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Cardiovascular and Metabolic Risk

Plasma Lipidomic Profiling and Risk of Type 2 Diabetes in the PREDIMED Trial

  1. Cristina Razquin1,2,3,
  2. Estefanía Toledo1,2,3,
  3. Clary B. Clish4,
  4. Miguel Ruiz-Canela1,2,3,
  5. Courtney Dennis4,
  6. Dolores Corella3,5,
  7. Christopher Papandreou3,6,
  8. Emilio Ros3,7,
  9. Ramon Estruch3,8,
  10. Marta Guasch-Ferré3,6,9,
  11. Enrique Gómez-Gracia3,10,
  12. Montserrat Fitó3,11,
  13. Edward Yu9,
  14. José Lapetra3,12,
  15. Dong Wang9,
  16. Dora Romaguera3,13,
  17. Liming Liang14,15,
  18. Angel Alonso-Gómez3,16,
  19. Amy Deik4,
  20. Mónica Bullo3,6,
  21. Lluis Serra-Majem3,17,
  22. Jordi Salas-Salvadó3,6,
  23. Frank B. Hu9,18 and
  24. Miguel A. Martínez-González1,2,3,9⇑
  1. 1Department of Preventive Medicine and Public Health, University of Navarra, Pamplona, Spain
  2. 2IdiSNA, Navarra Institute for Health Research, Pamplona, Spain
  3. 3CIBER Fisiopatología de la Obesidad y Nutrición (CIBERObn), Instituto de Salud Carlos III, Madrid, Spain
  4. 4Broad Institute of MIT and Harvard University, Cambridge, MA
  5. 5Department of Preventive Medicine, University of Valencia, Valencia, Spain
  6. 6Human Nutrition Unit, Faculty of Medicine and Health Sciences, Institut d’Investigació Sanitària Pere Virgili, Rovira i Virgili University, Reus, Spain
  7. 7Lipid Clinic, Department of Endocrinology and Nutrition, Institut d’Investigacions Biomediques August Pi Sunyer (IDI-BAPS), Hospital Clinic, University of Barcelona, Barcelona, Spain
  8. 8Department of Internal Medicine, Institut d’Investigacions Biomediques August Pi Sunyer (IDI-BAPS), Barcelona, Spain
  9. 9Department of Nutrition, Harvard T.H. Chan School of Public Health, Boston, MA
  10. 10Department of Preventive Medicine, University of Malaga, Malaga, Spain
  11. 11Cardiovascular and Nutrition Research Group, Institut de Recerca Hospital del Mar, Barcelona, Spain
  12. 12Research Unit, Department of Family Medicine, Distrito Sanitario Atención Primaria Sevilla, Seville, Spain
  13. 13Instituto de Investigación Sanitaria Illes Balears (IdISBa), University Hospital of Son Espases, Palma de Mallorca, Spain
  14. 14Department of Epidemiology, Harvard T.H. Chan School of Public Health, Boston, MA
  15. 15Department of Biostatistics, Harvard T.H. Chan School of Public Health, Boston, MA
  16. 16Department of Cardiology, University Hospital of Alava, Vitoria, Spain
  17. 17Research Institute of Biomedical and Health Sciences (IUIBS), University of Las Palmas de Gran Canaria, and Service of Preventive Medicine, Complejo Hospitalario Universitario Insular Materno Infantil (CHUIMI), Canary Health Service, Las Palmas de Gran Canaria, Spain
  18. 18Channing Division for Network Medicine, Department of Medicine, Brigham and Women’s Hospital and Harvard Medical School, Boston, MA
  1. Corresponding author: Miguel A. Martínez-González, mamartinez{at}unav.es.
Diabetes Care 2018 Dec; 41(12): 2617-2624. https://doi.org/10.2337/dc18-0840
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    Figure 1

    A: HRs per 1-SD increase in baseline lipid concentration for lipid groups inversely associated with T2D. Lipid species were inverse normally transformed, and HRs were calculated from weighted Cox models adjusted for age, sex, intervention group, BMI, smoking, hypertension, dyslipidemia, and baseline glucose (linear and quadratic term). B: HRs per 1-SD increase in baseline lipid concentration for lipid groups directly associated with T2D. Lipid species were inverse normally transformed, and HRs were calculated from weighted Cox models adjusted for age, sex, intervention group, BMI, smoking, hypertension, dyslipidemia, and baseline glucose (linear and quadratic term). C: HRs for T2D per 1 SD for the residual of each TAG over the total content of the considered TAG. Lipid species were inverse normally transformed before calculating the residual, and HRs were calculated from weighted Cox models adjusted for age, sex, intervention group, BMI, smoking, hypertension, dyslipidemia, and baseline glucose (linear and quadratic term).

