Skip to main content
Top
Published in: Cardiovascular Diabetology 1/2013

Open Access 01-12-2013 | Original investigation

Diabetes abrogates sex differences and aggravates cardiometabolic risk in postmenopausal women

Authors: Filipa Mascarenhas-Melo, Daniela Marado, Filipe Palavra, José Sereno, Álvaro Coelho, Rui Pinto, Edite Teixeira-Lemos, Frederico Teixeira, Flávio Reis

Published in: Cardiovascular Diabetology | Issue 1/2013

Login to get access

Abstract

Background

The aim of this study is to evaluate the effect of gender and menopause in cardiometabolic risk in a type 2 diabetes mellitus (T2DM) population, based on classical and non-traditional markers.

Methods

Seventy four volunteers and 110 T2DM patients were enrolled in the study. Anthropometric data, blood pressure, body mass index (BMI), waist circumference (WC) and the following serum markers were analyzed: glucose, Total-c, TGs, LDL-c, Oxidized-LDL, total HDL-c and large and small HDL-c subpopulations, paraoxonase 1 activity, hsCRP, uric acid, TNF-α, adiponectin and VEGF.

Results

Non-diabetic women, compared to men, presented lower glycemia, WC, small HDL-c, uric acid, TNF-α and increased large HDL-c. Diabetes abrogates the protective effect of female gender, since diabetic women showed increased BMI, WC, small HDL-c, VEGF, uric acid, TNF-α and hsCRP, as well as reduced adiponectin, when compared with non-diabetic. In diabetic females, but not in males, WC is directly and significantly associated with TNF-α, VEGF, hsCRP and uric acid; TNF-α is directly associated with VEGF and hsCRP, and inversely with adiponectin. Postmenopausal females presented a worsen cardiometabolic profile, viewed by the increased WC, small HDL-c, VEGF, uric acid, TNF-α and hsCRP. In this population, WC is directly and significantly associated with TNF-α, VEGF, hsCRP; TNF-α is directly associated with VEGF; and uric acid is inversely associated with large HDL-c and hsCRP with adiponectin, also inversely.

