Skip to main content
Top
Published in: Cardiovascular Diabetology 1/2019

Open Access 01-12-2019 | Original investigation

Prospective study of hemoglobin A1c and incident carotid artery plaque in Chinese adults without diabetes

Authors: Renying Xu, Ting Zhang, Yanping Wan, Zhuping Fan, Xiang Gao

Published in: Cardiovascular Diabetology | Issue 1/2019

Login to get access

Abstract

Background

Diabetes has been reported to be associated with carotid artery plaque (CAP). However, it remains unclear whether hemoglobin A1c (HbA1c) level, a marker for long-term glycemic status, is associated with altered CAP risk in individuals with fasting blood glucose (FBG) concentrations below the current cutoff for diabetes.

Methods

Included were 16,863 Chinese adults (aged 18 years or more; 9855 men and 7008 women) with fasting blood glucose < 7.0 mmol/L at baseline (2013). Both HbA1c level and CAP (assessed via ultrasound B-mode imaging) were annually assessed during 2014–2018. All the participants were further classified into three groups based on baseline HbA1c level: ≤ 5.6%, 5.7–6.4%, and ≥ 6.5%. We used Cox proportional-hazards model to evaluate the association between HbA1c level and incident CAP, adjusting for a series of potential confounders.

Results

During 5 years of follow up, 3942 incident CAP cases were identified. Individuals with higher baseline HbA1c had higher future risk of CAP (p-trend < 0.001). In the full-adjusted model, each percent increase of HbA1c was associated with a 56% (HR = 1.56, 95% CI 1.37, 1.78) higher risk of CAP. Excluding participants with chronic inflammation, as assessed by high-sensitivity C-reactive protein and white blood cell, and those with FBG ≥ 5.6 mmol/L at baseline generated similar results.

