Iranian Red Crescent Medical Journal

Published by: Kowsar

Effects of Acellular Amniotic Membrane Matrix and Bone Marrow-Derived Mesenchymal Stem Cells in Improving Random Skin Flap Survival in Rats

Farzaneh Chehelcheraghi 1 , * , Hossein Eimani 1 , Seyed Homayoonsadraie 1 , Giti Torkaman 2 , Abdollah Amini 3 , Hamid Alavi Majd 4 and Hashem Shemshadi 5
Authors Information
1 Department of Anatomical Sciences, School of Medicine, Lorestan University of Medical Sciences, Khorramabad, IR Iran
2 Department of Physical Therapy, Faculty of Medical Sciences, Tarbiat Modares University, Tehran, IR Iran
3 Department of Anatomy, Medical Faculty, Shahid Beheshti University of Medical Sciences, Tehran, IR Iran
4 Department of Biostatistics, Faculty of Paramedicine, Shahid Beheshti University of Medical Sciences, Tehran, IR Iran
5 Department of Speech Therapy, University of Welfare and Rehabilitation Sciences, Tehran, IR Iran
Article information
  • Iranian Red Crescent Medical Journal: June 01, 2016, 18 (6); e25588
  • Published Online: June 1, 2016
  • Article Type: Research Article
  • Received: November 30, 2014
  • Revised: March 3, 2015
  • Accepted: March 28, 2015
  • DOI: 10.5812/ircmj.25588

To Cite: Chehelcheraghi F, Eimani H, Homayoonsadraie S, Torkaman G, Amini A, et al. Effects of Acellular Amniotic Membrane Matrix and Bone Marrow-Derived Mesenchymal Stem Cells in Improving Random Skin Flap Survival in Rats, Iran Red Crescent Med J. 2016 ; 18(6):e25588. doi: 10.5812/ircmj.25588.

