Skip to main content
Top
Published in: Cardiovascular Diabetology 1/2018

Open Access 01-12-2018 | Original investigation

Long-term visit-to-visit glycemic variability as predictor of micro- and macrovascular complications in patients with type 2 diabetes: The Rio de Janeiro Type 2 Diabetes Cohort Study

Authors: C. R. L. Cardoso, N. C. Leite, C. B. M. Moram, G. F. Salles

Published in: Cardiovascular Diabetology | Issue 1/2018

Login to get access

Abstract

Background

Long-term visit-to-visit glycemic variability is an additional measure of glycemic control. We aimed to evaluate the prognostic value of several measures of glycemic variability for the occurrence of micro- and macrovascular complications, and all-cause mortality in patients with type 2 diabetes.

Methods

654 individuals were followed-up over a median of 9.3 years. Glycemic variability (SDs and coefficients of variation of HbA1c and fasting glycaemia) was measured during the first 12- and 24-months. Multivariate Cox analysis, adjusted for risk factors and mean HbA1c and fasting glycaemia levels, examined the associations between glycemic variability and the occurrence of microvascular (retinopathy, microalbuminuria, renal function deterioration, peripheral neuropathy) and macrovascular complications [total cardiovascular events (CVE), major adverse CVEs (MACE) and cardiovascular mortality], and of all-cause mortality.

Results

During follow-up, 128 patients had a CVE (96 MACE), and 158 patients died (67 from cardiovascular diseases); 152 newly-developed or worsened diabetic retinopathy, 183 achieved the renal composite outcome (89 newly developed microalbuminuria and 91 deteriorated renal function), and 96 newly-developed or worsened peripheral neuropathy. Glycemic variability, particularly the 24-month parameters either estimated by HbA1c or by fasting glycemia, predicted all endpoints, except for retinopathy and peripheral neuropathy development/progression, and was a better predictor than mean HbA1c. Glycemic variability predicted retinopathy development/progression in patients with good glycemic control (HbA1c ≤ 7.5%, 58 mmol/mol) and predicted new-incident peripheral neuropathy.

