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Biomechanics of the Aging Lung Parenchyma

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Book cover Mechanical Properties of Aging Soft Tissues

Part of the book series: Engineering Materials and Processes ((EMP))

Abstract

Aging is a process that affects cells, the extracellular matrix (ECM), tissues, and organs. The lung is the entry of oxygen into the body and any deterioration in its ability to take up and distribute oxygen uniformly in the parenchyma compromises the cardiovascular system and hence contributes to the aging of the organism. In this chapter, we provide an overview of the biochemical, structural, and biomechanical properties of the aging lung parenchyma. We also discuss several measurement techniques that are suitable to assess the biomechanical properties of the lung. Following a review of general constitutive relations used in lung biomechanics, we derive a specific multiscale constitutive equation for the lung tissue strip that allows us to partition the contributions of collagen, elastin, their volume fraction, and their interaction with the proteoglycan matrix. This model provides a better understanding of how airspace enlargement, local stiffening of ECM fibers and macroscopic lung compliance are related to each other. These constitutive relations have important implications for lung function during aging. Specifically, there is an increase in ECM stiffness due to cross-linking of collagen which influences cellular behavior at the microscale. Despite ECM stiffening, at the scale of thousands of alveoli , parenchymal stiffness may be near normal and lung compliance may even increase in the elderly due to the enlargement alveoli enabling relatively normal gas exchange in the absence of exercise . Finally, we discuss possible new research directions that may help better understand and reduce the risk of pulmonary diseases of old age.

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References

  1. Al Jamal R, Roughley PJ, Ludwig MS (2001) Effect of glycosaminoglycan degradation on lung tissue viscoelasticity. Am J Physiol Lung Cell Mol Physiol 280:L306–L315

    Google Scholar 

  2. Andreotti L, Bussotti A, Cammelli D, Aiello E, Sampognaro S (1983) Connective tissue in aging lung. Gerontology 29:377–387

    Article  Google Scholar 

  3. Antunes MA, Abreu SC, Damaceno-Rodrigues NR, Parra ER, Capelozzi VL, Pinart M, Romero PV, Silva PM, Martins MA, Rocco PR (2009) Different strains of mice present distinct lung tissue mechanics and extracellular matrix composition in a model of chronic allergic asthma. Respir Physiol Neurobiol 165:202–207

    Article  Google Scholar 

  4. Astrand I, Astrand PO, Hallback I, Kilbom A (1973) Reduction in maximal oxygen uptake with age. J Appl Physiol 35:649–654

    Google Scholar 

  5. Avery ME, Mead J (1959) Surface properties in relation to atelectasis and hyaline membrane disease. AMA J Dis Child 97:517–523

    Google Scholar 

  6. Avery NC, Bailey AJ (2005) Enzymic and non-enzymic cross-linking mechanisms in relation to turnover of collagen: relevance to aging and exercise. Scand J Med Sci Sports 15:231–240

    Article  Google Scholar 

  7. Bachofen H, Hildebrandt J, Bachofen M (1970) Pressure-volume curves of air- and liquid-filled excised lungs-surface tension in situ. J Appl Physiol 29:422–431

    Google Scholar 

  8. Bader H (1967) Dependence of wall stress in the human thoracic aorta on age and pressure. Circ Res 20:354–361

    Article  Google Scholar 

  9. Balestrini JL, Chaudhry S, Sarrazy V, Koehler A, Hinz B (2012) The mechanical memory of lung myofibroblasts. Integr Biol Quant Biosci Nano Macro 4:410–421

    Google Scholar 

  10. Barcus CE, Keely PJ, Eliceiri KW, Schuler LA (2013) Stiff collagen matrices increase tumorigenic prolactin signaling in breast cancer cells. J Biol Chem 288:12722–12732

    Article  Google Scholar 

  11. Barnas GM, Stamenovic D, Fredberg JJ (1991) Proportionality between chest wall resistance and elastance. J Appl Physiol 70:511–515

    Article  Google Scholar 

  12. Bartynski WS, Heller MT, Grahovac SZ, Rothfus WE, Kurs-Lasky M (2005) Severe thoracic kyphosis in the older patient in the absence of vertebral fracture: association of extreme curve with age. AJNR Am J Neuroradiol 26:2077–2085

    Google Scholar 

  13. Bates JH (2007) A recruitment model of quasi-linear power-law stress adaptation in lung tissue. Ann Biomed Eng 35:1165–1174

    Article  Google Scholar 

  14. Bates JH, Irvin CG, Farre R, Hantos Z (2011) Oscillation mechanics of the respiratory system. Compr Physiol 1:1233–1272

    Google Scholar 

  15. Bates JH, Maksym GN, Navajas D, Suki B (1994) Lung tissue rheology and 1/f noise. Ann Biomed Eng 22:674–681

    Article  Google Scholar 

  16. Bellingham CM, Woodhouse KA, Robson P, Rothstein SJ, Keeley FW (2001) Self-aggregation characteristics of recombinantly expressed human elastin polypeptides. Biochim Biophys Acta 1550:6–19