Copyright © 2016, Iranian Red Crescent Medical Journal. This is an open-access article distributed under the terms of the Creative Commons Attribution-NonCommercial 4.0 International License ( which permits copy and redistribute the material just in noncommercial usages, provided the original work is properly cited.
1. Background
2. Objectives
3. Materials and Methods
4. Results
5. Discussion
  • 1. Bayat M, Chelcheraghi F, Piryaei A, Rakhshan M, Mohseniefar Z, Rezaie F, et al. The effect of 30-day pretreatment with pentoxifylline on the survival of a random skin flap in the rat: an ultrastructural and biomechanical evaluation. Med Sci Monit. 2006; 12(6)-7[PubMed]
  • 2. Shandalov Y, Egozi D, Koffler J, Dado-Rosenfeld D, Ben-Shimol D, Freiman A, et al. An engineered muscle flap for reconstruction of large soft tissue defects. Proc Natl Acad Sci U S A. 2014; 111(16): 6010-5[DOI][PubMed]
  • 3. Wang JC, Xia L, Song XB, Wang CE, Wei FC. Transplantation of hypoxia preconditioned bone marrow mesenchymal stem cells improves survival of ultra-long random skin flap. Chin Med J (Engl). 2011; 124(16): 2507-11[PubMed]
  • 4. Ohara H, Kishi K, Nakajima T. Rat dorsal paired island skin flaps: a precise model for flap survival evaluation. Keio J Med. 2008; 57(4): 211-6[PubMed]
  • 5. Yang M, Sheng L, Li H, Weng R, Li QF. Improvement of the skin flap survival with the bone marrow-derived mononuclear cells transplantation in a rat model. Microsurgery. 2010; 30(4): 275-81[DOI][PubMed]
  • 6. Sheng L, Yang M, Li H, Du Z, Yang Y, Li Q. Transplantation of adipose stromal cells promotes neovascularization of random skin flaps. Tohoku J Exp Med. 2011; 224(3): 229-34[DOI][PubMed]
  • 7. Reichenberger MA, Mueller W, Schafer A, Heimer S, Leimer U, Lass U, et al. Fibrin-embedded adipose derived stem cells enhance skin flap survival. Stem Cell Rev. 2012; 8(3): 844-53[DOI][PubMed]
  • 8. Fu X, Li H. Mesenchymal stem cells and skin wound repair and regeneration: possibilities and questions. Cell Tissue Res. 2009; 335(2): 317-21[DOI][PubMed]
  • 9. Shumakov VI, Onishchenko NA, Rasulov MF, Krasheninnikov ME, Zaidenov VA. [The use of pre-differentiated mesenchymal bone marrow stem cells for treatment of deep burn wounds]. Vestn Khir Im I I Grek. 2003; 162(4): 38-42[PubMed]
  • 10. Mansilla E, Marin GH, Sturla F, Drago HE, Gil MA, Salas E, et al. Human mesenchymal stem cells are tolerized by mice and improve skin and spinal cord injuries. Transplant Proc. 2005; 37(1): 292-4[DOI][PubMed]
  • 11. Wu Y, Chen L, Scott PG, Tredget EE. Mesenchymal stem cells enhance wound healing through differentiation and angiogenesis. Stem Cells. 2007; 25(10): 2648-59[DOI][PubMed]
  • 12. Wang J, Cui W, Ye J, Ji S, Zhao X, Zhan L, et al. A cellular delivery system fabricated with autologous BMSCs and collagen scaffold enhances angiogenesis and perfusion in ischemic hind limb. J Biomed Mater Res A. 2012; 100(6): 1438-47[DOI][PubMed]
  • 13. Allen P, Melero-Martin J, Bischoff J. Type I collagen, fibrin and PuraMatrix matrices provide permissive environments for human endothelial and mesenchymal progenitor cells to form neovascular networks. J Tissue Eng Regen Med. 2011; 5(4)-86[DOI][PubMed]
  • 14. Kannan RY, Salacinski HJ, Sales K, Butler P, Seifalian AM. The roles of tissue engineering and vascularisation in the development of micro-vascular networks: a review. Biomaterials. 2005; 26(14): 1857-75[DOI][PubMed]
  • 15. Niknejad H, Peirovi H, Jorjani M, Ahmadiani A, Ghanavi J, Seifalian AM. Properties of the amniotic membrane for potential use in tissue engineering. Eur Cell Mater. 2008; 15: 88-99[PubMed]
