{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,30]],"date-time":"2026-09-30T13:44:07Z","timestamp":1790775847603,"version":"4.1.0"},"reference-count":26,"publisher":"ASME International","issue":"6","content-domain":{"domain":["asmedigitalcollection.asme.org"],"crossmark-restriction":true},"short-container-title":[],"published-print":{"date-parts":[[2009,6,1]]},"abstract":"<jats:p>The relationship between microstructural features and macroscopic mechanical properties of engineered tissues was investigated in pure and mixed composite scaffolds consisting of collagen Type I and fibrin proteins containing embedded smooth muscle cells. In order to vary the matrix microstructure, fibrin polymerization in mixed constructs was initiated using either the blood-derived enzyme thrombin or the snake venom-derived enzyme ancrod, each at low and high concentrations. Microstructural features of the matrix were quantified by analysis of high resolution scanning electron micrographs. Mechanical properties of the scaffolds were assessed by uniaxial tensile testing as well as creep testing. Viscoelastic parameters were determined by fitting creep data to Burger\u2019s four-parameter model. Oscillatory dynamic mechanical testing was used to determine the storage modulus, loss modulus, and phase shift of each matrix type. Mixed composite scaffolds exhibited improved tensile stiffness and strength, relative to pure collagen matrices, as well as decreased deformation and slower relaxation in creep tests. Storage and loss moduli were increased in mixed composites compared with pure collagen, while phase shift was reduced. A correlation analysis showed that the number of fiber bundles per unit volume was positively correlated with matrix modulus, strength, and dynamic moduli, though this parameter was negatively correlated with phase shift. Fiber diameter also was negatively correlated with scaffold strength. This study demonstrates how microstructural features can be related to the mechanical function of protein matrices and provides insight into structure-function relationships in such materials. This information can be used to identify and promote desirable microstructural features when designing biomaterials and engineered tissues.<\/jats:p>","DOI":"10.1115\/1.3128673","type":"journal-article","created":{"date-parts":[[2009,5,12]],"date-time":"2009-05-12T22:24:21Z","timestamp":1242167061000},"update-policy":"https:\/\/doi.org\/10.1115\/crossmarkpolicy-asme","source":"Crossref","is-referenced-by-count":32,"title":["Microstructure and Mechanics of Collagen-Fibrin Matrices Polymerized Using Ancrod Snake Venom Enzyme"],"prefix":"10.1115","volume":"131","author":[{"given":"Shaneen L.","family":"Rowe","sequence":"first","affiliation":[{"name":"Rensselaer Polytechnic Institute, Troy, NY 12180"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jan P.","family":"Stegemann","sequence":"additional","affiliation":[{"name":"Rensselaer Polytechnic Institute, Troy, NY 12180"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"33","published-online":{"date-parts":[[2009,5,8]]},"reference":[{"issue":"3","key":"2019100323153245600_c1","doi-asserted-by":"publisher","first-page":"481","DOI":"10.1016\/S0142-9612(02)00361-7","article-title":"Microarchitectural and Mechanical Characterization of Oriented Porous Polymer Scaffolds","volume":"24","author":"Lin","journal-title":"Biomaterials","ISSN":"https:\/\/id.crossref.org\/issn\/0142-9612","issn-type":"print"},{"issue":"4","key":"2019100323153245600_c2","doi-asserted-by":"publisher","first-page":"610","DOI":"10.1115\/1.2205371","article-title":"A Structural Model for the Flexural Mechanics of Nonwoven Tissue Engineering Scaffolds","volume":"128","author":"Engelmayr","journal-title":"ASME J. Biomech. Eng.","ISSN":"https:\/\/id.crossref.org\/issn\/0148-0731","issn-type":"print"},{"issue":"5","key":"2019100323153245600_c3","doi-asserted-by":"publisher","first-page":"742","DOI":"10.1115\/1.1992525","article-title":"The Development of Structural and Mechanical Anisotropy in Fibroblast Populated Collagen Gels","volume":"127","author":"Thomopoulos","journal-title":"ASME J. Biomech. Eng.","ISSN":"https:\/\/id.crossref.org\/issn\/0148-0731","issn-type":"print"},{"issue":"6","key":"2019100323153245600_c4","doi-asserted-by":"publisher","first-page":"536","DOI":"10.1115\/1.1411971","article-title":"Mechanical Properties and Microstructure of Intraluminal Thrombus From Abdominal Aortic Aneurysm","volume":"123","author":"Wang","journal-title":"ASME