    Article  Google Scholar 

  17. Bellmunt MJ, Portero M, Pamplona R, Cosso L, Odetti P, Prat J (1995) Evidence for the Maillard reaction in rat lung collagen and its relationship with solubility and age. Biochim Biophys Acta 1272:53–60

    Article  Google Scholar 

  18. Bellmunt MJ, Portero M, Pamplona R, Muntaner M, Prat J (1995) Age-related fluorescence in rat lung collagen. Lung 173:177–185

    Article  Google Scholar 

  19. Bihari-Varga M, Kadar A, Jacob MP, Robert L (1986) Physicochemical and ultrastructural properties of cholesterol esters bound to elastin. Conn Tissue Res 15:43–55

    Article  Google Scholar 

  20. Bradley KH, McConnell SD, Crystal RG (1974) Lung collagen composition and synthesis. Characterization and changes with age. J Biol Chem 249:2674–2683

    Google Scholar 

  21. Brewer KK, Sakai H, Alencar AM, Majumdar A, Arold SP, Lutchen KR, Ingenito EP, Suki B (2003) Lung and alveolar wall elastic and hysteretic behavior in rats: effects of in vivo elastase treatment. J Appl Physiol 95:1926–1936

    Google Scholar 

  22. Briscoe AM, Loring WE, Mc CJ (1959) Changes in human lung collagen and lipids with age. Proc Soci Exp Biol Med Soci Exp Biol Med 102:71–74

    Article  Google Scholar 

  23. Buckwalter JA, Rosenberg LC (1982) Electron microscopic studies of cartilage proteoglycans. Direct evidence for the variable length of the chondroitin sulfate-rich region of proteoglycan subunit core protein. J Biol Chem 257:9830–9839

    Google Scholar 

  24. Burtscher M (2013) Exercise limitations by the oxygen delivery and utilization systems in aging and disease: coordinated adaptation and deadaptation of the lung-heart muscle axis—a mini-review. Gerontology 59:289–296

    Article  Google Scholar 

  25. Calderwood SK, Murshid A, Prince T (2009) The shock of aging: molecular chaperones and the heat shock response in longevity and aging–a mini-review. Gerontology 55:550–558

    Article  Google Scholar 

  26. Campagnone R, Regan J, Rich CB, Miller M, Keene DR, Sakai L, Foster JA (1987) Pulmonary fibroblasts: a model system for studying elastin synthesis. Lab Invest 56:224–230

    Google Scholar 

  27. Cavalcante FS, Ito S, Brewer KK, Sakai H, Alencar AM, Almeida MP, Andrade JS Jr, Majumdar A, Ingenito EP, Suki B (2005) Mechanical interactions between collagen and proteoglycans: implications for the stability of lung tissue. J Appl Physiol 98:672–679

    Article  Google Scholar 

  28. Cerami A (1985) Hypothesis. Glucose as a mediator of aging. J Am Geriatr Soc 33:626–634

    Google Scholar 

  29. Chio KS, Tappel AL (1969) Synthesis and characterization of the fluorescent products derived from malonaldehyde and amino acids. Biochemistry 8:2821–2826

    Article  Google Scholar 

  30. Clercx C, Venker-van Haagen AJ, den Breejen JN, Haagsman HP, van den Brom WE, de Vries HW, van Golde LM (1989) Effects of age and breed on the phospholipid composition of canine surfactant. Lung 167:351–357

    Google Scholar 

  31. Cohn JE, Donoso HD (1963) Mechanical properties of lung in normal men over 60 years old. J Clin Investig 42:1406–1410

    Article  Google Scholar 

  32. Copley SJ, Wells AU, Hawtin KE, Gibson DJ, Hodson JM, Jacques AE, Hansell DM (2009) Lung morphology in the elderly: comparative CT study of subjects over 75 years old versus those under 55 years old. Radiology 251:566–573

    Article  Google Scholar 

  33. Crandall SH (1970) The role of damping in vibration theory. J Sound Vibr 11:3–18

    Article  MATH  Google Scholar 

  34. Crystal RG (1974) Lung collagen: definition, diversity and development. Fed Proc 33:2248–2255

    Google Scholar 

  35. Culham EG, Jimenez HA, King CE (1994) Thoracic kyphosis, rib mobility, and lung volumes in normal women and women with osteoporosis. Spine 19:1250–1255

    Article  Google Scholar 

  36. D’Errico A, Scarani P, Colosimo E, Spina M, Grigioni WF, Mancini AM (1989) Changes in the alveolar connective tissue of the ageing lung. An immunohistochemical study. Virchows Arch A Patholo Anat Histopathol 415:137–144

