Skip to main content
Log in

Stress failure of pulmonary capillaries as a limiting factor for maximal exercise

  • Invited Review
  • Published:
European Journal of Applied Physiology and Occupational Physiology Aims and scope Submit manuscript

Abstract

The pulmonary blood-gas barrier has a basic physiological dilemma. On the one hand it needs to be extremely thin for efficient gas exchange. On the other hand it also needs to be immensely strong because the stresses on the pulmonary capillary wall become extremely high when the capillary pressure rises on exercise. Maximal hydrostatic pressures in human pulmonary capillaries during exercise are not accurately known but must exceed 30 mmHg. In some animals, for example thoroughbred horses, the capillary pressure rises to about 100 mmHg. These pressures cause stresses in the capillary wall of 5–10 × 104 N·M−2 (50–100 kPa) which approach the breaking strength of collagen. The strength of the capillary wall on the thin side of the blood-gas barrier can be attributed to the type IV collagen of the extracellular matrix. Raising the capillary pressure to similar levels in experimental preparations causes ultrastructural changes in the wall including disruption of the capillary endothelium, alveolar epithelium, and basement membrane in the interstitium. Essentially all thoroughbred racehorses bleed into their lungs during exercise because they break their capillaries, and some elite human athletes apparently do the same. Avoiding stress failure of pulmonary capillaries poses a challenging problem for some species. Stress failure is a hitherto overlooked factor limiting maximal exercise.

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.

Similar content being viewed by others

References

  • Bevegard S, Holmgren A, Jonsson B (1960) The effect of body position on the circulation at rest and during exercise, with special reference to the influence of the stroke volume. Acta Physiol Scand 49:279–298

    Google Scholar 

  • Bhattacharya J, Nanjo S, Staub NC (1982) Micropuncture measurement of lung microvascular pressure during 5-HT infusion. J Appl Physiol 52:634–637

    Google Scholar 

  • Birks EK, Mathieu-Costello O, Fu Z, Tyler WS, et al (1994) Comparative aspects of the strength of pulmonary capillaries in rabbit, dog and horse. Respir Physiol 97:235–246

    Google Scholar 

  • Breisch EA, White F, Jones HM, Laurs RM (1983) Ultrastructural morphometry of the myocardium of Thunnus alalunga. Cell Tissue Res 233:427–438

    Google Scholar 

  • Costello ML, Mathieu-Costello O, West JB (1992) Stress failure of alveolar epithelial cells studied by scanning electron microscopy. Am Rev Respir Dis 145:1446–1455

    Google Scholar 

  • Crouch EC, Martin GR, Brody JS (1991) Basement membranes. In: Crystal RG, West JB (eds) The lung; scientific foundations. Raven Press, New York, pp 421–437

    Google Scholar 

  • Dempsey JA, Hanson PG, Henderson KS (1984) Exercise-induced alveolar hypoxemia in healthy human subjects at sealevel. J Physiol (Lond) 355:161–175

    Google Scholar 

  • Elliott AR, Fu Z, Tsukimoto K, Prediletto R, et al (1992) Shortterm reversibility of ultrastructural changes in pulmonary capillaries caused by stress failure. J Appl Physiol 73:1150–1158

    Google Scholar 

  • Erickson BK, Erickson HH, Coffman JR (1990) Pulmonary artery, aortic and oesophageal pressure changes during high intensity treadmill exercise in the horse: a possible relation to exercise-induced pulmonary haemorrhage. Equine Vet J [Suppl] 9:47–52

    Google Scholar 

  • Erickson HH, Hopper MK, Olsen SC, Pelletier N, et al (1992) Cardiopulmonary mechanisms of exercise-induced pulmonary hemorrhage and action of furosemide. In: Blake-Caddel L (ed) Proceedings of the Thirty-Seventh Annual Convention of the American Association of Equine Practitioners. American Association of Equine Practitioners, San Francisco, pp 651–661

    Google Scholar 

  • Everson RB, Schreinemachers DM, Devlin RB, Koren HS (1994) Host determinants of cellular and biochemical constituents of bronchoalveolar lavage fluids. Implications for design of epidemiologic studies. Am Rev Respir Crit Care Med 149:899–904

    Google Scholar 

  • Fisher RF, Wakely J (1976) The elastic constants and ultrastructural organization of a basement membrane (lens capsule). Proc R Soc Lond [Biol] 193:335–358

    Google Scholar 

  • Fu Z, Costello ML, Tsukimoto K, Prediletto R, et al (1992) High lung volume increases stress failure in pulmonary capillaries. J Appl Physiol 73:123–133

    Google Scholar 

  • Gehr P, Bachofen M, Weibel ER (1978) The normal human lung: ultrastructure and morphometric estimation of diffusion capacity. Respir Physiol 32:121–140

    Google Scholar 

  • Groves BM, Reeves JT, Sutton JR, Wagner PD, et al (1987) Operation Everest II: elevated high-altitude pulmonary resistance unresponsive to oxygen. J Appl Physiol 63:521–530

    Google Scholar 

  • Jones JH, Smith BL, Birks EK, Pascoe JR, et al (1992) Left atrial and pulmonary arterial pressures in exercising horses (abstract). FASEB J 6:A2020

    Google Scholar 

  • Kay JM, Edwards FR (1973) Ultrastructure of the alveolar-capillary wall in mitral stenosis. J Path 111:239–245

    Google Scholar 

  • King RR, Raskin RE, Rosbolt JP (1990) Exercise-induced pulmonary hemorrhage in the racing greyhound dog (abstract). J Vet Int Med 4:130

