Human Amniotic Membrane as a Biological Source for Regenerative Medicine

  • Mazaher Gholipourmalekabadi
  • Narendra Pal Singh Chauhan
  • Behrouz Farhadihosseinabad
  • Ali SamadikuchaksaraeiEmail author
Part of the Stem Cell Biology and Regenerative Medicine book series (STEMCELL)


The application of the matrix and cellular component of amniotic membrane to increase the regenerative potential of injured tissue dates back to several decades ago. The positive effects of this application have led to the in-depth studies of the properties of human amniotic membrane as a biological modality for regenerative medicine. In this chapter, the structural components and properties of human amniotic membrane and some of its applications are described.


Amnion Regenerative medicine Tissue engineering 



  1. Abbasi-Montazeri E, Khosravi AD, Feizabadi MM, Goodarzi H, Khoramrooz SS, Mirzaii M, Kalantar E, Darban-Sarokhalil D (2013) The prevalence of methicillin resistant Staphylococcus aureus (MRSA) isolates with high-level mupirocin resistance from patients and personnel in a burn center. Burns 39:650–654PubMedCrossRefGoogle Scholar
  2. Alemdaroğlu C, Değim Z, Çelebi N, Zor F, Özturk S, Erdoğan D (2006) An investigation on burn wound healing in rats with chitosan gel formulation containing epidermal growth factor. Burns 32:319–327PubMedCrossRefGoogle Scholar
  3. Alemdaroğlu C, Degim Z, Celebi N, Şengezer M, Alömeroglu M, Nacar A (2008) Investigation of epidermal growth factor containing liposome formulation effects on burn wound healing. J Biomed Mater Res A 85:271–283PubMedCrossRefGoogle Scholar
  4. Alibardi L (2003) Adaptation to the land: the skin of reptiles in comparison to that of amphibians and endotherm amniotes. J Exp Zool B Mol Dev Evol 298:12–41PubMedCrossRefGoogle Scholar
  5. Aplin J, Campbell S, Allen TD (1985) The extracellular matrix of human amniotic epithelium: ultrastructure, composition and deposition. J Cell Sci 79:119–136PubMedGoogle Scholar
  6. Atiyeh BS, Hayek SN, Gunn SW (2005) New technologies for burn wound closure and healing—review of the literature. Burns 31:944–956PubMedCrossRefGoogle Scholar
  7. Atiyeh BS, Costagliola M, Hayek SN, Dibo SA (2007) Effect of silver on burn wound infection control and healing: review of the literature. Burns 33:139–148PubMedCrossRefGoogle Scholar
  8. Azami M, Tavakol S, Samadikuchaksaraei A, Hashjin MS, Baheiraei N, Kamali M, Nourani MR (2012) A porous hydroxyapatite/gelatin nanocomposite scaffold for bone tissue repair: in vitro and in vivo evaluation. J Biomater Sci Polym Ed 23:2353–2368PubMedGoogle Scholar
  9. Azuara-Blanco A, Pillai C, Dua HS (1999) Amniotic membrane transplantation for ocular surface reconstruction. Br J Ophthalmol 83:399–402PubMedPubMedCentralCrossRefGoogle Scholar
  10. Barret JP, Dziewulski P, Ramzy PI, Wolf SE, Desai MH, Herndon DN (2000) Biobrane versus 1% silver sulfadiazine in second-degree pediatric burns. Plast Reconstr Surg 105:62–65PubMedCrossRefGoogle Scholar
  11. Baskovich B, Sampson EM, Schultz GS, Parnell LK (2008) Wound dressing components degrade proteins detrimental to wound healing. Int Wound J 5:543–551PubMedCrossRefGoogle Scholar
  12. Baulier E, Favreau F, LE Corf A, Jayle C, Schneider F, Goujon J-M, Feraud O, Bennaceur-Griscelli A, Hauet T, Turhan AG (2014) Amniotic fluid-derived mesenchymal stem cells prevent fibrosis and preserve renal function in a preclinical porcine model of kidney transplantation. Stem Cells Transl Med 3(7):809–820PubMedPubMedCentralCrossRefGoogle Scholar
