Skip to main content
SpringerLink
Log in

Effect of polyphenol supplements on redox status of blood cells: a randomized controlled exercise training trial

  • Original Contribution
  • Published:
European Journal of Nutrition Aims and scope Submit manuscript

Abstract

Purpose

The effect of endogenous antioxidants can be either an immediate response (relying on enzymatic activities) or a long-term adaptation (relying on gene modulation events), both susceptible to be modified by antioxidants from diet and supplementation. The aim of this work was to delve in these aspects in circulating white blood cells in a group of volunteers (n = 33, 20–22 years) performing eccentric exercises and consuming or not (n = 8) different polyphenolic antioxidants (Lippia citriodora extract-PLX® n = 8, almond beverage n = 9 or a mixture of both n = 8) during 21 days.

Methods

We have designed a single-blind, parallel-group, randomized controlled trial. Antioxidant enzyme activities, oxidative stress markers, and antioxidant gene expression were determined.

Results

Neutrophils and lymphocytes expressed high amounts of oxidative markers compared to plasma. Concerning enzymatic activities, increased superoxide dismutase levels were detected when certain supplements were consumed. However, catalase levels did not change. As for glutathione peroxidase levels, no differences were detected in lymphocytes, while neutrophils expressed increased levels in both placebo and PLX® groups. Glutathione reductase activity was decreased in all groups, except in neutrophils of PLX® group. At the level of gene expression, neither PLX® nor the almond beverage interfered with the expression of genes coding for the corresponding enzymes. However, the combined intake of both supplements affected the expression of glutathione reductase and Cu–Zn and Mn-superoxide dismutases in neutrophils.

Conclusions

Altogether, these results suggest that blood cell types respond and adapt differently to exercise-induced oxidative damage.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  1. McGinley C, Shafat A, Donnelly AE (2009) Does antioxidant vitamin supplementation protect against muscle damage? Sports Med 39:1011–1032

    Article  Google Scholar 

  2. Morton JP, Kayani AC, McArdle A, Drust B (2009) The exercise-induced stress response of skeletal muscle, with specific emphasis on humans. Sports Med 39:643–662

    Article  Google Scholar 

  3. Smith C, Kruger MJ, Smith RM, Myburgh KH (2008) The inflammatory response to skeletal muscle injury: illuminating complexities. Sports Med 38:947–969

    Article  Google Scholar 

  4. Toumi H, F’guyer S, Best TM (2006) The role of neutrophils in injury and repair following muscle stretch. J Anat 208:459–470

    Article  CAS  Google Scholar 

  5. Geering B, Simon HU (2011) Peculiarities of cell death mechanisms in neutrophils. Cell Death Differ 18:1457–1469

    Article  CAS  Google Scholar 

  6. Tauler P, Aguilo A, Gimeno I, Noguera A, Agusti A, Tur JA, Pons A (2003) Differential response of lymphocytes and neutrophils to high intensity physical activity and to vitamin C diet supplementation. Free Radic Res 37:931–938

    Article  CAS  Google Scholar 

  7. Cases N, Aguilo A, Tauler P, Sureda A, Llompart I, Pons A, Tur JA (2005) Differential response of plasma and immune cell’s vitamin E levels to physical activity and antioxidant vitamin supplementation. Eur J Clin Nutr 59:781–788

    Article  CAS  Google Scholar 

  8. Moreira A, Delgado L, Moreira P, Haahtela T (2009) Does exercise increase the risk of upper respiratory tract infections? Br Med Bull 90:111–131

    Article  Google Scholar 

  9. Gleeson M, Bishop NC (2000) Elite athlete immunology: importance of nutrition. Int J Sports Med 21(Suppl 1):S44–S50

    Article  CAS  Google Scholar 

  10. Sen CK (2001) Antioxidants in exercise nutrition. Sports Med 31:891–908

    Article  CAS  Google Scholar 

  11. Nikolaidis MG, Kerksick CM, Lamprecht M, McAnulty SR (2012) Does vitamin C and E supplementation impair the favourable adaptations of regular exercise? Oxid Med Cell Longev. doi:10.1155/2012/707941

    Google Scholar 

  12. Jakeman P, Maxwell S (1993) Effect of antioxidant vitamin supplementation on muscle function after eccentric exercise. Eur J Appl Phys Occup Physiol 67:426–430

    Article  CAS  Google Scholar 

  13. Shafat A, Butler P, Jensen RI, Donnelly AE (2004) Effects of dietary supplementation with vitamins C and E on muscle function during and after eccentric contractions in humans. Eur J Appl Physiol 93:196–202

