Pathological changes of Aortic Valve Calcification in Experimental Animal Models

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Published Aug 19, 2022
https://doi.org/10.70436/nuijb.v1i01.7
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Vol. 1 No. 01 (2022): August

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Abdul Ghafar Sherzad
Khalil Ahmad Behsodwal
Mohammad Azim Azimee
Muhibullah Shinwari
Imran Zafarzai
Shafiullah Zaheer
Nemat Arash
Alsarhan Osama
Qingchun Zeng

Abstract

Calcific Aortic Valve Disease (CAVD) is a sluggish and progressive disease that comprises “early sclerosis, characterized by leaflet thickening without left ventricular outflow obstruction, to late stenosis with stiffened leaflets, obstructed flow and compromised cardiac function”. CAVD was formerly believed to afflict the tricuspid or congenitally bicuspid aortic valve and be a passive, senile, or degenerative disorder. However, recent investigations have demonstrated that this is a pathobiological activity that is active and heavily cell-mediated, which shares several risk factors with atherosclerosis. Numerous studies show that CAVD are not a normal aspect of aging and may be linked to certain risk factors. Nevertheless, no pharmacological therapy available to halt or arrest the development of CAVD in a clinically relevant way, and surgery is the only effective treatment option. As a result, there is an urgent scientific need to determine pathobiological mechanism of CAVD and to find new ways to treat CAVD. Animal models are developing as crucial instruments to this aim, assisted by the development of new models and greater knowledge of the efficacy of old models. In this review paper, we will present the most extensively utilized large and small animal models that were used to explore CAVD.

Keywords

Calcific aortic valve diseases, Aortic valve calcification, Aortic valve stenosis, Atherosclerosis, Experimental Animal Models

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How to Cite
Sherzad, A. G., Behsodwal, K. A., Azimee, M. A., Shinwari, M., Zafarzai, I., Zaheer, S., Arash, N., Osama, A., & Zeng, Q. (2022). Pathological changes of Aortic Valve Calcification in Experimental Animal Models. Nangarhar University International Journal of Biosciences, 1(01), 37–60. https://doi.org/10.70436/nuijb.v1i01.7

References

  1. Agarwala, A., Billheimer, J., & Rader, D. J. (2013). Mighty minipig in fight against cardiovascular disease. Science translational medicine, 5(166), 166fs161-166fs161.
  2. Aicher, D., Urbich, C., Zeiher, A., Dimmeler, S., & Schäfers, H.-J. (2007). Endothelial nitric oxide synthase in bicuspid aortic valve disease. The Annals of thoracic surgery, 83(4), 1290-1294.
  3. Akat, K., Kaden, J. J., Schmitz, F., Ewering, S., Anton, A., Klomfaß, S., . . . Ortlepp, J. R. (2010). Calcium metabolism in adults with severe aortic valve stenosis and preserved renal function. The American journal of cardiology, 105(6), 862-864.
  4. Alushi, B., Curini, L., Christopher, M. R., Grubitzch, H., Landmesser, U., Amedei, A., & Lauten, A. (2020). Calcific aortic valve disease-natural history and future therapeutic strategies. Frontiers in Pharmacology, 11, 685.
  5. Anselmo, W., Branchetti, E., Grau, J. B., Li, G., Ayoub, S., Lai, E. K., . . . Sacks, M. S. (2018). Porphyrin‐Based SOD Mimic MnTnBu OE‐2‐PyP5+ Inhibits Mechanisms of Aortic Valve Remodeling in Human and Murine Models of Aortic Valve Sclerosis. Journal of the American Heart Association, 7(20), e007861.
  6. Arishiro, K., Hoshiga, M., Negoro, N., Jin, D., Takai, S., Miyazaki, M., . . . Hanafusa, T. (2007). Angiotensin receptor-1 blocker inhibits atherosclerotic changes and endothelial disruption of the aortic valve in hypercholesterolemic rabbits. Journal of the American College of Cardiology, 49(13), 1482-1489.
  7. Barbeau, M. L., Klemp, K. F., Guyton, J. R., & Rogers, K. A. (1997). Dietary fish oil: influence on lesion regression in the porcine model of atherosclerosis. Arteriosclerosis, thrombosis, and vascular biology, 17(4), 688-694.
  8. Beaty, T., Prenger, V., Virgil, D., Lewis, B., Kwiterovich, P., & Bachorik, P. (1992). A genetic model for control of hypertriglyceridemia and apolipoprotein B levels in the Johns Hopkins colony of St. Thomas Hospital rabbits. Genetics, 132(4), 1095-1104.