Conclusions

Long-term visit-to-visit glycemic variability is an additional and frequently a better glycemic parameter than mean HbA1c levels for assessing the risk of future development of micro- and macrovascular complications in patients with type 2 diabetes.
Literature
1.
go back to reference Zimmet PZ, Magliano DJ, Herman WH, Shaw JE. Diabetes: a 21st century challenge. Lancet Diabetes Endocrinol. 2014;2:56–64.CrossRefPubMed Zimmet PZ, Magliano DJ, Herman WH, Shaw JE. Diabetes: a 21st century challenge. Lancet Diabetes Endocrinol. 2014;2:56–64.CrossRefPubMed
2.
go back to reference Ward A, Alvarez P, Vo L, Martin S. Direct medical costs of complications of diabetes in the United States: estimates for event-year and annual state costs (USD 2012). J Med Econ. 2014;17:176–83.CrossRefPubMed Ward A, Alvarez P, Vo L, Martin S. Direct medical costs of complications of diabetes in the United States: estimates for event-year and annual state costs (USD 2012). J Med Econ. 2014;17:176–83.CrossRefPubMed
3.
go back to reference American Diabetes Association. Standards of medical care in diabetes-2017. Diabetes Care. 2017;40(Suppl. 1):S48–56.CrossRef American Diabetes Association. Standards of medical care in diabetes-2017. Diabetes Care. 2017;40(Suppl. 1):S48–56.CrossRef
4.
go back to reference Zhang Y, Hu G, Yuan Z, Chen L. Glycosylated hemoglobin in relationship to cardiovascular outcomes and death in patients with type 2 diabetes: a systematic review and meta-analysis. PLoS ONE. 2012;7:e42551.CrossRefPubMedPubMedCentral Zhang Y, Hu G, Yuan Z, Chen L. Glycosylated hemoglobin in relationship to cardiovascular outcomes and death in patients with type 2 diabetes: a systematic review and meta-analysis. PLoS ONE. 2012;7:e42551.CrossRefPubMedPubMedCentral
5.
go back to reference Holman RR, Paul SK, Bethel MA, Matthews DR, Neil HA. 10-year follow-up of intensive glucose control in type 2 diabetes. N Engl J Med. 2008;359:1577–89.CrossRefPubMed Holman RR, Paul SK, Bethel MA, Matthews DR, Neil HA. 10-year follow-up of intensive glucose control in type 2 diabetes. N Engl J Med. 2008;359:1577–89.CrossRefPubMed
6.
go back to reference Hayward RA, Reaven PD, Wiitala WL, Bahn GD, Reda DJ, Ge L, VADT Investigators, et al. Follow-up of glycemic control and cardiovascular outcomes in type 2 diabetes. N Engl J Med. 2015;372:2197–206.CrossRefPubMed Hayward RA, Reaven PD, Wiitala WL, Bahn GD, Reda DJ, Ge L, VADT Investigators, et al. Follow-up of glycemic control and cardiovascular outcomes in type 2 diabetes. N Engl J Med. 2015;372:2197–206.CrossRefPubMed
7.
go back to reference Action to Control Cardiovascular Risk in Diabetes Study Group, Gerstein HC, Miller ME, Byington RP, Goff DC Jr, Bigger JT, Buse JB, et al. Effects of intensive glucose lowering in type 2 diabetes. N Engl J Med. 2008;358:2545–59.CrossRef Action to Control Cardiovascular Risk in Diabetes Study Group, Gerstein HC, Miller ME, Byington RP, Goff DC Jr, Bigger JT, Buse JB, et al. Effects of intensive glucose lowering in type 2 diabetes. N Engl J Med. 2008;358:2545–59.CrossRef
8.
go back to reference Zoungas S, Chalmers J, Neal B, Billot L, Li Q, Hirakawa Y, ADVANCE-ON Collaborative Group, et al. Follow-up of blood-pressure lowering and glucose control in type 2 diabetes. N Engl J Med. 2014;371:1392–406.CrossRefPubMed Zoungas S, Chalmers J, Neal B, Billot L, Li Q, Hirakawa Y, ADVANCE-ON Collaborative Group, et al. Follow-up of blood-pressure lowering and glucose control in type 2 diabetes. N Engl J Med. 2014;371:1392–406.CrossRefPubMed
9.
go back to reference The Diabetes Control and Complications Trial Research Group. The relationship of glycemic exposure (HbA1c) to the risk of development and progression of retinopathy in the diabetes control and complications trial. Diabetes. 1995;44:968–83.CrossRef The Diabetes Control and Complications Trial Research Group. The relationship of glycemic exposure (HbA1c) to the risk of development and progression of retinopathy in the diabetes control and complications trial. Diabetes. 1995;44:968–83.CrossRef
10.
go back to reference Kilpatrick ES, Rigby AS, Atkin SL. A1C variability and the risk of microvascular complications in type 1 diabetes: data from the Diabetes Control and Complications Trial. Diabetes Care. 2008;31:2198–202.CrossRefPubMedPubMedCentral Kilpatrick ES, Rigby AS, Atkin SL. A1C variability and the risk of microvascular complications in type 1 diabetes: data from the Diabetes Control and Complications Trial. Diabetes Care. 2008;31:2198–202.CrossRefPubMedPubMedCentral
11.
