Clotting Mimicry from Robust Hemostatic Bandages Based on Self-Assembling Peptides

ACS Nano

Volumn 9, Issue 9, 2015, Pages 9394-9406

  Hsu, Bryan B ^a,b   Conway, William ^a   Tschabrunn, Cory M ^c   Mehta, Manav ^d   Perez Cuevas, Monica B ^e   Zhang, Shuguang ^a   Hammond, Paula T ^a,b  

^a MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^b Massachusetts Institute of Technology Cambridge   (United States)

^c BETH ISRAEL DEACONESS MEDICAL CENTER   (United States)

^d 3 D Matrix Medical Technology   (United States)

^e Georgia Institute of Technology   (United States)

Author keywords

bleeding; blood clots; hemorrhage; nanofibers; wound dressings

Indexed keywords

BIOCOMPATIBILITY; BIODEGRADATION; BLOOD; PEPTIDES;

BLEEDING; BLOOD CLOTS; HEMORRHAGE; PHYSIOLOGICAL CONDITION; SELF-ASSEMBLING PEPTIDES; TEMPERATURE CONDITIONS; THIN-FILM COATINGS; WOUND DRESSINGS;

NANOFIBERS;

HEMOSTATIC AGENT; NANOFIBER; PEPTIDE;

ANIMAL; BANDAGE; BLOOD CLOTTING; CHEMISTRY; DISEASE MODEL; DRUG EFFECTS; HEMORRHAGE; PIG; WOUND CLOSURE; WOUND HEALING;

ANIMALS; BANDAGES; BLOOD COAGULATION; DISEASE MODELS, ANIMAL; HEMORRHAGE; HEMOSTATICS; NANOFIBERS; PEPTIDES; SWINE; WOUND CLOSURE TECHNIQUES; WOUND HEALING;

EID: 84942134884     PISSN: 19360851     EISSN: 1936086X     Source Type: Journal    
DOI: 10.1021/acsnano.5b02374     Document Type: Article

References (46)

