Skip to main content
SpringerLink
Log in

Segmental differences in the orientation of smooth muscle cells in the tunica media of porcine aortae

  • Original Paper
  • Published:
Biomechanics and Modeling in Mechanobiology Aims and scope Submit manuscript

Abstract

The orientation of vascular smooth muscle cells of porcine aortae was assessed to test the widely accepted assumption that these smooth muscle cells are arranged in two helices. We used tangential histological sections of 82 samples of five anatomical segments of thoracic and abdominal porcine aortae and three age groups in animals ranging in age from 5 to 210 days. The distribution of the orientation of smooth muscle cell nuclei in five proximodistal segments of the porcine aortae was determined using an algorithm that fitted a mixture of one to five von Mises probability distributions of the data retrieved from histological micrographs. Automated tracking of the nuclei was confirmed by and consistent with manual histological analysis. The orientation of the vascular smooth muscle cells was successfully fitted using two von Mises distributions in most of the samples with different ages, wall thicknesses, and anatomical positions, which corresponds to two populations of vascular smooth muscle cells. A minor fraction of samples also required a tertiary von Mises distribution to describe the orientation of the smooth muscle cell nuclei. The distribution of vascular smooth muscle cells in five aortic segments ranging from the thoracic ascending aorta to the abdominal intrarenal aorta exhibited similar main directions but different shapes. These results are consistent with the widely used model of two muscular helices intermingling in the arterial wall. Furthermore, we calculated the central angles of symmetry and the mean value of angles between the two assumed smooth muscle directions. We also successfully approximated the orientation of the smooth muscle cells using a mixture of von Mises distributions and our open-source software named dist_mixtures. This method is openly available to researchers who are interested in mathematically assessing the orientation of cell nuclei in various tissues.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  • Agrawal V, Kollimada SA, Byju AG, Gundiah N (2013) Regional variations in the nonlinearity and anisotropy of bovine aortic elastin. Biomech Model Mechanobiol 12:1181–1194

    Article  Google Scholar 

  • Akaike H (1980) Likelihood and the Bayes procedure. In: Bernardo JM et al (eds) Bayesian statistics. University Press, Valencia, pp 143–166

    Google Scholar 

  • Cabrera-Fischer EI, Bia D, Zócalo Y, Wray S, Armentano R (2013) The adventitia layer modulates the arterial wall elastic response to intra-aortic counterpulsation: in vivo studies. Artif Organs 37:1041–1048

  • Casas-Carrillo E, Prill-Adams A, Price SG, Clutter AC, Kirkpatrick BW (1997) Mapping genomic regions associated with growth rate in pigs. J Anim Sci 75:2047–2053

    Google Scholar 

  • Cimrman R (2013) Dist\_mixtures. https://github.com/rc/dist_mixtures. Accessed 4 Feb 2014

  • Chen H, Luo T, Zhao X, Lu X, Huo Y, Kassab GS (2013) Microstructural constitutive model of active coronary media. Biomaterials 34:7575–7583

    Article  Google Scholar 

  • Cheng JK, Stoilov I, Mecham RP, Wagenseil JE (2013) A fiber-based constitutive model predicts changes in amount and organization of matrix proteins with development and disease in the mouse aorta. Biomech Model Mechanobiol 12:497–510

    Article  Google Scholar 

  • Driessen NJ, Wilson W, Bouten CV, Baaijens FP (2004) A computational model for collagen fibre remodelling in the arterial wall. J Theor Biol 226:53–64

    Article  Google Scholar 

  • Dziodzio T, Juraszek A, Reineke D, Jenni H, Zermatten E, Zimpfer D, Stoiber M, Scheikl V, Schima H, Grimm M, Czerny M (2011) Experimental acute type B aortic dissection: different sites of primary entry tears cause different ways of propagation. Ann Thorac Surg 91:724–727

    Article  Google Scholar 

  • Fischer EC, Santana DB, Zócalo Y, Camus J, de Forteza E, Armentano R (2010) Effects of removing the adventitia on the mechanical properties of ovine femoral arteries in vivo and in vitro. Circ J 74:1014–1022

