Potential damage in pulmonary arterial hypertension: An experimental study of pressure-induced damage of pulmonary artery
Yuheng Wang
Department of Mechanical Engineering, Michigan State University, East Lansing, Michigan, USA
Search for more papers by this authorHamidreza Gharahi
Department of Mechanical Engineering, Michigan State University, East Lansing, Michigan, USA
Search for more papers by this authorMarissa R. Grobbel
Department of Mechanical Engineering, Michigan State University, East Lansing, Michigan, USA
Search for more papers by this authorAkshay Rao
Department of Mechanical Engineering, Texas A&M University, College Station, Texas, USA
Search for more papers by this authorCorresponding Author
Sara Roccabianca
Department of Mechanical Engineering, Michigan State University, East Lansing, Michigan, USA
Correspondence
Sara Roccabianca, 428 S. Shaw Lane Room 2463, East Lansing, MI 48824.
Email: [email protected]
Search for more papers by this authorSeungik Baek
Department of Mechanical Engineering, Michigan State University, East Lansing, Michigan, USA
Search for more papers by this authorYuheng Wang
Department of Mechanical Engineering, Michigan State University, East Lansing, Michigan, USA
Search for more papers by this authorHamidreza Gharahi
Department of Mechanical Engineering, Michigan State University, East Lansing, Michigan, USA
Search for more papers by this authorMarissa R. Grobbel
Department of Mechanical Engineering, Michigan State University, East Lansing, Michigan, USA
Search for more papers by this authorAkshay Rao
Department of Mechanical Engineering, Texas A&M University, College Station, Texas, USA
Search for more papers by this authorCorresponding Author
Sara Roccabianca
Department of Mechanical Engineering, Michigan State University, East Lansing, Michigan, USA
Correspondence
Sara Roccabianca, 428 S. Shaw Lane Room 2463, East Lansing, MI 48824.
Email: [email protected]
Search for more papers by this authorSeungik Baek
Department of Mechanical Engineering, Michigan State University, East Lansing, Michigan, USA
Search for more papers by this authorFunding information: National Institutes of Health (NIH), Grant/Award Number: U01 1HL135842
Abstract
Pulmonary arterial hypertension (PAH) is associated with elevated pulmonary arterial pressure. PAH prognosis remains poor with a 15% mortality rate within 1 year, even with modern clinical management. Previous clinical studies proposed wall shear stress (WSS) to be an important hemodynamic factor affecting cell mechanotransduction, growth and remodeling, and disease progress in PAH. However, WSS in vivo is typically at most 2.5 Pa and a doubt has been cast whether WSS alone can drive disease progress. Furthermore, our current understanding of PAH pathology largely comes from small animals' studies in which caliber enlargement, a hallmark of PAH in humans, is rarely reported. Therefore, a large-animal experiment on pulmonary arteries (PAs) is needed to validate whether increased pressure can induce enlargement of PAs caliber. In this study, we use an inflation testing device to characterize the mechanical behavior, both nonlinear elastic behavior and irreversible damage of porcine arteries. The parameters of elastic behavior are estimated from the inflation test at a low-pressure range before and after over-pressurization. Then, histological images are qualitatively examined for medial and adventitial layers. This study sheds light on the relevance of pressure-induced damage mechanism in human PAH.
REFERENCES
- Akhtar, R., Sherratt, M. J., Cruickshank, J. K., & Derby, B. (2011). Characterizing the elastic properties of tissues. Materials Today, 14(3), 96–105.
- Baek, S., Gleason, R. L., Rajagopal, K. R., & Humphrey, J. D. (2007). Theory of small on large: Potential utility in computations of fluid–solid interactions in arteries. Computer Methods in Applied Mechanics and Engineering, 196(31–32), 3070–3078.
- Balzani, D., Schröder, J., & Gross, D. (2006). Simulation of discontinuous damage incorporating residual stresses in circumferentially overstretched atherosclerotic arteries. Acta Biomaterialia, 2(6), 609–618.
