Current Microbiology

, Volume 62, Issue 6, pp 1689–1696 | Cite as

Effect of a Probiotic Intake on Oxidant and Antioxidant Parameters in Plasma of Athletes During Intense Exercise Training

  • Daniele MartarelliEmail author
  • Maria Cristina Verdenelli
  • Stefania Scuri
  • Mario Cocchioni
  • Stefania Silvi
  • Cinzia Cecchini
  • Pierluigi Pompei


The aim of this study was to evaluate the effect of Lactobacillus rhamnosus IMC 501® and Lactobacillus paracasei IMC 502® on oxidative stress in athletes during a four-week period of intense physical activity. Two groups of twelve subjects each were selected for this analysis. The first group consumed a daily dose of a mixture of the two probiotic strains (1:1 L. rhamnosus IMC 501® and L. paracasei IMC 502®; ~109 cells/day) for 4 weeks. The second group (control) did not consume any supplements during the 4 weeks. Blood samples collected immediately before and after the supplementation were analyzed, and plasma levels of reactive oxygen metabolites and biological antioxidant potential were determined. Faeces were also collected and analyzed before and at the end of the probiotic supplementation. Antioxidative activity and oxidative stress resistance of the two strains were determined in vitro. Results demonstrated that intense physical activity induced oxidative stress and that probiotic supplementation increased plasma antioxidant levels, thus neutralizing reactive oxygen species. The two strains, L. rhamnosus IMC 501® and L. paracasei IMC 502®, exert strong antioxidant activity. Athletes and all those exposed to oxidative stress may benefit from the ability of these probiotics to increase antioxidant levels and neutralize the effects of reactive oxygen species.


Lactobacillus Probiotic Strain Reactive Oxygen Metabolite Probiotic Supplementation Intense Physical Activity 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.



This study was supported by the School of Pharmacy, Unit of Experimental Medicine and Public Health, the School of Pharmacy, Hygiene and Public Health Research Centre and the School of Biosciences and Biotechnology, University of Camerino.