Conclusions

Diabetes abrogates the protective effect of gender on non-diabetic women, and postmenopausal diabetic females presented worsen cardiometabolic risk, including a more atherogenic lipid sketch and a pro-inflammatory and pro-angiogenic profile. The classical cardiovascular risk factors (CVRFs) fail to completely explain these differences, which are better clarified using “non-traditional” factors, such as HDL-c subpopulations, rather than total HDL-c content, and markers of inflammation and angiogenesis, namely TNF-α, hsCRP, uric acid and VEGF. Multi-therapeutic intervention, directed to obesity, atherogenic lipid particles and inflammatory mediators is advisory in order to efficiently prevent the serious diabetic cardiovascular complications.
Appendix
Available only for authorised users
Literature
1.
go back to reference Barr EL, Zimmet PZ, Welborn TA, Jolley D, Magliano DJ, Dunstan DW, Cameron AJ, Dwyer T, Taylor HR, Tonkin AM, Wong TY, McNeil J, Shaw JE: Risk of cardiovascular and all-cause mortality in individuals with diabetes mellitus, impaired fasting glucose, and impaired glucose tolerance: the Australian Diabetes, Obesity, and Lifestyle Study (AusDiab). Circulation. 2007, 116 (2): 151-157. 10.1161/CIRCULATIONAHA.106.685628.CrossRefPubMed Barr EL, Zimmet PZ, Welborn TA, Jolley D, Magliano DJ, Dunstan DW, Cameron AJ, Dwyer T, Taylor HR, Tonkin AM, Wong TY, McNeil J, Shaw JE: Risk of cardiovascular and all-cause mortality in individuals with diabetes mellitus, impaired fasting glucose, and impaired glucose tolerance: the Australian Diabetes, Obesity, and Lifestyle Study (AusDiab). Circulation. 2007, 116 (2): 151-157. 10.1161/CIRCULATIONAHA.106.685628.CrossRefPubMed
2.
go back to reference Cortez-Dias N, Martins S, Belo A, Fiuza M: VALSIM. Prevalence, management and control of diabetes mellitus and associated risk factors in primary health care in Portugal. Rev Port Cardiol. 2010, 29 (4): 509-537.PubMed Cortez-Dias N, Martins S, Belo A, Fiuza M: VALSIM. Prevalence, management and control of diabetes mellitus and associated risk factors in primary health care in Portugal. Rev Port Cardiol. 2010, 29 (4): 509-537.PubMed
3.
go back to reference Gardete-Correia L, Boavida JM, Raposo JF, Mesquita AC, Fona C, Carvalho R, Massano-Cardoso S: First diabetes prevalence study in Portugal: PREVADIAB study. Diabet Med. 2010, 27 (8): 879-881. 10.1111/j.1464-5491.2010.03017.x.CrossRefPubMed Gardete-Correia L, Boavida JM, Raposo JF, Mesquita AC, Fona C, Carvalho R, Massano-Cardoso S: First diabetes prevalence study in Portugal: PREVADIAB study. Diabet Med. 2010, 27 (8): 879-881. 10.1111/j.1464-5491.2010.03017.x.CrossRefPubMed
4.
go back to reference Wild S, Roglic G, Green A, Sicree R, King H: Global prevalence of diabetes: estimates for the year 2000 and projections for 2030. Diabetes Care. 2004, 27: 1047-1053. 10.2337/diacare.27.5.1047.CrossRefPubMed Wild S, Roglic G, Green A, Sicree R, King H: Global prevalence of diabetes: estimates for the year 2000 and projections for 2030. Diabetes Care. 2004, 27: 1047-1053. 10.2337/diacare.27.5.1047.CrossRefPubMed
5.
go back to reference Fox CS: Cardiovascular disease risk factors, type 2 diabetes mellitus, and the Framingham Heart Study. Trends Cardiovasc Med. 2010, 20 (3): 90-95. 10.1016/j.tcm.2010.08.001.PubMedCentralCrossRefPubMed Fox CS: Cardiovascular disease risk factors, type 2 diabetes mellitus, and the Framingham Heart Study. Trends Cardiovasc Med. 2010, 20 (3): 90-95. 10.1016/j.tcm.2010.08.001.PubMedCentralCrossRefPubMed
6.