    Article  Google Scholar 

  • Funder JA, Frost MW, Klaaborg KE, Wierup P, Hjortdal V, Nygaard H, Hasenkam JM (2012) Aortic root distensibility after subcoronary stentless valve implantation. J Heart Valve Dis 21:181–188

    Google Scholar 

  • Gabner S, Tonar Z, Tichy A, Saalmüller A, Worliczek HL, Joachim A, Witter K (2012) Immunohistochemical detection and quantification of T cells in the small intestine of Isospora suis-infected piglets-influence of fixation technique and intestinal segment. Microsc Res Tech 75:408–415

    Article  Google Scholar 

  • Gasser TC, Ogden RW, Holzapfel GA (2006) Hyperelastic modelling of arterial layers with distributed collagen fibre orientations. J R Soc Interface 22:15–35

    Article  Google Scholar 

  • Haskett D, Johnson G, Zhou A, Utzinger U, Vande Geest J (2010) Microstructural and biomechanical alterations of the human aorta as a function of age and location. Biomech Model Mechanobiol 9:725–736

    Article  Google Scholar 

  • Hemmasizadeh A, Autieri M, Darvish K (2012) Material properties of different layers of aorta. In: 38th Annual Northeast Bioengineering Conference, NEBEC 2012, Art. no. 6207033, pp 201–202

  • Holzapfel GA (2006) Determination of material models for arterial walls from uniaxial extension tests and histological structure. J Theor Biol 238:290–302

    Article  MathSciNet  Google Scholar 

  • Holzapfel GA, Gasser TC (2001) A viscoelastic model for fiber-reinforced composites at finite strains: continuum basis, computational aspects and applications. Comput Methods Appl Mech 190:4379–4403

    Article  Google Scholar 

  • Holzapfel GA, Ogden RW (2010) Modelling the layer-specific three-dimensional residual stresses in arteries, with an application to the human aorta. J R Soc Interface 7:787–799

    Article  Google Scholar 

  • Holzapfel GA, Gasser TC, Stadler M (2002) A structural model for the viscoelastic behavior of arterial walls: continuum formulation and finite element analysis. Eur J Mech A Solids 21:441–463

    Article  MATH  Google Scholar 

  • Horný L, Netušil M, Voňavková T (2014) Axial prestretch and circumferential distensibility in biomechanics of abdominal aorta. Biomech Model Mechanobiol 13:783–799. doi:10.1007/s10237-013-0534-8

  • Houdek K, Moláček J, Třeška V, Křížková V, Eberlová L, Boudová L, Nedorost L, Tolinger P, Kočová J, Kobr J, Baxa J, Liška V, Witter K, Tonar Z (2013) Focal histopathological progression of porcine experimental abdominal aortic aneurysm is mitigated by atorvastatin. Int Angiol 32:291–306

    Google Scholar 

  • Humphrey JD, Holzapfel GA (2012) Mechanics, mechanobiology, and modeling of human abdominal aorta and aneurysms. J Biomech 45:805–814

    Article  Google Scholar 

  • Jirkovská M, Kučera T, Kaláb J, Jadrníček M, Niedobová V, Janáček J, Kubínová L, Moravcová M, Zižka Z, Krejčí V (2012) The branching pattern of villous capillaries and structural changes of placental terminal villi in type 1 diabetes mellitus. Placenta 33:343–351

    Article  Google Scholar 

  • Johnson JJ, Jacocks MA, Gauthier SC, Irwin DA, Wolf RF, Garwe T, Lerner MR, Lees JS (2013) Establishing a swine model to compare vascular prostheses in a contaminated field. J Surg Res 181:355–358

    Article  Google Scholar 

  • Kim J, Baek S (2011) Circumferential variations of mechanical behavior of the porcine thoracic aorta during the inflation test. J Biomech 44:1941–1947

