Abstract
Diabetic foot disease (DFD) is a complication of diabetes mellitus, characterized by multiple pathogenetic factors, bearing a very high burden of disability as well as of direct and indirect costs for individuals or healthcare systems. A further characteristic of DFD is that it is associated with a marked risk of subsequent hospitalizations for incident cardiovascular events, chronic renal failure or of allcause mortality. Additionally, DFD is strongly linked to the male sex, being much more prevalent among men. However, even if DFD mainly affects males, several past reports suggest that females are disadvantaged as regards the risk of subsequent adverse outcomes. This review aims to clarify this point, attempting to provide an explanation for this apparent oddity: being DFD a typically male complication of diabetes but, seemingly, with a greater load of subsequent consequences for females.
Keywords: Diabetic foot disease, sex-gender differences, foot ulcers, cardiovascular complications, chronic renal failure, mortality.
[1]
Boulton AJ. The diabetic foot: grand overview, epidemiology and pathogenesis. Diabetes Metab Res Rev 2008; 24(Suppl. 1): S3-6.
[http://dx.doi.org/10.1002/dmrr.833] [PMID: 18442166]
[http://dx.doi.org/10.1002/dmrr.833] [PMID: 18442166]
[2]
Boulton AJ, Vileikyte L, Ragnarson-Tennvall G, Apelqvist J. The global burden of diabetic foot disease. Lancet 2005; 366(9498): 1719-24.
[http://dx.doi.org/10.1016/S0140-6736(05)67698-2] [PMID: 16291066]
[http://dx.doi.org/10.1016/S0140-6736(05)67698-2] [PMID: 16291066]
[3]
Driver VR, Fabbi M, Lavery LA, Gibbons G. The costs of diabetic foot: the economic case for the limb salvage team. J Vasc Surg 2010; 52(3): 17S-22S.
[http://dx.doi.org/10.1016/j.jvs.2010.06.003] [PMID: 20804928]
[http://dx.doi.org/10.1016/j.jvs.2010.06.003] [PMID: 20804928]
[4]
Frykberg RG. Epidemiology of the diabetic foot: ulcerations and amputations. Adv Wound Care 1999; 12(3): 139-41.
[PMID: 10655794]
[PMID: 10655794]
[5]
Hicks CW, Selvin E. Epidemiology of Peripheral Neuropathy and Lower Extremity Disease in Diabetes. Curr Diab Rep 2019; 19(10): 86.
[http://dx.doi.org/10.1007/s11892-019-1212-8] [PMID: 31456118]
[http://dx.doi.org/10.1007/s11892-019-1212-8] [PMID: 31456118]
[6]
Singh N, Armstrong DG, Lipsky BA. Preventing foot ulcers in patients with diabetes. JAMA 2005; 293(2): 217-28.
[http://dx.doi.org/10.1001/jama.293.2.217] [PMID: 15644549]
[http://dx.doi.org/10.1001/jama.293.2.217] [PMID: 15644549]
[7]
Moulik PK, Mtonga R, Gill GV. Amputation and mortality in new-onset diabetic foot ulcers stratified by etiology. Diabetes Care 2003; 26(2): 491-4.
[http://dx.doi.org/10.2337/diacare.26.2.491] [PMID: 12547887]
[http://dx.doi.org/10.2337/diacare.26.2.491] [PMID: 12547887]
[8]
Lavery LA, Oz OK, Bhavan K, Wukich DK. Diabetic Foot Syndrome in the Twenty-First Century. Clin Podiatr Med Surg 2019; 36(3): 355-9.
[http://dx.doi.org/10.1016/j.cpm.2019.02.002] [PMID: 31079602]
[http://dx.doi.org/10.1016/j.cpm.2019.02.002] [PMID: 31079602]
[9]
Jeffcoate WJ, Vileikyte L, Boyko EJ, Armstrong DG, Boulton AJM. Current Challenges and Opportunities in the Prevention and Management of Diabetic Foot Ulcers. Diabetes Care 2018; 41(4): 645-52.
