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Original Article

C-Reactive Protein and 5-Year Survival in Type 2 Diabetes

The Casale Monferrato Study

  1. Graziella Bruno1,
  2. Paolo Fornengo1,
  3. Giulia Novelli1,
  4. Francesco Panero1,
  5. Massimo Perotto1,
  6. Olivia Segre1,
  7. Chiara Zucco1,
  8. PierCarlo Deambrogio2,
  9. Giuseppe Bargero2 and
  10. Paolo Cavallo Perin1
  1. 1Department of Internal Medicine, University of Torino, Torino, Italy; and
  2. 2Santo Spirito Hospital, Casale Monferrato, Alessandria, Italy.
  1. Corresponding author: Graziella Bruno, graziella.bruno{at}unito.it.
Diabetes 2009 Apr; 58(4): 926-933. https://doi.org/10.2337/db08-0900
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  • FIG. 1.
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    FIG. 1.

    Kaplan-Meier curves depicting the survival curves of the cohort by CRP levels (dotted line CRP ≤3 mg/l, solid line >3 mg/ml). Log-rank test P < 0.001.

Tables

  • Figures
  • TABLE 1

    Baseline characteristics of subjects with type 2 diabetes of the Casale Monferrato Study, by CRP values

    CRP tertiles
    P
    <1.6 mg/l1.6–4.4 mg/l>4.4 mg/l
    n759834788
    Men434 (57.2)422 (50.6)328 (41.6)<0.0001
    Age (years)67.1 ± 10.668.1 ± 9.967.7 ± 10.70.16
    Duration of diabetes (years)11.2 ± 8.410.3 ± 7.410.5 ± 8.00.06
    BMI (kg/m2)26.7 ± 4.028.7 ± 4.530.6 ± 6.0<0.0001
    Waist circumference (cm)93.9 ± 11.098.8 ± 11.6101.9 ± 12.5<0.0001
    Systolic blood pressure (mmHg)143.2 ± 15.9146.7 ± 15.9147.1 ± 17.0<0.0001
    Diastolic blood pressure (mmHg)81.8 ± 7.982.2 ± 8.183.4 ± 8.5<0.0001
    Hypertension653 (86.3)740 (89.1)718 (91.1)0.01
    Glucose (mg/dl)163.0 ± 48.7172.9 ± 52.9182.6 ± 61.0<0.0001
    A1C (%)6.8 ± 1.76.9 ± 1.77.3 ± 1.9<0.0001
    Total cholesterol (mg/dl)205.6 ± 40.6213.8 ± 38.7215.4 ± 40.6<0.0001
    LDL cholesterol (mg/dl)123.0 ± 35.5128.7 ± 31.9130.9 ± 35.0<0.0001
    HDL cholesterol (mg/dl)57.2 ± 16.154.5 ± 14.852.7 ± 14.2<0.0001
    Triglycerides (mg/dl)113 (79–155)134 (96–178)141 (101–192)<0.0001
    ApoA1 (mg/dl)160.5 ± 39.5154.7 ± 37.8147.1 ± 38.4<0.0001
    ApoB (mg/dl)96.1 ± 26.0103.5 ± 25.9106.7 ± 27.4<0.0001
    ApoB/apoA10.65 ± 0.310.72 ± 0.310.79 ± 0.37<0.0001
    Creatinine (mg/dl)0.84 (0.70–0.97)0.84 (0.71–0.98)0.86 (0.69–1.02)0.16
    Fibrinogen (g/l)353.5 ± 66.5371.8 ± 68.9413.1 ± 96.2<0.0001
    Uric acid (mg/dl)5.22 ± 1.445.57 ± 1.556.08 ± 2.53<0.0001
    AER (μg/min)10.9 (4.0–22.6)13.1 (4.6–27.7)16.3 (4.9–40.7)<0.0001
        20–200137 (22.9)169 (25.7)184 (29.8)<0.0001
        >20024 (4.0)31 (4.7)46 (7.5)
    CVD136 (17.9)180 (21.6)194 (24.6)0.006
    Smoking
        Former smoker243 (32.9)236 (29.7)221 (28.9)0.28
        Smoker112 (15.2)130 (16.3)109 (14.2)
    Glucose-lowering treatment
        Diet128 (17.0)135 (16.4)102 (13.1)0.21
        Oral drugs549 (73.0)605 (73.7)585 (75.4)
        Insulin75 (10.0)81 (9.9)89 (11.5)
    Statins163 (21.5)163 (19.5)151 (19.2)0.77
    • Data are means ± SD, n (%), or geometric means (95% CI).

