Skip to main content
SpringerLink
Log in

Contribution of gender and body fat distribution to inflammatory marker concentrations in apparently healthy young adults

  • Original Research Paper
  • Published:
Inflammation Research Aims and scope Submit manuscript

Abstract

Objective

This cross-sectional study assessed the potential contribution of gender, body fat distribution, and their interactions to some inflammatory marker concentrations [C-reactive protein (CRP), complement factor 3 (C3), and ceruloplasmin (Cp)] in young adults.

Methods

Measurements included body composition, lifestyle features, blood biochemical and selected inflammatory markers on 317 healthy subjects [122 males/195 females; 22 ± 3 years; 22.1 ± 2.8 kg/m2 (mean ± SD)].

Results

Women had significantly higher CRP and Cp concentrations than men. No gender difference was noted in C3 concentrations. In a multivariate model of the whole sample, body fat (BF), waist circumference (WC) and the sex × WC interaction term presented the highest R 2 for variance of CRP (11%), C3 (2%), and Cp (12%), respectively. In regression models separated by sex, BF was the adiposity indicator that explained the variability of CRP in men (13%) and women (7%). WC was the only variable significantly associated with C3 concentrations in women (3%). BF presented the highest partial R 2 for Cp in men (8%) and WC in women (16%).

Conclusion

Our findings indicate a relevant interaction between gender and body fat distribution on the variance of CRP, C3, and Cp concentrations in apparently healthy young adults.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  1. Moreno-Aliaga MJ, Campión J, Milagro FI, Berjón A, Martínez JA. Adiposity and proinflammatory state: the chicken or the egg. Adipocytes. 2005;1:1–16.

    Google Scholar 

  2. Volp AC, Alfenas Rde C, Costa NM, Minim VP, Stringueta PC, Bressan J. Inflammation biomarkers capacity in predicting the metabolic syndrome. Arq Bras Endocrinol Metabol. 2008;52:537–49.

    Article  PubMed  Google Scholar 

  3. Zulet MA, Puchau B, Navarro C, Marti A, Martínez JA. Inflammatory biomarkers: the link between obesity and associated pathologies. Nutr Hosp. 2007;22:511–27.

    PubMed  CAS  Google Scholar 

  4. Engström G, Hedblad B, Eriksson KF, Janzon L, Lindgarde F. Complement C3 is a risk factor for the development of diabetes: a population-based cohort study. Diabetes. 2005;54:570–5.

    Article  PubMed  Google Scholar 

  5. Festa A, D’Agostino R Jr, Williams K, Karter AJ, Mayer-Davis EJ, Tracy RP, et al. The relation of body fat mass and distribution to markers of chronic inflammation. Int J Obes Relat Metab Disord. 2001;25:1407–15.

    Article  PubMed  CAS  Google Scholar 

  6. Kim OY, Shin MJ, Moon J, Chung JH. Plasma ceruloplasmin as a biomarker for obesity: a proteomic approach. Clin Biochem. 2011;44:351–6.

    Article  PubMed  CAS  Google Scholar 

  7. Puchau B, Zulet MA, González de Echavarri A, Navarro-Blasco I, Martínez JA. Selenium intake reduces serum C3, an early marker of metabolic syndrome manifestations, in healthy young adults. Eur J Clin Nutr. 2009;63:858–64.

    Article  PubMed  CAS  Google Scholar 

  8. Choi EY, Park EH, Cheong YS, Rheem I, Park SG, Yoo S. Association of C-reactive protein with the metabolic risk factors among young and middle-aged Koreans. Metabolism. 2006;55:415–21.

    Article  PubMed  CAS  Google Scholar 

  9. Engström G, Hedblad B, Tyden P, Lindgarde F. Inflammation-sensitive plasma proteins are associated with increased incidence of heart failure: a population-based cohort study. Atherosclerosis. 2009;202:617–22.

    Article  PubMed  Google Scholar 

  10. Wang B, Li Q, Jiang Y, Liu Z, Zhong L, Luo R, et al. Serum complement C3 has a stronger association with insulin resistance than high sensitive C-reactive protein in non-diabetic Chinese. Inflamm Res. 2011;60:63–8.