  9. Bostick, B., Yue, Y., & Duan, D. (2011). Phenotyping cardiac gene therapy in mice. In Muscle Gene Therapy (pp. 91-104): Springer.
  10. Branchetti, E., Sainger, R., Poggio, P., Grau, J. B., Patterson-Fortin, J., Bavaria, J. E., . . . Levy, R. J. (2013). Antioxidant enzymes reduce DNA damage and early activation of valvular interstitial cells in aortic valve sclerosis. Arteriosclerosis, thrombosis, and vascular biology, 33(2), e66-e74.
  11. Brousseau, M. E., & Hoeg, J. M. (1999). Transgenic rabbits as models for atherosclerosis research. Journal of lipid research, 40(3), 365-375.
  12. Burnstock, G., & Aliev, G. (1998). Watanabe rabbits with heritable hypercholesterolaemia: a model of atherosclerosis. Histology and histopathology, 13(3), 797-817.
  13. Butcher, J. T., Mahler, G. J., & Hockaday, L. A. (2011). Aortic valve disease and treatment: the need for naturally engineered solutions. Advanced drug delivery reviews, 63(4-5), 242-268.
  14. Caira, F. C., Stock, S. R., Gleason, T. G., McGee, E. C., Huang, J., Bonow, R. O., . . . Rajamannan, N. M. (2006). Human degenerative valve disease is associated with up-regulation of low-density lipoprotein receptor-related protein 5 receptor-mediated bone formation. Journal of the American College of Cardiology, 47(8), 1707-1712.
  15. Chen, B., Bronson, R. T., Klaman, L. D., Hampton, T. G., Wang, J.-f., Green, P. J., . . . Neel, B. G. (2000). Mice mutant for Egfr and Shp2 have defective cardiac semilunar valvulogenesis. Nature genetics, 24(3), 296-299.
  16. Choi, S.-E., Jang, H.-J., Kang, Y., Jung, J. G., Han, S. J., Kim, H. J., . . . Lee, K.-W. (2010). Atherosclerosis induced by a high-fat diet is alleviated by lithium chloride via reduction of VCAM expression in ApoE-deficient mice. Vascular pharmacology, 53(5-6), 264-272.
  17. Chorro, F. J., Such-Belenguer, L., & López-Merino, V. (2009). Animal models of cardiovascular disease. Revista Española de Cardiología (English Edition), 62(1), 69-84.
  18. Cimini, M., Boughner, D. R., Ronald, J. A., Aldington, L., & Rogers, K. A. (2005). Development of aortic valve sclerosis in a rabbit model of atherosclerosis: an immunohistochemical and histological study. The Journal of heart valve disease, 14(3), 365-375.
  19. Cohen, D. J., Malave, D., Ghidoni, J. J., Iakovidis, P., Everett, M. M., You, S., . . . Boyan, B. D. (2004). Role of oral bacterial flora in calcific aortic stenosis: an animal model. The Annals of thoracic surgery, 77(2), 537-543.
  20. Davis, B. T., Wang, X.-J., Rohret, J. A., Struzynski, J. T., Merricks, E. P., Bellinger, D. A., . . . Rogers, C. S. (2014). Targeted disruption of LDLR causes hypercholesterolemia and atherosclerosis in Yucatan miniature pigs. PloS one, 9(4), e93457.
  21. Davis, H. R., Vesselinovitch, D., & Wissler, R. W. (1984). Reticuloendothelial system response to hyperlipidemia in rhesus and cynomolgus monkeys. Journal of leukocyte biology, 36(1), 63-80.
  22. De Smet, B., Van der Zande, J., Van Der Helm, Y., Kuntz, R., Borst, C., & Post, M. (1998). The atherosclerotic Yucatan animal model to study the arterial response after balloon angioplasty: the natural history of remodeling. Cardiovascular Research, 39(1), 224-232.
  23. Demer, L. L., & Tintut, Y. (2019). Heart valve calcification. In Principles of Heart Valve Engineering (pp. 307-319): Elsevier.
  24. Dixon, J. L., Stoops, J., Parker, J., Laughlin, M., Weisman, G., & Sturek, M. (1999). Dyslipidemia and vascular dysfunction in diabetic pigs fed an atherogenic diet. Arteriosclerosis, thrombosis, and vascular biology, 19(12), 2981-2992.
  25. Doevendans, P. A. (1995). Strategies for studying cardiovascular diseases in transgenic and gene-trageted mice. Strategies in transgenic animal science., 107-144.
  26. Drolet, M.-C., Arsenault, M., & Couet, J. (2003). Experimental aortic valve stenosis in rabbits. Journal of the American College of Cardiology, 41(7), 1211-1217.
