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Moderate effects of apple juice consumption on obesity-related markers in obese men: impact of diet–gene interaction on body fat content

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Abstract

Purpose

The effect of polyphenol-rich cloudy apple juice (CloA) consumption on plasma parameters related to the obesity phenotype and potential effects of interactions between CloA and allelic variants in obesity candidate genes were assessed in obese men.

Methods

In this controlled, randomized, and parallel study, n = 68, non-smoking, non-diabetic men with a BMI ≥27 kg/m2 received 750 mL/day CloA (802.5 mg polyphenols) or 750 mL/day control beverage (CB, isocaloric equivalent to CloA) for 4 weeks. Further, study participants were genotyped for single-nucleotide polymorphisms in PPARγ (rs1801282), UCP3 (rs1800849), IL-6 (rs1800795), FABP2 (rs1799883), INSIG2 (rs7566605), and PGC1 (rs8192678) genes. At the beginning and at the end of intervention plasma lipids, distinct adipokines and cytokines as well as anthropometric parameters were determined.

Results

CloA compared to CB had no significant effect on plasma lipids, plasma adipokine and cytokine levels, BMI, and waist circumference. However, CloA consumption significantly reduced percent body fat compared to CB (∆ % body fat: CloA: −1.0 ± 1.3 vs. CB: −0.2 ± 0.9, p < 0.05). The IL-6-174 G/C polymorphism showed an interaction with body fat reduction induced by CloA. Solely in C/C, but not in G/C or G/G variants, a significant reduction in body fat after 4 weeks of CloA intervention was detectable.

Conclusion

The observed diet–gene interaction might be a first indication for the impact of individual genetic background on CloA-mediated bioactivity on obesity-associated comorbidities.

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References

  1. Berghofer A, Pischon T, Reinhold T, Apovian CM, Sharma AM, Willich SN (2008) Obesity prevalence from a European perspective: a systematic review. BMC Public Health 8:200

    Article  Google Scholar 

  2. Kopelman PG (2000) Obesity as a medical problem. Nature 404:635–643

    CAS  Google Scholar 

  3. Rolls BJ, Ello-Martin JA, Tohill BC (2004) What can intervention studies tell us about the relationship between fruit and vegetable consumption and weight management? Nutr Rev 62:1–17

    Article  Google Scholar 

  4. Prentice AM, Jebb SA (2003) Fast foods, energy density and obesity: a possible mechanistic link. Obes Rev 4:187–194

    Article  CAS  Google Scholar 

  5. Hsu CL, Yen GC (2008) Phenolic compounds: evidence for inhibitory effects against obesity and their underlying molecular signaling mechanisms. Mol Nutr Food Res 52:53–61

    Article  CAS  Google Scholar 

  6. Pinent M, Blade C, Salvado MJ, Blay M, Pujadas G, Fernandez-Larrea J, Arola L, Ardevol A (2006) Procyanidin effects on adipocyte-related pathologies. Crit Rev Food Sci Nutr 46:543–550

    Article  CAS  Google Scholar 

  7. Tsuda T (2008) Regulation of adipocyte function by anthocyanins; possibility of preventing the metabolic syndrome. J Agric Food Chem 56:642–646

    Article  CAS  Google Scholar 

  8. Knekt P, Kumpulainen J, Jarvinen R, Rissanen H, Heliovaara M, Reunanen A, Hakulinen T, Aromaa A (2002) Flavonoid intake and risk of chronic diseases. Am J Clin Nutr 76:560–568

    CAS  Google Scholar 

  9. Vinson JA, Su X, Zubik L, Bose P (2001) Phenol antioxidant quantity and quality in foods: fruits. J Agric Food Chem 49:5315–5321

    Article  CAS  Google Scholar 

  10. Aprikian O, Busserolles J, Manach C, Mazur A, Morand C, Davicco MJ, Besson C, Rayssiguier Y, Remesy C, Demigne C (2002) Lyophilized apple counteracts the development of hypercholesterolemia, oxidative stress, and renal dysfunction in obese Zucker rats. J Nutr 132:1969–1976

    CAS  Google Scholar 

  11. Osada K, Suzuki T, Kawakami Y, Senda M, Kasai A, Sami M, Ohta Y, Kanda T, Ikeda M (2006) Dose-dependent hypocholesterolemic actions of dietary apple polyphenol in rats fed cholesterol. Lipids 41:133–139

    Article  CAS  Google Scholar 

  12. Ohta Y, Sami M, Kanda T, Saito K, Osada K, Kato H (2006) Gene expression analysis of the anti-obesity effect by apple polyphenols in rats fed a high fat diet or a normal diet. J Oleo Sci 55:305–314