    Article  CAS  Google Scholar 

  14. Gomez-Cabrera MC, Domenech E, Romagnoli M, Arduini A, Borras C, Pallardo FV, Sastre J, Viña J (2008) Oral administration of vitamin C decreases muscle mitochondria biogenesis and hampers training-induced adaptations in endurance performance. Am J Clin Nutr 87:142–149

    CAS  Google Scholar 

  15. Marshall RJ, Scott KC, Hill RC, Lewis DD, Sundstrom D, Jones GL, Harper J (2002) Supplemental vitamin C appears to slow racing greyhounds. J Nutr 132(Suppl 2):1616S–1621S

    CAS  Google Scholar 

  16. Bailey DM, Williams C, Betts JA, Thompson D, Hurst TL (2011) Oxidative stress, inflammation and recovery of muscle function after damaging exercise: effect of 6-week mixed antioxidant supplementation. Eur J Appl Physiol 111:925–936

    Article  CAS  Google Scholar 

  17. Yfanti C, Akerstrom T, Nielsen S, Nielsen AR, Mounier R, Mortensen OH, Lykkesfeldt J, Rose AJ, Fischer CP, Pedersen BK (2010) Antioxidant supplementation does not alter endurance training adaptation. Med Sci Sports Exerc 42:1388–1395

    Article  CAS  Google Scholar 

  18. Higashida K, Kim SH, Higuchi M, Holloszy JO, Han DH (2011) Normal adaptations to exercise despite protection against oxidative stress. Am J Physiol Endocrinol Metab 301:E779–E784

    Article  CAS  Google Scholar 

  19. Elhaimeur F, Courderot-Masuyer C, Nicod L, Guyon C, Richert I, Berthelot A (2002) Dietary vitamin C supplementation decreases blood pressure in DOCA-salt hypertensive male Sprague-Dawley rats and this is associated with increased liver oxidative stress. Mol Cell Biochem 237:77–83

    Article  CAS  Google Scholar 

  20. Nieman DC, Henson DA, McAnulty SR, McAnulty LS, Morrow JD, Ahmed A, Heward CB (2004) Vitamin E and immunity after the Kona Triathlon World Championship. Med Sci Sports Exerc 36:1328–1335

    Article  CAS  Google Scholar 

  21. McAnulty SR, McAnulty LS, Nieman DC, Morrow JD, Shooter LA, Holmes S, Heward C, Henson DA (2005) Effect of alpha-tocopherol supplementation on plasma homocysteine and oxidative stress in highly trained athletes before and after exhaustive exercise. J Nutr Biochem 16:530–537

    Article  CAS  Google Scholar 

  22. Close GL, Ashton T, Cable T, Doran D, Holloway C, McArdle F, McLaren DP (2006) Ascorbic acid supplementation does not attenuate post-exercise muscle soreness following muscle-damaging exercise but may delay the recovery process. Br J Nutr 95:976–981

    Article  CAS  Google Scholar 

  23. Rytter E, Vessby B, Asgard R, Ersson C, Moussavian S, Sjödin A, Abramsson-Zetterberg L, Möller L, Basu S (2010) Supplementation with a combination of antioxidants does not affect glycaemic control, oxidative stress or inflammation in type 2 diabetes subjects. Free Radic Res 44:1445–1453

    Article  CAS  Google Scholar 

  24. Theodorou AA, Nikolaidis MG, Paschalis V, Koutsias S, Panayiotou G, Fatouros IG, Koutedakis Y, Jamurtas AZ (2011) No effect of antioxidant supplementation on muscle performance and blood redox adaptations to eccentric training. Am J Clin Nutr 93:1373–1383

    Article  CAS  Google Scholar 

  25. Niess AM, Simon P (2007) Response and adaptation of skeletal muscle to exercise: the role of reactive oxygen species. Front Biosci 12:4826–4838

    Article  CAS  Google Scholar 

  26. Bucci LR (2000) Selected herbals and human exercise performance. Am J Clin Nutr 72(Suppl 2):624S–636S

    CAS  Google Scholar 

  27. Funes L, Fernandez-Arroyo S, Laporta O, Pons A, Roche E, Segura-Carretero A, Fernandez-Gutierrez A, Micol V (2009) Correlation between plasma antioxidant capacity and verbascoside levels in rats after oral administration of lemon verbena extracts. Food Chem 117:589–598

    Article  CAS  Google Scholar 

  28. Carrera-Quintanar L, Funes L, Viudes E, Tur J, Micol V, Roche E, Pons A (2012) Antioxidant effect of lemon verbena extracts in lymphocytes of university students performing aerobic training program. Scand J Med Sci Sports 22:454–461

    Article  CAS  Google Scholar 

  29. Funes L, Carrera-Quintanar L, Cerdan-Calero M, Ferrer MD, Drobnic F, Pons A, Roche E, Micol V (2011) Effect of lemon verbena supplementation on muscular damage markers, proinflammatory cytokines release and neutrophils’oxidative stress in chronic exercise. Eur J Appl Physiol 111:695–705

