Establishment of large animal model of bicuspid aortic valve_Chinese Journal of Clinical Thoracic and Cardiovascular Surgery

Authors：

YANG Quanlin ¹ ,  LIU Huan ² , SHAN Yan ³ , ZHU liming ² , SUN Xiaoning ² , YANG Ye ² , WANG Wenshuo ² , WEI Lai ² , WANG Chunsheng ²

1. Department of Cardiac Surgery, Zhongshan-Xiamen Hospital, Fudan University, Xiamen, 361015, Fujian, P. R. China;
2. Department of Cardiac Surgery, Zhongshan Hospital, Fudan University, Shanghai, 200032, P. R. China;
3. Department of Medical Imaging, Zhongshan Hospital, Fudan University, Shanghai, 200032, P. R. China;

Corresponding author：

LIU Huan, Email: liu.huan@zs-hospital.sh.cn

Keywords：

Bicuspid aortic valve; bicuspid aortopathy; animal model; wall shear stress

DOI：

10.7507/1007-4848.202202052

Video：

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Objective To discuss the feasibility of establishment of animal model of "functional" bicuspid aortic valve with swine and observe its effect on the wall shear stress inside the aorta. Methods Four common Shanghai White Swine with body weight between 50 kg to 55 kg were selected. Under general anesthesia and cardiopulmonary bypass, the aortic transverse incision approach was used, continuous suture with 6-0 polypropylene to align the left and right coronary valve leaflets to create a bicuspid valve morphology. After the operation, echocardiography was used to observe the aortic valve morphology and the hemodynamic changes of the aortic valve orifice. The effect on the wall shear stress inside the aorta was studied with 4D-Flow magnetic resonance imaging (MRI). Results A total of 4 swine "functional" bicuspid aortic valve models were established, with a success rate of 100.0%. Echocardiography showed that the blood flow velocity of the aortic valve orifice was faster than that before the operation (0.96 m/s vs. 1.80 m/s). 4D-Flow MRI showed abnormally increased wall shear stress and blood flow velocity in the aorta of the animal models. After the surgery, in model animals, the maximal wall shear stress inside the ascending aorta was greater than 1.36 Pa, and the maximum blood flow velocity was greater than 1.4 m/s. Conclusion Establishment of the animal model of "functional" bicuspid aortic valve in swine is feasible, scientific and reliable. It can be used in researches on evaluating the pathophysiological changes.

Citation： YANG Quanlin, LIU Huan, SHAN Yan, ZHU liming, SUN Xiaoning, YANG Ye, WANG Wenshuo, WEI Lai, WANG Chunsheng. Establishment of large animal model of bicuspid aortic valve. Chinese Journal of Clinical Thoracic and Cardiovascular Surgery, 2022, 29(11): 1485-1491. doi: 10.7507/1007-4848.202202052 Copy

