Skip to main content
SpringerLink
Log in

Lung oxidative stress as related to exercise and altitude. Lipid peroxidation evidence in exhaled breath condensate: a possible predictor of acute mountain sickness

  • Original Article
  • Published:
European Journal of Applied Physiology Aims and scope Submit manuscript

Abstract

Lung oxidative stress (OS) was explored in resting and in exercising subjects exposed to moderate and high altitude. Exhaled breath condensate (EBC) was collected under field conditions in male high-competition mountain bikers performing a maximal cycloergometric exercise at 670 m and at 2,160 m, as well as, in male soldiers climbing up to 6,125 m in Northern Chile. Malondialdehyde concentration [MDA] was measured by high-performance liquid chromatography in EBC and in serum samples. Hydrogen peroxide concentration [H2O2] was analysed in EBC according to the spectrophotometric FOX2 assay. [MDA] in EBC of bikers did not change while exercising at 670 m, but increased from 30.0±8.0 to 50.0±11.0 nmol l−1 (P<0.05) at 2,160 m. Concomitantly, [MDA] in serum and [H2O2] in EBC remained constant. On the other hand, in mountaineering soldiers, [H2O2] in EBC under resting conditions increased from 0.30±0.12 μmol l−1 at 670 m to 1.14±0.29 μmol l−1 immediately on return from the mountain. Three days later, [H2O2] in EBC (0.93 ±0.23 μmol l−1) continued to be elevated (P<0.05). [MDA] in EBC increased from 71±16 nmol l−1 at 670 m to 128±26 nmol l−1 at 3,000 m (P<0.05). Changes of [H2O2] in EBC while ascending from 670 m up to 3,000 m inversely correlated with concomitant variations in HbO2 saturation (r=−0.48, P<0.05). AMS score evaluated at 5,000 m directly correlated with changes of [MDA] in EBC occurring while the subjects moved from 670 to 3,000 m (r=0.51, P<0.05). Lung OS may constitute a pathogenic factor in AMS.

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
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Arnould T, Michiels C, Janssens D, Delaive E, Remacle J (1995) Hypoxia induces PMN adherence to umbilical vein endothelium. Cardiovasc Res 30:1009–1016

    Article  PubMed  CAS  Google Scholar 

  • 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  PubMed  CAS  Google Scholar 

  • Bailey DM, Davies B (2001) Acute mountain sickness; prophylactic benefits of antioxidant vitamin supplementation at high altitude. High Alt Med Biol 2:21–29

    Article  PubMed  CAS  Google Scholar 

  • Bailey DM, Davies B, Young IS, Hullin DA, Seddon PS (2001) A potential role for free radical-mediated skeletal muscle soreness in the pathophysiology of acute mountain sickness. Aviat Space Environ Med 72:513–521

    PubMed  CAS  Google Scholar 

  • Bailey DM, Kleger GR, Holzgraefe M, Ballmer PE, Bartsch P (2004) Pathophysiological significance of peroxidative stress, neuronal damage, and membrane permeability in acute mountain sickness. J Appl Physiol 96:1459–1463

    Article  PubMed  Google Scholar 

  • Baldwin SR, Simon RH, Grum CM, Ketai LH, Boxer LA, Devall LJ (1986) Oxidant activity in expired breath of patients with adult respiratory distress syndrome. Lancet 1(8471):11–14

    Article  PubMed  CAS  Google Scholar 

  • Beck-Schimmer B, Schimmer RC, Madjdpour C, Bonvini JM, Pasch T, Ward PA (2001) Hypoxia mediates increased neutrophil and macrophage adhesiveness to alveolar epithelial cells. Am J Respir Cell Mol Biol 25:780–787

    PubMed  CAS  Google Scholar 

  • Behn C, Estrada MI, Dávila E, Araneda O,González M, Soria R (1999) Altitude related changes in red blood cell membrane lipids and proteins. Possible link with redox equilibrium, acid-base status and cell calcium.Trace Elem Man Anim 10:399–404

    Google Scholar 

  • Carpagnano GE, Kharitonov SA, Resta O, Foschino-Barbaro MP, Gramiccioni E, Barnes PJ (2002) Increased 8-isoprostane and interleukin-6 in breath condensate of obstructive sleep apnea patients. Chest 122:1162–1167

    Article  PubMed  CAS  Google Scholar 

  • Carpenter C, Price P, Christman B (1998) Exhaled breath condensate isoprostanes are elevated in patients with acute lung injury or ARDS. Chest 114:1653–1659

    Article  PubMed  CAS  Google Scholar 

  • Casillan AJ, Gonzalez NC, Johnson JS, Steiner DR, Wood JG (2003) Mesenteric microvascular inflammatory responses to systemic hypoxia are mediated by PAF and LTB4. J Appl Physiol 94:2313–2322

    PubMed  CAS  Google Scholar 

  • Celedón G, González G, Sotomayor CP, Behn C (1998) Membrane lipid diffusion and band 3 protein changes in human erythrocytes due to acute hypobaric hypoxia. Am J Physiol 275:C1429–C1431