[http://dx.doi.org/10.2337/dc17-1836] [PMID: 29559450]
[http://dx.doi.org/10.2337/dc17-1836] [PMID: 29559450]
[10]
Zhang Y, Lazzarini PA, McPhail SM, van Netten JJ, Armstrong DG, Pacella RE. Global Disability Burdens of Diabetes-Related Lower-Extremity Complications in 1990 and 2016. Diabetes Care 2020; 43(5): 964-74.
[http://dx.doi.org/10.2337/dc19-1614] [PMID: 32139380]
[http://dx.doi.org/10.2337/dc19-1614] [PMID: 32139380]
[11]
Armstrong DG, Swerdlow MA, Armstrong AA, Conte MS, Padula WV, Bus SA. Five year mortality and direct costs of care for people with diabetic foot complications are comparable to cancer. J Foot Ankle Res 2020; 13(1): 16.
[http://dx.doi.org/10.1186/s13047-020-00383-2] [PMID: 32209136]
[http://dx.doi.org/10.1186/s13047-020-00383-2] [PMID: 32209136]
[12]
Cheng SW, Wang CY, Chen JH, Ko Y. Healthcare costs and utilization of diabetes-related complications in Taiwan: A claims database analysis. Medicine (Baltimore) 2018; 97(31)e11602
[http://dx.doi.org/10.1097/MD.0000000000011602] [PMID: 30075532]
[http://dx.doi.org/10.1097/MD.0000000000011602] [PMID: 30075532]
[13]
Tesfaye S, Boulton AJ, Dickenson AH. Mechanisms and management of diabetic painful distal symmetrical polyneuropathy. Diabetes Care 2013; 36(9): 2456-65.
[http://dx.doi.org/10.2337/dc12-1964] [PMID: 23970715]
[http://dx.doi.org/10.2337/dc12-1964] [PMID: 23970715]
[14]
Elgzyri T, Larsson J, Thörne J, Eriksson KF, Apelqvist J. Outcome of ischemic foot ulcer in diabetic patients who had no invasive vascular intervention. Eur J Vasc Endovasc Surg 2013; 46(1): 110-7.
[http://dx.doi.org/10.1016/j.ejvs.2013.04.013] [PMID: 23642521]
[http://dx.doi.org/10.1016/j.ejvs.2013.04.013] [PMID: 23642521]
[15]
Giurato L, Vainieri E, Meloni M, et al. Limb salvage in patients with diabetes is not a temporary solution but a life-changing procedure. Diabetes Care 2015; 38(10): e156-7.
[http://dx.doi.org/10.2337/dc15-0989] [PMID: 26294664]
[http://dx.doi.org/10.2337/dc15-0989] [PMID: 26294664]
[16]
Moxey PW, Gogalniceanu P, Hinchliffe RJ, et al. Lower extremity amputations--a review of global variability in incidence. Diabet Med 2011; 28(10): 1144-53.
[http://dx.doi.org/10.1111/j.1464-5491.2011.03279.x] [PMID: 21388445]
[http://dx.doi.org/10.1111/j.1464-5491.2011.03279.x] [PMID: 21388445]
[17]
Claessen H, Narres M, Haastert B, et al. Lower-extremity amputations in people with and without diabetes in Germany, 2008-2012 - an analysis of more than 30 million inhabitants. Clin Epidemiol 2018; 10: 475-88.
[http://dx.doi.org/10.2147/CLEP.S146484] [PMID: 29719421]
[http://dx.doi.org/10.2147/CLEP.S146484] [PMID: 29719421]
[18]
Lin CW, Armstrong DG, Lin CH, et al. Nationwide trends in the epidemiology of diabetic foot complications and lower-extremity amputation over an 8-year period. BMJ Open Diabetes Res Care 2019; 7(1)e000795
[http://dx.doi.org/10.1136/bmjdrc-2019-000795] [PMID: 31749971]
[http://dx.doi.org/10.1136/bmjdrc-2019-000795] [PMID: 31749971]
[19]
Lombardo FL, Maggini M, De Bellis A, Seghieri G, Anichini R. Lower extremity amputations in persons with and without diabetes in Italy: 2001-2010. PLoS One 2014; 9(1)e86405
[http://dx.doi.org/10.1371/journal.pone.0086405] [PMID: 24489723]
[http://dx.doi.org/10.1371/journal.pone.0086405] [PMID: 24489723]
[20]
Hopkins RB, Burke N, Harlock J, Jegathisawaran J, Goeree R. Economic burden of illness associated with diabetic foot ulcers in Canada. BMC Health Serv Res 2015; 15: 13.