  13. Bello YM, Phillips TJ (2000) Recent advances in wound healing. JAMA 283:716–718PubMedCrossRefGoogle Scholar
  14. Bilic G, Zeisberger SM, Mallik AS, Zimmermann R, Zisch AH (2008) Comparative characterization of cultured human term amnion epithelial and mesenchymal stromal cells for application in cell therapy. Cell Transplant 17:955–968PubMedCrossRefGoogle Scholar
  15. Bleggi-Torres L, Werner B, Piazza M (1997) Ultrastructural study of the neovagina following the utilization of human amniotic membrane for treatment of congenital absence of the vagina. Braz J Med Biol Res 30:861–864PubMedCrossRefGoogle Scholar
  16. Bose B (1979) Burn wound dressing with human amniotic membrane. Ann R Coll Surg Engl 61:444PubMedPubMedCentralGoogle Scholar
  17. Boulton AJ, Kirsner RS, Vileikyte L (2004) Neuropathic diabetic foot ulcers. N Engl J Med 351:48–55PubMedCrossRefGoogle Scholar
  18. Bravo D, Rigley TH, Gibran N, Strong DM, Newman-Gage H (2000) Effect of storage and preservation methods on viability in transplantable human skin allografts. Burns 26:367–378PubMedCrossRefGoogle Scholar
  19. Bromberg BE, Song IC, Mohn MP (1965) The use of pig skin as a temporary biological dressing. Plast Reconstr Surg 36:80–90PubMedCrossRefGoogle Scholar
  20. Brown GL, Nanney LB, Griffen J, Cramer AB, Yancey JM, Curtsinger LJ III, Holtzin L, Schultz GS, Jurkiewicz MJ, Lynch JB (1989) Enhancement of wound healing by topical treatment with epidermal growth factor. N Engl J Med 321:76–79PubMedCrossRefGoogle Scholar
  21. Bujang-Safawi E, Halim A, Khoo T, Dorai A (2010) Dried irradiated human amniotic membrane as a biological dressing for facial burns—A 7-year case series. Burns 36:876–882PubMedCrossRefGoogle Scholar
  22. Burgos H (1986) Angiogenic factor from human term placenta. Purification and partial characterization. Eur J Clin Investig 16:486–493CrossRefGoogle Scholar
  23. Cao Y, Rodriguez A, Vacanti M, Ibarra C, Arevalo C, Vacanti CA (1998) Comparative study of the use of poly (glycolic acid), calcium alginate and pluronics in the engineering of autologous porcine cartilage. J Biomater Sci Polym Ed 9:475–487PubMedCrossRefGoogle Scholar
  24. Carmeliet P (2003) Angiogenesis in health and disease. Nat Med 9:653–660PubMedCrossRefGoogle Scholar
  25. Chang J-W, Hung S-P, Wu H-H, Wu W-M, Yang A-H, Tsai H-L, Yang L-Y, Lee OK (2011) Therapeutic effects of umbilical cord blood-derived mesenchymal stem cell transplantation in experimental lupus nephritis. Cell Transplant 20:245–257PubMedCrossRefGoogle Scholar
  26. Chen J, Tseng S (1991) Abnormal corneal epithelial wound healing in partial-thickness removal of limbal epithelium. Invest Ophthalmol Vis Sci 32:2219–2233PubMedGoogle Scholar
  27. Chen C, Lumsden AB, Ofenloch JC, Noe B, Campbell EJ, Stratford PW, Yianni YP, Taylor AS, Hanson SR (1997) Phosphorylcholine coating of ePTFE grafts reduces neointimal hyperplasia in canine model. Ann Vasc Surg 11:74–79PubMedCrossRefGoogle Scholar
  28. Chen H-J, Pires RT, Tseng SC (2000) Amniotic membrane transplantation for severe neurotrophic corneal ulcers. Br J Ophthalmol 84:826–833PubMedPubMedCentralCrossRefGoogle Scholar
  29. Choi YS, Kim JY, Wee WR, Lee JH (1998) Effect of the application of human amniotic membrane on rabbit corneal wound healing after excimer laser photorefractive keratectomy. Cornea 17:389–395PubMedCrossRefGoogle Scholar
  30. Cohen S, Samadikuchaksaraei A, Polak JM, Bishop AE (2006) Antibiotics reduce the growth rate and differentiation of embryonic stem cell cultures. Tissue Eng 12:2025–2030PubMedCrossRefGoogle Scholar