Conclusions

Elevated HbA1c level was associated with high risk of developing CAP in Chinese adults without FBG defined diabetes.
Appendix
Available only for authorised users
Literature
1.
go back to reference Flaherty ML, Kissela B, Khoury JC, Alwell K, Moomaw CJ, Woo D, et al. Carotid artery stenosis as a cause of stroke. Neuroepidemiology. 2013;40(1):36–41.PubMedCrossRef Flaherty ML, Kissela B, Khoury JC, Alwell K, Moomaw CJ, Woo D, et al. Carotid artery stenosis as a cause of stroke. Neuroepidemiology. 2013;40(1):36–41.PubMedCrossRef
2.
go back to reference Kim G, Youn HJ, Choi YS, Jung HO, Chung WS, Kim CM. Is carotid artery evaluation necessary for primary prevention in asymptomatic high-risk patients without atherosclerotic cardiovascular disease? Clin Interv Aging. 2015;10:1111–9.PubMedPubMedCentralCrossRef Kim G, Youn HJ, Choi YS, Jung HO, Chung WS, Kim CM. Is carotid artery evaluation necessary for primary prevention in asymptomatic high-risk patients without atherosclerotic cardiovascular disease? Clin Interv Aging. 2015;10:1111–9.PubMedPubMedCentralCrossRef
3.
go back to reference Hata J, Kiyohara Y. Epidemiology of stroke and coronary artery disease in Asia. Circ J. 2013;77(8):1923–32.PubMedCrossRef Hata J, Kiyohara Y. Epidemiology of stroke and coronary artery disease in Asia. Circ J. 2013;77(8):1923–32.PubMedCrossRef
4.
go back to reference Herrington W, Lacey B, Sherliker P, Armitage J, Lewington S. Epidemiology of atherosclerosis and the potential to reduce the global burden of atherothrombotic disease. Circ Res. 2016;118(4):535–46.PubMedCrossRef Herrington W, Lacey B, Sherliker P, Armitage J, Lewington S. Epidemiology of atherosclerosis and the potential to reduce the global burden of atherothrombotic disease. Circ Res. 2016;118(4):535–46.PubMedCrossRef
5.
go back to reference Yahagi K, Kolodgie FD, Lutter C, Mori H, Romero ME, Finn AV, et al. Pathology of human coronary and carotid artery atherosclerosis and vascular calcification in diabetes mellitus. Arterioscler Thromb Vasc Biol. 2017;37(2):191–204.PubMedCrossRef Yahagi K, Kolodgie FD, Lutter C, Mori H, Romero ME, Finn AV, et al. Pathology of human coronary and carotid artery atherosclerosis and vascular calcification in diabetes mellitus. Arterioscler Thromb Vasc Biol. 2017;37(2):191–204.PubMedCrossRef
6.
go back to reference Yazdanpanah S, Rabiee M, Tahriri M, Abdolrahim M, Rajab A, Jazayeri HE, et al. Evaluation of glycated albumin (GA) and GA/HbA1c ratio for diagnosis of diabetes and glycemic control: a comprehensive review. Crit Rev Clin Lab Sci. 2017;54(4):219–32.CrossRef Yazdanpanah S, Rabiee M, Tahriri M, Abdolrahim M, Rajab A, Jazayeri HE, et al. Evaluation of glycated albumin (GA) and GA/HbA1c ratio for diagnosis of diabetes and glycemic control: a comprehensive review. Crit Rev Clin Lab Sci. 2017;54(4):219–32.CrossRef
7.
go back to reference Mostaza JM, Lahoz C, Salinero-Fort MA, de Burgos-Lunar C, Laguna F, Estirado E, et al. Carotid atherosclerosis severity in relation to glycemic status: a cross-sectional population study. Atherosclerosis. 2015;242(2):377–82.PubMedCrossRef Mostaza JM, Lahoz C, Salinero-Fort MA, de Burgos-Lunar C, Laguna F, Estirado E, et al. Carotid atherosclerosis severity in relation to glycemic status: a cross-sectional population study. Atherosclerosis. 2015;242(2):377–82.PubMedCrossRef
8.
go back to reference Verdoia M, Schaffer A, Cassetti E, Barbieri L, Di Ruocco MV, Perrone-Filardi P, et al. Glycosylated hemoglobin and coronary artery disease in patients without diabetes mellitus. Am J Prev Med. 2014;47(1):9–16.PubMedCrossRef Verdoia M, Schaffer A, Cassetti E, Barbieri L, Di Ruocco MV, Perrone-Filardi P, et al. Glycosylated hemoglobin and coronary artery disease in patients without diabetes mellitus. Am J Prev Med. 2014;47(1):9–16.PubMedCrossRef