  27. Drolet, M.-C., Couët, J., & Arsenault, M. (2008). Development of aortic valve sclerosis or stenosis in rabbits: role of cholesterol and calcium.
  28. Drolet, M.-C., Roussel, E., Deshaies, Y., Couet, J., & Arsenault, M. (2006). A high fat/high carbohydrate diet induces aortic valve disease in C57BL/6J mice. Journal of the American College of Cardiology, 47(4), 850-855.
  29. Dweck, M. R., Boon, N. A., & Newby, D. E. (2012). Calcific aortic stenosis: a disease of the valve and the myocardium. Journal of the American College of Cardiology, 60(19), 1854-1863.
  30. El Accaoui, R. N., Gould, S. T., Hajj, G. P., Chu, Y., Davis, M. K., Kraft, D. C., . . . Zimmerman, K. A. (2014). Aortic valve sclerosis in mice deficient in endothelial nitric oxide synthase. American Journal of Physiology-Heart and Circulatory Physiology, 306(9), H1302-H1313.
  31. Fan, J., Shimoyamada, H., Sun, H., Marcovina, S., Honda, K., & Watanabe, T. (2001). Transgenic rabbits expressing human apolipoprotein (a) develop more extensive atherosclerotic lesions in response to a cholesterol-rich diet. Arteriosclerosis, thrombosis, and vascular biology, 21(1), 88-94.
  32. Fernández-Jiménez, R., García-Prieto, J., Sánchez-González, J., Agüero, J., López-Martín, G. J., Galán-Arriola, C., . . . Ibáñez, B. (2015). Pathophysiology underlying the bimodal edema phenomenon after myocardial ischemia/reperfusion. Journal of the American College of Cardiology, 66(7), 816-828.
  33. Fernández, B., Durán, A. C., Fernández-Gallego, T., Fernández, M. C., Such, M., Arqué, J. M., & Sans-Coma, V. (2009). Bicuspid aortic valves with different spatial orientations of the leaflets are distinct etiological entities. Journal of the American College of Cardiology, 54(24), 2312-2318.
  34. Fujisaka, T., Hoshiga, M., Hotchi, J., Takeda, Y., Jin, D., Takai, S., . . . Ishizaka, N. (2013). Angiotensin II promotes aortic valve thickening independent of elevated blood pressure in apolipoprotein-E deficient mice. Atherosclerosis, 226(1), 82-87.
  35. Fuster, J. J., Castillo, A. I., Zaragoza, C., Ibáñez, B., & Andrés, V. (2012). Animal models of atherosclerosis. Progress in molecular biology and translational science, 105, 1-23.
  36. Gal, D., Rongione, A. J., Slovenkai, G. A., DeJesus, S. T., Lucas, A., Fields, C. D., & Isner, J. M. (1990). Atherosclerotic Yucatan microswine: An animalmodel with high-grade, fibrocalcific, nonfatty lesions suitable for testing catheter-based interventions. American heart journal, 119(2), 291-300.
  37. Galante, A., Pietroiusti, A., Vellini, M., Piccolo, P., Possati, G., De Bonis, M., . . . Favalli, C. (2001). C-reactive protein is increased in patients with degenerative aortic valvular stenosis. Journal of the American College of Cardiology, 38(4), 1078-1082.
  38. Garg, V., Muth, A. N., Ransom, J. F., Schluterman, M. K., Barnes, R., King, I. N., . . . Srivastava, D. (2005). Mutations in NOTCH1 cause aortic valve disease. nature, 437(7056), 270-274.
  39. Gerrity, R. G., Natarajan, R., Nadler, J. L., & Kimsey, T. (2001). Diabetes-induced accelerated atherosclerosis in swine. Diabetes, 50(7), 1654-1665.
  40. Ghaisas, N. K., Foley, J. B., O’Briain, D. S., Crean, P., Kelleher, D., & Walsh, M. (2000). Adhesion molecules in nonrheumatic aortic valve disease: endothelial expression, serum levels and effects of valve replacement. Journal of the American College of Cardiology, 36(7), 2257-2262.
  41. Gillis, K., Roosens, B., Bala, G., Remory, I., Hernot, S., Delvenne, P., . . . Cosyns, B. (2017). Interaction of renal failure and dyslipidaemia in the development of calcific aortic valve disease in rats. Acta Cardiologica, 72(5), 537-546.
  42. Go, J. L., Prem, K., Al-Hijji, M. A., Qin, Q., Noble, C., Young, M. D., . . . Lerman, A. (2018). Experimental metabolic syndrome model associated with mechanical and structural degenerative changes of the aortic valve. Scientific reports, 8(1), 1-11.