Tables

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  • Table 1

    Baseline characteristics of study participants according to outcome status

    Subcohort (n = 692)aCase subjects with T2D (n = 250)
    Age (years)66.5 (5.7)66.4 (5.7)
    Women (%)6355.2
    BMI (kg/m2)29.9 (3.6)30.8 (3.3)
    Waist circumference (cm)100 (11)103 (10)
    LTPA (METS-min/day)238 (238)249 (234)
    Fasting glucose (mg/dL)98 (14)117 (18)
    HDL cholesterol (mg/dL)56.9 (14.2)52.8 (11.6)
    LDL cholesterol (mg/dL)138.3 (30.5)135.0 (30.2)
    Total cholesterol (mg/dL)219.9 (35.6)218.4 (39.1)
    Triglycerides (mg/dL)129.8 (92.2–149.3)b160.9 (109–180)b
    Dyslipidemia (%)8580
    Hypertension (%)9196
    Smoking
     Nonsmoker (%)6153
     Current smoker (%)1625
     Former smoker (%)2322
    Total energy intake (kcal/day)2,276 (564)2,321 (616)
    Adherence to MedDiet8.6 (2.0)8.4 (2.0)
    Intervention group (%)
     Control (%)3236
     MedDiet + EVOO (%)3130
     MedDiet + nuts (%)3734
    • Data are mean (SD) unless otherwise indicated. LTPA, leisure-time physical activity.

    • ↵aIncluding 53 overlapping cases.

    • ↵bMedian (interquartile range).

  • Table 2

    Association between baseline lipid factors (PCA extracted) and T2D risk (adjusted for age, sex, and intervention group)

    Quartiles of factorsLinear trendPer SD increase
    Q1Q2Q3Q4
    Factor 3*Ref0.62 (0.37–1.05)0.79 (0.47–1.32)0.45 (0.26–0.79)0.0030.70 (0.57–0.85)
    Factor 7*Ref0.62 (0.39–0.97)0.39 (0.23–0.67)0.36 (0.20–0.63)<0.0010.58 (0.49–0.70)
    Factor 10*Ref0.80 (0.48–1.33)0.48 (0.28–0.81)0.56 (0.33–0.95)0.0120.74 (0.62–0.88)
    Factor 13*Ref1.00 (0.61–1.66)0.78 (0.47–1.32)0.58 (0.34–1.00)0.1660.93 (0.78–1.10)
    Factor 1*Ref1.39 (0.77–2.52)2.24 (1.29–3.88)2.72 (1.59–4.66)<0.0011.62 (1.36–1.92)
    Factor 5*Ref1.44 (0.83–2.45)1.14 (0.65–2.00)2.22 (1.31–3.77)0.0221.24 (1.04–1.47)
    Factor 11*Ref1.25 (0.72–2.18)1.78 (1.03–3.10)2.02 (1.15–3.54)0.0091.18 (0.99–1.40)
    • Data are HR (95% CI) unless otherwise indicated. Boldface type indicates P values <0.05 for the association with T2D (HR). Ref, reference; Q, quartile.

    • ↵*Additionally adjusted for the rest of the factors (1–15).

