Diet as moderator in the association of adiposity with inflammatory biomarkers among adolescents in the HELENA study

European Journal of Nutrition

Volumn 58, Issue 5, 2019, Pages 1947-1960

  Arouca, Aline ^a   Moreno, Luis A ^b,c   Gonzalez Gil, Esther M ^b,c   Marcos, Ascensión ^d   Widhalm, Kurt ^e   Molnár, Dénes ^f   Manios, Yannis ^g   Gottrand, Frederic ^h   Kafatos, Anthony ⁱ   Kersting, Mathilde ^j   Sjöström, Michael ^k   Amaro Gahete, Francisco J ^l   Ferrari, Marika ^m   Huybrechts, Inge ^a,n   Gonzalez Gross, Marcela ^o   De Henauw, Stefaan ^a   Michels, Nathalie ^a  

^a GHENT UNIVERSITY   (Belgium)

^b UNIVERSITY OF ZARAGOZA   (Spain)

^c Instituto de Salud Carlos III   (Spain)

^d INSTITUTE OF FOOD SCIENCE   (Spain)

^e MEDICAL UNIVERSITY OF VIENNA   (Austria)

^f UNIVERSITY OF PÉCS   (Hungary)

^g HAROKOPIO UNIVERSITY   (Greece)

^h UNIV LILLE   (France)

ⁱ UNIVERSITY OF CRETE   (Greece)

^j RUHR UNIVERSITY BOCHUM   (Germany)

^k KAROLINSKA INSTITUTE   (Sweden)

^l UNIVERSITY OF GRANADA   (Spain)

^m CREA RESEARCH CENTRE FOR FOOD AND NUTRITION   (Italy)

ⁿ INTERNATIONAL AGENCY FOR RESEARCH ON CANCER   (France)

^o UNIVERSIDAD POLITÉCNICA DE MADRID   (Spain)

more..

Author keywords

Adiposity; Adolescents; Low grade inflammation; Mediterranean diet score

Indexed keywords

ALANINE AMINOTRANSFERASE; C REACTIVE PROTEIN; CELL ADHESION MOLECULE; GAMMA GLUTAMYLTRANSFERASE; HOMOCYSTEINE; INTERLEUKIN 1; INTERLEUKIN 10; INTERLEUKIN 2; INTERLEUKIN 4; INTERLEUKIN 5; INTERLEUKIN 6; TRANSFORMING GROWTH FACTOR BETA1; TUMOR NECROSIS FACTOR; ANTIOXIDANT; BIOLOGICAL MARKER;

ACCELEROMETRY; ADOLESCENT; ANTIOXIDANT RICH DIET SCORE; ARTICLE; BODY COMPOSITION; BODY FAT; BODY MASS; FASTING; FEMALE; FOOD INTAKE; HEALTHY DIET; HUMAN; INFLAMMATION; MAJOR CLINICAL STUDY; MALE; MEDITERRANEAN DIET; MEDITERRANEAN DIET SCORE; MULTICENTER STUDY; NUTRITIONAL PARAMETERS; OBESITY; PHYSICAL ACTIVITY; PUBERTY; SCORING SYSTEM; SKINFOLD THICKNESS; SOCIAL STATUS; UNHEALTHY DIET; WAIST CIRCUMFERENCE; BLOOD; CROSS-SECTIONAL STUDY; DIET; EUROPE; PROCEDURES;

ADIPOSITY; ADOLESCENT; ANTIOXIDANTS; BIOMARKERS; CROSS-SECTIONAL STUDIES; DIET; DIET, HEALTHY; DIET, MEDITERRANEAN; EUROPE; FEMALE; HUMANS; INFLAMMATION; MALE;

EID: 85048526916     PISSN: 14366207     EISSN: 14366215     Source Type: Journal    
DOI: 10.1007/s00394-018-1749-3     Document Type: Article

References (64)