go back to reference Brownlee M, Hirsch IB. Glycemic variability: a hemoglobin A1c-independent risk factor for diabetic complications. JAMA. 2006;295:1707–8.CrossRefPubMed Brownlee M, Hirsch IB. Glycemic variability: a hemoglobin A1c-independent risk factor for diabetic complications. JAMA. 2006;295:1707–8.CrossRefPubMed
12.
go back to reference Gorst C, Kwok CS, Aslam S, Buchan I, Kontopantelis E, Myint PK, et al. Long-term glycemic variability and risk of adverse outcomes: a systematic review and meta-analysis. Diabetes Care. 2015;38:2354–69.CrossRefPubMed Gorst C, Kwok CS, Aslam S, Buchan I, Kontopantelis E, Myint PK, et al. Long-term glycemic variability and risk of adverse outcomes: a systematic review and meta-analysis. Diabetes Care. 2015;38:2354–69.CrossRefPubMed
13.
go back to reference Gimeno-Orna JA, Castro-Alonso FJ, Boned-Juliani B, Lou-Arnal LM. Fasting plasma glucose variability as a risk factor of retinopathy in type 2 diabetic patients. J Diabetes Complicat. 2003;17:78–81.CrossRefPubMed Gimeno-Orna JA, Castro-Alonso FJ, Boned-Juliani B, Lou-Arnal LM. Fasting plasma glucose variability as a risk factor of retinopathy in type 2 diabetic patients. J Diabetes Complicat. 2003;17:78–81.CrossRefPubMed
14.
go back to reference Zoppini G, Verlato G, Targher G, Casati S, Gusson E, Biasi V, et al. Is fasting glucose variability a risk factor for retinopathy in people with type 2 diabetes? Nutr Metab Cardiovasc Dis. 2009;19:334–9.CrossRefPubMed Zoppini G, Verlato G, Targher G, Casati S, Gusson E, Biasi V, et al. Is fasting glucose variability a risk factor for retinopathy in people with type 2 diabetes? Nutr Metab Cardiovasc Dis. 2009;19:334–9.CrossRefPubMed
15.
go back to reference Takao T, Ide T, Yanagisawa H, Kikuchi M, Kawazu S, Matsuyama Y. The effect of fasting plasma glucose variability on the risk of retinopathy in type 2 diabetic patients: retrospective long-term follow-up. Diabetes Res Clin Pract. 2010;89:296–302.CrossRefPubMed Takao T, Ide T, Yanagisawa H, Kikuchi M, Kawazu S, Matsuyama Y. The effect of fasting plasma glucose variability on the risk of retinopathy in type 2 diabetic patients: retrospective long-term follow-up. Diabetes Res Clin Pract. 2010;89:296–302.CrossRefPubMed
16.
go back to reference Penno G, Solini A, Bonora E, Fondelli C, Orsi E, Zerbini G, Renal Insufficiency And Cardiovascular Events Study Group, et al. HbA1c variability as an independent correlate of nephropathy, but not retinopathy, in patients with type 2 diabetes: the renal insufficiency and cardiovascular events (RIACE) Italian multicenter study. Diabetes Care. 2013;36:2301–10.CrossRefPubMedPubMedCentral Penno G, Solini A, Bonora E, Fondelli C, Orsi E, Zerbini G, Renal Insufficiency And Cardiovascular Events Study Group, et al. HbA1c variability as an independent correlate of nephropathy, but not retinopathy, in patients with type 2 diabetes: the renal insufficiency and cardiovascular events (RIACE) Italian multicenter study. Diabetes Care. 2013;36:2301–10.CrossRefPubMedPubMedCentral
17.
go back to reference Foo V, Quah J, Cheung G, Tan NC, Ma Zar KL, Chan CM, et al. HbA1c, systolic blood pressure variability and diabetic retinopathy in Asian type 2 diabetics. J Diabetes. 2017;9:200–7.CrossRefPubMed Foo V, Quah J, Cheung G, Tan NC, Ma Zar KL, Chan CM, et al. HbA1c, systolic blood pressure variability and diabetic retinopathy in Asian type 2 diabetics. J Diabetes. 2017;9:200–7.CrossRefPubMed
18.
go back to reference Takao T, Suka M, Yanagisawa H, Matsuyama Y, Iwamoto Y. Predictive ability of visit-to-visit variability in HbA1c and systolic blood pressure for the development of microalbuminuria and retinopathy in people with type 2 diabetes. Diabetes Res Clin Pract. 2017;128:15–23.CrossRefPubMed Takao T, Suka M, Yanagisawa H, Matsuyama Y, Iwamoto Y. Predictive ability of visit-to-visit variability in HbA1c and systolic blood pressure for the development of microalbuminuria and retinopathy in people with type 2 diabetes. Diabetes Res Clin Pract. 2017;128:15–23.CrossRefPubMed
19.
go back to reference Cummings DM, Larsen LC, Doherty L, Lea CS, Holbert D. Glycemic control patterns and kidney disease progression among primary care patients with diabetes mellitus. J Am Board Fam Med. 2011;24:391–8.CrossRefPubMed Cummings DM, Larsen LC, Doherty L, Lea CS, Holbert D. Glycemic control patterns and kidney disease progression among primary care patients with diabetes mellitus. J Am Board Fam Med. 2011;24:391–8.CrossRefPubMed
20.
