Regional structural and biomechanical alterations of the ovine main pulmonary artery during postnatal growth

Journal of Biomechanical Engineering

Volumn 135, Issue 2, 2013, Pages

  Fata, Bahar ^a   Carruthers, Christopher A ^a   Gibson, Gregory ^b   Watkins, Simon C ^b   Gottlieb, Danielle ^c   Mayer, John E ^c   Sacks, Michael S ^d  

^a University of Pittsburgh   (United States)

^b UNIVERSITY OF PITTSBURGH   (United States)

^c BOSTON CHILDREN S HOSPITAL   (United States)

^d The University of Texas at Austin   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANISOTROPY; BIFURCATION (MATHEMATICS); BIOMECHANICS; COLLAGEN; GLYCOPROTEINS; MECHANISMS; REPAIR; STRESSES;

BIAXIAL MECHANICAL PROPERTIES; BIOMECHANICAL BEHAVIOR; CONGENITAL DEFECTS; ENGINEERING FOUNDATION; GROWTH PATTERNS; POSTNATAL GROWTHS; PULMONARY ARTERY; STRUCTURAL BEHAVIORS; STRUCTURE-FUNCTION RELATIONSHIP; WALL STRESS;

ELASTIN;

COLLAGEN; ELASTIN;

ANISOTROPY; ARTICLE; BIOMECHANICS; BLOOD VESSEL DIAMETER; DEVELOPMENTAL STAGE; HOMEOSTASIS; MULTIPHOTON MICROSCOPY; NONHUMAN; POSTNATAL GROWTH; PULMONARY ARTERY; QUANTITATIVE ANALYSIS; SHEAR STRESS; THICKNESS; ANIMAL; GROWTH, DEVELOPMENT AND AGING; MECHANICAL STRESS; MECHANICS; METABOLISM; SHEEP;

ANIMALS; BIOMECHANICS; COLLAGEN; MECHANICAL PROCESSES; PULMONARY ARTERY; SHEEP; STRESS, MECHANICAL;

EID: 84873658622     PISSN: 01480731     EISSN: 15288951     Source Type: Journal    
DOI: 10.1115/1.4023389     Document Type: Article

References (61)