    Article  Google Scholar 

  37. Denny E, Schroter RC (1995) The mechanical behavior of a mammalian lung alveolar duct model. J Biomech Eng 117:254–261

    Article  Google Scholar 

  38. Denny E, Schroter RC (1997) Relationships between alveolar size and fibre distribution in a mammalian lung alveolar duct model. J Biomech Eng 119:289–297

    Article  Google Scholar 

  39. Denny E, Schroter RC (2000) Viscoelastic behavior of a lung alveolar duct model. J Biomech Eng 122:143–151

    Article  Google Scholar 

  40. Denny E, Schroter RC (2006) A model of non-uniform lung parenchyma distortion. J Biomech 39:652–663

    Article  Google Scholar 

  41. Desler C, Hansen TL, Frederiksen JB, Marcker ML, Singh KK, Juel Rasmussen L (2012) Is there a link between mitochondrial reserve respiratory capacity and aging? J Aging Res 2012:192503

    Google Scholar 

  42. Dewey TG (1997) Fractals in molecular biophysics. Oxford University Press, Oxford

    MATH  Google Scholar 

  43. Dolhnikoff M, Mauad T, Ludwig MS (1999) Extracellular matrix and oscillatory mechanics of rat lung parenchyma in bleomycin-induced fibrosis. Am J Respir Crit Care Med 160:1750–1757

    Article  Google Scholar 

  44. Dolhnikoff M, Morin J, Ludwig MS (1998) Human lung parenchyma responds to contractile stimulation. Am J Respir Crit Care Med 158:1607–1612

    Article  Google Scholar 

  45. Ebihara T, Venkatesan N, Tanaka R, Ludwig MS (2000) Changes in extracellular matrix and tissue viscoelasticity in bleomycin-induced lung fibrosis. Temporal aspects. Am J Respir Crit Care Med 162:1569–1576

    Article  Google Scholar 

  46. Eleftheriou CS, Trakas NB, Tzartos SJ (1991) Cellular ageing related proteins secreted by human fibroblasts. Mutat Res 256:127–138

    Article  Google Scholar 

  47. Elliott RJ, McGrath LT (1994) Calcification of the human thoracic aorta during aging. Calcif Tissue Int 54:268–273

    Article  Google Scholar 

  48. Engelhardt M, Martens UM (1998) The implication of telomerase activity and telomere stability for replicative aging and cellular immortality (Review). Oncol Rep 5:1043–1052

    Google Scholar 

  49. Escolar JD, Tejero C, Escolar MA, Montalvo F, Garisa R (1997) Architecture, elastic fiber, and collagen in the distal air portion of the lung of the 18-month-old rat. Anat Rec 248:63–69

    Article  Google Scholar 

  50. Eyre DR, Paz MA, Gallop PM (1984) Cross-linking in collagen and elastin. Annu Rev Biochem 53:717–748

    Article  Google Scholar 

  51. Faffe DS, Silva GH, Kurtz PM, Negri EM, Capelozzi VL, Rocco PR, Zin WA (2001) Lung tissue mechanics and extracellular matrix composition in a murine model of silicosis. J Appl Physiol 90:1400–1406

    Google Scholar 

  52. Foster JA, Curtiss SW (1990) The regulation of lung elastin synthesis. Am J Physiol 259:L13–L23

    Google Scholar 

  53. Frank NR, Mead J, Ferris BG Jr (1957) The mechanical behavior of the lungs in healthy elderly persons. J Clin Investig 36:1680–1687

    Article  Google Scholar 

  54. Fredberg JJ, Bunk D, Ingenito E, Shore SA (1993) Tissue resistance and the contractile state of lung parenchyma. J Appl Physiol 74:1387–1397

    Google Scholar 

  55. Fredberg JJ, Stamenovic D (1989) On the imperfect elasticity of lung tissue. J Appl Physiol 67:2408–2419

    Google Scholar 

  56. Freitas FS, Ibiapina CC, Alvim CG, Britto RR, Parreira VF (2010) Relationship between cough strength and functional level in elderly. Revista brasileira de fisioterapia 14:470–476

    Google Scholar 

  57. Fung YC (1988) A model of the lung structure and its validation. J Appl Physiol 64:2132–2141

    Google Scholar 

  58. Fung YC (1993) Biomechanics: mechanical properties of living tissues, 2nd edn. Springer, New York

    Book  Google Scholar 

  59. Fust A, LeBellego F, Iozzo RV, Roughley PJ, Ludwig MS (2005) Alterations in lung mechanics in decorin-deficient mice. Am J Physiol Lung Cell Mol Physiol 288:L159–L166

    Article  Google Scholar 

  60. Hance AJ, Crystal RG (1975) The connective tissue of lung. Am Rev Respir Dis 112:657–711

    Google Scholar 

  61. Hantos Z, Daroczy B, Suki B, Nagy S, Fredberg JJ (1992) Input impedance and peripheral inhomogeneity of dog lungs. J Appl Physiol 72:168–178