  43. Goody, P. R., Hosen, M. R., Christmann, D., Niepmann, S. T., Zietzer, A., Adam, M., . . . Jansen, F. (2020). Aortic valve stenosis: from basic mechanisms to novel therapeutic targets. Arteriosclerosis, thrombosis, and vascular biology, 40(4), 885-900.
  44. Granada, J. F., Kaluza, G. L., Wilensky, R. L., Biedermann, B. C., Schwartz, R. S., & Falk, E. (2009). Porcine models of coronary atherosclerosis and vulnerable plaque for imaging and interventional research. EuroIntervention, 5(1), 140-148.
  45. Granada, J. F., Moreno, P. R., Burke, A. P., Schulz, D. G., Raizner, A. E., & Kaluza, G. L. (2005). Endovascular needle injection of cholesteryl linoleate into the arterial wall produces complex vascular lesions identifiable by intravascular ultrasound: early development in a porcine model of vulnerable plaque. Coronary artery disease, 16(4), 217-224.
  46. Granada, J. F., Wallace-Bradley, D., Win, H. K., Alviar, C. L., Builes, A., Lev, E. I., . . . Kaluza, G. L. (2007). In vivo plaque characterization using intravascular ultrasound–virtual histology in a porcine model of complex coronary lesions. Arteriosclerosis, thrombosis, and vascular biology, 27(2), 387-393.
  47. Grunwald, K. A., Schueler, K., Uelmen, P. J., Lipton, B. A., Kaiser, M., Buhman, K., & Attie, A. D. (1999). Identification of a novel Arg→ Cys mutation in the LDL receptor that contributes to spontaneous hypercholesterolemia in pigs. Journal of lipid research, 40(3), 475-485.
  48. Guerraty, M., & Mohler, E. R. (2007). Models of aortic valve calcification. Journal of Investigative Medicine, 55(6), 278-283.
  49. Guerraty, M. A., Grant, G. R., Karanian, J. W., Chiesa, O. A., Pritchard, W. F., & Davies, P. F. (2010). Hypercholesterolemia Induces Side-Specific Phenotypic Changes and Peroxisome Proliferator–Activated Receptor-γ Pathway Activation in Swine Aortic Valve Endothelium. Arteriosclerosis, thrombosis, and vascular biology, 30(2), 225-231.
  50. Guerraty, M. A., Grant, G. R., Karanian, J. W., Chiesa, O. A., Pritchard, W. F., & Davies, P. F. (2011). Side-specific expression of activated leukocyte adhesion molecule (ALCAM; CD166) in pathosusceptible regions of swine aortic valve endothelium. The Journal of heart valve disease, 20(2), 165.
  51. Hakuno, D., Kimura, N., Yoshioka, M., Mukai, M., Kimura, T., Okada, Y., . . . Kudo, A. (2010). Periostin advances atherosclerotic and rheumatic cardiac valve degeneration by inducing angiogenesis and MMP production in humans and rodents. The Journal of clinical investigation, 120(7), 2292-2306.
  52. Hamilton, A. M., Boughner, D. R., Drangova, M., & Rogers, K. A. (2011). Statin treatment of hypercholesterolemic-induced aortic valve sclerosis. Cardiovascular Pathology, 20(2), 84-92.
  53. Hara, T., Tsukada, N., Okano, M., Ishida, T., Hirata, K.-i., & Shiomi, M. (2018). Progression of calcific aortic valve sclerosis in WHHLMI rabbits. Atherosclerosis, 273, 8-14.
  54. Hasler-Rapacz, J., Kempen, H. J., Princen, H. M., Kudchodkar, B. J., Lacko, A., & Rapacz, J. (1996). Effects of simvastatin on plasma lipids and apolipoproteins in familial hypercholesterolemic swine. Arteriosclerosis, thrombosis, and vascular biology, 16(1), 137-143.
  55. Hasler‐Rapacz, J., Ellegren, H., Fridolfsson, A. K., Kirkpatrick, B., Kirk, S., Andersson, L., & Rapacz, J. (1998). Identification of a mutation in the low density lipoprotein receptor gene associated with recessive familial hypercholesterolemia in swine. American journal of medical genetics, 76(5), 379-386.
  56. Helske, S., Oksjoki, R., Lindstedt, K. A., Lommi, J., Turto, H., Werkkala, K., . . . Kovanen, P. T. (2008). Complement system is activated in stenotic aortic valves. Atherosclerosis, 196(1), 190-200.
  57. Hinton Jr, R. B., Alfieri, C. M., Witt, S. A., Glascock, B. J., Khoury, P. R., Benson, D. W., & Yutzey, K. E. (2008). Mouse heart valve structure and function: echocardiographic and morphometric analyses from the fetus through the aged adult. American Journal of Physiology-Heart and Circulatory Physiology, 294(6), H2480-H2488.