9.
go back to reference Prasad K. Does HbA1cc play a role in the development of cardiovascular diseases? Curr Pharm Des. 2018;24(24):2876–82.PubMedCrossRef Prasad K. Does HbA1cc play a role in the development of cardiovascular diseases? Curr Pharm Des. 2018;24(24):2876–82.PubMedCrossRef
10.
go back to reference Marini MA, Fiorentino TV, Succurro E, Pedace E, Andreozzi F, Sciacqua A, et al. Association between hemoglobin glycation index with insulin resistance and carotid atherosclerosis in non-diabetic individuals. PLoS ONE. 2017;12(4):e0175547.PubMedPubMedCentralCrossRef Marini MA, Fiorentino TV, Succurro E, Pedace E, Andreozzi F, Sciacqua A, et al. Association between hemoglobin glycation index with insulin resistance and carotid atherosclerosis in non-diabetic individuals. PLoS ONE. 2017;12(4):e0175547.PubMedPubMedCentralCrossRef
11.
go back to reference American Diabetes A. Diagnosis and classification of diabetes mellitus. Diabetes Care. 2014;37(Suppl 1):S81–90.CrossRef American Diabetes A. Diagnosis and classification of diabetes mellitus. Diabetes Care. 2014;37(Suppl 1):S81–90.CrossRef
12.
go back to reference Selvin E, Steffes MW, Zhu H, Matsushita K, Wagenknecht L, Pankow J, et al. Glycated hemoglobin, diabetes, and cardiovascular risk in nondiabetic adults. N Engl J Med. 2010;362(9):800–11.PubMedPubMedCentralCrossRef Selvin E, Steffes MW, Zhu H, Matsushita K, Wagenknecht L, Pankow J, et al. Glycated hemoglobin, diabetes, and cardiovascular risk in nondiabetic adults. N Engl J Med. 2010;362(9):800–11.PubMedPubMedCentralCrossRef
13.
go back to reference Skriver MV, Borch-Johnsen K, Lauritzen T, Sandbaek A. HbA1c as predictor of all-cause mortality in individuals at high risk of diabetes with normal glucose tolerance, identified by screening: a follow-up study of the Anglo-Danish-Dutch Study of Intensive Treatment in People with Screen-Detected Diabetes in Primary Care (ADDITION). Denmark. Diabetologia. 2010;53(11):2328–33.PubMedCrossRef Skriver MV, Borch-Johnsen K, Lauritzen T, Sandbaek A. HbA1c as predictor of all-cause mortality in individuals at high risk of diabetes with normal glucose tolerance, identified by screening: a follow-up study of the Anglo-Danish-Dutch Study of Intensive Treatment in People with Screen-Detected Diabetes in Primary Care (ADDITION). Denmark. Diabetologia. 2010;53(11):2328–33.PubMedCrossRef
14.
go back to reference Alizargar J, Bai CH. Factors associated with carotid Intima media thickness and carotid plaque score in community-dwelling and non-diabetic individuals. BMC Cardiovasc Disord. 2018;18(1):21.PubMedPubMedCentralCrossRef Alizargar J, Bai CH. Factors associated with carotid Intima media thickness and carotid plaque score in community-dwelling and non-diabetic individuals. BMC Cardiovasc Disord. 2018;18(1):21.PubMedPubMedCentralCrossRef
15.
go back to reference Scicali R, Giral P, Gallo A, Di Pino A, Rabuazzo AM, Purrello F, et al. HbA1c increase is associated with higher coronary and peripheral atherosclerotic burden in non diabetic patients. Atherosclerosis. 2016;255:102–8.PubMedCrossRef Scicali R, Giral P, Gallo A, Di Pino A, Rabuazzo AM, Purrello F, et al. HbA1c increase is associated with higher coronary and peripheral atherosclerotic burden in non diabetic patients. Atherosclerosis. 2016;255:102–8.PubMedCrossRef
16.
go back to reference Ma X, Shen Y, Hu X, Hao Y, Luo Y, Tang J, et al. Associations of glycated haemoglobin A1c and glycated albumin with subclinical atherosclerosis in middle-aged and elderly Chinese population with impaired glucose regulation. Clin Exp Pharmacol Physiol. 2015;42(6):582–7.PubMedCrossRef Ma X, Shen Y, Hu X, Hao Y, Luo Y, Tang J, et al. Associations of glycated haemoglobin A1c and glycated albumin with subclinical atherosclerosis in middle-aged and elderly Chinese population with impaired glucose regulation. Clin Exp Pharmacol Physiol. 2015;42(6):582–7.PubMedCrossRef