  31. Cribbs R, Luquette M, Besner G (1998) Acceleration of partial-thickness burn wound healing with topical application of heparin-binding EGF-like growth factor (HB-EGF). J Burn Care Rehabil 19:95–101PubMedCrossRefGoogle Scholar
  32. Cribbs RK, Harding PA, Luquette MH, Besner GE (2002) Endogenous production of heparin-binding EGF-like growth factor during murine partial-thickness burn wound healing. J Burn Care Rehabil 23:116–125PubMedCrossRefGoogle Scholar
  33. Davis JS (1910) Skin transplantation. Johns Hopkins Hosp Rep 15:307–396Google Scholar
  34. Daya SM, Bell RD, Habib NE, Powell-Richards A, Dua HS (2000) Clinical and pathologic findings in human keratolimbal allograft rejection. Cornea 19:443–450PubMedCrossRefGoogle Scholar
  35. Deitch EA, Wheelahan TM, Rose MP, Clothier J, Cotter J (1983) Hypertrophic burn scars: analysis of variables. J Trauma Acute Care Surg 23:895–898CrossRefGoogle Scholar
  36. Diegelmann RF, Evans MC (2004) Wound healing: an overview of acute, fibrotic and delayed healing. Front Biosci 9:283–289PubMedCrossRefGoogle Scholar
  37. Dietrich-Ntoukas T, Hofmann-Rummelt C, Kruse FE, Schlotzer-Schrehardt U (2012) Comparative analysis of the basement membrane composition of the human limbus epithelium and amniotic membrane epithelium. Cornea 31:564–569PubMedCrossRefGoogle Scholar
  38. Dua HS, Azuara-Blanco A (2000) Autologous limbal transplantation in patients with unilateral corneal stem cell deficiency. Br J Ophthalmol 84:273–278PubMedPubMedCentralCrossRefGoogle Scholar
  39. Dua HS, Forrester JV (1990) The corneoscleral limbus in human corneal epithelial wound healing. Am J Ophthalmol 110:646–656PubMedCrossRefGoogle Scholar
  40. Dua HS, Gomes JA, King AJ, Maharajan VS (2004) The amniotic membrane in ophthalmology. Surv Ophthalmol 49:51–77PubMedCrossRefGoogle Scholar
  41. Eaglstein WH (1985) Experiences with biosynthetic dressings. J Am Acad Dermatol 12:434–440PubMedCrossRefGoogle Scholar
  42. Eftekharzadeh M, Nobakht M, Alizadeh A, Soleimani M, Hajghasem M, Kordestani Shargh B, Karkuki Osguei N, Behnam B, Samadikuchaksaraei A (2015) The effect of intrathecal delivery of bone marrow stromal cells on hippocampal neurons in rat model of Alzheimer’s disease. Iran J Basic Med Sci 18:520–525PubMedPubMedCentralGoogle Scholar
  43. Eppler SM, Combs DL, Henry TD, Lopez JJ, Ellis SG, Yi JH, Annex BH, McCluskey ER, Zioncheck TF (2002) A target‐mediated model to describe the pharmacokinetics and hemodynamic effects of recombinant human vascular endothelial growth factor in humans. Clin Pharmacol Ther 72:20–32PubMedCrossRefGoogle Scholar
  44. Epstein FH, Parry S, Strauss JF (1998) Premature rupture of the fetal membranes. N Engl J Med 338:663–670CrossRefGoogle Scholar
  45. Epstein FH, Singer AJ, Clark RA (1999) Cutaneous wound healing. N Engl J Med 341:738–746CrossRefGoogle Scholar
  46. Fang C-H, Jin J, Joe J-H, Song Y-S, So B-I, Lim SM, Cheon GJ, Woo S-K, Ra J-C, Lee Y-Y (2012) In vivo differentiation of human amniotic epithelial cells into cardiomyocyte-like cells and cell transplantation effect on myocardial infarction in rats: comparison with cord blood and adipose tissue-derived mesenchymal stem cells. Cell Transplant 21:1687–1696PubMedCrossRefGoogle Scholar
  47. Fijan A, Hashemi A, Namazi H (2014) A novel use of amniotic membrane for fingertip injuries. J Wound Care 23:255–258PubMedCrossRefGoogle Scholar
  48. Fukuda K, Chikama T-I, Nakamura M, Nishida T (1999) Differential distribution of subchains of the basement membrane components type IV collagen and laminin among the amniotic membrane, cornea, and conjunctiva. Cornea 18:73–79PubMedCrossRefGoogle Scholar