[http://dx.doi.org/10.1186/s12913-015-0687-5] [PMID: 25608648]
[http://dx.doi.org/10.1186/s12913-015-0687-5] [PMID: 25608648]
[21]
Alva ML, Gray A, Mihaylova B, Leal J, Holman RR. The impact of diabetes-related complications on healthcare costs: new results from the UKPDS (UKPDS 84). Diabet Med 2015; 32(4): 459-66.
[http://dx.doi.org/10.1111/dme.12647] [PMID: 25439048]
[http://dx.doi.org/10.1111/dme.12647] [PMID: 25439048]
[22]
Hicks CW, Selvarajah S, Mathioudakis N, et al. Burden of Infected Diabetic Foot Ulcers on Hospital Admissions and Costs. Ann Vasc Surg 2016; 33: 149-58.
[http://dx.doi.org/10.1016/j.avsg.2015.11.025] [PMID: 26907372]
[http://dx.doi.org/10.1016/j.avsg.2015.11.025] [PMID: 26907372]
[23]
Rice JB, Desai U, Cummings AK, Birnbaum HG, Skornicki M, Parsons NB. Burden of diabetic foot ulcers for medicare and private insurers. Diabetes Care 2014; 37(3): 651-8. [published correction appears in Diabetes Care. 2014 Sep;37(9):2660
[http://dx.doi.org/10.2337/dc13-2176] [PMID: 24186882]
[http://dx.doi.org/10.2337/dc13-2176] [PMID: 24186882]
[24]
Crawford F, Cezard G, Chappell FM, et al. A systematic review and individual patient data meta-analysis of prognostic factors for foot ulceration in people with diabetes: the international research collaboration for the prediction of diabetic foot ulcerations (PODUS). Health Technol Assess 2015; 19(57): 1-210.
[http://dx.doi.org/10.3310/hta19570] [PMID: 26211920]
[http://dx.doi.org/10.3310/hta19570] [PMID: 26211920]
[25]
Dietrich I, Braga GA, de Melo FG, da Costa Silva Silva ACC. The Diabetic Foot as a Proxy for Cardiovascular Events and Mortality Review. Curr Atheroscler Rep 2017; 19(11): 44.
[http://dx.doi.org/10.1007/s11883-017-0680-z] [PMID: 28971322]
[http://dx.doi.org/10.1007/s11883-017-0680-z] [PMID: 28971322]
[26]
Jones WS, Patel MR, Rockman CB, et al. Association of the ankle-brachial index with history of myocardial infarction and stroke. Am Heart J 2014; 167(4): 499-505.
[http://dx.doi.org/10.1016/j.ahj.2013.12.016] [PMID: 24655698]
[http://dx.doi.org/10.1016/j.ahj.2013.12.016] [PMID: 24655698]
[27]
Emdin CA, Anderson SG, Callender T, et al. Usual blood pressure, peripheral arterial disease, and vascular risk: cohort study of 4.2 million adults. BMJ 2015; 351: h4865.
[http://dx.doi.org/10.1136/bmj.h4865] [PMID: 26419648]
[http://dx.doi.org/10.1136/bmj.h4865] [PMID: 26419648]
[28]
Lin YS, Tung TH, Wang J, et al. Peripheral arterial disease and atrial fibrillation and risk of stroke, heart failure hospitalization and cardiovascular death: A nationwide cohort study. Int J Cardiol 2016; 203: 204-11.
