Metrics beyond hemoglobin A1C in diabetes management: Time in range, hypoglycemia, and other parameters

Diabetes Technology and Therapeutics

Volumn 19, Issue S2, 2017, Pages S16-S26

  Wright, Lorena Alarcon Casas ^a   Hirsch, Irl B ^a  

^a UNIVERSITY OF WASHINGTON MEDICAL CENTER   (United States)

Author keywords

Continuous glucose monitoring; Flash continuous glucose monitoring; Glucose metrics; Glycemic biomarkers

Indexed keywords

1,5 ANHYDROSORBITOL; BIOLOGICAL MARKER; GLUCOSE; GLYCOSYLATED PROTEIN; HEMOGLOBIN A1C; GLYCOSYLATED HEMOGLOBIN; HEMOGLOBIN A1C PROTEIN, HUMAN;

BLOOD GLUCOSE MONITORING; CALIBRATION; DIABETES MELLITUS; GLUCOSE BLOOD LEVEL; GLUCOSE SENSOR; HUMAN; HYPERGLYCEMIA; HYPOGLYCEMIA; MANAGED CARE; PARAMETERS; PRIORITY JOURNAL; REVIEW; TREATMENT OUTCOME; BLOOD; DIABETIC COMPLICATION; DISEASE MANAGEMENT; PROCEDURES; TIME FACTOR;

BLOOD GLUCOSE SELF-MONITORING; DIABETES COMPLICATIONS; DIABETES MELLITUS; DISEASE MANAGEMENT; GLYCATED HEMOGLOBIN A; HUMANS; HYPOGLYCEMIA; TIME FACTORS;

EID: 85019721838     PISSN: 15209156     EISSN: 15578593     Source Type: Journal    
DOI: 10.1089/dia.2017.0029     Document Type: Review

References (108)