go back to reference Hsu CC, Chang HY, Huang MC, Hwang SJ, Yang YC, Lee YS, et al. HbA1c variability is associated with microalbuminuria development in type 2 diabetes: a 7-year prospective cohort study. Diabetologia. 2012;55:3163–72.CrossRefPubMed Hsu CC, Chang HY, Huang MC, Hwang SJ, Yang YC, Lee YS, et al. HbA1c variability is associated with microalbuminuria development in type 2 diabetes: a 7-year prospective cohort study. Diabetologia. 2012;55:3163–72.CrossRefPubMed
21.
go back to reference Sugawara A, Kawai K, Motohashi S, Saito K, Kodama S, Yachi Y, et al. HbA(1c) variability and the development of microalbuminuria in type 2 diabetes: Tsukuba Kawai Diabetes Registry 2. Diabetologia. 2012;55:2128–31.CrossRefPubMed Sugawara A, Kawai K, Motohashi S, Saito K, Kodama S, Yachi Y, et al. HbA(1c) variability and the development of microalbuminuria in type 2 diabetes: Tsukuba Kawai Diabetes Registry 2. Diabetologia. 2012;55:2128–31.CrossRefPubMed
22.
go back to reference Rodríguez-Segade S, Rodríguez J, García López JM, Casanueva FF, Camiña F. Intrapersonal HbA(1c) variability and the risk of progression of nephropathy in patients with type 2 diabetes. Diabet Med. 2012;29:1562–6.CrossRefPubMed Rodríguez-Segade S, Rodríguez J, García López JM, Casanueva FF, Camiña F. Intrapersonal HbA(1c) variability and the risk of progression of nephropathy in patients with type 2 diabetes. Diabet Med. 2012;29:1562–6.CrossRefPubMed
23.
go back to reference Luk AO, Ma RC, Lau ES, Yang X, Lau WW, Yu LW, et al. Risk association of HbA1c variability with chronic kidney disease and cardiovascular disease in type 2 diabetes: prospective analysis of the Hong Kong Diabetes Registry. Diabetes Metab Res Rev. 2013;29:384–90.CrossRefPubMed Luk AO, Ma RC, Lau ES, Yang X, Lau WW, Yu LW, et al. Risk association of HbA1c variability with chronic kidney disease and cardiovascular disease in type 2 diabetes: prospective analysis of the Hong Kong Diabetes Registry. Diabetes Metab Res Rev. 2013;29:384–90.CrossRefPubMed
24.
go back to reference Lin CC, Chen CC, Chen FN, Li CI, Liu CS, Lin WY, et al. Risks of diabetic nephropathy with variation in hemoglobin A1c and fasting plasma glucose. Am J Med. 2013;126:1017.e1–10.CrossRefPubMed Lin CC, Chen CC, Chen FN, Li CI, Liu CS, Lin WY, et al. Risks of diabetic nephropathy with variation in hemoglobin A1c and fasting plasma glucose. Am J Med. 2013;126:1017.e1–10.CrossRefPubMed
25.
go back to reference Dorajoo SR, Ng JSL, Goh JHF, Lim SC, Yap CW, Chan A, et al. HbA1c variability in type 2 diabetes is associated with the occurrence of new-onset albuminuria within three years. Diabetes Res Clin Pract. 2017;128:32–9.CrossRefPubMed Dorajoo SR, Ng JSL, Goh JHF, Lim SC, Yap CW, Chan A, et al. HbA1c variability in type 2 diabetes is associated with the occurrence of new-onset albuminuria within three years. Diabetes Res Clin Pract. 2017;128:32–9.CrossRefPubMed
26.
go back to reference Low S, Lim SC, Yeoh LY, Liu YL, Liu JJ, Fun S, et al. Effect of long-term glycemic variability on estimated glomerular filtration rate decline among patients with type 2 diabetes mellitus: insights from the Diabetic Nephropathy Cohort in Singapore. J Diabetes. 2017;9:908–19.CrossRefPubMed Low S, Lim SC, Yeoh LY, Liu YL, Liu JJ, Fun S, et al. Effect of long-term glycemic variability on estimated glomerular filtration rate decline among patients with type 2 diabetes mellitus: insights from the Diabetic Nephropathy Cohort in Singapore. J Diabetes. 2017;9:908–19.CrossRefPubMed
27.
go back to reference Jun JE, Lee SE, Lee YB, Ahn JY, Kim G, Jin SM, et al. Glycated albumin and its variability as an indicator of cardiovascular autonomic neuropathy development in type 2 diabetic patients. Cardiovasc Diabetol. 2017;16:127.CrossRefPubMedPubMedCentral Jun JE, Lee SE, Lee YB, Ahn JY, Kim G, Jin SM, et al. Glycated albumin and its variability as an indicator of cardiovascular autonomic neuropathy development in type 2 diabetic patients. Cardiovasc Diabetol. 2017;16:127.CrossRefPubMedPubMedCentral
28.
go back to reference Bouchi R, Babazono T, Mugishima M, Yoshida N, Nyumura I, Toya K, et al. Fluctuations in HbA1c are associated with a higher incidence of cardiovascular disease in Japanese patients with type 2 diabetes. J Diabetes Investig. 2012;3:148–55.CrossRefPubMed Bouchi R, Babazono T, Mugishima M, Yoshida N, Nyumura I, Toya K, et al. Fluctuations in HbA1c are associated with a higher incidence of cardiovascular disease in Japanese patients with type 2 diabetes. J Diabetes Investig. 2012;3:148–55.CrossRefPubMed
29.
