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Pathophysiology

Inflammatory Markers and Risk of Developing Type 2 Diabetes in Women

  1. Frank B. Hu123,
  2. James B. Meigs4,
  3. Tricia Y. Li1,
  4. Nader Rifai5 and
  5. JoAnn E. Manson236
  1. 1Department of Nutrition, Harvard School of Public Health, Boston, Massachusetts
  2. 2Channing Laboratory, Harvard Medical School and Brigham and Women’s Hospital, Boston, Massachusetts
  3. 3Department of Epidemiology, Harvard School of Public Health, Boston, Massachusetts
  4. 4Department of Medicine, General Medicine Division, Massachusetts General Hospital and Harvard Medical School, Boston, Massachusetts
  5. 5Department of Pathology, Children’s Hospital Medical Center and Harvard Medical School, Boston, Massachusetts
  6. 6Division of Preventive Medicine, Department of Medicine, Harvard Medical School and Brigham and Women’s Hospital, Boston, Massachusetts
  1. Address correspondence and reprint requests to Dr. Frank Hu, Department of Nutrition, Harvard School of Public Health, 665 Huntington Ave., Boston, MA 02115. E-mail: frank.hu{at}channing.harvard.edu
Diabetes 2004 Mar; 53(3): 693-700. https://doi.org/10.2337/diabetes.53.3.693
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  • FIG. 1.
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    FIG. 1.

    A–D: Multivariate OR of type 2 diabetes according to joint classifications of plasma levels of inflammatory and endothelial markers. Adjusted for the same variables as in Table 3.

  • FIG. 2.
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    FIG. 2.

    Multivariate OR of type 2 diabetes according to quintiles of CRP levels stratified by regular aspirin use (≥1/week). P for interaction = 0.0002. Adjusted for the same variables as in Table 3.

Tables

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  • TABLE 1

    Comparison of diabetes risk factors between case and control subjects at baseline*

    CaseControlP
    n737785
    Age (years)56.3 ± 6.956.2 ± 6.90.69
    BMI (kg/m2)30.3 ± 5.626.2 ± 6.1<0.001
    Physical activity (METs/week)†12.3 ± 15.215.6 ± 27.20.004
    Alcohol consumption (g/day)3.7 ± 7.16.5 ± 9.0<0.001
    Waist circumference (in)35.3 ± 4.931.3 ± 4.9<0.001
    Diet score‡7.8 ± 2.78.2 ± 2.7<0.001
    Current smoking (%)14.113.30.62
    Postmenopausal status (%)36.042.30.01
    Current postmenopausal hormone use (%)39.836.00.35
    Family history of diabetes in first-degree relative (%)46.821.0<0.001
    Race (Caucasian) (%)94.894.30.68
    Aspirin use ≥1/week25.120.90.05
    Biomarkers (median values)
     TNF-αR2 (pg/ml)2,646.52,383.8<0.001
     CRP (mg/dl)0.360.16<0.001
     IL-6 (pg/ml)2.381.84<0.001
     E-selectin (pg/ml)61.2545.37<0.001
     Fasting insulin (uU/ml)§11.968.27<0.001
    • Data are means ± SE unless otherwise indicated.

    • *

      * Case and control subjects were matched on age, fasting status, and race.

    • †

      † MET, metabolic equivalent; 1 MET hour is equivalent to energy expended by sting quietly for 1 h.

    • ‡

      ‡ Intakes for trans fat, cereal fiber, glycemic load, and P-to-S (polyunsaturated fat-to-saturated fat) ratio were categorized into quintiles and for each participant, the quintile value for each nutrient (a higher quintile score represents a lower risk) was summed and the sum was recategorized into quintiles.

    • §

      § A total of 432 case and 398 control subjects had fasting insulin measurement.

  • TABLE 2

    Spearman correlation coefficients* between BMI, waist circumference, fasting insulin, and inflammatory markers in control subjects

    BMIWaist circumferenceFasting insulinCRPIL-6TNF-αR2E-selectin
    BMI1.0——————
    Waist circumference0.781.0—————
    Fasting insulin0.290.271.0————
    CRP0.440.370.261.0———
    IL-60.300.290.180.371.0——
    TNF-αR20.240.250.150.270.281.0—
    E-selectin0.280.270.260.240.250.231.0
    • *

      * All correlation coefficients were statistically significant at P < 0.05.

