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Pathological and Behavioral Risk Factors for Higher Serum C-Reactive Protein Concentrations in Free-Living Adults—a Brazilian Community-Based Study

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Abstract

Low-grade chronic systemic inflammation is often associated with chronic non-communicable diseases, and its most frequently used marker, the C-reactive protein (CRP), has become an identifier of such diseases as well as an independent predictor for cardiovascular disorders and mortality. CRP is produced in response to pro-inflammatory signaling and to individual and behavioral factors, leading to pathological states. The aim of this study was to rank the predicting factors of high CRP concentrations in free-living adults from a community-based sample. We evaluated 522 adults (40–84 years old; 381 women) for anthropometric characteristics, dietary intake, clinical and physical tests, and blood analysis. Subjects were assigned to groups, according to CRP concentrations, as normal CRP (G1; <3.0 mg/L; n = 269), high CRP (G2; 3.0–6.0 mg/L; n = 139), and very high CRP (G3; >6.0 mg/dL; n = 116). Statistical comparison between groups used one-way ANOVA or Kruskal–Wallis tests, and prediction of altered values in increasing CRP was evaluated by proportional hazard models (odds ratio). CRP distribution was influenced by gender, body mass index, body and abdominal fatness, blood leukocytes, and neutrophil counts. The higher CRP group was discriminated by the above variables in addition to lower VO2max, serum metabolic syndrome components (triglycerides, glucose, and HDL cholesterol), higher insulin, homeostasis assessment of insulin resistance, uric acid, gamma-GT, and homocysteine. After adjustments, only fatness, blood leukocytes, and hyperglycemia remained as independent predictors for increased serum CRP concentrations. Intervention procedures to treat low-grade chronic inflammation in overweight women would mainly focus on restoring muscle mass and functions in addition to an antioxidant-rich diet.

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Abbreviations

CRP:

C-Reactive protein

nCRP:

Normal C-reactive protein concentration group

hCRP:

High C-reactive protein concentration group

vhCRP:

Very high C-reactive protein concentration group

AIT:

Anti-inflammatory treatment

CNCD:

Chronic non-communicable diseases

MetS:

Metabolic syndrome

T2DM:

Type-two diabetes mellitus

NCEP-ATPIII:

National Cholesterol Education Program–Adult Treatment Panel III

BP:

Blood pressure

BMI:

Body mass index

MMI:

Muscle mass index

WC:

Waist circumference

%BF:

Percentage of body fat

HEI:

Healthy eating index

HGS:

Handgrip strength

VO2max :

Maximum oxygen uptake

FFA:

Free fat acids

NASH:

Non-alcoholic steatohepatitis

HOMA-IR:

Homeostasis assessment of insulin resistance

SCN− :

Salivary thiocyanate

Hcy:

Homocysteine

MDA:

Malonyldialdehyde

IL-6:

Interleukin 6

TNF-α:

Tumor necrosis factor alpha

NF-κB:

Nuclear factor kappa B

JNK:

c-Jun amino-terminal kinase

MAPK:

Mitogen-activated protein kinase

PGC1α:

Peroxisome proliferator-activated receptor gamma coactivator 1-alpha

AGEs:

Advanced glycation end

REFERENCES

  1. Heinrich, P.C., J.V. Castell, and T. Andus. 1990. Interleukin-6 and the acute phase response. Biochemical Journal 265: 621–636.

    PubMed  CAS  Google Scholar 

  2. Povoa, P., E. Almeida, P. Moreira, A. Fernandes, R. Mealha, A. Aragao, and H. Sabino. 1998. C-Reactive protein as an indicator of sepsis. Intensive Care Medicine 24: 1052–1056.

    Article  PubMed  CAS  Google Scholar 

  3. Neumaier, M., G. Metak, and M.A. Scherer. 2006. C-Reactive protein as a parameter of surgical trauma: CRP response after different types of surgery in 349 hip fractures. Acta Orthopaedica 77: 788–790.

