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Clinical nutrition, enteral and parenteral nutrition

Dietary factors associated with subclinical inflammation among girls

European Journal of Clinical Nutrition volume 67, pages 1264–1270 (2013)Cite this article

Subjects

Abstract

Background/Objectives:

Dietary patterns and biomarkers of inflammation have been scarcely associated. The aim was to assess dietary factors associated with subclinical inflammation among girls.

Subjects/Methods:

Fasting blood samples were collected from 12- to 17-year old girls (n=219) to measure adiponectin, leptin, tumor necrosis factor-alpha, plasminogen activator inhibitor 1 (PAI-1), interleukin-6 (IL-6) and high-sensitivity C-reactive protein (hs-CRP) levels. Body mass index (BMI) and waist-to-height ratio (WHtR), and food intake were also measured. Western (WDP) and Mediterranean (MDP) dietary patterns were identified.

Results:

BMI and WHtR were associated with adiponectin, leptin and hs-CRP (the last, only associated with BMI). Intakes of β-carotene equivalents and vitamin C were associated with adiponectin; saturated fatty acids (SFA), vitamin A, manganese and selenium with leptin; linoleic acid with PAI-1; and oleic acid and vitamin E with IL-6. Selenium was inversely associated with adiponectin, whereas magnesium was positively associated with IL-6. MDP was associated with higher plasma concentrations of adiponectin (β=0.174, P<0.05); after adjustment for BMI, associations were not significant (β=0.144, P=0.076). WDP was negatively associated with adiponectin (β=−0.177, P<0.05) and positively with IL-6 (β=0.183, P<0.05).

Conclusions:

Subclinical inflammation is detectable with increasing BMI and also WHtR. Measures of adiposity (BMI and WHtR) are significant predictors of adiponectin, leptin and hs-CRP. Dietary patterns per se have a small role in affecting inflammatory markers among adolescents.

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References

  1. Halpern A, Mancini MC, Magalhães ME, Fisberg M, Radominski R, Bertolami MC et al. Metabolic syndrome, dyslipidemia, hypertension and type 2 diabetes in youth: from diagnosis to treatment. Diabetol Metab Syndr 2010; 18: 55.

    Article  Google Scholar 

  2. Hamdy O . The role of adipose tissue as an endocrine gland. Curr Diab Rep 2005; 5: 317–319.

    Article  CAS  Google Scholar 

  3. Sbarbati A, Osculati F, Silvagni D, Benati D, Galiè M, Camoglio FS et al. Obesity and inflammation: evidence for an elementary lesion. Pediatrics 2006; 117: 220–223.

    Article  Google Scholar 

  4. Jéquier E . Leptin signaling, adiposity, and energy balance. Lipids and insulin resistance: the role of fatty acid metabolism and fuel partitioning. Ann NY Acad Sci 2002; 967: 379–388.

    Article  Google Scholar 

  5. Moran O . Phillip M. Leptin: obesity, diabetes and other peripheral effects—a review. Pediat Diab 2003; 4: 101–109.

    Article  CAS  Google Scholar 

  6. Giordano P, Del Vecchio GC, Cecinati V, Delvecchio M, Altomare M, De Palma F et al. Metabolic, inflammatory, endothelial and haemostatic markers in a group of Italian obese children and adolescents. Eur J Pediat 2011; 170: 845–850.

    Article  CAS  Google Scholar 

  7. Jiamsripong P, Mookadam M, Honda T, Khandheria BK, Mookadam F . The metabolic syndrome and cardiovascular disease: part I. Prev Cardiol 2008; 11: 155–161.

    Article  CAS  Google Scholar 

  8. Torres JL, Ridker PM . Clinical use of high sensitivity C-reactive protein for the prediction of adverse cardiovascular events. Curr Opin Cardiol 2003; 18: 471–478.

    Article  Google Scholar 

  9. Juhan-Vague I, Pyke SD, Alessi MC, Jespersen J, Haverkate F, Thompson SG . Fibrinolytic factors and the risk of myocardial infarction or sudden death in patients with angina pectoris. ECAT Study Group. European concerted action on thrombosis and disabilities. Circulation 1996; 94: 2057–2063.

    Article  CAS  Google Scholar 

  10. Huang H, Park PH, McMullen MR, Nagy LE . Mechanisms for the anti-inflammatory effects of adiponectin in macrophages. J Gastroenterol Hepatol 2008; 23 (Suppl 1), S50–S53.

