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Original Article

Open Access Gateway

Predictors of Subclinical Inflammatory Obesity: Plasma Levels of Leptin, Very Low-Density Lipoprotein Cholesterol and CD14 Expression of CD16+ Monocytes

Leite F.a,b,c · Leite Â.d · Santos A.b, c · Lima M.b, c · Barbosa J.e · Cosentino M.f · Ribeiro L.a,e,g

Author affiliations

aDepartment of Biochemistry, Faculty of Medicine, University of Porto, Porto, Portugal; bDepartment of Clinical Haematology, Centro Hospitalar do Porto, Porto, Portugal; cUMIB/ICBAS - Unit for Multidisciplinary Investigation in Biomedicine - Instituto de Ciências Biomédicas Abel Salazar, Porto, Portugal; dLusophone University of Oporto, Oporto, Portugal; eDepartment of Medical Education and Simulation, Faculty of Medicine, University of Porto, Porto, Portugal; fCenter of Research in Medical Pharmacology, University of Insubria, Varese, Italy; gI3S - Instituto de Investigação e Inovação em Saúde, Universidade do Porto, Porto, Portugal

Corresponding Author

Dr. Fernanda Leite

Department of Biochemistry, Faculty of Medicine

University of Porto

Alameda Prof. Hernani Monteiro, 4200-319 Porto, Portugal

fernandajtleite@hotmail.com

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Obes Facts 2017;10:308-322

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Abstract

Objective: Predictors of subclinical inflammatory obesity (SIO) can be important tools for early therapeutic interventions in obesity-related comorbidities. Waist circumference (WC) and BMI have different SIO sensitivity. We aimed to i) identify SIO predictors and ii) investigate whether CD16+ monocytes are associated with BMI- (generally) or WC-defined (centrally) obesity. Methods: Anthropometric and metabolic/endocrine (namely catecholamines, adrenaline and noradrenaline) parameters were evaluated, and CD16+ monocytes were studied by flow cytometry in the peripheral blood from 63 blood donors, and compared and correlated to each other. Multiple linear regression analysis was performed to identify variables that best predict SIO. Results: CD16+ monocyte counts were similar in BMI and WC groups. CD16+ monocytes from centrally obese (CO) showed a more inflammatory pattern, as compared to non-CO subjects. WC was sensitive to lipidemia and, in CO subjects, lipidemia was associated with a more inflammatory phenotype of CD16+ monocytes. These differences were not noticed between BMI groups. Adrenaline was correlated with CD16+ monocyte expansion with a lower inflammatory pattern. Leptin, very low-density lipoprotein cholesterol (VLDL-C), and CD14 expression of CD16+ monocytes were found to be CO predictors. Conclusions: WC-, but not BMI-defined obesity, was associated with a more inflammatory pattern of CD16+ monocytes, without monocyte expansion, suggesting that a monocyte maturation process rather than an independent arise of CD16+ monocytes occurs in CO. Thus, in a population with low cardiovascular risk, leptin, VLDL-C, and CD14 expression of CD16+ monocytes predict CO, constituting a putative tool for screening of SIO.