  49. Ghalambor A, Pipelzadeh MH, Khodadadi A (2000) The amniotic membrane: a suitable biological dressing to prevent infection in thermal burns. Med J Islamic Acad Sci 13:115–118Google Scholar
  50. Gholipourmalekabadi M, Nezafati N, Hajibaki L, Mozafari M, Moztarzadeh F, Hesaraki S, Samadikuchaksaraei A (2015a) Detection and qualification of optimum antibacterial and cytotoxic activities of silver-doped bioactive glasses. IET Nanobiotechnol 9(4):209–214PubMedCrossRefGoogle Scholar
  51. Gholipourmalekabadi M, Bandehpour M, Mozafari M, Hashemi A, Ghanbarian H, Sameni M, Salimi M, Gholami M, Samadikuchaksaraei A (2015b) Decellularized human amniotic membrane: more is needed for an efficient dressing for protection of burns against antibiotic-resistant bacteria isolated from burn patients. Burns 41:1488–1497PubMedCrossRefGoogle Scholar
  52. Gholipourmalekabadi M, Mozafari M, Bandehpour M, Salehi M, Sameni M, Caicedo HH, Mehdipour A, Hamidabadi HG, Samadikuchaksaraei A, Ghanbarian H (2015c) Optimization of nanofibrous silk fibroin scaffold as a delivery system for bone marrow adherent cells: in vitro and in vivo studies. Biotechnol Appl Biochem 62(6):785–794PubMedCrossRefGoogle Scholar
  53. Gholipourmalekabadi M, Mozafari M, Salehi M, Seifalian A, Bandehpour M, Ghanbarian H, Urbanska AM, Sameni M, Samadikuchaksaraei A, Seifalian AM (2015d) Development of a cost‐effective and simple protocol for decellularization and preservation of human amniotic membrane as a soft tissue replacement and delivery system for bone marrow stromal cells. Adv Healthc Mater 4:918–926PubMedCrossRefGoogle Scholar
  54. Gholipourmalekabadi M, Sameni M, Hashemi A, Zamani F, Rostami A, Mozafari M (2015e) Silver-and fluoride-containing mesoporous bioactive glasses versus commonly used antibiotics: activity against multidrug-resistant bacterial strains isolated from patients with burns. Burns 42(1):131–140PubMedCrossRefGoogle Scholar
  55. Gholipourmalekabadi M, Sameni M, Radenkovic D, Mozafari M, Mossahebi‐Mohammadi M, Seifalian A (2016) Decellularized human amniotic membrane: how viable is it as a delivery system for human adipose tissue‐derived stromal cells? Cell Prolif 49:115–121PubMedCrossRefGoogle Scholar
  56. Greenhalgh DG (1996) The role of growth factors in wound healing. J Trauma Acute Care Surg 41:159–167CrossRefGoogle Scholar
  57. Groeber F, Holeiter M, Hampel M, Hinderer S, Schenke-Layland K (2011) Skin tissue engineering—in vivo and in vitro applications. Adv Drug Deliv Rev 63:352–366PubMedCrossRefGoogle Scholar
  58. Grueterich M, Espana EM, Tseng SC (2003) Ex vivo expansion of limbal epithelial stem cells: amniotic membrane serving as a stem cell niche. Surv Ophthalmol 48:631–646PubMedCrossRefGoogle Scholar
  59. Gu H-W, Bian D-M, Hu N, Zhang J-F (2011) Effects of amniotic membrane transplantation on cytokines expression in chemically burned rat corneas. Int J Ophthalmol 4:33PubMedPubMedCentralGoogle Scholar
  60. Haberal M, Oner Z, Bayraktar U, Bilgin N (1987) The use of silver nitrate-incorporated amniotic membrane as a temporary dressing. Burns 13:159–163CrossRefGoogle Scholar
  61. Halim AS, Khoo TL, Yussof SJM (2010) Biologic and synthetic skin substitutes: An overview. Indian journal of plastic surgery 43:S23PubMedPubMedCentralCrossRefGoogle Scholar
  62. Hao Y, Ma DH-K, Hwang DG, Kim W-S, Zhang F (2000) Identification of antiangiogenic and antiinflammatory proteins in human amniotic membrane. Cornea 19:348–352PubMedCrossRefGoogle Scholar