  • TABLE 2

    Baseline characteristics of people with type 2 diabetes of the Casale Monferrato Study, by living status on 31 December 2006

    SurvivedDeceasedP
    n1,885496
    Men922 (48.9)262 (52.8)0.12
    Age (years)65.9 ± 10.274.1 ± 8.5<0.0001
    Duration of diabetes (years)10.2 ± 7.812.6 ± 8.4<0.0001
    CRP (mg/dl)2.5 (1.2–5.3)3.7 (1.6–9.1)<0.0001
        <1.6642 (34.1)117 (23.6)<0.0001
        1.6–4.4671 (35.6)163 (32.8)
        >4.4572 (30.3)216 (43.6)
    BMI (kg/m2)28.9 ± 5.028.0 ± 5.40.0009
    Waist circumference (cm)98.2 ± 12.298.3 ± 12.80.82
    Systolic blood pressure (mmHg)145.5 ± 16.2146.7 ± 17.10.14
    Diastolic blood pressure (mmHg)83.0 ± 8.282.3 ± 8.40.10
    Hypertension1,653 (87.9)458 (92.3)0.005
    Glucose (mg/dl)171.5 ± 53.5178.3 ± 60.00.014
    A1C (%)7.0 ± 1.77.3 ± 1.90.0003
    Total cholesterol (mg/dl)213.1 ± 40.0206.3 ± 40.20.001
    LDL cholesterol (mg/dl)129.0 ± 34.2122.3 ± 33.90.0002
    HDL cholesterol (mg/dl)54.7 ± 14.855.0 ± 16.60.70
    Triglycerides (mg/dl)129.6 (92–177)127.7 (87–175)0.57
    ApoA1 (mg/dl)154.9 ± 38.8150.7 ± 39.10.03
    ApoB (mg/dl)102.8 ± 26.3100.0 ± 28.30.04
    ApoB/apoA10.72 ± 0.330.72 ± 0.340.99
    Creatinine (mg/dl)0.83 (0.69–0.97)0.93 (0.73–1.11)<0.001
    Fibrinogen (g/l)372.1 ± 68.5406.9 ± 110.4<0.0001
    Uric acid (mg/dl)5.52 ± 1.736.04 ± 2.51<0.0001
    AER (μg/min)12.1 (4.2–25.5)21.3 (6.4–49.3)<0.0001
        20–200377 (24.3)113 (35.3)
        >20073 (4.7)28 (8.8)
    CVD353 (18.7)157 (31.6)0.0001
    Smoking
        Former smoker534 (29.3)166 (34.9)0.03
        Smoker291 (16.0)60 (12.6)
    Glucose-lowering treatment
        Diet303 (71.0)62 (12.7)<0.0001
        Oral drugs1,402 (75.4)337 (68.9)
        Insulin155 (8.3)90 (18.4)
    Statins379 (20.1)98 (19.8)0.98
    • Data are means ± SD, n (%), or geometric means (95% CI).

  • TABLE 3

    HRs (95% CI) of 5-year mortality in people with type 2 diabetes of the Casale Monferrato Study

    All-cause mortality
    Cardiovascular mortality
    Model 1Model 2Model 3Model 1Model 2Model 3
    CRP tertiles (mg/dl)
        <1.61.001.001.001.001.001.00
        1.6–4.41.27 (1.00–1.62)1.27 (0.98–1.64)1.35 (0.98–1.87)1.18 (0.82–1.68)1.07 (0.73–1.56)1.22 (0.74–2.00)
        >4.41.99 (1.58–2.49)1.81 (1.41–2.32)1.65 (1.20–2.28)1.94 (1.39–2.71)1.62 (1.13–2.33)1.76 (1.09–2.82)
        P for trend<0.0001<0.0001<0.0001<0.00010.0060.015
    CRP (mg/l)
        ≤3 mg/l1.001.001.001.001.001.00
        >3 mg/l1.64 (1.37–1.96)1.49 (1.22–1.82)1.51 (1.18–1.92)1.53 (1.17–1.99)1.32 (0.99–1.77)1.44 (0.99–2.08)
    AER
        <20 μg/min1.001.00
        ≥20 μg/min1.47 (1.15–1.87)1.47 (1.01–2.14)
    Hypertension1.02 (0.64–1.63)0.69 (0.36–1.34)
    LDL cholesterol (1 SD)0.89 (0.79–1.01)1.07 (0.89–1.28)
    HDL cholesterol (1 SD)0.99 (0.88–1.13)0.92 (0.76–1.12)
    A1C (1 SD)1.10 (0.97–1.26)1.19 (0.97–1.44)
    CVD1.70 (1.31–2.22)2.56 (1.74–3.76)
    Antidiabetes treatment
        Diet1.001.00
        Oral drugs1.09 (0.76–1.57)1.24 (0.68–2.24)
        Insulin1.81 (1.12–2.94)2.29 (1.08–4.84)
    Smoking
        Never1.001.00
        Former smoker1.34 (0.96–1.86)1.24 (0.74–2.06)
        Current smoker1.42 (0.94–2.15)0.74 (0.33–1.65)
    Central obesity0.87 (0.67–1.12)0.92 (0.62–1.37)
    Statins1.02 (0.75–1.37)1.31 (0.86–1.99)
    • Model 1: adjusted for age, sex, diabetes duration. Model 2: model 1 adjustments plus hypertension, LDL and HDL cholesterol, A1C, smoking status, CVD, diabetes treatment, waist circumference, and statins. Model 3: model 2 adjustments plus AER.

