Skip to main content Accessibility help

We use cookies to distinguish you from other users and to provide you with a better experience on our websites. Close this message to accept cookies or find out how to manage your cookie settings.

Close cookie message
×
Hostname: page-component-848d4c4894-ttngx Total loading time: 0 Render date: 2024-05-31T21:24:40.748Z Has data issue: false hasContentIssue false

Chapter 13 - Alveolarization into Adulthood

Published online by Cambridge University Press:  05 April 2016

By
Manjith Narayanan
Edited by
Alan H. Jobe ,
Jeffrey A. Whitsett  and
Steven H. Abman
Alan H. Jobe
Affiliation:
University of Cincinnati
Jeffrey A. Whitsett
Affiliation:
Cincinnati Children’s Hospital
Steven H. Abman
Affiliation:
University of Colorado School of Medicine
Get access

Summary

Abstract

Alveolarization has been traditionally thought to be complete in the human lung by three to seven years of age. These estimates were based on traditional morphologic measurements from autopsy specimens. Recently new techniques have been used to estimate airway dimensions and alveolar size and numbers with aerosol deposition and hyperpolarized helium in living subjects. hyperpolarized helium measurements by magnetic resonance demonstrated increases in alveolar numbers until adulthood, a result that changes concepts about lung growth. Further, this technology applied to school-age children who had been premature infants with bronchopulmonary dysplasia demonstrated catch-up alveolarization. Application of new imaging technologies to different patient groups will likely change concepts about how the lung grows, repairs, and remodels with age.

Type
Chapter
Information
Fetal and Neonatal Lung Development
Clinical Correlates and Technologies for the Future
 , pp. 238 - 252
Publisher: Cambridge University Press
Print publication year: 2016