1. Adatia, I., Kothari, S. S., and Feinstein, J. A., 2010, "Pulmonary Hypertension Associated With Congenital Heart Disease: Pulmonary Vascular Disease: The Global Perspective," Chest, 137(6 Suppl), pp. 52S-61S
2. Tulloh, R. M., 2005, "Congenital Heart Disease in Relation to Pulmonary Hypertension in Paediatric Practice," Paediatr. Respir. Rev., 6(3), pp. 174-180 (Pubitemid 41258647)
3. Deterling, R. A., Jr., and Clagett, O. T., 1947, "Aneurysm of the Pulmonary Artery: Review of the Literature and Report of a Case," Am. Heart J., 34(4), pp. 471-499
4. Kutty, S., Kaul, S., Danford, C. J., and Danford, D. A., 2010, "Main Pulmonary Artery Dilation in Association with Congenital Bicuspid Aortic Valve in the Absence of Pulmonary Valve Abnormality," Heart, 96(21), pp. 1756-1761
5. Patnaik, A. N., Barik, R., Babu, S., and Gullati, A. S., 2012, "A Rare Case of Left Lung Hypoplasia Associated With Congenital Pulmonary Artery Aneurysm and Ventricular Septal Defect," Pediatr. Cardiol. (in press)
6. Greenwald, S. E., Johnson, R. J., and Haworth, S. G., 1984, "Pulmonary Vascular Input Impedance in the Newborn and Infant Pig," Cardiovasc. Res., 18, pp. 44-50
7. Lammers, S. R., Kao, P. H., Qi, H. J., Hunter, K., Lanning, C., Albietz, J., Hofmeister, S., Mecham, R., Stenmark, K. R., and Shandas, R., 2008, "Changes in the Structure-Function Relationship of Elastin and Its Impact on the Proximal Pulmonary Arterial Mechanics of Hypertensive Calves," Am. J. Physiol. Heart Circ. Physiol., 295(4), pp. H1451-H1459
8. Kogon, B. E., Patel, M., Pernetz, M., Mcconnell, M., and Book, W., 2009, "Late Pulmonary Valve Replacement in Congenital Heart Disease Patients Without Original Congenital Pulmonary Valve Pathology," Pediatr. Cardiol., 31(1), pp. 74-79
9. Ono, M., Goerler, H., Kallenbach, K., Boethig, D., Westhoff-Bleck, M., and Breymann, T., 2007, "Aortic Valve-Sparing Reimplantation for Dilatation of the Ascending Aorta and Aortic Regurgitation Late After Repair of Congenital Heart Disease," J. Thorac. Cardiovasc. Surg., 133(4), pp. 876-879 (Pubitemid 46435908)
10. Rosenberg, H. G., Williams, W. G., Trusler, G. A., Higa, T., and Rabinovitch, M., 1987, "Structural Composition of Central Pulmonary Arteries. Growth Potential After Surgical Shunts," J. Thorac. Cardiovasc. Surg., 94(4), pp. 498-503 (Pubitemid 17141661)
11. Mayer, J. E., Jr., 1995, "Uses of Homograft Conduits for Right Ventricle to Pulmonary Artery Connections in the Neonatal Period," Semin. Thorac. Cardiovasc. Surg., 7(3), pp. 130-132
12. Cho, S. W., Kim, I. K., Kang, J. M., Song, K. W., Kim, H. S., Park, C. H., Yoo, K. J., and Kim, B. S., 2009, "Evidence for In Vivo Growth Potential and Vascular Remodeling of Tissue-Engineered Artery," Tissue Eng. Part A, 15(4), pp. 901-912
13. Hoerstrup, S. P., Cummings Mrcs, I., Lachat, M., Schoen, F. J., Jenni, R., Leschka, S., Neuenschwander, S., Schmidt, D., Mol, A., Gunter, C., Gossi, M., Genoni, M., and Zund, G., 2006, "Functional Growth in Tissue-Engineered Living, Vascular Grafts: Follow-up at 100 Weeks in a Large Animal Model," Circulation, 114(1 Suppl), pp. I159-I166 (Pubitemid 44297145)
14. Shinoka, T., Shum-Tim, D., Ma, P. X., Tanel, R. E., Isogai, N., Langer, R., Vacanti, J. P., and Mayer, J. E., Jr., 1998, "Creation of Viable Pulmonary Artery Autografts Through Tissue Engineering," J. Thorac. Cardiovasc. Surg., 115(3), pp. 536-546 (Pubitemid 28158068)