17.
go back to reference Zhu W, Sun T, Shi H, Li J, Zhu J, Qi W, et al. Combined effects of glycated hemoglobin A1c and blood pressure on carotid artery atherosclerosis in nondiabetic patients. Clin Cardiol. 2010;33(9):542–7.PubMedPubMedCentralCrossRef Zhu W, Sun T, Shi H, Li J, Zhu J, Qi W, et al. Combined effects of glycated hemoglobin A1c and blood pressure on carotid artery atherosclerosis in nondiabetic patients. Clin Cardiol. 2010;33(9):542–7.PubMedPubMedCentralCrossRef
18.
go back to reference Hung CS, Lee PC, Li HY, Ma WY, Lin MS, Wei JN, et al. Haemoglobin A1c is associated with carotid intima-media thickness in a Chinese population. Clin Endocrinol (Oxf). 2011;75(6):780–5.CrossRef Hung CS, Lee PC, Li HY, Ma WY, Lin MS, Wei JN, et al. Haemoglobin A1c is associated with carotid intima-media thickness in a Chinese population. Clin Endocrinol (Oxf). 2011;75(6):780–5.CrossRef
19.
go back to reference Nazish S, Zafar A, Shahid R, Albakr A, Alkhamis FA, Aljaafari D, et al. Relationship between glycated haemoglobin and carotid atherosclerotic disease among patients with acute ischaemic stroke. Sultan Qaboos Univ Med J. 2018;18(3):e311–7.PubMedPubMedCentralCrossRef Nazish S, Zafar A, Shahid R, Albakr A, Alkhamis FA, Aljaafari D, et al. Relationship between glycated haemoglobin and carotid atherosclerotic disease among patients with acute ischaemic stroke. Sultan Qaboos Univ Med J. 2018;18(3):e311–7.PubMedPubMedCentralCrossRef
20.
go back to reference Lee YH, Shin MH, Choi JS, Rhee JA, Nam HS, Jeong SK, et al. HbA1c is significantly associated with arterial stiffness but not with carotid atherosclerosis in a community-based population without type 2 diabetes: the Dong-gu study. Atherosclerosis. 2016;247:1–6.PubMedCrossRef Lee YH, Shin MH, Choi JS, Rhee JA, Nam HS, Jeong SK, et al. HbA1c is significantly associated with arterial stiffness but not with carotid atherosclerosis in a community-based population without type 2 diabetes: the Dong-gu study. Atherosclerosis. 2016;247:1–6.PubMedCrossRef
21.
go back to reference McNeely MJ, McClelland RL, Bild DE, Jacobs DR Jr, Tracy RP, Cushman M, et al. The association between A1C and subclinical cardiovascular disease: the multi-ethnic study of atherosclerosis. Diabetes Care. 2009;32(9):1727–33.PubMedPubMedCentralCrossRef McNeely MJ, McClelland RL, Bild DE, Jacobs DR Jr, Tracy RP, Cushman M, et al. The association between A1C and subclinical cardiovascular disease: the multi-ethnic study of atherosclerosis. Diabetes Care. 2009;32(9):1727–33.PubMedPubMedCentralCrossRef
22.
go back to reference Sander D, Schulze-Horn C, Bickel H, Gnahn H, Bartels E, Conrad B. Combined effects of hemoglobin A1c and C-reactive protein on the progression of subclinical carotid atherosclerosis: the INVADE study. Stroke. 2006;37(2):351–7.PubMedCrossRef Sander D, Schulze-Horn C, Bickel H, Gnahn H, Bartels E, Conrad B. Combined effects of hemoglobin A1c and C-reactive protein on the progression of subclinical carotid atherosclerosis: the INVADE study. Stroke. 2006;37(2):351–7.PubMedCrossRef
23.
go back to reference Ma H, Gao X, Lin HD, Hu Y, Li XM, Gao J, et al. Glycated haemoglobin in diagnosis of diabetes mellitus and pre-diabetes among middle-aged and elderly population: Shanghai Changfeng study. Biomed Environ Sci. 2013;26(3):155–62.PubMed Ma H, Gao X, Lin HD, Hu Y, Li XM, Gao J, et al. Glycated haemoglobin in diagnosis of diabetes mellitus and pre-diabetes among middle-aged and elderly population: Shanghai Changfeng study. Biomed Environ Sci. 2013;26(3):155–62.PubMed
24.