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

Mead, J. The lung's “quiet zone.” N Engl J Med. 1970 Jun 4;282(23):1318–1319.CrossRefGoogle ScholarPubMed
Hsia, CC, Hyde, DM, Ochs, M, Weibel, ER. ATS/ERS Joint Task Force on Quantitative Assessment of Lung Structure. An official research policy statement of the American Thoracic Society/European Respiratory Society: standards for quantitative assessment of lung structure. Am J Respir Crit Care Med. 2010 Feb 15;181(4):394–418.CrossRefGoogle ScholarPubMed
Calverley, PM, Walker, P. Chronic obstructive pulmonary disease. Lancet. 2003 Sep 27;362(9389):1053–1061.CrossRefGoogle ScholarPubMed
Gelfand, EW, Kraft, M. The importance and features of the distal airways in children and adults. J Allergy Clin Immunol. 2009 Dec;124(6 Suppl):S84–87.CrossRefGoogle ScholarPubMed
Tiddens, HA, Donaldson, SH, Rosenfeld, M, Pare, PD. Cystic fibrosis lung disease starts in the small airways: can we treat it more effectively? Pediatr Pulmonol. 2010 Feb;45(2):107–117.CrossRefGoogle ScholarPubMed
Baraldi, E, Filippone, M. Chronic lung disease after premature birth. N Engl J Med. 2007 Nov 8;357(19):1946–1955.CrossRefGoogle ScholarPubMed
IJsselstijn, H, Tibboel, D. The lungs in congenital diaphragmatic hernia: do we understand? Pediatr Pulmonol. 1998;26(3):204–218.3.0.CO;2-K>CrossRefGoogle ScholarPubMed
Svanes, C, Sunyer, J, Plana, E, Dharmage, S, Heinrich, J, Jarvis, D, et al. Early life origins of chronic obstructive pulmonary disease. Thorax. 2010 Jan;65(1):14–20.CrossRefGoogle ScholarPubMed
Weibel, ER, Gomez, DM. A principle for counting tissue structures on random sections. J Appl Physiol. 1962 Mar;17:343–348.CrossRefGoogle ScholarPubMed
Dunnill, MS. Postnatal growth of the lung. Thorax. 1962;17:329–333.CrossRefGoogle Scholar
Thurlbeck, WM. Postnatal human lung growth. Thorax. 1982 Aug;37(8):564–571.CrossRefGoogle ScholarPubMed
Thurlbeck, WM, Angus, GE. Growth and aging of the normal human lung. Chest. 1975 Feb;67(2 Suppl):3S–6S.CrossRefGoogle ScholarPubMed
Zeltner, TB, Burri, PH. The postnatal development and growth of the human lung. II. Morphology-Respir Physiol. 1987 Mar;67(3):269–82. (0034–5687 (Print)).Google ScholarPubMed
Hislop, AA. Airway and blood vessel interaction during lung development. J Anat. 2002 Oct;201(4):325–334.CrossRefGoogle ScholarPubMed
Hyde, DM, Blozis, SA, Avdalovic, MV, et al. Alveoli increase in number but not size from birth to adulthood in rhesus monkeys. Am J Physiol Lung Cell Mol Physiol. 2007 Sep;293(3):L570–579.CrossRefGoogle Scholar
Kovar, J, Sly, PD, Willet, KE. Postnatal alveolar development of the rabbit. J Appl Physiol. 2002 Aug;93(2):629–635.CrossRefGoogle ScholarPubMed
Mayo, JR, Hayden, ME. Hyperpolarized helium 3 diffusion imaging of the lung. Radiology. 2002 Jan;222(1):8–11.CrossRefGoogle ScholarPubMed
Saam, BT, Yablonskiy, DA, Kodibagkar, VD, et al. MR imaging of diffusion of (3)He gas in healthy and diseased lungs. Magn Reson Med. 2000 Aug;44(2):174–179.3.0.CO;2-4>CrossRefGoogle ScholarPubMed
Weibel, ER. Morphometry of the Human Lung. Berlin: Springer; 1963.CrossRefGoogle Scholar
Weibel, ER, Gomez, DM. Architecture of the human lung. Use of quantitative methods establishes fundamental relations between size and number of lung structures. Science. 1962 Aug 24;137:577–585.CrossRefGoogle ScholarPubMed
Davies, G, Reid, L. Growth of the alveoli and pulmonary arteries in childhood. Thorax. 1970 Nov;25(6):669–681.CrossRefGoogle ScholarPubMed
Angus, GE, Thurlbeck, WM. Number of alveoli in the human lung. J Appl Physiol. 1972 Apr;32(4):483–485.CrossRefGoogle ScholarPubMed
Hislop, AA, Wigglesworth, JS, Desai, R. Alveolar development in the human fetus and infant. Early Hum Dev. 1986 Feb;13(1):1–11.CrossRefGoogle ScholarPubMed
Burri, PH. Structural aspects of prenatal and postnatal development and growth of the lung. In: McDonald, J, ed. Lung Growth and Development. New York: Marcel Dekker; 1997:1–35.Google Scholar
