journal article·2026-08Open access

Pyriphenone modification of glutaraldehyde pretreated bovine pericardium mitigates advanced glycation end products, calcification, and platelet adhesion

Andrey Zakharchenko, Nikia T. Toomey, Ivan Alferiev, Alexis Martinez, Devin Laurence, Oksana Horyn, Alireza Mohammad Karim, Arianna Adamo, Hajime Takano, Chandrasekaran Nagaswami, Stanley J. Stachelek, Giovanni Ferrari, Robert J. Levy

Acta Biomaterialia· Volume 219

Abstract

Heterograft biomaterials, such as glutaraldehyde-pretreated bovine pericardium (BP), are used to fabricate bioprosthetic heart valves (BHV). BHV durability is limited by structural valve degeneration (SVD), which is caused by either advanced glycation end products (AGE) with associated serum protein deposition, calcification, or both. Vitamin B6 vitamers have been investigated experimentally and clinically for mitigating AGE formation that complicates diabetes. In the present study, we investigated a vitamin B6-based photo-responsive molecule, Pyriphenone (PPh), hypothesizing that PPh could mitigate both BP AGE-serum protein uptake and BP calcification in vivo. PPh was synthesized by reacting pyridoxamine with benzophenone. PPh was optimally soluble in ethanol, and PPh-ethanol solutions were used for all PPh studies. PPh was demonstrated to become covalently and stably attached to BP with exposure to ultraviolet light. PPh-BP demonstrated significantly reduced in vitro AGE deposition and associated serum albumin uptake, versus unmodified BP. PPh-BP showed significant resistance to oxidation in vitro and demonstrated comparable biaxial mechanical properties to unmodified BP. In vitro hydrodynamic testing of trileaflet BHV fabricated from BP-PPh demonstrated no alterations of functionality, compared to unmodified BHV. In vivo 28-day subdermal implants in juvenile rats with either PPh-BP or unmodified BP demonstrated that PPh significantly mitigated AGE and serum albumin uptake, and calcification versus unmodified BP. Ex vivo studies of BP-PPh exposed to human whole blood demonstrated significantly reduced adhesion of platelets and white blood cells versus unmodified BP. In conclusion, PPh-BP mitigates calcification, AGE, and serum albumin uptake and reduces platelet and white blood cell adhesion. STATEMENT OF SIGNIFICANCE: Heart valve disease is highly prevalent, affecting millions. At this time, it can only be treated by either surgical valve repair or replacement of the diseased valve with a prosthesis. Bioprosthetic heart valves, fabricated from heterograft materials, are the most widely used heart valve replacements. However, these devices have poor durability due to calcification and advanced glycation end-product (AGE) deposition, which cause structural valve degeneration. Pyriphenone, the subject of this paper, is a compound synthesized by the authors that is shown in this paper to confer resistance to bioprosthetic valve calcification and AGE deposition.
Source: europepmc · Quality: candidate unverified · Source record ↗

Research context

OpenAlex topics: Cardiac Valve Diseases and Treatments · Electrospun Nanofibers in Biomedical Applications · Cardiac and Coronary Surgery Techniques

SciVX discovery tags are terminology-based. OpenAlex topics are source-provided classifications.

References (72)