  58. Hisamatsu, T., Miura, K., Fujiyoshi, A., Kadota, A., Miyagawa, N., Satoh, A., . . . Ueshima, H. (2018). Serum magnesium, phosphorus, and calcium levels and subclinical calcific aortic valve disease: A population-based study. Atherosclerosis, 273, 145-152.
  59. Hjortnaes, J., Shapero, K., Goettsch, C., Hutcheson, J. D., Keegan, J., Kluin, J., . . . Aikawa, E. (2015). Valvular interstitial cells suppress calcification of valvular endothelial cells. Atherosclerosis, 242(1), 251-260.
  60. Hoffman, J. I., & Kaplan, S. (2002). The incidence of congenital heart disease. Journal of the American College of Cardiology, 39(12), 1890-1900.
  61. Holvoet, P., Theilmeier, G., Shivalkar, B., Flameng, W., & Collen, D. s. (1998). LDL hypercholesterolemia is associated with accumulation of oxidized LDL, atherosclerotic plaque growth, and compensatory vessel enlargement in coronary arteries of miniature pigs. Arteriosclerosis, thrombosis, and vascular biology, 18(3), 415-422.
  62. Honda, S., Miyamoto, T., Watanabe, T., Narumi, T., Kadowaki, S., Honda, Y., . . . Funayama, A. (2014). A novel mouse model of aortic valve stenosis induced by direct wire injury. Arteriosclerosis, thrombosis, and vascular biology, 34(2), 270-278.
  63. Hulin, A., Hego, A., Lancellotti, P., & Oury, C. (2018). Advances in pathophysiology of calcific aortic valve disease propose novel molecular therapeutic targets. Frontiers in cardiovascular medicine, 5, 21.
  64. Ignatowski, A. (1908). Influence of animal food on the organsim of rabbits. Izvest Imper Voennomed Akad St Petersburg, 16, 154-173.
  65. Ishii, A., Vinuela, F., Murayama, Y., Yuki, I., Nien, Y., Yeh, D., & Vinters, H. (2006). Swine model of carotid artery atherosclerosis: experimental induction by surgical partial ligation and dietary hypercholesterolemia. American Journal of Neuroradiology, 27(9), 1893-1899.
  66. Jialal, I., Stein, D., Balis, D., Grundy, S. M., Adams-Huet, B., & Devaraj, S. (2001). Effect of hydroxymethyl glutaryl coenzyme a reductase inhibitor therapy on high sensitive C-reactive protein levels. Circulation, 103(15), 1933-1935.
  67. Kamath, A. R., & Pai, R. G. (2008). Risk factors for progression of calcific aortic stenosis and potential therapeutic targets. The International journal of angiology: official publication of the International College of Angiology, Inc, 17(2), 63.
  68. Laforest, B., Andelfinger, G., & Nemer, M. (2011). Loss of Gata5 in mice leads to bicuspid aortic valve. The Journal of clinical investigation, 121(7), 2876-2887.
  69. Le Quang, K., Bouchareb, R., Lachance, D., Laplante, M.-A., Husseini, D. E., Boulanger, M.-C., . . . Pibarot, P. (2014). Early development of calcific aortic valve disease and left ventricular hypertrophy in a mouse model of combined dyslipidemia and type 2 diabetes mellitus. Arteriosclerosis, thrombosis, and vascular biology, 34(10), 2283-2291.
  70. Lee, Y. T., Laxton, V., Lin, H. Y., Chan, Y. W. F., Fitzgerald‑Smith, S., To, T. L. O., . . . Tse, G. (2017). Animal models of atherosclerosis. Biomedical reports, 6(3), 259-266.
  71. Leong, X.-F., Ng, C.-Y., & Jaarin, K. (2015). Animal models in cardiovascular research: hypertension and atherosclerosis. BioMed research international, 2015.
  72. Lerman, D. A., Prasad, S., & Alotti, N. (2015). Calcific aortic valve disease: molecular mechanisms and therapeutic approaches. European Cardiology Review, 10(2), 108.
  73. Lilly, L. S., & Braunwald, E. (2012). Braunwald's heart disease: a textbook of cardiovascular medicine (Vol. 2): Elsevier Health Sciences.
  74. Lindman, B., Clavel, M., & Mathieu, P. (2016). lung, B., Lancellotti, P., Otto, CM, Pibarot. Calcific aortic stenosis. Nat Rev Dis Primers, 3(2), 16006.
  75. Liu, A. (2007). Joag VR, Gotlieb AI. The emerging role of valve interstitial cell phenotypes in regulating heart valve pathobiology. Am J Pathol, 171, 1407-1418.