go back to reference Sarwar N, Gao P, Seshasai SR, Gobin R, Kaptoge S, Di Angelantonio E, Ingelsson E, Lawlor DA, Selvin E, Stampfer M, Stehouwer CD, Lewington S, Pennells L, Thompson A, Sattar N, White IR, Ray KK, Danesh J: Emerging risk factors collaboration. Diabetes mellitus, fasting blood glucose concentration, and risk of vascular disease: a collaborative meta-analysis of 102 prospective studies. Lancet. 2010, 375: 2215-2222. 10.1016/S0140-6736(10)60484-9.CrossRefPubMed Sarwar N, Gao P, Seshasai SR, Gobin R, Kaptoge S, Di Angelantonio E, Ingelsson E, Lawlor DA, Selvin E, Stampfer M, Stehouwer CD, Lewington S, Pennells L, Thompson A, Sattar N, White IR, Ray KK, Danesh J: Emerging risk factors collaboration. Diabetes mellitus, fasting blood glucose concentration, and risk of vascular disease: a collaborative meta-analysis of 102 prospective studies. Lancet. 2010, 375: 2215-2222. 10.1016/S0140-6736(10)60484-9.CrossRefPubMed
7.
go back to reference Lakka HM, Laaksonen DE, Lakka TA, Niskanen LK, Kumpusalo E, Tuomilehto J, Salonen JT: The metabolic syndrome and total and cardiovascular disease mortality in middle-aged men. JAMA. 2002, 288 (21): 2709-2716. 10.1001/jama.288.21.2709.CrossRefPubMed Lakka HM, Laaksonen DE, Lakka TA, Niskanen LK, Kumpusalo E, Tuomilehto J, Salonen JT: The metabolic syndrome and total and cardiovascular disease mortality in middle-aged men. JAMA. 2002, 288 (21): 2709-2716. 10.1001/jama.288.21.2709.CrossRefPubMed
8.
go back to reference Leuzzi C, Marzullo R, Modena MG: Is menopause a risk factor for ischemic heart disease in women?. G Ital Cardiol. 2012, 13: 401-406. Leuzzi C, Marzullo R, Modena MG: Is menopause a risk factor for ischemic heart disease in women?. G Ital Cardiol. 2012, 13: 401-406.
9.
go back to reference Saltiki K, Doukas C, Kanakakis J, Anastasiou E, Mantzou E, Alevizaki M: Severity of cardiovascular disease in women: relation with exposure to endogenous estrogen. Maturitas. 2006, 55: 51-57. 10.1016/j.maturitas.2005.12.008.CrossRefPubMed Saltiki K, Doukas C, Kanakakis J, Anastasiou E, Mantzou E, Alevizaki M: Severity of cardiovascular disease in women: relation with exposure to endogenous estrogen. Maturitas. 2006, 55: 51-57. 10.1016/j.maturitas.2005.12.008.CrossRefPubMed
10.
go back to reference Carr MC: The emergence of the metabolic syndrome with menopause. J Clin Endocrinol Metab. 2003, 88: 2404-2411. 10.1210/jc.2003-030242.CrossRefPubMed Carr MC: The emergence of the metabolic syndrome with menopause. J Clin Endocrinol Metab. 2003, 88: 2404-2411. 10.1210/jc.2003-030242.CrossRefPubMed
11.
go back to reference Hubert HB, Feinleib M, McNamara PM, Castelli WP: Obesity as an independent risk factor for cardiovascular disease: a 26 year follow up of participants in the Framingham Heart Study. Circulation. 1983, 67: 968-977. 10.1161/01.CIR.67.5.968.CrossRefPubMed Hubert HB, Feinleib M, McNamara PM, Castelli WP: Obesity as an independent risk factor for cardiovascular disease: a 26 year follow up of participants in the Framingham Heart Study. Circulation. 1983, 67: 968-977. 10.1161/01.CIR.67.5.968.CrossRefPubMed
12.
go back to reference Kautzky-Willer A, Kamyar MR, Gerhat D, Handisurya A, Stemer G, Hudson S, Luger A, Lemmens-Gruber R: Sex-specific differences in metabolic control, cardiovascular risk, and interventions in patients with type 2 diabetes mellitus. Gend Med. 2010, 7: 571-583. 10.1016/j.genm.2010.12.001.CrossRefPubMed Kautzky-Willer A, Kamyar MR, Gerhat D, Handisurya A, Stemer G, Hudson S, Luger A, Lemmens-Gruber R: Sex-specific differences in metabolic control, cardiovascular risk, and interventions in patients with type 2 diabetes mellitus. Gend Med. 2010, 7: 571-583. 10.1016/j.genm.2010.12.001.CrossRefPubMed
13.
go back to reference Pan WH, Cedres LB, Liu K, Dyer A, Schoenberger JA, Shekelle RB, Stamler R, Smith D, Collette P, Stamler J: Relationship of clinical diabetes and asymptomatic hyperglycemia to risk of coronary heart disease mortality in men and women. Am J Epidemiol. 1986, 123: 504-516.PubMed Pan WH, Cedres LB, Liu K, Dyer A, Schoenberger JA, Shekelle RB, Stamler R, Smith D, Collette P, Stamler J: Relationship of clinical diabetes and asymptomatic hyperglycemia to risk of coronary heart disease mortality in men and women. Am J Epidemiol. 1986, 123: 504-516.PubMed
14.