  • 16. Bourne GL. The microscopic anatomy of the human amnion and chorion. Am J Obstet Gynecol. 1960; 79: 1070-3[PubMed]
  • 17. Chen YJ, Chung MC, Jane Yao CC, Huang CH, Chang HH, Jeng JH, et al. The effects of acellular amniotic membrane matrix on osteogenic differentiation and ERK1/2 signaling in human dental apical papilla cells. Biomaterials. 2012; 33(2): 455-63[DOI][PubMed]
  • 18. Riau AK, Beuerman RW, Lim LS, Mehta JS. Preservation, sterilization and de-epithelialization of human amniotic membrane for use in ocular surface reconstruction. Biomaterials. 2010; 31(2): 216-25[DOI][PubMed]
  • 19. Malak TM, Ockleford CD, Bell SC, Dalgleish R, Bright N, Macvicar J. Confocal immunofluorescence localization of collagen types I, III, IV, V and VI and their ultrastructural organization in term human fetal membranes. Placenta. 1993; 14(4): 385-406[PubMed]
  • 20. Vorotnikova E, McIntosh D, Dewilde A, Zhang J, Reing JE, Zhang L, et al. Extracellular matrix-derived products modulate endothelial and progenitor cell migration and proliferation in vitro and stimulate regenerative healing in vivo. Matrix Biol. 2010; 29(8): 690-700[DOI][PubMed]
  • 21. Barkan D, Green JE, Chambers AF. Extracellular matrix: a gatekeeper in the transition from dormancy to metastatic growth. Eur J Cancer. 2010; 46(7): 1181-8[DOI][PubMed]
  • 22. Nelson CM, Bissell MJ. Of extracellular matrix, scaffolds, and signaling: tissue architecture regulates development, homeostasis, and cancer. Annu Rev Cell Dev Biol. 2006; 22: 287-309[DOI][PubMed]
  • 23. Taylor KR, Gallo RL. Glycosaminoglycans and their proteoglycans: host-associated molecular patterns for initiation and modulation of inflammation. FASEB J. 2006; 20(1): 9-22[DOI][PubMed]
  • 24. Nagase H, Visse R, Murphy G. Structure and function of matrix metalloproteinases and TIMPs. Cardiovasc Res. 2006; 69(3): 562-73[DOI][PubMed]
  • 25. Werner S, Grose R. Regulation of wound healing by growth factors and cytokines. Physiol Rev. 2003; 83(3): 835-70[DOI][PubMed]
  • 26. Bornstein P, Sage EH. Matricellular proteins: extracellular modulators of cell function. Curr Opin Cell Biol. 2002; 14(5): 608-16[PubMed]
  • 27. Azizi SA, Stokes D, Augelli BJ, DiGirolamo C, Prockop DJ. Engraftment and migration of human bone marrow stromal cells implanted in the brains of albino rats--similarities to astrocyte grafts. Proc Natl Acad Sci U S A. 1998; 95(7): 3908-13[PubMed]
  • 28. Strober W. Trypan blue exclusion test of cell viability. Curr Protoc Immunol. 2001; [DOI][PubMed]
  • 29. Yang L, Shirakata Y, Tokumaru S, Xiuju D, Tohyama M, Hanakawa Y, et al. Living skin equivalents constructed using human amnions as a matrix. J Dermatol Sci. 2009; 56(3): 188-95[DOI][PubMed]
  • 30. Portmann-Lanz CB, Ochsenbein-Kolble N, Marquardt K, Luthi U, Zisch A, Zimmermann R. Manufacture of a cell-free amnion matrix scaffold that supports amnion cell outgrowth in vitro. Placenta. 2007; 28(1): 6-13[DOI][PubMed]
  • 31. Zacchigna S, Papa G, Antonini A, Novati F, Moimas S, Carrer A, et al. Improved Survival of Ischemic Cutaneous and Musculocutaneous Flaps after Vascular Endothelial Growth Factor Gene Transfer Using Adeno-Associated Virus Vectors. Am J Pathol. 2005; 167(4): 981-91[DOI]
  • 32. Jeschke MG, Rose C, Angele P, Fuchtmeier B, Nerlich MN, Bolder U. Development of new reconstructive techniques: use of Integra in combination with fibrin glue and negative-pressure therapy for reconstruction of acute and chronic wounds. Plast Reconstr Surg. 2004; 113(2): 525-30[DOI][PubMed]
  • 33. Reichenberger MA, Heimer S, Schaefer A, Lass U, Gebhard MM, Germann G, et al. Adipose derived stem cells protect skin flaps against ischemia-reperfusion injury. Stem Cell Rev. 2012; 8(3): 854-62[DOI][PubMed]