go back to reference Hirakawa Y, Arima H, Zoungas S, Ninomiya T, Cooper M, Hamet P, et al. Impact of visit-to-visit glycemic variability on the risks of macrovascular and microvascular events and all-cause mortality in type 2 diabetes: the ADVANCE trial. Diabetes Care. 2014;37:2359–65.CrossRefPubMed Hirakawa Y, Arima H, Zoungas S, Ninomiya T, Cooper M, Hamet P, et al. Impact of visit-to-visit glycemic variability on the risks of macrovascular and microvascular events and all-cause mortality in type 2 diabetes: the ADVANCE trial. Diabetes Care. 2014;37:2359–65.CrossRefPubMed
30.
go back to reference Takao T, Matsuyama Y, Suka M, Yanagisawa H, Iwamoto Y. The combined effect of visit-to-visit variability in HbA1c and systolic blood pressure on the incidence of cardiovascular events in patients with type 2 diabetes. BMJ Open Diabetes Res Care. 2015;3:e000129.CrossRefPubMedPubMedCentral Takao T, Matsuyama Y, Suka M, Yanagisawa H, Iwamoto Y. The combined effect of visit-to-visit variability in HbA1c and systolic blood pressure on the incidence of cardiovascular events in patients with type 2 diabetes. BMJ Open Diabetes Res Care. 2015;3:e000129.CrossRefPubMedPubMedCentral
31.
go back to reference Bonke FC, Donnachie E, Schneider A, Mehring M. Association of the average rate of change in HbA1c with severe adverse events: a longitudinal evaluation of audit data from the Bavarian Disease Management Program for patients with type 2 diabetes mellitus. Diabetologia. 2016;59:286–93.CrossRefPubMed Bonke FC, Donnachie E, Schneider A, Mehring M. Association of the average rate of change in HbA1c with severe adverse events: a longitudinal evaluation of audit data from the Bavarian Disease Management Program for patients with type 2 diabetes mellitus. Diabetologia. 2016;59:286–93.CrossRefPubMed
32.
go back to reference Prentice JC, Pizer SD, Conlin PR. Identifying the independent effect of HbA1c variability on adverse health outcomes in patients with type 2 diabetes. Diabet Med. 2016;33:1640–8.CrossRefPubMed Prentice JC, Pizer SD, Conlin PR. Identifying the independent effect of HbA1c variability on adverse health outcomes in patients with type 2 diabetes. Diabet Med. 2016;33:1640–8.CrossRefPubMed
33.
go back to reference Wan EY, Fung CS, Fong DY, Lam CL. Association of variability in hemoglobin A1c with cardiovascular diseases and mortality in Chinese patients with type 2 diabetes mellitus—a retrospective population-based cohort study. J Diabetes Complicat. 2016;30:1240–7.CrossRefPubMed Wan EY, Fung CS, Fong DY, Lam CL. Association of variability in hemoglobin A1c with cardiovascular diseases and mortality in Chinese patients with type 2 diabetes mellitus—a retrospective population-based cohort study. J Diabetes Complicat. 2016;30:1240–7.CrossRefPubMed
34.
go back to reference Laiteerapong N, Karter AJ, Moffet HH, Cooper JM, Gibbons RD, Liu JY, et al. Ten-year hemoglobin A1c trajectories and outcomes in type 2 diabetes mellitus: the Diabetes & Aging Study. J Diabetes Complicat. 2017;31:94–100.CrossRefPubMed Laiteerapong N, Karter AJ, Moffet HH, Cooper JM, Gibbons RD, Liu JY, et al. Ten-year hemoglobin A1c trajectories and outcomes in type 2 diabetes mellitus: the Diabetes & Aging Study. J Diabetes Complicat. 2017;31:94–100.CrossRefPubMed
35.
go back to reference Lee MY, Hsiao PJ, Huang YT, Huang JC, Hsu WH, Chen SC, et al. Greater HbA1c variability is associated with increased cardiovascular events in type 2 diabetes patients with preserved renal function, but not in moderate to advanced chronic kidney disease. PLoS ONE. 2017;12:e0178319.CrossRefPubMedPubMedCentral Lee MY, Hsiao PJ, Huang YT, Huang JC, Hsu WH, Chen SC, et al. Greater HbA1c variability is associated with increased cardiovascular events in type 2 diabetes patients with preserved renal function, but not in moderate to advanced chronic kidney disease. PLoS ONE. 2017;12:e0178319.CrossRefPubMedPubMedCentral
36.
go back to reference Zinman B, Marso SP, Poulter NR, Emerson SS, Pieber TR, Pratley RE, DEVOTE Study Group, et al. Day-to-day fasting glycaemic variability in DEVOTE: associations with severe hypoglycaemia and cardiovascular outcomes (DEVOTE 2). Diabetologia. 2018;61:48–57.CrossRefPubMed Zinman B, Marso SP, Poulter NR, Emerson SS, Pieber TR, Pratley RE, DEVOTE Study Group, et al. Day-to-day fasting glycaemic variability in DEVOTE: associations with severe hypoglycaemia and cardiovascular outcomes (DEVOTE 2). Diabetologia. 2018;61:48–57.CrossRefPubMed
37.