    Article  Google Scholar 

  62. Hantos Z, Suki B, Csendes T, Daroczy B (1987) Constant-phase modelling of pulmonary tissue impedance (Abstract). Bull Eur Physiopathol Respir 23(Suppl. 12):326s

    Google Scholar 

  63. Hildebrandt J (1969) Comparison of mathematical models for cat lung and viscoelastic balloon derived by laplace transform methods from pressure-volume data. Bull Math Biophys 31:651–667

    Article  MATH  Google Scholar 

  64. Hildebrandt J (1969) Dynamic properties of air-filled excised cat lung determined by liquid plethysmograph. J Appl Physiol 27:246–250

    Google Scholar 

  65. Huang K, Mitzner W, Rabold R, Schofield B, Lee H, Biswal S, Tankersley CG (2007) Variation in senescent-dependent lung changes in inbred mouse strains. J Appl Physiol 102:1632–1639

    Article  Google Scholar 

  66. Huang K, Rabold R, Schofield B, Mitzner W, Tankersley CG (2007) Age-dependent changes of airway and lung parenchyma in C57BL/6 J mice. J Appl Physiol 102:200–206

    Article  Google Scholar 

  67. Hukins DWL (1984) Connective tissue matrix. Macmillan, London

    Google Scholar 

  68. Ingenito EP, Mark L, Davison B (1994) Effects of acute lung injury on dynamic tissue properties. J Appl Physiol 77:2689–2697

    Google Scholar 

  69. Ito S, Bartolak-Suki E, Shipley JM, Parameswaran H, Majumdar A, Suki B (2006) Early emphysema in the tight skin and pallid mice: roles of microfibril-associated glycoproteins, collagen, and mechanical forces. Am J Respir Cell Mol Biol 34:688–694

    Article  Google Scholar 

  70. Ito S, Ingenito EP, Arold SP, Parameswaran H, Tgavalekos NT, Lutchen KR, Suki B (2004) Tissue heterogeneity in the mouse lung: effects of elastase treatment. J Appl Physiol 97:204–212

    Article  Google Scholar 

  71. Ito S, Ingenito EP, Brewer KK, Black LD, Parameswaran H, Lutchen KR, Suki B (2005) Mechanics, nonlinearity, and failure strength of lung tissue in a mouse model of emphysema: possible role of collagen remodeling. J Appl Physiol 98:503–511

    Article  Google Scholar 

  72. Ito S, Lutchen KR, Suki B (2007) Effects of heterogeneities on the partitioning of airway and tissue properties in normal mice. J Appl Physiol 102:859–869

    Article  Google Scholar 

  73. Ito S, Majumdar A, Kume H, Shimokata K, Naruse K, Lutchen KR, Stamenovic D, Suki B (2006b) Viscoelastic and dynamic nonlinear properties of airway smooth muscle tissue: roles of mechanical force and the cytoskeleton. Am J Physiol Lung Cell Mol Physiol 290(6):L1227–L1237

    Google Scholar 

  74. Janssens JP, Pache JC, Nicod LP (1999) Physiological changes in respiratory function associated with ageing. Eur Respir J 13:197–205

    Article  Google Scholar 

  75. Jesudason R, Black L, Majumdar A, Stone P, Suki B (2007) Differential effects of static and cyclic stretching during elastase digestion on the mechanical properties of extracellular matrices. J Appl Physiol 103:803–811

    Article  Google Scholar 

  76. John R, Thomas J (1972) Chemical compositions of elastins isolated from aortas and pulmonary tissues of humans of different ages. Biochem J 127:261–269

    Google Scholar 

  77. Khorramizadeh MR, Tredget EE, Telasky C, Shen Q, Ghahary A (1999) Aging differentially modulates the expression of collagen and collagenase in dermal fibroblasts. Mol Cell Biochem 194:99–108

    Article  Google Scholar 

  78. Kielty CM, Sherratt MJ, Shuttleworth CA (2002) Elastic fibres. J Cell Sci 115:2817–2828

    Google Scholar 

  79. Knudson RJ, Clark DF, Kennedy TC, Knudson DE (1977) Effect of aging alone on mechanical properties of the normal adult human lung. J Appl Physiol Respir Environ Exerc Physiol 43:1054–1062

    Google Scholar 

  80. Konno K, Arai H, Motomiya M, Nagai H, Ito M, Sato H, Satoh K (1982) A biochemical study on glycosaminoglycans (mucopolysaccharides) in emphysematous and in aged lungs. Am Rev Respir Dis 126:797–801

    Google Scholar 

  81. Kononov S, Brewer K, Sakai H, Cavalcante FS, Sabayanagam CR, Ingenito EP, Suki B (2001) Roles of mechanical forces and collagen failure in the development of elastase-induced emphysema. Am J Respir Crit Care Med 164:1920–1926