1. The effect of intensive treatment of diabetes on the development and progression of long-term complications in insulin-dependent diabetes mellitus. The Diabetes Control and Complications Trial Research Group. N Engl J Med 1993;329:977-986.
2. Intensive blood-glucose control with sulphonylureas or insulin compared with conventional treatment and risk of complications in patients with type 2 diabetes (UKPDS 33). UK Prospective Diabetes Study (UKPDS) Group. Lancet 1998;352:837-853.
3. Effect of intensive blood-glucose control with metformin on complications in overweight patients with type 2 diabetes (UKPDS 34). UK Prospective Diabetes Study (UKPDS) Group. Lancet 1998;352:854-865.
4. Standards of Medical Care in Diabetes-2017: Summary of revisions. Diabetes Care 2017;40(Suppl 1):S4-S5.
5. Sacks DB: Hemoglobin A1c in diabetes: panacea or pointless? Diabetes 2013;62:41-43.
6. Herman WH, Ma Y, Uwaifo G, et al.: Differences in A1C by race and ethnicity among patients with impaired glucose tolerance in the Diabetes Prevention Program. Diabetes Care 2007;30:2453-2457.
7. Saydah S, Cowie C, Eberhardt MS, et al.: Race and ethnic differences in glycemic control among adults with diagnosed diabetes in the United States. Ethn Dis 2007;17: 529-535.
8. Herman WH, Dungan KM, Wolffenbuttel BH, et al.: Racial and ethnic differences in mean plasma glucose, hemoglobin A1c, and 1,5-anhydroglucitol in over 2000 patients with type 2 diabetes. J Clin Endocrinol Metab 2009;94:1689-1694.
9. Yudkin JS, Forrest RD, Jackson CA, et al.: Unexplained variability of glycated haemoglobin in non-diabetic subjects not related to glycaemia. Diabetologia 1990;33:208-215.
10. Khera PK, Joiner CH, Carruthers A, et al.: Evidence for interindividual heterogeneity in the glucose gradient across the human red blood cell membrane and its relationship to hemoglobin glycation. Diabetes 2008;57:2445-2452.
11. Selvin E, Francis LM, Ballantyne CM, et al.: Nontraditional markers of glycemia: associations with microvascular conditions. Diabetes Care 2011;34:960-967.
12. Armbruster DA: Fructosamine: structure, analysis, and clinical usefulness. Clin Chem 1987;33:2153-2163.
13. Selvin E, Rawlings AM, Grams M, et al.: Fructosamine and glycated albumin for risk stratification and prediction of incident diabetes and microvascular complications: a prospective cohort analysis of the Atherosclerosis Risk in Communities (ARIC) study. Lancet Diabetes Endocrinol 2014;2:279-288.
14. Mukai N, Yasuda M, Ninomiya T, et al.: Thresholds of various glycemic measures for diagnosing diabetes based on prevalence of retinopathy in community-dwelling Japanese subjects: the Hisayama Study. Cardiovasc Diabetol 2014;13:45.
15. Kondaveeti SB, Kumaraswamy D, Mishra S, Kumar A, Shaker IA: Evaluation of glycated albumin and microalbuminuria as early risk markers of nephropathy in type 2 diabetes mellitus. J Clin Diagn Res 2013;7:1280-1283.
16. Furusyo N, Koga T, Ai M, et al.: Plasma glycated albumin level and atherosclerosis: results from the Kyushu and Okinawa Population Study (KOPS). Int J Cardiol 2013; 167:2066-2072.
17. Lu L, Pu LJ, Xu XW, et al.: Association of serum levels of glycated albumin, C-reactive protein and tumor necrosis factor-alpha with the severity of coronary artery disease and renal impairment in patients with type 2 diabetes mellitus. Clin Biochem 2007;40:810-816.
18. Jin C, Lu L, Zhang RY, et al.: Association of serum glycated albumin, C-reactive protein and ICAM-1 levels with diffuse coronary artery disease in patients with type 2 diabetes mellitus. Clin Chim Acta 2009;408:45-49.
19. Lu L, Pu LJ, Zhang Q, et al.: Increased glycated albumin and decreased esRAGE levels are related to angiographic severity and extent of coronary artery disease in patients with type 2 diabetes. Atherosclerosis 2009;206: 540-545.
20. Song SO, Kim KJ, Lee BW, et al.: Serum glycated albumin predicts the progression of carotid arterial atherosclerosis. Atherosclerosis 2012;225:450-455.
21. Shen Y, Pu LJ, Lu L, et al.: Glycated albumin is superior to hemoglobin A1c for evaluating the presence and severity of coronary artery disease in type 2 diabetic patients. Cardiology 2012;123:84-90.