    PubMed  Google Scholar 

  • Corradi M, Rubinstein I, Andreoli R, Manini P, Caglieri A, Poli D, Alinovi R, Mutti A (2003) Aldehydes in exhaled breath condensate of patients with chronic obstructive pulmonary disease. Am J Respir Crit Care Med 167:1380–1386

    Article  PubMed  Google Scholar 

  • Cracowski JL, Cracowski C, Bessard G, Pepin JL, Bessard J, Schwebel C, Stanke-Labesque F, Pison C (2001) Increased lipid peroxidation in patients with pulmonary hypertension. Am J Respir Crit Care Med 164:1038–1042

    PubMed  CAS  Google Scholar 

  • Eldridge MW, Braun RK, Yoneda KY, Walby WF, Bennett S, Hyde DM (1998) Lung injury after heavy exercise at altitude. Chest 114:66S–67S

    Article  PubMed  CAS  Google Scholar 

  • Garey KW, Neuhauser MM, Robbins RA, Danziger LH, Rubinstein I (2004) Markers of inflammation in exhaled breath condensate of young healthy smokers. Chest 125:22–26

    Article  PubMed  CAS  Google Scholar 

  • González G, Celedón G, Sandoval M, González GE, Ferrer V, Astete R, Behn C (2002) Hypobaric hypoxia-reoxygenation diminishes band 3 protein functions in human erythrocytes. Pflügers Arch 445:337–341

    Article  PubMed  Google Scholar 

  • Hackett P, Oelz O (1992) The Lake Louise consensus on the definition and quantification of altitude illnes. In: Sutton JR, Coates G, Houston CS (eds) Hypoxia and mountain medicine. Queen City Printers, Burlington, pp 327–330

    Google Scholar 

  • Hassoun PM, Yu FS, Cote CG, Zulueta JJ, Sawhney R, Skinner KA, Skinner HB, Parks DA, Lanzillo JJ (1998) Upregulation of xanthine oxidase by lipopolysaccharide, interleukin-1, and hypoxia. Role in acute lung injury. Am J Respir Crit Care Med 158:299–305

    PubMed  CAS  Google Scholar 

  • Horvath I, Donnelly LE, Kiss A, Kharitonov SA, Lim S, Fan Chung K, Barnes PJ (1998) Combined use of exhaled hydrogen peroxide and nitric oxide in monitoring asthma. Am J Respir Crit Care Med 158:1042–1046

    PubMed  CAS  Google Scholar 

  • Hoshikawa Y, Ono S, Suzuki S, Tanita T, Chida M, Song C, Noda M, Tabata T, Voelkel NF, Fujimura S (2001) Generation of oxidative stress contributes to the development of pulmonary hypertension induced by hypoxia. J Appl Physiol 90:1299–1306

    PubMed  CAS  Google Scholar 

  • Jackson RM, Parish G, Ho YS (1996) Effects of hypoxia on expression of superoxide dismutases in cultured ATII cells and lung fibroblasts. Am J Physiol 271:L955–L962

    PubMed  CAS  Google Scholar 

  • Joanny P, Steinberg J, Robach P, Richalet JP, Gortan C, Gardette B, Jammes Y (2001) Operation Everest III (Comex’97): the effect of simulated sever hypobaric hypoxia on lipid peroxidation and antioxidant defence systems in human blood at rest and after maximal exercise. Resuscitation 49:307–314

    Article  PubMed  CAS  Google Scholar 

  • 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  PubMed  CAS  Google Scholar 

  • Loukides S, Bouros D, Papatheodorou G, Lachanis S, Panagou P, Siafakas NM (2002) Exhaled H2O2 in steady-state bronchiectasis: relationship with cellular composition in induced sputum, spirometry, and extent and severity of disease. Chest 121:81–87

    Article  PubMed  CAS  Google Scholar 

  • Madjdpour C, Jewell UR, Kneller S, Ziegler U, Schwendener R, Booy C, Klausli L, Pasch T, Schimmer RC, Beck-Schimmer B (2003) Decreased alveolar oxygen induces lung inflammation. Am J Physiol Lung Cell Mol Physiol 284:L360–L367

    Google Scholar 

  • Merker MP, Pitt BR, Choi AM, Hassoun PM, Dawson CA, Fisher AB (2000) Lung redox homeostasis: emerging concepts. Am J Physiol Lung Cell Mol Physiol 279:L413–L417

    PubMed  CAS  Google Scholar 

  • Minko T, Stefanov A, Pozharov V (2002) Lung edema clearence: 20 years of progress selected contribution : lung hypoxia:antioxidant and antiapoptotic effects of liposomal α-tocopherol. J Appl Physiol 93:1550–1560