© 2017 The Author(s) Published by S. Karger GmbH, Freiburg


References

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  2. Kau AL, Ahern PP, Griffin NW, Goodman AL, Gordon JI: Human nutrition, the gut microbiome and the immune system. Nature 2011;474:327-336.
  3. Cancello R, Henegar C, Viguerie N, Taleb S, Poitou C, Rouault C, Coupaye M, Pelloux V, Hugol D, Bouillot JL, Bouloumié A, Barbatelli G, Cinti S, Svensson PA, Barsh GS, Zucker JD, Basdevant A, Langin D, Clément K: Reduction of macrophage infiltration and chemoattractant gene expression changes in white adipose tissue of morbidly obese subjects after surgery-induced weight loss. Diabetes 2005;54:2277-2286.
  4. Weisberg SP, McCann D, Desai M, Rosenbaum M, Leibel RL, Ferrante AW Jr: Obesity is associated with macrophage accumulation in adipose tissue. J Clin Invest 2003;112:1796-1808.
  5. Waterhouse DF, Cahill RA, Sheehan F, McCreery C: Prediction of calculated future cardiovascular disease by monocyte count in an asymptomatic population. Vasc Health Risk Manag 2008;4:177-187.
    External Resources
  6. Zimmermann MB, Aeberli I. Dietary determinants of subclinical inflammation, dyslipidemia and components of the metabolic syndrome in overweight children: a review. Int J Obes (Lond) 2008;32(suppl 6):S11-18.
  7. Deng T1, Lyon CJ, Bergin S, Caligiuri MA, Hsueh WA: Obesity, inflammation, and cancer. Annu Rev Pathol 2016;11:421-449.
  8. Klein S, Allison DB, Heymsfield SB, Kelley DE, Leibel RL, Nonas C, Kahn R: Waist circumference and cardiometabolic risk: a consensus statement from Shaping America's Health: Association for Weight Management and Obesity Prevention; NAASO, The Obesity Society; the American Society for Nutrition; and the American Diabetes Association. Am J Clin Nutr 2007;85:1197-1202.
    External Resources
  9. Enzi G, Gasparo M, BiondettiPR, Fiore D, Semisa M, Zurlo F: Subcutaneous and visceral fat distribution according to sex, age and overweight, evaluated by computed tomography. Am J Clin Nutr 1986;44:739-746.
    External Resources
  10. Xiong XQ, Chen WW, Zhu GQ: Adipose afferent reflex: sympathetic activation and obesity hypertension. Acta Physiol (Oxf) 2013;210:468-478.
  11. Flierl MA, Rittirsch D, Huber-Lang M: Catecholamines: crafty weapons in the inflammatory arsenal of immune/inflammatory cells or opening Pandora's box? Mol Med 2008;14:195-204.
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    External Resources
  21. Austin PC, Steyerberg EW: The number of subjects per variable required in linear regression analyses. J Clin Epidemiol 2015;68:627-636.
  22. Aeberli I, Molinari L, Spinas G, et al: Dietary intakes of fat and antioxidant vitamins are predictors of subclinical inflammation in overweight Swiss children. Am J Clin Nutr 2006;84:748-755.
    External Resources
  23. Goh LG, Dhaliwal SS, Welborn TA, et al: Anthropometric measurements of general and central obesity and the prediction of cardiovascular disease risk in women: a cross-sectional study. BMJ Open 2014;4:e004138.
  24. Naylor C, Petri WA Jr: Leptin regulation of immune responses. Trends Mol Med 2016;22:88-98.
  25. Howard BV, Ruotolo G, Robbins DC: Obesity and dyslipidemia. Endocrinol Metab Clin North Am 2003;32:855-867.
  26. Ziegler-Heitbrock L, Hofer TPJ: Toward a refined definition of monocyte subsets. Front Immunol. 2013;4:23.
  27. Frankenberger M, Hofer TPJ, Marei A, Dayyani F, Schewe S, Strasser C, Aldraihim A, Stanzel F, Lang R, Hoffmann R, Prazeres da Costa O, Buch T, Ziegler-Heitbrock L: Transcript profiling of CD16-positive monocytes reveals a unique molecular fingerprint. Eur J Immunol 2012;42:957-974.