22. Selvin E, Rawlings AM, Lutsey PL, et al.: Fructosamine and glycated albumin and the risk of cardiovascular outcomes and death. Circulation 2015;132:269-277.
23. Nathan DM, McGee P, Steffes MW, Lachin JM: Relationship of glycated albumin to blood glucose and HbA1c values and to retinopathy, nephropathy, and cardiovascular outcomes in the DCCT/EDIC study. Diabetes 2014;63:282-290.
24. Cohen RM, LeCaire TJ, Lindsell CJ, et al.: Relationship of prospective GHb to glycated serum proteins in incident diabetic retinopathy: implications of the glycation gap for mechanism of risk prediction. Diabetes Care 2008;31: 151-153.
25. Inaba M, Okuno S, Kumeda Y, et al.: Glycated albumin is a better glycemic indicator than glycated hemoglobin values in hemodialysis patients with diabetes: effect of anemia and erythropoietin injection. J Am Soc Nephrol 2007;18:896-903.
26. Vos FE, Schollum JB, Coulter CV, et al.: Assessment of markers of glycaemic control in diabetic patients with chronic kidney disease using continuous glucose monitoring. Nephrology (Carlton) 2012;17:182-188.
27. Freedman BI, Shihabi ZK, Andries L, et al.: Relationship between assays of glycemia in diabetic subjects with advanced chronic kidney disease. Am J Nephrol 2010;31: 375-379.
28. Shafi T, Sozio SM, Plantinga LC, et al.: Serum fructosamine and glycated albumin and risk of mortality and clinical outcomes in hemodialysis patients. Diabetes Care 2013;36:1522-1533.
29. Hashimoto K, Noguchi S, Morimoto Y, et al.: A1C but not serum glycated albumin is elevated in late pregnancy owing to iron deficiency. Diabetes Care 2008;31:1945-1948.
30. Trenti T, Cristani A, Cioni G, et al.: Fructosamine and glycated hemoglobin as indices of glycemic control in patients with liver cirrhosis. Ric Clin Lab 1990;20:261-267.
31. Constanti C, Simo JM, Joven J, Camps J: Serum fructosamine concentration in patients with nephrotic syndrome and with cirrhosis of the liver: the influence of hypoalbuminaemia and hypergammaglobulinaemia. Ann Clin Biochem 1992;29 (Pt 4):437-442.
32. Triger DR, Wright R: Hyperglobulinaemia in liver disease. Lancet 1973;1:1494-1496.
33. Koga M, Saito H, Mukai M, et al.: Serum glycated albumin levels are influenced by smoking status, independent of plasma glucose levels. Acta Diabetol 2009;46: 141-144.
34. Koga M, Murai J, Saito H, et al.: Serum glycated albumin, but not glycated haemoglobin, is low in relation to glycemia in hyperuricemic men. Acta Diabetol 2010;47: 173-177.
35. Koga M, Murai J, Saito H, et al.: Serum glycated albumin, but not glycated hemoglobin, is low in relation to glycemia in men with hypertriglyceridemia. J Diabetes Investig 2010;1:202-207.
36. Koga M, Murai J, Saito H, et al.: Serum glycated albumin levels, but not glycated hemoglobin, is low in relation to glycemia in non-diabetic men with nonalcoholic fatty liver disease with high alanine aminotransferase levels. Clin Biochem 2010;43:1023-1025.
37. Koga M, Otsuki M, Matsumoto S, et al.: Negative association of obesity and its related chronic inflammation with serum glycated albumin but not glycated hemoglobin levels. Clin Chim Acta 2007;378:48-52.
38. Kohzuma T, Yamamoto T, Uematsu Y, et al.: Basic performance of an enzymatic method for glycated albumin and reference range determination. J Diabetes Sci Technol 2011;5:1455-1462.
39. Kohzuma T, Koga M: Lucica GA-L glycated albumin assay kit: a new diagnostic test for diabetes mellitus. Mol Diagn Ther 2010;14:49-51.
40. Juraschek SP, Steffes MW, Selvin E: Associations of alternative markers of glycemia with hemoglobin A(1c) and fasting glucose. Clin Chem 2012;58:1648-1655.
41. Jung CH, Hwang YC, Kim KJ, et al.: Development of an HbA1c-based conversion equation for estimating glycated albumin in a Korean population with a wide range of glucose intolerance. PLoS One 2014;9:e95729.
42. Inoue K, Tsujimoto T, Yamamoto-Honda R, et al.: A newer conversion equation for the correlation between HbA1c and glycated albumin. Endocr J 2014;61:553-560.
