Opposing changes in thoracic and abdominal aortic biomechanical properties in rodent models of vascular calcification and hypertension

American Journal of Physiology - Heart and Circulatory Physiology

Volumn 307, Issue 2, 2014, Pages

  Ameer, Omar Z ^a   Salman, Ibrahim M ^a   Avolio, Alberto P ^a   Phillips, Jacqueline K ^a   Butlin, Mark ^a  

^a MACQUARIE UNIVERSITY   (Australia)

Author keywords

Aortic stiffness; Calcification; Elastin fragmentation; Hypertension; Regional changes

Indexed keywords

CALCIUM; COLECALCIFEROL; COLLAGEN; ELASTIN; NICOTINE;

ABDOMINAL AORTA; ANIMAL EXPERIMENT; ANIMAL MODEL; AORTA; AORTA DISEASE; AORTIC REMODELING; ARTERIAL STIFFNESS; ARTERIAL WALL THICKNESS; ARTICLE; BIOMECHANICS; BLOOD PRESSURE; BLOOD VESSEL CALCIFICATION; CHRONIC KIDNEY DISEASE; CONTROLLED STUDY; ELASTICITY; ENERGY ABSORPTION; FEMALE; HEART HEMODYNAMICS; HISTOLOGY; HYPERTENSION; KIDNEY POLYCYSTIC DISEASE; MALE; MORPHOMETRICS; NONHUMAN; PRIORITY JOURNAL; PROXIMAL AORTA; RAT; RODENT MODEL; SPONTANEOUSLY HYPERTENSIVE RAT; STRESS STRAIN RELATIONSHIP; TENSILE STRENGTH; THORACIC AORTA;

AORTIC STIFFNESS; CALCIFICATION; ELASTIN FRAGMENTATION; HYPERTENSION; REGIONAL CHANGES;

ANIMALS; AORTA, ABDOMINAL; AORTA, THORACIC; BIOMECHANICAL PHENOMENA; CHOLECALCIFEROL; COLLAGEN; DISEASE MODELS, ANIMAL; ELASTIN; FEMALE; HEMODYNAMICS; HYPERTENSION; MALE; OXAZINES; RATS; RATS, INBRED LEW; RATS, INBRED SHR; RATS, INBRED WKY; RENAL INSUFFICIENCY, CHRONIC; TENSILE STRENGTH; VASCULAR CALCIFICATION; VASCULAR STIFFNESS;

EID: 84904312022     PISSN: 03636135     EISSN: 15221539     Source Type: Journal    
DOI: 10.1152/ajpheart.00139.2014     Document Type: Article

References (60)