[http://dx.doi.org/10.1016/j.ijcard.2015.10.091] [PMID: 26512838]
[http://dx.doi.org/10.1016/j.ijcard.2015.10.091] [PMID: 26512838]
[29]
Mohammedi K, Woodward M, Hirakawa Y, et al. ADVANCE Collaborative Group. Presentations of major peripheral arterial disease and risk of major outcomes in patients with type 2 diabetes: results from the ADVANCE-ON study. Cardiovasc Diabetol 2016; 15(1): 129.
[http://dx.doi.org/10.1186/s12933-016-0446-x] [PMID: 27590190]
[http://dx.doi.org/10.1186/s12933-016-0446-x] [PMID: 27590190]
[30]
Chammas NK, Hill RL, Edmonds ME. Increased Mortality in Diabetic Foot Ulcer Patients: The Significance of Ulcer Type. J Diabetes Res 2016.20162879809
[http://dx.doi.org/10.1155/2016/2879809] [PMID: 27213157]
[http://dx.doi.org/10.1155/2016/2879809] [PMID: 27213157]
[31]
Prompers L, Schaper N, Apelqvist J, et al. Prediction of outcome in individuals with diabetic foot ulcers: focus on the differences between individuals with and without peripheral arterial disease. The EURODIALE Study. Diabetologia 2008; 51(5): 747-55.
[http://dx.doi.org/10.1007/s00125-008-0940-0] [PMID: 18297261]
[http://dx.doi.org/10.1007/s00125-008-0940-0] [PMID: 18297261]
[32]
Seghieri G, Policardo L, Anichini R, et al. The Effect of Sex and Gender on Diabetic Complications. Curr Diabetes Rev 2017; 13(2): 148-60.
[http://dx.doi.org/10.2174/1573399812666160517115756] [PMID: 27183843]
[http://dx.doi.org/10.2174/1573399812666160517115756] [PMID: 27183843]
[33]
Marino M, Masella R, Bulzomi P, Campesi I, Malorni W, Franconi F. Nutrition and human health from a sex-gender perspective. Mol Aspects Med 2011; 32(1): 1-70.
[http://dx.doi.org/10.1016/j.mam.2011.02.001] [PMID: 21356234]
[http://dx.doi.org/10.1016/j.mam.2011.02.001] [PMID: 21356234]
[34]
Kautzky-Willer A, Harreiter J, Pacini G. Sex and Gender Differences in Risk, Pathophysiology and Complications of Type 2 Diabetes Mellitus. Endocr Rev 2016; 37(3): 278-316.
[http://dx.doi.org/10.1210/er.2015-1137] [PMID: 27159875]
[http://dx.doi.org/10.1210/er.2015-1137] [PMID: 27159875]
[35]
Maric-Bilkan C. Sex differences in micro- and macro-vascular complications of diabetes mellitus. Clin Sci (Lond) 2017; 131(9): 833-46.
[http://dx.doi.org/10.1042/CS20160998] [PMID: 28424377]
[http://dx.doi.org/10.1042/CS20160998] [PMID: 28424377]
[36]
Ritter R, Jong M, Vos RC, et al. Sex differences in the risk of vascular disease associated with diabetes. Biol Sex Differ 2020; 11(1): 1.
[http://dx.doi.org/10.1186/s13293-019-0277-z] [PMID: 31900228]
[http://dx.doi.org/10.1186/s13293-019-0277-z] [PMID: 31900228]
[37]
Prospective Studies Collaboration and Asia Pacific Cohort Studies Collaboration. Sex-specific relevance of diabetes to occlusive vascular and other mortality: a collaborative meta-analysis of individual data from 980 793 adults from 68 prospective studies. Lancet Diabetes Endocrinol 2018; 6(7): 538-46.
[http://dx.doi.org/10.1016/S2213-8587(18)30079-2] [PMID: 29752194]
[http://dx.doi.org/10.1016/S2213-8587(18)30079-2] [PMID: 29752194]
[38]
Peters SAE, Woodward M. Sex Differences in the Burden and Complications of Diabetes. Curr Diab Rep 2018; 18(6): 33.