Show source-provided references
1. 2017 AHA/ACC focused update of the 2014 AHA/ACC guideline for the management of patients with valvular heart disease: a report of the American College of Cardiology/American heart association task force on clinical practice guidelines10.1161/CIR.0000000000000503 ↗
2. National trends in utilization and in-hospital outcomes of mechanical versus bioprosthetic aortic valve replacements10.1016/j.jtcvs.2015.01.052 ↗
3. Bioprosthetic vs mechanical aortic valve replacement in patients 40 to 75 years of age10.1016/j.jacc.2025.01.013 ↗
4. Degeneration of bioprosthetic heart valves: update 202010.1161/JAHA.120.018506 ↗
5. Calcification and oxidative modifications are associated with progressive bioprosthetic heart valve dysfunction10.1161/JAHA.117.005648 ↗
6. Aortic valve replacement with bovine pericardial tissue valve in children and young adults10.1161/CIRCULATIONAHA.118.037187 ↗
7. Onset and progression of experimental bioprosthetic heart valve calcification
8. Prevention of calcification in bioprosthetic heart valves: challenges and perspectives10.1517/14712598.4.12.1971 ↗
9. Determinants of aortic bioprosthetic valve calcification assessed by multidetector CT10.1136/heartjnl-2014-306445 ↗
10. Noncalcific mechanisms of bioprosthetic structural valve degeneration10.1161/JAHA.120.018921 ↗
11. Glycation and serum albumin infiltration contribute to the structural degeneration of bioprosthetic heart valves10.1016/j.jacbts.2020.06.008 ↗
12. Advanced glycation end-products (AGEs): formation, chemistry, classification, receptors, and diseases related to AGEs10.3390/cells11081312 ↗
13. Receptor for age (RAGE) is a gene within the major histocompatibility class III region: implications for host response mechanisms in homeostasis and chronic disease
14. Mechanisms of disease: advanced glycation end-products and their receptor in inflammation and diabetes complications, Nature clinical practice
15. Advanced glycation end products and vascular inflammation: implications for accelerated atherosclerosis in diabetes10.1016/j.cardiores.2004.05.001 ↗
16. Advanced glycation end products and diabetic complications10.4196/kjpp.2014.18.1.1 ↗
17. Advanced glycation end products in Alzheimer's disease and other neurodegenerative diseases10.1016/S0002-9440(10)65659-3 ↗
18. Advanced glycation end products and the kidney10.1152/ajprenal.00398.2004 ↗
19. Model studies of advanced glycation end product modification of heterograft biomaterials: the effects of in vitro glucose, glyoxal, and serum albumin on collagen structure and mechanical properties10.1016/j.actbio.2020.12.053 ↗
20. Poly-2-methyl-2-oxazoline-modified bioprosthetic heart valve leaflets have enhanced biocompatibility and resist structural degeneration10.1073/pnas.2120694119 ↗
21. Formation pathways for lysine-arginine cross-links derived from hexoses and pentoses by Maillard processes: unraveling the structure of a pentosidine precursor10.1074/jbc.M102035200 ↗
22. Bioprosthetic heart valve structural degeneration associated with metabolic syndrome: mitigation with polyoxazoline modification10.1073/pnas.2219054120 ↗
23. Inhibition of advanced glycation end product formation and serum protein infiltration in bioprosthetic heart valve leaflets: investigations of anti-glycation agents and anticalcification interactions with ethanol pretreatment10.1016/j.biomaterials.2022.121782 ↗
24. Photochemical attachment of polymer films to solid surfaces via monolayers of benzophenone derivatives10.1021/ja990962+ ↗
25. Prevention of bioprosthetic heart valve calcification by ethanol preincubation. Efficacy and mechanisms10.1161/01.CIR.95.2.479 ↗
26. Ex vivo experimental characterizations for understanding the interrelationship between tissue mechanics and collagen microstructure of porcine mitral valve leaflets10.1016/j.jmbbm.2022.105401 ↗
27. Diminished adhesion and activation of platelets and neutrophils with CD47 functionalized blood contacting surfaces10.1016/j.biomaterials.2012.04.051 ↗
28. Tissue characterization and calcification potential of commercial bioprosthetic heart valves10.1016/S0003-4975(01)02493-6 ↗
29. Endothelial cell injury due to copper-catalyzed hydrogen peroxide generation from homocysteine10.1172/JCI112442 ↗
30. Vitamin B6 suppresses apoptosis of NM-1 bovine endothelial cells induced by homocysteine and copper10.1016/j.bbagen.2006.11.009 ↗
31. Response of fluorescein to carbon dioxide in dimethyl sulfoxide–water mixtures10.1039/FT9959100881 ↗
32. The impact of calcium phosphate on FITC-BSA loading of sonochemically prepared PLGA nanoparticles for inner ear drug delivery elucidated by two different fluorimetric quantification methods10.1016/j.ultsonch.2021.105783 ↗
33. Methods for quantifying fibrillar collagen alignment10.1007/978-1-4939-7113-8_28 ↗
34. Linking collagen fiber architecture to tissue-level biaxial mechanical behaviors of porcine semilunar heart valve cusps10.1016/j.jmbbm.2021.104907 ↗
35. Rate-dependent mechanical behaviour of semilunar valves under biaxial deformation: from quasi-static to physiological loading rates10.1016/j.jmbbm.2020.103645 ↗