    Article  CAS  Google Scholar 

  30. Sureda A, Tauler P, Aguilo A, Cases N, Llompart I, Tur JA, Pons A (2007) Antioxidant supplementation influences the neutrophil tocopherol associated protein expression, but not the inflammatory response to exercise. Cent Eur J Biol 2:56–70

    CAS  Google Scholar 

  31. Sureda A, Tauler P, Aguilo A, Cases N, Llompart I, Tur JA, Pons A (2008) Influence of an antioxidant vitamin-enriched drink on pre- and post-exercise lymphocyte antioxidant system. Ann Nutr Metab 52:233–240

    Article  CAS  Google Scholar 

  32. Venkatachalam M, Sathe SK (2006) Chemical composition of selected edible nut seeds. J Agric Food Chem 54:4705–4714

    Article  CAS  Google Scholar 

  33. Mestre-Alfaro A, Ferrer MD, Sureda A, Tauler P, Martinez E, Bibiloni MM, Micol V, Tur JA, Pons A (2011) Phytoestrogens enhance antioxidant enzymes after swimming exercise and modulate sex hormone plasma levels in female swimmers. Eur J Appl Physiol 111:2281–2294

    Article  CAS  Google Scholar 

  34. Quirantes-Piné R, Herranz-López M, Funes L, Borrás-Linares I, Micol V, Segura-Carretero A, Fernández-Gutiérrez A (2013) Phenylpropanoids and their metabolites are the major compounds responsible for blood-cell protection against oxidative stress after administration of Lippia citriodora in rats. Phytomedicine 20:1112–1118

    Article  Google Scholar 

  35. Marfell-Jones M, Olds T, Steward A, Carter L (2006) International standards for anthropometric assessment. ISAK, Potchefstroom

    Google Scholar 

  36. Boyum A (1964) Separation of white blood cells. Nature 204:793–794

    Article  CAS  Google Scholar 

  37. Trinder P (1969) Determination of blood glucose using an oxidase–peroxidase system with a non-carcinogenic chromogen. J Clin Pathol 22:158–161

    Article  CAS  Google Scholar 

  38. Bucolo G, David H (1973) Quantitative determination of serum triglycerides by the use of enzymes. Clin Chem 19:476–482

    CAS  Google Scholar 

  39. Fossati P, Prencipe L, Berti G (1980) Use of 3,5-dichloro-2-hydroxybenzenesulfonic acid/4-aminophenazone chromogenic system in direct enzymic assay of uric acid in serum and urine. Clin Chem 26:227–231

    CAS  Google Scholar 

  40. Bowers LD, Wong ET (1980) Kinetic serum creatineine assays. II. A critical evaluation and review. Clin Chem 26:555–561

    CAS  Google Scholar 

  41. Weisshaar D, Gossrau E, Faderl B (1975) Normal ranges of alpha-HBDH, LDH, AP, and LAP as measured with substrate-optimated test charges. Med Welt 26:387–392

    CAS  Google Scholar 

  42. Young DS, Friedman RB (2001) Effects of disease on clinical laboratory tests. AACC Press, Washington DC

    Google Scholar 

  43. McCord JM, Fridovich I (1969) Superoxide dismutase. An enzymic function for erythrocuprein (hemocuprein). J Biol Chem 244:6049–6055

    CAS  Google Scholar 

  44. Aebi H (1984) Catalase in vitro. Methods Enzymol 105:121–126

    Article  CAS  Google Scholar 

  45. Flohé L, Gunzler WA (1984) Assays of glutathione peroxidase. Methods Enzymol 105:114–121

    Article  Google Scholar 

  46. Goldberg DM, Spooner RJ (1985) Glutathione reductase. In: Bergmeyer HU (ed) Methods of enzymatic analysis. Verlag Chemie, Basel, pp 258–265

    Google Scholar 

  47. Levine RL, Williams JA, Stadtman ER, Shacter E (1994) Carbonyl assays for determination of oxidatively modified proteins. Methods Enzymol 233:346–357

    Article  CAS  Google Scholar 

  48. Laporta O, Funes L, Garzon MT, Villalain J, Micol V (2007) Role of membranes on the antibacterial and anti-inflammatory activities of the bioactive compounds from hypoxis rooperi corm extract. Arch Biochem Biophys 467:119–131

    Article  CAS  Google Scholar 

  49. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(−ΔΔCt) method. Methods 25:402–408