    Article  PubMed  Google Scholar 

  4. Bassuk, S.S., N. Rifai, and P.M. Ridker. 2004. High-sensitivity C-reactive protein: clinical importance. Current Problems in Cardiology 29: 439–493.

    PubMed  Google Scholar 

  5. Medzhitov, R. 2008. Origin and physiological roles of inflammation. Nature 454: 428–435.

    Article  PubMed  CAS  Google Scholar 

  6. Bensinger, S.J., and P. Tontonoz. 2008. Integration of metabolism and inflammation by lipid-activated nuclear receptors. Nature 454: 470–477.

    Article  PubMed  CAS  Google Scholar 

  7. Belfki, H., S. Ben Ali, S. Bougatef, D. Ben Ahmed, N. Haddad, A. Jmal, M. Abdennebi, and H. Ben Romdhane. 2012. Association between C-reactive protein and type 2 diabetes in a Tunisian population. Inflammation 35: 684–689.

    Article  PubMed  CAS  Google Scholar 

  8. Ridker, P.M. 2008. High-sensitivity C-reactive protein as a predictor of all-cause mortality: implications for research and patient care. Clinical Chemistry 54: 234–237.

    Article  PubMed  CAS  Google Scholar 

  9. Devaraj, S., S.K. Venugopal, U. Singh, and I. Jialal. 2005. Hyperglycemia induces monocytic release of interleukin-6 via induction of protein kinase c-{alpha} and -{beta}. Diabetes 54: 85–91.

    Article  PubMed  CAS  Google Scholar 

  10. Puglisi, M.J., and M.L. Fernandez. 2008. Modulation of C-reactive protein, tumor necrosis factor-alpha, and adiponectin by diet, exercise, and weight loss. Journal of Nutrition 138: 2293–2296.

    Article  PubMed  CAS  Google Scholar 

  11. Hotamisligil, G.S. 2006. Inflammation and metabolic disorders. Nature 444: 860–867.

    Article  PubMed  CAS  Google Scholar 

  12. Janssen, I., S.B. Heymsfield, R.N. Baumgartner, and R. Ross. 2000. Estimation of skeletal muscle mass by bioelectrical impedance analysis. Journal of Applied Physiology 89: 465–471.

    PubMed  CAS  Google Scholar 

  13. LA Philippi, S.T., A.T.R. Cruz, and L.C. Ribeiro. 1999. Adapted food pyramid: a guide for a right food choice. Revista de Nutrição 12: 16.

    Article  Google Scholar 

  14. Mota, J.F., A.E.M. Rinaldi, A.F. Pereira, N. Maestá, M.M. Scarpin, and R.C. Burini. 2008. Adaptation of the healthy eating index to the food guide of the Brazilian population. Revista de Nutrição 21: 8.

    Article  Google Scholar 

  15. Balke, B., and R.W. Ware. 1959. An experimental study of physical fitness of air force personnel. United States Armed Forces Medical Journal 10: 675–688.

    PubMed  CAS  Google Scholar 

  16. Galanti, L.M. 1997. Specificity of salivary thiocyanate as marker of cigarette smoking is not affected by alimentary sources. Clinical Chemistry 43: 184–185.

    PubMed  CAS  Google Scholar 

  17. Ubbink, J.B., W.J. Hayward Vermaak, and S. Bissbort. 1991. Rapid high-performance liquid chromatographic assay for total homocysteine levels in human serum. Journal of Chromatography 565: 441–446.

    Article  PubMed  CAS  Google Scholar 

  18. Nielsen, F., B.B. Mikkelsen, J.B. Nielsen, H.R. Andersen, and P. Grandjean. 1997. Plasma malondialdehyde as biomarker for oxidative stress: reference interval and effects of life-style factors. Clinical Chemistry 43: 1209–1214.

    PubMed  CAS  Google Scholar 

  19. Grundy, S.M., J.I. Cleeman, S.R. Daniels, K.A. Donato, R.H. Eckel, B.A. Franklin, D.J. Gordon, R.M. Krauss, P.J. Savage, S.C. Smith Jr., et al. 2005. Diagnosis and management of the metabolic syndrome: an American Heart Association/National Heart, Lung, and Blood Institute Scientific Statement. Circulation 112: 2735–2752.