    Article  CAS  Google Scholar 

  11. Babio N, Bulló M, Salas-Salvadó J . Mediterranean diet and metabolic syndrome: the evidence. Pub Health Nutr 2009; 12: 1607–1617.

    Article  Google Scholar 

  12. Myers JL, Allen JC . Nutrition and inflammation: insights on dietary pattern, obesity, and asthma. Am J Lifestyle Med 2012; 6: 14–17.

    Article  Google Scholar 

  13. Bressan J, Hermsdorff HH, Zulet MA, Marti-nez JA . Hormonal and inflammatory impact of different dietetic composition: emphasis on dietary patterns and specific dietary factors. Arq Bras Endocrinol Metabol 2009; 53: 572–581.

    Article  Google Scholar 

  14. Aeberli I, Molinari L, Spinas G, Lehmann R, l'Allemand D, Zimmermann MB . Dietary intakes of fat and antioxidant vitamins are predictors of subclinical inflammation in overweight Swiss children. Am J Clin Nutr 2006; 84: 748–755.

    Article  CAS  Google Scholar 

  15. Birch LL, Anzman SL . Learning to eat in an obesogenic environment: a developmental systems perspective on childhood obesity. Child Dev Persp 2010; 4: 138–143.

    Article  Google Scholar 

  16. Raatz SK, Bibus D, Thomas W, Kris-Etherton P . Total fat intake modifies plasma fatty acid composition in humans. J Nutr 2001; 131: 231–234.

    Article  CAS  Google Scholar 

  17. Wolk A, Furuheim M, Vessby B . Fatty acid composition of adipose tissue and serum lipids are valid biological markers of dairy fat intake in men. J Nutr 2001; 131: 828–833.

    Article  CAS  Google Scholar 

  18. Esposito K, Giugliano D . Diet and inflammation: a link to metabolic and cardiovascular diseases. Eur Heart J 2006; 27: 15–20.

    Article  Google Scholar 

  19. 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–S18.

    Article  CAS  Google Scholar 

  20. IPAQ—International Physical Activity Questionnaire. Guidelines for data processing and analysis of the International Physical Activity Questionnaire (IPAQ). Available at: http://www.ipaq.ki.se/ipaq.htm Accessed on 20 March 2009.

  21. Food and Nutrition Board. Institute of Medicine of the National Academies. Dietary reference intakes. Chapter 12. Physical activity. The National Academies Press: Washington, DC, 2005, pp 880–935.

  22. Bibiloni MM, Martinez E, Llull R, Juarez MD, Pons A, Tur JA . Prevalence and risk factors for obesity in Balearic Islands adolescents. Br J Nutr 2010; 103: 99–106.

    Article  CAS  Google Scholar 

  23. Bibiloni MM, Martínez E, Llull R, Maffiotte E, Riesco M, Llompart I et al. Metabolic syndrome in adolescents in the Balearic Islands, a Mediterranean region. Nutr Metab Cardiovasc Dis 2011; 21: 446–454.

    Article  Google Scholar 

  24. De Onis M, Onyango AW, Borghi E, Siyam A, Nishida C, Siekmann J . Development of a WHO growth reference for school-aged children an adolescents. Bull WHO 2007; 85: 660–667.

    PubMed  Google Scholar 

  25. Martin-Moreno JM, Boyle P, Gorgojo L, Maisonneuve P, Fernandez-Rodriguez JC, Salvini S et al. Development and validation of a food frequency ques- tionnaire in Spain. Int J Epidemiol 1993; 22: 512–519.

    Article  CAS  Google Scholar 

  26. Lazarou C, Panagiotakos DB, Matalas AL . Level of adherence to the Mediterranean diet among children from Cyprus: the CYKIDS study. Pub Health Nutr 2009; 12: 991–1000.

    Article  Google Scholar 

  27. Lazarou C, Panagiotakos DB, Kouta C, Matalas AL . Dietary and other lifestyle characteristics of Cypriot school children: results from the nationwide CYKIDS study. BMC Pub Health 2009; 9: 147.

    Article  Google Scholar 

  28. Bibiloni MM, Martínez E, Llull R, Pons A, Tur JA . Western and Mediterranean dietary patterns among Balearic Islands' adolescents: socio-economic and lifestyle determinants. Pub Health Nutr 2012; 15: 683–692.