    Article  Google Scholar 

  82. Labat-Robert J, Robert L (1988) Aging of the extracellular matrix and its pathology. Exp Gerontol 23:5–18

    Article  Google Scholar 

  83. Lai-Fook SJ, Hyatt RE (2000) Effects of age on elastic moduli of human lungs. J Appl Physiol 89:163–168

    Google Scholar 

  84. Lanir Y (1983) Constitutive equations for the lung tissue. J Biomech Eng 105:374–380

    Article  Google Scholar 

  85. Lee HC, Wei YH (2001) Mitochondrial alterations, cellular response to oxidative stress and defective degradation of proteins in aging. Biogerontology 2:231–244

    Article  Google Scholar 

  86. Lee HY, Han L, Roughley PJ, Grodzinsky AJ, Ortiz C (2013) Age-related nanostructural and nanomechanical changes of individual human cartilage aggrecan monomers and their glycosaminoglycan side chains. J Struct Biol 181:264–273

    Article  Google Scholar 

  87. Lee KW, Chung SY, Yang I, Lee Y, Ko EY, Park MJ (2000) Correlation of aging and smoking with air trapping at thin-section CT of the lung in asymptomatic subjects. Radiology 214:831–836

    Article  Google Scholar 

  88. Liu F, Tschumperlin DJ (2011) Micro-mechanical characterization of lung tissue using atomic force microscopy. J Vis Exp (54). pii: 2911. doi:10.3791/2911

  89. Luque T, Melo E, Garreta E, Cortiella J, Nichols J, Farre R, Navajas D (2013) Local micromechanical properties of decellularized lung scaffolds measured with atomic force microscopy. Acta Biomater 9:6852–6859

    Article  Google Scholar 

  90. Lutchen KR, Yang K, Kaczka DW, Suki B (1993) Optimal ventilation waveforms for estimating low-frequency respiratory impedance. J Appl Physiol 75:478–488

    Google Scholar 

  91. Mackay EH, Banks J, Sykes B, Lee G (1978) Structural basis for the changing physical properties of human pulmonary vessels with age. Thorax 33:335–344

    Article  Google Scholar 

  92. Magoon MW, Wright JR, Baritussio A, Williams MC, Goerke J, Benson BJ, Hamilton RL, Clements JA (1983) Subfractionation of lung surfactant. Implications for metabolism and surface activity. Biochim Biophys Acta 750:18–31

    Article  Google Scholar 

  93. Maksym GN, Bates JH (1997) A distributed nonlinear model of lung tissue elasticity. J Appl Physiol 82:32–41

    Google Scholar 

  94. Maksym GN, Bates JH (1997) Nonparametric block-structured modeling of rat lung mechanics. Ann Biomed Eng 25:1000–1008

    Article  Google Scholar 

  95. Maksym GN, Kearney RE, Bates JH (1998) Nonparametric block-structured modeling of lung tissue strip mechanics. Ann Biomed Eng 26:242–252

    Article  Google Scholar 

  96. Martin CJ, Chihara S, Chang DB (1977) A comparative study of the mechanical properties in aging alveolar wall. Am Rev Respir Dis 115:981–988

    Google Scholar 

  97. Mays PK, McAnulty RJ, Campa JS, Laurent GJ (1991) Age-related changes in collagen synthesis and degradation in rat tissues. Importance of degradation of newly synthesized collagen in regulating collagen production. Biochem J 276 (Pt 2):307–313

    Google Scholar 

  98. McAnulty RJ, Laurent GJ (1987) Collagen synthesis and degradation in vivo. Evidence for rapid rates of collagen turnover with extensive degradation of newly synthesized collagen in tissues of the adult rat. Collagen Relat Res 7:93–104

    Article  Google Scholar 

  99. Mijailovich SM, Stamenovic D, Brown R, Leith DE, Fredberg JJ (1994) Dynamic moduli of rabbit lung tissue and pigeon ligamentum propatagiale undergoing uniaxial cyclic loading. J Appl Physiol 76:773–782

    Article  Google Scholar 

  100. Mijailovich SM, Stamenovic D, Fredberg JJ (1993) Toward a kinetic theory of connective tissue micromechanics. J Appl Physiol 74:665–681

    Google Scholar 

  101. Mithieux SM, Weiss AS (2005) Elastin. Adv Protein Chem 70:437–461

    Article  Google Scholar 

  102. Miyata T, Ishikawa N, van Ypersele de Strihou C (2003) Carbonyl stress and diabetic complications. Clinical chemistry and laboratory medicine : CCLM/FESCC 41:1150–1158