1. Abdelbaky A, Corsini E, Figueroa AL, Fontanez S, Subramanian S, Ferencik M, Brady TJ, Hoffmann U, Tawakol A. Focal arterial inflammation precedes subsequent calcification in the same location: a longitudinal FDG-PET/CT study. Circ Cardiovasc Imaging 6: 747-754, 2013.
2. Aikawa E, Aikawa M, Libby P, Figueiredo JL, Rusanescu G, Iwamoto Y, Fukuda D, Kohler RH, Shi GP, Jaffer FA, Weissleder R. Arterial and aortic valve calcification abolished by elastolytic cathepsin S deficiency in chronic renal disease. Circulation 119: 1785-1794, 2009.
3. Assoul N, Flaud P, Chaouat M, Letourneur D, Bataille I. Mechanical properties of rat thoracic and abdominal aortas. J Biomech 41: 2227-2236, 2008.
4. 3 plus nicotine diminishes arterial distensibility in rats. Am J Physiol Heart Circ Physiol 266: H540-H547, 1994.
5. Atkinson J. Age-related medial elastocalcinosis in arteries: mechanisms, animal models, and physiological consequences. J Appl Physiol 105: 1643-1651, 2008.
6. Bergel D. The static elastic properties of the arterial wall. J Physiol 156: 445-457, 1961.
7. Berry CL, Greenwald SE. Effects of hypertension on the static mechanical properties and chemical composition of the rat aorta. Cardiovasc Res 10: 437-451, 1976.
8. Bézie Y, Lacolley P, Laurent S, Gabella G. Connection of smooth muscle cells to elastic lamellae in aorta of spontaneously hypertensive rats. Hypertension 32: 166-169, 1998.
9. Bézie Y, Lamazière JM, Laurent S, Challande P, Cunha RS, Bonnet J, Lacolley P. Fibronectin expression and aortic wall elastic modulus in spontaneously hypertensive rats. Arterioscler Thromb Vasc Biol 18: 1027-1034, 1998.
10. Boutouyrie P, Laurent S, Benetos A, Girerd XJ, Hoeks AP, Safar ME. Opposing effects of ageing on distal and proximal large arteries in hypertensives. J Hypertens Suppl 10: S87-S91, 1992.
11. Brüel A, Oxlund H, Brüel A. Changes in biomechanical properties, composition of collagen and elastin, and advanced glycation endproducts of the rat aorta in relation to age. Atherosclerosis 127: 155-165, 1996.
12. Cantini C, Kieffer P, Corman B, Limiñana P, Atkinson J, Lartaud-Idjouadiene I, Liminana P. Aminoguanidine and aortic wall mechanics, structure, and composition in aged rats. Hypertension 38: 943-948, 2001.
13. Cavalcante JL, Lima JAC, Redheuil A, Al-Mallah MH. Aortic stiffness: current understanding and future directions. J Am Coll Cardiol 57: 1511-1522, 2011.
14. Chirinos JA, Segers P. Noninvasive evaluation of left ventricular afterload: part 1: pressure and flow measurements and basic principles of wave conduction and reflection. Hypertension 56: 555-562, 2010.
15. Chirinos JA. Arterial stiffness: basic concepts and measurement techniques. J Cardiol 5: 243-255, 2012.
16. Dao HH, Essalihi R, Bouvet C, Moreau P. Evolution and modulation of age-related medial elastocalcinosis: impact on large artery stiffness and isolated systolic hypertension. Cardiovasc Res 66: 307-317, 2005.
17. Dart A, Silagy C, Dewar E, Jennings G, McNeil J. Aortic distensibility and left ventricular structure and function in isolated systolic hypertension. Eur Heart J 14: 1465-1470, 1993.
18. Greenwald S. Ageing of the conduit arteries. J Pathol 211: 157-172, 2007.
19. Han W, Chen J, Wu L, Zhu D, Gao P. Different biomechanical properties of medial and adventitial layers of thoracic aorta in Wistar-Kyoto and spontaneously hypertensive rats. Acta Pharmacol Sin 31: 1319-1323, 2010.
20. Haskett D, Johnson G, Zhou A, Utzinger U, Vande Geest J. Microstructural and biomechanical alterations of the human aorta as a function of age and location. Biomech Model Mechanobiol 9: 725-736, 2010.
21. Head RJ. Hypernoradrenergic innervation: its relationship to functional and hyperplastic changes in the vasculature of the spontaneously hypertensive rat. Blood Vessels 26: 1-20, 1989.