  1. 1.
    Alberti A, Bolognini L, Macciantelli D, Carratelli M (2000) The radical caion of N,N-diethyl-para-phenylendiamine: a possible indicator of oxidative stress in biological samples. Res Chem Intermed 26:253–267CrossRefGoogle Scholar
  2. 2.
    An H, Zhou H, Huang Y, Wang G, Luan C, Mou J, Luo Y, Hao Y (2010) High-level expression of heme-dependent catalase gene katA from Lactobacillus Sakei protects Lactobacillus rhamnosus from oxidative stress. Mol Biotechnol 45:155–160PubMedCrossRefGoogle Scholar
  3. 3.
    Annuk H, Shchepetova J, Kullisaar T, Songisepp E, Zilmer M, Mikelsaar M (2003) Characterization of intestinal lactobacilli as putative probiotic candidates. J Appl Microbiol 94:403–412PubMedCrossRefGoogle Scholar
  4. 4.
    Bonomini F, Tengattini S, Fabiano A, Bianchi R, Rezzani R (2008) Atherosclerosis and oxidative stress. Histol Histopathol 23:381–390PubMedGoogle Scholar
  5. 5.
    Bowen PE, Borthakur G (2004) Postprandial lipid oxidation and cardiovascular disease risk. Curr Atheroscler Rep 6(6):477–484PubMedCrossRefGoogle Scholar
  6. 6.
    Burcelin R, Luche E, Serino M, Amar J (2009) The gut microbiota ecology: a new opportunity for the treatment of metabolic diseases? Front Biosci 14:5107–5117PubMedCrossRefGoogle Scholar
  7. 7.
    Cani PD, Delzenne NM, Amar J, Burcelin R (2008) Role of gut microflora in the development of obesity and insulin resistance following high-fat diet feeding. Pathol Biol (Paris) 56:305–309Google Scholar
  8. 8.
    Ceriello A, Bortolotti N, Crescentini A et al (1998) Antioxidant defences are reduced during oral glucose tolerance test in normal and non-insulin dependent diabetic subjects. Eur J Clin Invest 28:329–333PubMedCrossRefGoogle Scholar
  9. 9.
    Ceriello A, Bortolotti N, Motz E et al (1998) Meal-generated oxidative stress in type 2 diabetic patients. Diabetes Care 21:1529–1533PubMedCrossRefGoogle Scholar
  10. 10.
    Ceriello A, Bortolotti N, Motz E et al (1999) Meal-induced oxidative stress and low-density lipoprotein oxidation in diabetes: the possible role of hyperglycemia. Metabolism 48:1503–1508PubMedCrossRefGoogle Scholar
  11. 11.
    Cesarone MR, Belcaro G, Carratelli M et al (1999) A simple test to monitor oxidative stress. Int Angiol 18:127–130PubMedGoogle Scholar
  12. 12.
    Cornelli U, Terranova R, Luca S, Cornelli M, Alberti A (2001) Bioavailability and antioxidant activity of some food supplements in men and women using the D-Roms Test as a marker of oxidative stress. J Nutr 131:3208–3211PubMedGoogle Scholar
  13. 13.
    Deaton CM, Marlin DJ (2003) Exercise-associated oxidative stress. Clin Tech Equine Prac 2:278–291CrossRefGoogle Scholar
  14. 14.
    Decker E, Faraji H (1990) Inhibition of lipid oxidation by carnosine. JAOCS 67:650–652CrossRefGoogle Scholar
  15. 15.
    Dhalla NS, Temsah RM, Netticadan T (2000) Role of oxidative stress in cardiovascular diseases. J Hypertens 18:655–673PubMedCrossRefGoogle Scholar
  16. 16.
    Fabian E, Elmadfa I (2007) The effect of daily consumption of probiotic and conventional yoghurt on oxidant and anti-oxidant parameters in plasma of young healthy women. Int J Vitam Nutr Res 77:79–88PubMedGoogle Scholar
  17. 17.
    Fabian E, Majchrzak D, Dieminger B, Meyer E, Elmadfa I (2008) Influence of probiotic and conventional yoghurt on the status of vitamins B1, B2 and B6 in young healthy women. Ann Nutr Metab 52:29–36PubMedCrossRefGoogle Scholar
  18. 18.
    Filippin LI, Vercelino R, Marroni NP, Xavier RM (2008) Redox signalling and the inflammatory response in rheumatoid arthritis. Clin Exp Immunol 152:415–422PubMedCrossRefGoogle Scholar
  19. 19.
    Halliwell B, Chirico S (1993) Lipid peroxidation, its mechanism, measurement and significance. J Clin Nutr 57:715S–725SGoogle Scholar
  20. 20.