1. Obesity: preventing and managing the global epidemic. Report of a WHO consultation. World Health Organ Tech Rep Ser 894:i–xii, 1–253
2. Moreno LA, Kersting M, de Henauw S, González-Gross M, Sichert-Hellert W, Matthys C, Mesana MI, Ross N (2005) How to measure dietary intake and food habits in adolescence: the European perspective. Int J Obes (Lond) 29(Suppl 2):S66–S77
3. Calder PC, Ahluwalia N, Brouns F, Buetler T, Clement K, Cunningham K, Esposito K, Jönsson LS, Kolb H, Lansink M, Marcos A, Margioris A, Matusheski N, Nordmann H, O’Brien J, Pugliese G, Rizkalla S, Schalkwijk C, Tuomilehto J, Wärnberg J, Watzl B, Winklhofer-Roob BM (2011) Dietary factors and low-grade inflammation in relation to overweight and obesity. Br J Nutr 106(Suppl 3):S5–S78. 10.1017/S0007114511005460
4. Calder PC (1997) n-3 polyunsaturated fatty acids and cytokine production in health and disease. Ann Nutr Metab 41(4):203–234
5. Ferrari M, Cuenca-García M, Valtueña J, Moreno LA, Censi L, González-Gross M, Androutsos O, Gilbert CC, Huybrechts I, Dallongeville J, Sjöström M, Molnar D, De Henauw S, Gómez-Martínez S, de Moraes AC, Kafatos A, Widhalm K, Leclercq C, Group HS (2015) Inflammation profile in overweight/obese adolescents in Europe: an analysis in relation to iron status. Eur J Clin Nutr 69(2):247–255. 10.1038/ejcn.2014.154
6. Steene-Johannessen J, Kolle E, Reseland JE, Anderssen SA, Andersen LB (2010) Waist circumference is related to low-grade inflammation in youth. Int J Pediatr Obes 5(4):313–319. 10.3109/17477160903497035
7. Galcheva SV, Iotova VM, Yotov YT, Bernasconi S, Street ME (2011) Circulating proinflammatory peptides related to abdominal adiposity and cardiometabolic risk factors in healthy prepubertal children. Eur J Endocrinol 164(4):553–558. 10.1530/EJE-10-1124
8. O’Keefe JH, Gheewala NM, O’Keefe JO (2008) Dietary strategies for improving post-prandial glucose, lipids, inflammation, and cardiovascular health. J Am Coll Cardiol 51(3):249–255. 10.1016/j.jacc.2007.10.016
9. Navarro E, Funtikova AN, Fíto M, Schröder H (2015) Can metabolically healthy obesity be explained by diet, genetics, and inflammation? Mol Nutr Food Res 59(1):75–93. 10.1002/mnfr.201400521
10. Connaughton RM, McMorrow AM, McGillicuddy FC, Lithander FE, Roche HM (2016) Impact of anti-inflammatory nutrients on obesity-associated metabolic-inflammation from childhood through to adulthood. Proc Nutr Soc 75(2):115–124. 10.1017/S0029665116000070
11. Chrysohoou C, Panagiotakos DB, Pitsavos C, Das UN, Stefanadis C (2004) Adherence to the Mediterranean diet attenuates inflammation and coagulation process in healthy adults: the ATTICA Study. J Am Coll Cardiol 44(1):152–158. 10.1016/j.jacc.2004.03.039
12. Casas R, Sacanella E, Estruch R (2014) The immune protective effect of the Mediterranean diet against chronic low-grade inflammatory diseases. Endocr Metab Immune Disord Drug Targets 14(4):245–254
13. Schwingshackl L, Hoffmann G (2014) Mediterranean dietary pattern, inflammation and endothelial function: a systematic review and meta-analysis of intervention trials. Nutr Metab Cardiovasc Dis 24(9):929–939. 10.1016/j.numecd.2014.03.003
14. Bonaccio M, Cerletti C, Iacoviello L, de Gaetano G (2015) Mediterranean diet and low-grade subclinical inflammation: the Moli-sani study. Endocr Metab Immune Disord Drug Targets 15(1):18–24
15. Root MM, McGinn MC, Nieman DC, Henson DA, Heinz SA, Shanely RA, Knab AM, Jin F (2012) Combined fruit and vegetable intake is correlated with improved inflammatory and oxidant status from a cross-sectional study in a community setting. Nutrients 4(1):29–41. 10.3390/nu4010029
16. Shivappa N, Hébert JR, Rietzschel ER, De Buyzere ML, Langlois M, Debruyne E, Marcos A, Huybrechts I (2015) Associations between dietary inflammatory index and inflammatory markers in the Asklepios Study. Br J Nutr 113(4):665–671. 10.1017/S000711451400395X