    Article  CAS  Google Scholar 

  50. Bloomer RJ (2008) Effect of exercise on oxidative stress biomarkers. Adv Clin Chem 46:1–50

    Article  CAS  Google Scholar 

  51. Vander A, Sherman J, Luciano D (2001) Human physiology. McGraw Hill, Boston

    Google Scholar 

  52. Hausser J, Syed AP, Selevsek N, van Nimwegen E, Jaskiewick L, Aebersold R, Zavolan M (2013) Timescales and bottlenecks in miRNA-dependent gene regulation. Mol Syst Biol 9:711

    Article  CAS  Google Scholar 

  53. Vogel C, Marcotte EM (2012) Insights into the regulation of protein abundance from proteomic and transcriptomic analyses. Nat Rev Genet 13:227–232

    CAS  Google Scholar 

  54. Serafini M, Miglio C, Peluso I, Petrosino T (2011) Modulation of plasma non enzimatic antioxidant capacity (NEAC) by plant foods: the role of polyphenols. Curr Top Med Chem 11:1821–1846

    Article  CAS  Google Scholar 

  55. Yamada K, Tachibana H (2000) Recent topics in anti-oxidant factors. BioFactors 13:167–172

    Article  CAS  Google Scholar 

  56. Osawa T (1999) Protective role of dietary polyphenols in oxidative stress. Mech Ageing Dev 111:133–139

    Article  CAS  Google Scholar 

  57. Rice-Evans C (1995) Plant polyphenols: free radical scavengers or chain-breaking antioxidants? Biochem Soc Symp 61:103–116

    Article  CAS  Google Scholar 

  58. Joven J, Rull A, Rodríguez-Gallego E, Camps J, Riera-Borrull M, Hernández-Aguilera A, Martín-Paredero V, Segura-Carretero A, Micol V, Alonso-Villaverde C, Menéndez JA (2013) Multifunctional targets of dietary polyphenols in disease: a case for chemokine network and energy metabolism. Food Chem Toxicol 51:267–279

    Article  CAS  Google Scholar 

  59. Bouayed J, Bohn T (2010) Exogenous antioxidants, double-edge swords in cellular redox state. Oxid Med Cell Longev 3:228–237

    Article  Google Scholar 

  60. Sureda A, Batle JM, Tauler P, Aguiló A, Cases N, Tur JA, Pons A (2004) Hypoxia/reoxygenation and vitamin C intake influence NO synthesis and antioxidant defenses of neutrophils. Free Radic Biol Med 37:1744–1755

    Article  CAS  Google Scholar 

Download references

Acknowledgments

We thank Jose Maria Adsuar for technical assistance in blood analysis. This work was supported by grants from Spanish Science Ministry AGL2007-62806/ALI to AP, AGL2007-60778 and AGL 2011-29857-C03-03 to VM and PROMETEO/2012/007 from Generalitat Valenciana to VM and ER. ER is recipient of Instituto de Salud Carlos III-FEDER (PS09/01093) and Fundacion Salud 2000-Merck Serono grants. AP, VM and ER are members of the “Centro de Investigación Biomédica en Red de Fisiopatología de la Obesidad y Nutrición” CIBERobn (CB12/03/30038). LC-Q and LF were recipients of CONACYT-Mexico (ref 197139) and FPI (Spanish Science Ministry) fellowships, respectively.

Conflict of interest

Authors declare that there are no conflicts of interest.

Author information

Authors and Affiliations

  1. Department of Applied Biology-Nutrition and Institute of Bioengineering, University Miguel Hernandez, Avda de la Universidad sn, 03202, Elche, Alicante, Spain

    Lucrecia Carrera-Quintanar, Nestor Vicente-Salar & Enrique Roche

  2. Institute of Molecular and Cellular Biology, University Miguel Hernandez, Elche, Alicante, Spain

    Lorena Funes & Vicente Micol

  3. Department of Physical Education and Sports, University of Valencia, Valencia, Spain

    Cristina Blasco-Lafarga

  4. Department for Basic Biology and Health Sciences, University of Balearic Islands, Palma de Mallorca, Spain

    Antoni Pons

  5. CIBERobn (Fisiopatología de la Obesidad y la Nutrición CB12/03/30038), Instituto de Salud Carlos III, Madrid, Spain

    Antoni Pons, Vicente Micol & Enrique Roche

Authors
  1. Lucrecia Carrera-Quintanar
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Lorena Funes
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Nestor Vicente-Salar
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Cristina Blasco-Lafarga
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Antoni Pons
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Vicente Micol
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Enrique Roche
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Enrique Roche.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOC 42 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Carrera-Quintanar, L., Funes, L., Vicente-Salar, N. et al. Effect of polyphenol supplements on redox status of blood cells: a randomized controlled exercise training trial. Eur J Nutr 54, 1081–1093 (2015). https://doi.org/10.1007/s00394-014-0785-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00394-014-0785-x

Keywords

Search

Navigation