1. Kelly, J. F.; Ritenour, A. E.; McLaughlin, D. F.; Bagg, K. A.; Apodaca, A. N.; Mallak, C. T.; Pearse, L.; Lawnick, M. M.; Champion, H. R.; Wade, C. E. et al. Injury Severity and Causes of Death from Operation Iraqi Freedom and Operation Enduring Freedom: 2003-2004 Versus 2006 J. Trauma 2008, 64, S21-S26 10.1097/TA.0b013e318160b9fb
2. Evans, J. A.; van Wessem, K. J. P.; McDougall, D.; Lee, K. A.; Lyons, T.; Balogh, Z. J. Epidemiology of Traumatic Deaths: Comprehensive Population-Based Assessment World J. Surg. 2010, 34, 158-163 10.1007/s00268-009-0266-1
3. Belmont, P. J.; Schoenfeld, A. J.; Goodman, G. Epidemiology of Combat Wounds in Operation Iraqi Freedom and Operation Enduring Freedom: Orthopaedic Burden of Disease J. Surg. Orthop. Adv. 2010, 19, 2-7
4. Brohi, K.; Cohen, M. J.; Ganter, M. T.; Schultz, M. J.; Levi, M.; Mackersie, R. C.; Pittet, J. F. Acute Coagulopathy of Trauma: Hypoperfusion Induces Systemic Anticoagulation and Hyperfibrinolysis J. Trauma 2008, 64, 1211-7 discussion 1217. 10.1097/TA.0b013e318169cd3c
5. Brohi, K.; Singh, J.; Heron, M.; Coats, T. Acute Traumatic Coagulopathy J. Trauma 2003, 54, 1127-1130 10.1097/01.TA.0000069184.82147.06
6. Niles, S. E.; McLaughlin, D. F.; Perkins, J. G.; Wade, C. E.; Li, Y.; Spinella, P. C.; Holcomb, J. B. Increased Mortality Associated with the Early Coagulopathy of Trauma in Combat Casualties J. Trauma 2008, 64, 1459-63 discussion 1463-5. 10.1097/TA.0b013e318174e8bc
7. Kheirabadi, B. Evaluation of Topical Hemostatic Agents for Combat Wound Treatment U.S. Army Med. Dep. J. 2011, 25-37
8. Achneck, H. E.; Sileshi, B.; Jamiolkowski, R. M.; Albala, D. M.; Shapiro, M. L.; Lawson, J. H. A Comprehensive Review of Topical Hemostatic Agents: Efficacy and Recommendations for Use Ann. Surg. 2010, 251, 217-228 10.1097/SLA.0b013e3181c3bcca
9. Gordy, S. D.; Rhee, P.; Schreiber, M. A. Military Applications of Novel Hemostatic Devices Expert Rev. Med. Devices 2011, 8, 41-47 10.1586/erd.10.69
10. Capturing the Full Power of Biomaterials for Military Medicine: Report of a Workshop; The National Academies Press: Washington, D.C., 2004.
11. Bennett, B. L.; Littlejohn, L. F.; Kheirabadi, B. S.; Butler, F. K.; Kotwal, R. S.; Dubick, M. A.; Bailey, J. A. Management of External Hemorrhage in Tactical Combat Casualty Care: Chitosan-Based Hemostatic Gauze Dressings-Tccc Guidelines-Change 13-05 J. Spec. Oper. Med. 2014, 14, 40-57
12. Rall, J. M.; Cox, J. M.; Songer, A. G.; Cestero, R. F.; Ross, J. D. Comparison of Novel Hemostatic Dressings with Quikclot Combat Gauze in a Standardized Swine Model of Uncontrolled Hemorrhage J. Trauma Acute Care Surg. 2013, 75, S150-6 10.1097/TA.0b013e318299d909
13. Grissom, T. E.; Fang, R. Topical Hemostatic Agents and Dressings in the Prehospital Setting Curr. Opin. Anaesthesiol. 2015, 28, 210-6 10.1097/ACO.0000000000000166
14. Ellis-Behnke, R. At the Nanoscale: Nanohemostat, a New Class of Hemostatic Agent Wiley Interdiscip. Rev. Nanomed. Nanobiotechnol. 2011, 3, 70-78 10.1002/wnan.110
15. Arosio, P.; Owczarz, M.; Wu, H.; Butté, A.; Morbidelli, M. End-to-End Self-Assembly of Rada 16-I Nanofibrils in Aqueous Solutions Biophys. J. 2012, 102, 1617-1626 10.1016/j.bpj.2012.03.012
