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Obesity Studies

Increased Infiltration of Macrophages in Omental Adipose Tissue Is Associated With Marked Hepatic Lesions in Morbid Human Obesity

  1. Raffaella Cancello123,
  2. Joan Tordjman123,
  3. Christine Poitou123,
  4. Gaël Guilhem123,
  5. Jean Luc Bouillot4,
  6. Danielle Hugol5,
  7. Christiane Coussieu6,
  8. Arnaud Basdevant123,
  9. Avner Bar Hen7,
  10. Pierre Bedossa89,
  11. Michèle Guerre-Millo123 and
  12. Karine Clément123
  1. 1Institut National de la Santé et de la Recherche Médicale (INSERM), U755 Nutriomique, Paris, France
  2. 2Pierre and Marie Curie-Paris 6 University, Faculty of Medicine, Les Cordeliers, IFR58, Paris, France
  3. 3Nutrition Department, AP-HP, Hôtel-Dieu Hospital, Paris, France
  4. 4Surgery Department, AP-HP, Hôtel Dieu Hospital, Paris, France
  5. 5Anatomo-Pathology Department, AP-HP, Hôtel Dieu Hospital, Paris, France
  6. 6Biochemistry Department, AP-HP, Hôtel Dieu Hospital, Paris, France
  7. 7LIM and BIO, Paris 13 University, Bobigny, France
  8. 8Pathology Department, AP-HP Beaujon Hospital, Clichy France
  9. 9National Center for Scientific Research, Unité Mixte de Recherche 149, Paris, France
  1. Address correspondence and reprint requests to Prof. Karine Clément, INSERM, U755 Nutriomique, Service de Nutrition, Hôtel-Dieu, 1 Place du Parvis Notre-Dame, 75004 Paris, France. E-mail: karine.clement{at}htd.ap-hop-paris.fr
Diabetes 2006 Jun; 55(6): 1554-1561. https://doi.org/10.2337/db06-0133
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  • FIG. 1.
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    FIG. 1.

    Immunohistochemical detection of HAM 56+ macrophages in omental WAT (A and C) and subcutaneous WAT (B and D) of one representative obese woman. A: Macrophages are both dispersed into the omental WAT parenchyma and in crown arrangement (A, arrow heads). B: Only crown-like structures are visible in subcutaneous WAT parenchyma. Higher magnification (60×) of crown structures in omental WAT (C) and subcutaneous WAT (D). oWAT, omental WAT; scWAT, subcutaneous WAT.

  • FIG. 2.
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    FIG. 2.

    Percentage of macrophage infiltration (A) and adipocyte diameter (B) in omental WAT (▪) and subcutaneous WAT (□). Data are the means ± SE. *P < 0.01; **P < 0.001. C: Correlations between the percentage of macrophage infiltration and adipocyte diameter in omental WAT (▪) and subcutaneous WAT (□). Lines are linear regressions in omental WAT (solid line) and in subcutaneous WAT (dotted line). oWAT, omental WAT; scWAT, subcutaneous WAT.

  • FIG. 3.
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    FIG. 3.

    Correlations between the percentage of macrophages and triglycerides (A) or HDL cholesterol (B) in omental WAT (▪) and subcutaneous WAT (□). Lines are linear regressions in omental WAT (solid line) and in subcutaneous WAT (dotted line).

  • FIG. 4.
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    FIG. 4.

    Percentage of macrophages in omental WAT (A) and in subcutaneous WAT (B) in 39 subjects scored for hepatic fibroinflammatory lesions. Horizontal lines are the mean value in each group. *P < 0.05 using Student’s test for each pair, compared with mild and absent group. oWAT, omental WAT; scWAT, subcutaneous WAT.

Tables

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  • TABLE 1

    Clinical and biological parameters of 55 morbidly obese subjects

    PhenotypeWhole populationLiver subset
    n5539
    F/M46/9 (83)31/8 (80)
    Age (years)39.5 ± 1.4438.3 ± 1.63
    BMI (kg/m2)47.9 ± 0.9347.8 ± 1.15
    Glucose homeostasis
        Glucose (mmol/l)6.15 ± 0.296.24 ± 0.33
        Insulin (μU/ml)15.0 ± 1.2715.6 ± 1.44
        QUICKI0.320.32
    Type 2 diabetes
        Glycemia >7 mmol/l or treatment12/55 (22)9/39 (23)
    Lipids homeostasis
        Cholesterol (mmol/l)5.32 ± 0.125.37 ± 0.14
        HDL cholesterol (mmol/l)1.34 ± 0.061.33 ± 0.05
        Triglycerides (mmol/l)1.49 ± 0.111.47 ± 0.14
    Adipokines
        Leptin (ng/ml)62.4 ± 3.8061.2 ± 4.13
        Adiponectin (μg/ml)7.01 ± 0.426.81 ± 0.51
    Risk factors
        HDL <1.03 mmol/l (M), <1.29 mmol/l (F)25 (45)18 (46)
        Hypertension ≥130/85 mmHg24 (44)16 (41)
        Glucose ≥5.6 mmol/l25 (45)21 (54)
        Triglycerides ≥1.7 mmol/l17 (31)11 (28)
    Inflammatory factors
        TNF-α (pg/ml)1.79 ± 0.071.87 ± 0.09
        Interleukin 6 (pg/ml)2.63 ± 0.182.74 ± 0.23
        High-sensitivity CRP (mg/dl)0.89 ± 0.090.91 ± 0.12
        Orosomucoid (g/l)0.99 ± 0.030.99 ± 0.03
        Serum amyloid A (μg/ml)31.5 ± 7.635.1 ± 10.1
    Hepatic factors
        AST (IU/l)22.8 ± 1.5723.7 ± 1.98
        Alanine aminotransferase (IU/l)32.8 ± 3.7633.5 ± 4.40
        γGT (mg/dl)36.8 ± 2.9537.1 ± 3.31
    • Data are the means ± SE or n (%). Histology of hepatic biopsies was suitable for 39 individuals of the cohort, designated as the “liver subset.” No significant differences were observed between the two groups.