go back to reference Muggeo M, Zoppini G, Bonora E, Brun E, Bonadonna RC, Moghetti P, et al. Fasting plasma glucose variability predicts 10-year survival of type 2 diabetic patients: the Verona Diabetes Study. Diabetes Care. 2000;23:45–50.CrossRefPubMed Muggeo M, Zoppini G, Bonora E, Brun E, Bonadonna RC, Moghetti P, et al. Fasting plasma glucose variability predicts 10-year survival of type 2 diabetic patients: the Verona Diabetes Study. Diabetes Care. 2000;23:45–50.CrossRefPubMed
38.
go back to reference Lin CC, Li CI, Yang SY, Liu CS, Chen CC, Fuh MM, et al. Variation of fasting plasma glucose: a predictor of mortality in patients with type 2 diabetes. Am J Med. 2012;125:416.e9–18.PubMed Lin CC, Li CI, Yang SY, Liu CS, Chen CC, Fuh MM, et al. Variation of fasting plasma glucose: a predictor of mortality in patients with type 2 diabetes. Am J Med. 2012;125:416.e9–18.PubMed
39.
go back to reference Ma WY, Li HY, Pei D, Hsia TL, Lu KC, Tsai LY, et al. Variability in hemoglobin A1c predicts all-cause mortality in patients with type 2 diabetes. J Diabetes Complicat. 2012;26:296–300.CrossRefPubMed Ma WY, Li HY, Pei D, Hsia TL, Lu KC, Tsai LY, et al. Variability in hemoglobin A1c predicts all-cause mortality in patients with type 2 diabetes. J Diabetes Complicat. 2012;26:296–300.CrossRefPubMed
40.
go back to reference Takao T, Matsuyama Y, Yanagisawa H, Kikuchi M, Kawazu S. Association between HbA1c variability and mortality in patients with type 2 diabetes. J Diabetes Complicat. 2014;28:494–9.CrossRefPubMed Takao T, Matsuyama Y, Yanagisawa H, Kikuchi M, Kawazu S. Association between HbA1c variability and mortality in patients with type 2 diabetes. J Diabetes Complicat. 2014;28:494–9.CrossRefPubMed
41.
go back to reference Skriver MV, Sandbæk A, Kristensen JK, Støvring H. Relationship of HbA1c variability, absolute changes in HbA1c, and all-cause mortality in type 2 diabetes: a Danish population-based prospective observational study. BMJ Open Diabetes Res Care. 2015;3:e000060.CrossRefPubMedPubMedCentral Skriver MV, Sandbæk A, Kristensen JK, Støvring H. Relationship of HbA1c variability, absolute changes in HbA1c, and all-cause mortality in type 2 diabetes: a Danish population-based prospective observational study. BMJ Open Diabetes Res Care. 2015;3:e000060.CrossRefPubMedPubMedCentral
42.
go back to reference Hirsch IB. Glycemic variability and diabetes complications: does it matter? Of course it does! Diabetes Care. 2015;38:1610–4.CrossRefPubMed Hirsch IB. Glycemic variability and diabetes complications: does it matter? Of course it does! Diabetes Care. 2015;38:1610–4.CrossRefPubMed
43.
go back to reference Bergenstal RM. Glycemic variability and diabetes complications: does it matter? Simply put, there are better glycemic markers! Diabetes Care. 2015;38:1615–21.CrossRefPubMed Bergenstal RM. Glycemic variability and diabetes complications: does it matter? Simply put, there are better glycemic markers! Diabetes Care. 2015;38:1615–21.CrossRefPubMed
44.
go back to reference Cardoso CR, Leite NC, Ferreira MT, Salles GF. Prognostic importance of baseline and serial glycated hemoglobin levels in high-risk patients with type 2 diabetes: The Rio de Janeiro Type 2 Diabetes Cohort Study. Acta Diabetol. 2015;52:21–9.CrossRefPubMed Cardoso CR, Leite NC, Ferreira MT, Salles GF. Prognostic importance of baseline and serial glycated hemoglobin levels in high-risk patients with type 2 diabetes: The Rio de Janeiro Type 2 Diabetes Cohort Study. Acta Diabetol. 2015;52:21–9.CrossRefPubMed
45.
go back to reference Cardoso CR, Moran CB, Marinho FS, Ferreira MT, Salles GF. Increased aortic stiffness predicts future development and progression of peripheral neuropathy in patients with type 2 diabetes: The Rio de Janeiro Type 2 Diabetes Cohort Study. Diabetologia. 2015;58:2161–8.CrossRefPubMed Cardoso CR, Moran CB, Marinho FS, Ferreira MT, Salles GF. Increased aortic stiffness predicts future development and progression of peripheral neuropathy in patients with type 2 diabetes: The Rio de Janeiro Type 2 Diabetes Cohort Study. Diabetologia. 2015;58:2161–8.CrossRefPubMed
46.
go back to reference Cardoso CRL, Leite NC, Dib E, Salles GF. Predictors of development and progression of retinopathy in patients with type 2 diabetes: importance of blood pressure parameters. Sci Rep. 2017;7:4867.CrossRefPubMedPubMedCentral Cardoso CRL, Leite NC, Dib E, Salles GF. Predictors of development and progression of retinopathy in patients with type 2 diabetes: importance of blood pressure parameters. Sci Rep. 2017;7:4867.CrossRefPubMedPubMedCentral
47.