  28. Mukherjee R, Kanti Barman P, Kumar Thatoi P, Tripathy R, Kumar Das B, Ravindran B: Non-classical monocytes display inflammatory features: validation in sepsis and systemic lupus erythematous. Sci Rep 2015;5:13886.
  29. Kittner JM, Jacobs R, Pawlak CR, Heijnen CJ, Schedlowski M, Schmidt RE: Adrenaline-induced immunological changes are altered in patients with rheumatoid arthritis. Rheumatology 2002;41:1031-1039.
  30. Min D, Brooks B, Wong J, Salomon R, Bao W, Harrisberg B, Twigg SM, Yue DK, McLennan SV: Alterations in monocyte CD16 in association with diabetes complications. Mediators Inflamm 2012;649083. doi: 10.1155/2012/649083.
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  32. Berg KE, Ljungcrantz I, Andersson L, Bryngelsson C, Hedblad B, Fredrikson GN, Nilsson J, Björkbacka H: Elevated CD14++CD16- monocytes predict cardiovascular events. Circ Cardiovasc Genet 2012;5:122-131.
  33. Cifarelli V, Libman IM, Deluca A, Becker D, Trucco M, Luppi P: Increased expression of monocyte CD11b (Mac-1) in overweight recent-onset type 1 diabetic children. Rev Diabet Stud 2007;4:112-117.
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  37. Buckman LB, Hasty AH, Flaherty DK, Buckman CT, Thompson MM, Matlock BK, Weller K, Ellacott KL: Obesity induced by a high-fat diet is associated with increased immune cell entry into the central nervous system. Brain Behav Immun 2014;35:33-42.
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  42. Sarigianni M, Bekiari E, Tsapas A, Kaloyianni M, Koliakos G, Paletas K: Effect of leptin and insulin resistance on properties of human monocytes in lean and obese healthy participants. Angiology 2010;61:768-774.
  43. Rickles AS, Iannuzzi JC, Mironov O, Deeb AP, Sharma A, Fleming FJ, Monson JR: Visceral obesity and colorectal cancer: are we missing the boat with BMI? J Gastrointest Surg 2013;17:133-143; discussion p.143.
  44. Steppich B, Dayyani F, Gruber R, Lorenz R, Mack M, Ziegler-Heitbrock HW: Selective mobilization of CD14(+)CD16(+) monocytes by exercise. Am J Physiol Cell Physiol 2000;279:C578-586.
    External Resources
  45. Teraguchi I, Imanishi T, Ozaki Y, Tanimoto T, Orii M, Shiono Y, Shimamura K, Ishibashi K, Yamano T, Ino Y, Yamaguchi T, Hirata K, Kubo T, Akasaka T: Impact of glucose fluctuation and monocyte subsets on coronary plaque rupture. Nutr Metab Cardiovasc Dis 2014;24:309-314.
  46. Takahashi HK, Mori S, Liu K, Wake H, Zhang J, Liu R, Yoshino T, Nishibori M: Beta2-adrenoceptor stimulation inhibits advanced glycation end products-induced adhesion molecule expression and cytokine production in human peripheral blood mononuclear cells. Eur J Pharmacol 2010;627:313-317.
  47. Scanzano A, Cosentino M: Adrenergic regulation of innate immunity: a review. Front Pharmacol. 2015;6:171.
  48. Browning LM, Krebs JD, Magee EC, Frühbeck G, Jebb SA: Circulating markers of inflammation and their link to indices of adiposity. Obes Facts 2008;1:259-265.
  49. Rossi IA, Bochud M, Bovet P, Paccaud F, Waeber G, Vollenweider P, Taffé P: Sex difference and the role of leptin in the association between high-sensitivity C-reactive protein and adiposity in two different populations. Eur J Epidemiol 2012;27:379-384.
  50. Thorand B, Baumert J, Döring A, Herder C, Kolb H, Rathmann W, Giani G, Koenig W; KORA Group: Sex differences in the relation of body composition to markers of inflammation. Atherosclerosis 2006;184:216-224.
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Article / Publication Details