    Article  CAS  Google Scholar 

  13. Osada K, Funayama M, Fuchi S, Sami M, Ohta Y, Kanda T, Ikeda M (2006) Effects of dietary procyanidins and tea polyphenols on adipose tissue mass and fatty acid metabolism in rats on a high fat diet. J Oleo Sci 55:79–89

    Article  CAS  Google Scholar 

  14. Nagasako-Akazome Y, Kanda T, Ohtake Y, Shimasaki H, Kobayashi T (2007) Apple polyphenols influence cholesterol metabolism in healthy subjects with relatively high body mass index. J Oleo Sci 56:417–428

    Article  CAS  Google Scholar 

  15. deOliveira MC, Sichieri R, Venturim MR (2008) A low-energy-dense diet adding fruit reduces weight and energy intake in women. Appetite 51:291–295

    Article  Google Scholar 

  16. Song Y, Manson JE, Buring JE, Sesso HD, Liu S (2005) Associations of dietary flavonoids with risk of type 2 diabetes, and markers of insulin resistance and systemic inflammation in women: a prospective study and cross-sectional analysis. J Am Col Nutr 24:376–384

    CAS  Google Scholar 

  17. Scalbert A, Manach C, Morand C, Remesy C, Jimenez L (2005) Dietary polyphenols and the prevention of disease. Crit Rev Food Sci Nutr 45:287–306

    Article  CAS  Google Scholar 

  18. Koch TC, Briviba K, Watzl B, Fähndrich C, Bub A, Rechkemmer G, Barth SW (2009) Prevention of colon carcinogenesis by apple juice in vivo: impact of juice constituents and obesity. Mol Nutr Food Res 53:1289–1302

    Article  CAS  Google Scholar 

  19. Matsui N, Ito R, Nishimura E, Yoshikawa M, Kato M, Kamei M, Shibata H, Matsumoto I, Abe K, Hashizume S (2005) Ingested cocoa can prevent high-fat diet-induced obesity by regulating the expression of genes for fatty acid metabolism. Nutrition 21:594–601

    Article  CAS  Google Scholar 

  20. Terra X, Montagut G, Bustos M, Llopiz N, Ardevol A, Blade C, Fernandez-Larrea J, Pujadas G, Salvado J, Arola L, Blay M (2009) Grape-seed procyanidins prevent low-grade inflammation by modulating cytokine expression in rats fed a high-fat diet. J Nutr Biochem 20:210–218

    Article  CAS  Google Scholar 

  21. Hofker M, Wijmenga C (2009) A supersized list of obesity genes. Nat Genet 41:139–140

    Article  CAS  Google Scholar 

  22. Rankinen T, Zuberti A, Chagnon YC, Weisnagel SJ, Argyropoulos G, Walts B (2006) The human obesity gene map: the 2005 update. Obesity 14:529–644

    Article  Google Scholar 

  23. Barth SW, Fahndrich C, Bub A, Dietrich H, Watzl B, Will F, Briviba K, Rechkemmer G (2005) Cloudy apple juice decreases DNA damage, hyperproliferation and aberrant crypt foci development in the distal colon of DMH-initiated rats. Carcinogenesis 26:1414–1421

    Article  CAS  Google Scholar 

  24. Newton CR, Graham A, Heptinstall LE, Powell SJ, Summers C, Kalsheker N, Smith JC, Markham AF (1989) Analysis of any point mutation in DNA. The amplification refractory mutation system (ARMS). Nucleic Acids Res 17:2503–2516

    Article  CAS  Google Scholar 

  25. Okayama H, Curiel DT, Brantly ML, Holmes MD, Crystal RG (1989) Rapid, nonradioactive detection of mutations in the human genome by allele-specific amplification. J Lab Clin Med 114:105–113

    CAS  Google Scholar 

  26. Nazarenko IA, Bhatnagar SK, Hohman RJ (1997) A closed tube format for amplification and detection of DNA based on energy transfer. Nucleic Acids Res 25:2516–2521

    Article  CAS  Google Scholar 

  27. Nakazato K, Song H, Waga T (2006) Effects of dietary apple polyphenol on adipose tissues weights in Wistar rats. Exp Anim 55:383–389

    Article  CAS  Google Scholar 

  28. Akazome Y, Kametani N, Kanda T, Shimasaki H, Kobayashi S (2010) Evaluation of safety of excessive intake and efficacy of long-term intake of beverages containing apple polyphenols. J Oleo Sci 59:321–333

    Article  CAS  Google Scholar 

  29. Moreno-Aliaga MJ, Santos JL, Marti A, Martinez JA (2005) Does weight loss prognosis depend on genetic make-up? Obes Rev 6:155–168