    Google Scholar 

  103. Moliva JI, Rajaram MV, Sidiki S, Sasindran SJ, Guirado E, Pan XJ, Wang SH, Ross P, Jr., Lafuse WP, Schlesinger LS, Turner J, Torrelles JB (2014) Molecular composition of the alveolar lining fluid in the aging lung. Age 51(1):66–77

    Google Scholar 

  104. Monnier VM (1990) Nonenzymatic glycosylation, the Maillard reaction and the aging process. J Gerontol 45:B105–B111

    Article  Google Scholar 

  105. Moretto A, Dallaire M, Romero P, Ludwig M (1994) Effect of elastase on oscillation mechanics of lung parenchymal strips. J Appl Physiol 77:1623–1629

    Google Scholar 

  106. Navajas D, Maksym GN, Bates JH (1995) Dynamic viscoelastic nonlinearity of lung parenchymal tissue. J Appl Physiol 79:348–356

    Google Scholar 

  107. Niewoehner DE, Kleinerman J (1974) Morphologic basis of pulmonary resistance in the human lung and effects of aging. J Appl Physiol 36:412–418

    Google Scholar 

  108. Noguchi A, Reddy R, Kursar JD, Parks WC, Mecham RP (1989) Smooth muscle isoactin and elastin in fetal bovine lung. Exp Lung Res 15:537–552

    Article  Google Scholar 

  109. Parameswaran H, Majumdar A, Suki B (2011) Linking microscopic spatial patterns of tissue destruction in emphysema to macroscopic decline in stiffness using a 3D computational model. PLoS Comput Biol 7:e1001125

    Article  Google Scholar 

  110. Pierce JA, Hocott JB (1960) Studies on the collagen and elastin content of the human lung. J Clin Investig 39:8–14

    Article  Google Scholar 

  111. Pierce JA, Resnick H, Henry PH (1967) Collagen and elastin metabolism in the lungs, skin, and bones of adult rats. J Lab Clin Med 69:485–493

    Google Scholar 

  112. Pillow JJ, Korfhagen TR, Ikegami M, Sly PD (2001) Overexpression of TGF-alpha increases lung tissue hysteresivity in transgenic mice. J Appl Physiol 91:2730–2734

    Google Scholar 

  113. Polkey MI, Harris ML, Hughes PD, Hamnegard CH, Lyons D, Green M, Moxham J (1997) The contractile properties of the elderly human diaphragm. Am J Respir Crit Care Med 155:1560–1564

    Article  Google Scholar 

  114. Poole A, Myllyla R, Wagner JC, Brown RC (1985) Collagen biosynthesis enzymes in lung tissue and serum of rats with experimental silicosis. Br J Exp Pathol 66:567–575

    Google Scholar 

  115. Prockop DJ, Kivirikko KI, Tuderman L, Guzman NA (1979) The biosynthesis of collagen and its disorders (first of two parts). N Engl J Med 301:13–23

    Article  Google Scholar 

  116. Qiu H, Zhu Y, Sun Z, Trzeciakowski JP, Gansner M, Depre C, Resuello RR, Natividad FF, Hunter WC, Genin GM, Elson EL, Vatner DE, Meininger GA, Vatner SF (2010) Short communication: vascular smooth muscle cell stiffness as a mechanism for increased aortic stiffness with aging. Circ Res 107:615–619

    Article  Google Scholar 

  117. Ranga V, Kleinerman J, Ip MP, Sorensen J (1979) Age-related changes in elastic fibers and elastin of lung. Am Rev Respir Dis 119:369–376

    Google Scholar 

  118. Rebello CM, Jobe AH, Eisele JW, Ikegami M (1996) Alveolar and tissue surfactant pool sizes in humans. Am J Respir Crit Care Med 154:625–628

    Article  Google Scholar 

  119. Reiser KM, Hennessy SM, Last JA (1987) Analysis of age-associated changes in collagen crosslinking in the skin and lung in monkeys and rats. Biochim Biophys Acta 926:339–348

    Article  Google Scholar 

  120. Robert L (1998) Mechanisms of aging of the extracellular matrix: role of the elastin-laminin receptor. Gerontology 44:307–317

    Article  Google Scholar 

  121. Robert L, Robert AM, Fulop T (2008) Rapid increase in human life expectancy: will it soon be limited by the aging of elastin? Biogerontology 9:119–133

    Article  Google Scholar 

  122. Romero FJ, Pastor A, Lopez J, Romero PV (1998) A recruitment-based rheological model for mechanical behavior of soft tissues. Biorheology 35:17–35

    Article  Google Scholar 

  123. Romero PV, Faffe DS, Canete C (2011) Dynamic nonlinearity of lung tissue: frequency dependence and harmonic distortion. J Appl Physiol 111:420–426

    Article  Google Scholar 

  124. Sakai H, Ingenito EP, Mora R, Abbay S, Cavalcante FS, Lutchen KR, Suki B (2001) Hysteresivity of the lung and tissue strip in the normal rat: effects of heterogeneities. J Appl Physiol 91:737–747