    Article  PubMed  CAS  Google Scholar 

  11. Baumann H, Gauldie J. Regulation of hepatic acute phase plasma protein genes by hepatocyte stimulating factors and other mediators of inflammation. Mol Biol Med. 1990;7:147–59.

    PubMed  CAS  Google Scholar 

  12. Eder K, Baffy N, Falus A, Fulop AK. The major inflammatory mediator interleukin-6 and obesity. Inflamm Res. 2009;58:727–36.

    Article  PubMed  CAS  Google Scholar 

  13. Hermsdorff HHM, Puchau B, Zulet MA, Martínez JA. Association of body fat distribution with proinflammatory gene expression in peripheral blood mononuclear cells from young adult subjects. OMICS. 2010;14:297–307.

    Article  PubMed  CAS  Google Scholar 

  14. Hermsdorff HHM, Zulet MA, Puchau B, Martínez JA. Central adiposity rather than total adiposity measurements are specifically involved in the inflammatory status from healthy young adults. Inflammation. 2011;34:161–70.

    Article  PubMed  CAS  Google Scholar 

  15. Lapice E, Maione S, Patti L, Cipriano P, Rivellese AA, Riccardi G, et al. Abdominal adiposity is associated with elevated C-reactive protein independent of BMI in healthy nonobese people. Diabetes Care. 2009;32:1734–6.

    Article  PubMed  CAS  Google Scholar 

  16. Forsythe LK, Wallace JM, Livingstone MB. Obesity and inflammation: the effects of weight loss. Nutr Res Rev. 2008;21:117–33.

    Article  PubMed  CAS  Google Scholar 

  17. Hermsdorff HHM, Zulet MA, Bressan J, Martínez-González MA, Martínez JA. Impact of caloric restriction and Mediterranean food-based diets on inflammation accompanying obesity and metabolic syndrome features. Obes Metab. 2009;5:69–77.

    Google Scholar 

  18. Vague J. Sexual differentiation. A determinant factor of the forms of obesity. 1947. Obes Res. 1996;4:201–3.

    PubMed  CAS  Google Scholar 

  19. Lemieux S, Prud’homme D, Bouchard C, Tremblay A, Després JP. Sex differences in the relation of visceral adipose tissue accumulation to total body fatness. Am J Clin Nutr. 1993;58:463–7.

    PubMed  CAS  Google Scholar 

  20. Cartier A, Cote M, Lemieux I, Perusse L, Tremblay A, Bouchard C, et al. Sex differences in inflammatory markers: what is the contribution of visceral adiposity? Am J Clin Nutr. 2009;89:1307–14.

    Article  PubMed  CAS  Google Scholar 

  21. Leung J, Jayachandran M, Kendall-Thomas J, Behrenbeck T, Araoz P, Miller VM. Pilot study of sex differences in chemokine/cytokine markers of atherosclerosis in humans. Gend Med. 2008;5:44–52.

    Article  PubMed  Google Scholar 

  22. Pou KM, Massaro JM, Hoffmann U, Vasan RS, Maurovich-Horvat P, Larson MG, et al. Visceral and subcutaneous adipose tissue volumes are cross-sectionally related to markers of inflammation and oxidative stress: the Framingham Heart Study. Circulation. 2007;116:1234–41.

    Article  PubMed  CAS  Google Scholar 

  23. Saltevo J, Vanhala M, Kautiainen H, Kumpusalo E, Laakso M. Gender differences in C-reactive protein, interleukin-1 receptor antagonist and adiponectin levels in the metabolic syndrome: a population-based study. Diabet Med. 2008;25:747–50.

    Article  PubMed  CAS  Google Scholar 

  24. Hermsdorff HHM, Zulet MA, Puchau B, Bressan J, Martínez JA. Association of retinol-binding protein-4 with dietary selenium intake and other lifestyle features in young healthy women. Nutrition. 2009;25:392–9.

    Article  PubMed  CAS  Google Scholar 

  25. Pérez S, Parra MD, Martínez de Morentin B, Rodríguez MC, Martínez JA. Evaluación de la variabilidad intraindividual de la medida de composición corporal mediante bioimpedancia en voluntarias sanas y su relación con el índice de masa corporal y el pliegue tricipital. Enferm Clin. 2005;15:307–14.