- Bellini, C., Ferruzzi, J., Roccabianca, S., Di Martino, E. S., & Humphrey, J. D. (2014). A microstructurally motivated model of arterial wall mechanics with mechanobiological implications. Annals of Biomedical Engineering, 42(3), 488–502.
- Botney, M. D. (1999). Role of hemodynamics in pulmonary vascular remodeling: Implications for primary pulmonary hypertension. American Journal of Respiratory and Critical Care Medicine, 159(2), 361–364.
- Bürk, J., Blanke, P., Stankovic, Z., Barker, A., Russe, M., Geiger, J., … Markl, M. (2012). Evaluation of 3D blood flow patterns and wall shear stress in the normal and dilated thoracic aorta using flow-sensitive 4D CMR. Journal of Cardiovascular Magnetic Resonance, 14(1), 84.
- Calvo, B., Peña, E., Martinez, M. A., & Doblaré, M. (2007). An uncoupled directional damage model for fibred biological soft tissues. Formulation and computational aspects. International Journal for Numerical Methods in Engineering, 69(10), 2036–2057.
- Converse, M. I., Walther, R. G., Ingram, J. T., Li, Y., Yu, S. M., & Monson, K. L. (2018). Detection and characterization of molecular-level collagen damage in overstretched cerebral arteries. Acta Biomaterialia, 67, 307–318.
- Cunningham, K. S., & Gotlieb, A. I. (2005). The role of shear stress in the pathogenesis of atherosclerosis. Laboratory Investigation, 85(1), 9–23.
- Dobrin, P. B., Baker, W. H., & Gley, W. C. (1984). Elastolytic and collagenolytic studies of arteries: Implications for the mechanical properties of aneurysms. Archives of Surgery, 119(4), 405–409.
- Edwards, P. D., Bull, R. K., & Coulden, R. (1998). CT measurement of main pulmonary artery diameter. The British Journal of Radiology, 71(850), 1018–1020.
- Ferrara, A., & Pandolfi, A. N. (2008a). Numerical modelling of fracture in human arteries. Computer Methods in Biomechanics and Biomedical Engineering, 11(5), 553–567.
- Ferrara, A., & Pandolfi, A. N. (2008b). Numerical simulation of arterial plaque ruptures. International Journal of Material Forming, 1(1), 1095–1098.
- Ferruzzi, J., Collins, M. J., Yeh, A. T., & Humphrey, J. D. (2011). Mechanical assessment of elastin integrity in fibrillin-1-deficient carotid arteries: Implications for Marfan syndrome. Cardiovascular Research, 92(2), 287–295.
- Gasser, T. C., Ogden, R. W., & Holzapfel, G. A. (2006). Hyperelastic modelling of arterial layers with distributed collagen fibre orientations. Journal of the Royal Society Interface, 3(6), 15–35.
- Gundiah, N., Ratcliffe, M. B., & Pruitt, L. A. (2009). The biomechanics of arterial elastin. Journal of the Mechanical Behavior of Biomedical Materials, 2(3), 288–296.
- Guo, X., Kono, Y., Mattrey, R., & Kassab, G. S. (2002). Morphometry and strain distribution of the C57BL/6 mouse aorta. American Journal of Physiology-Heart and Circulatory Physiology, 283(5), H1829–H1837.
- Han, H. C., & Fung, Y. C. (1995). Longitudinal strain of canine and porcine aortas. Journal of Biomechanics, 28(5), 637–641.
- Hokanson, J., & Yazdani, S. (1997). A constitutive model of the artery with damage. Mechanics Research Communications, 24(2), 151–159.
- Holzapfel, G. A., Gasser, T. C., & Ogden, R. W. (2000). A new constitutive framework for arterial wall mechanics and a comparative study of material models. Journal of Elasticity and the Physical Science of Solids, 61(1–3), 1–48.