17. Lambert M, Delvin EE, Paradis G, O’Loughlin J, Hanley JA, Levy E (2004) C-reactive protein and features of the metabolic syndrome in a population-based sample of children and adolescents. Clin Chem 50(10):1762–1768. 10.1373/clinchem.2004.036418
18. McCrindle BW (2015) Cardiovascular consequences of childhood obesity. Can J Cardiol 31(2):124–130. 10.1016/j.cjca.2014.08.017
19. Moreno LA, De Henauw S, González-Gross M, Kersting M, Molnár D, Gottrand F, Barrios L, Sjöström M, Manios Y, Gilbert CC, Leclercq C, Widhalm K, Kafatos A, Marcos A, Group HS (2008) Design and implementation of the Healthy Lifestyle in Europe by Nutrition in Adolescence Cross-Sectional Study. Int J Obes (Lond) 32(Suppl 5):S4–S11. 10.1038/ijo.2008.177
20. Diethelm K, Huybrechts I, Moreno L, De Henauw S, Manios Y, Beghin L, González-Gross M, Le Donne C, Cuenca-García M, Castillo MJ, Widhalm K, Patterson E, Kersting M (2014) Nutrient intake of European adolescents: results of the HELENA (Healthy Lifestyle in Europe by Nutrition in Adolescence) Study. Public Health Nutr 17(3):486–497. 10.1017/S1368980013000463
21. Vereecken CA, Covents M, Matthys C, Maes L (2005) Young adolescents’ nutrition assessment on computer (YANA-C). Eur J Clin Nutr 59(5):658–667. 10.1038/sj.ejcn.1602124
22. Trichopoulou A, Kouris-Blazos A, Wahlqvist ML, Gnardellis C, Lagiou P, Polychronopoulos E, Vassilakou T, Lipworth L, Trichopoulos D (1995) Diet and overall survival in elderly people. BMJ 311(7018):1457–1460
23. Trichopoulou A, Costacou T, Bamia C, Trichopoulos D (2003) Adherence to a Mediterranean diet and survival in a Greek population. N Engl J Med 348(26):2599–2608. 10.1056/NEJMoa025039
24. Trichopoulou A (2004) Traditional Mediterranean diet and longevity in the elderly: a review. Public Health Nutr 7(7):943–947
25. Cole TJ, Bellizzi MC, Flegal KM, Dietz WH (2000) Establishing a standard definition for child overweight and obesity worldwide: international survey. BMJ 320(7244):1240–1243
26. Nagy E, Vicente-Rodriguez G, Manios Y, Béghin L, Iliescu C, Censi L, Dietrich S, Ortega FB, De Vriendt T, Plada M, Moreno LA, Molnar D, Group HS (2008) Harmonization process and reliability assessment of anthropometric measurements in a multicenter study in adolescents. Int J Obes (Lond) 32(Suppl 5):S58–S65. 10.1038/ijo.2008.184
27. Tanner JM, Whitehouse RH (1976) Clinical longitudinal standards for height, weight, height velocity, weight velocity, and stages of puberty. Arch Dis Child 51(3):170–179
28. González-Gross M, Breidenassel C, Gómez-Martínez S, Ferrari M, Béghin L, Spinneker A, Díaz LE, Maiani G, Demailly A, Al-Tahan J, Albers U, Wärnberg J, Stoffel-Wagner B, Jiménez-Pavón D, Libersa C, Pietrzik K, Marcos A, Stehle P (2008) Sampling and processing of fresh blood samples within a European multicenter nutritional study: evaluation of biomarker stability during transport and storage. Int J Obes (Lond) 32(Suppl 5):S66–S75. 10.1038/ijo.2008.185
29. Minihane AM, Vinoy S, Russell WR, Baka A, Roche HM, Tuohy KM, Teeling JL, Blaak EE, Fenech M, Vauzour D, McArdle HJ, Kremer BH, Sterkman L, Vafeiadou K, Benedetti MM, Williams CM, Calder PC (2015) Low-grade inflammation, diet composition and health: current research evidence and its translation. Br J Nutr 114(7):999–1012. 10.1017/S0007114515002093
30. Akdis M, Burgler S, Crameri R, Eiwegger T, Fujita H, Gomez E, Klunker S, Meyer N, O’Mahony L, Palomares O, Rhyner C, Ouaked N, Quaked N, Schaffartzik A, Van De Veen W, Zeller S, Zimmermann M, Akdis CA (2011) Interleukins, from 1 to 37, and interferon-γ: receptors, functions, and roles in diseases. J Allergy Clin Immunol 127(3):701–721.e701–770. 10.1016/j.jaci.2010.11.050