    Article  Google Scholar 

  29. Mataix J, Mañas M, Llopis J, Martínez de Victoria E, Juan J, Borregón A . Tablas de composición de alimentos españoles 4th edn. INTA-Universidad de Granada: Granada, 2004.

    Google Scholar 

  30. Ortega RM, López AM, Requejo AM, Carvajales PA . La composición de los alimentos. Herramienta básica para la valoración nutricional. Editorial Complutense: Madrid, 2004.

    Google Scholar 

  31. Feinberg M, Favier JC, Ireland-Ripert J . Répertoire general des aliments. Tec & Doc Lavoisier: París, 1995.

    Google Scholar 

  32. Ripoll L . La cocina de las Islas Baleares 5th edn. L. Ripoll Pub. Co.: Palma de Mallorca, 1992.

  33. Livingstone MBE, Black AE . Biomarkers of nutritional exposure and nutritional status. J Nutr 2005; 133 (Suppl 3), S895–S920.

    Google Scholar 

  34. Johansson L, Solvoll K, Bjørneboe GA, Drevon CA . Under- and overreporting of energy intake related to weight status and lifestyle in a nationwide sample. Am J Clin Nutr 1998; 68: 266–274.

    Article  CAS  Google Scholar 

  35. Mendez MA, Wynter S, Wilks R, Forrester T . Under- and overreporting of energy is related to obesity, lifestyle factors and food group intakes in Jamaican adults. Pub Health Nutr 2003; 7: 9–19.

    Google Scholar 

  36. Maffeis C, Banzato C, Talamini G . Obesity Study Group of the Italian Society of Pediatric Endocrinology and Diabetology. Waist-to-height ratio, a useful index to identify high metabolic risk in overweight children. J Pediatr 2008; 152: 207–213.

    Article  Google Scholar 

  37. Esmaillzadeh A, Kimiagar M, Mehrabi Y, Azadbakht L, Hu FB, Willett WC . Dietary patterns and markers of systemic inflammation among Iranian women. J Nutr 2007; 137: 992–998.

    Article  CAS  Google Scholar 

  38. Wärnberg J, Nova E, Romeo J, Moreno LA, Sjöström M, Marcos A . Lifestyle-related determinants of inflammation in adolescence. Br J Nutr 2007; 98 (Suppl 1), S116–S120.

    Article  Google Scholar 

  39. González M, Bibiloni MM, Pons A, Llompart I, Tur JA . Inflammatory markers and metabolic syndrome among adolescents. Eur J Clin Nutr 2012; 66: 1141–1145.

    Article  Google Scholar 

  40. Maffeis C, Silvagni D, Bonadonna R, Grezzani A, Banzato C, Tatò L . Fat cell size, insulin sensitivity, and inflammation in obese children. J Pediatr 2007; 151: 647–652.

    Article  CAS  Google Scholar 

  41. Lopez-Garcia E, Schulze MB, Fung TT, Meigs JB, Rifai N, Manson JE et al. Major dietary patterns are related to plasma concentrations of markers of inflammation and endothelial dysfunction. Am J Clin Nutr 2004; 80: 1029–1035.

    Article  CAS  Google Scholar 

  42. Fung TT, Rimm EB, Spiegelman D, Rifai N, Tofler GH, Willett WC et al. Association between dietary patterns and plasma biomarkers of obesity and cardiovascular disease risk. Am J Clin Nutr 2001; 73: 61–67.

    Article  CAS  Google Scholar 

  43. Schulze MB, Hoffmann K, Manson JE, Willett WC, Meigs JB, Weikert C et al. Dietary pattern, inflammation, and incidence of type 2 diabetes in women. Am J Clin Nutr 2005; 82: 675–684.

    Article  CAS  Google Scholar 

  44. Chrysohoou C, Panagiotakos DB, Pitsavos C, Das UN, Stefanadis C . Adherence to the Mediterranean diet attenuates inflammation and coagulation process in healthy adults: the ATTICA Study. J Am Coll Cardiol 2004; 44: 152–158.

    Article  Google Scholar 

  45. Eilat-Adar S, Mete M, Nobmann ED, Xu J, Fabsitz RR, Ebbesson SO et al. Dietary patterns are linked to cardiovascular risk factors but not to inflammatory markers in Alaska Eskimos. J Nutr 2009; 139: 2322–2328.