Weibel, ER, Hsia, CC, Ochs, M. How much is there really? Why stereology is essential in lung morphometry. J Appl Physiol. 2007 Jan;102(1):459–467.CrossRefGoogle ScholarPubMed
Weibel, ER. Morphological quantitation of emphysema: a debate. J Appl Physiol (1985). 2006 Apr;100(4):1419–1420; author reply 1420–1421.CrossRefGoogle ScholarPubMed
Mitzner, W. Morphologic quantification of heterogeneous parenchyma. J Appl Physiol (1985). 2006 Apr;100(4):1421–1422.Google ScholarPubMed
Hsia, CC. Morphological quantitation of emphysema: a debate. J Appl Physiol (1985). 2006 Apr;100(4):1422–1423.Google ScholarPubMed
Fehrenbach, H. Morphological quantitation of emphysema: a debate. J Appl Physiol (1985). 2006 Apr;100(4):1423–1424.Google ScholarPubMed
Butler, JP. Morphological quantitation of emphysema: a debate. J Appl Physiol (1985). 2006 Apr;100(4):1424–1425.Google ScholarPubMed
Bachofen, M, Bachofen, H. Fixation of human lungs. In: Gil, J, ed. Models of Lung Disease: Microscopy and Structural Methods. New York: Marcel Dekker; 1990:23–36.Google Scholar
Hyde, DM, Tyler, NK, Plopper, CG. Morphometry of the respiratory tract: avoiding the sampling, size, orientation, and reference traps. Toxicol Pathol. 2007;35(1):41–48. (0192–6233 (Print)).CrossRefGoogle ScholarPubMed
Hyde, DM, Harkema, JR, Tyler, NK, et al. Design-based sampling and quantitation of the respiratory airways. Toxicol Pathol. 2006;34(3):286–295.CrossRefGoogle ScholarPubMed
Sterio, DC. The unbiased estimation of number and sizes of arbitrary particles using the disector. J Microsc. 1984 May;134(Pt 2):127–136.CrossRefGoogle ScholarPubMed
Mayhew, TM, Gundersen, HJ. “If you assume, you can make an ass out of u and me”: a decade of the disector for stereological counting of particles in 3D space. J Anat. 1996 Feb;188(Pt 1):1–15.Google Scholar
Kato, Y, Takaki, R, Toriwaki, J, eds. Stereology of arbitrarily shaped particles: unbiased estimation of number and sizes. In: Science on Form: Proceedings of the First International Symposium for Science on Form. Tokyo: KTK Scientific Publishers; 1986.Google Scholar
Hyde, DM, Tyler, NK, Putney, LF, Singh, P, Gundersen, HJ. Total number and mean size of alveoli in mammalian lung estimated using fractionator sampling and unbiased estimates of the Euler characteristic of alveolar openings. Anat Rec A Discov Mol Cell Evol Biol. 2004 Mar;277(1):216–26.Google ScholarPubMed
Ochs, M, Nyengaard, JR, Jung, A, et al. The number of alveoli in the human lung. Am J Respir Crit Care Med. 2004 Jan 1;169(1):120–124.CrossRefGoogle ScholarPubMed
Goodson, BM. Nuclear magnetic resonance of laser-polarized noble gases in molecules, materials, and organisms. J Magn Reson. 2002 Apr;155(2):157–216.CrossRefGoogle ScholarPubMed
Hornak, JP. The Basics of MRI. Available at: http://www.cis.rit.edu/htbooks/mri/. Accessed July 1, 2014.Google Scholar
Golman, K, Olsson, LE, Axelsson, O, Mansson, S, Karlsson, M, Petersson, JS. Molecular imaging using hyperpolarized 13C. Br J Radiol. 2003;76(Spec No 2):S118–127.CrossRefGoogle ScholarPubMed
Swift, AJ, Wild, JM, Fichele, S, et al. Emphysematous changes and normal variation in smokers and COPD patients using diffusion 3He MRI. Eur J Radiol. 2005 Jun;54(3):352–358.CrossRefGoogle Scholar
Salerno, M, de Lange, EE, Altes, TA, Truwit, JD, Brookeman, JR, Mugler, JP III. Emphysema: hyperpolarized helium 3 diffusion MR imaging of the lungs compared with spirometric indexes–initial experience. Radiology. 2002 Jan;222(1):252–260.CrossRefGoogle ScholarPubMed
Fain, SB, Panth, SR, Evans, MD, et al. Early emphysematous changes in asymptomatic smokers: detection with 3He MR imaging. Radiology. 2006 Jun;239(3):875–883.CrossRefGoogle ScholarPubMed
Chen, XJ, Hedlund, LW, Moller, HE, Chawla, MS, Maronpot, RR, Johnson, GA. Detection of emphysema in rat lungs by using magnetic resonance measurements of 3He diffusion. Proc Natl Acad Sci U S A. 2000 Oct 10;97(21):11478–11481.CrossRefGoogle ScholarPubMed
