Skip to main content
Log in

Increase of pro-oxidants with no evidence of lipid peroxidation in exhaled breath condensate after a 10-km race in non-athletes

  • Original Paper
  • Published:
Journal of Physiology and Biochemistry Aims and scope Submit manuscript

Abstract

It is a well-established fact that exercise increases pro-oxidants and favors oxidative stress; however, this phenomenon has been poorly studied in human lungs. Pro-oxidative generation (H2O2, NO2 ), lipid peroxidation markers (MDA), and inflammation (pH) in exhaled breath condensate (EBC) have been determined through data from 10 active subjects who ran 10 km; samples were obtained immediately before, at 20, and at 80 min post-exertion. In EBC, the concentration of H2O2 at 80 min post-exertion was increased. NO2 concentration showed a tendency to increase at 80 min post-exertion, with no variations in MDA and pH. No variations of NO2 were found in plasma, while there was an increase of NO2 at 80 min post-exertion in the relation between EBC and plasma. NO2 in EBC did not correlate to plasmatic NO2 , while it did correlate directly with H2O2 in EBC, suggesting a localized origin for the exercise-related NO2 increase in EBC. MDA in plasma did not increase nor correlate with MDA in EBC. In conclusion, high-intensity exercise increases lung-originated pro-oxidants in non-athlete subjects with no evidence of early lipid peroxidation and changes in the pH value in EBC.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  1. Araneda OF, Garcia C, Lagos N, Quiroga G, Cajigal J, Salazar MP, Behn C (2005) Lung oxidative stress as related to exercise and altitude. Lipid peroxidation evidence in exhaled breath condensate: a possible predictor of acute mountain sickness. Eur J Appl Physiol 95:383–390

    Article  CAS  PubMed  Google Scholar 

  2. Araneda OF, Salazar MP (2009) Design and evaluation of a device for collecting exhaled breath condensate. J Bras Pneumol 35:69–72

    Article  Google Scholar 

  3. Araneda OF, Guevara AJ, Contreras C, Lagos N, Berral FJ (2012) Exhaled breath condensate analysis after long distance races. Int J Sports Med 33:955–961

    Article  CAS  PubMed  Google Scholar 

  4. Asami S, Hirano T, Yamaguchi R, Tsurudome Y, Itoh H, Kasai H (1998) Effects of forced and spontaneous exercise on 8-hydroxydeoxyguanosine levels in rat organs. Biochem Biophys Res Commun 243:678–682

    Article  CAS  PubMed  Google Scholar 

  5. Bloomer RJ, Canale RE, Blankenship MM, Fisher-Wellman KH (2010) Effect of Ambrotose AO(R) on resting and exercise-induced antioxidant capacity and oxidative stress in healthy adults. Nutr J 9:49

    Article  PubMed Central  PubMed  Google Scholar 

  6. Bonsignore MR, Morici G, Riccobono L, Insalaco G, Bonanno A, Profita M, Paterno A, Vassalle C, Mirabella A, Vignola AM (2001) Airway inflammation in nonasthmatic amateur runners. Am J Physiol Lung Cell Mol Physiol 281:L668–L676

    CAS  PubMed  Google Scholar 

  7. Brooks SV, Vasilaki A, Larkin LM, McArdle A, Jackson MJ (2008) Repeated bouts of aerobic exercise lead to reductions in skeletal muscle free radical generation and nuclear factor κB activation. J Physiol 586:3979–3990

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  8. Bryan NS (2006) Nitrite in nitric oxide biology: cause or consequence? A systems-based review. Free Radic Biol Med 41:691–701

    Article  CAS  PubMed  Google Scholar 

  9. Cathcart MP, Love S, Sutton DG, Reardon RJ, Hughes KJ (2013) The application of exhaled breath analysis in racing thoroughbreds and the influence of high intensity exercise and ambient temperature on the concentration of carbon monoxide and pH in exhaled breath. Vet J. doi:10.1016/j.tvjl.2012.12.022