15. Mol, A., Smits, A. I., Bouten, C. V., and Baaijens, F. P., 2009, "Tissue Engineering of Heart Valves: Advances and Current Challenges," Expert Rev. Med. Devices, 6(3), pp. 259-275
16. Huang, Y., Guo, X., and Kassab, G. S., 2006, "Axial Nonuniformity of Geometric and Mechanical Properties of Mouse Aorta is Increased During Postnatal Growth," Am. J. Physiol. Heart Circ. Physiol., 290(2), pp. H657-H664
17. Sugimoto, T., Miyazaki, H., and Hayashi, K., 2003, "Age-Related Changes in the Morphology and Mechanics of Arterial Wall in the Rat," JSME Int. J., 46(4), pp. 1312-1320 (Pubitemid 38265644)
18. Wells, S. M., Langille, B. L., and Adamson, S. L., 1998, "In Vivo and In Vitro Mechanical Properties of the Sheep Thoracic Aorta in the Perinatal Period and Adulthood," Am. J. Physiol., 274(43), pp. H1749-H1760
19. Wells, S. M., Langille, B. L., Lee, J. M., and Adamson, S. L., 1999, "Determinants of Mechanical Properties in the Developing Ovine Thoracic Aorta," Am. J. Physiol., 277(4), pp. H1385-H1391 (Pubitemid 29522667)
20. Haskett, D., Johnson, G., Zhou, A., Utzinger, U., and Vande Geest, J., 2010, "Microstructural and Biomechanical Alterations of the Human Aorta as a Function of Age and Location," Biomech. Model. Mechanobiol., 9(6), pp. 725-736
21. Bruel, A., and Oxlund, H., 1996, "Changes in Biomechanical Properties, Composition of Collagen and Elastin, and Advanced Glycation Endproducts of the Rat Aorta in Relation to Age," Atherosclerosis, 127(2), pp. 155-165 (Pubitemid 27045829)
22. Gaballa, M. A., Jacob, C. T., Raya, T. E., Liu, J., Simon, B., and Goldman, S., 1998, "Large Artery Remodeling During Aging: Biaxial Passive and Active Stiffness," Hypertension, 32(3), pp. 437-443 (Pubitemid 28429131)
23. Boumaza, S., Arribas, S. M., Osborne-Pellegrin, M., Mcgrath, J. C., Laurent, S., Lacolley, P., and Challande, P., 2001, "Fenestrations of the Carotid Internal Elastic Lamina and Structural Adaptation in Stroke-Prone Spontaneously Hypertensive Rats," Hypertension, 37(4), pp. 1101-1107 (Pubitemid 32304011)
24. Gottlieb, D., Kunal, T., Emani, S., Aikawa, E., Brown, D. W., Powell, A. J., Nedder, A., Engelmayr, G. C., Jr., Melero-Martin, J. M., Sacks, M. S., and Mayer, J. E., Jr., 2010, "In Vivo Monitoring of Function of Autologous Engineered Pulmonary Valve," J. Thorac. Cardiovasc. Surg., 139(3), pp. 723-731
25. Gottlieb, D., Fata, B., Powell, A. J., Cois, A., Annese, D., Tandon, K., Stetten, G., Mayer, J. E., Jr., and Sacks, M. S., "Pulmonary Artery Dimensional Changes in a Growing Ovine Model: Comparisons With the Ascending Aorta," J. Heart Valve Dis. (in-press)
26. Fata, B., Gottlieb, D., Mayer, J. E., and Sacks, M. S., "Postnatal In Vivo Surface Growth Deformation Patterns of the Ovine Main Pulmonary Artery and Ascending Aorta," J. Biomech. Eng. (submitted)
27. Grashow, J., 2005, "Evaluation of the Biaxial Mechanical Properties of the Mitral Valve Leaflet Under Physiological Loading Conditions," Ph.D. thesis, University of Pittsburgh, Pittsburgh, PA
28. Han, H. C., and Fung, Y. C., 1996, "Direct Measurement of Transverse Residual Strains in Aorta," Am. J. Physiol., 270(2 Pt 2), pp. H750-H759
29. Meijering, E., Jacob, M., Sarria, J. C. F., Steiner, P., Hirling, H., and Unser, M., 2004, "Design and Validation of a Tool for Neurite Tracing and Analysis in Fluorescence Microscopy Images," Cytometry, Part A, 58A(2), pp. 167-176 (Pubitemid 38509178)
