Role of Biomechanical Stress in the Pathology of the Aorta

  • Giuseppina CaligiuriEmail author
  • Bernard P. Levy
  • Antonino Nicoletti
  • Jean-Baptiste Michel


The study of the pathology of the aorta must necessarily take into account the role of biomechanical stress that continuously impact on the biology of the cellular and molecular components of its wall. In mammals, the circulation requires a highly organized system, in which organ-regulated directional blood flow is propelled through the conductance arterial tree with a defined wall structure, by the pumping action of the mammalian heart.

A high blood pressure is therefore a compulsory biomechanical stress in human aortic biology. Fluids (radial convection) and particulate components (collision) play different and complementary role in the determinism of aortic pathologies and the relative complications linked to biomechanical stress such as atherosclerotic and aneurysmal diseases.

Hemodynamics in the phylogenetically selected, highly pressurized and branched arterial tree is indeed the most important common denominator of all arterial pathologies. Understanding the role played by biomechanical stress is therefore crucial for researchers and clinicians working within the field of aortic diseases, and nothing makes sense in the arterial pathology, except in the light of hemodynamics.


Pressure Flow Impedance Arterial bifurcation Chronic dilation Acute rupture Atheroma Aneurysms Dissection 


  1. 1.
    Bank AJ, Wang H, Holte JE, Shammas R, Kubo SH. Contribution of collagen, elastin, and smooth muscle to in vivo human brachial artery wall stress and elastic modulus. Circulation. 1996;94:3263–70.CrossRefGoogle Scholar
  2. 2.
    Cantini C, Kieffer P, Corman B, Liminana P, Atkinson J, Lartaud-Idjouadiene I. Aminoguanidine and aortic wall mechanics, structure, and composition in aged rats. Hypertension. 2001;38:943–8.CrossRefGoogle Scholar
  3. 3.
    O’Rourke MF, Staessen JA, Vlachopoulos C, Duprez D, Plante GE. Clinical applications of arterial stiffness; definitions and reference values. Am J Hypertens. 2002;15:426–44.CrossRefGoogle Scholar
  4. 4.
    O’Rourke MF, Taylor MG. Input impedance of the systemic circulation. Circ Res. 1967;20:365–80.CrossRefGoogle Scholar
  5. 5.
    Pythoud F, Stergiopulos N, Westerhof N, Meister JJ. Method for determining distribution of reflection sites in the arterial system. Am J Phys. 1996;271:H1807–13.Google Scholar
  6. 6.
    McEniery CM, Yasmin N, Hall IR, Qasem A, Wilkinson IB, Cockcroft JR. Normal vascular aging: differential effects on wave reflection and aortic pulse wave velocity: the Anglo-Cardiff Collaborative Trial (ACCT). J Am Coll Cardiol. 2005;46:1753–60.CrossRefGoogle Scholar
  7. 7.
    Laurent SP, Boutouyrie P. Recent advances in arterial stiffness and wave reflection in human hypertension. Hypertension. 2007;49:1202–6.CrossRefGoogle Scholar
  8. 8.
    O’Rourke MF, Nichols WW. Aortic diameter, aortic stiffness, and wave reflection increase with age and isolated systolic hypertension. Hypertension. 2005;45:652–8.CrossRefGoogle Scholar
  9. 9.
    Back M, Gasser TC, Michel B, Caliguri G. Biomechanical factors in the biology of aortic wall and aortic valve diseases. Cardiovasc Res. 2013;99:232–41.CrossRefGoogle Scholar
  10. 10.
    Kolodgie FD, Burke AP, Nakazawa G, Virmani R. Is pathologic intimal thickening the key to understanding early plaque progression in human atherosclerotic disease? Arterioscler Thromb Vasc Biol. 2007;27:986–9.CrossRefGoogle Scholar
  11. 11.
    Lacolley P, Regnault V, Nicoletti A, Li Z, Michel JB. The vascular smooth muscle cell in arterial pathology: a cell that can take on multiple roles. Cardiovasc Res. 2012;95:194–204.CrossRefGoogle Scholar
  12. 12.
