Advertisement

Mediterranean diet, physical activity and subcutaneous advanced glycation end-products’ accumulation: a cross-sectional analysis in the ILERVAS project

  • Enric Sánchez
  • Àngels Betriu
  • Jordi Salas-Salvadó
  • Reinald Pamplona
  • Ferrán Barbé
  • Francesc Purroy
  • Cristina Farràs
  • Elvira Fernández
  • Carolina López-Cano
  • Chadia Mizab
  • Albert LecubeEmail author
  • the ILERVAS project investigators
Original Contribution

Abstract

Purpose

Adherence to Mediterranean diet (MedDiet) and physical activity have been associated to lower cardiovascular risk and mortality. Our purpose was to test the modification of advanced glycation end-products (AGEs) as one of the underlying mechanisms explaining this relationship.

Methods

Cross-sectional study assessing the adherence to MedDiet (14-item Mediterranean Diet Adherence Screener) and physical activity (International Physical Activity Questionnaire short form) in 2646 middle-aged subjects without known cardiovascular disease and type 2 diabetes from the ILERVAS study. Skin autofluorescence (SAF), a non-invasive assessment of subcutaneous AGEs, was measured. Multivariable logistic regression models were done to study interactions and independent associations with a likelihood ratio test.

Results

Participants with a high adherence to MedDiet had lower SAF than those with low adherence (1.8 [IR 1.6; 2.1] vs. 2.0 [IR 1.7; 2.3] arbitrary units, p < 0.001), without differences according to categories of physical activity. There was an independent association between high adherence to MedDiet and the SAF values [OR 0.59 (0.37–0.94), p = 0.026]. When adherence to MedDiet was substituted by its individual food components, high intake of vegetables, fruits and nuts, and low intake of sugar-sweetened soft beverages were independently associated with a decreased SAF (p ≤ 0.045). No interaction between MedDiet and physical activity on SAF values was observed except for nuts consumption (p = 0.047).

Conclusions

Adherence to the MedDiet, but not physical activity, was negatively associated to SAF measurements. This association can be explained by some typical food components of the MedDiet. The present study offers a better understanding of the plausible biological conditions underlying the prevention of cardiovascular disease with MedDiet.

ClinTrials.gov identifier: NCT03228459.

Keywords

Advanced glycation end-products Mediterranean diet Physical activity Questionnaire Skin autofluorescence 

Notes

Acknowledgements

This study was supported by Grants from the Diputació de Lleida, Generalitat de Catalunya (2017SGR696 and SLT0021600250) and Instituto de Salud Carlos III (Action Plan II14//00008). CIBER de Diabetes y Enfermedades Metabólicas Asociadas and CIBER de Enfermedades Respiratorias are initiatives of the Instituto de Salud Carlos III. The authors would also like to thank Fundació Renal Jaume Arnó, all Nurses of the Bus of health and the Primary Care Lleida Units for recruiting subjects and their efforts in the accurate development of the ILERVAS project.

Author contributions

ÀB, RP, FB, FP, CF, EF, and AL designed the research; ES CL-C and CM: conducted the research; ES and JS-S analysed data; ES, ÀB and AL wrote the paper; AL had primary responsibility for final content. All authors have read and approved the final manuscript.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no competing interests.

Ethical approval

The protocol was approved by the Arnau de Vilanova University Hospital ethics committee (CEIC-1410). Additionally, the study was conducted according to the ethical guidelines of the Helsinki Declaration and Spanish legislation regarding the protection of personal information was also followed.

Informed consent

Informed consent was obtained from all individual participants included in the study.

Supplementary material

394_2019_1983_MOESM1_ESM.tif (44.3 mb)
Supplementary material 1 (TIFF 45355 kb)
394_2019_1983_MOESM2_ESM.docx (13 kb)
Supplementary file2 (DOCX 12 kb)