31. Targher G (2010) Elevated serum gamma-glutamyltransferase activity is associated with increased risk of mortality, incident type 2 diabetes, cardiovascular events, chronic kidney disease and cancer—a narrative review. Clin Chem Lab Med 48(2):147–157. 10.1515/CCLM.2010.031
32. Fraser A, Longnecker MP, Lawlor DA (2007) Prevalence of elevated alanine aminotransferase among US adolescents and associated factors: NHANES 1999–2004. Gastroenterology 133(6):1814–1820. 10.1053/j.gastro.2007.08.077
33. Martinez-Gomez D, Ortega FB, Ruiz JR, Vicente-Rodriguez G, Veiga OL, Widhalm K, Manios Y, Béghin L, Valtueña J, Kafatos A, Molnar D, Moreno LA, Marcos A, Castillo MJ, Sjöström M, Group Hs (2011) Excessive sedentary time and low cardiorespiratory fitness in European adolescents: the HELENA study. Arch Dis Child 96(3):240–246. 10.1136/adc.2010.187161
34. Vanhelst J, Béghin L, Turck D, Gottrand F (2011) New validated thresholds for various intensities of physical activity in adolescents using the Actigraph accelerometer. Int J Rehabil Res 34(2):175–177. 10.1097/MRR.0b013e328340129e
35. Jiménez Pavón D, Ortega FP, Ruiz JR, España Romero V, García Artero E, Moliner Urdiales D, Gómez Martínez S, Vicente Rodríguez G, Manios Y, Béghin L, Répasy J, Sjöstrom M, Moreno LA, González Gross M, Castillo MJ, Group HS (2010) Socioeconomic status influences physical fitness in European adolescents independently of body fat and physical activity: the HELENA study. Nutr Hosp 25(2):311–316
36. Hayes AF, Rockwood NJ (2016) Regression-based statistical mediation and moderation analysis in clinical research: observations, recommendations, and implementation. Behav Res Ther. 10.1016/j.brat.2016.11.001
37. Hayes A (2013) Introduction to mediation, moderation, and conditional process analysis: a regression-based approach. Guilford Publications, New York. ISBN 978-1-60918-230-4
38. Dai J, Miller AH, Bremner JD, Goldberg J, Jones L, Shallenberger L, Buckham R, Murrah NV, Veledar E, Wilson PW, Vaccarino V (2008) Adherence to the mediterranean diet is inversely associated with circulating interleukin-6 among middle-aged men: a twin study. Circulation 117(2):169–175. 10.1161/CIRCULATIONAHA.107.710699
39. Hoebeeck LI, Rietzschel ER, Langlois M, De Buyzere M, De Bacquer D, De Backer G, Maes L, Gillebert T, Huybrechts I (2011) The relationship between diet and subclinical atherosclerosis: results from the Asklepios Study. Eur J Clin Nutr 65(5):606–613. 10.1038/ejcn.2010.286
40. Dinarello CA (1997) Proinflammatory and anti-inflammatory cytokines as mediators in the pathogenesis of septic shock. Chest 112(6 Suppl):321S–329S
41. Calder PC (1998) Immunoregulatory and anti-inflammatory effects of n-3 polyunsaturated fatty acids. Braz J Med Biol Res 31(4):467–490
42. Giugliano D, Ceriello A, Esposito K (2006) The effects of diet on inflammation: emphasis on the metabolic syndrome. J Am Coll Cardiol 48(4):677–685. 10.1016/j.jacc.2006.03.052
43. Kiecolt-Glaser JK (2010) Stress, food, and inflammation: psychoneuroimmunology and nutrition at the cutting edge. Psychosom Med 72(4):365–369. 10.1097/PSY.0b013e3181dbf489
44. Border WA, Ruoslahti E (1992) Transforming growth factor-beta in disease: the dark side of tissue repair. J Clin Invest 90(1):1–7. 10.1172/JCI115821
45. Hasegawa T, Yoneda M, Nakamura K, Makino I, Terano A (2001) Plasma transforming growth factor-beta1 level and efficacy of alpha-tocopherol in patients with non-alcoholic steatohepatitis: a pilot study. Aliment Pharmacol Ther 15(10):1667–1672
46. Divoux A, Tordjman J, Lacasa D, Veyrie N, Hugol D, Aissat A, Basdevant A, Guerre-Millo M, Poitou C, Zucker JD, Bedossa P, Clément K (2010) Fibrosis in human adipose tissue: composition, distribution, and link with lipid metabolism and fat mass loss. Diabetes 59(11):2817–2825. 10.2337/db10-0585
47. Reggio S, Rouault C, Poitou C, Bichet JC, Prifti E, Bouillot JL, Rizkalla S, Lacasa D, Tordjman J, Clément K (2016) Increased basement membrane components in adipose tissue during obesity: links with TGFβ and metabolic phenotypes. J Clin Endocrinol Metab 101(6):2578–2587. 10.1210/jc.2015-4304