    Article  CAS  Google Scholar 

  30. Wernstedt I, Eriksson AL, Berndtsson A, Hoffstedt J, Skrtic S, Hedner T, Hultén LM, Wiklund O, Ohlsson C, Jansson JO (2004) A common polymorphism in the interleukin-6 gene promoter is associated with overweight. Int J Obes Relat Metab Disord 28:1272–1279

    Article  CAS  Google Scholar 

  31. Strandberg L, Mellström D, Ljunggren O, Grundberg E, Karlsson MK, Holmberg AH, Orwoll ES, Eriksson AL, Svedberg J, Bengtsson M, Ohlsson C, Jansson JO (2008) IL6 and IL1B polymorphisms are associated with fat mass in older men: the MrOS Study Sweden. Obesity 16:710–713

    Article  CAS  Google Scholar 

  32. Humphries SE, Luong LA, Ogg MS, Hawe E, Miller GJ (2001) The interleukin-6-174 G/C promoter polymorphism is associated with risk of coronary heart disease and systolic blood pressure in healthy men. Eur Heart J 22:2243–2252

    Article  CAS  Google Scholar 

  33. Herbert A, Liu C, Karamohamed S, Liu J, Manning A, Fox CS, Meigs JB, Cupples LA (2006) BMI modifies associations of IL-6 genotypes with insulin resistance: the Framingham Study. Obesity 14:1454–1461

    Article  CAS  Google Scholar 

  34. Goyenechea E, Parra D, Martínez JA (2007) Impact of interleukin 6–174G&gt;C polymorphism on obesity-related metabolic disorders in people with excess in body weight. Metabolism 56:1643–1648

    Article  CAS  Google Scholar 

  35. Bobe G, Murphy G, Albert PS, Sansbury LB, Young MR, Lanza E, Schatzkin A, Colburn NH, Cross AJ (2011) Do interleukin polymorphisms play a role in the prevention of colorectal adenoma recurrence by dietary flavonols? Eur J Cancer Prev 20:86–95

    Article  CAS  Google Scholar 

  36. Marotta F, Koike K, Lorenzetti A, Naito Y, Fayet F, Shimizu H, Marandola P (2007) Nutraceutical strategy in aging: targeting heat shock protein and inflammatory profile through understanding interleukin-6 polymorphism. Ann NY Acad Sci 1119:196–202

    Article  CAS  Google Scholar 

  37. Ukkola O, Tremblay A, Sun G, Chagnon YC, Bouchard C (2001) Genetic variation at the uncoupling protein 1, 2 and 3 loci and the response to long-term overfeeding. Eur J Clin Nutr 55:1008–1015

    Article  CAS  Google Scholar 

  38. Yoon Y, Park BL, Cha MN, Kim KS, Cheong HS, Choi YH, Shin HD (2007) Effects of genetic polymorphisms of UCP2 and UCP3 on very low calorie diet-induced body fat reduction in Korean female subjects. Biochem Biophys Res Commun 359:451–456

    Article  CAS  Google Scholar 

  39. Ricciardi R, Talbot LA (2007) Use of bioelectrical impedance analysis in the evaluation, treatment, and prevention of overweight and obesity. J Am Acad Nurse Pract 19:235–241

    Article  Google Scholar 

  40. Sugiyama H, Akazome Y, Shoji T, Yamaguchi A, Yasue M, Kanda T, Ohtake Y (2007) Oligomeric procyanidins in apple polyphenol are main active components for inhibition of pancreatic lipase and triglyceride absorption. J Agric Food Chem 55:4604–4609

    Article  CAS  Google Scholar 

  41. de la Garza AL, Milagro FI, Boque N, Campión J, Martínez JA (2011) Natural inhibitors of pancreatic lipase as new players in obesity treatment. Planta Med 77:773–785

    Article  Google Scholar 

  42. Pinent M, Blade MC, Salvado MJ, Arola L, Ardevol A (2005) Intracellular mediators of procyanidin-induced lipolysis in 3T3-L1 adipocytes. J Agric Food Chem 53:262–266

    Article  CAS  Google Scholar 

  43. Vogels N, Nijs IM, Westerterp-Plantenga MS (2004) The effect of grape-seed extract on 24 h energy intake in humans. Eur J Clin Nutr 58:667–673

    Article  CAS  Google Scholar 

  44. Ardevol A, Blade C, Salvado MJ, Arola L (2000) Changes in lipolysis and hormone-sensitive lipase expression caused by procyanidins in 3T3-L1 adipocytes. Int J Obes Relat Metab Disord 24:319–324