References

  1. 1.
    Eckel RH, Jakicic JM, Ard JD et al (2014) 2013 AHA/ACC guideline on lifestyle management to reduce cardiovascular risk: a report of the American College of Cardiology/American Heart Association Task Force on Practice Guidelines. Circulation 129(25 Suppl 2):S76–99CrossRefGoogle Scholar
  2. 2.
    US Department of Health and Human Services (2008) Physical activity guidelines for americans. Washington, DC: US Department of Health and Human Services, pp 1–61. https://www.health.gov/PAGuidelines. Accessed 28 Jan 2018
  3. 3.
    Masana L, Ros E, Sudano I, Angoulvant D, Lifestyle Expert Working Group (2017) Is there a role for lifestyle changes in cardiovascular prevention? What, when and how? Atheroscler Suppl 26:2–15CrossRefGoogle Scholar
  4. 4.
    Estruch R, Ros E, Salas-Salvadó J et al (2018) Retraction and republication: primary prevention of cardiovascular disease with a Mediterranean Diet. N Engl J Med 2013 368:1279–1290 (N Engl J Med. 378: 2441–2442) Google Scholar
  5. 5.
    Garcia M, Bihuniak JD, Shook J et al (2016) The effect of the traditional Mediterranean-Style Diet on metabolic risk factors: a meta-analysis. Nutrients 8:168CrossRefGoogle Scholar
  6. 6.
    Salas-Salvadó J, Becerra-Tomás N, García-Gavilán JF et al (2018) Mediterranean Diet and cardiovascular disease prevention: what do we know? Prog Cardiovasc Dis 61:62–67CrossRefGoogle Scholar
  7. 7.
    Fitó M, Guxens M, Corella D et al (2007) Effect of a traditional Mediterranean diet on lipoprotein oxidation: a randomized controlled trial. Arch Intern Med 167:1195–1203CrossRefGoogle Scholar
  8. 8.
    Mena MP, Sacanella E, Vazquez-Agell M et al (2009) Inhibition of circulating immune cell activation: a molecular antiinflammatory effect of the Mediterranean diet. Am J Clin Nutr 89:248–256CrossRefGoogle Scholar
  9. 9.
    Fuentes F, López-Miranda J, Sánchez E et al (2001) Mediterranean and low-fat diets improve endothelial function in hypercholesterolemic men. Ann Intern Med 134:1115–1119CrossRefGoogle Scholar
  10. 10.
    Gielen S, Schuler G, Adams V (2010) Cardiovascular effects of exercise training: molecular mechanisms. Circulation 122:1221–1238CrossRefGoogle Scholar
  11. 11.
    Hambrecht R, Adams V, Erbs S et al (2003) Regular physical activity improves endothelial function in patients with coronary artery disease by increasing phosphorylation of endothelial nitric oxide synthase. Circulation 107:3152–3158CrossRefGoogle Scholar
  12. 12.
    Kuo L, Davis MJ, Chilian WM (1995) Longitudinal gradients for endothelium-dependent and-independent vascular responses in the coronary microcirculation. Circulation 92:518–525CrossRefGoogle Scholar
  13. 13.
    Laufs U, Wassmann S, Czech T et al (2005) Physical inactivity increases oxidative stress, endothelial dysfunction, and atherosclerosis. Arterioscler Thromb Vasc Biol 25:809–814CrossRefGoogle Scholar
  14. 14.
    Willemsen S, Hartog JW, Hummel YM et al (2011) Tissue advanced glycation end products are associated with diastolic function and aerobic exercise capacity in diabetic heart failure patients. Eur J Heart Fail 13:76–82CrossRefGoogle Scholar
  15. 15.
    Kotani K, Caccavello R, Sakane N et al (2011) Influence of physical activity intervention on circulating soluble receptor for advanced glycation end products in elderly subjects. J Clin Med Res 3:252–257Google Scholar
  16. 16.
    Nilsson A, Bergens O, Kadi F (2018) Physical activity alters inflammation in older adults by different intensity levels. Med Sci Sports Exerc 50:1502–1507CrossRefGoogle Scholar
  17. 17.
    Kaltsatou A, Karatzaferi C, Mitrou GI et al (2016) Intra-renal hemodynamic changes after habitual physical activity in patients with chronic kidney disease. Curr Pharm Des 22:3700–3714CrossRefGoogle Scholar
  18. 18.