30. Hill, M. R., Duan, X., Gibson, G. A., Watkins, S., and Robertson, A. M., 2012, "A Theoretical and Non-Destructive Experimental Approach for Direct Inclusion of Collagen Orientaiton and Recruitment Into Mechanical Models of the Artery Wall," J. Biomech., 45(5), pp. 762-771
31. Courtney, T., Sacks, M. S., Stankus, J., Guan, J., and Wagner, W. R., 2006, "Design and Analysis of Tissue Engineering Scaffolds That Mimic Soft Tissue Mechanical Anisotropy," Biomaterials, 27(19), pp. 3631-3638
32. Vande Geest, J. P., Di Martino, E. S., Bohra, A., Makaroun, M. S., and Vorp, D. A., 2006, "A Biomechanics-Based Rupture Potential Index for Abdominal Aortic Aneurysm Risk Assessment: Demonstrative Application," Ann. N. Y. Acad. Sci., 1085, pp. 11-21 (Pubitemid 47092017)
33. Gozna, E. R., Marble, A. E., Shaw, A., and Holland, J. G., 1974, "Age-Related Changes in the Machanics of the Aorta and Pulmonary Artery of Man," J. Appl. Physiol., 36(4), pp. 407-411
34. Vande Geest, J. P., Sacks, M. S., and Vorp, D. A., 2004, "Age Dependency of the Biaxial Biomechanical Behavior of Human Abdominal Aorta," J. Biomech. Eng., 126(6), pp. 815-822 (Pubitemid 40293730)
35. Choudhury, N., Bouchot, O., Rouleau, L., Tremblay, D., Cartier, R., Butany, J., Mongrain, R., and Leask, R. L., 2009, "Local Mechanical and Structural Properties of Healthy and Diseased Human Ascending Aorta Tissue," Cardiovasc. Pathol., 18(2), pp. 83-91
36. Patel, D. J., Schilder, D. P., and Mallos, A. J., 1960, "Mechanical Properties and Dimensions of the Major Pulmonary Arteries," J. Appl. Physiol., 15(1), pp. 92-96
37. Drexler, E. S., Quinn, T. P., Slifka, A. J., Mccowan, C. N., Bischoff, J. E., Wright, J. E., Ivy, D. D., and Shandas, R., 2007, "Comparison of Mechanical Behavior Among the Extrapulmonary Arteries from Rats," J. Biomech., 40(4), pp. 812-819 (Pubitemid 46273462)
38. Hunter, K. S., Albietz, J. A., Lee, P. F., Lanning, C. J., Lammers, S. R., Hofmeister, S. H., Kao, P. H., Qi, H. J., Stenmark, K. R., and Shandas, R., 2010, "In Vivo Measurement of Proximal Pulmonary Artery Elastic Modulus in the Neonatal Calf Model of Pulmonary Hypertension: Development and Ex Vivo Validation," J. Appl. Physiol., 108(4), pp. 968-975
39. Chesler, N. C., Thompson-Figueroa, J., and Millburne, K., 2004, "Measurements of Mouse Pulmonary Artery Biomechanics," J. Biomech. Eng., 126(2), pp. 309-314 (Pubitemid 38621145)
40. Patel, D. J., Freitas, F. M. D., and Mallos, A. J., 1962, "Mechanical Function of the Main Pulmonary Artery," J. Appl. Physiol., 17(2), pp. 205-208
41. Chuong, C. J., and Fung, Y. C., 1986, "On Residual Stress in Arteries," J. Biomech. Eng., 108, pp. 189-192
42. Fung, Y. C., 1990, Biomechanics: Motion, Flow, Stress, and Growth, Springer, New York, p. 569
43. Vaishnav, R. N., and Vossoughi, J., 1983, "Estimation of Residual Strains in Aortic Segments," Biomechanical Engineering II, Recent Developments, Pergamon, New York, pp. 330-333 (Pubitemid 17470884)
44. Jiang, Z. L., Kassab, G. S., and Fung, Y. C., 1994, "Diameter- Defined Strahler System and Connectivity Matrix of the Pulmonary Arterial Tree," J. Appl. Physiol., 76(2), pp. 882-892 (Pubitemid 24075640)
45. Fung, Y. C., 1991, "What Are the Residual Stresses Doing in Our Blood Vessels?," Ann. Biomed. Eng., 19(3), pp. 237-249