go back to reference Cardoso CRL, Leite NC, Salles GC, Ferreira MT, Salles GF. Aortic stiffness and ambulatory blood pressure as predictors of diabetic kidney disease: a competing risks analysis from The Rio de Janeiro Type 2 Diabetes Cohort Study. Diabetologia. 2018;61:455–65.CrossRefPubMed Cardoso CRL, Leite NC, Salles GC, Ferreira MT, Salles GF. Aortic stiffness and ambulatory blood pressure as predictors of diabetic kidney disease: a competing risks analysis from The Rio de Janeiro Type 2 Diabetes Cohort Study. Diabetologia. 2018;61:455–65.CrossRefPubMed
48.
go back to reference Niskanen L, Virkamäki A, Hansen JB, Saukkonen T. Fasting plasma glucose variability as a marker of nocturnal hypoglycemia in diabetes: evidence from the PREDICTIVE study. Diabetes Res Clin Pract. 2009;86:e15–8.CrossRefPubMed Niskanen L, Virkamäki A, Hansen JB, Saukkonen T. Fasting plasma glucose variability as a marker of nocturnal hypoglycemia in diabetes: evidence from the PREDICTIVE study. Diabetes Res Clin Pract. 2009;86:e15–8.CrossRefPubMed
49.
go back to reference Pieber TR, Marso SP, McGuire DK, Zinman B, Poulter NR, Emerson SS, DEVOTE Study Group, et al. DEVOTE 3: temporal relationships between severe hypoglycaemia, cardiovascular outcomes and mortality. Diabetologia. 2018;61:58–65.CrossRefPubMed Pieber TR, Marso SP, McGuire DK, Zinman B, Poulter NR, Emerson SS, DEVOTE Study Group, et al. DEVOTE 3: temporal relationships between severe hypoglycaemia, cardiovascular outcomes and mortality. Diabetologia. 2018;61:58–65.CrossRefPubMed
50.
go back to reference Rutter MK. Devoting attention to glucose variability and hypoglycaemia in type 2 diabetes. Diabetologia. 2018;61:43–7.CrossRefPubMed Rutter MK. Devoting attention to glucose variability and hypoglycaemia in type 2 diabetes. Diabetologia. 2018;61:43–7.CrossRefPubMed
51.
go back to reference Ouchi S, Shimada K, Miyazaki T, Takahashi S, Sugita Y, Shimizu M, et al. Low 1,5-anhydroglucitol levels are associated with long-term cardiac mortality in acute coronary syndrome patients with hemoglobin A1c levels less than 7.0. Cardiovasc Diabetol. 2017;16:151.CrossRefPubMedPubMedCentral Ouchi S, Shimada K, Miyazaki T, Takahashi S, Sugita Y, Shimizu M, et al. Low 1,5-anhydroglucitol levels are associated with long-term cardiac mortality in acute coronary syndrome patients with hemoglobin A1c levels less than 7.0. Cardiovasc Diabetol. 2017;16:151.CrossRefPubMedPubMedCentral
52.
go back to reference Takahashi S, Shimada K, Miyauchi K, Miyazaki T, Sai E, Ogita M, et al. Low and exacerbated levels of 1,5-anhydroglucitol are associated with cardiovascular events in patients after first-time elective percutaneous coronary intervention. Cardiovasc Diabetol. 2016;15:145.CrossRefPubMedPubMedCentral Takahashi S, Shimada K, Miyauchi K, Miyazaki T, Sai E, Ogita M, et al. Low and exacerbated levels of 1,5-anhydroglucitol are associated with cardiovascular events in patients after first-time elective percutaneous coronary intervention. Cardiovasc Diabetol. 2016;15:145.CrossRefPubMedPubMedCentral
53.
go back to reference Monnier L, Mas E, Ginet C, Michel F, Villon L, Cristol JP, et al. Activation of oxidative stress by acute glucose fluctuations compared with sustained chronic hyperglycemia in patients with type 2 diabetes. JAMA. 2006;295:1681–7.CrossRefPubMed Monnier L, Mas E, Ginet C, Michel F, Villon L, Cristol JP, et al. Activation of oxidative stress by acute glucose fluctuations compared with sustained chronic hyperglycemia in patients with type 2 diabetes. JAMA. 2006;295:1681–7.CrossRefPubMed
54.
go back to reference Ceriello A, Esposito K, Piconi L, Ihnat MA, Thorpe JE, Testa R, et al. Oscillating glucose is more deleterious to endothelial function and oxidative stress than mean glucose in normal and type 2 diabetic patients. Diabetes. 2008;57:1349–54.CrossRefPubMed Ceriello A, Esposito K, Piconi L, Ihnat MA, Thorpe JE, Testa R, et al. Oscillating glucose is more deleterious to endothelial function and oxidative stress than mean glucose in normal and type 2 diabetic patients. Diabetes. 2008;57:1349–54.CrossRefPubMed
55.
go back to reference Kuroda M, Shinke T, Otake H, Sugiyama D, Takaya T, Takahashi H, et al. Effects of daily glucose fluctuations on the healing response to everolimus-eluting stent implantation as assessed using continuous glucose monitoring and optical coherence tomography. Cardiovasc Diabetol. 2016;15:79.CrossRefPubMedPubMedCentral Kuroda M, Shinke T, Otake H, Sugiyama D, Takaya T, Takahashi H, et al. Effects of daily glucose fluctuations on the healing response to everolimus-eluting stent implantation as assessed using continuous glucose monitoring and optical coherence tomography. Cardiovasc Diabetol. 2016;15:79.CrossRefPubMedPubMedCentral