go back to reference Xu R, Zhang Y, Gao X, Wan Y, Fan Z. High-sensitivity CRP (C-Reactive Protein) is associated with incident carotid artery plaque in Chinese aged adults. Stroke. 2019;50(7):1655–60.PubMedCrossRef Xu R, Zhang Y, Gao X, Wan Y, Fan Z. High-sensitivity CRP (C-Reactive Protein) is associated with incident carotid artery plaque in Chinese aged adults. Stroke. 2019;50(7):1655–60.PubMedCrossRef
25.
go back to reference Mathiesen EB, Johnsen SH. Ultrasonographic measurements of subclinical carotid atherosclerosis in prediction of ischemic stroke. Acta Neurol Scand Suppl. 2009;189:68–72.CrossRef Mathiesen EB, Johnsen SH. Ultrasonographic measurements of subclinical carotid atherosclerosis in prediction of ischemic stroke. Acta Neurol Scand Suppl. 2009;189:68–72.CrossRef
26.
go back to reference Kong X, Ma Y, Chen J, Luo Q, Yu X, Li Y, et al. Evaluation of the Chronic Kidney Disease Epidemiology Collaboration equation for estimating glomerular filtration rate in the Chinese population. Nephrol Dial Transplant. 2013;28(3):641–51.PubMedCrossRef Kong X, Ma Y, Chen J, Luo Q, Yu X, Li Y, et al. Evaluation of the Chronic Kidney Disease Epidemiology Collaboration equation for estimating glomerular filtration rate in the Chinese population. Nephrol Dial Transplant. 2013;28(3):641–51.PubMedCrossRef
27.
go back to reference Wu Z, Huang Z, Jin W, Rimm EB, Lichtenstein AH, Kris-Etherton PM, et al. Peripheral inflammatory biomarkers for myocardial infarction risk: a prospective community-based study. Clin Chem. 2017;63(3):663–72.PubMedCrossRef Wu Z, Huang Z, Jin W, Rimm EB, Lichtenstein AH, Kris-Etherton PM, et al. Peripheral inflammatory biomarkers for myocardial infarction risk: a prospective community-based study. Clin Chem. 2017;63(3):663–72.PubMedCrossRef
28.
go back to reference Jin C, Chen S, Vaidya A, Wu Y, Wu Z, Hu FB, et al. Longitudinal change in fasting blood glucose and myocardial infarction risk in a population without diabetes. Diabetes Care. 2017;40(11):1565–72.PubMedPubMedCentralCrossRef Jin C, Chen S, Vaidya A, Wu Y, Wu Z, Hu FB, et al. Longitudinal change in fasting blood glucose and myocardial infarction risk in a population without diabetes. Diabetes Care. 2017;40(11):1565–72.PubMedPubMedCentralCrossRef
29.
go back to reference Fernandez-Friera L, Fuster V, Lopez-Melgar B, Oliva B, Sanchez-Gonzalez J, Macias A, et al. Vascular Inflammation in Subclinical Atherosclerosis Detected by Hybrid PET/MRI. J Am Coll Cardiol. 2019;73(12):1371–82.PubMedCrossRef Fernandez-Friera L, Fuster V, Lopez-Melgar B, Oliva B, Sanchez-Gonzalez J, Macias A, et al. Vascular Inflammation in Subclinical Atherosclerosis Detected by Hybrid PET/MRI. J Am Coll Cardiol. 2019;73(12):1371–82.PubMedCrossRef
30.
go back to reference Jorgensen L, Jenssen T, Joakimsen O, Heuch I, Ingebretsen OC, Jacobsen BK. Glycated hemoglobin level is strongly related to the prevalence of carotid artery plaques with high echogenicity in nondiabetic individuals: the Tromso study. Circulation. 2004;110(4):466–70.PubMedCrossRef Jorgensen L, Jenssen T, Joakimsen O, Heuch I, Ingebretsen OC, Jacobsen BK. Glycated hemoglobin level is strongly related to the prevalence of carotid artery plaques with high echogenicity in nondiabetic individuals: the Tromso study. Circulation. 2004;110(4):466–70.PubMedCrossRef
31.
go back to reference Hernandez M, Lopez C, Real J, Valls J, Ortega-Martinez de Victoria E, Vazquez F, et al. Preclinical carotid atherosclerosis in patients with latent autoimmune diabetes in adults (LADA), type 2 diabetes and classical type 1 diabetes. Cardiovasc Diabetol. 2017;16(1):94.PubMedPubMedCentralCrossRef Hernandez M, Lopez C, Real J, Valls J, Ortega-Martinez de Victoria E, Vazquez F, et al. Preclinical carotid atherosclerosis in patients with latent autoimmune diabetes in adults (LADA), type 2 diabetes and classical type 1 diabetes. Cardiovasc Diabetol. 2017;16(1):94.PubMedPubMedCentralCrossRef