Peces-Barba, G, Ruiz-Cabello, J, Cremillieux, Y, et al. Helium-3 MRI diffusion coefficient: correlation to morphometry in a model of mild emphysema. Eur Respir J. 2003 Jul;22(1):14–19.CrossRefGoogle Scholar
Mata, JF, Altes, TA, Cai, J, et al. Evaluation of emphysema severity and progression in a rabbit model: comparison of hyperpolarized 3He and 129Xe diffusion MRI with lung morphometry. J Appl Physiol. 2007 Mar;102(3):1273–1280.CrossRefGoogle Scholar
Woods, JC, Choong, CK, Yablonskiy, DA, et al. Hyperpolarized 3He diffusion MRI and histology in pulmonary emphysema. Magn Reson Med. 2006 Dec;56(6):1293–1300.CrossRefGoogle ScholarPubMed
Yablonskiy, DA, Sukstanskii, AL, Leawoods, JC, et al. Quantitative in vivo assessment of lung microstructure at the alveolar level with hyperpolarized 3He diffusion MRI. Proc Natl Acad Sci U S A. 2002 Mar 5;99(5):3111–3116.CrossRefGoogle ScholarPubMed
Yablonskiy, DA, Sukstanskii, AL, Woods, JC, et al. Quantification of lung microstructure with hyperpolarized 3He diffusion MRI. J Appl Physiol. 2009 Oct;107(4):1258–1265.CrossRefGoogle ScholarPubMed
Jacob, RE, Minard, KR, Laicher, G, Timchalk, C. 3D 3He diffusion MRI as a local in vivo morphometric tool to evaluate emphysematous rat lungs. J Appl Physiol (1985). 2008 Oct;105(4):1291–1300.CrossRefGoogle ScholarPubMed
Shanbhag, DD, Altes, TA, Miller, GW, Mata, JF, Knight-Scott, J. q-Space analysis of lung morphometry in vivo with hyperpolarized 3He spectroscopy. J Magn Reson Imaging. 2006 Jul;24(1):84–94.CrossRefGoogle ScholarPubMed
Heyder, J. Charting human thoracic airways by aerosols. Clin Phys Physiol Meas. 1983 Feb;4(1):29–37.CrossRefGoogle ScholarPubMed
Brand, P, Rieger, C, Beinert, T, Heyder, J. Aerosol derived airway morphometry in healthy subjects. Eur Respir J. 1995 Oct;8(10):1639–1646.CrossRefGoogle ScholarPubMed
Zeman, KL, Bennett, WD. Measuring alveolar dimensions at total lung capacity by aerosol-derived airway morphometry. J Aerosol Med. 1995 Summer;8(2):135–147.CrossRefGoogle ScholarPubMed
Blanchard, JD, Heyder, J, O'Donnell, CR, Brain, JD. Aerosol-derived lung morphometry: comparisons with a lung model and lung function indexes. J Appl Physiol (1985). 1991 Oct;71(4):1216–1224.CrossRefGoogle ScholarPubMed
Nikiforov, AI, Lippmann, M, Palmes, ED. Validation of an in vivo Aerosol Probe Technique by measurements of deposition and morphometry in excised human lungs. Ann Occup Hyg. 1988;32(inhaled particles VI):33–39.Google Scholar
Horsfield, K. Diameters, generations, and orders of branches in the bronchial tree. J Appl Physiol (1985). 1990 Feb;68(2):457–461.CrossRefGoogle ScholarPubMed
Parker, H, Horsfield, K, Cumming, G. Morphology of distal airways in the human lung. J Appl Physiol. 1971 Sep;31(3):386–391.CrossRefGoogle ScholarPubMed
Horsfield, K, Cumming, G. Functional consequences of airway morphology. J Appl Physiol. 1968 Mar;24(3):384–390.CrossRefGoogle ScholarPubMed
Tsuda, A, Henry, FS, Butler, JP. Gas and aerosol mixing in the acinus. Respir Physiol Neurobiol. 2008 Nov 30;163(1–3):139–149.CrossRefGoogle ScholarPubMed
Fichele, S, Paley, MN, Woodhouse, N, Griffiths, PD, van Beek, EJ, Wild, JM. Measurements and modeling of long range 3He diffusion in the lung using a “slice-washout” method. J Magn Reson. 2005 May;174(1):28–33.CrossRefGoogle ScholarPubMed
Altes, TA, Mata, J, de Lange, EE, Brookeman, JR, Mugler, JP III. Assessment of lung development using hyperpolarized helium-3 diffusion MR imaging. J Magn Reson Imaging. 2006 Dec;24(6):1277–1283.CrossRefGoogle ScholarPubMed
Zeman, KL, Bennett, WD. Growth of the small airways and alveoli from childhood to the adult lung measured by aerosol-derived airway morphometry. J Appl Physiol. 2006 Mar;100(3):965–971.CrossRefGoogle Scholar
Cotton, DJ, Graham, BL. Single-breath carbon monoxide diffusing capacity or transfer factor. In: Hamid, Q, Shannon, J, Martin, J, eds. Physiologic Basis of Respiratory Disease. Hamilton, Canada: BC Decker Inc.; 2005:659–669.Google Scholar