    Google Scholar 

  125. Salerno FG, Dallaire M, Ludwig MS (1995) Does the anatomic makeup of parenchymal lung strips affect oscillatory mechanics during induced constriction? J Appl Physiol 79:66–72

    Google Scholar 

  126. Schachtschabel DO, Wever J (1978) Age-related decline in the synthesis of glycosaminoglycans by cultured human fibroblasts (WI-38). Mech Ageing Dev 8:257–264

    Article  Google Scholar 

  127. Schmid K, Grundboeck-Jusco J, Kimura A, Tschopp FA, Zollinger R, Binette JP, Lewis W, Hayashi S (1982) The distribution of the glycosaminoglycans in the anatomic components of the lung and the changes in concentration of these macromolecules during development and aging. Biochim Biophys Acta 716:178–187

    Article  Google Scholar 

  128. Scott JE (1992) Supramolecular organization of extracellular matrix glycosaminoglycans, in vitro and in the tissues. Faseb J 6:2639–2645

    Google Scholar 

  129. Seyer JM, Hutcheson ET, Kang AH (1976) Collagen polymorphism in idiopathic chronic pulmonary fibrosis. J Clin Investig 57:1498–1507

    Article  Google Scholar 

  130. Shapiro SD, Endicott SK, Province MA, Pierce JA, Campbell EJ (1991) Marked longevity of human lung parenchymal elastic fibers deduced from prevalence of D-aspartate and nuclear weapons-related radiocarbon. J Clin Investig 87:1828–1834

    Article  Google Scholar 

  131. Shi Y, Dong Y, Duan Y, Jiang X, Chen C, Deng L (2013) Substrate stiffness influences TGF-beta1-induced differentiation of bronchial fibroblasts into myofibroblasts in airway remodeling. Mol Med Rep 7:419–424

    Google Scholar 

  132. Sly PD, Collins RA, Thamrin C, Turner DJ, Hantos Z (2003) Volume dependence of airway and tissue impedances in mice. J Appl Physiol 94:1460–1466

    Google Scholar 

  133. Sobin SS, Fung YC, Tremer HM (1988) Collagen and elastin fibers in human pulmonary alveolar walls. J Appl Physiol 64:1659–1675

    Google Scholar 

  134. Stromberg DD, Wiederhielm CA (1969) Viscoelastic description of a collagenous tissue in simple elongation. J Appl Physiol 26:857–862

    Google Scholar 

  135. Sugihara T, Martin CJ, Hildebrandt J (1971) Length-tension properties of alveolar wall in man. J Appl Physiol 30:874–878

    Google Scholar 

  136. Suki B (1993) Nonlinear phenomena in respiratory mechanical measurements. J Appl Physiol 74:2574–2584

    Google Scholar 

  137. Suki B (2014) Assessing the functional mechanical properties of bioengineered organs with emphasis on the lung. J Cell Physiol 229(9):1134–1140

    Google Scholar 

  138. Suki B, Barabasi AL, Hantos Z, Petak F, Stanley HE (1994) Avalanches and power-law behaviour in lung inflation. Nature 368:615–618

    Article  Google Scholar 

  139. Suki B, Barabasi AL, Lutchen KR (1994) Lung tissue viscoelasticity: a mathematical framework and its molecular basis. J Appl Physiol 76:2749–2759

    Google Scholar 

  140. Suki B, Bates JH (1991) A nonlinear viscoelastic model of lung tissue mechanics. J Appl Physiol 71:826–833

    Google Scholar 

  141. Suki B, Bates JH, Frey U (2011) Complexity and emergent phenomena. In: Fredberg JJ, Sieck GC, Gerthoffer WT (eds) Comprehensive physiology, the respiratory system, respiration mechanics: organ cell, molecule. Wiley-Blackwell, Oxford, pp 995–1029

    Google Scholar 

  142. Suki B, Lutchen KR (1992) Pseudorandom signals to estimate apparent transfer and coherence functions of nonlinear systems: applications to respiratory mechanics. IEEE Trans Biomed Eng 39:1142–1151

    Article  Google Scholar 

  143. Suki B, Stamenovic D, Hubmayr RD (2011) Lung parenchymal mechanics. Compr Physiol 1(3):1317–1351

    Google Scholar 

  144. Suki B, Zhang Q, Lutchen KR (1995) Relationship between frequency and amplitude dependence in the lung: a nonlinear block-structured modeling approach. J Appl Physiol 79:660–671

    Google Scholar 

  145. Takahashi A, Majumdar A, Parameswaran H, Bartolak-Suki E, Suki B (2014) Proteoglycans maintain lung stability in an elastase-treated mouse model of emphysema. Am J Respir Cell Mol Biol 51(1):26–33

