Hostname: page-component-cd9895bd7-p9bg8 Total loading time: 0 Render date: 2024-12-23T20:12:13.341Z Has data issue: false hasContentIssue false

Modeling of the oxygen transfer in the respiratory process

Published online by Cambridge University Press:  13 June 2013

Sébastien Martin
Affiliation:
INRIA Paris Rocquencourt, REO project – BP 105, 78153 Le Chesnay cedex, France Laboratoire de Mathématiques d’Orsay, Université Paris-Sud, 91405 Orsay cedex, France.. [email protected]
Bertrand Maury
Affiliation:
Laboratoire de Mathématiques d’Orsay, Université Paris-Sud, 91405 Orsay cedex, France.. [email protected]
Get access

Abstract

In this article, we propose an integrated model for oxygen transfer into the blood,coupled with a lumped mechanical model for the ventilation process. Objectives.We aim at investigating oxygen transfer into the blood at rest or exercise. Thefirst task consists in describing nonlinear effects of the oxygen transfer under normalconditions. We also include the possible diffusion limitation in oxygen transfer observedin extreme regimes involving parameters such as alveolar and venous blood oxygen partialpressures, capillary volume, diffusing capacity of the membrane, oxygen binding byhemoglobin and transit time of the red blood cells in the capillaries. The second taskconsists in discussing the oxygen concentration heterogeneity along the path length in theacinus. Method. A lumped mechanical model is considered: a double-balloonmodel is built upon physiological properties such as resistance of the branches connectingalveoli to the outside air, and elastic properties of the surrounding medium. Then, wefocus on oxygen transfer: while the classical [F.J. Roughton and R.E. Forster, J.Appl. Physiol. 11 (1957) 290–302]. approach accounts for thereaction rate with hemoglobin by means of an extra resistance between alveolar air andblood, we propose an alternate description. Under normal conditions, the Hill’s saturationcurve simply quantifies the net oxygen transfer during the time that venous blood stays inthe close neighborhood of alveoli (transit time). Under degraded and/or exerciseconditions (impaired alveolar-capillary membrane, reduced transit time, high altitude)diffusion limitation of oxygen transfer is accounted for by means of the nonlinearequation representing the evolution of oxygen partial pressure in the plasma during thetransit time. Finally, a one-dimensional model is proposed to investigate the effects oflongitudinal heterogeneity of oxygen concentration in the respiratory tract during theventilation cycle, including previous considerations on oxygen transfer. Results.This integrated approach allows us to recover the right orders of magnitudes interms of oxygen transfer, at rest or exercise, by using well-documented data, without anyparameter tuning or curve fitting procedure. The diffusing capacity of thealveolar-capillary membrane does not affect the oxygen transfer rate in the normal regimebut, as it decreases (e.g. because of emphysema) below a critical value,it becomes a significant parameter. The one-dimensional model allows to investigate thescreening phenomenon, i.e. the possibility that oxygen transfer might besignificantly affected by the fact that the exchange area in the peripheral acinus poorlyparticipates to oxygen transfer at rest, thereby providing a natural reserve of transfercapacity for exercise condition. We do not recover this effect: in particular we showthat, at rest, although the oxygen concentration is slightly smaller in terminal alveoli,transfer mainly occurs in the acinar periphery.