43. Tahara Y: Analysis of the method for conversion between levels of HbA1c and glycated albumin by linear regression analysis using a measurement error model. Diabetes Res Clin Pract 2009;84:224-229.
44. Van Dieijen-Visser MP, Seynaeve C, Brombacher PJ: Influence of variations in albumin or total-protein concentration on serum fructosamine concentration. Clin Chem 1986;32:1610.
45. Howey JE, Browning MC, Fraser CG: Assay of serum fructosamine that minimizes standardization and matrix problems: use to assess components of biological variation. Clin Chem 1987;33(2 Pt 1):269-272.
46. Kuenen JC, Borg R, Kuik DJ, et al.: Does glucose variability influence the relationship between mean plasma glucose and HbA1c levels in type 1 and type 2 diabetic patients? Diabetes Care 2011;34:1843-1847.
47. Rodriguez-Segade S, Rodriguez J, Cabezas-Agricola JM, et al.: Progression of nephropathy in type 2 diabetes: the glycation gap is a significant predictor after adjustment for glycohemoglobin (Hb A1c). Clin Chem 2011;57:264-271.
48. Cohen RM, Holmes YR, Chenier TC, Joiner CH: Discordance between HbA1c and fructosamine: evidence for a glycosylation gap and its relation to diabetic nephropathy. Diabetes Care 2003;26:163-167.
49. Buse JB, Freeman JL, Edelman SV, et al.: Serum 1,5-anhydroglucitol (GlycoMark): a short-term glycemic marker. Diabetes Technol Ther 2003;5:355-363.
50. Kim WJ, Park CY, Park SE, et al.: Serum 1,5-anhydroglucitol is associated with diabetic retinopathy in Type 2 diabetes. Diabet Med 2012;29:1184-1190.
51. Selvin E, Rawlings AM, Grams M, et al.: Association of 1,5-anhydroglucitol with diabetes and microvascular conditions. Clin Chem 2014;60:1409-1418.
52. Takahashi S, Shimada K, Miyauchi K, 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.
53. Selvin E, Rawlings A, Lutsey P, et al.: Association of 1,5-anhydroglucitol with cardiovascular disease and mortality. Diabetes 2016;65:201-208.
54. Fujiwara T, Yoshida M, Yamada H, et al.: Lower 1,5-anhydroglucitol is associated with denovo coronary artery disease in patients at high cardiovascular risk. Heart Vessels 2015;30:469-476.
55. Tetsuo M, Hamada T, Yoshimatsu K, et al.: Serum levels of 1,5-anhydro-D-glucitol during the normal and diabetic pregnancy and puerperium. Acta Obstet Gynecol Scand 1990;69:479-485.
56. Nowak N, Skupien J, Cyganek K, et al.: 1,5-Anhydroglucitol as a marker of maternal glycaemic control and predictor of neonatal birthweight in pregnancies complicated by type 1 diabetes mellitus. Diabetologia 2013; 56:709-713.
57. Wright LA, Hirsch IB, Gooley TA, Brown Z: 1,5-anhydroglucitol and neonatal complications in pregnancy complicated by diabetes. Endocr Pract 2015;21:725-733.
58. Delaney SS, Coley RY, Brown Z: 1,5-Anhydroglucitol: a new predictor of neonatal birth weight in diabetic pregnancies. Eur J Obstet Gynecol Reprod Biol 2015;189:55-58.
59. Balis DA, Tong C, Meininger G: Effect of canagliflozin, a sodium-glucose cotransporter 2 inhibitor, on measurement of serum 1,5-anhydroglucitol. J Diabetes 2014;6:378-380.
60. Pal A, Farmer AJ, Dudley C, et al.: Evaluation of serum 1,5 anhydroglucitol levels as a clinical test to differentiate subtypes of diabetes. Diabetes Care 2010;33:252-257.
61. Miller KM, Beck RW, Bergenstal RM, et al.: Evidence of a strong association between frequency of self-monitoring of blood glucose and hemoglobin A1c levels in T1D exchange clinic registry participants. Diabetes Care 2013;36: 2009-2014.
62. Monnier L, Colette C, Dunseath GJ, Owens DR: The loss of postprandial glycemic control precedes stepwise deterioration of fasting with worsening diabetes. Diabetes Care 2007;30:263-269.
63. Monnier L, Lapinski H, Colette C: Contributions of fasting and postprandial plasma glucose increments to the overall diurnal hyperglycemia of type 2 diabetic patients: variations with increasing levels of HbA(1c). Diabetes Care 2003;26:881-885.
64. Riddle M, Umpierrez G, DiGenio A, et al.: Contributions of basal and postprandial hyperglycemia over a wide range of A1C levels before and after treatment intensification in type 2 diabetes. Diabetes Care 2011;34:2508-2514.
65. Standl E, Schnell O, Ceriello A: Postprandial hyperglycemia and glycemic variability: should we care? Diabetes Care 2011;34 Suppl 2:S120-S127.
