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e-Letters: Observations

Hyperglycemia Is the Main Mediator of Prediabetes- and Type 2 Diabetes–Associated Impairment of Microvascular Function: The Maastricht Study

  1. Ben M. Sörensen1,2,
  2. Alfons J.H.M. Houben1,2,
  3. Tos T.J.M. Berendschot3,
  4. Jan S.A.G. Schouten3,
  5. Abraham A. Kroon1,2,
  6. Carla J.H. van der Kallen1,2,
  7. Ronald M.A. Henry1,2,4,
  8. Annemarie Koster5,6,
  9. Koen D. Reesink1,7,
  10. Pieter C. Dagnelie1,5,8,
  11. Nicolaas C. Schaper1,2,5,
  12. Casper G. Schalkwijk1,2,
  13. Miranda T. Schram1,2,4 and
  14. Coen D.A. Stehouwer1,2⇑
  1. 1School for Cardiovascular Diseases (CARIM), Maastricht University, Maastricht, the Netherlands
  2. 2Department of Internal Medicine, Maastricht University Medical Center+, Maastricht, the Netherlands
  3. 3University Clinic for Ophthalmology, Maastricht University Medical Center+, Maastricht, the Netherlands
  4. 4Heart and Vascular Center, Maastricht University Medical Center+, Maastricht, the Netherlands
  5. 5Care and Public Health Research Institute (CAPHRI), Maastricht University, Maastricht, the Netherlands
  6. 6Department of Social Medicine, Maastricht University, Maastricht, the Netherlands
  7. 7Department of Biomedical Engineering, Maastricht University, Maastricht, the Netherlands
  8. 8Department of Epidemiology, Maastricht University, Maastricht, the Netherlands
  1. Corresponding author: Coen D.A. Stehouwer, cda.stehouwer{at}mumc.nl.
Diabetes Care 2017 Aug; 40(8): e103-e105. https://doi.org/10.2337/dc17-0574
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  • Table 1

    General characteristics and retinal and skin measures for the retinal study population according to glucose metabolism status