[http://dx.doi.org/10.1007/s11892-018-1005-5] [PMID: 29671082]
[http://dx.doi.org/10.1007/s11892-018-1005-5] [PMID: 29671082]
[39]
Policardo L, Seghieri G, Francesconi P, Anichini R, Franconi F, Del Prato S. Gender difference in diabetes related excess risk of cardiovascular events: When does the ‘risk window’ open? J Diabetes Complications 2017; 31(1): 74-9.
[http://dx.doi.org/10.1016/j.jdiacomp.2016.09.010] [PMID: 27746087]
[http://dx.doi.org/10.1016/j.jdiacomp.2016.09.010] [PMID: 27746087]
[40]
Sowers JR. Diabetes mellitus and cardiovascular disease in women. Arch Intern Med 1998; 158(6): 617-21.
[http://dx.doi.org/10.1001/archinte.158.6.617] [PMID: 9521226]
[http://dx.doi.org/10.1001/archinte.158.6.617] [PMID: 9521226]
[41]
Steinberg HO, Paradisi G, Cronin J, et al. Type II diabetes abrogates sex differences in endothelial function in premenopausal women. Circulation 2000; 101(17): 2040-6.
[http://dx.doi.org/10.1161/01.CIR.101.17.2040] [PMID: 10790344]
[http://dx.doi.org/10.1161/01.CIR.101.17.2040] [PMID: 10790344]
[42]
Koh KK, Kang MH, Jin DK, et al. Vascular effects of estrogen in type II diabetic postmenopausal women. J Am Coll Cardiol 2001; 38(5): 1409-15.
[http://dx.doi.org/10.1016/S0735-1097(01)01566-2] [PMID: 11691516]
[http://dx.doi.org/10.1016/S0735-1097(01)01566-2] [PMID: 11691516]
[43]
Eskes T, Haanen C. Why do women live longer than men? Eur J Obstet Gynecol Reprod Biol 2007; 133(2): 126-33.
[http://dx.doi.org/10.1016/j.ejogrb.2007.01.006] [PMID: 17324494]
[http://dx.doi.org/10.1016/j.ejogrb.2007.01.006] [PMID: 17324494]
[44]
Gordon EH, Hubbard RE. Differences in frailty in older men and women. Med J Aust 2020; 212(4): 183-8.
[http://dx.doi.org/10.5694/mja2.50466] [PMID: 31886526]
[http://dx.doi.org/10.5694/mja2.50466] [PMID: 31886526]
[45]
Norhammar A, Schenck-Gustafsson K. Type 2 diabetes and cardiovascular disease in women. Diabetologia 2013; 56(1): 1-9.
[http://dx.doi.org/10.1007/s00125-012-2694-y] [PMID: 22945305]
[http://dx.doi.org/10.1007/s00125-012-2694-y] [PMID: 22945305]
[46]
Rossi MC, Cristofaro MR, Gentile S, et al. AMD Annals Study Group. Sex disparities in the quality of diabetes care: biological and cultural factors may play a different role for different outcomes: a cross-sectional observational study from the AMD Annals initiative. Diabetes Care 2013; 36(10): 3162-8.
[http://dx.doi.org/10.2337/dc13-0184] [PMID: 23835692]
[http://dx.doi.org/10.2337/dc13-0184] [PMID: 23835692]
[47]
Howard BV, Cowan LD, Go O, Welty TK, Robbins DC, Lee ET. Adverse effects of diabetes on multiple cardiovascular disease risk factors in women. The Strong Heart Study. Diabetes Care 1998; 21(8): 1258-65.
[http://dx.doi.org/10.2337/diacare.21.8.1258] [PMID: 9702430]
[http://dx.doi.org/10.2337/diacare.21.8.1258] [PMID: 9702430]
[48]
Rivellese AA, Riccardi G, Vaccaro O. Cardiovascular risk in women with diabetes. Nutr Metab Cardiovasc Dis 2010; 20(6): 474-80.