22. Hickson SS, Butlin M, Graves M, Taviani V, Avolio AP, McEniery CM, Wilkinson IB. The relationship of age with regional aortic stiffness and diameter. JACC Cardiovasc Imaging 3: 1247-1255, 2010.
23. Jegger D, Silva da R, Jeanrenaud X, Nasratullah M, Tevaearai H, Segesser von LK, Segers P, Gaillard V, Atkinson J, Lartaud I, Stergiopulo N, et al. Ventricular-arterial coupling in a rat model of reduced arterial compliance provoked by hypervitaminosis D and nicotine. Am J Physiol Heart Circ Physiol 291: H1942-H1951, 2006.
24. Judy WV, Watanabe AM, Henry DP, Besch H Jr, Murphy WR, Hockel GM. Sympathetic nerve activity: role in regulation of blood pressure in the spontaenously hypertensive rat. Circ Res 38: 21-29, 1976.
25. Kanemaru K, Seya K, Miki I, Motomura S, Furukawa KI. Calcification of aortic smooth muscle cells isolated from spontaneously hypertensive rats. J Pharmacol Sci 106: 280-286, 2008.
26. Kieffer P, Robert A, Capdeville-Atkinson C, Atkinson J, Lartaud-Idjouadiene I. Age-related arterial calcification in rats. Life Sci 66: 2371-2381, 2000.
27. Konishi M, Su C. Role of endothelium in dilator responses of spontaneously hypertensive rat arteries. Hypertension 5: 881-886, 1983.
28. Lakatta EG. Arterial aging is risky. J Appl Physiol 105: 1321-1322, 2008.
29. Latham RD, Westerhof N, Sipkema P, Rubal BJ, Reuderink P, Murgo JP. Regional wave travel and reflections along the human aorta: a study with six simultaneous micromanometric pressures. Circulation 72: 1257-1269, 1985.
30. Liu J, Ormsby A, Oja-Tebbe N, Pagano PJ. Gene transfer of NAD(P)H oxidase inhibitor to the vascular adventitia attenuates medial smooth muscle hypertrophy. Circ Res 95: 587-594, 2004.
31. London GM, Marchais SJ, Guérin AP, Métivier F. Arteriosclerosis, vascular calcifications and cardiovascular disease in uremia. Curr Opin Nephrol Hypertens 14: 525-531, 2005.
32. Marque V, Kieffer P, Atkinson J, Lartaud-Idjouadiene I. Elastic properties and composition of the aortic wall in old spontaneously hypertensive rats. Hypertension 34: 415-422, 1999.
33. McCooke JK, Appels R, Barrero RA, Ding A, Ozimek-Kulik JE, Bellgard MI, Morahan G, Phillips JK. A novel mutation causing nephronophthisis in the Lewis polycystic kidney rat localises to a conserved RCC1 domain in Nek8. BMC Genomics 13: 393, 2012.
34. McEniery CM, McDonnell BJ, So A, Aitken S, Bolton CE, Munnery M, Hickson SS, Yasmin Maki-Petaja KM, Cockcroft JR, Dixon AK, Wilkinson IB. Aortic calcification is associated with aortic stiffness and isolated systolic hypertension in healthy individuals. Hypertension 53: 524-531, 2009.
35. McNulty M, Mahmud A, Feely J. Advanced glycation end-products and arterial stiffness in hypertension. Am J Hypertens 20: 242-247, 2007.
36. Meema HE, Oreopoulos DG. Morphology, progression, and regression of arterial and periarterial calcifications in patients with end-stage renal disease. Radiology 158: 671-677, 1986.
37. Mitchell GF, Hwang SJ, Vasan RS, Larson MG, Pencina MJ, Hamburg NM, Vita JA, Levy D, Benjamin EJ. Arterial stiffness and cardiovascular events: the Framingham Heart Study. Circulation 121: 505-511, 2010.
38. Moe SM, Chen NX. Mechanisms of vascular calcification in chronic kidney disease. J Am Soc Nephrol 19: 213-216, 2008.
39. Ng K, Butlin M, Avolio AP. Persistent effect of early, brief angiotensinconverting enzyme inhibition on segmental pressure dependency of aortic stiffness in spontaneously hypertensive rats. J Hypertens 30: 1782-1790, 2012.
40. Ng K, Hildreth CM, Phillips JK, Avolio AP. Aortic stiffness is associated with vascular calcification and remodelling in a chronic kidney disease rat model. Am J Physiol Renal Physiol 300: F1431-F1436, 2011.