go back to reference Pyorala K, Laakso M, Uusitupa M: Diabetes and atherosclerosis: an epidemiologic view. Diabetes Metab Rev. 1987, 3: 463-524. 10.1002/dmr.5610030206.CrossRefPubMed Pyorala K, Laakso M, Uusitupa M: Diabetes and atherosclerosis: an epidemiologic view. Diabetes Metab Rev. 1987, 3: 463-524. 10.1002/dmr.5610030206.CrossRefPubMed
15.
go back to reference Asztalos BF, Schaefer EJ: HDL in atherosclerosis: actor or bystender?. Atherosclerosis. 2003, 4 (Suppl 1): 21-29.CrossRefPubMed Asztalos BF, Schaefer EJ: HDL in atherosclerosis: actor or bystender?. Atherosclerosis. 2003, 4 (Suppl 1): 21-29.CrossRefPubMed
16.
go back to reference Hayden MR, Tyagi SC: Isolated low high density lipoprotein-cholesterol (HDL-C): implications of global risk reduction. Case report and systematic scientific review. Cardiovasc Diabetol. 2005, 4 (1): 1-10.1186/1475-2840-4-1.PubMedCentralCrossRefPubMed Hayden MR, Tyagi SC: Isolated low high density lipoprotein-cholesterol (HDL-C): implications of global risk reduction. Case report and systematic scientific review. Cardiovasc Diabetol. 2005, 4 (1): 1-10.1186/1475-2840-4-1.PubMedCentralCrossRefPubMed
17.
go back to reference Taskinen MR: Diabetic dyslipidemia: from basic research to clinical practice. Diabetologia. 2003, 46: 733-749. 10.1007/s00125-003-1111-y.CrossRefPubMed Taskinen MR: Diabetic dyslipidemia: from basic research to clinical practice. Diabetologia. 2003, 46: 733-749. 10.1007/s00125-003-1111-y.CrossRefPubMed
18.
go back to reference Asztalos BF, Roheim PS, Milani RL, Lefevre M, McNamara JR, Horvath KV, Schaefer EJ: Distribution of ApoA-I-containing HDL subpopulations in patients with coronary heart disease. Arterioscler Thromb Vasc Biol. 2000, 20: 2670-2676. 10.1161/01.ATV.20.12.2670.CrossRefPubMed Asztalos BF, Roheim PS, Milani RL, Lefevre M, McNamara JR, Horvath KV, Schaefer EJ: Distribution of ApoA-I-containing HDL subpopulations in patients with coronary heart disease. Arterioscler Thromb Vasc Biol. 2000, 20: 2670-2676. 10.1161/01.ATV.20.12.2670.CrossRefPubMed
19.
go back to reference Pirillo A, Norata GD, Catapano AL: High-density lipoprotein subfractions - what the clinicians need to know. Cardiology. 2013, 124: 116-125. 10.1159/000346463.CrossRefPubMed Pirillo A, Norata GD, Catapano AL: High-density lipoprotein subfractions - what the clinicians need to know. Cardiology. 2013, 124: 116-125. 10.1159/000346463.CrossRefPubMed
20.
go back to reference Mackness MI, Durrington PN, Mackness B: The role of paraoxonase 1 activity in cardiovascular disease: potential for therapeutic intervention. Am J Cardiovasc Drugs. 2004, 4: 211-217. 10.2165/00129784-200404040-00002.CrossRefPubMed Mackness MI, Durrington PN, Mackness B: The role of paraoxonase 1 activity in cardiovascular disease: potential for therapeutic intervention. Am J Cardiovasc Drugs. 2004, 4: 211-217. 10.2165/00129784-200404040-00002.CrossRefPubMed
21.
go back to reference Mertens A, Holvoet P: Oxidized LDL and HDL: antagonists in atherothrombosis. FASEB J. 2001, 15: 2073-2084. 10.1096/fj.01-0273rev.CrossRefPubMed Mertens A, Holvoet P: Oxidized LDL and HDL: antagonists in atherothrombosis. FASEB J. 2001, 15: 2073-2084. 10.1096/fj.01-0273rev.CrossRefPubMed
22.
go back to reference Mangge H, Almer G, Truschnig-Wilders M, Schmidt A, Gasser R, Fuchs D: Inflammation, adiponectin, obesity and cardiovascular risk. Curr Med Chem. 2010, 17: 4511-4520. 10.2174/092986710794183006.CrossRefPubMed Mangge H, Almer G, Truschnig-Wilders M, Schmidt A, Gasser R, Fuchs D: Inflammation, adiponectin, obesity and cardiovascular risk. Curr Med Chem. 2010, 17: 4511-4520. 10.2174/092986710794183006.CrossRefPubMed
23.
go back to reference Huang SS, Huang PH, Chen YH, Chiang KH, Chen JW, Lin SJ: Association of adiponectin with future cardiovascular events in patients after acute myocardial infarction. J Atheroscler Thromb. 2010, 17: 295-303. 10.5551/jat.3533.CrossRefPubMed Huang SS, Huang PH, Chen YH, Chiang KH, Chen JW, Lin SJ: Association of adiponectin with future cardiovascular events in patients after acute myocardial infarction. J Atheroscler Thromb. 2010, 17: 295-303. 10.5551/jat.3533.CrossRefPubMed
24.