- Holzapfel, G. A., Sommer, G., Gasser, C. T., & Regitnig, P. (2005). Determination of layer-specific mechanical properties of human coronary arteries with nonatherosclerotic intimal thickening and related constitutive modeling. American Journal of Physiology-Heart and Circulatory Physiology, 289(5), H2048–H2058.
- Humphrey, J., & Delange, S. L. (2016). Introduction to biomechanics. New York: Springer-Verlag.
- Humphrey, J. D. (2013). Cardiovascular solid mechanics: Cells, tissues, and organs, New York: Springer Science & Business Media.
- Humphrey, J. D., & Tellides, G. (2019). Central artery stiffness and thoracic aortopathy. American Journal of Physiology-Heart and Circulatory Physiology, 316(1), H169–H182.
- Kaess, B. M., Rong, J., Larson, M. G., Hamburg, N. M., Vita, J. A., Levy, D., … Mitchell, G. F. (2012). Aortic stiffness, blood pressure progression, and incident hypertension. Journal of the American Medical Association, 308(9), 875–881.
- Kim, J., & Baek, S. (2011). Circumferential variations of mechanical behavior of the porcine thoracic aorta during the inflation test. Journal of Biomechanics, 44(10), 1941–1947.
- Lammers, S., Scott, D., Hunter, K., Tan, W., Shandas, R., & Stenmark, K. R. (2011). Mechanics and function of the pulmonary vasculature: Implications for pulmonary vascular disease and right ventricular function. Comprehensive Physiology, 2(1), 295–319.
- Lammers, S. R., Kao, P. H., Qi, H. J., Hunter, K., Lanning, C., Albietz, J., … Shandas, R. (2008). Changes in the structure-function relationship of elastin and its impact on the proximal pulmonary arterial mechanics of hypertensive calves. American Journal of Physiology-Heart and Circulatory Physiology, 295(4), H1451–H1459.
- Li, D., & Robertson, A. M. (2009). A structural multi-mechanism damage model for cerebral arterial tissue. Journal of Biomechanical Engineering, 131(10), 101013.
- Li, M., Scott, D. E., Shandas, R., Stenmark, K. R., & Tan, W. (2009). High pulsatility flow induces adhesion molecule and cytokine mRNA expression in distal pulmonary artery endothelial cells. Annals of Biomedical Engineering, 37(6), 1082–1092.
- Li, M., Stenmark, K. R., Shandas, R., & Tan, W. (2009). Effects of pathological flow on pulmonary artery endothelial production of vasoactive mediators and growth factors. Journal of Vascular Research, 46(6), 561–571.
- MacLean, N. F., Dudek, N. L., & Roach, M. R. (1999). The role of radial elastic properties in the development of aortic dissections. Journal of Vascular Surgery, 29(4), 703–710.
- Martin, C., Sun, W., Pham, T., & Elefteriades, J. (2013). Predictive biomechanical analysis of ascending aortic aneurysm rupture potential. Acta Biomaterialia, 9(12), 9392–9400.
- McLaughlin, V. V., Shah, S. J., Souza, R., & Humbert, M. (2015). Management of pulmonary arterial hypertension. Journal of the American College of Cardiology, 65(18), 1976–1997.
- Mitchell, G. F. (2014). Arterial stiffness and hypertension. Hypertension, 64(1), 13–18.
- Richens, D., Field, M., Neale, M., & Oakley, C. (2002). The mechanism of injury in blunt traumatic rupture of the aorta. European Journal of Cardio-Thoracic Surgery, 21(2), 288–293.
- Roach, M. R., & Burton, A. C. (1957). The reason for the shape of the distensibility curves of arteries. Canadian Journal of Biochemistry and Physiology, 35(8), 681–690.
- Sanz, J., Kariisa, M., Dellegrottaglie, S., Prat-González, S., Garcia, M. J., Fuster, V., & Rajagopalan, S. (2009). Evaluation of pulmonary artery stiffness in pulmonary hypertension with cardiac magnetic resonance. JACC: Cardiovascular Imaging, 2(3), 286–295.