    Article  Google Scholar 

  • Kim J, Peruski B, Hunley C, Kwon S, Baek S (2013) Influence of surrounding tissues on biomechanics of aortic wall. Int J Exp Comput Biomech 2:105–117

    Article  Google Scholar 

  • Kochová P, Cimrman R, Janáček J, Witter K, Tonar Z (2011) How to asses, visualize and compare the anisotropy of linear structures reconstructed from optical sections—a study based on histopathological quantification of human brain microvessels. J Theor Biol 286:67–78

    Article  Google Scholar 

  • Kochová P, Kuncová J, Svíglerová J, Cimrman R, Miklíková M, Liška V, Tonar Z (2012) The contribution of vascular smooth muscle, elastin and collagen on the passive mechanics of porcine carotid arteries. Physiol Meas 33:1335–1351

    Article  Google Scholar 

  • Lanir Y (1983) Constitutive equations for fibrous connective tissue. J Biomech 16:1–12

    Article  Google Scholar 

  • Lillie MA, Armstrong TE, Gérard SG, Shadwick RE, Gosline JM (2012) Contribution of elastin and collagen to the inflation response of the pig thoracic aorta: assessing elastin’s role in mechanical homeostasis. J Biomech 45:2133–2141

    Article  Google Scholar 

  • Martufi G, Gasser TC, Appoo JJ, Di Martino ES (2014) Mechano-biology in the thoracic aortic aneurysm: a review and case study. Biomech Model Mechanobiol. doi:10.1007/s10237-014-0557-9

  • Mayersbach H (1956) Der Wandbau der Gefäßübergangsstrecken zwischen Arterien rein elastischen und rein muskulösen Typs. Anat Anz 102:333–360

    Google Scholar 

  • McLaren CE, Legler JM, Brittenham GM (1994) The generalized chi-square goodness-of-fit test. J R Stat Soc Ser D Stat 43:247–258

    Google Scholar 

  • McPherson RL, Ji F, Wu G, Blanton JR Jr, Kim SW (2004) Growth and compositional changes of fetal tissues in pigs. J Anim Sci 82:2534–2540

    Google Scholar 

  • Molácek J, Treska V, Kobr J, Certík B, Skalický T, Kuntscher V, Krízková V (2009) Optimization of the model of abdominal aortic aneurysm-experiment in an animal model. J Vasc Res 46:1–5

    Google Scholar 

  • Nickel R, Schummer A, Seiferle E (1996) Lehrbuch der Anatomie der Haustiere. Band III Kreislaufsystem. Haut und Hauotgane, 3rd edn. Parey Buchverlag, Berlin

  • Okuno T, Yamaguchi M, Okada T, Takahashi T, Sakamoto N, Ueshima E, Sugimura K, Sugimoto K (2012) Endovascular creation of aortic dissection in a swine model with technical considerations. J Vasc Surg 55:1410–1418

    Article  Google Scholar 

  • Ondrovics M, Silbermayr K, Mitreva M, Young ND, Razzazi-Fazeli E, Gasser RB, Joachim A (2013) Proteomic analysis of Oesophagostomum dentatum (Nematoda) during larval transition, and the effects of hydrolase inhibitors on development. PLoS ONE 8, Art. no. e63955

  • Reeps C, Maier A, Pelisek J, Härtl F, Grabher-Meier V, Wall WA, Essler M, Eckstein HH, Gee MW (2013) Measuring and modeling patient-specific distributions of material properties in abdominal aortic aneurysm wall. Biomech Model Mechanobiol 12:717– 733

    Article  Google Scholar 

  • Rezakhaniha R, Agianniotis A, Schrauwen JT, Griffa A, Sage D, Bouten CV, van de Vosse FN, Unser M, Stergiopulos N (2012) Experimental investigation of collagen waviness and orientation in the arterial adventitia using confocal laser scanning microscopy. Biomech Model Mechanobiol 11:461–473