go back to reference Hagberg CE, Mehlem A, Falkevall A, Muhl L, Fam BC, Ortsäter H, Scotney P, Nyqvist D, Samén E, Lu L, Stone-Elander S, Proietto J, Andrikopoulos S, Sjöholm A, Nash A, Eriksson U: Targeting VEGF-B as a novel treatment for insulin resistance and type 2 diabetes. Nature. 2012, 490 (7420): 426-430. 10.1038/nature11464.CrossRefPubMed Hagberg CE, Mehlem A, Falkevall A, Muhl L, Fam BC, Ortsäter H, Scotney P, Nyqvist D, Samén E, Lu L, Stone-Elander S, Proietto J, Andrikopoulos S, Sjöholm A, Nash A, Eriksson U: Targeting VEGF-B as a novel treatment for insulin resistance and type 2 diabetes. Nature. 2012, 490 (7420): 426-430. 10.1038/nature11464.CrossRefPubMed
25.
go back to reference Li Q, Yang Z, Lu B, Wen J, Ye Z, Chen L, He M, Tao X, Zhang W, Huang Y, Zhang Z, Qu S, Hu R: Serum uric acid level and its association with metabolic syndrome and carotid atherosclerosis in patients with type 2 diabetes. Cardiovasc Diabetol. 2011, 10: 72-10.1186/1475-2840-10-72.PubMedCentralCrossRefPubMed Li Q, Yang Z, Lu B, Wen J, Ye Z, Chen L, He M, Tao X, Zhang W, Huang Y, Zhang Z, Qu S, Hu R: Serum uric acid level and its association with metabolic syndrome and carotid atherosclerosis in patients with type 2 diabetes. Cardiovasc Diabetol. 2011, 10: 72-10.1186/1475-2840-10-72.PubMedCentralCrossRefPubMed
26.
go back to reference Dehghan A, van Hoek M, Sijbrands EJ, Hofman A, Witteman JC: High serum uric acid as a novel risk factor for type 2 diabetes. Diabetes Care. 2008, 31 (2): 361-362.CrossRefPubMed Dehghan A, van Hoek M, Sijbrands EJ, Hofman A, Witteman JC: High serum uric acid as a novel risk factor for type 2 diabetes. Diabetes Care. 2008, 31 (2): 361-362.CrossRefPubMed
27.
go back to reference Kaushik M, Sontineni SP, Hunter C: Cardiovascular disease and androgens: a review. Int J Cardiol. 2010, 142: 8-14. 10.1016/j.ijcard.2009.10.033.CrossRefPubMed Kaushik M, Sontineni SP, Hunter C: Cardiovascular disease and androgens: a review. Int J Cardiol. 2010, 142: 8-14. 10.1016/j.ijcard.2009.10.033.CrossRefPubMed
28.
go back to reference Rossouw JE, Anderson GL, Prentice RL, LaCroix AZ, Kooperberg C, Stefanick ML, Jackson RD, Beresford SA, Howard BV, Johnson KC, Kotchen JM, Ockene J: Risks and benefits of estrogen plus progestin in healthy postmenopausal women: principal results from the women’s health initiative randomized controlled trial. JAMA. 2002, 288: 321-333. 10.1001/jama.288.3.321.CrossRefPubMed Rossouw JE, Anderson GL, Prentice RL, LaCroix AZ, Kooperberg C, Stefanick ML, Jackson RD, Beresford SA, Howard BV, Johnson KC, Kotchen JM, Ockene J: Risks and benefits of estrogen plus progestin in healthy postmenopausal women: principal results from the women’s health initiative randomized controlled trial. JAMA. 2002, 288: 321-333. 10.1001/jama.288.3.321.CrossRefPubMed
29.
go back to reference Casiglia E, Tikhonoff V, Caffi S, Bascelli A, Schiavon L, Guidotti F, Saugo M, Giacomazzo M, Martini B, Mazza A, D’este D, Pessina AC: Menopause does not affect blood pressure and risk profile, and menopausal women do not become similar to men. J Hypertens. 2008, 26: 1983-1992. 10.1097/HJH.0b013e32830bfdd9.CrossRefPubMed Casiglia E, Tikhonoff V, Caffi S, Bascelli A, Schiavon L, Guidotti F, Saugo M, Giacomazzo M, Martini B, Mazza A, D’este D, Pessina AC: Menopause does not affect blood pressure and risk profile, and menopausal women do not become similar to men. J Hypertens. 2008, 26: 1983-1992. 10.1097/HJH.0b013e32830bfdd9.CrossRefPubMed
30.
go back to reference Toth MJ, Tchernof A, Sites CK, Poehlman ET: Effect of menopausal status on body composition and abdominal fat distribution. Int J Obes Relat Metab Disord. 2000, 24: 226-231. 10.1038/sj.ijo.0801118.CrossRefPubMed Toth MJ, Tchernof A, Sites CK, Poehlman ET: Effect of menopausal status on body composition and abdominal fat distribution. Int J Obes Relat Metab Disord. 2000, 24: 226-231. 10.1038/sj.ijo.0801118.CrossRefPubMed
31.