    Google Scholar 

  146. Tanaka R, Al-Jamal R, Ludwig MS (2001) Maturational changes in extracellular matrix and lung tissue mechanics. J Appl Physiol 91:2314–2321

    Google Scholar 

  147. Tanaka R, Ludwig MS (1999) Changes in viscoelastic properties of rat lung parenchymal strips with maturation. J Appl Physiol 87:2081–2089

    Google Scholar 

  148. Teramoto S, Fukuchi Y, Uejima Y, Teramoto K, Oka T, Orimo H (1994) A novel model of senile lung: senescence-accelerated mouse (SAM). Am J Respir Crit Care Med 150:238–244

    Article  Google Scholar 

  149. Thurlbeck WM (1967) The internal surface area of nonemphysematous lungs. Am Rev Respir Dis 95:765–773

    Google Scholar 

  150. Turner JM, Mead J, Wohl ME (1968) Elasticity of human lungs in relation to age. J Appl Physiol 25:664–671

    Google Scholar 

  151. Ueda T, Cheng G, Kuroki Y, Sano H, Sugiyama K, Motojima S, Fukuda T (2000) Effects of aging on surfactant forms in rats. Eur Respir J 15:80–84

    Article  Google Scholar 

  152. Veldhuizen R, Nag K, Orgeig S, Possmayer F (1998) The role of lipids in pulmonary surfactant. Biochim Biophys Acta 1408:90–108

    Article  Google Scholar 

  153. Verbeken EK, Cauberghs M, Mertens I, Clement J, Lauweryns JM, Van de Woestijne KP (1992) The senile lung. Comparison with normal and emphysematous lungs. 1. Structural aspects. Chest 101:793–799

    Article  Google Scholar 

  154. Verbeken EK, Cauberghs M, Mertens I, Lauweryns JM, Van de Woestijne KP (1992) Tissue and airway impedance of excised normal, senile, and emphysematous lungs. J Appl Physiol 72:2343–2353

    Google Scholar 

  155. Weale RA (1993) Have human biological functions evolved in support of a life-span? Mech Ageing Dev 69:65–77

    Article  Google Scholar 

  156. Weibel ER, Gil J (1977) Structure-function relationships at the alveolar level. In: West JB (ed) Bioengineering Aspects of the Lung. Dekker, New York pp 1–81

    Google Scholar 

  157. Wilson TA, Bachofen H (1982) A model for mechanical structure of the alveolar duct. J Appl Physiol 52:1064–1070

    Google Scholar 

  158. Withers JR, Aston DE (2006) Nanomechanical measurements with AFM in the elastic limit. Adv Colloid Interface Sci 120:57–67

    Article  Google Scholar 

  159. Yasuoka S, Manabe H, Ozaki T, Tsubura E (1977) Effect of age on the saturated lecithin contents of human and rat lung tissues. J Gerontol 32:387–391

    Article  Google Scholar 

  160. Yuan H, Ingenito EP, Suki B (1997) Dynamic properties of lung parenchyma: mechanical contributions of fiber network and interstitial cells. J Appl Physiol 83:1420–1431 (discussion 1418–1429)

    Google Scholar 

  161. Yuan H, Kononov S, Cavalcante FS, Lutchen KR, Ingenito EP, Suki B (2000) Effects of collagenase and elastase on the mechanical properties of lung tissue strips. J Appl Physiol 89:3–14

    Google Scholar 

  162. Yuan H, Westwick DT, Ingenito EP, Lutchen KR, Suki B (1999) Parametric and nonparametric nonlinear system identification of lung tissue strip mechanics. Ann Biomed Eng 27:548–562

    Article  Google Scholar 

  163. Zhang Q, Suki B, Lutchen KR (1995) Harmonic distortion from nonlinear systems with broadband inputs: applications to lung mechanics. Ann Biomed Eng 23:672–681

    Article  Google Scholar 

  164. Zulliger MA, Fridez P, Hayashi K, Stergiopulos N (2004) A strain energy function for arteries accounting for wall composition and structure. J Biomech 37:989–1000

    Article  Google Scholar 

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Acknowledgments

This study was funded by NIH grants HL-098976 and HL111745.

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  1. Department of Biomedical Engineering, Boston University, Boston, USA

    Béla Suki & Erzsébet Bartolák-Suki

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  1. Béla Suki
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Correspondence to Béla Suki .

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  1. University of Manchester Materials Science Center, Manchester, United Kingdom

    Brian Derby

  2. University of Liverpool, Liverpool, United Kingdom

    Riaz Akhtar

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Suki, B., Bartolák-Suki, E. (2015). Biomechanics of the Aging Lung Parenchyma. In: Derby, B., Akhtar, R. (eds) Mechanical Properties of Aging Soft Tissues. Engineering Materials and Processes. Springer, Cham. https://doi.org/10.1007/978-3-319-03970-1_5

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