  • TABLE 2

    Clinical and biological parameters of 39 obese patients classified by the severity of liver fibroinflammatory scores

    Hepatic fibroinflammatory score
    P
    Absent (0)Mild (1–2)Marked (>2)
    n71715—
    F/M6/1 (86)16/1 (94)9/6 (60)—
    Age (years)41.4 ± 4.637.4 ± 2.539.0 ± 2.50.67
    BMI (kg/m2)44.5 ± 3.547.6 ± 1.549.8 ± 1.90.28
    Glucose (mmol/l)5.57 ± 0.395.79 ± 0.377.17 ± 0.71*0.11
    Insulin (μU/ml)8.9 ± 1.7514.5 ± 1.7619.3 ± 2.82†0.036
    QUICKI0.350.32‡0.30*0.009
    Type 2 diabetes03 (18)6 (40)0.09
    Cholesterol (mmol/l)5.63 ± 0.245.23 ± 0.185.47 ± 0.290.56
    HDL cholesterol (mmol/l)1.53 ± 0.151.35 ± 0.091.24 ± 0.060.26
    Triglycerides (mmol/l)1.17 ± 0.101.26 ± 0.171.89 ± 0.29*0.11
    Triglyceride–to–HDL cholesterol ratio0.84 ± 0.401.04 ± 0.251.74 ± 0.270.10
    Leptin (ng/ml)49.8 ± 5.5269.4 ± 6.0056.7 ± 7.90.14
    Adiponectin (μg/ml)7.19 ± 1.357.82 ± 0.905.59 ± 0.59*0.11
    TNF-α (pg/ml)1.87 ± 0.161.85 ± 0.181.90 ± 0.110.84
    Interleukin 6 (pg/ml)2.34 ± 0.612.54 ± 0.283.12 ± 0.410.33
    High-sensitivity CRP (mg/dl)1.09 ± 0.410.79 ± 0.130.97 ± 0.220.82
    Orosomucoid (g/l)1.00 ± 0.071.04 ± 0.050.93 ± 0.040.37
    Serum amyloid A (μg/ml)21.8 ± 8.636.8 ± 15.539.4 ± 19.70.83
    HDL <1.03 mmol/l (M), <1.29 mmol/l (F)2 (29)8 (44)8 (53)0.55
    Hypertension ≥130/85 mmHg2 (29)6 (35)8 (53)0.44
    Glucose ≥5.6 mmol/l3 (43)8 (44)10 (66)0.43
    Triglycerides ≥1.7 mmol/l03 (18)‡8 (53)*0.015
    Macrophages in omental WAT (%)22.2 ± 7.224.9 ± 3.8‡40.7 ± 4.5*0.016
    Adipocyte diameter omental WAT (μm)72.8 ± 7.672.3 ± 4.275.2 ± 3.10.75
    Macrophages in subcutaneous WAT (%)15.5 ± 1.5314.9 ± 2.4712.2 ± 3.130.12
    Adipocyte diameter in subcutaneous WAT (μm)95.8 ± 5.0584.0 ± 3.685.2 ± 2.80.11
    AST (IU/l)19.7 ± 3.319.6 ± 1.230.4 ± 4.3*0.012
    Alanine aminotransferase (IU/l)27.7 ± 10.925.9 ± 2.845.3 ± 9.3†0.043
    γGT (mg/dl)32.3 ± 10.932.6 ± 3.945.4 ± 5.3†0.045
    • Data are the means ± SE, R2, or n (%). P values were obtained by ANOVA test for continuous values or by χ2 test for noncontinuous values. A different label (*, †, ‡) indicates significant differences using Student’s t test for each pair (P < 0.05 for

    • *

      * mild vs. marked,

    • †

      † absent vs. marked, and

    • ‡

      ‡ absent vs. mild, respectively).

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Increased Infiltration of Macrophages in Omental Adipose Tissue Is Associated With Marked Hepatic Lesions in Morbid Human Obesity
Raffaella Cancello, Joan Tordjman, Christine Poitou, Gaël Guilhem, Jean Luc Bouillot, Danielle Hugol, Christiane Coussieu, Arnaud Basdevant, Avner Bar Hen, Pierre Bedossa, Michèle Guerre-Millo, Karine Clément
Diabetes Jun 2006, 55 (6) 1554-1561; DOI: 10.2337/db06-0133

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Increased Infiltration of Macrophages in Omental Adipose Tissue Is Associated With Marked Hepatic Lesions in Morbid Human Obesity
Raffaella Cancello, Joan Tordjman, Christine Poitou, Gaël Guilhem, Jean Luc Bouillot, Danielle Hugol, Christiane Coussieu, Arnaud Basdevant, Avner Bar Hen, Pierre Bedossa, Michèle Guerre-Millo, Karine Clément
Diabetes Jun 2006, 55 (6) 1554-1561; DOI: 10.2337/db06-0133
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