    Article  PubMed  Google Scholar 

  20. Nicklas, B.J., and T.E. Brinkley. 2009. Exercise training as a treatment for chronic inflammation in the elderly. Exercise and Sport Sciences Reviews 37: 165–170.

    PubMed  Google Scholar 

  21. Thorand, B., J. Baumert, A. Doring, C. Herder, H. Kolb, W. Rathmann, G. Giani, and W. Koenig. 2006. Sex differences in the relation of body composition to markers of inflammation. Atherosclerosis 184: 216–224.

    Article  PubMed  CAS  Google Scholar 

  22. Kupelian, V., G.R. Chiu, A.B. Araujo, R.E. Williams, R.V. Clark, and J.B. McKinlay. 2010. Association of sex hormones and C-reactive protein levels in men. Clinical Endocrinology 72: 527–533.

    Article  PubMed  CAS  Google Scholar 

  23. Albert, M.A., R.J. Glynn, J. Buring, and P.M. Ridker. 2004. C-reactive protein levels among women of various ethnic groups living in the United States (from the Women's Health Study). The American Journal of Cardiology 93: 1238–1242.

    Article  PubMed  CAS  Google Scholar 

  24. Lakoski, S.G., M. Cushman, M. Criqui, T. Rundek, R.S. Blumenthal, R.B. D'Agostino Jr., and D.M. Herrington. 2006. Gender and C-reactive protein: data from the Multiethnic Study of Atherosclerosis (MESA) cohort. American Heart Journal 152: 593–598.

    Article  PubMed  CAS  Google Scholar 

  25. Povoa, P., A.M. Teixeira-Pinto, and A.H. Carneiro. 2011. C-Reactive protein, an early marker of community-acquired sepsis resolution: a multi-center prospective observational study. Critical Care 15: R169.

    Article  PubMed  Google Scholar 

  26. Rogowski, O., I. Shapira, O.K. Bassat, T. Chundadze, T. Finn, S. Berliner, and A. Steinvil. 2010. Waist circumference as the predominant contributor to the micro-inflammatory response in the metabolic syndrome: a cross sectional study. Journal of Inflammation (London) 7: 35.

    Article  Google Scholar 

  27. Maki, K.C., T.M. Rains, M. Bell, M.S. Reeves, M.V. Farmer, and K. Yasunaga. 2011. Fat mass, abdominal fat distribution, and C-reactive protein concentrations in overweight and obese men and women. Metab Syndre Relat Disord 9: 291–6.

    Article  CAS  Google Scholar 

  28. Lin, C.C., S.L. Kardia, C.I. Li, C.S. Liu, M.M. Lai, W.Y. Lin, P.C. Chang, Y.D. Lee, C.C. Chen, C.H. Lin, et al. 2010. The relationship of high sensitivity C-reactive protein to percent body fat mass, body mass index, waist-to-hip ratio, and waist circumference in a Taiwanese population. BMC Public Health 10: 579.

    Article  PubMed  Google Scholar 

  29. Zuliani, G., S. Volpato, M. Galvani, A. Ble, S. Bandinelli, A.M. Corsi, F. Lauretani, M. Maggio, J.M. Guralnik, R. Fellin, and L. Ferrucci. 2009. Elevated C-reactive protein levels and metabolic syndrome in the elderly: the role of central obesity data from the InChianti study. Atherosclerosis 203: 626–632.

    Article  PubMed  CAS  Google Scholar 

  30. Tarantino, G., A. Colao, D. Capone, P. Conca, M. Tarantino, E. Grimaldi, D. Chianese, C. Finelli, F. Contaldo, F. Scopacasa, and S. Savastano. 2011. Circulating levels of cytochrome C, gamma-glutamyl transferase, triglycerides and unconjugated bilirubin in overweight/obese patients with non-alcoholic fatty liver disease. Journal of Biological Regulators and Homeostatic Agents 25: 47–56.