  • Table 3

    Association between baseline lipid scores and T2D risk

    Quartiles of scoresLinear trendPer SD
    Q1Q2Q3Q4
    LP score (LPCs and LPEs); n molecules = 18
     M1*Ref0.82 (0.56–1.19)0.49 (0.32–0.75)0.46 (0.29–0.71)<0.0010.73 (0.63–0.85)
     M2*Ref0.86 (0.58–1.27)0.48 (0.31–0.76)0.51 (0.32–0.81)<0.0010.74 (0.63–0.87)
     M3*Ref1.09 (0.69–1.73)0.54 (0.30–0.97)0.66 (0.38–1.16)0.0400.79 (0.65–0.96)
    PC-PL score; n molecules = 15
     M1*Ref0.78 (0.53–1.17)0.77 (0.52–1.16)0.36 (0.22–0.58)<0.0010.78 (0.68–0.90)
     M2*Ref0.80 (0.53–1.21)0.81 (0.54–1.22)0.38 (0.23–0.64)0.0010.82 (0.71–0.95)
     M3*Ref0.81 (0.49–1.33)0.66 (0.39–1.09)0.37 (0.20–0.68)0.0010.76 (0.62–0.92)
    SM score; n molecules = 11
     M1*Ref0.49 (0.32–0.75)0.58 (0.38–0.89)0.32 (0.19–0.54)<0.0010.67 (0.56–0.80)
     M2*Ref0.46 (0.30–0.72)0.56 (0.35–0.87)0.31 (0.18–0.52)<0.0010.69 (0.57–0.83)
     M3*Ref0.30 (0.17–0.52)0.51 (0.30–0.88)0.24 (0.13–0.45)<0.0010.67 (0.54–0.84)
    CE score; n molecules = 13
     M1*Ref0.76 (0.50–1.14)0.64 (0.43–0.95)0.34 (0.21–0.54)<0.0010.68 (0.58–0.79)
     M2*Ref0.87 (0.56–1.35)0.74 (0.49–1.12)0.39 (0.24–0.65)<0.0010.70 (0.59–0.84)
     M3*Ref0.64 (0.36–1.15)0.56 (0.34–0.91)0.40 (0.22–0.74)0.0020.68 (0.56–0.83)
    TAG score (≤56 C and ≤3 double bonds); n molecules = 40
     M1*Ref1.73 (1.06–2.83)2.18 (1.35–3.51)2.94 (1.85–4.67)<0.0011.49 (1.27–1.75)
     M2*Ref1.77 (1.06–2.94)2.10 (1.28–3.43)2.55 (1.58–4.11)<0.0011.39 (1.18–1.64)
     M3*Ref1.60 (0.82–3.14)2.01 (1.04–3.86)2.02 (1.05–3.87)0.0441.23 (1.00–1.52)
    DAG score; n molecules = 14
     M1*Ref1.14 (0.70–1.86)2.13 (1.35–3.36)2.76 (1.77–4.29)<0.0011.58 (1.33–1.86)
     M2*Ref1.25 (0.75–2.08)1.95 (1.21–3.14)2.46 (1.56–3.88)<0.0011.48 (1.24–1.77)
     M3*Ref1.18 (0.61–2.30)1.52 (0.84–2.74)1.93 (1.10–3.37)0.0081.31 (1.07–1.61)
    PE score; n molecules = 12
     M1*Ref1.51 (0.95–2.39)1.57 (0.95–2.39)2.55 (1.64–3.95)<0.0011.45 (1.23–1.70)
     M2*Ref1.43 (0.89–2.31)1.48 (0.92–2.38)2.13 (1.35–3.35)0.0011.35 (1.15–1.59)
     M3*Ref1.30 (0.74–2.78)0.95 (0.52–2.42)1.39 (0.80–2.42)0.3211.13 (0.93–1.37)
    • Data are HR (95% CI) unless otherwise indicated. Boldface type indicates P values <0.05 for the association with T2D (HR).

    • ↵*M1: adjusted for age, sex, and intervention group; M2: M1 additionally adjusted for BMI, smoking, hypertension, and dyslipidemia; M3: M2 additionally adjusted for baseline glucose (linear and quadratic term). Ref, reference; Q, quartile.

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Plasma Lipidomic Profiling and Risk of Type 2 Diabetes in the PREDIMED Trial
Cristina Razquin, Estefanía Toledo, Clary B. Clish, Miguel Ruiz-Canela, Courtney Dennis, Dolores Corella, Christopher Papandreou, Emilio Ros, Ramon Estruch, Marta Guasch-Ferré, Enrique Gómez-Gracia, Montserrat Fitó, Edward Yu, José Lapetra, Dong Wang, Dora Romaguera, Liming Liang, Angel Alonso-Gómez, Amy Deik, Mónica Bullo, Lluis Serra-Majem, Jordi Salas-Salvadó, Frank B. Hu, Miguel A. Martínez-González
Diabetes Care Dec 2018, 41 (12) 2617-2624; DOI: 10.2337/dc18-0840

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Plasma Lipidomic Profiling and Risk of Type 2 Diabetes in the PREDIMED Trial
Cristina Razquin, Estefanía Toledo, Clary B. Clish, Miguel Ruiz-Canela, Courtney Dennis, Dolores Corella, Christopher Papandreou, Emilio Ros, Ramon Estruch, Marta Guasch-Ferré, Enrique Gómez-Gracia, Montserrat Fitó, Edward Yu, José Lapetra, Dong Wang, Dora Romaguera, Liming Liang, Angel Alonso-Gómez, Amy Deik, Mónica Bullo, Lluis Serra-Majem, Jordi Salas-Salvadó, Frank B. Hu, Miguel A. Martínez-González
Diabetes Care Dec 2018, 41 (12) 2617-2624; DOI: 10.2337/dc18-0840
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