Hakulinen, AL, Jarvenpaa, AL, Turpeinen, M, Sovijarvi, A. Diffusing capacity of the lung in school-aged children born very preterm, with and without bronchopulmonary dysplasia. Pediatr Pulmonol. 1996 Jun;21(6):353–360.3.0.CO;2-M>CrossRefGoogle ScholarPubMed
Vrijlandt, EJ, Gerritsen, J, Boezen, HM, Grevink, RG, Duiverman, EJ. Lung function and exercise capacity in young adults born prematurely. Am J Respir Crit Care Med. 2006 Apr 15;173(8):890–896.CrossRefGoogle ScholarPubMed
Balinotti, JE, Chakr, VC, Tiller, C, et al. Growth of lung parenchyma in infants and toddlers with chronic lung disease of infancy. Am J Respir Crit Care Med. 2010 May 15;181(10):1093–1097.CrossRefGoogle ScholarPubMed
Colebatch, HJ, Greaves, IA. Exponential analysis of lung elastic behavior. Am Rev Respir Dis. 1980 May;121(5):898–899.Google ScholarPubMed
Haber, PS, Colebatch, HJ, Ng, CK, et al. Alveolar size as a determinant of pulmonary distensibility in mammalian lungs. J Appl Physiol. 1983 Mar;54(3):837–845.Google Scholar
Greaves, IA, Colebatch, HJ. Elastic behavior and structure of normal and emphysematous lungs post mortem. Am Rev Respir Dis. 1980 Jan;121(1):127–136.Google ScholarPubMed
Hsia, CC, Herazo, LF, Fryder-Doffey, F, Weibel, ER. Compensatory lung growth occurs in adult dogs after right pneumonectomy. J Clin Invest. 1994 Jul;94(1):405–412.CrossRefGoogle ScholarPubMed
Fehrenbach, H, Voswinckel, R, Michl, V, et al. Neoalveolarisation contributes to compensatory lung growth following pneumonectomy in mice. Eur Respir J. 2008 Mar;31(3):515–522.CrossRefGoogle ScholarPubMed
Karlinsky, JB, Goldstein, RH, Ojserkis, B, Snider, GL. Lung mechanics and connective tissue levels in starvation-induced emphysema in hamsters. Am J Physiol. 1986 Aug;251(2 Pt 2):R282–288.Google ScholarPubMed
Massaro, D, Massaro, GD, Baras, A, Hoffman, EP, Clerch, LB. Calorie-related rapid onset of alveolar loss, regeneration, and changes in mouse lung gene expression. Am J Physiol Lung Cell Mol Physiol. 2004 May;286(5):L896–906.CrossRefGoogle ScholarPubMed
Massaro, GD, Massaro, D. Formation of alveoli in rats: postnatal effect of prenatal dexamethasone. Am J Physiol. 1992 Jul;263(1 Pt 1):L37–41.Google ScholarPubMed
Schittny, JC, Mund, SI, Stampanoni, M. Evidence and structural mechanism for late lung alveolarization. Am J Physiol Lung Cell Mol Physiol. 2008 Feb;294(2):L246–254.CrossRefGoogle ScholarPubMed
Narayanan, M, Owers-Bradley, J, Beardsmore, CS, et al. Alveolarization continues during childhood and adolescence: new evidence from helium-3 magnetic resonance. Am J Respir Crit Care Med. 2012 Jan 15;185(2):186–191.CrossRefGoogle ScholarPubMed
Butler, JP, Loring, SH, Patz, S, Tsuda, A, Yablonskiy, DA, Mentzer, SJ. Evidence for adult lung growth in humans. N Engl J Med. 2012 Jul 19;367(3):244–247.CrossRefGoogle ScholarPubMed
Bonikos, DS, Bensch, KG, Northway, WH Jr, Edwards, DK. Bronchopulmonary dysplasia: the pulmonary pathologic sequel of necrotizing bronchiolitis and pulmonary fibrosis. Hum Pathol. 1976 Nov;7(6):643–666.CrossRefGoogle ScholarPubMed
Husain, AN, Siddiqui, NH, Stocker, JT. Pathology of arrested acinar development in postsurfactant bronchopulmonary dysplasia. Hum Pathol. 1998 Jul;29(7):710–717.CrossRefGoogle ScholarPubMed
Sobonya, RE, Logvinoff, MM, Taussig, LM, Theriault, A. Morphometric analysis of the lung in prolonged bronchopulmonary dysplasia. Pediatr Res. 1982 Nov;16(11):969–972.CrossRefGoogle ScholarPubMed
Hislop, AA, Wigglesworth, JS, Desai, R, Aber, V. The effects of preterm delivery and mechanical ventilation on human lung growth. Early Hum Dev. 1987 May;15(3):147–164.CrossRefGoogle ScholarPubMed
Coalson, JJ, Winter, VT, Siler-Khodr, T, Yoder, BA. Neonatal chronic lung disease in extremely immature baboons. Am J Respir Crit Care Med. 1999 Oct;160(4):1333–1346.CrossRefGoogle ScholarPubMed
Eber, E, Zach, MS. Long term sequelae of bronchopulmonary dysplasia (chronic lung disease of infancy). Thorax. 2001 Apr;56(4):317–323.CrossRefGoogle ScholarPubMed