    PubMed  CAS  Google Scholar 

  • Montuschi P, Ciabattoni G, Paredi P, Pantelidis P, du Bois RM, Kharitonov SA, Barnes PJ (1998) 8-Isoprostane as a biomarker of oxidative stress in interstitial lung diseases. Am J Respir Crit Care Med 158:1524–1527

    PubMed  CAS  Google Scholar 

  • Montuschi P, Kharitonov SA, Ciabattoni G, Corradi M, van Rensen L, Geddes DM, Hodson ME, Barnes PJ (2000) Exhaled 8-isoprostane as a new non-invasive biomarker of oxidative stress in cystic fibrosis. Thorax 55:205–209

    Article  PubMed  CAS  Google Scholar 

  • Nakanishi K, Tajima F, Nakamura A, Yagura S, Ookawara T, Yamashita H, Suzuki K, Taniguchi N, Ohno H (1995) Effects of hypobaric hypoxia on antioxidant enzymes in rats. J Physiol 489:869–876

    PubMed  CAS  Google Scholar 

  • Nielsen VG, Tan S, Weinbroum A, McCammon AT, Samuelson PN, Gelman S, Parks DA (1996) Lung injury after hepatoenteric ischemia-reperfusion: role of xanthine oxidase. Am J Respir Crit Care Med 154:1364–1369

    PubMed  CAS  Google Scholar 

  • 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  PubMed  CAS  Google Scholar 

  • 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  PubMed  CAS  Google Scholar 

  • 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  PubMed  CAS  Google Scholar 

  • 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  PubMed  CAS  Google Scholar 

  • Russell WJ, Ho YS, Parish G, Jackson RM (1995) Effects of hypoxia on MnSOD expression in mouse lung. Am J Physiol 269:L221–L226

    PubMed  CAS  Google Scholar 

  • Sulkowska M (1997) Morphological studies of the lungs in chronic hypobaric hypoxia. Pol J Pathol 48:225–234

    PubMed  CAS  Google Scholar 

  • Szkudlarek U, Maria L, Kasielski M, Kaucka S, Nowak D (2003) Exhaled hydrogen peroxide correlates with the release of reactive oxygen species by blood phagocytes in healthy subjects. Respir Med 97:718–725

    Article  PubMed  CAS  Google Scholar 

  • Sznajder JI, Fraiman A, Hall JB, Sanders W, Schmidt G, Crawford G, Nahum A, Factor P, Wood LD (1989) Increased hydrogen peroxide in the expired breath of patients with acute hypoxemic respiratory failure. Chest 96:606–612

    Article  PubMed  CAS  Google Scholar 

  • Vasankari TJ, Kujala UM, Rusko H, Sarna S, Ahotupa M (1997) The effect of endurance exercise at moderate altitude on serum lipid peroxidation and antioxidative functions in humans. Eur J Appl Physiol Occup Physiol 75:396–399

    Article  PubMed  CAS  Google Scholar 

  • Wilhelm J, Frydrychova M, Vizek M (1999) Hydrogen peroxide in the breath of rats: the effects of hypoxia and paraquat. Physiol Res 48:445–449

    PubMed  CAS  Google Scholar 

  • Wilhelm J, Vankova M, Maxova H, Siskova A (2003) Hydrogen peroxide production by alveolar macrophages is increased and its concentration is elevated in the breath of rats exposed to hypoxia: relationship to lung lipid peroxidation. Physiol Res 52:327–332

    PubMed  CAS  Google Scholar 

  • Wood JG, Johnson JS, Mattioli LF, Gonzalez NC (2000) Systemic hypoxia increases leukocyte emigration and vascular permeability in conscious rats. J Appl Physiol 89: 1561–1568

    PubMed  CAS  Google Scholar 

Download references

Acknowledgements

We thank Mr. Luis Pizarro and Mr. Humberto Monsalve for skilful technical help. Valuable facilities for realization of the present work were kindly provided both by Federación Chilena de Ciclismo and by Escuela de los Servicios y Educación Física del Ejército de Chile. Financially, the work was supported by FONDECYT Project Nr. 1000858.

Author information

Authors and Affiliations

  1. Laboratorio de Ambientes Extremos, Programa de Fisiología y Biofísica, ICBM, Facultad de Medicina, Universidad de Chile, Santiago, Chile

    OF Araneda, C García, N Lagos, MP Salazar & C Behn

  2. Servicio de Laboratorios Clínicos, Pontificia Universidad Católica de Chile, Santiago, Chile

    G Quiroga

  3. Departamento de Ciencias del Deporte, Instituto Nacional de Deportes, Santiago, Chile

    J Cajigal

  4. Departamento de Educación Física, Facultad de Educación, Universidad Mayor, Santiago, Chile

    OF Araneda

Authors
  1. OF Araneda
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. C García
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. N Lagos
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. G Quiroga
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. J Cajigal
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. MP Salazar
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. C Behn
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to OF Araneda.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Araneda, O., García, C., Lagos, N. et al. 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 (2005). https://doi.org/10.1007/s00421-005-0047-y

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00421-005-0047-y

Keywords

Search

Navigation