    Chakravarthy U, Hayes RG, Stitt AW et al (1998) Constitutive nitric oxide synthase expression in retinal vascular endothelial cells is suppressed by high glucose and advanced glycation end products. Diabetes 47:945–952CrossRefGoogle Scholar
  19. 19.
    Barbato JE, Tzeng E (2004) Nitric oxide and arterial disease. J Vasc Surg 40:187–193CrossRefGoogle Scholar
  20. 20.
    Chaudhuri J, Bains Y, Guha S et al (2018) The role of advanced glycation end products in aging and metabolic diseases: bridging association and causality. Cell Metab 28:337–352CrossRefGoogle Scholar
  21. 21.
    Hanssen NM, Wouters K, Huijberts MS et al (2014) Higher levels of advanced glycation endproducts in human carotid atherosclerotic plaques are associated with a rupture-prone phenotype. Eur Heart J 35:1137–1146CrossRefGoogle Scholar
  22. 22.
    Couppé C, Dall CH, Svensson RB et al (2017) Skin autofluorescence is associated with arterial stiffness and insulin level in endurance runners and healthy controls—effects of aging and endurance exercise. Exp Gerontol 91:9–14CrossRefGoogle Scholar
  23. 23.
    Momma H, Niu K, Kobayashi Y et al (2011) Skin advanced glycation end product accumulation and muscle strength among adult men. Eur J Appl Physiol 111:1545–1552CrossRefGoogle Scholar
  24. 24.
    Momma H, Niu K, Kobayashi Y et al (2012) Skin advanced glycation end-product accumulation is negatively associated with calcaneal osteo-sono assessment index among non-diabetic adult Japanese men. Osteoporosis Int 23:1673–1681CrossRefGoogle Scholar
  25. 25.
    Kato M, Kubo A, Sugioka Y et al (2017) Relationship between advanced glycation end-product accumulation and low skeletal muscle mass in Japanese men and women. Geriatr Gerontol Int 17:785–790CrossRefGoogle Scholar
  26. 26.
    Couppé C, Svensson RB, Grosset JF et al (2014) Life-long endurance running is associated with reduced glycation and mechanical stress in connective tissue. Age (Dordr) 36:9665CrossRefGoogle Scholar
  27. 27.
    Uribarri J, Woodruff S, Goodman S et al (2010) Advanced glycation end products in foods and a practical guide to their reduction in the diet. J Am Diet Assoc 110:911–16.e12CrossRefGoogle Scholar
  28. 28.
    Thorpe SR, Baynes JW (2003) Maillard reaction products in tissue proteins: new products and new perspectives. Amino Acids 25:275–281CrossRefGoogle Scholar
  29. 29.
    Betriu À, Farràs C, Abajo M et al (2016) Randomised intervention study to assess the prevalence of subclinical vascular disease and hidden kidney disease and its impact on morbidity and mortality: the ILERVAS project. Nefrologia 36:389–396CrossRefGoogle Scholar
  30. 30.
    Bolíbar B, Fina Avilés F, Morros R et al (2012) SIDIAP database: electronic clinical records in primary care as a source of information for epidemiologic research. Med Clin (Barc) 138:617–621CrossRefGoogle Scholar
  31. 31.
    American Diabetes Association (2019) Classification and diagnosis of diabetes: standards of medical care in diabetes—2019. Diabetes Care 42:S13–S28CrossRefGoogle Scholar
  32. 32.
    Schröder H, Fitó M, Estruch R et al (2011) A short screener is valid for assessing mediterranean diet adherence among older Spanish men and women. J Nutr 141:1140–1145CrossRefGoogle Scholar
  33. 33.
    Estruch R, Martínez-González MA, Corella D et al (2006) Effects of a Mediterranean-style diet on cardiovascular risk factors: a randomized trial. Ann Intern Med 145:1–11CrossRefGoogle Scholar
  34. 34.
    Craig CL, Marshall AL, Sjöström M et al (2003) International physical activity questionnaire: 12-country reliability and validity. Med Sci Sports Exerc 35:1381–1395CrossRefGoogle Scholar
  35. 35.
    Meerwaldt R, Graaff R, Oomen PHN et al (2004) Simple non-invasive assessment of advanced glycation endproduct accumulation. Diabetologia 47:1324–1330CrossRefGoogle Scholar
  36. 36.
    Koetsier M, Lutgers HL, de Jonge C et al (2010) Reference values of skin autofluorescence. Diabetes Technol Ther 12:399–403CrossRefGoogle Scholar
  37. 37.