32.
go back to reference Larsen JR, Brekke M, Bergengen L, Sandvik L, Arnesen H, Hanssen KF, et al. Mean HbA1c over 18 years predicts carotid intima media thickness in women with type 1 diabetes. Diabetologia. 2005;48(4):776–9.PubMedCrossRef Larsen JR, Brekke M, Bergengen L, Sandvik L, Arnesen H, Hanssen KF, et al. Mean HbA1c over 18 years predicts carotid intima media thickness in women with type 1 diabetes. Diabetologia. 2005;48(4):776–9.PubMedCrossRef
33.
go back to reference Nathan DM, Lachin J, Cleary P, Orchard T, Brillon DJ, Backlund JY, et al. Intensive diabetes therapy and carotid intima-media thickness in type 1 diabetes mellitus. N Engl J Med. 2003;348(23):2294–303.PubMedCrossRef Nathan DM, Lachin J, Cleary P, Orchard T, Brillon DJ, Backlund JY, et al. Intensive diabetes therapy and carotid intima-media thickness in type 1 diabetes mellitus. N Engl J Med. 2003;348(23):2294–303.PubMedCrossRef
34.
go back to reference Owens DR, Monnier L, Barnett AH. Future challenges and therapeutic opportunities in type 2 diabetes: changing the paradigm of current therapy. Diabetes Obes Metab. 2017;19(10):1339–52.PubMedPubMedCentralCrossRef Owens DR, Monnier L, Barnett AH. Future challenges and therapeutic opportunities in type 2 diabetes: changing the paradigm of current therapy. Diabetes Obes Metab. 2017;19(10):1339–52.PubMedPubMedCentralCrossRef
35.
36.
go back to reference Magodoro IM, Feng M, North CM, Vorechovska D, Kraemer JD, Kakuhikire B, et al. Female sex and cardiovascular disease risk in rural Uganda: a cross-sectional, population-based study. BMC Cardiovasc Disord. 2019;19(1):96.PubMedPubMedCentralCrossRef Magodoro IM, Feng M, North CM, Vorechovska D, Kraemer JD, Kakuhikire B, et al. Female sex and cardiovascular disease risk in rural Uganda: a cross-sectional, population-based study. BMC Cardiovasc Disord. 2019;19(1):96.PubMedPubMedCentralCrossRef
37.
go back to reference Ding EL, Song Y, Malik VS, Liu S. Sex differences of endogenous sex hormones and risk of type 2 diabetes: a systematic review and meta-analysis. JAMA. 2006;295(11):1288–99.PubMedCrossRef Ding EL, Song Y, Malik VS, Liu S. Sex differences of endogenous sex hormones and risk of type 2 diabetes: a systematic review and meta-analysis. JAMA. 2006;295(11):1288–99.PubMedCrossRef
38.
go back to reference Marzona I, Proietti M, Farcomeni A, Romiti GF, Romanazzi I, Raparelli V, et al. Sex differences in stroke and major adverse clinical events in patients with atrial fibrillation: a systematic review and meta-analysis of 993,600 patients. Int J Cardiol. 2018;269:182–91.PubMedCrossRef Marzona I, Proietti M, Farcomeni A, Romiti GF, Romanazzi I, Raparelli V, et al. Sex differences in stroke and major adverse clinical events in patients with atrial fibrillation: a systematic review and meta-analysis of 993,600 patients. Int J Cardiol. 2018;269:182–91.PubMedCrossRef
39.
go back to reference Rovella V, Anemona L, Cardellini M, Scimeca M, Saggini A, Santeusanio G, et al. The role of obesity in carotid plaque instability: interaction with age, gender, and cardiovascular risk factors. Cardiovasc Diabetol. 2018;17(1):46.PubMedPubMedCentralCrossRef Rovella V, Anemona L, Cardellini M, Scimeca M, Saggini A, Santeusanio G, et al. The role of obesity in carotid plaque instability: interaction with age, gender, and cardiovascular risk factors. Cardiovasc Diabetol. 2018;17(1):46.PubMedPubMedCentralCrossRef
40.
go back to reference Rannelli LA, MacRae JM, Mann MC, Ramesh S, Hemmelgarn BR, Rabi D, et al. Sex differences in associations between insulin resistance, heart rate variability, and arterial stiffness in healthy women and men: a physiology study. Can J Physiol Pharmacol. 2017;95(4):349–55.PubMedCrossRef Rannelli LA, MacRae JM, Mann MC, Ramesh S, Hemmelgarn BR, Rabi D, et al. Sex differences in associations between insulin resistance, heart rate variability, and arterial stiffness in healthy women and men: a physiology study. Can J Physiol Pharmacol. 2017;95(4):349–55.PubMedCrossRef