    PubMed  Google Scholar 

  10. Cuzzolin L, Lussignoli S, Crivellente F, Adami A, Schena F, Bellavite P, Brocco G, Benoni G (2000) Influence of an acute exercise on neutrophil and platelet adhesion, nitric oxide plasma metabolites in inactive and active subjects. Int J Sports Med 21:289–293

    Article  CAS  PubMed  Google Scholar 

  11. Denguezli M, Ben Chiekh I, Ben Saad H, Zaouali-Ajina M, Tabka Z, Abdelkrim Z (2008) One-year endurance training: effects on lung function and airway inflammation. J Sports Sci 26:1351–1359

    Article  PubMed  Google Scholar 

  12. Fatouros IG, Chatzinikolaou A, Douroudos II, Nikolaidis MG, Kyparos A, Margonis K, Michailidis Y, Vantarakis A, Taxildaris K, Katrabasas I, Mandalidis D, Kouretas D, Jamurtas AZ (2010) Time-course of changes in oxidative stress and antioxidant status responses following a soccer game. J Strength Cond Res 24:3278–3286

    Article  PubMed  Google Scholar 

  13. Ferdinands JM, Crawford CA, Greenwald R, Van Sickle D, Hunter E, Teague WG (2008) Breath acidification in adolescent runners exposed to atmospheric pollution: a prospective, repeated measures observational study. Environ Health 7:10

    Article  PubMed Central  PubMed  Google Scholar 

  14. Font-Ribera L, Kogevinas M, Zock JP, Gomez FP, Barreiro E, Nieuwenhuijsen MJ, Fernandez P, Lourencetti C, Perez-Olabarria M, Bustamante M, Marcos R, Grimalt JO, Villanueva CM (2010) Short-term changes in respiratory biomarkers after swimming in a chlorinated pool. Environ Health Perspect 118:1538–1544

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  15. Gay CA, Gebicki JM (2002) Perchloric acid enhances sensitivity and reproducibility of the ferric-xylenol orange peroxide assay. Anal Biochem 304:42–46

    Article  CAS  PubMed  Google Scholar 

  16. Green LC, Wagner DA, Glogowski J, Skipper PL, Wishnok JS, Tannenbaum SR (1982) Analysis of nitrate, nitrite, and [15N]nitrate in biological fluids. Anal Biochem 126:131–138

    Article  CAS  PubMed  Google Scholar 

  17. Heinicke I, Boehler A, Rechsteiner T, Bogdanova A, Jelkmann W, Hofer M, Rawlings P, Araneda OF, Behn C, Gassmann M, Heinicke K (2009) Moderate altitude but not additional endurance training increases markers of oxidative stress in exhaled breath condensate. Eur J Appl Physiol 106:599–604

    Article  CAS  PubMed  Google Scholar 

  18. Hoffmeyer F, Raulf-Heimsoth M, Bruning T (2009) Exhaled breath condensate and airway inflammation. Curr Opin Allergy Clin Immunol 9:16–22

    Article  PubMed  Google Scholar 

  19. Hunt JF, Erwin E, Palmer L, Vaughan J, Malhotra N, Platts-Mills TA, Gaston B (2002) Expression and activity of pH-regulatory glutaminase in the human airway epithelium. Am J Respir Crit Care Med 165:101–107

    Article  PubMed  Google Scholar 

  20. Hunt J (2007) Exhaled breath condensate pH assays. Immunol Allergy Clin North Am 27:597–606

    Article  PubMed Central  PubMed  Google Scholar 

  21. Ji LL (2008) Modulation of skeletal muscle antioxidant defense by exercise: role of redox signaling. Free Radic Biol Med 44:142–152

    Article  CAS  PubMed  Google Scholar 

  22. Kippelen P, Fitch KD, Anderson SD, Bougault V, Boulet LP, Rundell KW, Sue-Chu M, McKenzie DC (2012) Respiratory health of elite athletes—preventing airway injury: a critical review. Br J Sports Med 46:471–476