66. Hanefeld M, Fischer S, Julius U, et al.: Risk factors for myocardial infarction and death in newly detected NIDDM: the Diabetes Intervention Study, 11-year followup. Diabetologia 1996;39:1577-1583.
67. Cavalot F, Pagliarino A, Valle M, et al.: Postprandial blood glucose predicts cardiovascular events and all-cause mortality in type 2 diabetes in a 14-year follow-up: lessons from the San Luigi Gonzaga Diabetes Study. Diabetes Care 2011;34:2237-2243.
68. Ceriello A: Postprandial hyperglycemia and cardiovascular disease: is the HEART2D study the answer? Diabetes Care 2009;32:521-522.
69. Raz I, Ceriello A, Wilson PW, et al.: Post hoc subgroup analysis of the HEART2D trial demonstrates lower cardiovascular risk in older patients targeting postprandial versus fasting/premeal glycemia. Diabetes Care 2011;34: 1511-1513.
70. Raz I, Wilson PW, Strojek K, et al.: Effects of prandial versus fasting glycemia on cardiovascular outcomes in type 2 diabetes: the HEART2D trial. Diabetes Care 2009; 32:381-386.
71. Hill NR, Hindmarsh PC, Stevens RJ, et al.: A method for assessing quality of control from glucose profiles. Diabet Med 2007;24:753-758.
72. Kovatchev BP, Otto E, Cox D, et al.: Evaluation of a new measure of blood glucose variability in diabetes. Diabetes Care 2006;29:2433-2438.
73. Pitsillides AN, Anderson SM, Kovatchev B: Hypoglycemia risk and glucose variability indices derived from routine self-monitoring of blood glucose are related to laboratory measures of insulin sensitivity and epinephrine counterregulation. Diabetes Technol Ther 2011;13:11-17.
74. Kim SK, Kwon SB, Yoon KH, et al.: Assessment of glycemic lability and severity of hypoglycemia in Korean patients with type 1 diabetes. Endocr J 2011;58:433-440.
75. Kohnert KD, Vogt L, Augstein P, et al.: Relationships between glucose variability and conventional measures of glycemic control in continuously monitored patients with type 2 diabetes. Horm Metab Res 2009;41:137-141.
76. Patton SR, Clements MA: Average daily risk range as a measure for clinical research and routine care. J Diabetes Sci Technol 2013;7:1370-1375.
77. Pepper GM, Steinsapir J, Reynolds K: Effect of short-term iPRO continuous glucose monitoring on hemoglobin A1c levels in clinical practice. Diabetes Technol Ther 2012;14: 654-657.
78. Patrascioiu I, Quiros C, Rios P, et al.: Transitory beneficial effects of professional continuous glucose monitoring on the metabolic control of patients with type 1 diabetes. Diabetes Technol Ther 2014;16:219-223.
79. Leinung M, Nardacci E, Patel N, et al.: Benefits of shortterm professional continuous glucose monitoring in clinical practice. Diabetes Technol Ther 2013;15:744-747.
80. Wright L, Vasudevan S, Huynh P, et al. Professional continuous glucose monitoring improves hemoglobin a1c in insulin-requiring diabetic patients. Endocr Rev 2014; 35:MON-1004. http://press.endocrine.org/doi/abs/10.1210/endo-meetings.2014.DGM.3.MON-1004 (accessed May 7, 2017).
81. Bergenstal RM, Ahmann AJ, Bailey T, et al.: Recommendations for standardizing glucose reporting and analysis to optimize clinical decision making in diabetes: the Ambulatory Glucose Profile (AGP). Diabetes Technol Ther 2013;15:198-211.
82. Brewer KW, Chase HP, Owen S, Garg SK: Slicing the pie. Correlating HbA-values with average blood glucose values in a pie chart form. Diabetes Care 1998;21:209-212.
83. 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: 968-983.
84. Qu Y, Jacober SJ, Zhang Q, et al.: Rate of hypoglycemia in insulin-treated patients with type 2 diabetes can be predicted from glycemic variability data. Diabetes Technol Ther 2012;14:1008-1012.
85. Monnier L, Wojtusciszyn A, Colette C, Owens D: The contribution of glucose variability to asymptomatic hypoglycemia in persons with type 2 diabetes. Diabetes Technol Ther 2011;13:813-818.
86. Kovatchev BP, Cox DJ, Gonder-Frederick LA, et al.: Assessment of risk for severe hypoglycemia among adults with IDDM: validation of the low blood glucose index. Diabetes Care 1998;21:1870-1875.