Type
Research Article
Copyright
© EDP Sciences, SMAI, 2013

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

E. Agostoni and R.E. Hyatt, Static behavior of the respiratory system, in Handbook of physiology, edited by S.R. Geiger, 2nd edition. American Physiological Society, Bethesda (1986) 113–130.
Bates, D.V., Varvis, C.J., Donevan, R.E. and Christie, R.V., Variations in the pulmonary capillary blood volume and membrane diffusion component in health and disease. J. Clin. Invest. 39 (1960) 14011412. Google ScholarPubMed
Begin, R., Renzetti, A.D. Jr., Bigler, A.H. and Watanabe, S., Flow and age dependence of airway closure and dynamic compliance. J. Appl. Physiol. 38 (1975) 199207. Google ScholarPubMed
Ben-Tal, A., Simplified models for gas exchange in the human lungs. J. Theor. Biol. 238 (2006) 474495. Google ScholarPubMed
Brighenti, C., Gnudi, G. and Avanzolini, G., A simulation model of the oxygen alveolo-capillary exchange in normal and pathological conditions. Physiol. Meas. 24 (2003) 261275. Google ScholarPubMed
Brochard, L., Mancebo, J., Wysocki, M., Lofaso, F., Conti, G., Rauss, A., Simonneau, G., Benito, S., Gasparetto, A., Lemaire, F., Isabey, D. and Harf, A., Noninvasive ventilation for acute exacerbations of chronic obstructive pulmonary disease. N. Engl. J. Med. 333 (1995) 817822. Google ScholarPubMed
J.E. Cotes, D.J. Chinn and M.R. Miller, Lung function: Physiology, Measurement and Application in Medicine, 6th edition. Blackwell Publishing Ltd. (2006).
Cotes, J.E., Chinn, D.J., Quanjer, Ph., Roca, J. and Yernault, J.C., Standardization of the measurement of transfer factor (diffusing capacity). Eur. Respir. J. suppl 16 (1993) 4152. Google Scholar
Crandall, E.D. and Flumerfelt, R.W., Effect of time-varying blood flow on oxygen uptake in the pulmonary capillaries. Appl. Physiol. 23 (1967) 944953. Google ScholarPubMed
The lung: Scientific Foundations, edited by R.G. Crystal, J.B. West, E.R. Weibel and P.J. Barnes, 2nd edition. Lippincott-Raven Press, Philadelphia 2 (1997).
Eaton, W.A., Henry, E.R., Hofrichter, J. and Mozzarelli, A., Is cooperative oxygen binding by hemoglobin really understood?. Nat. Struct. Biol. 6 (1999) 351358. Google ScholarPubMed
Felici, M., Filoche, M. and Sapoval, B., Diffusional screening in the human pulmonary acinus. J. Appl. Physiol. 94 (2003) 20102016. Google ScholarPubMed
Felici, M., Filoche, M. and Sapoval, B., Renormalized random walk study of oxygen absorption in the human lung. Phys. Rev. Lett. 92 (2004) 068101. Google ScholarPubMed
Felici, M., Filoche, M., Straus, C., Similowski, T. and Sapoval, B., Diffusional screening in real 3D human acini – a theoretical study. Respir. Physiol. Neurobiol. 145 (2005) 279293. Google ScholarPubMed
Filoche, M. and Florens, M., The stationary flow in a heterogeneous compliant vessel network. J. Phys. Conf. Ser. 319 (2011) 012008. Google Scholar
A. Foucquier, Dynamique du transport et du transfert de l’oxygène au sein de l’acinus pulmonaire humain. Ph.D. thesis, École Polytechnique (2010).
Gehr, P., Bachofen, M. and Weibel, E.R., The normal human lung: ultrastructure and morphometric estimation of diffusion capacity. Respir. Physiol. 32 (1978) 121140. Google ScholarPubMed
A.C. Guyton and J.E. Hall, Textbook of medical physiology, 9th edition. W.B. Saunders Co, Philadelphia (1996).
M.P. Hlastala and A.J. Berger, Physiology of Respiration, 2nd edition. Oxford University Press, Oxford (2001).
C. Hou, S. Gheorghiu, M.-O. Coppens, V.H. Huxley and P. Pfeifer, Gas diffusion through the fractal landscape of the lung: How deep does oxygen enter the alveolar system? in Fractals in Biology and Medicine, edited by G.A. Losa, D. Merlini, T.F. Nonnenmacher, E.R. Weibel. Basel: Birkhäuser IV (2005) 17–30.
J.M.B. Hughes, Pulmonary gas exchange. in Lung Function Testing, edited by R. Gosselink and H. Stam. European Respiratory Monograph 10 (2005) 106–126.
J. Keener and J. Sneyd, Mathematical Physiology. Interdisciplinary Applied Mathematics. Springer (1998).
Kelman, G.R., Digital computer subroutine for the conversion of oxygen tension into saturation. J. Appl. Physiol. 21 (1966) 13751376. Google ScholarPubMed