16. Luo, Z.; Wang, S.; Zhang, S. Fabrication of Self-Assembling D-Form Peptide Nanofiber Scaffold D-Eak16 for Rapid Hemostasis Biomaterials 2011, 32, 2013-2020 10.1016/j.biomaterials.2010.11.049
17. Yokoi, H.; Kinoshita, T.; Zhang, S. G. Dynamic Reassembly of Peptide Rada16 Nanofiber Scaffold Proc. Natl. Acad. Sci. U. S. A. 2005, 102, 8414-8419 10.1073/pnas.0407843102
18. Ye, Z.; Zhang, H.; Luo, H.; Wang, S.; Zhou, Q.; Du, X.; Tang, C.; Chen, L.; Liu, J.; Shi, Y.-K. et al. Temperature and Ph Effects on Biophysical and Morphological Properties of Self-Assembling Peptide Rada16-1 J. Pept. Sci. 2008, 14, 152-162 10.1002/psc.988
19. Cormier, A. R.; Ruiz-Orta, C.; Alamo, R. G.; Paravastu, A. K. Solid State Self-Assembly Mechanism of Rada16-I Designer Peptide Biomacromolecules 2012, 13, 1794-1804 10.1021/bm300313h
20. Wang, T.; Zhong, X.; Wang, S.; Lv, F.; Zhao, X. Molecular Mechanisms of Rada16-1 Peptide on Fast Stop Bleeding in Rat Models Int. J. Mol. Sci. 2012, 13, 15279-15290 10.3390/ijms131115279
21. Ellis-Behnke, R. G.; Liang, Y.-X.; Tay, D. K. C.; Kau, P. W. F.; Schneider, G. E.; Zhang, S.; Wu, W.; So, K.-F. Nano Hemostat Solution: Immediate Hemostasis at the Nanoscale Nanomedicine 2006, 2, 207-15 10.1016/j.nano.2006.08.001
22. Gelain, F.; Horii, A.; Zhang, S. Designer Self-Assembling Peptide Scaffolds for 3-D Tissue Cell Cultures and Regenerative Medicine Macromol. Biosci. 2007, 7, 544-551 10.1002/mabi.200700033
23. Ho, D.; Fitzgerald, M.; Bartlett, C. A.; Zdyrko, B.; Luzinov, I. A.; Dunlop, S. A.; Iyer, K. S. The Effects of Concentration-Dependent Morphology of Self-Assembling Rada16 Nanoscaffolds on Mixed Retinal Cultures Nanoscale 2011, 3, 907-910 10.1039/C0NR00666A
24. Song, H.; Zhang, L.; Zhao, X. Hemostatic Efficacy of Biological Self-Assembling Peptide Nanofibers in a Rat Kidney Model Macromol. Biosci. 2010, 10, 33-39 10.1002/mabi.200900129
25. Decher, G. Fuzzy Nanoassemblies: Toward Layered Polymeric Multicomposites Science 1997, 277, 1232-1237 10.1126/science.277.5330.1232
26. Shiratori, S. S.; Rubner, M. F. Ph-Dependent Thickness Behavior of Sequentially Adsorbed Layers of Weak Polyelectrolytes Macromolecules 2000, 33, 4213-4219 10.1021/ma991645q
27. Xu, L.; Ankner, J. F.; Sukhishvili, S. A. Steric Effects in Ionic Pairing and Polyelectrolyte Interdiffusion within Multilayered Films: A Neutron Reflectometry Study Macromolecules 2011, 44, 6518-6524 10.1021/ma200986d
28. Clark, S. L.; Hammond, P. T. The Role of Secondary Interactions in Selective Electrostatic Multilayer Deposition Langmuir 2000, 16, 10206-10214 10.1021/la000418a
29. Gilbert, J. B.; Rubner, M. F.; Cohen, R. E. Depth-Profiling X-Ray Photoelectron Spectroscopy (Xps) Analysis of Interlayer Diffusion in Polyelectrolyte Multilayers Proc. Natl. Acad. Sci. U. S. A. 2013, 110, 6651-6656 10.1073/pnas.1222325110
30. Sui, Z.; Salloum, D.; Schlenoff, J. B. Effect of Molecular Weight on the Construction of Polyelectrolyte Multilayers: Stripping Versus Sticking Langmuir 2003, 19, 2491-2495 10.1021/la026531d
31. Halthur, T. J.; Claesson, P. M.; Elofsson, U. M. Stability of Polypeptide Multilayers as Studied by in Situ Ellipsometry: Effects of Drying and Post-Buildup Changes in Temperature and Ph J. Am. Chem. Soc. 2004, 126, 17009-17015 10.1021/ja0464645