Coalson, JJ, Winter, VT, Gerstmann, DR, Idell, S, King, RJ, Delemos, RA. Pathophysiologic, morphometric, and biochemical studies of the premature baboon with bronchopulmonary dysplasia. Am Rev Respir Dis. 1992 Apr;145(4 Pt 1):872–881.CrossRefGoogle ScholarPubMed
Coalson, JJ, Winter, V, deLemos, RA. Decreased alveolarization in baboon survivors with bronchopulmonary dysplasia. Am J Respir Crit Care Med. 1995 Aug;152(2):640–646.CrossRefGoogle ScholarPubMed
Narayanan, M, Beardsmore, CS, Owers-Bradley, J, et al. Catch-up alveolarization in ex-preterm children: evidence from (3)He magnetic resonance. Am J Respir Crit Care Med. 2013 May 15;187(10):1104–1109.CrossRefGoogle ScholarPubMed
Jobe, AH. Good news for lung repair in preterm infants. Am J Respir Crit Care Med. 2013 May 15;187(10):1043–1044.CrossRefGoogle ScholarPubMed
Burri, PH. Structural aspects of postnatal lung development-alveolar formation and growth. Biol Neonate. 2006;89(4):313–322.CrossRefGoogle ScholarPubMed
Massaro, D, Massaro, GD. Invited Review: pulmonary alveoli: formation, the “call for oxygen,” and other regulators. Am J Physiol Lung Cell Mol Physiol. 2002 Mar;282(3):L345–358.CrossRefGoogle ScholarPubMed
Tenney, SM, Remmers, JE. Comparative quantitative morphology of the mammalian lung: diffusing area. Nature. 1963 Jan 5;197:54–56.CrossRefGoogle ScholarPubMed
Sapoval, B, Filoche, M, Weibel, ER. Smaller is better–but not too small: a physical scale for the design of the mammalian pulmonary acinus. Proc Natl Acad Sci U S A. 2002 Aug 6;99(16):10411–10416.CrossRefGoogle ScholarPubMed
Massaro, GD, Radaeva, S, Clerch, LB, Massaro, D. Lung alveoli: endogenous programmed destruction and regeneration. Am J Physiol Lung Cell Mol Physiol. 2002 Aug;283(2):L305–309.CrossRefGoogle ScholarPubMed
Coxson, HO, Chan, IH, Mayo, JR, Hlynsky, J, Nakano, Y, Birmingham, CL. Early emphysema in patients with anorexia nervosa. Am J Respir Crit Care Med. 2004 Oct 1;170(7):748–752.CrossRefGoogle ScholarPubMed
Massaro, D, Massaro, GD. Hunger disease and pulmonary alveoli. Am J Respir Crit Care Med. 2004 Oct 1;170(7):723–724.CrossRefGoogle ScholarPubMed
Gillooly, M, Lamb, D. Airspace size in lungs of lifelong non-smokers: effect of age and sex. Thorax. 1993 Jan;48(1):39–43.CrossRefGoogle ScholarPubMed
Waters, B, Owers-Bradley, J, Silverman, M. Acinar structure in symptom-free adults by Helium-3 magnetic resonance. Am J Respir Crit Care Med. 2006 Apr 15;173(8):847–851.CrossRefGoogle ScholarPubMed
Armour, J, Donnelly, PM, Bye, PT. The large lungs of elite swimmers: an increased alveolar number? Eur Respir J. 1993 Feb;6(2):237–247.CrossRefGoogle ScholarPubMed
Narang, I, Bush, A, Rosenthal, M. Gas transfer and pulmonary blood flow at rest and during exercise in adults 21 years after preterm birth. Am J Respir Crit Care Med. 2009 Aug 15;180(4):339–345.CrossRefGoogle ScholarPubMed

Save book to Kindle

To save this book to your Kindle, first ensure coreplatform@cambridge.org is added to your Approved Personal Document E-mail List under your Personal Document Settings on the Manage Your Content and Devices page of your Amazon account. Then enter the ‘name’ part of your Kindle email address below. Find out more about saving to your Kindle.

Note you can select to save to either the @free.kindle.com or @kindle.com variations. ‘@free.kindle.com’ emails are free but can only be saved to your device when it is connected to wi-fi. ‘@kindle.com’ emails can be delivered even when you are not connected to wi-fi, but note that service fees apply.

Find out more about the Kindle Personal Document Service.

Available formats
×

Save book to Dropbox

To save content items to your account, please confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your account. Find out more about saving content to Dropbox.

Available formats
×

Save book to Google Drive

To save content items to your account, please confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your account. Find out more about saving content to Google Drive.

Available formats
×