1.	Geeraert P, Jamalidinan F, Fatehi Hassanabad A, et al. Bicuspid aortic valve disease is associated with abnormal wall shear stress, viscous energy loss, and pressure drop within the ascending thoracic aorta: A cross-sectional study. Medicine (Baltimore), 2021, 100(26): e26518.
2.	Stock S, Mohamed SA, Sievers HH. Bicuspid aortic valve related aortopathy. Gen Thorac Cardiovasc Surg, 2019, 67(1): 93-101.
3.	汪咏莳, 刘宏宇, 孔德红, 等. 先天二叶式主动脉瓣畸形临床及超声心动图特征分析. 中国临床医学, 2021, 28(1): 60-64.
4.	Shan Y, Li J, Wang Y, et al. Aortic shear stress in patients with bicuspid aortic valve with stenosis and insufficiency. J Thorac Cardiovasc Surg, 2017, 153(6): 1263-1272.
5.	Roman MJ, Pugh NL, Devereux RB, et al. Aortic dilatation associated with bicuspid aortic valve: Relation to sex, hemodynamics, and valve morphology (the National Heart Lung and Blood Institute-Sponsored National Registry of Genetically Triggered Thoracic Aortic Aneurysms and Cardiovascular Conditions). Am J Cardiol, 2017, 120(7): 1171-1175.
6.	Bollache E, Guzzardi DG, Sattari S, et al. Aortic valve-mediated wall shear stress is heterogeneous and predicts regional aortic elastic fiber thinning in bicuspid aortic valve-associated aortopathy. J Thorac Cardiovasc Surg, 2018, 156(6): 2112-2120.
7.	Piatti F, Sturla F, Bissell MM, et al. 4D flow analysis of bav-related fluid-dynamic alterations: Evidences of wall shear stress alterations in absence of clinically-relevant aortic anatomical remodeling. Front Physiol, 2017, 8: 441.
8.	Salerno M, Chandrashekhar Y. CMR 4D-Flow wall shear stress and aortic dilation in bicuspid aortic valve. JACC Cardiovasc Imaging, 2022, 15(1): 177-179.
9.	van Ooij P, Farag ES, Blanken CPS, et al. Fully quantitative mapping of abnormal aortic velocity and wall shear stress direction in patients with bicuspid aortic valves and repaired coarctation using 4D flow cardiovascular magnetic resonance. J Cardiovasc Magn Reson, 2021, 23(1): 9.
10.	Borger MA, Fedak PWM, Stephens EH, et al. The American Association for Thoracic Surgery consensus guidelines on bicuspid aortic valve-related aortopathy: Full online-only version. J Thorac Cardiovasc Surg, 2018, 156(2): e41-e74.
11.	Etz CD, Haunschild J, Girdauskas E, et al. Surgical management of the aorta in BAV patients. Prog Cardiovasc Dis, 2020, 63(4): 475-481.
12.	Zhu Y, Imbrie-Moore AM, Park MH, et al. Ex vivo analysis of a porcine bicuspid aortic valve and aneurysm disease model. Ann Thorac Surg, 2021, 111(2): e113-e115.
13.	Della Corte A, Michelena HI, Citarella A, et al. Risk stratification in bicuspid aortic valve aortopathy: Emerging evidence and future perspectives. Curr Probl Cardiol, 2021, 46(3): 100428.
14.	Fatehi Hassanabad A, Garcia J, Verma S, et al. Utilizing wall shear stress as a clinical biomarker for bicuspid valve-associated aortopathy. Curr Opin Cardiol, 2019, 34(2): 124-131.
15.	Guala A, Dux-Santoy L, Teixido-Tura G, et al. Wall shear stress predicts aortic dilation in patients with bicuspid aortic valve. JACC Cardiovasc Imaging, 2022, 15(1): 46-56.
16.	Oliveira D, Rosa SA, Tiago J, et al. Bicuspid aortic valve aortopathies: An hemodynamics characterization in dilated aortas. Comput Methods Biomech Biomed Engin, 2019, 22(8): 815-826.
17.	Pasta S, Agnese V, Gallo A, et al. Shear stress and aortic strain associations with biomarkers of ascending thoracic aortic aneurysm. Ann Thorac Surg, 2020, 110(5): 1595-1604.
18.	Rahman O, Scott M, Bollache E, et al. Interval changes in aortic peak velocity and wall shear stress in patients with bicuspid aortic valve disease. Int J Cardiovasc Imaging, 2019, 35(10): 1925-1934.
19.	Gomez A, Wang Z, Xuan Y, et al. Wall stress distribution in bicuspid aortic valve-associated ascending thoracic aortic aneurysms. Ann Thorac Surg, 2020, 110(3): 807-814.
20.	Schmitt R, Tscheuschler A, Laschinski P, et al. Matrix metalloproteinase-2 isoforms differ within the aortic wall of ascending aortic aneurysms associated with bicuspid aortic valve. Cardiol Res Pract, 2020, 2020: 1306425.
21.	Girdauskas E, Petersen J. Update on bicuspid aortic valve aortopathy. Curr Opin Cardiol, 2017, 32(6): 651-654.
22.	Sophocleous F, Milano EG, Pontecorboli G, et al. Enlightening the association between bicuspid aortic valve and aortopathy. J Cardiovasc Dev Dis, 2018, 5(2): 21.
23.	Minderhoud SCS, Roos-Hesselink JW, Chelu RG, et al. Wall shear stress angle is associated with aortic growth in bicuspid aortic valve patients. Eur Heart J Cardiovasc Imaging, 2022: jeab290.
24.	Messner B, Bernhard D. Bicuspid aortic valve-associated aortopathy: Where do we stand? J Mol Cell Cardiol, 2019, 133: 76-85.
25.	Mitsouras D, Hope MD. A radiologist's excursion in four-dimensional flow and the bicuspid aortic valve: Vorticity, helicity, wall shear stress, and all that. Radiology, 2019, 293(3): 551-553.