  76. Malergue, M., Urena, P., Prieur, P., Guedon-Rapoud, C., & Petrover, M. (1997). Incidence and development of aortic stenosis in chronic hemodialysis. An ultrasonographic and biological study of 112 patients. Archives des Maladies du Coeur et des Vaisseaux, 90(12), 1595-1601.
  77. McBride, K. L., Zender, G. A., Fitzgerald–Butt, S. M., Seagraves, N. J., Fernbach, S. D., Zapata, G., . . . Belmont, J. W. (2011). Association of common variants in ERBB4 with congenital left ventricular outflow tract obstruction defects. Birth Defects Research Part A: Clinical and Molecular Teratology, 91(3), 162-168.
  78. Miller, J. D., Weiss, R. M., & Heistad, D. D. (2011). Calcific aortic valve stenosis: methods, models, and mechanisms. Circulation research, 108(11), 1392-1412.
  79. Miller, J. D., Weiss, R. M., Serrano, K. M., & Brooks, R. M. (2009). Lowering plasma cholesterol levels halts progression of aortic valve disease in mice. Circulation, 119(20), 2693.
  80. Mills, W. R., Einstadter, D., & Finkelhor, R. S. (2004). Relation of calcium-phosphorus product to the severity of aortic stenosis in patients with normal renal function. The American journal of cardiology, 94(9), 1196-1198.
  81. Monetti, M., Canavesi, M., Camera, M., Parente, R., Paoletti, R., Tremoli, E., . . . Bellosta, S. (2007). Rosuvastatin displays anti-atherothrombotic and anti-inflammatory properties in apoE-deficient mice. Pharmacological research, 55(5), 441-449.
  82. Mourino-Alvarez, L., Baldan-Martin, M., Sastre-Oliva, T., Martin-Lorenzo, M., Maroto, A. S., Corbacho-Alonso, N., . . . Alvarez-Llamas, G. (2018). A comprehensive study of calcific aortic stenosis: from rabbit to human samples. Disease models & mechanisms, 11(6).
  83. Ngo, D. T., Stafford, I., Kelly, D. J., Sverdlov, A. L., Wuttke, R. D., Weedon, H., . . . Chirkov, Y. Y. (2008). Vitamin D2 supplementation induces the development of aortic stenosis in rabbits: Interactions with endothelial function and thioredoxin-interacting protein. European journal of pharmacology, 590(1-3), 290-296.
  84. Niepmann, S. T., Steffen, E., Zietzer, A., Adam, M., Nordsiek, J., Gyamfi-Poku, I., . . . Kelm, M. (2019). Graded murine wire-induced aortic valve stenosis model mimics human functional and morphological disease phenotype. Clinical Research in Cardiology, 108(8), 847-856.
  85. Nigam, V., & Srivastava, D. (2009). Notch1 represses osteogenic pathways in aortic valve cells. Journal of molecular and cellular cardiology, 47(6), 828-834.
  86. Nus, M., MacGrogan, D., Martínez-Poveda, B., Benito, Y., Casanova, J. C., Fernández-Avilés, F., . . . de la Pompa, J. L. (2011). Diet-induced aortic valve disease in mice haploinsufficient for the Notch pathway effector RBPJK/CSL. Arteriosclerosis, thrombosis, and vascular biology, 31(7), 1580-1588.
  87. O’Brien, K. D. (2006). Pathogenesis of calcific aortic valve disease: a disease process comes of age (and a good deal more). Arteriosclerosis, thrombosis, and vascular biology, 26(8), 1721-1728.
  88. O’Brien, K. D., Reichenbach, D. D., Marcovina, S. M., Kuusisto, J., Alpers, C. E., & Otto, C. M. (1996). Apolipoproteins B,(a), and E accumulate in the morphologically early lesion of ‘degenerative’valvular aortic stenosis. Arteriosclerosis, thrombosis, and vascular biology, 16(4), 523-532.
  89. Ohukainen, P., Ruskoaho, H., & Rysa, J. (2018). Cellular mechanisms of valvular thickening in early and intermediate calcific aortic valve disease. Current Cardiology Reviews, 14(4), 264-271.
  90. Panepinto, L., & Phillips, R. (1986). The Yucatan miniature pig: characterization and utilization in biomedical research. Laboratory animal science, 36(4), 344-347.
  91. Parisi, V., Leosco, D., Ferro, G., Bevilacqua, A., Pagano, G., de Lucia, C., . . . Ferrara, N. (2015). The lipid theory in the pathogenesis of calcific aortic stenosis. Nutrition, Metabolism and Cardiovascular Diseases, 25(6), 519-525.