    Hill AB (1965) The environment and disease: association or causation? Proc R Soc Med 58:295–300Google Scholar
  38. 38.
    Trichopoulou A (2004) Traditional Mediterranean diet and longevity in the elderly: a review. Public Health Nutr 7:943–947CrossRefGoogle Scholar
  39. 39.
    Lopez-Moreno J, Quintana-Navarro GM, Delgado-Lista J et al (2016) Mediterranean diet reduces serum advanced glycation end products and increases antioxidant defences in elderly adults: a randomized controlled trial. J Am Geriatr Soc 64:901–904CrossRefGoogle Scholar
  40. 40.
    Rodríguez JM, Leiva Balich L, Concha MJ et al (2015) Reduction of serum advanced glycation end-products with a low calorie Mediterranean diet. Nutr Hosp 31:2511–2517Google Scholar
  41. 41.
    Kellow NJ, Coughlan MT, Reid CM (2018) Association between habitual dietary and lifestyle behaviours and skin autofluorescence (SAF), a marker of tissue accumulation of advanced glycation endproducts (AGEs), in healthy adults. Eur J Nutr 57:2209–2216CrossRefGoogle Scholar
  42. 42.
    Chow CK, Jolly S, Rao-Melacini P et al (2010) Association of diet, exercise, and smoking modification with risk of early cardiovascular events after acute coronary syndromes. Circulation 121:750–758CrossRefGoogle Scholar
  43. 43.
    Alvarez-Alvarez I, de Rojas JP, Fernandez-Montero A et al (2018) Strong inverse associations of Mediterranean diet, physical activity and their combination with cardiovascular disease: the Seguimiento Universidad de Navarra (SUN) cohort. Eur J Prev Cardiol 25:1186–1197CrossRefGoogle Scholar
  44. 44.
    Pereira MA (2014) Sugar-sweetened and artificially-sweetened beverages in relation to obesity risk. Adv Nutr 5:797–808CrossRefGoogle Scholar
  45. 45.
    Imamura F, O'Connor L, Ye Z et al (2015) Consumption of sugar sweetened beverages, artificially sweetened beverages, and fruit juice and incidence of type 2 diabetes: systematic review, meta-analysis, and estimation of population attributable fraction. BMJ 351:h3576CrossRefGoogle Scholar
  46. 46.
    Narain A, Kwok CS, Mamas MA (2017) Soft drink intake and the risk of metabolic syndrome: a systematic review and meta-analysis. Int J Clin Pract.  https://doi.org/10.1111/ijcp.12927 Google Scholar
  47. 47.
    Cheungpasitporn W, Thongprayoon C, Edmonds PJ et al (2015) Sugar and artificially sweetened soda consumption linked to hypertension: a systematic review and meta-analysis. Clin Exp Hypertens 37:587–593CrossRefGoogle Scholar
  48. 48.
    Cheungpasitporn W, Thongprayoon C, O'Corragain OA et al (2014) Associations of sugar-sweetened and artificially sweetened soda with chronic kidney disease: a systematic review and meta-analysis. Nephrology (Carlton) 19:791–797CrossRefGoogle Scholar
  49. 49.
    Siqueira JM, Mill JG, Velasquez-Melendez G et al (2018) Sugar-sweetened soft drinks and fructose consumption are associated with hyperuricemia: cross-sectional analysis from the Brazilian Longitudinal Study of Adult Health (ELSA-Brasil). Nutrients 10:E981CrossRefGoogle Scholar
  50. 50.
    Trichopoulou A, Martínez-González MA, Tong TY et al (2014) Definitions and potential health benefits of the Mediterranean diet: views from experts around the world. BMC Med 12:112CrossRefGoogle Scholar
  51. 51.
    Trichopoulou A, Bamia C, Trichopoulous D (2009) Anatomy of health effects of Mediterranean diet Greek EPIC prospective cohort study. BMJ 338:b2337CrossRefGoogle Scholar
  52. 52.
    Hernandez-Hernandez A, Gea A, Ruiz-Canela M et al (2015) Mediterranean alcohol-drinking pattern and the incidence of cardiovascular disease and cardiovascular mortality: the SUN project. Nutrients 7:9116–9126CrossRefGoogle Scholar
  53. 53.
    Gea A, Bes-Rastrollo M, Toledo E et al (2014) Mediterranean alcohol-drinking pattern and mortality in the SUN (Seguimiento Universidad de Navarra) Project: a prospective cohort study. Br J Nutr 111:1871–1880CrossRefGoogle Scholar