  • TABLE 3

    RR (95% CI) of type 2 diabetes according to quintiles of inflammatory markers estimated from conditional logistic regression models

    Q1Q2Q3Q4Q5P for trend
    TNFαR2 (pg/ml)
     Range≤1,927.71,827.8–2,224.42,224.5–2,530.02,530.1–3,023.5≥3,023.6
     Median1,705.62,085.52,385.92,737.53,448.4
     n96/16798/155124/153192/155227/155
     Crude RR*1.001.14 (0.79, 1.65)1.29 (0.90, 1.84)2.10 (1.49, 2.95)2.59 (1.84, 3.65)<0.001
     BMI-adjusted RR†1.001.00 (0.68, 1.48)1.11 (0.76, 1.62)1.56 (1.08, 2.24)1.67 (1.16, 2.42)<0.001
     Multivariate RR‡1.000.89 (0.58, 1.37)1.09 (0.73, 1.64)1.47 (0.99, 2.18)1.64 (1.10, 2.45)0.001
    IL-6 (pg/ml)
     Range≤1.121.13–1.621.63–2.132.15–3.07≥3.08
     Median0.881.341.842.554.24
     n88/185110/150134/150176/151229/149
     Crude RR1.001.60 (1.11, 2.31)1.77 (1.24, 2.53)2.44 (1.71, 3.46)3.25 (2.30, 4.58)<0.001
     BMI-adjusted RR1.001.29 (0.87, 1.90)1.21 (0.83, 1.78)1.55 (1.06, 2.26)1.95 (1.34, 2.84)<0.001
     Multivariate RR1.001.24 (0.82, 1.88)1.23 (0.81, 1.86)1.43 (0.95, 2.15)1.91 (1.27, 2.86)0.001
    CRP (mg/dl)
     Range≤0.0550.056–0.1180.119–0.2080.209–0.404≥0.405
     Median0.030.0830.1580.2910.627
     n55/17658/15289/153216/152319/152
     Crude RR1.001.36 (0.87, 2.13)2.11 (1.38, 3.22)4.93 (3.33, 7.31)7.08 (4.84, 10.37)<0.001
     BMI-adjusted RR1.001.20 (0.75, 1.91)1.68 (1.08, 2.62)3.64 (2.42, 5.49)4.18 (2.78, 6.29)<0.001
     Multivariate RR1.001.30 (0.80, 2.13)1.62 (1.01, 2.06)3.61 (2.33, 5.60)4.36 (2.80, 6.80)<0.001
    • *

      * Conditioned on matching variables: age, fasting status, and race;

    • †

      † BMI as a continuous variable;

    • ‡

      ‡ adjusted for time at blood drawn, alcohol consumption (nondrinkers, 0–4.9, 5–10, and >10 g/day), physical activity (quintiles of METs/week), smoking status (never, past, and current smoking of 1–14, 15–24, and ≥25 cigarettes per day), BMI (continuous), family history of diabetes, postmenopausal hormone use and menopausal status (never/unknown user or premenopausal status, past, and current user), and diet score (in quintiles).

  • TABLE 4

    Multivariate RR (95% CI) of type 2 diabetes according to quintiles of inflammatory markers stratified by BMI, physical activity, diet score, and family history of diabetes*