First-Page Preview
Abstract of Original Article

Received: August 31, 2016
Accepted: February 15, 2017
Published online: July 22, 2017
Issue release date: August 2017

Number of Print Pages: 15
Number of Figures: 2
Number of Tables: 4

ISSN: 1662-4025 (Print)
eISSN: 1662-4033 (Online)

For additional information: https://www.karger.com/OFA

References

  1. Hotamisligil GS: Inflammation and metabolic disorders. Nature 2006;444:860-867.
  2. Kau AL, Ahern PP, Griffin NW, Goodman AL, Gordon JI: Human nutrition, the gut microbiome and the immune system. Nature 2011;474:327-336.
  3. Cancello R, Henegar C, Viguerie N, Taleb S, Poitou C, Rouault C, Coupaye M, Pelloux V, Hugol D, Bouillot JL, Bouloumié A, Barbatelli G, Cinti S, Svensson PA, Barsh GS, Zucker JD, Basdevant A, Langin D, Clément K: Reduction of macrophage infiltration and chemoattractant gene expression changes in white adipose tissue of morbidly obese subjects after surgery-induced weight loss. Diabetes 2005;54:2277-2286.
  4. Weisberg SP, McCann D, Desai M, Rosenbaum M, Leibel RL, Ferrante AW Jr: Obesity is associated with macrophage accumulation in adipose tissue. J Clin Invest 2003;112:1796-1808.
  5. Waterhouse DF, Cahill RA, Sheehan F, McCreery C: Prediction of calculated future cardiovascular disease by monocyte count in an asymptomatic population. Vasc Health Risk Manag 2008;4:177-187.
    External Resources
  6. Zimmermann MB, Aeberli I. Dietary determinants of subclinical inflammation, dyslipidemia and components of the metabolic syndrome in overweight children: a review. Int J Obes (Lond) 2008;32(suppl 6):S11-18.
  7. Deng T1, Lyon CJ, Bergin S, Caligiuri MA, Hsueh WA: Obesity, inflammation, and cancer. Annu Rev Pathol 2016;11:421-449.
  8. Klein S, Allison DB, Heymsfield SB, Kelley DE, Leibel RL, Nonas C, Kahn R: Waist circumference and cardiometabolic risk: a consensus statement from Shaping America's Health: Association for Weight Management and Obesity Prevention; NAASO, The Obesity Society; the American Society for Nutrition; and the American Diabetes Association. Am J Clin Nutr 2007;85:1197-1202.
    External Resources
  9. Enzi G, Gasparo M, BiondettiPR, Fiore D, Semisa M, Zurlo F: Subcutaneous and visceral fat distribution according to sex, age and overweight, evaluated by computed tomography. Am J Clin Nutr 1986;44:739-746.
    External Resources
  10. Xiong XQ, Chen WW, Zhu GQ: Adipose afferent reflex: sympathetic activation and obesity hypertension. Acta Physiol (Oxf) 2013;210:468-478.
  11. Flierl MA, Rittirsch D, Huber-Lang M: Catecholamines: crafty weapons in the inflammatory arsenal of immune/inflammatory cells or opening Pandora's box? Mol Med 2008;14:195-204.
  12. Than A, Ye F, Xue R, Ong JW, Poh CL, Chen P: The crosstalks between adipokines and catecholamines. Mol Cell Endocrinol 2011;332:261-270.
  13. Ziegler-Heitbrock L: The CD14+ CD16+ blood monocytes: their role in infection and inflammation. J Leukoc Biol 2007;81:584-592.
  14. Wong KL, Tai JJ, Wong WC, Han H, Sem X, Yeap WH, Kourilsky P, Wong SC: Gene expression profiling reveals the defining features of the classical, intermediate, and nonclassical human monocyte subsets. Blood 2011;118:e16-e31.
  15. Heine GH, Ortiz A, Massy ZA, Lindholm B, Wiecek A, Martínez-Castelao A, Covic A, Goldsmith D, Süleymanlar G, London GM, Parati G, Sicari R, Zoccali C, Fliser D; European Renal and Cardiovascular Medicine (EURECA‑m) Working Group of the European Renal Association-European Dialysis and Transplant Association (ERA-EDTA): Monocyte subpopulations and cardiovascular risk in chronic kidney disease. Nat Rev Nephrol 2012;8:362-369.
  16. Rogacev KS, Ulrich C, Blömer L, Hornof F, Oster K, Ziegelin M, Cremers B, Grenner Y, Geisel J, Schlitt A, Köhler H, Fliser D, Girndt M, Heine GH: Monocyte heterogeneity in obesity and subclinical atherosclerosis. Eur Heart J 2010;31:369-376.