    Article  CAS  Google Scholar 

  46. Galland L . Diet and inflammation. Nutr Clin Pract 2010; 25: 634–640.

    Article  Google Scholar 

  47. Helmersson J, Arnlöv J, Vessby B, Larsson A, Alfthan G, Basu S . Serum selenium predicts levels of F2-isoprostanes and prostaglandin F2alpha in a 27 year follow-up study of Swedish men. Free Radic Res 2005; 39: 763–770.

    Article  CAS  Google Scholar 

  48. Kilander L, Berglund L, Boberg M, Vessby B, Lithell H . Education, lifestyle factors and mortality from cardiovascular disease and cancer. A 25-year follow-up of Swedish 50-year-old men. Int J Epidemiol 2001; 30: 1119–1126.

    Article  CAS  Google Scholar 

  49. Salonen JT, Alfthan G, Huttunen JK, Pikkarainen J, Puska P . Association between cardiovascular death and myocardial infarction and serum selenium in a matched-pair longitudinal study. Lancet 1982; 2: 175–179.

    Article  CAS  Google Scholar 

  50. Suadicani P, Hein HO, Gyntelberg F . Serum selenium concentration and risk of ischaemic heart disease in a prospective cohort study of 3000 males. Atherosclerosis 1992; 96: 33–42.

    Article  CAS  Google Scholar 

  51. Salonen JT, Salonen R, Seppanen K, Kantola M, Suntioinen S, Korpela H . Interactions of serum copper, selenium, and low density lipoprotein cholesterol in atherogenesis. BMJ 1991; 302: 756–760.

    Article  CAS  Google Scholar 

  52. Kok FJ, de Bruijn AM, Vermeeren R, Hofman A, van Laar A, de Bruin M et al. Serum selenium, vitamin antioxidants, and cardiovascular mortality: A 9-year follow-up study in the Netherlands. Am J Clin Nutr 1987; 45: 462–468.

    Article  CAS  Google Scholar 

  53. Salvini S, Hennekens CH, Morris JS, Willett WC, Stampfer MJ . Plasma levels of the antioxidant selenium and risk of myocardial infarction among U.S. physicians. Am J Cardiol 1995; 76: 1218–1221.

    Article  CAS  Google Scholar 

  54. Aranceta J . Spanish food patterns. Pub Health Nutr 2001; 4: 1399–1402.

    CAS  Google Scholar 

  55. Schulze MB, Hoffman K, Kroke A, Boeing H . An approach to construct simplified measures of dietary patterns from exploratory factor analysis. Br J Nutr 2003; 89: 409–419.

    Article  CAS  Google Scholar 

  56. Bogaty P, Brophy JM, Boyer L, Simard S, Joseph L, Bertrand F et al. Fluctuating inflammatory markers in patients with stable ischemic heart disease. Arch Intern Med 2005; 165: 221–226.

    Article  Google Scholar 

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Acknowledgements

This study is supported by Spanish Ministry of Health and Consumption Affairs (Programme of Promotion of Biomedical Research and Health Sciences, Projects 05/1276, 08/1259 and 11/01791, Red Predimed-RETIC RD06/0045/1004 and CIBERobn CB12/03/30038), Spanish Ministry of Education and Science (FPU Programme, PhD fellowship to Maria del Mar Bibiloni). The Research Group on Community Nutrition and Oxidative Stress, University of Balearic Islands belongs to the Centre Català de la Nutrició (IEC) and Exernet Network.

AUTHOR CONTRIBUTIONS

MdelMB and JAT conceived, designed and devised the study, MdelMB, CM, IL, AP and JAT collected and supervised the samples, and analysed the data and wrote the manuscript. MdelMB and JAT supervised the study. AP and JAT obtained funding.

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Authors and Affiliations

  1. Research Group on Community Nutrition and Oxidative Stress, University of Balearic Islands, Palma de Mallorca, Spain

    M del Mar Bibiloni, I Llompart, A Pons & J A Tur

  2. CIBER: CB12/03/30038 Fisiopatología de la Obesidad y la Nutrición, CIBERobn, Palma de Mallorca, Spain

    M del Mar Bibiloni, I Llompart, A Pons & J A Tur

  3. Department of Life and Reproduction Sciences, Unit of Pediatric Diabetes, Clinical Nutrition and Obesity, University of Verona, Verona, Italy

    C Maffeis

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Correspondence to J A Tur.

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del Mar Bibiloni, M., Maffeis, C., Llompart, I. et al. Dietary factors associated with subclinical inflammation among girls. Eur J Clin Nutr 67, 1264–1270 (2013). https://doi.org/10.1038/ejcn.2013.196

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