  • 34. Chang EI, Bonillas RG, El-ftesi S, Chang EI, Ceradini DJ, Vial IN, et al. Tissue engineering using autologous microcirculatory beds as vascularized bioscaffolds. FASEB J. 2009; 23(3): 906-15[DOI][PubMed]
  • 35. Peng CC, Yang MH, Chiu WT, Chiu CH, Yang CS, Chen YW, et al. Composite nano-titanium oxide-chitosan artificial skin exhibits strong wound-healing effect-an approach with anti-inflammatory and bactericidal kinetics. Macromol Biosci. 2008; 8(4): 316-27[DOI][PubMed]
  • 36. Zebardast N, Lickorish D, Davies JE. Human umbilical cord perivascular cells (HUCPVC): A mesenchymal cell source for dermal wound healing. Organogenesis. 2010; 6(4): 197-203[DOI][PubMed]
  • 37. Han CM, Zhang LP, Sun JZ, Shi HF, Zhou J, Gao CY. Application of collagen-chitosan/fibrin glue asymmetric scaffolds in skin tissue engineering. J Zhejiang Univ Sci B. 2010; 11(7): 524-30[DOI][PubMed]
  • 38. Bauer SM, Goldstein LJ, Bauer RJ, Chen H, Putt M, Velazquez OC. The bone marrow-derived endothelial progenitor cell response is impaired in delayed wound healing from ischemia. J Vasc Surg. 2006; 43(1): 134-41[DOI][PubMed]
  • 39. Walgenbach KJ, Voigt M, Riabikhin AW, Andree C, Schaefer DJ, Galla TJ, et al. Tissue engineering in plastic reconstructive surgery. Anat Rec. 2001; 263(4): 372-8[PubMed]
  • 40. Wilshaw SP, Kearney JN, Fisher J, Ingham E. Production of an acellular amniotic membrane matrix for use in tissue engineering. Tissue Eng. 2006; 12(8): 2117-29[DOI][PubMed]
  • 41. Hughes D. Transvascular fluid dynamics. Vet Anaesth Analgesia. 2000; 27(1): 63-9
  • 42. Dua HS, Gomes JA, King AJ, Maharajan VS. The amniotic membrane in ophthalmology. Surv Ophthalmol. 2004; 49(1): 51-77[PubMed]
  • 43. Faulk WP, Matthews R, Stevens PJ, Bennett JP, Burgos H, Hsi BL. Human amnion as an adjunct in wound healing. Lancet. 1980; 1(8179): 1156-8[PubMed]
  • 44. Kneser U, Voogd A, Ohnolz J, Buettner O, Stangenberg L, Zhang YH, et al. Fibrin gel-immobilized primary osteoblasts in calcium phosphate bone cement: in vivo evaluation with regard to application as injectable biological bone substitute. Cells Tissues Organs. 2005; 179(4): 158-69[DOI][PubMed]
  • 45. Mao J, Zhao L, De Yao K, Shang Q, Yang G, Cao Y. Study of novel chitosan-gelatin artificial skin in vitro. J Biomed Mater Res A. 2003; 64(2): 301-8[DOI][PubMed]
  • 46. Wang TW, Huang YC, Sun JS, Lin FH. Organotypic keratinocyte-fibroblast cocultures on a bilayer gelatin scaffold as a model of skin equivalent. Biomed Sci Instrum. 2003; 39: 523-8[PubMed]
  • 47. Wechselberger G, Russell RC, Neumeister MW, Schoeller T, Piza-Katzer H, Rainer C. Successful transplantation of three tissue-engineered cell types using capsule induction technique and fibrin glue as a delivery vehicle. Plast Reconstr Surg. 2002; 110(1): 123-9[PubMed]
  • 48. Yoon IS, Chung CW, Sung JH, Cho HJ, Kim JS, Shim WS, et al. Proliferation and chondrogenic differentiation of human adipose-derived mesenchymal stem cells in porous hyaluronic acid scaffold. J Biosci Bioeng. 2011; 112(4): 402-8[DOI][PubMed]
  • 49. Quirinia A, Viidik A. Ischemia in wound healing. II: Design of a flap model--biomechanical properties. Scand J Plast Reconstr Surg Hand Surg. 1992; 26(2): 133-9[PubMed]
  • 50. Quirinia A, Jensen FT, Viidik A. Ischemia in wound healing. I: Design of a flap model--changes in blood flow. Scand J Plast Reconstr Surg Hand Surg. 1992; 26(1): 21-8[PubMed]
Creative Commons License Except where otherwise noted, this work is licensed under Creative Commons Attribution Non Commercial 4.0 International License .

Search Relations:



Create Citiation Alert
via Google Reader

Readers' Comments