[http://dx.doi.org/10.1016/j.numecd.2010.01.008] [PMID: 20621459]
[http://dx.doi.org/10.1016/j.numecd.2010.01.008] [PMID: 20621459]
[49]
Wannamethee SG, Papacosta O, Lawlor DA, et al. Do women exhibit greater differences in established and novel risk factors between diabetes and non-diabetes than men? The British Regional Heart Study and British Women’s Heart Health Study. Diabetologia 2012; 55(1): 80-7.
[http://dx.doi.org/10.1007/s00125-011-2284-4] [PMID: 21861177]
[http://dx.doi.org/10.1007/s00125-011-2284-4] [PMID: 21861177]
[50]
Catalan M, Herreras Z, Pinyol M, et al. Prevalence by sex of preclinical carotid atherosclerosis in newly diagnosed type 2 diabetes. Nutr Metab Cardiovasc Dis 2015; 25(8): 742-8.
[http://dx.doi.org/10.1016/j.numecd.2015.04.009] [PMID: 26033395]
[http://dx.doi.org/10.1016/j.numecd.2015.04.009] [PMID: 26033395]
[51]
Peek ME. Gender differences in diabetes-related lower extremity amputations. Clin Orthop Relat Res 2011; 469(7): 1951-5.
[http://dx.doi.org/10.1007/s11999-010-1735-4] [PMID: 21161738]
[http://dx.doi.org/10.1007/s11999-010-1735-4] [PMID: 21161738]
[52]
Benjamin EJ, Blaha MJ, Chiuve SE, et al. American Heart Association Statistics Committee and Stroke Statistics Subcommittee. Heart Disease and Stroke Statistics-2017 Update: A Report From the American Heart Association. Circulation 2017; 135(10): e146-603.
[http://dx.doi.org/10.1161/CIR.0000000000000485] [PMID: 28122885]
[http://dx.doi.org/10.1161/CIR.0000000000000485] [PMID: 28122885]
[53]
Miao JJ, Hendryx M, Shadyab AH, et al. Social Support, Social Network Size, Social Strain, Stressful Life Events, and Coronary Heart Disease in Women With Type 2 Diabetes: A Cohort Study Based on the Women’s Health Initiative. Diabetes Care 2020.dc192065 [published online ahead of print, 2020 Jun 4
[http://dx.doi.org/10.2337/dc19-2065] [PMID: 32499383]
[http://dx.doi.org/10.2337/dc19-2065] [PMID: 32499383]
[54]
Bruun C, Siersma V, Guassora AD, Holstein P, de Fine Olivarius N. Amputations and foot ulcers in patients newly diagnosed with type 2 diabetes mellitus and observed for 19 years. The role of age, gender and co-morbidity. Diabet Med 2013; 30(8): 964-72.
[http://dx.doi.org/10.1111/dme.12196] [PMID: 23617411]
[http://dx.doi.org/10.1111/dme.12196] [PMID: 23617411]
[55]
Amin L, Shah BR, Bierman AS, et al. Gender differences in the impact of poverty on health: disparities in risk of diabetes-related amputation. Diabet Med 2014; 31(11): 1410-7.
[http://dx.doi.org/10.1111/dme.12507] [PMID: 24863747]
[http://dx.doi.org/10.1111/dme.12507] [PMID: 24863747]
[56]
Murabito JM, Evans JC, Nieto K, Larson MG, Levy D, Wilson PW. Prevalence and clinical correlates of peripheral arterial disease in the Framingham Offspring Study. Am Heart J 2002; 143(6): 961-5.
[http://dx.doi.org/10.1067/mhj.2002.122871] [PMID: 12075249]
[http://dx.doi.org/10.1067/mhj.2002.122871] [PMID: 12075249]
[57]
Kumakura H, Kanai H, Araki Y, et al. Sex-related differences in Japanese patients with peripheral arterial disease. Atherosclerosis 2011; 219(2): 846-50.