  63. Harder J, Meyer-Hoffert U, Teran LM, Schwichtenberg L, Bartels J, Maune S, Schroder J-M (2000) Mucoid Pseudomonas aeruginosa, TNF-α, and IL-1 β, but Not IL-6, induce human β-defensin-2 in respiratory epithelia. Am J Respir Cell Mol Biol 22:714–721PubMedCrossRefGoogle Scholar
  64. He Q, Chen B, Wang Z, Li Q (2002) [The experimental study of culture in vitro of fibroblasts seeded onto human amnion extracellular matrix (HA-ECM)]. Zhonghua zheng xing wai ke za zhi 18:229–231PubMedGoogle Scholar
  65. Heiligenhaus A, Heinz C, Schmitz K, Tappeiner C, Bauer D, Meller D (2008) Amniotic membrane transplantation for the treatment of corneal ulceration in infectious keratitis. In: Cornea and external eye disease. Springer, New YorkGoogle Scholar
  66. Herndon DN, Barrow RE, Rutan RL, Rutan TC, Desai MH, Abston S (1989) A comparison of conservative versus early excision. Therapies in severely burned patients. Ann Surg 209:547PubMedPubMedCentralCrossRefGoogle Scholar
  67. Higa K, Shimmura S, Shimazaki J, Tsubota K (2005) Hyaluronic acid-CD44 interaction mediates the adhesion of lymphocytes by amniotic membrane stroma. Cornea 24:206–212PubMedCrossRefGoogle Scholar
  68. Höckel M, Schlenger K, Doctrow S, Kissel T, Vaupel P (1993) Therapeutic angiogenesis. Arch Surg 128:423–429PubMedCrossRefGoogle Scholar
  69. Hodde J (2002) Naturally occurring scaffolds for soft tissue repair and regeneration. Tissue Eng 8:295–308PubMedCrossRefGoogle Scholar
  70. Hodge A, Lourensz D, Vaghjiani V, Nguyen H, Tchongue J, Wang B, Murthi P, Sievert W, Manuelpillai U (2014) Soluble factors derived from human amniotic epithelial cells suppress collagen production in human hepatic stellate cells. Cytotherapy 16:1132–1144PubMedCrossRefGoogle Scholar
  71. Holland EJ (1996) Epithelial transplantation for the management of severe ocular surface disease. Trans Am Ophthalmol Soc 94:677PubMedPubMedCentralGoogle Scholar
  72. Huang ES, Basu A, O’Grady M, Capretta JC (2009) Projecting the future diabetes population size and related costs for the US. Diabetes Care 32:2225–2229PubMedPubMedCentralCrossRefGoogle Scholar
  73. Inge E, Talmi YP, Sigler L, Finkelstein Y, Zohar Y (1991) Antibacterial properties of human amniotic membranes. Placenta 12:285–288PubMedCrossRefGoogle Scholar
  74. Insausti CL, Blanquer M, Bleda P, Iniesta P, Majado Martínez M, Castellanos G, Moraleda Jimenez JM (2010) The amniotic membrane as a source of stem cells. Histol Histopathol 25(1):91–98PubMedGoogle Scholar
  75. Jafari J, Emami SH, Samadikuchaksaraei A, Bahar MA, Gorjipour F (2011) Electrospun chitosan-gelatin nanofiberous scaffold: fabrication and in vitro evaluation. Biomed Mater Eng 21:99–112PubMedGoogle Scholar
  76. Jahovic N, Guzel E, Arbak S, Yeğen BÇ (2004) The healing-promoting effect of saliva on skin burn is mediated by epidermal growth factor (EGF): role of the neutrophils. Burns 30:531–538PubMedCrossRefGoogle Scholar
  77. Jelenko C III (1967) Studies in burns. I. Water loss from the body surface. Ann Surg 165:83PubMedPubMedCentralCrossRefGoogle Scholar
  78. John A, Oommen J (2010) Use of amniotic membrane in dermatology. Indian Journal of Dermatology, Venereology, and Leprology 76:196CrossRefGoogle Scholar
  79. Jones CA, Williams KA, Finlay-Jones JJ, Hart PH (1995) Interleukin 4 production by human amnion epithelial cells and regulation of its activity by glycosaminoglycan binding. Biol Reprod 52:839–847PubMedCrossRefGoogle Scholar
  80. Kardas P, Devine S, Golembesky A, Roberts C (2005) A systematic review and meta-analysis of misuse of antibiotic therapies in the community. Int J Antimicrob Agents 26:106–113PubMedCrossRefGoogle Scholar