J.D. Kibble and C. Halsey, Medical Physiology, The Big Picture. McGraw Hill (2009).
Liu, C.H., Niranjan, S.C., Clark, J.W., San, K.Y., Zwischenberger, J.B. and Bidani, A., Airway mechanics, gas exchange, and blood flow in a nonlinear model of the normal human lung. J. Appl Physiol. 84 (1998) 14471469. Google Scholar
Martin, S., Similowski, T., Straus, C. and Maury, B., Impact of respiratory mechanics model parameter on gas exchange efficiency. ESAIM Proc. 23 (2008) 3047. Google Scholar
Mauroy, B. and Bokov, P., Influence of variability on the optimal shape of a dichotomous airway tree branching asymmetrically. Phys. Biol. 7 (2010) 016007. Google Scholar
Mauroy, B., Filoche, M., Andrade, J.S. Jr. and Sapoval, B., Interplay between flow distribution and geometry in an airway tree. Phys. Rev. Lett. 90 (2003) 14. Google Scholar
Mauroy, B., Filoche, M., Weibel, E.R., and Sapoval, B., An optimal bronchial tree may be dangerous. Nature 427 (2004) 633636. Google ScholarPubMed
Mauroy, B. and Meunier, N., Optimal Poiseuille flow in a finite elastic dyadic tree. ESAIM: M2AN 42 (2008) 507534. Google Scholar
Paiva, M. and Engel, L.A., Model analysis of gas distribution within human lung acinus. J. Appl. Physiol. 56 (1984) 418425. Google ScholarPubMed
Piiper, J. and Scheid, P., Respiration: alveolar gas exchange. Annu. Rev. Physiol. 33 (1971) 131154. Google ScholarPubMed
Roughton, F.J. and Forster, R.E., Relative importance of diffusion and chemical reaction rates in determining rate of exchange of gases in the human lung, with special reference to true diffusing capacity of pulmonary membrane and volume of blood in the lung capillaries. J. Appl. Physiol. 11 (1957) 290302. Google ScholarPubMed
Sapoval, B. and Filoche, M., Role of diffusion screening in pulmonary diseases. Adv. Exp. Med. Biol. 605 (2008) 173178. Google ScholarPubMed
Sapoval, B., Filoche, M. and Weibel, E.R., Smaller is better − but not too small: a physical scale for the design of the mammalian pulmonary acinus. Proc. Natl. Acad. Sci. USA 99 (2002) 10411. Google Scholar
Similowski, T. and Bates, J.H.T., Two-compartment modelling of respiratory system mechanics at low frequencies: gas redistribution or tissue rheology? Eur. Respir. J. 4 (1991) 353358. Google ScholarPubMed
Soong, T.T., Nicolaides, P., Yu, C.P. and Soong, S.C., A statistical description of the human tracheobronchial tree geometry. Respir. Physiol. 37 (1979) 16172. Google ScholarPubMed
Swan, A.J. and Tawhai, M.H., Evidence for minimal oxygen heterogeneity in the healthy human pulmonary acinus. J. Appl. Physiol. 110 (2011) 528537. Google ScholarPubMed
Sznitman, J., Convective gas transport in the pulmonary acinus: comparing roles of convective and diffusive lengths. J. Biomech. 42 (2009) 789792. Google ScholarPubMed
Tantucci, C., Duguet, A., Giampiccolo, P., Similowski, T., Zelter, M. and Derenne, J.-P., The best peak expiratory flow is flow-limited and effort-independent in normal subjects. Am. J. Respir. Crit. Care Med. 165 (2002) 13041308. Google ScholarPubMed
Tawhai, M.H. and Hunter, P.J., Characterising respiratory airway gas mixing using a lumped parameter model of the pulmonary acinus. Respir. Physiol. 127 (2001) 241248. Google ScholarPubMed
E.R. Weibel, Morphometry of the human lung, Springer Verlag and Academic Press, Berlin, New York (1963).
E.R. Weibel, The pathway for oxygen, Harvard University Press (1984).
E.R. Weibel, Design and morphometry of the pulmonary gas exchanger, in The lung: scientific foundations, 2nd edition, edited by R.G. Crystal, J.B. West, E.R. Weibel, P.J. Barnes. Lippincott-Raven Press, Philadelphia 1 (1997) 1147–1157.
Weibel, E.R., Sapoval, B. and Filoche, M., Design of peripheral airways for efficient gas exchange. Resp. Phys. Neur. 148 (2005) 321. Google ScholarPubMed
Weibel, E.R., How does lung structure affect gas exchange? Chest 83 (1983) 657665. Google ScholarPubMed
J.B. West, Respiratory physiology: the essentials, Baltimore: Williams and Wilkins (1974).
Whiteley, J.P., Gavaghan, D.J. and Hahn, C.E., Some factors affecting oxygen uptake by red blood cells in the pulmonary capillaries. Math. Biosci. 169 (2001) 153172. Google ScholarPubMed