  54. 54.
    Del Turco S, Basta G (2016) Can dietary polyphenols prevent the formation of toxic compounds from Maillard reaction? Curr Drug Metab 17:598–607CrossRefGoogle Scholar
  55. 55.
    Haseeb S, Alexander B, Baranchuk A (2017) Wine and cardiovascular health: a comprehensive review. Circulation 136:1434–1448CrossRefGoogle Scholar
  56. 56.
    Pavlidou E, Mantzorou M, Fasoulas A et al (2018) Wine: an aspiring agent in promoting longevity and preventing chronic diseases. Diseases 6:E73CrossRefGoogle Scholar
  57. 57.
    Snopek L, Mlcek J, Sochorova L et al (2018) Contribution of red wine consumption to human health protection. Molecules 23:E1684CrossRefGoogle Scholar
  58. 58.
    Hansen AL, Carstensen B, Helge JW et al (2013) Combined heart rate- and accelerometer-assessed physical activity energy expenditure and associations with glucose homeostasis markers in a population at high risk of developing diabetes: the ADDITION-PRO study. Diabetes Care 36:3062–3069CrossRefGoogle Scholar
  59. 59.
    Taber DR, Stevens J, Murray DM et al (2009) The effect of a physical activity intervention on bias in self-reported activity. Ann Epidemiol 19:316–322CrossRefGoogle Scholar
  60. 60.
    Drenth H, Zuidema SU, Krijnen WP et al (2018) Advanced glycation end-products are associated with physical activity and physical functioning in the older population. J Gerontol A Biol Sci Med Sci. 73:1545–1551CrossRefGoogle Scholar
  61. 61.
    Mori H, Kuroda A, Araki M et al (2017) Advanced glycation end-products are a risk for muscle weakness in Japanese patients with type 1 diabetes. J Diabetes Investig 8:377–382CrossRefGoogle Scholar
  62. 62.
    Duda-Sobczak A, Falkowski B, Araszkiewicz A, Zozulinska-Ziolkiewicz D (2018) Association between self-reported physical activity and skin autofluorescence, a marker of tissue accumulation of advanced glycation end products in adults with type 1 diabetes: a cross-sectional study. Clin Ther 40:872–880CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  • Enric Sánchez
    • 1
  • Àngels Betriu
    • 2
  • Jordi Salas-Salvadó
    • 3
    • 4
  • Reinald Pamplona
    • 5
  • Ferrán Barbé
    • 6
    • 7
  • Francesc Purroy
    • 8
  • Cristina Farràs
    • 9
  • Elvira Fernández
    • 2
  • Carolina López-Cano
    • 1
  • Chadia Mizab
    • 1
  • Albert Lecube
    • 1
    • 10
    Email author
  • the ILERVAS project investigators
  1. 1.Endocrinology and Nutrition DepartmentUniversity Hospital Arnau de Vilanova, Obesity, Diabetes and Metabolism (ODIM) Research Group, IRBLleida, University of LleidaLleidaSpain
  2. 2.Unit for the Detection and Treatment of Atherothrombotic Diseases (UDETMA V&R)University Hospital Arnau de Vilanova, Vascular and Renal Translational Research Group, IRBLleida, University of LleidaLleidaSpain
  3. 3.Department of Human Nutrition Unit, Biochemistry and Biotechnology, Faculty of Medicine and Health SciencesUniversity Hospital of Sant Joan de Reus, IISPV, Rovira i Virgili UniversityReusSpain
  4. 4.Centro de Investigación Biomédica en Red de Fisiopatología de la Obesidad y la Nutrición (CIBEROBN), Instituto de Salud Carlos III (ISCIII)MadridSpain
  5. 5.Experimental Medicine DepartmentIRBLleida, University of LleidaLleidaSpain
  6. 6.Respiratory DepartmentUniversity Hospital Arnau de Vilanova-Santa María, Translational Research in Respiratory Medicine, IRBLleida, University of LleidaLleidaSpain
  7. 7.Centro de Investigación Biomédica en Red de Enfermedades Respiratorias (CIBERES), Instituto de Salud Carlos III (ISCIII)MadridSpain
  8. 8.Stroke UnitUniversity Hospital Arnau de Vilanova, Clinical Neurosciences Group, IRBLleida, University of LleidaLleidaSpain
  9. 9.Primary Health Care UnitLleidaSpain
  10. 10.Centro de Investigación Biomédica en Red de Diabetes y Enfermedades Metabólicas Asociadas (CIBERDEM), Instituto de Salud Carlos III (ISCIII)MadridSpain

Personalised recommendations