    PubMed  CAS  Google Scholar 

  31. Esposito, K., F. Nappo, R. Marfella, G. Giugliano, F. Giugliano, M. Ciotola, L. Quagliaro, A. Ceriello, and D. Giugliano. 2002. Inflammatory cytokine concentrations are acutely increased by hyperglycemia in humans: role of oxidative stress. Circulation 106: 2067–2072.

    Article  PubMed  CAS  Google Scholar 

  32. Mota, J.F., F. Moreto, W.L. Medina, E.C. Leite Pereira, and R.C. Burini. 2011. Nutritional and metabolic risk factors for insulin resistance in adults. International Journal of Nutrition and Metabolism 7: 3.

    Google Scholar 

  33. Pradhan, A.D., J.E. Manson, N. Rifai, J.E. Buring, and P.M. Ridker. 2001. C-reactive protein, interleukin 6, and risk of developing type 2 diabetes mellitus. JAMA 286: 327–334.

    Article  PubMed  CAS  Google Scholar 

  34. Kado, S., T. Nagase, and N. Nagata. 1999. Circulating levels of interleukin-6, its soluble receptor and interleukin-6/interleukin-6 receptor complexes in patients with type 2 diabetes mellitus. Acta Diabetologica 36: 67–72.

    Article  PubMed  CAS  Google Scholar 

  35. Shikano, M., H. Sobajima, H. Yoshikawa, T. Toba, H. Kushimoto, H. Katsumata, M. Tomita, and S. Kawashima. 2000. Usefulness of a highly sensitive urinary and serum IL-6 assay in patients with diabetic nephropathy. Nephron 85: 81–85.

    Article  PubMed  CAS  Google Scholar 

  36. Mohamed-Ali, V., S. Goodrick, A. Rawesh, D.R. Katz, J.M. Miles, J.S. Yudkin, S. Klein, and S.W. Coppack. 1997. Subcutaneous adipose tissue releases interleukin-6, but not tumor necrosis factor-alpha, in vivo. Journal of Clinical Endocrinology and Metabolism 82: 4196–4200.

    Article  PubMed  CAS  Google Scholar 

  37. Mota, J.F., W.L. Medina, F. Moreto, and R.C. Burini. 2009. Influence of adiposity on inflammation risk in patients with fasting glucose impairment. Revista de Nutrição 22: 6.

    Article  Google Scholar 

  38. Schmidt, A.M., S.D. Yan, J.L. Wautier, and D. Stern. 1999. Activation of receptor for advanced glycation end products: a mechanism for chronic vascular dysfunction in diabetic vasculopathy and atherosclerosis. Circulation Research 84: 489–497.

    Article  PubMed  CAS  Google Scholar 

  39. Vallerie, S.N., and G.S. Hotamisligil. 2010. The role of JNK proteins in metabolism. Science Translational Medicine 2: 60rv65.

    Article  Google Scholar 

  40. Petersen, A.M., and B.K. Pedersen. 2005. The anti-inflammatory effect of exercise. Journal of Applied Physiology 98: 1154–1162.

    Article  PubMed  CAS  Google Scholar 

  41. Church, T.S., C.P. Earnest, A.M. Thompson, E.L. Priest, R.Q. Rodarte, T. Saunders, R. Ross, and S.N. Blair. 2010. Exercise without weight loss does not reduce C-reactive protein: the INFLAME study. Medicine and Science in Sports and Exercise 42: 708–716.

    Article  PubMed  CAS  Google Scholar 

  42. Jae, S.Y., B. Fernhall, K.S. Heffernan, M. Jeong, E.M. Chun, J. Sung, S.H. Lee, Y.J. Lim, and W.H. Park. 2006. Effects of lifestyle modifications on C-reactive protein: contribution of weight loss and improved aerobic capacity. Metabolism 55: 825–831.