    Hitchon CA, El-Gabalawy HS (2004) Oxidation in rheumatoid arthritis. Arthritis Res Ther 6:265–278PubMedCrossRefGoogle Scholar
  21. 21.
    Hütt P, Andreson H, Kullisaar T, Vihalemm T, Unt E, Kals J, Kampus P, Zilmer M, Mikelsaar M (2009) Effects of a synbiotic product on blood antioxidative activity in subjects colonized with Helicobacter pylori. Lett Appl Microbiol 48:797–800PubMedGoogle Scholar
  22. 22.
    Ilhan N, Kamanli A, Ozmerdivenli R, Ilhan N (2004) Variable effects of exercise intensity on reduced glutathione, thiobarbituric acid reactive substance levels, and glucose concentration. Arch Med Res 35:294–300PubMedCrossRefGoogle Scholar
  23. 23.
    Jacobsen CN, Rosenfeldt Nielsen V, Hayford AE, Møller PL, Michaelsen KF, Pærregaard A, Sandstrom B, Tvede M, Jakobsen M (1999) Screening of probiotic activities of forty-seven strains of Lactobacillus spp. by in vitro techniques and evaluation of the colonization ability of five selected strains in humans. Appl Environ Microbiol 65:4949–4956PubMedGoogle Scholar
  24. 24.
    Jenner P, Olanow CW (1996) Oxidative stress and the pathogenesis of Parkinson’s disease. Neurology 47:S161–S170PubMedGoogle Scholar
  25. 25.
    Kregel KC, Zhang HJ (2007) An integrated view of oxidative stress in aging: basic mechanisms, functional effects, and pathological considerations. Am J Physiol Regul Integr Comp Physiol 292:R18–R36PubMedCrossRefGoogle Scholar
  26. 26.
    Kullisaar T, Songisepp E, Mikelsaar M, Zilmer K, Vihalemm T, Zilmer M (2003) Antioxidative probiotic fermented goats’ milk decreases oxidative stress-mediated atherogenicity in human subjects. Br J Nutr 90:449–456PubMedCrossRefGoogle Scholar
  27. 27.
    Kumar KV, Das UN (1993) Are free radicals involved in the pathobiology of human essential hypertension? Free RadicRes Commun 19:59–66CrossRefGoogle Scholar
  28. 28.
    Lin MY, Chang FJ (2000) Antioxidative effect of intestinal bacteria Bifidobacterium longum ATCC 15708 and Lactobacillus acidophilus ATCC 4356. Dig Dis Sci 45:1617–1622PubMedCrossRefGoogle Scholar
  29. 29.
    Lukienko PI, Mel’nichenko NG, Zverinskii IV, Zabrodskaya SV (2000) Antioxidant properties of thiamine. Bull Exp Biol Med 130(9):874–876PubMedCrossRefGoogle Scholar
  30. 30.
    Mahfouz MM, Zhou SQ, Kummerow FA (2009) Vitamin B6 compounds are capable of reducing the superoxide radical and lipid peroxide levels induced by H2O2 in vascular endothelial cells in culture. Int J Vitam Nutr Res 79:218–229PubMedCrossRefGoogle Scholar
  31. 31.
    Markesbery WR (1997) Oxidative stress hypothesis in Alzheimer’s disease. Free Radic Biol Med 23:134–147PubMedCrossRefGoogle Scholar
  32. 32.
    Martarelli D, Cocchioni M, Scuri S, Pompei P (2009) Diaphragmatic breathing reduces exercise-induced oxidative stress. Evid Based Complement Alternat Med. doi: 10.1093/ecam/nep169
  33. 33.
    Martarelli D, Pompei P (2009) Oxidative stress and antioxidant changes during a 24-hours mountain bike endurance exercise in master athletes. J Sports Med Phys Fitness 49:122–127PubMedGoogle Scholar
  34. 34.
    Mikelsaar M, Zilmer M (2009) Lactobacillus fermentum ME-3—an antimicrobial and antioxidative probiotic. Microb Ecol Health Dis 21:1–27PubMedCrossRefGoogle Scholar
  35. 35.
    Molavi B, Mehta JL (2004) Oxidative stress in cardiovascular disease: molecular basis of its deleterious effects, its detection, and therapeutic considerations. Curr Opin Cardiol 19:488–493PubMedCrossRefGoogle Scholar
  36. 36.
    Nagata K, Hasegawa T, Hirokado Y, Kiyama K, Otsuki C (2008) Lifestyle-related diseases and the oxidative stress regulation system. J Psychosom Med 4:176–183Google Scholar
  37. 37.
    Ong Sl, Zhang Y, Whitworth JA (2008) Reactive oxygen species and glucocorticoid-induced hypertension. Clin Exp Pharmacol Physiol 35:477–482PubMedCrossRefGoogle Scholar
  38. 38.
    Paoletti R, Samuelsson B, Catapano AL et al (1994) Oxidative processes and antioxidants. Raven Press, New YorkGoogle Scholar