    Article  Google Scholar 

  26. World Health Organization (WHO). Programme of nutrition, family and reproductive health. obesity. Preventing and managing the global epidemic. Report of a WHO consultation on obesity. Geneva, 1997. 1998.

  27. Durnin JV, Womersley J. Body fat assessed from total body density and its estimation from skinfold thickness: measurements on 481 men and women aged from 16 to 72 years. Br J Nutr. 1974;32:77–97.

    Article  PubMed  CAS  Google Scholar 

  28. Siri WE. The gross composition of the body. Adv Biol Med Phys. 1956;4:239–80.

    PubMed  CAS  Google Scholar 

  29. Whitworth JA, Chalmers J. World health organisation-international society of hypertension (WHO/ISH) hypertension guidelines. Clin Exp Hypertens. 2004;26:747–52.

    Article  PubMed  Google Scholar 

  30. Matthews DR, Hosker JP, Rudenski AS, Naylor BA, Treacher DF, Turner RC. Homeostasis model assessment: insulin resistance and beta-cell function from fasting plasma glucose and insulin concentrations in man. Diabetologia. 1985;28:412–9.

    Article  PubMed  CAS  Google Scholar 

  31. Castelli WP. Cholesterol and lipids in the risk of coronary artery disease—the Framingham Heart Study. Can J Cardiol 1988; 4 Suppl A:5A–10A.

  32. Willett WC. Nutritional epidemiology. New York: Oxford University Press; 1998.

    Book  Google Scholar 

  33. Hermsdorff HHM, Monteiro JB. Visceral, subcutaneous or intramuscular fat: where is the problem? Arq Bras Endocrinol Metabol. 2004;48:803–11.

    Article  PubMed  Google Scholar 

  34. Van Gaal LF, Mertens IL, De Block CE. Mechanisms linking obesity with cardiovascular disease. Nature. 2006;444:875–80.

    Article  PubMed  Google Scholar 

  35. Hermsdorff HHM, Zulet MA, Abete I, Martínez JA. Discriminated benefits of a Mediterranean dietary pattern within a hypocaloric diet program on plasma RBP4 concentrations and other inflammatory markers in obese subjects. Endocrine. 2009;36:445–51.

    Article  PubMed  CAS  Google Scholar 

  36. Hermsdorff HHM, Zulet MA, Abete I, Martínez JA. A legume-based hypocaloric diet reduces proinflammatory status and improves metabolic features in overweight/obese subjects. Eur J Nutr. 2011;50:61–9.

    Article  PubMed  CAS  Google Scholar 

  37. Lee IS, Shin G, Choue R. A 12-week regimen of caloric restriction improves levels of adipokines and pro-inflammatory cytokines in Korean women with BMIs greater than 23 kg/m2. Inflamm Res. 2010;59:399–405.

    Article  PubMed  CAS  Google Scholar 

  38. Nishida M, Moriyama T, Sugita Y, Yamauchi-Takihara K. Abdominal obesity exhibits distinct effect on inflammatory and anti-inflammatory proteins in apparently healthy Japanese men. Cardiovasc Diabetol. 2007;6:27.

    Article  PubMed  Google Scholar 

  39. Santos AC, Lopes C, Guimaraes JT, Barros H. Central obesity as a major determinant of increased high-sensitivity C-reactive protein in metabolic syndrome. Int J Obes (Lond). 2005;29:1452–6.

    Article  CAS  Google Scholar 

  40. Cignarelli M, DePergola G, Picca G, Sciaraffia M, Pannacciulli N, Tarallo M, et al. Relationship of obesity and body fat distribution with ceruloplasmin serum levels. Int J Obes Relat Metab Disord. 1996;20:809–13.

    PubMed  CAS  Google Scholar 

  41. Khera A, Vega GL, Das SR, Ayers C, McGuire DK, Grundy SM, et al. Sex differences in the relationship between C-reactive protein and body fat. J Clin Endocrinol Metab. 2009;94:3251–8.