    Michel JB, Thaunat O, Houard X, Meilhac O, Caliguri G, Nicoletti A. Topological determinants and consequences of adventitial responses to arterial wall injury. Arterioscler Thromb Vasc Biol. 2007;27:1259–68.CrossRefGoogle Scholar
  13. 13.
    Ingber DE. Tensegrity-based mechanosensing from macro to micro. Prog Biophys Mol Biol. 2008;97:163–79.CrossRefGoogle Scholar
  14. 14.
    Michel JB. Anoikis in the cardiovascular system: known and unknown extracellular mediators. Arterioscler Thromb Vasc Biol. 2003;23:2146–54.CrossRefGoogle Scholar
  15. 15.
    Wang N, Tytell JD, Ingber DE. Mechanotransduction at a distance: mechanically coupling the extracellular matrix with the nucleus. Nat Rev Mol Cell Biol. 2009;10:75–82.CrossRefGoogle Scholar
  16. 16.
    Isermann P, Lammerding J. Nuclear mechanics and mechanotransduction in health and disease. Curr Biol. 2013;23:1113–21.CrossRefGoogle Scholar
  17. 17.
    Chen LJ, Wei SY, Chiu JJ. Mechanical regulation of epigenetics in vascular biology and pathobiology. J Cell Mol Med. 2013;17:437–48.CrossRefGoogle Scholar
  18. 18.
    Aarts PA, van den Broek SA, Prins GW, Kulken GD, Sixma JJ, Heethaar RM. Blood platelets are concentrated near the wall and red blood cells, in the center in flowing blood. Arteriosclerosis. 1988;8:819–24.CrossRefGoogle Scholar
  19. 19.
    Ho-Tin-Noe B, Le Dall J, Gomez D, Louedec L, Vranckx R, El-bouchtaoui M, Legres L, Meilhac O, Michel JB. Early atheroma-derived agonists of peroxisome proliferator-activated receptor-gamma trigger intramedial angiogenesis in a smooth muscle cell-dependent manner. Circ Res. 2011;109:1003–14.CrossRefGoogle Scholar
  20. 20.
    Tabas I, Williams KJ, Boren J. Subendothelial lipoprotein retention as the initiating process in atherosclerosis: update and therapeutic implications. Circulation. 2007;116:1832–44.CrossRefGoogle Scholar
  21. 21.
    Madureira PA, Surette AP, Phipps KD, Taboski MA, Miller VA, Waisman DM. The role of the annexin A2 heterotetramer (AIIt) in vascular fibrinolysis. Blood. 2011;118:4789–97.CrossRefGoogle Scholar
  22. 22.
    DiDonato JA, Huang Y, Aulak KS, Even-Or O, Gerstenecker G, Gogonea V, Wu Y, Fox PL, et al. Function and distribution of apolipoprotein A1 in the artery wall are markedly distinct from those in plasma. Circulation. 2013;128:1644–55.CrossRefGoogle Scholar
  23. 23.
    Virmani R, Avolio AP, Mergner WJ, Robinowitz M, Herderick EE, Cornhill JF, Guo SY, Liu TH, Ou DY, O’Rourke M. Effect of aging on aortic morphology in populations with high and low prevalence of hypertension and atherosclerosis. Comparison between occidental and Chinese communities. Am J Pathol. 1991;139:1119–29.PubMedPubMedCentralGoogle Scholar
  24. 24.
    Chow B, Rabkin SW. The relationship between arterial stiffness and heart failure with preserved ejection fraction: a systemic meta-analysis. Heart Fail Rev. 2015;20:291–303.CrossRefGoogle Scholar
  25. 25.
    Sloop GD, Perret RS, Brahney JS, Oalmann M. A description of two morphologic patterns of aortic fatty streaks, and a hypothesis of their pathogenesis. Atherosclerosis. 1998;141:153–60.CrossRefGoogle Scholar
  26. 26.
    Mohamied Y, Rowland EM, Bailey EL, Sherwin SJ, Schwartz MA, Weinberg PD. Change of direction in the biomechanics of atherosclerosis. Ann Biomed Eng. 2015;43:16–25.CrossRefGoogle Scholar
  27. 27.
    Trachet B, Fraga-Silva RA, Piersigilli A, Tedgui A, Sordet-Dessimoz J, Asolfo A, Van der Donckt C, et al. Dissecting abdominal aortic aneurysm in Ang II-infused mice: suprarenal branch ruptures and apparent luminal dilatation. Cardiovasc Res. 2015;105:213–22.CrossRefGoogle Scholar
  28. 28.
    Ho-Tin-Noe B, Michel JB. Initiation of angiogenesis in atherosclerosis: smooth muscle cells as mediators of the angiogenic response to atheroma formation. Trends Cardiovasc Med. 2011;21:183–7.CrossRefGoogle Scholar
  29. 29.