    Q1Q2Q3Q4Q5P for trendP for interaction
    TNFαR2
     BMI <30 kg/m21.000.95 (0.58–1.57)1.16 (0.72–1.87)1.62 (1.02–2.59)2.25 (1.39–3.62)<0.001
     BMI ≥30 kg/m21.000.67 (0.26–1.68)1.33 (0.53–3.35)1.05 (0.45–2.44)0.93 (0.41–2.09)0.990.01
     Physical activity levels
      Low1.001.02 (0.58–1.77)1.74 (1.02–2.98)1.96 (1.18–3.28)2.14 (1.29–3.54)<0.001
      High1.000.75 (0.41–1.38)0.86 (0.48–1.54)1.29 (0.74–2.26)1.30 (0.72–2.34)0.110.72
     Diet score
      Low1.000.74 (0.42–1.29)1.04 (0.61–1.76)1.45 (0.89–2.36)2.05 (1.25–3.36)<0.001
      High1.001.06 (0.58–1.94)1.32 (0.73–2.38)1.78 (0.98–3.23)1.18 (0.64–2.18)0.480.21
     Family history of diabetes
      Yes1.000.73 (0.38–1.39)0.75 (0.38–1.45)1.15 (0.60–2.19)1.51 (0.75–3.07)0.07
      No1.000.93 (0.54–1.62)1.45 (0.87–2.41)1.82 (1.12–2.96)1.88 (1.16–3.04)0.0020.46
    IL-6
     BMI <30 kg/m21.001.20 (0.75–1.92)1.14 (0.70–1.84)1.44 (0.90–2.30)1.84 (1.16–2.94)0.006
     BMI ≥30 kg/m21.000.90 (0.31–2.62)1.11 (0.41–3.00)1.07 (0.41–2.78)1.46 (0.57–3.76)0.170.29
     Physical activity levels
      Low1.001.31 (0.75–2.29)1.27 (0.73–2.23)1.70 (1.00–2.91)2.47 (1.44–4.24)<0.001
      High1.001.38 (0.77–2.45)1.63 (0.93–2.86)1.44 (0.81–2.53)1.77 (1.01–3.08)0.090.73
     Diet score
      Low1.000.96 (0.56–1.65)1.36 (0.80–2.29)1.30 (0.78–2.16)1.86 (1.12–3.09)0.004
      High1.001.74 (0.96–3.15)1.28 (0.69–2.36)1.85 (1.01–3.37)2.16 (1.19–3.92)0.0240.38
     Family history of diabetes
      Yes1.001.99 (1.02–3.88)1.79 (0.90–3.55)2.19 (1.14–4.20)1.97 (1.04–3.73)0.16
      No1.000.90 (0.54–1.50)1.15 (0.70–1.87)1.29 (0.80–2.10)1.95 (1.21–3.13)<0.0010.13
    CRP
     BMI <30 kg/m21.000.80 (0.46–1.37)0.98 (0.57–1.69)2.42 (1.49–3.95)3.57 (2.13–5.96)<0.001
     BMI ≥30 kg/m21.001.74 (0.48–6.27)1.42 (0.49–4.18)2.76 (1.01–7.58)3.38 (1.31–8.77)0.0040.13
     Physical activity levels
      Low1.001.28 (0.69–2.37)1.51 (0.83–2.74)3.71 (2.14–6.43)4.28 (2.47–7.43)<0.001
      High1.000.86 (0.42–1.78)1.34 (0.68–2.62)2.81 (1.49–5.30)4.01 (2.09–7.68)<0.0010.87
     Diet score
      Low1.001.03 (0.55–1.92)1.28 (0.72–2.27)2.91 (1.70–5.01)4.33 (2.50–7.49)<0.001
      High1.001.23 (0.61–2.49)1.69 (0.83–3.46)3.89 (2.05–7.36)4.10 (2.13–7.88)<0.0010.94
     Family history of diabetes
      Yes1.001.49 (0.66–3.36)1.84 (0.89–3.79)3.27 (1.61–6.61)3.73 (1.85–7.56)<0.001
      No1.000.94 (0.51–1.72)1.15 (0.64–2.11)3.30 (1.97–5.52)4.66 (2.74–7.89)<0.0010.15
    • *

      * Physical activity and diet score were classified into low and high groups according to median values. RRs were adjusted for the same variables as in table 3.

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Inflammatory Markers and Risk of Developing Type 2 Diabetes in Women
Frank B. Hu, James B. Meigs, Tricia Y. Li, Nader Rifai, JoAnn E. Manson
Diabetes Mar 2004, 53 (3) 693-700; DOI: 10.2337/diabetes.53.3.693

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Inflammatory Markers and Risk of Developing Type 2 Diabetes in Women
Frank B. Hu, James B. Meigs, Tricia Y. Li, Nader Rifai, JoAnn E. Manson
Diabetes Mar 2004, 53 (3) 693-700; DOI: 10.2337/diabetes.53.3.693
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