.26.3.960","article-title":"Evidence for associated cutaneous microangiopathy in diabetic patients with neuropathic foot ulceration","volume":"26","author":"LeDevehat","year":"2003","journal-title":"Lett. Diabetes Care"},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"1343","DOI":"10.2337\/diacare.27.6.1343","article-title":"Comparative roles of microvascular and nerve function in foot ulceration in type 2 diabetes","volume":"27","author":"Krishnan","year":"2004","journal-title":"Diabetes Care"},{"key":"ref_7","doi-asserted-by":"crossref","unstructured":"Veves, A., Giurini, J., and Guzman, R. (2018). Microvascular Changes in the Diabetic Foot. The Diabetic Foot, Humana.","DOI":"10.1007\/978-3-319-89869-8"},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"832","DOI":"10.2337\/db18-0694","article-title":"Neurovascular Response to Pressure in Patients With Diabetic Foot Ulcer","volume":"68","author":"Vouillarmet","year":"2019","journal-title":"Diabetes"},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"1810","DOI":"10.2337\/diacare.24.10.1810","article-title":"Early detection of microcirculatory impairment in diabetic patients with foot at risk","volume":"24","author":"Zimny","year":"2001","journal-title":"Diabetes Care"},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"1190","DOI":"10.1007\/s00125-010-2030-3","article-title":"Risk stratification systems for diabetic foot ulcers: A systematic review","volume":"54","author":"Boyko","year":"2011","journal-title":"Diabetologia"},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"109063","DOI":"10.1016\/j.diabres.2021.109063","article-title":"Screening, diagnosis and management of diabetic sensorimotor polyneuropathy in clinical practice: International expert consensus recommendations","volume":"186","author":"Ziegler","year":"2022","journal-title":"Diabetes Res. Clin. Pract."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"377","DOI":"10.1046\/j.1464-5491.2002.00698.x","article-title":"The North-West Diabetes Foot Care Study: Incidence of, and risk factors for, new diabetic foot ulceration in a community based patient cohort","volume":"10","author":"Abbot","year":"2002","journal-title":"Diabet. Med."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"491","DOI":"10.1097\/01.ASW.0000453211.28954.99","article-title":"Sensitivity and specificity of a new test for thermographic evaluation of the foot in the diagnosis of diabetic peripheral polyneuropathy","volume":"27","author":"Munuera","year":"2014","journal-title":"Adv. Skin Wound Care"},{"key":"ref_14","doi-asserted-by":"crossref","unstructured":"Vinik, A.I., Nevoret, M.L., and Casellini, C. (2015). The New Age of Sudomotor Function Testing: A Sensitive and Specific Biomarker for Diagnosis, Estimation of Severity, Monitoring Progression, and Regression in Response to Intervention. Front. Endocrinol., 6.","DOI":"10.3389\/fendo.2015.00094"},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"198","DOI":"10.1016\/S1385-299X(00)00013-1","article-title":"Progressive calibrated pressure device to measure cutaneous blood flow changes to external pressure strain","volume":"5","author":"Fromy","year":"2000","journal-title":"Brain Res. Protoc."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"1542","DOI":"10.1007\/s00125-016-3961-0","article-title":"Prospective study on microangiopathy in type 2 diabetic foot ulcer","volume":"59","author":"Fiordaliso","year":"2016","journal-title":"Diabetologia"},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"e00175","DOI":"10.1002\/edm2.175","article-title":"Risk factors for diabetic foot complications in type 2 diabetes\u2014A systematic review","volume":"4","author":"Rossboth","year":"2021","journal-title":"Endocrinol. Diabetes Metab."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"e3605","DOI":"10.1002\/dmrr.3605","article-title":"Diabetic retinopathy relates to the incidence of foot ulcers and amputations in type 2 diabetes","volume":"39","author":"Borderie","year":"2023","journal-title":"Diabetes Metab. Res. Rev."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"302","DOI":"10.1111\/j.1464-5491.2009.02677.x","article-title":"Sudomotor dysfunction is associated with foot ulceration in diabetes","volume":"26","author":"Tentolouris","year":"2009","journal-title":"Diabet. Med."