    Article  CAS  Google Scholar 

  45. Hsu CL, Yen GC (2007) Effects of flavonoids and phenolic acids on the inhibition of adipogenesis in 3T3-L1 adipocytes. J Agric Food Chem 55:8404–8410

    Article  CAS  Google Scholar 

  46. Pinent M, Blade MC, Salvado MJ, Arola L, Hackl H, Quackenbush J, Trajanoski Z, Ardevol A (2005) Grape-seed derived procyanidins interfere with adipogenesis of 3T3-L1 cells at the onset of differentiation. Int J Obes 29:934–941

    Article  CAS  Google Scholar 

  47. Fruhbeck G, Jebb SA, Prentice AM (1998) Leptin: physiology and pathophysiology. Clin Physiol 18:399–419

    Article  CAS  Google Scholar 

  48. Steppan CM, Bailey ST, Bhat S, Brown EJ, Banerjee RR, Wright CM, Patel HR, Ahima RS, Lazar MA (2001) The hormone resistin links obesity to diabetes. Nature 409:307–312

    Article  CAS  Google Scholar 

  49. Xu A, Wang Y, Xu JY, Stejskal D, Tam S, Zhang J, Wat NM, Wong WK, Lam KS (2006) Adipocyte fatty acid-binding protein is a plasma biomarker closely associated with obesity and metabolic syndrome. Clin Chem 52:405–413

    Article  CAS  Google Scholar 

  50. Yang Q, Graham TE, Mody N, Preitner F, Peroni OD, Zabolotny JM, Kotani K, Quadro L, Kahn BB (2005) Serum retinol binding protein 4 contributes to insulin resistance in obesity and type 2 diabetes. Nature 436:356–362

    Article  CAS  Google Scholar 

  51. Lumeng CN, Saltiel AR (2011) Inflammatory links between obesity and metabolic disease. J Clin Invest 121:2111–2117

    Article  CAS  Google Scholar 

  52. Tilg H, Moschen AR (2006) Adipocytokines: mediators linking adipose tissue, inflammation and immunity. Nat Rev Immunol 6:772–783

    Article  CAS  Google Scholar 

  53. Bantle JP, Raatz SK, Thomas W, Georgopoulos A (2000) Effects of dietary fructose on plasma lipids in healthy subjects. Am J Clin Nutr 72:1128–1134

    CAS  Google Scholar 

  54. Parks EJ, Hellerstein MK (2000) Carbohydrate-induced hypertriacylglycerolemia: historical perspective and review of biological mechanisms. Am J Clin Nutr 71:412–433

    CAS  Google Scholar 

  55. Miller M, Stone NJ, Ballantyne C et al (2011) Triglycerides and cardiovascular disease: a scientific statement from the American Heart Association. Circulation 123:2292–2333

    Article  Google Scholar 

  56. Singleton VL, Rossi JA (1965) Colorimetry of total phenolics with phosphomolybdic–phosphotungstic acid reagents. Am J Enol Vitic 16:144–158

    CAS  Google Scholar 

  57. Oki K, Yamane K, Kamei N, Asao T, Awaya T, Kohno N (2009) The single nucleotide polymorphism upstream of insulin-induced gene 2 (INSIG2) is associated with the prevalence of hypercholesterolaemia, but not with obesity, in Japanese American women. Br J Nutr 101:322–327

    Article  CAS  Google Scholar 

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Acknowledgments

This study was supported by the German Federal Ministry of Education and Research (Project grant -01-EA0505-). The technical staff of the Department of Physiology and Biochemistry of Nutrition at the Max Rubner-Institut is acknowledged for the valuable contribution. Further, we thank all study participants for taking part in this study.

Conflict of interest

The authors declare no conflict of interest.

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Authors and Affiliations

  1. Department of Physiology and Biochemistry of Nutrition, Max Rubner-Institut, Haid-und-Neu-Strasse 9, 76131, Karlsruhe, Germany

    Stephan W. Barth, Tatiana C. L. Koch, Bernhard Watzl & Achim Bub

  2. Institute of Enology and Beverage Research, Section of Wine Analysis and Beverage Research, Research Institute of Geisenheim, Geisenheim, Germany

    Helmut Dietrich & Frank Will

Authors
  1. Stephan W. Barth
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  2. Tatiana C. L. Koch
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  3. Bernhard Watzl
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  5. Frank Will
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  6. Achim Bub
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Correspondence to Achim Bub.

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Barth, S.W., Koch, T.C.L., Watzl, B. et al. Moderate effects of apple juice consumption on obesity-related markers in obese men: impact of diet–gene interaction on body fat content. Eur J Nutr 51, 841–850 (2012). https://doi.org/10.1007/s00394-011-0264-6

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  • DOI: https://doi.org/10.1007/s00394-011-0264-6

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