  17. Leite F, Lima M, Marino F, Cosentino M, Ribeiro L: Dopaminergic Receptors and tyrosine hydroxylase expression in peripheral blood mononuclear cells: a distinct pattern in central obesity. PLoS One 2016;11:e0147483.
  18. International Diabetes Federation: The IDF Consensus Worldwide Definition of the Metabolic Syndrome. www.idf.org/e-library/consensus-statements/60-idfconsensus-worldwide-definitionof-the-metabolic-syndrome (last accessed July 13, 2017).
  19. Pearson TA, Mensah GA, Alexander RW, Anderson JL, Cannon RO 3rd, Criqui M, Fadl YY, Fortmann SP, Hong Y, Myers GL, Rifai N, Smith SC Jr, Taubert K, Tracy RP, Vinicor F; Centers for Disease Control and Prevention; American Heart Association: Markers of inflammation and cardiovascular disease: application to clinical and public health practice: a statement for healthcare professionals from the Centers for Disease Control and Prevention and the American Heart Association. Circulation 2003;107:499-511.
  20. Lima M, Almeida J, Montero AG, Teixeira Mdos A, Queirós ML, Santos AH, Balanzategui A, Estevinho A, Algueró Mdel C, Barcena P, Fonseca S, Amorim ML, Cabeda JM, Pinho L, Gonzalez M, San Miguel J, Justiça B, Orfão A: Clinicobiological, immunophenotypic, and molecular characteristics of monoclonal CD56-/+dim chronic natural killer cell large granular lymphocytosis. Am J Pathol 2004;165:1117-1127.
    External Resources
  21. Austin PC, Steyerberg EW: The number of subjects per variable required in linear regression analyses. J Clin Epidemiol 2015;68:627-636.
  22. Aeberli I, Molinari L, Spinas G, et al: Dietary intakes of fat and antioxidant vitamins are predictors of subclinical inflammation in overweight Swiss children. Am J Clin Nutr 2006;84:748-755.
    External Resources
  23. Goh LG, Dhaliwal SS, Welborn TA, et al: Anthropometric measurements of general and central obesity and the prediction of cardiovascular disease risk in women: a cross-sectional study. BMJ Open 2014;4:e004138.
  24. Naylor C, Petri WA Jr: Leptin regulation of immune responses. Trends Mol Med 2016;22:88-98.
  25. Howard BV, Ruotolo G, Robbins DC: Obesity and dyslipidemia. Endocrinol Metab Clin North Am 2003;32:855-867.
  26. Ziegler-Heitbrock L, Hofer TPJ: Toward a refined definition of monocyte subsets. Front Immunol. 2013;4:23.
  27. Frankenberger M, Hofer TPJ, Marei A, Dayyani F, Schewe S, Strasser C, Aldraihim A, Stanzel F, Lang R, Hoffmann R, Prazeres da Costa O, Buch T, Ziegler-Heitbrock L: Transcript profiling of CD16-positive monocytes reveals a unique molecular fingerprint. Eur J Immunol 2012;42:957-974.
  28. Mukherjee R, Kanti Barman P, Kumar Thatoi P, Tripathy R, Kumar Das B, Ravindran B: Non-classical monocytes display inflammatory features: validation in sepsis and systemic lupus erythematous. Sci Rep 2015;5:13886.
  29. Kittner JM, Jacobs R, Pawlak CR, Heijnen CJ, Schedlowski M, Schmidt RE: Adrenaline-induced immunological changes are altered in patients with rheumatoid arthritis. Rheumatology 2002;41:1031-1039.
  30. Min D, Brooks B, Wong J, Salomon R, Bao W, Harrisberg B, Twigg SM, Yue DK, McLennan SV: Alterations in monocyte CD16 in association with diabetes complications. Mediators Inflamm 2012;649083. doi: 10.1155/2012/649083.
  31. Fogelstrand L, Hulthe J, Hulten LM, Wiklund O, Fagerberg B. Monocytic expression of CD14 and CD18, circulating adhesion molecules and inflammatory markers in women with diabetes mellitus and impaired glucose tolerance. Diabetologia 2004;47:1948-1952.
  32. Berg KE, Ljungcrantz I, Andersson L, Bryngelsson C, Hedblad B, Fredrikson GN, Nilsson J, Björkbacka H: Elevated CD14++CD16- monocytes predict cardiovascular events. Circ Cardiovasc Genet 2012;5:122-131.
  33. Cifarelli V, Libman IM, Deluca A, Becker D, Trucco M, Luppi P: Increased expression of monocyte CD11b (Mac-1) in overweight recent-onset type 1 diabetic children. Rev Diabet Stud 2007;4:112-117.
  34. Kennedy DJ, Kuchibhotla S, Westfall KM, Silverstein RL, Morton RE, Febbraio M: A CD36-dependent pathway enhances macrophage and adipose tissue inflammation and impairs insulin signalling. Cardiovasc Res 2011;89:604-613.