48. Parola M, Muraca R, Dianzani I, Barrera G, Leonarduzzi G, Bendinelli P, Piccoletti R, Poli G (1992) Vitamin E dietary supplementation inhibits transforming growth factor beta 1 gene expression in the rat liver. FEBS Lett 308(3):267–270
49. Koenig G, Seneff S (2015) Gamma-glutamyltransferase: a predictive biomarker of cellular antioxidant inadequacy and disease risk. Dis Markers 2015:818570. 10.1155/2015/818570
50. Lee DH, Blomhoff R, Jacobs DR (2004) Is serum gamma glutamyltransferase a marker of oxidative stress? Free Radic Res 38(6):535–539
51. Kunutsor SK (2016) Gamma-glutamyltransferase-friend or foe within? Liver Int 36(12):1723–1734. 10.1111/liv.13221
52. Whitfield JB (2001) Gamma glutamyl transferase. Crit Rev Clin Lab Sci 38(4):263–355. 10.1080/20014091084227
53. Mason JE, Starke RD, Van Kirk JE (2010) Gamma-glutamyl transferase: a novel cardiovascular risk biomarker. Prev Cardiol 13(1):36–41. 10.1111/j.1751-7141.2009.00054.x
54. Yamada J, Tomiyama H, Yambe M, Koji Y, Motobe K, Shiina K, Yamamoto Y, Yamashina A (2006) Elevated serum levels of alanine aminotransferase and gamma glutamyltransferase are markers of inflammation and oxidative stress independent of the metabolic syndrome. Atherosclerosis 189(1):198–205. 10.1016/j.atherosclerosis.2005.11.036
55. Whitfield JB (2007) Serum gamma-glutamyltransferase and risk of disease. Clin Chem 53(1):1–2. 10.1373/clinchem.2006.080911
56. Wiegand S, Keller KM, Röbl M, L’Allemand D, Reinehr T, Widhalm K, Holl RW, Adipositas A-SGatGCN (2010) Obese boys at increased risk for nonalcoholic liver disease: evaluation of 16,390 overweight or obese children and adolescents. Int J Obes (Lond) 34(10):1468–1474. 10.1038/ijo.2010.106
57. Marzuillo P, Grandone A, Perrone L, Miraglia Del Giudice E (2015) Understanding the pathophysiological mechanisms in the pediatric non-alcoholic fatty liver disease: The role of genetics. World J Hepatol 7(11):1439–1443. 10.4254/wjh.v7.i11.1439
58. Ahn MB, Bae WR, Han KD, Cho WK, Cho KS, Park SH, Jung MH, Suh BK (2015) Association between serum alanine aminotransferase level and obesity indices in Korean adolescents. Korean J Pediatr 58(5):165–171. 10.3345/kjp.2015.58.5.165
59. Kim WR, Flamm SL, Di Bisceglie AM, Bodenheimer HC, Disease PPCotAAftSoL (2008) Serum activity of alanine aminotransferase (ALT) as an indicator of health and disease. Hepatology 47(4):1363–1370. 10.1002/hep.22109
60. Boyraz M, Pirgon Ö, Dündar B, Çekmez F, Hatipoğlu N (2015) Long-term treatment with n-3 polyunsaturated fatty acids as a monotherapy in children with nonalcoholic fatty liver disease. J Clin Res Pediatr Endocrinol 7(2):121–127. 10.4274/jcrpe.1749
61. Zhu FS, Liu S, Chen XM, Huang ZG, Zhang DW (2008) Effects of n-3 polyunsaturated fatty acids from seal oils on nonalcoholic fatty liver disease associated with hyperlipidemia. World J Gastroenterol 14(41):6395–6400
62. Nobili V, Bedogni G, Alisi A, Pietrobattista A, Risé P, Galli C, Agostoni C (2011) Docosahexaenoic acid supplementation decreases liver fat content in children with non-alcoholic fatty liver disease: double-blind randomised controlled clinical trial. Arch Dis Child 96(4):350–353. 10.1136/adc.2010.192401
63. Rodríguez G, Moreno LA, Blay MG, Blay VA, Fleta J, Sarría A, Bueno M, Group A-ZS (2005) Body fat measurement in adolescents: comparison of skinfold thickness equations with dual-energy X-ray absorptiometry. Eur J Clin Nutr 59(10):1158–1166. 10.1038/sj.ejcn.1602226
64. Sarría A, García-Llop LA, Moreno LA, Fleta J, Morellón MP, Bueno M (1998) Skinfold thickness measurements are better predictors of body fat percentage than body mass index in male Spanish children and adolescents. Eur J Clin Nutr 52(8):573–576