    Article  PubMed Central  PubMed  Google Scholar 

  23. Larstad M, Ljungkvist G, Olin AC, Toren K (2002) Determination of malondialdehyde in breath condensate by high-performance liquid chromatography with fluorescence detection. J Chromatogr B Analyt Technol Biomed Life Sci 766:107–114

    Article  CAS  PubMed  Google Scholar 

  24. Lee SK, Kim CS, Kim HS, Cho EJ, Joo HK, Lee JY, Lee EJ, Park JB, Jeon BH (2009) Endothelial nitric oxide synthase activation contributes to post-exercise hypotension in spontaneously hypertensive rats. Biochem Biophys Res Commun 382:711–714

    Article  CAS  PubMed  Google Scholar 

  25. Marek E, Platen P, Volke J, Muckenhoff K, Marek W (2009) Hydrogen peroxide release and acid–base status in exhaled breath condensate at rest and after maximal exercise in young, healthy subjects. Eur J Med Res 14:134–139

    Article  PubMed Central  PubMed  Google Scholar 

  26. Mercken EM, Hageman GJ, Schols AM, Akkermans MA, Bast A, Wouters EF (2005) Rehabilitation decreases exercise-induced oxidative stress in chronic obstructive pulmonary disease. Am J Respir Crit Care Med 172:994–1001

    Article  PubMed  Google Scholar 

  27. Mickleborough TD, Vaughn CL, Shei RJ, Davis EM, Wilhite DP (2013) Marine lipid fraction PCSO-524™ (lyprinol(®)/omega XL(®)) of the New Zealand green lipped mussel attenuates hyperpnea-induced bronchoconstriction in asthma. Respir Med 107:1152–1163

    Article  PubMed  Google Scholar 

  28. Nieman DC, Konrad M, Henson DA, Kennerly K, Shanely RA, Wallner-Liebmann SJ (2012) Variance in the acute inflammatory response to prolonged cycling is linked to exercise intensity. J Interferon Cytokine Res 32:12–17

    Article  CAS  PubMed  Google Scholar 

  29. Niess AM, Sommer M, Schlotz E, Northoff H, Dickhuth HH, Fehrenbach E (2000) Expression of the inducible nitric oxide synthase (iNOS) in human leukocytes: responses to running exercise. Med Sci Sports Exerc 32:1220–1225

    Article  CAS  PubMed  Google Scholar 

  30. Nikolaidis MG, Jamurtas AZ (2009) Blood as a reactive species generator and redox status regulator during exercise. Arch Biochem Biophys 490:77–84

    Article  CAS  PubMed  Google Scholar 

  31. Nourooz-Zadeh J, Tajaddini-Sarmadi J, Wolff SP (1994) Measurement of plasma hydroperoxide concentrations by the ferrous oxidation–xylenol orange assay in conjunction with triphenylphosphine. Anal Biochem 220:403–409

    Article  CAS  PubMed  Google Scholar 

  32. Nowak D, Kalucka S, Bialasiewicz P, Krol M (2001) Exhalation of H2O2 and thiobarbituric acid reactive substances (TBARs) by healthy subjects. Free Radic Biol Med 30:178–186

    Article  CAS  PubMed  Google Scholar 

  33. Paget-Brown AO, Ngamtrakulpanit L, Smith A, Bunyan D, Hom S, Nguyen A, Hunt JF (2006) Normative data for pH of exhaled breath condensate. Chest 129:426–430

    Article  PubMed  Google Scholar 

  34. Pinho RA, Chiesa D, Mezzomo KM, Andrades ME, Bonatto F, Gelain D, Dal Pizzol F, Knorst MM, Moreira JC (2007) Oxidative stress in chronic obstructive pulmonary disease patients submitted to a rehabilitation program. Respir Med 101:1830–1835

    Article  CAS  PubMed  Google Scholar 

  35. Poveda JJ, Riestra A, Salas E, Cagigas ML, Lopez-Somoza C, Amado JA, Berrazueta JR (1997) Contribution of nitric oxide to exercise-induced changes in healthy volunteers: effects of acute exercise and long-term physical training. Eur J Clin Invest 27:967–971