  81. Keelan JA, Sato T, Mitchell MD (1997) Interleukin (IL)-6 and IL-8 production by human amnion: regulation by cytokines, growth factors, glucocorticoids, phorbol esters, and bacterial lipopolysaccharide. Biol Reprod 57:1438–1444PubMedCrossRefGoogle Scholar
  82. Kesting MR, Wolff K-D, Hohlweg-Majert B, Steinstraesser L (2008) The role of allogenic amniotic membrane in burn treatment. Journal of burn care & research 29:907–916CrossRefGoogle Scholar
  83. Kim JC, Tseng SC (1995) Transplantation of preserved human amniotic membrane for surface reconstruction in severely damaged rabbit corneas. Cornea 14:473–484PubMedCrossRefGoogle Scholar
  84. Kim JS, Kim JC, Na BK, Jeong JM, Song CY (2000) Amniotic membrane patching promotes healing and inhibits proteinase activity on wound healing following acute corneal alkali burn. Exp Eye Res 70:329–337PubMedCrossRefGoogle Scholar
  85. Kim J, Kang HM, Kim H, Kim MR, Kwon HC, Gye MC, Kang SG, Yang HS, You J (2007) Ex vivo characteristics of human amniotic membrane-derived stem cells. Cloning and stem cells 9:581–594PubMedCrossRefGoogle Scholar
  86. Kim CH, Kim SS, Shon SK, Kim DH, Song CG, Kim HJ (2008) The effect of human amniotic membrane, epidermal cells and marrow mesenchymal stem cells in healing a skin defect. Journal of the Korean Orthopaedic Association 43:276–286CrossRefGoogle Scholar
  87. King AE, Critchley HO, Sallenave J-M, Kelly RW (2003) Elafin in human endometrium: an antiprotease and antimicrobial molecule expressed during menstruation. The Journal of Clinical Endocrinology & Metabolism 88:4426–4431CrossRefGoogle Scholar
  88. Koizumi N, Inatomi T, Quantock AJ, Fullwood NJ, Dota A, Kinoshita S (2000a) Amniotic membrane as a substrate for cultivating limbal corneal epithelial cells for autologous transplantation in rabbits. Cornea 19:65–71PubMedCrossRefGoogle Scholar
  89. Koizumi N, Inatomi T, Sotozono C, Fullwood NJ, Quantock AJ, Kinoshita S (2000b) Growth factor mRNA and protein in preserved human amniotic membrane. Curr Eye Res 20:173–177PubMedCrossRefGoogle Scholar
  90. Kondo T, Ishida Y (2010) Molecular pathology of wound healing. Forensic Sci Int 203:93–98PubMedCrossRefGoogle Scholar
  91. Kruse FE, Rohrschneider K, Völcker HE (1999) Multilayer amniotic membrane transplantation for reconstruction of deep corneal ulcers. Ophthalmology 106:1504–1511PubMedCrossRefGoogle Scholar
  92. Kuckelkorn R, Keller G, Redbrake C (2001) Long-term results of large diameter keratoplasties in the treatment of severe chemical and thermal eye burns. Klin Monatsbl Augenheilkd 218:542–552PubMedCrossRefGoogle Scholar
  93. Lee S-H, Tseng SC (1997) Amniotic membrane transplantation for persistent epithelial defects with ulceration. Am J Ophthalmol 123:303–312PubMedCrossRefGoogle Scholar
  94. Lee S-B, Li D-Q, Tan DT, Meller D, Tseng SC (2000) Suppression of TGF-ß signaling in both normal conjunctival fibroblasts and pterygial body fibroblasts by amniotic membrane. Curr Eye Res 20:325–334PubMedCrossRefGoogle Scholar
  95. Lei H, Kalluri R, Furth EE, Baker AH, Strauss JF (1999) Rat amnion type IV collagen composition and metabolism: implications for membrane breakdown. Biol Reprod 60:176–182PubMedCrossRefGoogle Scholar
  96. Lo V, Pope E (2009) Amniotic membrane use in dermatology. Int J Dermatol 48:935–940PubMedCrossRefGoogle Scholar
  97. Loeffelbein DJ, Baumann C, Stoeckelhuber M, Hasler R, Mucke T, Steinsträßer L, Drecoll E, Wolff KD, Kesting MR (2012) Amniotic membrane as part of a skin substitute for full‐thickness wounds: an experimental evaluation in a porcine model. J Biomed Mater Res B Appl Biomater 100:1245–1256PubMedCrossRefGoogle Scholar