go back to reference Kaseta JR, Skafar DF, Ram JL, Jacober SJ, Sowers JR: Cardiovascular disease in the diabetic woman. J Clin Endocrinol Metab. 1999, 84: 1835-1838. 10.1210/jc.84.6.1835.CrossRefPubMed Kaseta JR, Skafar DF, Ram JL, Jacober SJ, Sowers JR: Cardiovascular disease in the diabetic woman. J Clin Endocrinol Metab. 1999, 84: 1835-1838. 10.1210/jc.84.6.1835.CrossRefPubMed
32.
go back to reference Steinberg HO, Paradisi G, Cronin J, Crowde K, Hempfling A, Hook G, Baron AD: Type II diabetes abrogates sex differences in endothelial function in premenopausal women. Circulation. 2000, 101: 2040-2046. 10.1161/01.CIR.101.17.2040.CrossRefPubMed Steinberg HO, Paradisi G, Cronin J, Crowde K, Hempfling A, Hook G, Baron AD: Type II diabetes abrogates sex differences in endothelial function in premenopausal women. Circulation. 2000, 101: 2040-2046. 10.1161/01.CIR.101.17.2040.CrossRefPubMed
33.
go back to reference Haffner SM, Lehto S, Ronnemaa T, Pyorala K, Laakso M: Mortality from coronary heart disease in subjects with type 2 diabetes and in non-diabetic subjects with and without prior myocardial infarction. N Engl J Med. 1998, 339: 229-234. 10.1056/NEJM199807233390404.CrossRefPubMed Haffner SM, Lehto S, Ronnemaa T, Pyorala K, Laakso M: Mortality from coronary heart disease in subjects with type 2 diabetes and in non-diabetic subjects with and without prior myocardial infarction. N Engl J Med. 1998, 339: 229-234. 10.1056/NEJM199807233390404.CrossRefPubMed
34.
go back to reference Eckel RH, Kahn R, Robertson RM, Rizza RA: Preventing cardiovascular disease and diabetes: a call to action from the American Diabetes Association and the American Heart Association. Diabetes Care. 2006, 29: 1697-1699. 10.2337/dc06-9911.CrossRefPubMed Eckel RH, Kahn R, Robertson RM, Rizza RA: Preventing cardiovascular disease and diabetes: a call to action from the American Diabetes Association and the American Heart Association. Diabetes Care. 2006, 29: 1697-1699. 10.2337/dc06-9911.CrossRefPubMed
35.
go back to reference Barrett-Connor EL, Cohn BA, Wingard DL, Edelstein SL: Why is diabetes mellitus a stronger risk factor for fatal ischemic heart disease in women than in men? The Rancho Bernardo Study. JAMA. 1991, 265: 627-631. 10.1001/jama.1991.03460050081025.CrossRefPubMed Barrett-Connor EL, Cohn BA, Wingard DL, Edelstein SL: Why is diabetes mellitus a stronger risk factor for fatal ischemic heart disease in women than in men? The Rancho Bernardo Study. JAMA. 1991, 265: 627-631. 10.1001/jama.1991.03460050081025.CrossRefPubMed
36.
go back to reference Zhang L, Qiao Q, Tuomilehto J, Hammar N, Ruotolo G, Stehouwer CD, Heine RJ, Eliasson M, Zethelius B, DECODE Study Group: The impact of dyslipidaemia on cardiovascular mortality in individuals without a prior history of diabetes in the DECODE Study. Atherosclerosis. 2009, 206 (1): 298-302. 10.1016/j.atherosclerosis.2008.12.043.CrossRefPubMed Zhang L, Qiao Q, Tuomilehto J, Hammar N, Ruotolo G, Stehouwer CD, Heine RJ, Eliasson M, Zethelius B, DECODE Study Group: The impact of dyslipidaemia on cardiovascular mortality in individuals without a prior history of diabetes in the DECODE Study. Atherosclerosis. 2009, 206 (1): 298-302. 10.1016/j.atherosclerosis.2008.12.043.CrossRefPubMed
37.
go back to reference Pollex RL, Joy TR, Hegele RA: Emerging antidyslipidemic drugs. Expert Opin Emerg Drugs. 2008, 13 (2): 363-381. 10.1517/14728214.13.2.363.CrossRefPubMed Pollex RL, Joy TR, Hegele RA: Emerging antidyslipidemic drugs. Expert Opin Emerg Drugs. 2008, 13 (2): 363-381. 10.1517/14728214.13.2.363.CrossRefPubMed
38.
go back to reference Tenenbaum A, Fisman EZ, Motro M, Adler Y: Atherogenic dyslipidemia in metabolic syndrome and type 2 diabetes: therapeutic options beyond statins. Cardiovasc Diabetol. 2006, 5: 20-10.1186/1475-2840-5-20.PubMedCentralCrossRefPubMed Tenenbaum A, Fisman EZ, Motro M, Adler Y: Atherogenic dyslipidemia in metabolic syndrome and type 2 diabetes: therapeutic options beyond statins. Cardiovasc Diabetol. 2006, 5: 20-10.1186/1475-2840-5-20.PubMedCentralCrossRefPubMed
39.