    Article  CAS  PubMed  Google Scholar 

  36. Radak Z, Nakamura A, Nakamoto H, Asano K, Ohno H, Goto S (1998) A period of anaerobic exercise increases the accumulation of reactive carbonyl derivatives in the lungs of rats. Pflugers Arch 435:439–441

    Article  CAS  PubMed  Google Scholar 

  37. Radak Z, Chung HY, Goto S (2008) Systemic adaptation to oxidative challenge induced by regular exercise. Free Radic Biol Med 44:153–159

    Article  CAS  PubMed  Google Scholar 

  38. Reddy KV, Kumar TC, Prasad M, Reddanna P (1998) Pulmonary lipid peroxidation and antioxidant defenses during exhaustive physical exercise: the role of vitamin E and selenium. Nutrition 14:448–451

    Article  CAS  PubMed  Google Scholar 

  39. Riediker M, Danuser B (2007) Exhaled breath condensate pH is increased after moderate exercise. J Aerosol Med 20:13–18

    Article  PubMed  Google Scholar 

  40. Senturk UK, Yalcin O, Gunduz F, Kuru O, Meiselman HJ, Baskurt OK (2005) Effect of antioxidant vitamin treatment on the time course of hematological and hemorheological alterations after an exhausting exercise episode in human subjects. J Appl Physiol 98:1272–1279

    Article  CAS  PubMed  Google Scholar 

  41. Sue-Chu M, Larsson L, Moen T, Rennard SI, Bjermer L (1999) Bronchoscopy and bronchoalveolar lavage findings in cross-country skiers with and without “ski asthma”. Eur Respir J 13:626–632

    Article  CAS  PubMed  Google Scholar 

  42. Sue-Chu M, Brannan JD, Anderson SD, Chew N, Bjermer L (2010) Airway hyperresponsiveness to methacholine, adenosine 5-monophosphate, mannitol, eucapnic voluntary hyperpnoea and field exercise challenge in elite cross-country skiers. Br J Sports Med 44:827–832

    Article  PubMed Central  PubMed  Google Scholar 

  43. Sue-Chu M (2012) Winter sports athletes: long-term effects of cold air exposure. Br J Sports Med 46:397–401

    Article  PubMed  Google Scholar 

  44. Sugiura H, Ichinose M (2011) Nitrative stress in inflammatory lung diseases. Nitric Oxide 25:138–144

    Article  CAS  PubMed  Google Scholar 

  45. Verges S, Flore P, Favre-Juvin A, Lévy P, Wuyam B (2005) Exhaled nitric oxide during normoxic and hypoxic exercise in endurance athletes. Acta Physiol Scand 185:123–131

    Article  CAS  PubMed  Google Scholar 

  46. Veszelovsky E, Holford NH, Thomsen LL, Knowles RG, Baguley BC (1995) Plasma nitrate clearance in mice: modeling of the systemic production of nitrate following the induction of nitric oxide synthesis. Cancer Chemother Pharmacol 36:155–159

    Article  CAS  PubMed  Google Scholar 

  47. Walsh NP, Gleeson M, Shephard RJ, Gleeson M, Woods JA, Bishop NC, Fleshner M, Green C, Pedersen BK, Hoffman-Goetz L, Rogers CJ, Northoff H, Abbasi A, Simon P (2011) Position statement. Part one: Immune function and exercise. Exerc Immunol Rev 17:6–63

    PubMed  Google Scholar 

Download references

Acknowledgments

We acknowledge Mr. Luis Pizarro Zúñiga for his technical assistance in sample collection and chemical analysis of the samples.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to O. F. Araneda.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Araneda, O.F., Urbina-Stagno, R., Tuesta, M. et al. Increase of pro-oxidants with no evidence of lipid peroxidation in exhaled breath condensate after a 10-km race in non-athletes. J Physiol Biochem 70, 107–115 (2014). https://doi.org/10.1007/s13105-013-0285-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13105-013-0285-0

Keywords

Navigation