[http://dx.doi.org/10.1016/j.atherosclerosis.2011.08.037] [PMID: 21920520]
[http://dx.doi.org/10.1016/j.atherosclerosis.2011.08.037] [PMID: 21920520]
[58]
Peters SA, Huxley RR, Woodward M. Diabetes as risk factor for incident coronary heart disease in women compared with men: a systematic review and meta-analysis of 64 cohorts including 858,507 individuals and 28,203 coronary events. Diabetologia 2014; 57(8): 1542-51.
[http://dx.doi.org/10.1007/s00125-014-3260-6] [PMID: 24859435]
[http://dx.doi.org/10.1007/s00125-014-3260-6] [PMID: 24859435]
[59]
Peters SA, Huxley RR, Woodward M. Diabetes as a risk factor for stroke in women compared with men: a systematic review and meta-analysis of 64 cohorts, including 775,385 individuals and 12,539 strokes. Lancet 2014; 383(9933): 1973-80.
[http://dx.doi.org/10.1016/S0140-6736(14)60040-4] [PMID: 24613026]
[http://dx.doi.org/10.1016/S0140-6736(14)60040-4] [PMID: 24613026]
[60]
Tseng CH. Sex difference in the distribution of atherosclerotic risk factors and their association with peripheral arterial disease in Taiwanese type 2 diabetic patients. Circ J 2007; 71(7): 1131-6.
[http://dx.doi.org/10.1253/circj.71.1131] [PMID: 17587723]
[http://dx.doi.org/10.1253/circj.71.1131] [PMID: 17587723]
[61]
Vaccaro O, Lodato S, Mariniello P, De Feo E. Diabetes-related lower extremity amputations in the community: a study based on hospital discharge diagnoses. Nutr Metab Cardiovasc Dis 2002; 12(6): 331-6.
[PMID: 12669680]
[PMID: 12669680]
[62]
Seghieri G, Policardo L, Gualdani E, Anichini R, Francesconi P. Gender difference in the risk for cardiovascular events or mortality of patients with diabetic foot syndrome. Acta Diabetol 2019; 56(5): 561-7.
[http://dx.doi.org/10.1007/s00592-019-01292-y] [PMID: 30725263]
[http://dx.doi.org/10.1007/s00592-019-01292-y] [PMID: 30725263]
[63]
Arnetz L, Ekberg NR, Alvarsson M. Sex differences in type 2 diabetes: focus on disease course and outcomes. Diabetes Metab Syndr Obes 2014; 7: 409-20.
[http://dx.doi.org/10.2147/DMSO.S51301] [PMID: 25258546]
[http://dx.doi.org/10.2147/DMSO.S51301] [PMID: 25258546]
[64]
Pollak AW. PAD in women: the ischemic continuum. Curr Atheroscler Rep 2015; 17(6): 513.
[http://dx.doi.org/10.1007/s11883-015-0513-x] [PMID: 25939674]
[http://dx.doi.org/10.1007/s11883-015-0513-x] [PMID: 25939674]
[65]
Sigvant B, Wiberg-Hedman K, Bergqvist D, et al. A population-based study of peripheral arterial disease prevalence with special focus on critical limb ischemia and sex differences. J Vasc Surg 2007; 45(6): 1185-91.
[http://dx.doi.org/10.1016/j.jvs.2007.02.004] [PMID: 17543683]
[http://dx.doi.org/10.1016/j.jvs.2007.02.004] [PMID: 17543683]
[66]
Simmons A, Steffen K. Peripheral arterial disease in women. Rev Cardiovasc Med 2011; 12(3): 123-31.
[67]
Regensteiner JG, Golden S, Huebschmann AG, et al. American Heart Association Diabetes Committee of the Council on Lifestyle and Cardiometabolic Health, Council on Epidemiology and Prevention, Council on Functional Genomics and Translational Biology, and Council on Hypertension. Sex Differences in the Cardiovascular Consequences of Diabetes Mellitus: A Scientific Statement From the American Heart Association. Circulation 2015; 132(25): 2424-47.