  39. 39.
    Serino M, Luche E, Chabo C, Amar J, Burcelin R (2009) Intestinal microflora and metabolic diseases. Diabetes Metab 35:262–272PubMedCrossRefGoogle Scholar
  40. 40.
    Silvi S, Verdenelli MC, Orpianesi C, Cresci A (2003) EU project Crownalife: functional foods, gut microflora and healthy ageing. Isolation and identification of Lactobacillus and Bifidobacterium strains from faecal samples of elderly subjects for a possible probiotic use in functional foods. J Food Engin 56:195–200CrossRefGoogle Scholar
  41. 41.
    Slyshenkov VS, Rakowska M, Moiseenok AG, Lm Wojtczak (1995) Pantothenic acid and its derivatives protect Ehrlich ascites tumor cells against lipid peroxidation. Free Radic Biol Med 19:767–772PubMedCrossRefGoogle Scholar
  42. 42.
    Songisepp E, Kals J, Kullisaar T, Mändar R, Hütt P, Zilmer M, Mikelsaar M (2005) Evaluation of the functional efficacy of an antioxidative probiotic in healthy volunteers. Nutr J Aug 4:4–22Google Scholar
  43. 43.
    Talwalkar A, Kailasapathy K (2004) A review of oxygen toxicity in probiotic yoghurts: influence on the survival of probiotic bacteria and protective techniques. IFT Compr Rev Food Sci Food Saf 3:117–124CrossRefGoogle Scholar
  44. 44.
    Ursini F, Sevanian A (2002) Postprandial oxidative stress. Biol Chem 383:599–605PubMedCrossRefGoogle Scholar
  45. 45.
    Uskova MA, Kravchenko LV (2009) Antioxidant properties of lactic acid bacteria–probiotic and yogurt strains. Vopr Pitan 78:18–23PubMedGoogle Scholar
  46. 46.
    Verdenelli MC, Ghelfi F, Silvi S, Orpianesi C, Cecchini C, Cresci A (2009) Probiotic properties of Lactobacillus rhamnosus and Lactobacillus paracasei isolated from human faeces. Eur J Nutr 48:355–363PubMedCrossRefGoogle Scholar
  47. 47.
    Verdenelli MC, Ricciutelli M, Gigli F, Cenci G, Trotta F, Caldini G, Cresci A, Orpianesi C (2010) Investigation of the antigenotoxic properties of the probiotic Lactobacillus rhamnosus IMC 501® by gas chromatography-mass spectrometry. Int J Food Sci 22:473–478Google Scholar
  48. 48.
    Wanasundrara U, Amarowicz R, Shanhidi F (1994) Isolation and identification of an antioxidative component in canola meal. J Agric Food Chem 420:1285–1290CrossRefGoogle Scholar
  49. 49.
    Watson TA, Callister R, Taylor RD, Sibbritt DW, MacDonald-Wicks LK, Garg ML (2005) Antioxidant restriction and oxidative stress in short-duration exhaustive exercise. Med Sci Sports Exerc 37:63–71PubMedCrossRefGoogle Scholar
  50. 50.
    West NP, Pyne DB, Peake JM, Cripps AW (2009) Probiotics, immunity and exercise: a review. Exerc Immunol Rev 15:107–126PubMedGoogle Scholar
  51. 51.
    Winrow VR, Winyard PG, Morris CJ, Blake DR (1993) Free radicals in inflammation: second messengers and mediators of tissue destruction. Br Med Bull 49:506–522PubMedGoogle Scholar
  52. 52.
    Wojtczak L, Slyshenkov VS (2003) Protection by pantothenic acid against apoptosis and cell damage by oxygen free radicals–the role of glutathione. Biofactors 17:61–73PubMedCrossRefGoogle Scholar
  53. 53.
    Christen Yves (2000) Oxidative stress and Alzheimer disease. Am J Clin Nutr 71:621s–629sPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2011

Authors and Affiliations

  • Daniele Martarelli
    • 1
    Email author
  • Maria Cristina Verdenelli
    • 2
  • Stefania Scuri
    • 3
  • Mario Cocchioni
    • 3
  • Stefania Silvi
    • 2
  • Cinzia Cecchini
    • 2
  • Pierluigi Pompei
    • 1
  1. 1.School of Pharmacy, Unit of Experimental Medicine and Public HealthUniversity of CamerinoCamerinoItaly
  2. 2.School of Biosciences and BiotechnologiesUniversity of CamerinoCamerinoItaly
  3. 3.School of Pharmacy, Hygiene and Public Health Research CentreUniversity of CamerinoCamerinoItaly

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