    Article  PubMed  CAS  Google Scholar 

  43. Kelley, G.A., and K.S. Kelley. 2006. Effects of aerobic exercise on C-reactive protein, body composition, and maximum oxygen consumption in adults: a meta-analysis of randomized controlled trials. Metabolism 55: 1500–1507.

    Article  PubMed  CAS  Google Scholar 

  44. Handschin, C., and B.M. Spiegelman. 2008. The role of exercise and PGC1alpha in inflammation and chronic disease. Nature 454: 463–469.

    Article  PubMed  CAS  Google Scholar 

  45. Niu, K., A. Hozawa, S. Kuriyama, K. Ohmori-Matsuda, T. Shimazu, N. Nakaya, K. Fujita, I. Tsuji, and R. Nagatomi. 2006. Dietary long-chain n-3 fatty acids of marine origin and serum C-reactive protein concentrations are associated in a population with a diet rich in marine products. American Journal of Clinical Nutrition 84: 223–229.

    PubMed  CAS  Google Scholar 

  46. Esmaillzadeh, A., M. Kimiagar, Y. Mehrabi, L. Azadbakht, F.B. Hu, and W.C. Willett. 2006. Fruit and vegetable intakes, C-reactive protein, and the metabolic syndrome. American Journal of Clinical Nutrition 84: 1489–1497.

    PubMed  CAS  Google Scholar 

  47. de Oliveira Otto, M.C., A. Alonso, D.H. Lee, G.L. Delclos, N.S. Jenny, R. Jiang, J.A. Lima, E. Symanski, D.R. Jacobs Jr., and J.A. Nettleton. 2011. Dietary micronutrient intakes are associated with markers of inflammation but not with markers of subclinical atherosclerosis. Journal of Nutrition 141: 1508–1515.

    Article  PubMed  Google Scholar 

  48. Takahashi, M.M., E.P. de Oliveira, F. Moreto, K.C. Portero-McLellan, and R.C. Burini. 2010. Association of dyslipidemia with intakes of fruit and vegetables and the body fat content of adults clinically selected for a lifestyle modification program. Archivos Latinoamericanos de Nutricion 60: 148–154.

    PubMed  Google Scholar 

  49. Mecca, M.S., F. Moreto, F.H. Burini, R.C. Dalanesi, K.C. McLellan, and R.C. Burini. 2012. Ten-week lifestyle changing program reduces several indicators for metabolic syndrome in overweight adults. Diabetology and Metabolic Syndrome 4: 1.

    Article  PubMed  Google Scholar 

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ACKNOWLEDGMENTS

We thank the Grupo de Apoio à Pesquisa (Research Support Group) of the Botucatu School of Medicine for the English language review of the manuscript. We also thank Dr. José Eduardo Corrente for the statistical analysis. Financial support for this study came from CAPES, CNPq, and FUNDAP.

Conflict of Interest

This study has no conflicts of interest.

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Authors and Affiliations

  1. Department of Pathology, Botucatu School of Medicine, UNESP–Univ Estadual Paulista, Botucatu, SP, Brazil

    Fernando Moreto, Erick Prado de Oliveira, Rodrigo Minoru Manda, Gabriel Augusto Torezan & Okesley Teixeira

  2. Center for Nutritional and Exercise Metabolism (CeMENutri), Department of Public Health, Botucatu School of Medicine, UNESP–Univ Estadual Paulista, Botucatu, SP, Brazil

    Fernando Moreto, Erick Prado de Oliveira, Rodrigo Minoru Manda, Gabriel Augusto Torezan, Okesley Teixeira, Edilaine Michelin & Roberto Carlos Burini

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  1. Fernando Moreto
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Correspondence to Fernando Moreto.

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Moreto, F., de Oliveira, E.P., Manda, R.M. et al. Pathological and Behavioral Risk Factors for Higher Serum C-Reactive Protein Concentrations in Free-Living Adults—a Brazilian Community-Based Study. Inflammation 36, 15–25 (2013). https://doi.org/10.1007/s10753-012-9515-9

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