87. Rodbard D: Clinical interpretation of indices of quality of glycemic control and glycemic variability. Postgrad Med 2011;123:107-118.
88. Rodbard D, Bailey T, Jovanovic L, et al.: Improved quality of glycemic control and reduced glycemic variability with use of continuous glucose monitoring. Diabetes Technol Ther 2009;11:717-723.
89. Bragd J, Adamson U, Backlund LB, et al.: Can glycaemic variability, as calculated from blood glucose selfmonitoring, predict the development of complications in type 1 diabetes over a decade? Diabetes Metab 2008;34(6 Pt 1):612-616.
90. Soupal J, Skrha J, Jr., Fajmon M, et al.: Glycemic variability is higher in type 1 diabetes patients with microvascular complications irrespective of glycemic control. Diabetes Technol Ther 2014;16:198-203.
91. Snell-Bergeon JK, Roman R, Rodbard D, et al.: Glycaemic variability is associated with coronary artery calcium in men with Type 1 diabetes: the Coronary Artery Calcification in Type 1 Diabetes study. Diabet Med 2010; 27:1436-1442.
92. Kovatchev BP, Cox DJ, Gonder-Frederick LA, Clarke W: Symmetrization of the blood glucose measurement scale and its applications. Diabetes Care 1997;20:1655-1658.
93. Hirsch IB: Glycemic variability: it's not just about A1C anymore! Diabetes Technol Ther 2005;7:780-783.
94. Rodbard D: Hypo-and hyperglycemia in relation to the mean, standard deviation, coefficient of variation, and nature of the glucose distribution. Diabetes Technol Ther 2012;14:868-876.
95. Mazze RS, Strock E, Wesley D, et al.: Characterizing glucose exposure for individuals with normal glucose tolerance using continuous glucose monitoring and ambulatory glucose profile analysis. Diabetes Technol Ther 2008;10:149-159.
96. Mazze RS, Lucido D, Langer O, et al.: Ambulatory glucose profile: representation of verified self-monitored blood glucose data. Diabetes Care 1987;10:111-117.
97. Cryer PE: Hypoglycaemia: the limiting factor in the glycaemic management of type I and type II diabetes. Diabetologia 2002;45:937-948.
98. Zoungas S, Patel A, Chalmers J, et al.: Severe hypoglycemia and risks of vascular events and death. N Engl J Med 2010;363:1410-1418.
99. Seaquist ER, Miller ME, Bonds DE, et al.: The impact of frequent and unrecognized hypoglycemia on mortality in the ACCORD study. Diabetes Care 2012;35:409-414.
100. McCoy RG, Van Houten HK, Ziegenfuss JY, et al.: Increased mortality of patients with diabetes reporting severe hypoglycemia. Diabetes Care 2012;35:1897-1901.
101. Defining and reporting hypoglycemia in diabetes: a report from the American Diabetes Association Workgroup on Hypoglycemia. Diabetes Care 2005;28:1245-1249.
102. International Hypoglycaemia Study Group: Glucose concentrations of less than 3.0mmol/L (54mg/dL) should be reported in clinical trials: a joint position statement of the American Diabetes Association and the European Association for the Study of Diabetes. Diabetes Care 2017;40:155-157.
103. BaileyT,BodeBW,ChristiansenMP, et al.:The performance and usability of a factory-calibrated flash glucose monitoring system. Diabetes Technol Ther 2015;17:787-794.
104. Ish-Shalom M, Wainstein J, Raz I, Mosenzon O: Improvement in glucose control in difficult-to-control patients with diabetes using a novel flash glucose monitoring device. J Diabetes Sci Technol 2016;10:1412-1413.
105. Bolinder J, Antuna R, Geelhoed-Duijvestijn P, et al.: Novel glucose-sensing technology and hypoglycaemia in type 1 diabetes: a multicentre, non-masked, randomised controlled trial. Lancet 2016;388:2254-2263.
106. Haak T, Hanaire H, Ajjan R, et al.: Flash glucose-sensing technology as a replacement for blood glucose monitoring for the management of insulin-treated type 2 diabetes: a multicenter, open-label randomized controlled trial. Diabetes Ther 2016;8:55-73.
107. Bonora B, Maran A, Ciciliot S, et al.: Head-to-head comparison between flash and continuous glucose monitoring systems in outpatients with type 1 diabetes. J Endocrinol Invest 2016;39:1391-1399.
108. Dover AR, Stimson RH, Zammitt NN, Gibb FW: Flash glucose monitoring improves outcomes in a type 1 diabetes clinic. J Diabetes Sci Technol 2017;11(2):442-443.