go back to reference Cardenas GA, Lavie CJ, Cardenas V, Milani RV, McCullough PA: The importance of recognizing and treating low levels of high-density lipoprotein cholesterol: a new era in atherosclerosis management. Rev Cardiovasc Med. 2008, 9 (4): 239-258.PubMed Cardenas GA, Lavie CJ, Cardenas V, Milani RV, McCullough PA: The importance of recognizing and treating low levels of high-density lipoprotein cholesterol: a new era in atherosclerosis management. Rev Cardiovasc Med. 2008, 9 (4): 239-258.PubMed
40.
go back to reference Sharma RK, Singh VN, Reddy HK: Thinking beyond low-density lipoprotein cholesterol: strategies to further reduce cardiovascular risk. Vasc Health Risk Manag. 2009, 5: 793-799.PubMedCentralCrossRefPubMed Sharma RK, Singh VN, Reddy HK: Thinking beyond low-density lipoprotein cholesterol: strategies to further reduce cardiovascular risk. Vasc Health Risk Manag. 2009, 5: 793-799.PubMedCentralCrossRefPubMed
41.
go back to reference Calle MC, Fernandez ML: Inflammation and type 2 diabetes. Diabetes Metab. 2012, 38 (3): 183-191. 10.1016/j.diabet.2011.11.006.CrossRefPubMed Calle MC, Fernandez ML: Inflammation and type 2 diabetes. Diabetes Metab. 2012, 38 (3): 183-191. 10.1016/j.diabet.2011.11.006.CrossRefPubMed
42.
go back to reference Miazgowski T, Noworyta-Zietara M, Safranow K, Ziemak J, Widecka K: Serum adiponectin, bone mineral density and bone turnover markers in post-menopausal women with newly diagnosed Type 2 diabetes: a 12-month follow-up. Diabet Med. 2012, 29: 62-69. 10.1111/j.1464-5491.2011.03381.x.CrossRefPubMed Miazgowski T, Noworyta-Zietara M, Safranow K, Ziemak J, Widecka K: Serum adiponectin, bone mineral density and bone turnover markers in post-menopausal women with newly diagnosed Type 2 diabetes: a 12-month follow-up. Diabet Med. 2012, 29: 62-69. 10.1111/j.1464-5491.2011.03381.x.CrossRefPubMed
43.
go back to reference Kawamoto R, Tabara Y, Kohara K, Miki T, Kusunoki T, Takayama S, Abe M, Katoh T, Ohtsuka N: Association between fasting plasma glucose and high-sensitivity C-reactive protein: gender differences in a Japanese community-dwelling population. Cardiovasc Diabetol. 2011, 10: 51-10.1186/1475-2840-10-51.PubMedCentralCrossRefPubMed Kawamoto R, Tabara Y, Kohara K, Miki T, Kusunoki T, Takayama S, Abe M, Katoh T, Ohtsuka N: Association between fasting plasma glucose and high-sensitivity C-reactive protein: gender differences in a Japanese community-dwelling population. Cardiovasc Diabetol. 2011, 10: 51-10.1186/1475-2840-10-51.PubMedCentralCrossRefPubMed
44.
go back to reference Goodarzi MT, Babaahmadi-Rezaei H, Kadkhodaei-Eliaderani M, Haddadinezhad S: Relationship of serum adiponectin with blood lipids, HbA(1)c, and hs-CRP in type II diabetic postmenopausal women. J Clin Lab Anal. 2007, 21 (3): 197-200. 10.1002/jcla.20175.CrossRefPubMed Goodarzi MT, Babaahmadi-Rezaei H, Kadkhodaei-Eliaderani M, Haddadinezhad S: Relationship of serum adiponectin with blood lipids, HbA(1)c, and hs-CRP in type II diabetic postmenopausal women. J Clin Lab Anal. 2007, 21 (3): 197-200. 10.1002/jcla.20175.CrossRefPubMed
45.
go back to reference Rasul S, Ilhan A, Reiter MH, Baumgartner-Parzer S, Kautzky-Willer A: Relations of adiponectin to levels of metabolic parameters and sexual hormones in elderly type 2 diabetic patients. Gend Med. 2011, 8 (2): 93-102. 10.1016/j.genm.2011.01.004.CrossRefPubMed Rasul S, Ilhan A, Reiter MH, Baumgartner-Parzer S, Kautzky-Willer A: Relations of adiponectin to levels of metabolic parameters and sexual hormones in elderly type 2 diabetic patients. Gend Med. 2011, 8 (2): 93-102. 10.1016/j.genm.2011.01.004.CrossRefPubMed
46.
go back to reference Shepherd J: Dyslipidaemia in diabetic patients: time for a rethink. Diabetes Obes Metab. 2007, 9: 609-616. 10.1111/j.1463-1326.2006.00642.x.CrossRefPubMed Shepherd J: Dyslipidaemia in diabetic patients: time for a rethink. Diabetes Obes Metab. 2007, 9: 609-616. 10.1111/j.1463-1326.2006.00642.x.CrossRefPubMed
47.