J. Biomech. Eng.","ISSN":"https:\/\/id.crossref.org\/issn\/0148-0731","issn-type":"print"},{"issue":"4","key":"2019100323153245600_c5","doi-asserted-by":"publisher","first-page":"611","DOI":"10.1115\/1.2746387","article-title":"Multiscale, Structure-Based Modeling for the Elastic Mechanical Behavior of Arterial Walls","volume":"129","author":"Stylianopoulos","journal-title":"ASME J. Biomech. Eng.","ISSN":"https:\/\/id.crossref.org\/issn\/0148-0731","issn-type":"print"},{"key":"2019100323153245600_c6","doi-asserted-by":"publisher","first-page":"1651","DOI":"10.1016\/j.jbiomech.2005.05.003","article-title":"A Structural Basis for the Aortic Stress-Strain Relation in Uniaxial Tension","volume":"39","author":"Sokolis","journal-title":"J. Biomech.","ISSN":"https:\/\/id.crossref.org\/issn\/0021-9290","issn-type":"print"},{"issue":"2","key":"2019100323153245600_c7","doi-asserted-by":"publisher","first-page":"214","DOI":"10.1115\/1.1449904","article-title":"Tensile Mechanical Properties of Three-Dimensional Type I Collagen Extracellular Matrices With Varied Microstructure","volume":"124","author":"Roeder","journal-title":"ASME J. Biomech. Eng.","ISSN":"https:\/\/id.crossref.org\/issn\/0148-0731","issn-type":"print"},{"key":"2019100323153245600_c8","doi-asserted-by":"publisher","first-page":"841","DOI":"10.1002\/bip.21024","article-title":"Influence of Chondroitin Sulfate on Collagen Gel Structure and Mechanical Properties at Physiologically Relevant Levels","volume":"89","author":"Stuart","journal-title":"Biopolymers","ISSN":"https:\/\/id.crossref.org\/issn\/0006-3525","issn-type":"print"},{"issue":"11","key":"2019100323153245600_c9","doi-asserted-by":"publisher","first-page":"2942","DOI":"10.1021\/bm0602233","article-title":"Interpenetrating Collagen-Fibrin Composite Matrices With Varying Protein Contents and Ratios","volume":"7","author":"Rowe","journal-title":"Biomacromolecules","ISSN":"https:\/\/id.crossref.org\/issn\/1525-7797","issn-type":"print"},{"issue":"17","key":"2019100323153245600_c10","doi-asserted-by":"publisher","first-page":"3699","DOI":"10.1016\/j.biomaterials.2003.10.073","article-title":"Properties of Engineered Vascular Constructs Made From Collagen, Fibrin, and Collagen-Fibrin Mixtures","volume":"25","author":"Cummings","journal-title":"Biomaterials","ISSN":"https:\/\/id.crossref.org\/issn\/0142-9612","issn-type":"print"},{"issue":"3","key":"2019100323153245600_c11","doi-asserted-by":"publisher","first-page":"618","DOI":"10.1016\/j.cardiores.2007.04.018","article-title":"Functional Tissue-Engineered Blood Vessels From Bone Marrow Progenitor Cells","volume":"75","author":"Liu","journal-title":"Cardiovasc. Res.","ISSN":"https:\/\/id.crossref.org\/issn\/0008-6363","issn-type":"print"},{"issue":"1","key":"2019100323153245600_c12","doi-asserted-by":"publisher","first-page":"25","DOI":"10.1161\/01.RES.0000196867.12470.84","article-title":"Small-Diameter Artificial Arteries Engineered In Vitro","volume":"98","author":"Isenberg","journal-title":"Circ. Res.","ISSN":"https:\/\/id.crossref.org\/issn\/0009-7330","issn-type":"print"},{"key":"2019100323153245600_c13","doi-asserted-by":"crossref","first-page":"11","DOI":"10.1111\/j.1749-6632.2001.tb03491.x","article-title":"The Structure and Biological Features of Fibrinogen and Fibrin","volume":"936","author":"Mosesson","journal-title":"Ann. N. Y. Acad. Sci.","ISSN":"https:\/\/id.crossref.org\/issn\/0077-8923","issn-type":"print"},{"key":"2019100323153245600_c14","doi-asserted-by":"publisher","first-page":"1171","DOI":"10.1016\/j.toxicon.2005.02.016","article-title":"Practical Applications of Snake Venom Toxins in Haemostasis","volume":"45","author":"Marsh","journal-title":"Toxicon","ISSN":"https:\/\/id.crossref.org\/issn\/0041-0101","issn-type":"print"},{"key":"2019100323153245600_c15","doi-asserted-by":"publisher","first-page":"843","DOI":"10.1007\/s00018-003-3325-z","article-title":"Snake Venom Thrombin-Like Enzymes: From Reptilase to Now","volume":"61","author":"Castro","journal-title":"Cell. Mol. Life Sci.","ISSN":"https:\/\/id.crossref.org\/issn\/1420-682X","issn-type":"print"},{"key":"2019100323153245600_c16","first-page":"303","article-title":"Ancrod: Understanding the Agent","volume":"9","author":"Illig","journal-title":"Semin Vasc. Surg.","ISSN":"https:\/\/id.crossref.org\/issn\/0895-7967","issn-type":"print"},{"key":"2019100323153245600_c17","first-page":"H629","article-title":"Role of Fibrinopeptide B Release: Comparison of Fibrins Produced by Thrombin and