46. Liu, S. Q., and Fung, Y. C., 1992, "Changes in the Rheological Properties of Blood Vessel Tissue Remodeling in the Course of Development of Diabetes," Biorheology, 29(5-6), pp. 443-457 (Pubitemid 23104929)
47. Zou, Y., and Zhang, Y., 2009, "An Experimental and Theoretical Study on the Anisotropy of Elastin Network," Ann. Biomed. Eng., 37(8), pp. 1572-1583
48. Lillie, M. A., Shadwick, R. E., and Gosline, J. M., 2010, "Mechanical Anisotropy of Inflated Elastic Tissue From the Pig Aorta," J. Biomech., 43(11), pp. 2070-2078
49. Roach, M. R., and Burton, A. C., 1957, "The Reason for the Shape of the Distensibility Curves of Arteries," Can. J. Biochem. Physiol., 35, pp. 681-690
50. Hill, M., 2011, "A Novel Approach for Combining Biomechanical and Micro-Structural Analyses to Assess the Mechanical and Damage Properties of the Artery Wall," Ph.D. thesis, University of Pittsburgh, Pittsburgh, PA
51. Keyes, J. T., Lockwood, D. R., Utzinger, U., Montilla, L. G., Witte, R. S., and Vande Geest, J. P., 2012, "Comparisons of Planar and Tubular Biaxial Tensile Testing Protocols of the Same Porcine Coronary Arteries," Ann. Biomed. Eng. (in press)
52. Keyes, J. T., Haskett, D. G., Utzinger, U., Azhar, M., and Vande Geest, J. P., 2011, "Adaptation of a Planar Microbiaxial Optomechanical Device for the Tubular Biaxial Microstructural and Macroscopic Characterization of Small Vascular Tissues," J. Biomech. Eng., 133(7), p. 075001
53. Hollander, Y., Durban, D., Lu, X., Kassab, G. S., and Lanir, Y., 2011, "Experimentally Validated Microstructural 3d Constitutive Model of Coronary Arterial Media," J. Biomech. Eng., 133(3), p. 031007
54. Hollander, Y., Durban, D., Lu, X., Kassab, G. S., and Lanir, Y., 2011, "Constitutive Modeling of Coronary Arterial Media-Comparison of Three Model Classes," J. Biomech. Eng., 133(6), p. 061008
55. Freed, A. D., and Doehring, T. C., 2005, "Elastic Model for Crimped Collagen Fibrils," J. Biomech. Eng., 127(4), pp. 587-593 (Pubitemid 41116917)
56. Prot, V., Skallerud, B., Sommer, G., and Holzapfel, G. A., 2010, "On Modelling and Analysis of Healthy and Pathological Human Mitral Valves: Two Case Studies," J. Mech. Behav. Biomed. Mater., 3(2), pp. 167-177
57. Ooi, C. Y., Wang, Z., Tabima, D. M., Eickhoff, J. C., and Chesler, N. C., 2010, "The Role of Collagen in Extralobar Pulmonary Artery Stiffening in Response to Hypoxia-Induced Pulmonary Hypertension," Am. J. Physiol. Heart Circ. Physiol., 299(6), pp. H1823-H1831
58. Tozzi, C. A., Christiansen, D. L., Poiani, G. J., and Riley, D. J., 1994, "Excess Collagen in Hypertensive Pulmonary Arteries Decreases Vascular Distensibility," Am. J. Respir. Crit. Care Med., 149(5), pp. 1317-1326 (Pubitemid 24147076)
59. Poiani, G. J., Tozzi, C. A., Yohn, S. E., Pierce, R. A., Belsky, S. A., Berg, R. A., Yu, S. Y., Deak, S. B., and Riley, D. J., 1990, "Collagen and Elastin Metabolism in Hypertensive Pulmonary Arteries of Rats," Circ. Res., 66(4), pp. 968-978 (Pubitemid 20126428)
60. Berry, C. L., Looker, T., and Germain, J., 1972, "The Growth and Development of the Rat Aorta. I. Morphological Aspects," J. Anat., 113(Pt 1), pp. 1-16
61. Leung, D. Y. M., Glagov, S., and Mathews, M. B., 1977, "Elastin and Collagen Accumulation in Rabbit Ascending Aorta and Pulmonary Trunk During Postnatal Growth. Correlation of Cellular Synthetic Response With Medial Tension," Circ. Res., 41(3), pp. 316-323. (Pubitemid 8185852)