go back to reference Russo GT, Horvath KV, Di Benedetto A, Giandalia A, Cucinotta D, Asztalos B: Influence of menopause and cholesteryl ester transfer protein (CETP) TaqIB polymorphism on lipid profile and HDL subpopulations distribution in women with and without type 2 diabetes. Atherosclerosis. 2010, 210: 294-301. 10.1016/j.atherosclerosis.2009.11.011.CrossRefPubMed Russo GT, Horvath KV, Di Benedetto A, Giandalia A, Cucinotta D, Asztalos B: Influence of menopause and cholesteryl ester transfer protein (CETP) TaqIB polymorphism on lipid profile and HDL subpopulations distribution in women with and without type 2 diabetes. Atherosclerosis. 2010, 210: 294-301. 10.1016/j.atherosclerosis.2009.11.011.CrossRefPubMed
48.
go back to reference Hyvärinen M, Tuomilehto J, Laatikainen T, Söderberg S, Eliasson M, Nilsson P, Qiao Q: The impact of diabetes on coronary heart disease differs from that on ischaemic stroke with regard to the gender. Cardiovasc Diabetol. 2009, 8: 17-10.1186/1475-2840-8-17.PubMedCentralCrossRefPubMed Hyvärinen M, Tuomilehto J, Laatikainen T, Söderberg S, Eliasson M, Nilsson P, Qiao Q: The impact of diabetes on coronary heart disease differs from that on ischaemic stroke with regard to the gender. Cardiovasc Diabetol. 2009, 8: 17-10.1186/1475-2840-8-17.PubMedCentralCrossRefPubMed
49.
go back to reference Liu Z, Ho SC: The association of serum C-reactive protein, uric acid and magnesium with insulin resistance in Chinese postmenopausal women with prediabetes or early untreated diabetes. Maturitas. 2011, 70: 176-181. 10.1016/j.maturitas.2011.07.007.CrossRefPubMed Liu Z, Ho SC: The association of serum C-reactive protein, uric acid and magnesium with insulin resistance in Chinese postmenopausal women with prediabetes or early untreated diabetes. Maturitas. 2011, 70: 176-181. 10.1016/j.maturitas.2011.07.007.CrossRefPubMed
50.
go back to reference Göbl CS, Bozkurt L, Lueck J, El-Samahi M, Grösser P, Clodi M, Luger A, Kautzky-Willer A: Sex-specific differences in long-term glycemic control and cardiometabolic parameters in patients with type 1 diabetes treated at a tertiary care centre: gender aspects in type 1 diabetes. Wien Klin Wochenschr. 2012, 124: 742-749. 10.1007/s00508-012-0246-6.CrossRefPubMed Göbl CS, Bozkurt L, Lueck J, El-Samahi M, Grösser P, Clodi M, Luger A, Kautzky-Willer A: Sex-specific differences in long-term glycemic control and cardiometabolic parameters in patients with type 1 diabetes treated at a tertiary care centre: gender aspects in type 1 diabetes. Wien Klin Wochenschr. 2012, 124: 742-749. 10.1007/s00508-012-0246-6.CrossRefPubMed
51.
go back to reference Lin W-Y, Yang W-S, Lee L-T, Chen C-Y, Liu C-S, Lin C-C, Huang K-C: Insulin resistance, obesity, and metabolic syndrome among non-diabetic pre- and post-menopausal women in North Taiwan. Int J Obes. 2006, 30: 912-917. 10.1038/sj.ijo.0803240.CrossRef Lin W-Y, Yang W-S, Lee L-T, Chen C-Y, Liu C-S, Lin C-C, Huang K-C: Insulin resistance, obesity, and metabolic syndrome among non-diabetic pre- and post-menopausal women in North Taiwan. Int J Obes. 2006, 30: 912-917. 10.1038/sj.ijo.0803240.CrossRef
52.
go back to reference Saltiki K, Cimponeriu A, Lili K, Peppa M, Anastasiou E, Alevizaki M: Severity of coronary artery disease in postmenopausal diabetic women. Hormones. 2008, 7 (2): 148-155.PubMed Saltiki K, Cimponeriu A, Lili K, Peppa M, Anastasiou E, Alevizaki M: Severity of coronary artery disease in postmenopausal diabetic women. Hormones. 2008, 7 (2): 148-155.PubMed
Metadata
Title
Diabetes abrogates sex differences and aggravates cardiometabolic risk in postmenopausal women
Authors
Filipa Mascarenhas-Melo
Daniela Marado
Filipe Palavra
José Sereno
Álvaro Coelho
Rui Pinto
Edite Teixeira-Lemos
Frederico Teixeira
Flávio Reis
Publication date
01-12-2013
Publisher
BioMed Central
Published in
Cardiovascular Diabetology / Issue 1/2013
Electronic ISSN: 1475-2840
DOI
https://doi.org/10.1186/1475-2840-12-61

Other articles of this Issue 1/2013

Cardiovascular Diabetology 1/2013 Go to the issue