  92. Pawade, T. A., Newby, D. E., & Dweck, M. R. (2015). Calcification in aortic stenosis: the skeleton key. Journal of the American College of Cardiology, 66(5), 561-577.
  93. Porras, A. M., Shanmuganayagam, D., Meudt, J. J., Krueger, C. G., Hacker, T. A., Rahko, P. S., . . . Masters, K. S. (2015). Development of aortic valve disease in familial hypercholesterolemic swine: implications for elucidating disease etiology. Journal of the American Heart Association, 4(10), e002254.
  94. Rajamannan, N. M., Evans, F. J., Aikawa, E., Grande-Allen, K. J., Demer, L. L., Heistad, D. D., . . . O'Brien, K. D. (2011). Calcific aortic valve disease: Not simply a degenerative process a review and agenda for research from the National Heart and Lung and Blood Institute Aortic Stenosis Working Group. Circulation, 124(16), 1783.
  95. Rajamannan, N. M., Subramaniam, M., Caira, F., Stock, S. R., & Spelsberg, T. C. (2005). Atorvastatin inhibits hypercholesterolemia-induced calcification in the aortic valves via the Lrp5 receptor pathway. Circulation, 112(9_supplement), I-229-I-234.
  96. Rajamannan, N. M., Subramaniam, M., Springett, M., Sebo, T. C., Niekrasz, M., McConnell, J. P., . . . Spelsberg, T. C. (2002). Atorvastatin inhibits hypercholesterolemia-induced cellular proliferation and bone matrix production in the rabbit aortic valve. Circulation, 105(22), 2660-2665.
  97. Rajamannan, N. M., Subramaniam, M., Stock, S., Stone, N., Springett, M., Ignatiev, K., . . . Spelsberg, T. (2005). Atorvastatin inhibits calcification and enhances nitric oxide synthase production in the hypercholesterolaemic aortic valve. Heart, 91(6), 806-810.
  98. Rattazzi, M., Faggin, E., Bertacco, E., Nardin, C., Pagliani, L., Plebani, M., . . . Pauletto, P. (2018). Warfarin, but not rivaroxaban, promotes the calcification of the aortic valve in ApoE−/− mice. Cardiovascular therapeutics, 36(4), e12438.
  99. Reitman, J., Mahley, R., & Fry, D. (1982). Yucatan miniature swine as a model for diet-induced atherosclerosis. Atherosclerosis, 43(1), 119-132.
  100. Roosens, B., Bala, G., Droogmans, S., Van Camp, G., Breyne, J., & Cosyns, B. (2013). Animal models of organic heart valve disease. International journal of cardiology, 165(3), 398-409.
  101. Rutkovskiy, A., Malashicheva, A., Sullivan, G., Bogdanova, M., Kostareva, A., Stensløkken, K. O., . . . Vaage, J. (2017). Valve interstitial cells: the key to understanding the pathophysiology of heart valve calcification. Journal of the American Heart Association, 6(9), e006339.
  102. Scatena, M., Jackson, M. F., Speer, M. Y., Leaf, E. M., Wallingford, M. C., & Giachelli, C. M. (2018). Increased Calcific Aortic Valve Disease in response to a diabetogenic, procalcific diet in the LDLr-/-ApoB100/100 mouse model. Cardiovascular Pathology, 34, 28-37.
  103. Shiomi, M., & Ito, T. (2009). The Watanabe heritable hyperlipidemic (WHHL) rabbit, its characteristics and history of development: a tribute to the late Dr. Yoshio Watanabe. Atherosclerosis, 207(1), 1-7.
  104. Shiomi, M., Ito, T., Yamada, S., Kawashima, S., & Fan, J. (2003). Development of an animal model for spontaneous myocardial infarction (WHHLMI rabbit). Arteriosclerosis, thrombosis, and vascular biology, 23(7), 1239-1244.
  105. Sider, K. L., Blaser, M. C., & Simmons, C. A. (2011). Animal models of calcific aortic valve disease. International journal of inflammation, 2011.
  106. Sider, K. L., Zhu, C., Kwong, A. V., Mirzaei, Z., de Langé, C. F., & Simmons, C. A. (2014). Evaluation of a porcine model of early aortic valve sclerosis. Cardiovascular Pathology, 23(5), 289-297.
  107. Simmons, C. A., Grant, G. R., Manduchi, E., & Davies, P. F. (2005). Spatial heterogeneity of endothelial phenotypes correlates with side-specific vulnerability to calcification in normal porcine aortic valves. Circulation research, 96(7), 792-799.