56.
go back to reference Zhang JW, He LJ, Cao SJ, Yang Q, Yang SW, Zhou YJ. Effect of glycemic variability on short term prognosis in acute myocardial infarction subjects undergoing primary percutaneous coronary interventions. Diabetol Metab Syndr. 2014;6:76.CrossRefPubMedPubMedCentral Zhang JW, He LJ, Cao SJ, Yang Q, Yang SW, Zhou YJ. Effect of glycemic variability on short term prognosis in acute myocardial infarction subjects undergoing primary percutaneous coronary interventions. Diabetol Metab Syndr. 2014;6:76.CrossRefPubMedPubMedCentral
57.
go back to reference Xia J, Xu J, Hu S, Hao H, Yin C, Xu D. Impact of glycemic variability on the occurrence of periprocedural myocardial infarction and major adverse cardiovascular events (MACE) after coronary intervention in patients with stable angina pectoris at 6 months follow-up. Clin Chim Acta. 2017;471:196–200.CrossRefPubMed Xia J, Xu J, Hu S, Hao H, Yin C, Xu D. Impact of glycemic variability on the occurrence of periprocedural myocardial infarction and major adverse cardiovascular events (MACE) after coronary intervention in patients with stable angina pectoris at 6 months follow-up. Clin Chim Acta. 2017;471:196–200.CrossRefPubMed
58.
go back to reference Schisano B, Tripathi G, McGee K, McTernan PG, Ceriello A. Glucose oscillations, more than constant high glucose, induce p53 activation and a metabolic memory in human endothelial cells. Diabetologia. 2011;54:1219–26.CrossRefPubMed Schisano B, Tripathi G, McGee K, McTernan PG, Ceriello A. Glucose oscillations, more than constant high glucose, induce p53 activation and a metabolic memory in human endothelial cells. Diabetologia. 2011;54:1219–26.CrossRefPubMed
59.
go back to reference Keating ST, El-Osta A. Glycemic memories and the epigenetic component of diabetic nephropathy. Curr Diab Rep. 2013;13:574–81.CrossRefPubMed Keating ST, El-Osta A. Glycemic memories and the epigenetic component of diabetic nephropathy. Curr Diab Rep. 2013;13:574–81.CrossRefPubMed
60.
go back to reference Groop PH, Forsblom C, Thomas MC. Mechanisms of disease: pathway-selective insulin resistance and microvascular complications of diabetes. Nat Clin Pract Endocrinol Metab. 2005;1:100–10.CrossRefPubMed Groop PH, Forsblom C, Thomas MC. Mechanisms of disease: pathway-selective insulin resistance and microvascular complications of diabetes. Nat Clin Pract Endocrinol Metab. 2005;1:100–10.CrossRefPubMed
61.
go back to reference Del Guerra S, Grupillo M, Masini M, Lupi R, Bugliani M, Torri S, et al. Gliclazide protects human islet beta-cells from apoptosis induced by intermittent high glucose. Diabetes Metab Res Rev. 2007;23:234–8.CrossRefPubMed Del Guerra S, Grupillo M, Masini M, Lupi R, Bugliani M, Torri S, et al. Gliclazide protects human islet beta-cells from apoptosis induced by intermittent high glucose. Diabetes Metab Res Rev. 2007;23:234–8.CrossRefPubMed
62.
go back to reference FLAT-SUGAR Trial Investigators. Glucose variability in a 26-week randomized comparison of mealtime treatment with rapid-acting insulin versus GLP-1 agonist in participants with type 2 diabetes at high cardiovascular risk. Diabetes Care. 2016;39:973–81.CrossRef FLAT-SUGAR Trial Investigators. Glucose variability in a 26-week randomized comparison of mealtime treatment with rapid-acting insulin versus GLP-1 agonist in participants with type 2 diabetes at high cardiovascular risk. Diabetes Care. 2016;39:973–81.CrossRef
63.
go back to reference Siegelaar SE, Kerr L, Jacober SJ, Devries JH. A decrease in glucose variability does not reduce cardiovascular event rates in type 2 diabetic patients after acute myocardial infarction: a reanalysis of the HEART2D study. Diabetes Care. 2011;34:855–7.CrossRefPubMedPubMedCentral Siegelaar SE, Kerr L, Jacober SJ, Devries JH. A decrease in glucose variability does not reduce cardiovascular event rates in type 2 diabetic patients after acute myocardial infarction: a reanalysis of the HEART2D study. Diabetes Care. 2011;34:855–7.CrossRefPubMedPubMedCentral
Metadata
Title
Long-term visit-to-visit glycemic variability as predictor of micro- and macrovascular complications in patients with type 2 diabetes: The Rio de Janeiro Type 2 Diabetes Cohort Study
Authors
C. R. L. Cardoso
N. C. Leite
C. B. M. Moram
G. F. Salles
Publication date
01-12-2018
Publisher
BioMed Central
Published in
Cardiovascular Diabetology / Issue 1/2018
Electronic ISSN: 1475-2840
DOI
https://doi.org/10.1186/s12933-018-0677-0

Other articles of this Issue 1/2018

Cardiovascular Diabetology 1/2018 Go to the issue