    Michel JB, Martin-Ventura JL, Egido J, Sakalihasan N, Treska V, Lindholt J, Allaire E, et al. Novel aspects of the pathogenesis of aneurysms of the abdominal aorta in humans. Cardiovasc Res. 2011;90:18–27.CrossRefGoogle Scholar
  30. 30.
    Adolph R, Vorp DA, Steed DL, Webster MW, Kameneva MV, Watkins SC. Cellular content and permeability of intraluminal thrombus in abdominal aortic aneurysm. J Vasc Surg. 1997;25:916–26.CrossRefGoogle Scholar
  31. 31.
    Touat Z, Lepage L, Ollivier V, Nataf P, Hvass U, Labreuche J, Jandrot-Perrus M, Michel JB, Jondeau G. Dilation-dependent activation of platelets and prothrombin in human thoracic ascending aortic aneurysm. Arterioscler Thromb Vasc Biol. 2008;28:940–6.CrossRefGoogle Scholar
  32. 32.
    Jondeau G, Michel JB, Boileau C. The translational science of Marfan syndrome. Heart. 2011;97:1206–14.CrossRefGoogle Scholar
  33. 33.
    Borges LF, Gomez D, Quintana M, Touat Z, Jondeau G, Leclercq A, Meilhac O, Jandrot-Perrus M, Gutierrez PS, Freymuller E, et al. Fibrinolytic activity is associated with presence of cystic medial degeneration in aneurysms of the ascending aorta. Histopathology. 2010;57:917–32.CrossRefGoogle Scholar
  34. 34.
    Holm TM, Habashi JP, Doyle JJ, Bedja D, Chen Y, van Erp C, Lindsay ME, Kim D, et al. Noncanonical TGFbeta signaling contributes to aortic aneurysm progression in Marfan syndrome mice. Science. 2011;332:358–61.CrossRefGoogle Scholar
  35. 35.
    Gomez D, Al Haj Zen A, Borges LF, Philippe M, Gutierrez PS, Jondeau G, Michel JB, Vranckx R. Syndromic and non-syndromic aneurysms of the human ascending aorta share activation of the Smad2 pathway. J Pathol. 2009;218:131–42.CrossRefGoogle Scholar
  36. 36.
    Gomez D, Kessler K, Borges LF, Richard B, Touat Z, Ollivier V, Mansilla S, et al. Smad2-dependent protease Nexin-1 overexpression differentiates chronic aneurysms from acute dissections of human ascending aorta. Arterioscler Thromb Vasc Biol. 2013;33:2222–32.CrossRefGoogle Scholar
  37. 37.
    Renard M, Callewaert B, Baetens M, Campens L, MacDermot K, Fryns JP, Bonduelle M, et al. Novel MYH11 and ACTA2 mutations reveal a role for enhanced TGFbeta signaling in FTAAD. Int J Cardiol. 2013;165:14–21.Google Scholar
  38. 38.
    Humphrey JD, Schwartz MA, Tellides G, Milewicz DM. Role of mechanotransduction in vascular biology: focus on thoracic aortic aneurysms and dissections. Circ Res. 2015;116:1448–61.CrossRefGoogle Scholar
  39. 39.
    Rossignol P, Ho-Tin-Noe B, Vranckx R, Bouton MC, Meilhac O, Lijnen HR, Guillin MC, Michel JB, Angles-Cano E. Protease nexin-1 inhibits plasminogen activation-induced apoptosis of adherent cells. J Biol Chem. 2004;279:10346–56.CrossRefGoogle Scholar
  40. 40.
    Tsai TT, Fattori R, Trimarchi S, Isselbacher E, Myrmel T, Evangelista A, Hutchison S, et al. Long-term survival in patients presenting with type B acute aortic dissection: insights from the international registry of acute aortic dissection. Circulation. 2006;114:2226–31.CrossRefGoogle Scholar
  41. 41.
    Sakalihasan N, Nienaber CA, Hustinx R, Lovinfosse P, El Hachemi M, Cheramy-Bien JP, Seidel L, et al. (Tissue PET) Vascular metabolic imaging and peripheral plasma biomarkers in the evolution of chronic aortic dissections. Eur Heart J Cardiovasc Imaging. 2015;16:626–33.CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Austria, part of Springer Nature 2019

Authors and Affiliations

  • Giuseppina Caligiuri
    • 1
    • 2
    Email author
  • Bernard P. Levy
    • 3
  • Antonino Nicoletti
    • 4
    • 2
  • Jean-Baptiste Michel
    • 2
  1. 1.Cardiology DepartmentUniversity Hospital Xavier BichatParisFrance
  2. 2.Inserm U1148ParisFrance
  3. 3.Vessels and Blood InstituteParis-Centre de Recherche Cardiovasculaire (PARCC)ParisFrance
  4. 4.Department of ImmunologyUniversity Paris DiderotParisFrance

Personalised recommendations