  • TABLE 4

    HRs (95% CI) of 5-year mortality in people with type 2 diabetes of the Casale Monferrato Study

    All-cause mortality
    Cardiovascular mortality
    Number of deathsHR (95% CI) for CRP >3.0 mg/lNumber of deathsHR (95% CI) for CRP >3.0 mg/l
    Men2621.41 (1.02–1.96)1051.61 (0.94–2.74)
    Women2341.66 (1.14–2.41)1181.51 (0.88–2.57)
    Subjects without CVD at baseline
        All cohort3391.67 (1.24–2.24)1331.36 (0.83–2.24)
        Men1711.55 (1.03–2.32)571.11 (0.52–2.37)
        Women1681.71 (1.09–2.69)761.62 (0.82–3.22)
    A1C (%)
        ≤6.72161.54 (1.08–2.19)891.20 (0.67–2.14)
        >6.72681.51 (1.07–2.11)1281.56 (0.94–2.57)
    Diabetes duration (years)
        ≤8.72021.60 (1.11–2.32)761.29 (0.70–2.40)
        >8.72911.48 (1.06–2.06)1441.54 (0.94–2.51)
    LDL cholesterol (mg/dl)
        ≤1262651.38 (1.00–1.90)951.41 (0.80–2.50)
        >1281991.72 (1.18–2.50)1101.49 (0.91–2.46)
    HDL cholesterol (mg/dl)
        ≤512371.55 (1.09–2.21)1091.50 (0.88–2.54)
        >512421.52 (1.08–2.14)1061.45 (0.84–2.49)
    Central obesity
        No2411.40 (0.98–1.99)1021.46 (0.83–2.58)
        Yes2551.71 (1.20–2.43)1211.48 (0.88–2.50)
    • HRs adjusted for age, sex, diabetes duration, LDL and HDL cholesterol, A1C, smoking status, CVD, AER, diabetes treatment, waist circumference, and statins, apart from the stratification variable.

  • TABLE 5

    HR (95% CI) of 5-year mortality in people with type 2 diabetes of the Casale Monferrato Study

    All-cause mortality
    Cardiovascular mortality
    HR (95% CI)
    HR (95% CI)
    AER <20 μg/minAER ≥20 μg/minAER <20 μg/minAER ≥20 μg/min
    CRP ≤3 mg/l1.001.48 (1.03–2.13)1.001.74 (1.00–3.04)
    CRP >3 mg/l1.52 (1.11–2.09)2.22 (1.60–3.09)1.64 (1.00–2.69)2.13 (1.26–3.61)
    • HRs adjusted for age, sex, diabetes duration, LDL and HDL cholesterol, A1C, smoking status, CVD, diabetes treatment, waist circumference, and statins.

  • TABLE 6

    Measures of discrimination and calibration in the Casale Monferrato Study, by selected variables

    All-causes mortalityCardiovascular mortality
    Discrimination
        C statistic
            Nonmodifiable risk factors (age, sex, and diabetes duration) (model 1)0.7060.717
            Established risk factors (model 2)0.7440.793
            Established risk factors plus AER0.7500.799
            Established risk factors plus AER and CRP0.7560.802
        LR test
            Established risk factors (model 2)LR = 66, df = 11, P < 0.0001LR = 61.85, df = 11, P < 0.0001
            Established risk factors plus AERLR = 10.76, df = 1, P = 0.001LR = 4.69, df = 1, P = 0.03
            Established risk factors plus AER and CRPLR = 9.94, df = 1, P = 0.002LR = 3.03, df = 1, P = 0.08
        Bayes information criterion
            Nonmodifiable risk factors (age, sex, and diabetes duration) (model 1)4,021.241,693.40
            Established risk factors4,036.781,713.18
            Established risk factors plus AER4,033.451,715.90
            Established risk factors plus AER and CRP4,030.931,720.29
    Calibration
        Grønnesby and Borgan test
        Nonmodifiable risk factors (age, sex, and diabetes duration) (model 1)P = 0.28P = 0.10
        Established risk factorsP = 0.44P = 0.21
        Established risk factors plus AERP = 0.42P = 0.27
        Established risk factors plus AER and CRPP = 0.10P = 0.28
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C-Reactive Protein and 5-Year Survival in Type 2 Diabetes
Graziella Bruno, Paolo Fornengo, Giulia Novelli, Francesco Panero, Massimo Perotto, Olivia Segre, Chiara Zucco, PierCarlo Deambrogio, Giuseppe Bargero, Paolo Cavallo Perin
Diabetes Apr 2009, 58 (4) 926-933; DOI: 10.2337/db08-0900

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C-Reactive Protein and 5-Year Survival in Type 2 Diabetes
Graziella Bruno, Paolo Fornengo, Giulia Novelli, Francesco Panero, Massimo Perotto, Olivia Segre, Chiara Zucco, PierCarlo Deambrogio, Giuseppe Bargero, Paolo Cavallo Perin
Diabetes Apr 2009, 58 (4) 926-933; DOI: 10.2337/db08-0900
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