Ancrod","volume":"232","author":"Shen","journal-title":"Am. J. Physiol.","ISSN":"https:\/\/id.crossref.org\/issn\/0002-9513","issn-type":"print"},{"key":"2019100323153245600_c18","doi-asserted-by":"publisher","first-page":"1176","DOI":"10.1115\/1.2073487","article-title":"Viscoelastic Testing Methodologies for Tissue Engineered Blood Vessels","volume":"127","author":"Berglund","journal-title":"ASME J. Biomech. Eng.","ISSN":"https:\/\/id.crossref.org\/issn\/0148-0731","issn-type":"print"},{"issue":"5","key":"2019100323153245600_c19","doi-asserted-by":"publisher","first-page":"726","DOI":"10.1007\/s10439-005-9058-4","article-title":"Development of Ligament-Like Structural Organization and Properties in Cell-Seeded Collagen Scaffolds In Vitro","volume":"34","author":"Gentleman","journal-title":"Ann. Biomed. Eng.","ISSN":"https:\/\/id.crossref.org\/issn\/0090-6964","issn-type":"print"},{"key":"2019100323153245600_c20","doi-asserted-by":"publisher","first-page":"241","DOI":"10.1089\/107632704322791880","article-title":"Design and Application of a Test System for Viscoelastic Characterization of Collagen Gels","volume":"10","author":"Krishnan","journal-title":"Tissue Eng.","ISSN":"https:\/\/id.crossref.org\/issn\/1076-3279","issn-type":"print"},{"key":"2019100323153245600_c21","doi-asserted-by":"publisher","first-page":"761","DOI":"10.1016\/j.jbiomech.2004.05.019","article-title":"Dynamic Mechanical Characteristics of Intact and Structurally Modified Bovine Pericardial Tissues","volume":"38","author":"Mavrilas","journal-title":"J. Biomech.","ISSN":"https:\/\/id.crossref.org\/issn\/0021-9290","issn-type":"print"},{"key":"2019100323153245600_c22","doi-asserted-by":"publisher","first-page":"388","DOI":"10.1021\/ja01194a066","article-title":"Preparation and Properties of Serum and Plasma Proteins. VII. The Conversion of Human Fibrinogen to Fibrin Under Various Conditions","volume":"69","author":"Ferry","journal-title":"J. Am. Chem. Soc.","ISSN":"https:\/\/id.crossref.org\/issn\/0002-7863","issn-type":"print"},{"key":"2019100323153245600_c23","doi-asserted-by":"crossref","first-page":"862","DOI":"10.1016\/S0021-9258(17)36175-6","article-title":"Effects of Thrombospondin on Fibrin Polymerization and Structure","volume":"261","author":"Bale","journal-title":"J. Biol. Chem.","ISSN":"https:\/\/id.crossref.org\/issn\/0021-9258","issn-type":"print"},{"key":"2019100323153245600_c24","doi-asserted-by":"publisher","first-page":"59","DOI":"10.1016\/j.actbio.2006.08.006","article-title":"Influence of Thrombin Concentration on the Mechanical and Morphological Properties of Cell-Seeded Fibrin Hydrogels","volume":"3","author":"Rowe","journal-title":"Acta Biomater.","ISSN":"https:\/\/id.crossref.org\/issn\/1742-7061","issn-type":"print"},{"key":"2019100323153245600_c25","doi-asserted-by":"publisher","first-page":"1871","DOI":"10.1016\/S0140-6736(06)69776-6","article-title":"Intravenous Ancrod for Acute Ischaemic Stroke in the European Stroke Treatment With Ancrod Trial: A Randomised Controlled Trial","volume":"368","author":"Hennerici","journal-title":"Lancet","ISSN":"https:\/\/id.crossref.org\/issn\/0140-6736","issn-type":"print"},{"key":"2019100323153245600_c26","doi-asserted-by":"publisher","first-page":"58","DOI":"10.1006\/jsre.1996.0081","article-title":"Adhesion Prevention With Ancrod Released Via a Tissue-Adherent Hydrogel","volume":"61","author":"Chowdhury","journal-title":"J. Surg. Res.","ISSN":"https:\/\/id.crossref.org\/issn\/0022-4804","issn-type":"print"}],"container-title":["Journal of Biomechanical Engineering"],"original-title":[],"language":"en","link":[{"URL":"http:\/\/asmedigitalcollection.asme.org\/biomechanical\/article-pdf\/doi\/10.1115\/1.3128673\/5552757\/061012_1.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"syndication"},{"URL":"http:\/\/asmedigitalcollection.asme.org\/biomechanical\/article-pdf\/doi\/10.1115\/1.3128673\/5552757\/061012_1.pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2021,10,5]],"date-time":"2021-10-05T09:04:55Z","timestamp":1633424695000},"score":1,"resource":{"primary":{"URL":"https:\/\/asmedigitalcollection.asme.org\/biomechanical\/article\/doi\/10.1115\/1.3128673\/399688\/Microstructure-and-Mechanics-of-CollagenFibrin"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2009,5,8]]},"references-count":26,"journal-issue":{"issue":"6","published-print":{"date-parts":[[2009,6,1]]}},"URL":"https:\/\/doi.org\/10.1115\/1.3128673","relation":{},"ISSN":["0148-0731","1528-8951"],"issn-type":[{"value":"0148-0731","type":"print"},{"value":"1528-8951","type":"electronic"}],"subject":[],"published":{"date-parts":[[2009,5,8]]},"article-number":"061012"}}