41.
go back to reference van Dijk AC, Donkel SJ, Zadi T, Sonneveld MAH, Schreuder F, Chohan MF, et al. Association between fibrinogen and fibrinogen gamma’ and atherosclerotic plaque morphology and composition in symptomatic carotid artery stenosis: Plaque-At-RISK study. Thromb Res. 2019;177:130–5.PubMedCrossRef van Dijk AC, Donkel SJ, Zadi T, Sonneveld MAH, Schreuder F, Chohan MF, et al. Association between fibrinogen and fibrinogen gamma’ and atherosclerotic plaque morphology and composition in symptomatic carotid artery stenosis: Plaque-At-RISK study. Thromb Res. 2019;177:130–5.PubMedCrossRef
42.
go back to reference Brzezinski RY, Etz-Hadar I, Grupper A, Ehrenwald M, Shapira I, Zeltser D, et al. Sex difference in the risk for exercise-induced albuminuria correlates with hemoglobin A1C and abnormal exercise ECG test findings. Cardiovasc Diabetol. 2017;16(1):79.PubMedPubMedCentralCrossRef Brzezinski RY, Etz-Hadar I, Grupper A, Ehrenwald M, Shapira I, Zeltser D, et al. Sex difference in the risk for exercise-induced albuminuria correlates with hemoglobin A1C and abnormal exercise ECG test findings. Cardiovasc Diabetol. 2017;16(1):79.PubMedPubMedCentralCrossRef
43.
go back to reference O’Neil A, Scovelle AJ, Milner AJ, Kavanagh A. Gender/sex as a social determinant of cardiovascular risk. Circulation. 2018;137(8):854–64.PubMedCrossRef O’Neil A, Scovelle AJ, Milner AJ, Kavanagh A. Gender/sex as a social determinant of cardiovascular risk. Circulation. 2018;137(8):854–64.PubMedCrossRef
44.
go back to reference Hussain MA, Saposnik G, Raju S, Salata K, Mamdani M, Tu JV, et al. Association between statin use and cardiovascular events after carotid artery revascularization. J Am Heart Assoc. 2018;7(16):e009745.PubMedPubMedCentralCrossRef Hussain MA, Saposnik G, Raju S, Salata K, Mamdani M, Tu JV, et al. Association between statin use and cardiovascular events after carotid artery revascularization. J Am Heart Assoc. 2018;7(16):e009745.PubMedPubMedCentralCrossRef
45.
go back to reference Katakami N, Mita T, Irie Y, Takahara M, Matsuoka TA, Gosho M, et al. Effect of sitagliptin on tissue characteristics of the carotid wall in patients with type 2 diabetes: a post hoc sub-analysis of the sitagliptin preventive study of intima-media thickness evaluation (SPIKE). Cardiovasc Diabetol. 2018;17(1):24.PubMedPubMedCentralCrossRef Katakami N, Mita T, Irie Y, Takahara M, Matsuoka TA, Gosho M, et al. Effect of sitagliptin on tissue characteristics of the carotid wall in patients with type 2 diabetes: a post hoc sub-analysis of the sitagliptin preventive study of intima-media thickness evaluation (SPIKE). Cardiovasc Diabetol. 2018;17(1):24.PubMedPubMedCentralCrossRef
46.
go back to reference Paraskevas KI, Mikhailidis DP, Veith FJ, Spence JD. Definition of best medical treatment in asymptomatic and symptomatic carotid artery stenosis. Angiology. 2016;67(5):411–9.PubMedCrossRef Paraskevas KI, Mikhailidis DP, Veith FJ, Spence JD. Definition of best medical treatment in asymptomatic and symptomatic carotid artery stenosis. Angiology. 2016;67(5):411–9.PubMedCrossRef
Metadata
Title
Prospective study of hemoglobin A1c and incident carotid artery plaque in Chinese adults without diabetes
Authors
Renying Xu
Ting Zhang
Yanping Wan
Zhuping Fan
Xiang Gao
Publication date
01-12-2019
Publisher
BioMed Central
Published in
Cardiovascular Diabetology / Issue 1/2019
Electronic ISSN: 1475-2840
DOI
https://doi.org/10.1186/s12933-019-0963-5

Other articles of this Issue 1/2019

Cardiovascular Diabetology 1/2019 Go to the issue