    Google Scholar 

  • Lindstedt SL, Hokanson JF, Wells DJ, Swain SD, et al (1991) Running energetics in the pronghorn antelope. Nature 353:748–750

    Google Scholar 

  • Low FN (1953) The pulmonary alveolar epithelium of laboratory mammals and man. Anat Rec 117:241–263

    Google Scholar 

  • Manohar M (1993) Pulmonary artery wedge pressure increases with high-intensity exercise in horses. Am J Vet Res 54:142–146

    Google Scholar 

  • Markham G (1688) Markham's master-piece revived: containing all knowledge belonging to the smith, furrier or horse-leach. John Richardson for Tho. Passinger, London

    Google Scholar 

  • McKechnie JK, Leary WP, Noakes TD, Kallmeyer JC, et al (1979) Acute pulmonary oedema in two athletes during a 90km running race. S Afr Med J 56:261–265

    Google Scholar 

  • Merker H-J (1994) Morphology of the basement membrane. Microsc Res Technique 28:95–124

    Google Scholar 

  • Olson KR (1991) Vasculature of the fish gill: anatomical correlates of physiological functions. J Electron Microsc Technique 19:389–405

    Google Scholar 

  • Pascoe JR, Ferraro GL, Cannon JH, Arthur RM, et al (1981) Exercise-induced pulmonary hemorrhage in racing thoroughbreds: a preliminary study. Am J Vet Res 42:703–707

    Google Scholar 

  • Reeves JT, Groves BM, Cymerman A, Sutton JR, et al (1990) Operation Everest II: cardiac filling pressures during cycle exercise at sea level. Respir Physiol 80:147–154

    Google Scholar 

  • Seeherman HJ, Taylor CR, Maloiy GMO, Armstrong RB (1981) Design of the mammalian respiratory system, II. Measuring maximum aerobic capacity. Respir Physiol 44:11–23

    Google Scholar 

  • Stevens ED, Neill WH (1978) Body temperature relations of tunas, especially skipjack. In: Hoar WS, Randall DJ (eds) Fish physiology, vol VII. Academic Press, New York, pp 315–359

    Google Scholar 

  • Sweeney CR (1991) Exercise-induced pulmonary hemorrhage. Vet Clin North Am 7:93–104

    Google Scholar 

  • Timpl R, Wiedemann H, van Delden V, Furthmayr H, et al (1981) A network model for the organization of type IV collagen molecules in basement membranes. Eur J Biochem 120:203–211

    Google Scholar 

  • Tsukimoto K, Mathieu-Costello O, Prediletto R, Elliott AR, et al (1991) Ultrastructural appearances of pulmonary capillaries at high transmural pressures. J Appl Physiol 71:573–582

    Google Scholar 

  • Tsukimoto K, Yoshimura N, Ichioka M, Tojo N, et al (1994) Protein, cell, and leukotriene B4 concentrations of lung edema fluid produced by high capillary pressures in rabbit. J Appl Physiol 76:321–327

    Google Scholar 

  • Vaccaro CA, Brody JS (1981) Structural features of alveolar wall basement membrane in the adult rat lung. J Cell Biol 91:427–437

    Google Scholar 

  • Wagner PD, Gale GE, Moon RE, Torre-Bueno JR, et al (1986) Pulmonary gas exchange in humans exercising at sea level and simulated altitude. J Appl Physiol 61:260–270

    Google Scholar 

  • Wagner PD, Gillespie JR, Landgren GL, Fedde MR, et al (1989) Mechanism of exercise-induced hypoxemia in horses. J Appl Physiol 66:1227–1233

    Google Scholar 

  • Welling LW, Grantham JJ (1972) Physical properties of isolated perfused renal tubules and tubular basement membranes. J Clin Invest 51:1063–1075

    Google Scholar 

  • West JB, Mathieu-Costello O (1992) Strength of the pulmonary blood-gas barrier. Respir Physiol 88:141–148

    Google Scholar 

  • West JB, Mathieu-Costello O, Geddes DM (1991a) Intrapulmonary hemorrhage caused by stress failure of pulmonary capillaries during exercise (abstract). Am Rev Respir Dis 143: A569

    Google Scholar 

  • West JB, Tsukimoto K, Mathieu-Costello O, Prediletto R (1991b) Stress failure in pulmonary capillaries. J Appl Physiol 70:1731–1742

    Google Scholar 

  • West JB, Mathieu-Costello O, Jones JH, Birks EK, et al (1993) Stress failure of pulmonary capillaries in racehorses with exercise-induced pulmonary hemorrhage. J Appl Physiol 75:1097–1109

    Google Scholar 

  • Whitwell KE, Greet TRC (1984) Collection and evaluation of tracheobronchial washes in the horse. Equine Vet J 16:499–508

    Google Scholar 

  • Williamson JR, Vogler NJ, Kilo C (1971) Regional variations in the width of the basement membrane of muscle capillaries in man and giraffe. Am J Pathol 63:359–370

    Google Scholar 

  • Younes M, Bshouty Z, Ali J (1987) Longitudinal distribution of pulmonary vascular resistance with very high pulmonary blood flow. J Appl Physiol 62:344–358

    Google Scholar 

  • Yurchenco PD, Schittny JC (1990) Molecular architecture of basement membranes. FASEB J 4:1577–1590

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

West, J.B., Mathieu-Costello, O. Stress failure of pulmonary capillaries as a limiting factor for maximal exercise. Eur J Appl Physiol 70, 99–108 (1995). https://doi.org/10.1007/BF00361536

Download citation

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00361536

Key words

Navigation