32. Raposo, M.; Pontes, R. S.; Mattoso, L. H. C.; Oliveira, O. N. Kinetics of Adsorption of Poly(O-Methoxyaniline) Self-Assembled Films Macromolecules 1997, 30, 6095-6101 10.1021/ma970228f
33. Wang, L.; Wang, L.; Su, Z. Surface Defects in Polyelectrolyte Multilayers: Effects of Drying and Deposition Cycle Soft Matter 2011, 7, 4851-4855 10.1039/c1sm05158j
34. Decher, G.; Lvov, Y.; Schmitt, J. Proof of Multilayer Structural Organization in Self-Assembled Polycation Polyanion Molecular Films Thin Solid Films 1994, 244, 772-777 10.1016/0040-6090(94)90569-X
35. Lvov, Y.; Ariga, K.; Onda, M.; Ichinose, I.; Kunitake, T. A Careful Examination of the Adsorption Step in the Alternate Layer-by-Layer Assembly of Linear Polyanion and Polycation Colloids Surf., A 1999, 146, 337-346 10.1016/S0927-7757(98)00789-4
36. Krogman, K. C.; Lowery, J. L.; Zacharia, N. S.; Rutledge, G. C.; Hammond, P. T. Spraying Asymmetry into Functional Membranes Layer-by-Layer Nat. Mater. 2009, 8, 512-518 10.1038/nmat2430
37. Krogman, K. C.; Zacharia, N. S.; Schroeder, S.; Hammond, P. T. Automated Process for Improved Uniformity and Versatility of Layer-by-Layer Deposition Langmuir 2007, 23, 3137-3141 10.1021/la063085b
38. Krogman, K. C.; Cohen, R. E.; Hammond, P. T.; Rubner, M. F.; Wang, B. N. Industrial-Scale Spray Layer-by-Layer Assembly for Production of Biomimetic Photonic Systems Bioinspiration Biomimetics 2013, 8, 045005 10.1088/1748-3182/8/4/045005
39. Shukla, A.; Fang, J. C.; Puranam, S.; Jensen, F. R.; Hammond, P. T. Hemostatic Multilayer Coatings Adv. Mater. 2012, 24, 492-496 10.1002/adma.201103794
40. Andrews, D. A.; Low, P. S. Role of Red Blood Cells in Thrombosis Curr. Opin. Hematol. 1999, 6, 76-82 10.1097/00062752-199903000-00004
41. Monroe, D.; Hoffman, M.; Roberts, H. R. Platelets and Thrombin Generation Arterioscler., Thromb., Vasc. Biol. 2002, 22, 1381-1389 10.1161/01.ATV.0000031340.68494.34
42. Cheng, T.-Y.; Wu, H.-C.; Huang, M.-Y.; Chang, W.-H.; Lee, C.-H.; Wang, T.-W. Self-Assembling Functionalized Nanopeptides for Immediate Hemostasis and Accelerative Liver Tissue Regeneration Nanoscale 2013, 5, 2734-2744 10.1039/c3nr33710c
43. Rao, S. B.; Sharma, C. P. Use of Chitosan as a Biomaterial: Studies on Its Safety and Hemostatic Potential J. Biomed. Mater. Res. 1997, 34, 21-28 10.1002/(SICI)1097-4636(199701)34:1<21::AID-JBM4>3.0.CO;2-P
44. Klokkevold, P. R.; Fukayama, H.; Sung, E. C.; Bertolami, C. N. The Effect of Chitosan (Poly-N-Acetyl Glucosamine) on Lingual Hemostasis in Heparinized Rabbits J. Oral Maxillofac. Surg. 1999, 57, 49-52 10.1016/S0278-2391(99)90632-8
45. Dowling, M. B.; Kumar, R.; Keibler, M. A.; Hess, J. R.; Bochicchio, G. V.; Raghavan, S. R. A Self-Assembling Hydrophobically Modified Chitosan Capable of Reversible Hemostatic Action Biomaterials 2011, 32, 3351-3357 10.1016/j.biomaterials.2010.12.033
46. Pusateri, A. E.; McCarthy, S. J.; Gregory, K. W.; Harris, R. A.; Cardenas, L.; McManus, A. T.; Goodwin, C. W., Jr. Effect of a Chitosan-Based Hemostatic Dressing on Blood Loss and Survival in a Model of Severe Venous Hemorrhage and Hepatic Injury in Swine J. Trauma 2003, 54, 177-82 10.1097/00005373-200301000-00023