36. Calcification of bovine pericardium: glutaraldehyde versus No-react biomodification10.1016/0003-4975(96)00277-9 ↗
37. Biologic determinants of dystrophic calcification and osteocalcin deposition in glutaraldehyde-preserved porcine aortic valve leaflets implanted subcutaneously in rats
38. Calcification of bovine pericardium used in cardiac valve bioprostheses. Implications for the mechanisms of bioprosthetic tissue mineralization
39. Chemically determined mineral content of explanted porcine aortic valve bioprostheses: correlation with radiographic assessment of calcification and clinical data10.1161/01.CIR.76.5.1061 ↗
40. Metabolic syndrome is associated with faster degeneration of bioprosthetic valves
41. Type 2 diabetes mellitus is associated with faster degeneration of bioprosthetic valve: results from a propensity score-matched Italian multicenter study10.1161/CIRCULATIONAHA.111.025064 ↗
42. Age-related enhanced degeneration of bioprosthetic valves due to leaflet calcification, tissue crosslinking, and structural changes10.1093/cvr/cvac002 ↗
43. Mechanical versus bioprosthetic aortic valve replacement10.1093/eurheartj/ehx141 ↗
44. Dual-crosslinked bioprosthetic heart valves prepared by glutaraldehyde crosslinked pericardium and poly-2-hydroxyethyl methacrylate exhibited improved antithrombogenicity and anticalcification properties10.1016/j.actbio.2022.10.036 ↗
45. The study of dry biological valve crosslinked with a combination of carbodiimide and polyphenol10.1093/rb/rbaa049 ↗
46. Hemocompatibility tuning of an innovative glutaraldehyde-free preparation strategy using riboflavin/UV crosslinking and electron irradiation of bovine pericardium for cardiac substitutes
47. Advancements and perspectives in the bioprosthetic heart valve: a comprehensive review on biomaterial processing and emerging polymeric materials10.1161/JAHA.125.043061 ↗
48. Polymeric prosthetic heart valves: a review of current technologies and future directions10.3389/fcvm.2023.1137827 ↗
49. Triglycidyl amine crosslinking combined with ethanol inhibits bioprosthetic heart valve calcification10.1016/j.athoracsur.2011.04.104 ↗
50. In vitro evaluation of cytotoxicity of diepoxy compounds used for biomaterial modification10.1002/jbm.820290707 ↗
51. Allografts and xenografts for right ventricular outflow tract reconstruction in Ross patients10.1093/ejcts/ezaa244 ↗
52. Diepoxy- versus glutaraldehyde-treated xenografts: outcomes of right ventricular outflow tract reconstruction in children10.1177/2150135119885900 ↗
53. Results of the Ross procedure in adults: a single-centre experience of 741 operations10.1093/ejcts/ezw047 ↗
54. Calcific degeneration as the main cause of porcine bioprosthetic valve failure10.1016/0002-9149(84)90638-6 ↗
55. Mechanism of efficacy of 2-amino oleic acid for inhibition of calcification of glutaraldehyde-pretreated porcine bioprosthetic heart valves10.1161/01.CIR.90.1.323 ↗
56. A randomized assessment of an advanced tissue preservation technology in the juvenile sheep model10.1016/j.jtcvs.2014.09.062 ↗
57. Treatment of bioprosthetic heart valve tissue with long chain alcohol solution to lower calcification potential10.1002/jbm.a.20129 ↗
58. Subclinical leaflet thrombosis in surgical and transcatheter bioprosthetic aortic valves: an observational study10.1016/S0140-6736(17)30757-2 ↗
59. Subclinical valve leaflet thrombosis following bioprosthetic aortic valve replacement10.1097/HCO.0000000000001161 ↗
60. Subclinical bioprosthetic aortic valve thrombosis: clinical and translational implications10.1097/HCO.0000000000000373 ↗
61. Possible Subclinical leaflet thrombosis in bioprosthetic aortic valves10.1056/NEJMoa1509233 ↗
62. Advanced glycation end products and oxidative stress in type 2 diabetes mellitus10.3390/biom5010194 ↗
63. Advanced glycation end-products: a review10.1007/s001250051591 ↗
64. Cross-linking of glycated collagen in the pathogenesis of arterial and myocardial stiffening of aging and diabetes10.1097/00004872-200301000-00002 ↗
65. Advanced glycation end products activate endothelium through signal-transduction receptor RAGE10.1161/hc0702.104183 ↗
66. Assessing pyridoxine adjuvant therapy effects on blood glucose levels in type 2 diabetes: a randomized clinical trial10.25122/jml-2023-0178 ↗
67. Effects of pyridoxamine in combined phase 2 studies of patients with type 1 and type 2 diabetes and overt nephropathy10.1159/000108104 ↗
68. Pyridorin in type 2 diabetic nephropathy10.1681/ASN.2011030272 ↗
69. Effect of vitamin B6 on pain, disease severity, and psychological profile of fibromyalgia patients; a randomized, double-blinded clinical trial10.1186/s12891-022-05637-7 ↗
70. Prevention of glutaraldehyde-fixed bioprosthetic heart valve calcification by alcohol pretreatment: further mechanistic studies
71. Effect of 2-amino oleic acid exposure conditions on the inhibition of calcification of glutaraldehyde cross-linked porcine aortic valves10.1002/jbm.820281214 ↗
72. Bioprosthetic heart valve heterograft biomaterials: structure, mechanical behavior and computational simulation10.1586/17434440.3.6.817 ↗