- Schrauwen, J. T., Vilanova, A., Rezakhaniha, R., Stergiopulos, N., Van De Vosse, F. N., & Bovendeerd, P. H. (2012). A method for the quantification of the pressure dependent 3D collagen configuration in the arterial adventitia. Journal of Structural Biology, 180(2), 335–342.
- Schriefl, A. J., Schmidt, T., Balzani, D., Sommer, G., & Holzapfel, G. A. (2015). Selective enzymatic removal of elastin and collagen from human abdominal aortas: Uniaxial mechanical response and constitutive modeling. Acta Biomaterialia, 17, 125–136.
- Schroeder, F., Polzer, S., Slažanský, M., Man, V., & Skácel, P. (2018). Predictive capabilities of various constitutive models for arterial tissue. Journal of the Mechanical Behavior of Biomedical Materials, 78, 369–380.
- Scott, S., Ferguson, G. G., & Roach, M. R. (1972). Comparison of the elastic properties of human intracranial arteries and aneurysms. Canadian Journal of Physiology and Pharmacology, 50(4), 328–332.
- Simo, J. C. (1987). On a fully three-dimensional finite-strain viscoelastic damage model: Formulation and computational aspects. Computer Methods in Applied Mechanics and Engineering, 60(2), 153–173.
- Sommer, G., Regitnig, P., Költringer, L., & Holzapfel, G. A. (2010). Biaxial mechanical properties of intact and layer-dissected human carotid arteries at physiological and supraphysiological loadings. American Journal of Physiology-Heart and Circulatory Physiology, 298(3), H898–H912.
- Sun, W., & Chan, S. Y. (2018). Pulmonary arterial stiffness: An early and pervasive driver of pulmonary arterial hypertension. Frontiers in Medicine, 5, 204.
- Thubrikar, M. J., & Robicsek, F. (1995). Pressure-induced arterial wall stress and atherosclerosis. The Annals of Thoracic Surgery, 59(6), 1594–1603.
- Tian, L., Lammers, S. R., Kao, P. H., Albietz, J. A., Stenmark, K. R., Qi, H. J., … Hunter, K. S. (2012). Impact of residual stretch and remodeling on collagen engagement in healthy and pulmonary hypertensive calf pulmonary arteries at physiological pressures. Annals of Biomedical Engineering, 40(7), 1419–1433.
- Truong, U., Fonseca, B., Dunning, J., Burgett, S., Lanning, C., Ivy, D. D., … Barker, A. J. (2013). Wall shear stress measured by phase contrast cardiovascular magnetic resonance in children and adolescents with pulmonary arterial hypertension. Journal of Cardiovascular Magnetic Resonance, 15(1), 81.
- Valentin, A., Cardamone, L., Baek, S., & Humphrey, J. D. (2009). Complementary vasoactivity and matrix remodelling in arterial adaptations to altered flow and pressure. Journal of the Royal Society Interface, 6(32), 293–306.
- Vorp, D. A., Wang, D. H. J., Webster, M. W., & Federspiel, W. J. (1998). Effect of intraluminal thrombus thickness and bulge diameter on the oxygen diffusion in abdominal aortic aneurysm. Journal of Biomechanical Engineering, 120, 579–583.
- Weisbrod, R. M., Shiang, T., Al Sayah, L., Fry, J. L., Bajpai, S., Reinhart-King, C. A., … Seta, F. (2013). Arterial stiffening precedes systolic hypertension in diet-induced obesity. Hypertension, 62(6), 1105–1110.
- Zambrano, B. A., Gharahi, H., Lim, C., Jaberi, F. A., Choi, J., Lee, W., & Baek, S. (2016). Association of intraluminal thrombus, hemodynamic forces, and abdominal aortic aneurysm expansion using longitudinal CT images. Annals of Biomedical Engineering, 44(5), 1502–1514.