41. 3 plus nicotine. J Vasc Res 34: 386-98, 1997.
42. Niederhoffer N, Lartaud-Idjouadiene I, Giummelly P, Duvivier C, Peslin R, Atkinson J. Calcification of medial elastic fibers and aortic elasticity. Hypertension 29: 999-1006, 1997.
43. O'Rourke MF, Safar ME. Relationship between aortic stiffening and microvascular disease in brain and kidney: cause and logic of therapy. Hypertension 46: 200-204, 2005.
44. Pfeffer MA, Pfeffer JM, Frohlich ED. Pumping ability of the hypertrophying left ventricle of the spontaneously hypertensive rat. Circ Res 38: 423-429, 1976.
45. Phillips JK, Hopwood D, Loxley RA, Ghatora K, Coombes JD, Tan YS, Harrison JL, McKitrick DJ, Holobotvskyy V, Arnolda LF, Rangan GK. Temporal relationship between renal cyst development, hypertension and cardiac hypertrophy in a new rat model of autosomal recessive polycystic kidney disease. Kidney Blood Press Res 30: 129-144, 2007.
46. Quinn U, Tomlinson LA, Cockcroft JR. Arterial stiffness. JRSM Cardiovasc Dis 1: 1-8, 2012.
47. 18F-FDG uptake and calcification in health-screening subjects. Ann Nucl Med 27: 239-246, 2013.
48. Safar ME, Levy BI, Struijker-Boudier H. Current perspectives on arterial stiffness and pulse pressure in hypertension and cardiovascular diseases. Circulation 107: 2864-2869, 2003.
49. Salman IM, Hildreth CM, Ameer OZ, Phillips JK. Differential contribution of afferent and central pathways to the development of baroreflex dysfunction in chronic kidney disease. Hypertension 63: 804-810, 2013.
50. Schulze-Bauer CAJ, Regitnig P, Holzapfel GA. Mechanics of the human femoral adventitia including the high-pressure response. Am J Physiol Heart Circ Physiol 282: H2427-H2440, 2002.
51. Smith ER, Tomlinson LA, Ford ML, McMahon LP, Rajkumar C, Holt SG. Elastin degradation is associated with progressive aortic stiffening and all-cause mortality in predialysis chronic kidney disease. Hypertension 59: 973-978, 2012.
52. Sokolis DP, Boudoulas H, Karayannacos PE. Assessment of the aortic stress-strain relation in uniaxial tension. J Biomech 35: 1213-1223, 2002.
53. Sokolis DP, Boudoulas H, Karayannacos PE. Segmental differences of aortic function and composition: clinical implications. Hellenic J Cardiol 49: 145-154, 2008.
54. Stenmark KR, Yeager ME, El Kasmi KC, Nozik-Grayck E, Gerasimovskaya EV, Li M, Riddle SR, Frid MG. The adventitia: essential regulator of vascular wall structure and function. Annu Rev Physiol 75: 23-47, 2013.
55. Tatchum-Talom R, Niederhoffer N, Amin F, Makki T, Tankosic P, Atkinson J. Aortic stiffness and left ventricular mass in a rat model of isolated systolic hypertension. Hypertension 26: 963-970, 1995.
56. Vermeersch SJ, Rietzschel ER, De Buyzere ML, De Bacquer D, De Backer G, Van Bortel LM, Gillebert TC, Verdonck PR, Segers P. Determining carotid artery pressure from scaled diameter waveforms: comparison and validation of calibration techniques in 2026 subjects. Physiol Meas 29: 1267-1280, 2008.
57. Wallin R, Wajih N, Greenwood GT, Sane DC. Arterial calcification: a review of mechanisms, animal models, and the prospects for therapy. Med Res Rev 21: 274-301, 2001.
58. Wang Y, Zhang Z, Chen X, Wang X, Cao H, Liu S. Advanced glycation end products promote human aortic smooth muscle cell calcification in vitro via activating NF-B and down-regulating IGF1R expression. Acta Pharmacol Sin 34: 480-486, 2013.
59. Wilson PW, Kauppila LI, O'Donnell CJ, Kiel DP, Hannan M, Polak JM, Cupples LA. Abdominal aortic calcific deposits are an important predictor of vascular morbidity and mortality. Circulation 103: 1529-1534, 2001.
60. Zhao J, Day J, Yuan ZF, Gregersen H. Regional arterial stress-strain distributions referenced to the zero-stress state in the rat. Am J Physiol Heart Circ Physiol 282: H622-H629, 2002.