    Article  Google Scholar 

  • Rizzoni D, Aalkjaer C, De Ciuceis C, Porteri E, Rossini C, Rosei CA, Sarkar A, Rosei EA (2011) How to assess microvascular structure in humans. High Blood Press Cardiovasc Prev 18:169–177

    Article  Google Scholar 

  • Roccabianca S, Ateshian GA, Humphrey JD (2014) Biomechanical roles of medial pooling of glycosaminoglycans in thoracic aortic dissection. Biomech Model Mechanobiol 13:13–25

    Article  Google Scholar 

  • Romeis B (1989) Mikroskopische Technik. Urban & Schwarzenberg, München

    Google Scholar 

  • Ruckman JL, Luvalle PA, Hill KE, Giro MG, Davidson JM (1994) Phenotypic stability and variation in cells of the porcine aorta: collagen and elastin production. Matrix Biol 14:135–145

    Article  Google Scholar 

  • Saari P, Lähteenvuo M, Honkonen K, Manninen H (2012) Antegrade in situ fenestration of aortic stent graft: in-vivo experiments using a pig model. Acta Radiol 53:754–758

    Article  Google Scholar 

  • Sarda-Mantel L, Alsac JM, Boisgard R, Hervatin F, Montravers F, Tavitian B, Michel JB, Le Guludec D (2012) Comparison of 18F-fluoro-deoxy-glucose, 18F-fluoro-methyl-choline, and 18F-DPA714 for positron-emission tomography imaging of leukocyte accumulation in the aortic wall of experimental abdominal aneurysms. J Vasc Surg 56:765–773

    Article  Google Scholar 

  • Schneider CA, Rasband WS, Eliceiri KW (2012) NIH Image to ImageJ: 25 years of image analysis. Nat Methods 9:671–675

    Article  Google Scholar 

  • Schriefl AJ, Zeindlinger G, Pierce DM, Regitnig P, Holzapfel GA (2012a) Determination of the layer-specific distributed collagen fibre orientations in human thoracic and abdominal aortas and common iliac arteries. J R Soc Interface 9:1275–1286

    Article  Google Scholar 

  • Schriefl AJ, Reinisch AJ, Sankaran S, Pierce DM, Holzapfel GA (2012b) Quantitative assessment of collagen fibre orientations from two-dimensional images of soft biological tissues. J R Soc Interface 9:3081–3093

    Article  Google Scholar 

  • Schriefl AJ, Wolinski H, Regitnig P, Kohlwein SD, Holzapfel GA (2012c) An automated approach for three-dimensional quantification of fibrillar structures in optically cleared soft biological tissues. J R Soc Interface 10:20120760

    Article  Google Scholar 

  • Schwarz GE (1978) Estimating the dimension of a model. Ann Stat 6:461–464

    Article  MATH  Google Scholar 

  • Shadwick RE (1999) Mechanical design in arteries. J Exp Biol 202:3305–3313

    Google Scholar 

  • Sokolis DP, Boudoulas H, Karayannacos PE (2008) Segmental differences of aortic function and composition: clinical implications. Hellenic J Cardiol 49:145–154

    Google Scholar 

  • Strathe AB, Sorensen H, Danfaer A (2009) A new mathematical model for combining growth and energy intake in animals: the case of the growing pig. J Theor Biol 261:165–175

    Article  Google Scholar 

  • The Statsmodels Development Team (2013) Statsmodels. http://statsmodels.sourceforge.net/. Accessed 4 Feb 2014

  • Thorne BC, Hayenga HN, Humphrey JD, Peirce SM (2011) Toward a multi-scale computational model of arterial adaptation in hypertension: verification of a multi-cell agent based model. Front Physiol 2:20

    Article  Google Scholar 

  • Tremblay D, Cartier R, Mongrain R, Leask RL (2010) Regional dependency of the vascular smooth muscle cell contribution to the mechanical properties of the pig ascending aortic tissue. J Biomech 43:2448–2451