  108. Skold, B., Getty, R., & Ramsey, F. (1966). Spontaneous atherosclerosis in the arterial system of aging swine. American journal of veterinary research, 27(116), 257-273.
  109. Srivastava, S., Sithu, S. D., Vladykovskaya, E., Haberzettl, P., Hoetker, D. J., Siddiqui, M. A., . . . Bhatnagar, A. (2011). Oral exposure to acrolein exacerbates atherosclerosis in apoE-null mice. Atherosclerosis, 215(2), 301-308.
  110. Swinkels, D. W., & Demacker, P. N. (1988). Comparative studies on the low density lipoprotein subfractions from pig and man. Comparative Biochemistry and Physiology Part B: Comparative Biochemistry, 90(2), 297-300.
  111. Tanaka, K., Sata, M., Fukuda, D., Suematsu, Y., Motomura, N., Takamoto, S., . . . Nagai, R. (2005). Age-associated aortic stenosis in apolipoprotein E-deficient mice. Journal of the American College of Cardiology, 46(1), 134-141.
  112. Thim, T., Hagensen, M. K., Drouet, L., Bonneau, M., Granada, J., Nielsen, L., . . . Falk, E. (2010). Familial hypercholesterolaemic downsized pig with human-like coronary atherosclerosis: a model for preclinical studies. EuroIntervention: journal of EuroPCR in collaboration with the Working Group on Interventional Cardiology of the European Society of Cardiology, 6(2), 261-268.
  113. Tkatchenko, T. V., Moreno-Rodriguez, R. A., Conway, S. J., Molkentin, J. D., Markwald, R. R., & Tkatchenko, A. V. (2009). Lack of periostin leads to suppression of Notch1 signaling and calcific aortic valve disease. Physiological genomics, 39(3), 160-168.
  114. Tsang, H., Rashdan, N., Whitelaw, C., Corcoran, B., Summers, K., & MacRae, V. (2016). Large animal models of cardiovascular disease. Cell biochemistry and function, 34(3), 113-132.
  115. Walters, E. M., Wolf, E., Whyte, J. J., Mao, J., Renner, S., Nagashima, H., . . . Critser, J. K. (2012). Completion of the swine genome will simplify the production of swine as a large animal biomedical model. BMC medical genomics, 5(1), 1-11.
  116. Wang, Y., Wu, B., Farrar, E., Lui, W., Lu, P., Zhang, D., . . . Yang, D. (2017). Notch-Tnf signalling is required for development and homeostasis of arterial valves. European heart journal, 38(9), 675-686.
  117. Watanabe, Y. (1980). Serial inbreeding of rabbits with hereditary hyperlipidemia (WHHL-rabbit): incidence and development of atherosclerosis and xanthoma. Atherosclerosis, 36(2), 261-268.
  118. Weisell, J. (2020). Studies on calcific aortic valve disease: from experimental models to human disease. Itä-Suomen yliopisto,
  119. Weiss, R. M., Chu, Y., Brooks, R. M., Lund, D. D., Cheng, J., Zimmerman, K. A., . . . Shao, J. Q. (2018). Discovery of an experimental model of unicuspid aortic valve. Journal of the American Heart Association, 7(13), e006908.
  120. Weiss, R. M., Ohashi, M., Miller, J. D., Young, S. G., & Heistad, D. D. (2006). Calcific aortic valve stenosis in old hypercholesterolemic mice. Circulation, 114(19), 2065-2069.
  121. Wirrig, E. E., & Yutzey, K. E. (2011). Transcriptional regulation of heart valve development and disease. Cardiovascular Pathology, 20(3), 162-167.
  122. Xu, S., Liu, A. C., & Gotlieb, A. I. (2010). Common pathogenic features of atherosclerosis and calcific aortic stenosis: role of transforming growth factor-β. Cardiovascular Pathology, 19(4), 236-247.
  123. Yi, B., Zeng, W., Lv, L., & Hua, P. (2021). Changing epidemiology of calcific aortic valve disease: 30-year trends of incidence, prevalence, and deaths across 204 countries and territories. Aging (Albany NY), 13(9), 12710-12732. doi:10.18632/aging.202942
  124. Yoshioka, M., Yuasa, S., Matsumura, K., Kimura, K., Shiomi, T., Kimura, N., . . . Shin, H. (2006). Chondromodulin-I maintains cardiac valvular function by preventing angiogenesis. Nature medicine, 12(10), 1151-1159.
  125. Zeadin, M., Butcher, M., Werstuck, G., Khan, M., Yee, C. K., & Shaughnessy, S. G. (2009). Effect of leptin on vascular calcification in apolipoprotein E–deficient mice. Arteriosclerosis, thrombosis, and vascular biology, 29(12), 2069-2075.

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