  35. Sun Y, Scavini M, Orlando RA, Murata GH, Servilla KS, Tzamaloukas AH, Schrader R, Bedrick EJ, Burge MR, Abumrad NA, Zager PG: Increased CD36 expression signals monocyte activation among patients with type 2 diabetes. Diabetes Care 2010;33:2065-2067.
  36. Zheng C, Yang Q, Xu C, Shou P, Cao J, Jiang M, Chen Q, Cao G, Han Y, Li F, Cao W, Zhang L, Zhang L, Shi Y, Wang Y: CD11b regulates obesity-induced insulin resistance via limiting alternative activation and proliferation of adipose tissue macrophages. Proc Natl Acad Sci U S A 2015;112:E7239-7248.
  37. Buckman LB, Hasty AH, Flaherty DK, Buckman CT, Thompson MM, Matlock BK, Weller K, Ellacott KL: Obesity induced by a high-fat diet is associated with increased immune cell entry into the central nervous system. Brain Behav Immun 2014;35:33-42.
  38. Figueroa-Vega N, Moreno-Frías C, Malacara JM: Alterations in adhesion molecules, pro-inflammatory postmenopausal women. PLoS One 2015;10:e0120990.
  39. Thaler B, Hohensinner PJ, Krychtiuk KA, Matzneller P, Koller L, Brekalo M, Maurer G, Huber K, Zeitlinger M, Jilma B, Wojta J, Speidl WS: Differential in vivo activation of monocyte subsets during low-grade inflammation through experimental endotoxemia in humans. Sci Rep 2016;6:30162.
  40. Takeda Y, Marumo M, Wakabayashi I: Attenuated phagocytic activity of monocytes in type 2 diabetic Goto-Kakizaki rats. Immunobiology 2011;216:1094-1102.
  41. Gómez-Bañuelos E, Martín-Márquez BT, Martínez-García EA, Figueroa-Sanchez M, Nuñez-Atahualpa L, Rocha-Muñoz AD, Sánchez-Hernández PE, Navarro-Hernandez RE, Madrigal-Ruiz PM, Saldaña-Millan AA, Duran-Barragan S, Gonzalez-Lopez L, Gamez-Nava JI, Vázquez-Del Mercado M: Low levels of CD36 in peripheral blood monocytes in subclinical atherosclerosis in rheumatoid arthritis: a cross-sectional study in a Mexican population. Biomed Res Int 2014;736786.
  42. Sarigianni M, Bekiari E, Tsapas A, Kaloyianni M, Koliakos G, Paletas K: Effect of leptin and insulin resistance on properties of human monocytes in lean and obese healthy participants. Angiology 2010;61:768-774.
  43. Rickles AS, Iannuzzi JC, Mironov O, Deeb AP, Sharma A, Fleming FJ, Monson JR: Visceral obesity and colorectal cancer: are we missing the boat with BMI? J Gastrointest Surg 2013;17:133-143; discussion p.143.
  44. Steppich B, Dayyani F, Gruber R, Lorenz R, Mack M, Ziegler-Heitbrock HW: Selective mobilization of CD14(+)CD16(+) monocytes by exercise. Am J Physiol Cell Physiol 2000;279:C578-586.
    External Resources
  45. Teraguchi I, Imanishi T, Ozaki Y, Tanimoto T, Orii M, Shiono Y, Shimamura K, Ishibashi K, Yamano T, Ino Y, Yamaguchi T, Hirata K, Kubo T, Akasaka T: Impact of glucose fluctuation and monocyte subsets on coronary plaque rupture. Nutr Metab Cardiovasc Dis 2014;24:309-314.
  46. Takahashi HK, Mori S, Liu K, Wake H, Zhang J, Liu R, Yoshino T, Nishibori M: Beta2-adrenoceptor stimulation inhibits advanced glycation end products-induced adhesion molecule expression and cytokine production in human peripheral blood mononuclear cells. Eur J Pharmacol 2010;627:313-317.
  47. Scanzano A, Cosentino M: Adrenergic regulation of innate immunity: a review. Front Pharmacol. 2015;6:171.
  48. Browning LM, Krebs JD, Magee EC, Frühbeck G, Jebb SA: Circulating markers of inflammation and their link to indices of adiposity. Obes Facts 2008;1:259-265.
  49. Rossi IA, Bochud M, Bovet P, Paccaud F, Waeber G, Vollenweider P, Taffé P: Sex difference and the role of leptin in the association between high-sensitivity C-reactive protein and adiposity in two different populations. Eur J Epidemiol 2012;27:379-384.
  50. Thorand B, Baumert J, Döring A, Herder C, Kolb H, Rathmann W, Giani G, Koenig W; KORA Group: Sex differences in the relation of body composition to markers of inflammation. Atherosclerosis 2006;184:216-224.
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