1. Geeraert P, Jamalidinan F, Fatehi Hassanabad A, et al. Bicuspid aortic valve disease is associated with abnormal wall shear stress, viscous energy loss, and pressure drop within the ascending thoracic aorta: A cross-sectional study. Medicine (Baltimore), 2021, 100(26): e26518.
2. Stock S, Mohamed SA, Sievers HH. Bicuspid aortic valve related aortopathy. Gen Thorac Cardiovasc Surg, 2019, 67(1): 93-101.
3. 汪咏莳, 刘宏宇, 孔德红, 等. 先天二叶式主动脉瓣畸形临床及超声心动图特征分析. 中国临床医学, 2021, 28(1): 60-64.
4. Shan Y, Li J, Wang Y, et al. Aortic shear stress in patients with bicuspid aortic valve with stenosis and insufficiency. J Thorac Cardiovasc Surg, 2017, 153(6): 1263-1272.
5. Roman MJ, Pugh NL, Devereux RB, et al. Aortic dilatation associated with bicuspid aortic valve: Relation to sex, hemodynamics, and valve morphology (the National Heart Lung and Blood Institute-Sponsored National Registry of Genetically Triggered Thoracic Aortic Aneurysms and Cardiovascular Conditions). Am J Cardiol, 2017, 120(7): 1171-1175.
6. Bollache E, Guzzardi DG, Sattari S, et al. Aortic valve-mediated wall shear stress is heterogeneous and predicts regional aortic elastic fiber thinning in bicuspid aortic valve-associated aortopathy. J Thorac Cardiovasc Surg, 2018, 156(6): 2112-2120.
7. Piatti F, Sturla F, Bissell MM, et al. 4D flow analysis of bav-related fluid-dynamic alterations: Evidences of wall shear stress alterations in absence of clinically-relevant aortic anatomical remodeling. Front Physiol, 2017, 8: 441.
8. Salerno M, Chandrashekhar Y. CMR 4D-Flow wall shear stress and aortic dilation in bicuspid aortic valve. JACC Cardiovasc Imaging, 2022, 15(1): 177-179.
9. van Ooij P, Farag ES, Blanken CPS, et al. Fully quantitative mapping of abnormal aortic velocity and wall shear stress direction in patients with bicuspid aortic valves and repaired coarctation using 4D flow cardiovascular magnetic resonance. J Cardiovasc Magn Reson, 2021, 23(1): 9.
10. Borger MA, Fedak PWM, Stephens EH, et al. The American Association for Thoracic Surgery consensus guidelines on bicuspid aortic valve-related aortopathy: Full online-only version. J Thorac Cardiovasc Surg, 2018, 156(2): e41-e74.
11. Etz CD, Haunschild J, Girdauskas E, et al. Surgical management of the aorta in BAV patients. Prog Cardiovasc Dis, 2020, 63(4): 475-481.
12. Zhu Y, Imbrie-Moore AM, Park MH, et al. Ex vivo analysis of a porcine bicuspid aortic valve and aneurysm disease model. Ann Thorac Surg, 2021, 111(2): e113-e115.
13. Della Corte A, Michelena HI, Citarella A, et al. Risk stratification in bicuspid aortic valve aortopathy: Emerging evidence and future perspectives. Curr Probl Cardiol, 2021, 46(3): 100428.
14. Fatehi Hassanabad A, Garcia J, Verma S, et al. Utilizing wall shear stress as a clinical biomarker for bicuspid valve-associated aortopathy. Curr Opin Cardiol, 2019, 34(2): 124-131.
15. Guala A, Dux-Santoy L, Teixido-Tura G, et al. Wall shear stress predicts aortic dilation in patients with bicuspid aortic valve. JACC Cardiovasc Imaging, 2022, 15(1): 46-56.
16. Oliveira D, Rosa SA, Tiago J, et al. Bicuspid aortic valve aortopathies: An hemodynamics characterization in dilated aortas. Comput Methods Biomech Biomed Engin, 2019, 22(8): 815-826.
17. Pasta S, Agnese V, Gallo A, et al. Shear stress and aortic strain associations with biomarkers of ascending thoracic aortic aneurysm. Ann Thorac Surg, 2020, 110(5): 1595-1604.
18. Rahman O, Scott M, Bollache E, et al. Interval changes in aortic peak velocity and wall shear stress in patients with bicuspid aortic valve disease. Int J Cardiovasc Imaging, 2019, 35(10): 1925-1934.
19. Gomez A, Wang Z, Xuan Y, et al. Wall stress distribution in bicuspid aortic valve-associated ascending thoracic aortic aneurysms. Ann Thorac Surg, 2020, 110(3): 807-814.
20. Schmitt R, Tscheuschler A, Laschinski P, et al. Matrix metalloproteinase-2 isoforms differ within the aortic wall of ascending aortic aneurysms associated with bicuspid aortic valve. Cardiol Res Pract, 2020, 2020: 1306425.
21. Girdauskas E, Petersen J. Update on bicuspid aortic valve aortopathy. Curr Opin Cardiol, 2017, 32(6): 651-654.
22. Sophocleous F, Milano EG, Pontecorboli G, et al. Enlightening the association between bicuspid aortic valve and aortopathy. J Cardiovasc Dev Dis, 2018, 5(2): 21.
23. Minderhoud SCS, Roos-Hesselink JW, Chelu RG, et al. Wall shear stress angle is associated with aortic growth in bicuspid aortic valve patients. Eur Heart J Cardiovasc Imaging, 2022: jeab290.
24. Messner B, Bernhard D. Bicuspid aortic valve-associated aortopathy: Where do we stand? J Mol Cell Cardiol, 2019, 133: 76-85.
25. Mitsouras D, Hope MD. A radiologist's excursion in four-dimensional flow and the bicuspid aortic valve: Vorticity, helicity, wall shear stress, and all that. Radiology, 2019, 293(3): 551-553.

Chinese Journal of Clinical Thoracic and Cardiovascular Surgery

Establishment of large animal model of bicuspid aortic valve

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