[http://dx.doi.org/10.1161/CIR.0000000000000343] [PMID: 26644329]
[http://dx.doi.org/10.1161/CIR.0000000000000343] [PMID: 26644329]
[68]
Gardner AW, Parker DE, Montgomery PS, et al. Gender and racial differences in endothelial oxidative stress and inflammation in patients with symptomatic peripheral artery disease. J Vasc Surg 2015; 61(5): 1249-57.
[http://dx.doi.org/10.1016/j.jvs.2014.02.045] [PMID: 24703977]
[http://dx.doi.org/10.1016/j.jvs.2014.02.045] [PMID: 24703977]
[69]
Arhuidese I, Nejim B, Aji EA, Canner J, Malas MB. Survival after major lower extremity amputation in patients with end-stage renal disease. J Vasc Surg 2019; 70(4): 1291-8.
[http://dx.doi.org/10.1016/j.jvs.2018.12.055] [PMID: 31543169]
[http://dx.doi.org/10.1016/j.jvs.2018.12.055] [PMID: 31543169]
[70]
Franzini L, Ardigò D, Cavalot F, et al. IT Study Group of the Italian Society of Diabetology. Women show worse control of type 2 diabetes and cardiovascular disease risk factors than men: results from the MIND. Nutr Metab Cardiovasc Dis 2013; 23(3): 235-41.
[http://dx.doi.org/10.1016/j.numecd.2011.12.003] [PMID: 22397873]
[http://dx.doi.org/10.1016/j.numecd.2011.12.003] [PMID: 22397873]
[71]
Pinto A, Tuttolomondo A, Di Raimondo D, et al. Cardiovascular risk profile and morbidity in subjects affected by type 2 diabetes mellitus with and without diabetic foot. Metabolism 2008; 57(5): 676-82.
[http://dx.doi.org/10.1016/j.metabol.2008.01.004] [PMID: 18442633]
[http://dx.doi.org/10.1016/j.metabol.2008.01.004] [PMID: 18442633]
[72]
Wolf G, Müller N, Busch M, et al. Diabetic foot syndrome and renal function in type 1 and 2 diabetes mellitus show close association. Nephrol Dial Transplant 2009; 24(6): 1896-901.
[http://dx.doi.org/10.1093/ndt/gfn724] [PMID: 19131351]
[http://dx.doi.org/10.1093/ndt/gfn724] [PMID: 19131351]
[73]
Monge L, Gnavi R, Carnà P, Broglio F, Boffano GM, Giorda CB. Incidence of hospitalization and mortality in patients with diabetic foot regardless of amputation: a population study. Acta Diabetol 2020; 57(2): 221-8.
[http://dx.doi.org/10.1007/s00592-019-01412-8] [PMID: 31468200]
[http://dx.doi.org/10.1007/s00592-019-01412-8] [PMID: 31468200]
[74]
Penno G, Solini A, Bonora E, et al. Renal Insufficiency And Cardiovascular Events (RIACE) Study Group. Clinical significance of nonalbuminuric renal impairment in type 2 diabetes. J Hypertens 2011; 29(9): 1802-9.
[http://dx.doi.org/10.1097/HJH.0b013e3283495cd6] [PMID: 21738053]
[http://dx.doi.org/10.1097/HJH.0b013e3283495cd6] [PMID: 21738053]
[75]
Meloni M, Izzo V, Giurato L, Lázaro-Martínez JL, Uccioli L. Prevalence, Clinical Aspects and Outcomes in a Large Cohort of Persons with Diabetic Foot Disease: Comparison between Neuropathic and Ischemic Ulcers. J Clin Med 2020; 9(6)E1780
[http://dx.doi.org/10.3390/jcm9061780] [PMID: 32521700]
[http://dx.doi.org/10.3390/jcm9061780] [PMID: 32521700]
[76]
Campesi I, Carru C, Zinellu A, et al. Regular cigarette smoking influences the transsulfuration pathway, endothelial function, and inflammation biomarkers in a sex-gender specific manner in healthy young humans. Am J Transl Res 2013; 5(5): 497-509.
[PMID: 23977409]
[PMID: 23977409]
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