    Article  PubMed  CAS  Google Scholar 

  42. Després JP, Allard C, Tremblay A, Talbot J, Bouchard C. Evidence for a regional component of body fatness in the association with serum lipids in men and women. Metabolism. 1985;34:967–73.

    Article  PubMed  Google Scholar 

  43. Onat A, Hergenc G, Can G, Kaya Z, Yuksel H. Serum complement C3: a determinant of cardiometabolic risk, additive to the metabolic syndrome, in middle-aged population. Metabolism. 2009;59:628–34.

    Article  PubMed  Google Scholar 

  44. Regitz-Zagrosek V, Lehmkuhl E, Mahmoodzadeh S. Gender aspects of the role of the metabolic syndrome as a risk factor for cardiovascular disease. Gend Med 2007; 4 Suppl B:S162–S177.

  45. Saltevo J, Kautiainen H, Vanhala M. Gender differences in adiponectin and low-grade inflammation among individuals with normal glucose tolerance, prediabetes, and type 2 diabetes. Gend Med. 2009;6:463–70.

    Article  PubMed  Google Scholar 

  46. Johnson PE, Milne DB, Lykken GI. Effects of age and sex on copper absorption, biological half-life, and status in humans. Am J Clin Nutr. 1992;56:917–25.

    PubMed  CAS  Google Scholar 

  47. Wener MH, Daum PR, McQuillan GM. The influence of age, sex, and race on the upper reference limit of serum C-reactive protein concentration. J Rheumatol. 2000;27:2351–9.

    PubMed  CAS  Google Scholar 

  48. Garmizo G, Frauens BJ. Corneal copper deposition secondary to oral contraceptives. Optom Vis Sci. 2008;85:E802–7.

    Article  PubMed  Google Scholar 

  49. van Rooijen M, Hansson LO, Frostegard J, Silveira A, Hamsten A, Bremme K. Treatment with combined oral contraceptives induces a rise in serum C-reactive protein in the absence of a general inflammatory response. J Thromb Haemost. 2006;4:77–82.

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

We wish to thank the physician Blanca E. Martínez de Morentín, the nurse Salomé Pérez, and the technician Verónica Ciaurriz as well as the nursing assistant Elisângela Lessa for excellent technical assistance in the University of Navarra and Federal University of Viçosa, respectively. We also thank to The Capes Foundation, Ministry of Education of Brazil, as well as the Ministry of Education of Spain for supporting the Interuniversity Cooperation between the Federal University of Viçosa (CAPES/MECD-DGU 109/06) and the University of Navarra (PHB-2005-0119-PC). Finally, this work was supported by the Health Department of the Government of Navarra (22/2007), Línea Especial about Nutrition, Obesity and Health (University of Navarra LE/97), and by the Foundation for Research Support of the State of Minas Gerais (FAPEMIG-CDS 303/06).

Author information

Authors and Affiliations

  1. Department of Nutrition, Food Science, Physiology and Toxicology, University of Navarra, C/Irunlarrea, 1, 31008, Pamplona, Spain

    Helen Hermana M. Hermsdorff, Blanca Puchau, M. Ángeles Zulet & J. Alfredo Martínez

  2. Department of Clinical and Social Nutrition, Federal University of Ouro Preto, Ouro Preto, Brazil

    Ana Carolina P. Volp

  3. Nutrition Center, Federal University of Sergipe, Aracaju, Brazil

    Kiriaque B. F. Barbosa

  4. Department of Nutrition and Health, Federal University of Viçosa, Viçosa, Brazil

    Josefina Bressan

Authors
  1. Helen Hermana M. Hermsdorff
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ana Carolina P. Volp
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Blanca Puchau
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Kiriaque B. F. Barbosa
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. M. Ángeles Zulet
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Josefina Bressan
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. J. Alfredo Martínez
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to J. Alfredo Martínez.

Additional information

Responsible Editor: Claudia Kasserra.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Hermsdorff, H.H., Volp, A.C., Puchau, B. et al. Contribution of gender and body fat distribution to inflammatory marker concentrations in apparently healthy young adults. Inflamm. Res. 61, 427–435 (2012). https://doi.org/10.1007/s00011-011-0429-z

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00011-011-0429-z

Keywords

Search

Navigation