    CharacteristicsNGM (n = 1,040)Prediabetes (n = 276)T2D (n = 475)
    Age (years)58.0 ± 8.261.5 ± 7.262.9 ± 7.6
    Women596 (57.3)130 (47.1)147 (30.9)
    Diabetes duration (years)*——6.0 (3.0–12.0)
    Diabetes medication use
     Any type——359 (75.6)
     Insulin——86 (18.1)
     Oral glucose-lowering medication——338 (71.2)
    BMI (kg/m2)25.5 ± 3.427.5 ± 4.029.5 ± 4.5
    Waist circumference (cm)
     Men96.3 ± 9.1101.6 ± 9.4106.7 ± 11.6
     Women85.6 ± 9.792.7 ± 12.1100.9 ± 13.6
    Smoking
     Never/former/current, n409/502/11675/161/33136/264/62
     Never/former/current, %39.8/48.9/11.327.9/59.9/12.329.4/57.1/13.4
    History of cardiovascular disease116 (11.4)30 (11.2)118 (25.8)
    eGFR (mL/min/1.73 m2)89.9 ± 13.087.2 ± 14.085.3 ± 17.2
    eGFR <60 mL/min/1.73 m218 (1.7)10 (3.6)45 (9.5)
    (Micro)albuminuria†47 (4.6)15 (5.4)77 (16.2)
    Retinopathy1 (0.1)1 (0.4)18 (3.9)
    Composite indices of potential mediators‡
    Markers of hyperglycemia
     HbA1c (%)‡5.4 ± 0.45.7 ± 0.46.8 ± 0.9
     HbA1c (mmol/mol)35.8 ± 3.738.4 ± 4.550.6 ± 9.9
     Fasting glucose (mmol/L)‡5.2 ± 0.45.9 ± 0.67.7 ± 1.7
     2-h postload glucose (mmol/L)‡§5.4 ± 1.18.2 ± 1.714.2 ± 3.9
     Skin autofluorescence (AU)‡2.3 ± 0.52.4 ± 0.52.6 ± 0.6
    Markers of blood pressure
     Ambulatory 24-h SBP (mmHg)‡117.3 ± 11.1120.1 ± 11.9122.4 ± 11.7
     Ambulatory 24-h DBP (mmHg)‡73.6 ± 7.274.5 ± 7.373.0 ± 7.0
     Antihypertensive medication use‡226 (21.7)113 (40.9)333 (70.1)
    Markers of lipid profile
     Total-to-HDL cholesterol ratio3.5 ± 1.13.9 ± 1.33.7 ± 1.1
     LDL cholesterol (mmol/L)3.3 ± 0.93.3 ± 1.12.4 ± 0.9
     Total cholesterol (mmol/L)‡5.6 ± 1.05.5 ± 1.24.4 ± 1.1
     HDL cholesterol (mmol/L)‡1.7 ± 0.51.5 ± 0.41.3 ± 0.4
     Triglycerides (mmol/L)‡1.2 ± 0.61.6 ± 1.01.8 ± 0.9
     Lipid-modifying medication use‡178 (17.1)93 (33.7)350 (73.7)
    Markers of insulin resistance
     HOMA2-IRInsulin (AU)‡1.3 ± 0.71.9 ± 1.12.4 ± 1.4
     HOMA2-IRC-peptide (AU)‡1.3 ± 0.51.7 ± 0.72.1 ± 0.9
    Markers of low-grade inflammation
     hs-CRP (mg/L)‡1.1 (0.6–2.2)1.8 (0.8–3.5)1.5 (0.7–3.3)
     Serum amyloid A (mg/L)‡3.0 (1.9–5.0)3.6 (2.3–5.7)3.5 (2.2–6.0)
     Soluble ICAM-1 (ng/mL)‡338.6 ± 80.2365.8 ± 103.2383.8 ± 115.9
     Interleukin-6 (pg/mL)‡0.5 (0.4–0.8)0.6 (0.4–0.9)0.8 (0.6–1.1)
     Interleukin-8 (pg/mL)‡3.7 (3.0–4.6)4.3 (3.3–5.3)4.8 (4.0–6.1)
     Tumor necrosis factor-α (pg/mL)‡2.1 (1.8–2.4)2.2 (1.9–2.6)2.5 (2.1–2.9)
    Markers of arterial stiffness
     Carotid-femoral pulse wave velocity (m/s)‡8.4 ± 1.79.2 ± 2.19.9 ± 2.3
     Carotid distensibility coefficient (103/kPa)‡15.1 ± 5.213.7 ± 4.813.3 ± 4.9
    Microvascular outcomes
    Baseline arteriolar diameter (MU)115.3 ± 15.3114.8 ± 15.9116.0 ± 15.9
    Arteriolar average dilation (%)
     Mean ± SD3.4 ± 2.83.1 ± 2.82.4 ± 2.7
     Median [interquartile range]3.0 (1.1–5.3)2.8 (0.8–5.0)1.6 (0.4–3.9)
    Baseline skin blood flow (PU)‖10.8 ± 6.411.7 ± 7.211.0 ± 5.7
    Skin hyperemic response (%)‖
     Mean ± SD1,252.6 ± 813.41,107.4 ± 710.8941.7 ± 701.1
     Median [interquartile range]1,104.0 (668.7–1,656.9)1,006.9 (604.9–1,536.9)821.2 (479.0–1,209.8)
    • Data are reported as mean ± SD, median [interquartile range], or number (%) as appropriate. AU, arbitrary units; DBP, diastolic blood pressure; eGFR, estimated glomerular filtration rate; HOMA2-IR, HOMA of insulin resistance; ICAM, intercellular adhesion molecule; MU, measurement units; PU, perfusion units; SBP, systolic blood pressure.

    • ↵* Available in 313 individuals with type 2 diabetes.

    • ↵† (Micro)albuminuria was defined as a urinary albumin excretion of >30 mg per 24 h.

    • ↵‡ Indicates that the individual marker is part of the corresponding composite index.

    • ↵§ Available in 389 individuals with T2D, as the oral glucose tolerance test was not performed in individuals who were on insulin treatment.

    • ↵‖ Heat-induced skin hyperemia measures were available in a different subset of n = 1,281.

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Hyperglycemia Is the Main Mediator of Prediabetes- and Type 2 Diabetes–Associated Impairment of Microvascular Function: The Maastricht Study
Ben M. Sörensen, Alfons J.H.M. Houben, Tos T.J.M. Berendschot, Jan S.A.G. Schouten, Abraham A. Kroon, Carla J.H. van der Kallen, Ronald M.A. Henry, Annemarie Koster, Koen D. Reesink, Pieter C. Dagnelie, Nicolaas C. Schaper, Casper G. Schalkwijk, Miranda T. Schram, Coen D.A. Stehouwer
Diabetes Care Aug 2017, 40 (8) e103-e105; DOI: 10.2337/dc17-0574

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Hyperglycemia Is the Main Mediator of Prediabetes- and Type 2 Diabetes–Associated Impairment of Microvascular Function: The Maastricht Study
Ben M. Sörensen, Alfons J.H.M. Houben, Tos T.J.M. Berendschot, Jan S.A.G. Schouten, Abraham A. Kroon, Carla J.H. van der Kallen, Ronald M.A. Henry, Annemarie Koster, Koen D. Reesink, Pieter C. Dagnelie, Nicolaas C. Schaper, Casper G. Schalkwijk, Miranda T. Schram, Coen D.A. Stehouwer
Diabetes Care Aug 2017, 40 (8) e103-e105; DOI: 10.2337/dc17-0574
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