},{"key":"ref_20","doi-asserted-by":"crossref","unstructured":"Panagoulias, G.S., Eleftheriadou, I., Papanas, N., Manes, C., Kamenov, Z., Tesic, D., Bousboulas, S., Tentolouris, A., Jude, E.B., and Tentolouris, N. (2020). Dryness of Foot Skin Assessed by the Visual Indicator Test and Risk of Diabetic Foot Ulceration: A Prospective Observational Study. Front. Endocrinol., 11.","DOI":"10.3389\/fendo.2020.00625"},{"key":"ref_21","doi-asserted-by":"crossref","unstructured":"Carbajal-Ram\u00edrez, A., Hern\u00e1ndez-Dom\u00ednguez, J.A., Molina-Ayala, M.A., Rojas-Uribe, M.M., and Ch\u00e1vez-Negret, A. (2019). Early identification of peripheral neuropathy based on sudomotor dysfunction in Mexican patients with type 2 diabetes. BMC Neurol., 19.","DOI":"10.1186\/s12883-019-1332-4"},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"472","DOI":"10.1055\/s-0043-116673","article-title":"The Application of SUDOSCAN for Screening Diabetic Peripheral Neuropathy in Chinese Population","volume":"126","author":"Jin","year":"2018","journal-title":"Exp. Clin. Endocrinol. Diabetes"},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"29","DOI":"10.1186\/s40200-016-0252-8","article-title":"Electrochemical skin conductance to detect sudomotor dysfunction, peripheral neuropathy and the risk of foot ulceration among Saudi patients with diabetes mellitus","volume":"15","author":"Sheshah","year":"2016","journal-title":"J. Diabetes Metab. Disord."},{"key":"ref_24","doi-asserted-by":"crossref","unstructured":"Selvarajah, D., Cash, T., Davies, J., Sankar, A., Rao, G., Grieg, M., Pallai, S., Gandhi, R., Wilkinson, I.D., and Tesfaye, S. (2015). SUDOSCAN: A Simple, Rapid, and Objective Method with Potential for Screening for Diabetic Peripheral Neuropathy. PLoS ONE, 10.","DOI":"10.1371\/journal.pone.0138224"},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"126","DOI":"10.1016\/j.diabet.2012.09.004","article-title":"Screening of cardiovascular autonomic neuropathy in patients with diabetes using non-invasive quick and simple assessment of sudomotor function","volume":"39","author":"Yajnik","year":"2013","journal-title":"Diabetes Metab."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"1711","DOI":"10.1016\/S0140-6736(05)67696-9","article-title":"Early changes in the skin microcirculation and muscle metabolism of the diabetic foot Lancet","volume":"366","author":"Greenman","year":"2005","journal-title":"Lancet"},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"467","DOI":"10.1042\/cs0890467","article-title":"Microvascular response to tissue injury and capillary ultrastructure in the foot skin of type I diabetic patients","volume":"89","author":"Rayman","year":"1995","journal-title":"Clin. Sci."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"1305","DOI":"10.1016\/j.jdiacomp.2017.05.005","article-title":"Post-occlusive reactive hyperaemia of skin microvasculature and foot complications in type 2 diabetes","volume":"31","author":"Lanting","year":"2017","journal-title":"J. Diabetes Complicat."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"570","DOI":"10.1111\/j.1464-5491.1988.tb01053.x","article-title":"Reduced hyperaemic response under the diabetic neuropathic foot","volume":"5","author":"Newrick","year":"1988","journal-title":"Diabet. Med."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"1487","DOI":"10.1111\/j.1464-5491.2005.01659.x","article-title":"Pilot study of the effects of local pressure on microvascular function in the diabetic foot","volume":"22","author":"Newton","year":"2005","journal-title":"Diabet. Med."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"887","DOI":"10.1111\/dme.13630","article-title":"One-stop microvascular screening service: An effective model for the early detection of diabetic peripheral neuropathy and the high-risk foot","volume":"35","author":"Selvarajah","year":"2018","journal-title":"Diabet. Med."}],"container-title":["Medicina"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/1648-9144\/61\/1\/2\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T16:59:09Z","timestamp":1760115549000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/1648-9144\/61\/1\/2"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2024,12,24]]},"references-count":31,"journal-issue":{"issue":"1","published-online":{"date-parts":[[2025,1]]}},"alternative-id":["medicina61010002"],"URL":"https:\/\/doi.org\/10.3390\/medicina61010002","relation":{},"ISSN":["1648-9144"],"issn-type":[{"value":"1648-9144","type":"electronic"}],"subject":[],"published":{"date-parts":[[2024,12,24]]}}}