    Article  Google Scholar 

  • Valentin A, Holzapfel GA (2012) Constrained mixture models as tools for testing competing hypotheses in arterial biomechanics: a brief survey. Mech Res Commun 42:126–133

    Article  Google Scholar 

  • Vallet JL, Freking BA (2006) Changes in fetal organ weights during gestation after selection for ovulation rate and uterine capacity in swine. J Anim Sci 84:2338–2345

    Article  Google Scholar 

  • van Essen GJ, Vernooij JC, Heesterbeek JA, Anjema D, Merkus D, Duncker DJ (2011) Cardiovascular performance of adult breeding sows fails to obey allometric scaling laws. J Anim Sci 89:376–382

    Article  Google Scholar 

  • Wales DJ, Doye JPK (1997) Global optimization by basin-hopping and the lowest energy structures of Lennard-Jones clusters containing up to 110 atoms. J Phys Chem A 101:5111–5116

    Article  Google Scholar 

  • Weisbecker H, Pierce DM, Regitnig P, Holzapfel GA (2012) Layer-specific damage experiments and modeling of human thoracic and abdominal aortas with non-atherosclerotic intimal thickening. J Mech Behav Biomed Mater 12:93–106

  • Wilson JS, Baek S, Humphrey JD (2012) Importance of initial aortic properties on the evolving regional anisotropy, stiffness and wall thickness of human abdominal aortic aneurysms. J R Soc Interface 9:2047–2058

    Article  Google Scholar 

  • Wilson JS, Baek S, Humphrey JD (2013) Parametric study of effects of collagen turnover on the natural history of abdominal aortic aneurysms. Proc Math Phys Eng Sci 469:20120556

    Article  MathSciNet  Google Scholar 

  • Witter K, Tonar Z, MatejkaVM Martinca T, Jonák J, Rokosný S, Pirk J (2010) Tissue reaction to three different types of tissue glues in an experimental aorta dissection model: a quantitative approach. Histochem Cell Biol 133:241–259

    Article  Google Scholar 

  • Worliczek HL, Buggelsheim M, Alexandrowicz R, Witter K, Schmidt P, Gerner W, Saalmüller A, Joachim A (2010) Changes in lymphocyte populations in suckling piglets during primary infections with Isospora suis. Parasite Immunol 32:232–244

    Article  Google Scholar 

Download references

Acknowledgments

The study was supported by the ERDF project “NTIS - New Technologies for Information Society,” European Centre of Excellence, CZ.1.05/1.1.00/02.0090. The authors also received support from the project CENTEM No. CZ.1.05/2.1.00/03.0088, which was cofounded by the ERDF within the OP RDI program of the Ministry of Education, Youth, and Sports. We would like to thank Ms. Brigitte Machac and Dr. Simone Gabner for their valuable help during the collection and histological processing of the tissue samples.

Author information

Authors and Affiliations

  1. NTIS, European Centre of Excellence, Faculty of Applied Sciences, University of West Bohemia, Univerzitní 22, 306 14 , Plzeň, Czech Republic

    Zbynek Tonar & Petra Kochova

  2. New Technologies - Research Centre, University of West Bohemia, Univerzitní 8, 306 14 , Plzeň, Czech Republic

    Robert Cimrman

  3. 156 Avenue Willowdale, Outremont, QC, H3T1E9, Canada

    Josef Perktold

  4. Department of Pathobiology, Institute of Anatomy, Histology and Embryology, University of Veterinary Medicine Vienna, Veterinärplatz 1, 1210 , Vienna, Austria

    Kirsti Witter

Authors
  1. Zbynek Tonar
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Petra Kochova
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Robert Cimrman
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Josef Perktold
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Kirsti Witter
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Zbynek Tonar.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Tonar, Z., Kochova, P., Cimrman, R. et al. Segmental differences in the orientation of smooth muscle cells in the tunica media of porcine aortae. Biomech Model Mechanobiol 14, 315–332 (2015). https://doi.org/10.1007/s10237-014-0605-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10237-014-0605-5

Keywords

Search

Navigation