  98. Loeffelbein DJ, Rohleder NH, Eddicks M, Baumann CM, Stoeckelhuber M, Wolff KD, Drecoll E, Steinstraesser L, Hennerbichler S, Kesting MR (2014). Evaluation of human amniotic membrane as a wound dressing for split-thickness skin-graft donor sites. Biomed Res Int 2014 Article ID 572183, 12 pagesGoogle Scholar
  99. Luo J, Li X, Yang Z (2004) Preparation of human acellular amniotic membrane and its cytocompatibility and biocompatibility. Zhongguo xiu fu chong jian wai ke za zhi 18:108–111PubMedGoogle Scholar
  100. Lynch J, Blocker T (1979) Thermal burns. Plastic Surgery 2:611–620Google Scholar
  101. Madison KC (2003) Barrier function of the skin: “la raison d’etre” of the epidermis. J Investig Dermatol 121:231–241PubMedCrossRefGoogle Scholar
  102. Margolis DJ, Kantor J, Berlin JA (1999) Healing of diabetic neuropathic foot ulcers receiving standard treatment. A meta-analysis. Diabetes Care 22:692–695PubMedCrossRefGoogle Scholar
  103. McCarthy DW, Downing MT, Brigstock DR, Luquette MH, Brown KD, Abad MS, Besner GE (1996) Production of heparin-binding epidermal growth factor-like growth factor (HB-EGF) at sites of thermal injury in pediatric patients. J Investig Dermatol 106:49–56PubMedCrossRefGoogle Scholar
  104. Meinert M, Eriksen GV, Petersen AC, Helmig RB, Laurent C, Uldbjerg N, Malmström A (2001) Proteoglycans and hyaluronan in human fetal membranes. Am J Obstet Gynecol 184:679–685PubMedCrossRefGoogle Scholar
  105. Meller D, Tseng SC (1999) Conjunctival epithelial cell differentiation on amniotic membrane. Investig Ophthalmol Vis Sci 40:878–886Google Scholar
  106. Mendelsohn M, Dunlop G (1998) Gore-tex augmentation grafting in rhinoplasty--Is it safe? Journal of Otolaryngology-Head & Neck Surgery 27:337Google Scholar
  107. Mermet I, Pottier N, Sainthillier JM, Malugani C, Cairey‐Remonnay S, Maddens S, Riethmuller D, Tiberghien P, Humbert P, Aubin F (2007) Use of amniotic membrane transplantation in the treatment of venous leg ulcers. Wound Repair Regen 15:459–464PubMedCrossRefGoogle Scholar
  108. Meyer U, Handschel J, Meyer T, Wiesmann HP (2009) Fundamentals of tissue engineering and regenerative medicine. Springer, New YorkCrossRefGoogle Scholar
  109. Midwood KS, Williams LV, Schwarzbauer JE (2004) Tissue repair and the dynamics of the extracellular matrix. Int J Biochem Cell Biol 36:1031–1037PubMedCrossRefGoogle Scholar
  110. Mligiliche N, Endo K, Okamoto K, Fujimoto E, Ide C (2002) Extracellular matrix of human amnion manufactured into tubes as conduits for peripheral nerve regeneration. J Biomed Mater Res 63:591–600PubMedCrossRefGoogle Scholar
  111. Mobini S, Hoyer B, Solati-Hashjin M, Lode A, Nosoudi N, Samadikuchaksaraei A, Gelinsky M (2013a) Fabrication and characterization of regenerated silk scaffolds reinforced with natural silk fibers for bone tissue engineering. J Biomed Mater Res A 101:2392–2404PubMedCrossRefGoogle Scholar
  112. Mobini S, Solati-Hashjin M, Peirovi H, Osman NAA, Gholipourmalekabadi M, Barati M, Samadikuchaksaraei A (2013b) Bioactivity and biocompatibility studies on silk-based scaffold for bone tissue engineering. J Med Biol Eng 33:207–214CrossRefGoogle Scholar
  113. Modesti A, Scarpa S, D’Orazi G, Simonelli L, Caramia FG (1989) Localization of type IV and V collagens in the stroma of human amnion. Prog Clin Biol Res 296:459PubMedGoogle Scholar
  114. Mohammadi AA, Jafari SMS, Kiasat M, Tavakkolian AR, Imani MT, Ayaz M, Tolide-Ie HR (2013) Effect of fresh human amniotic membrane dressing on graft take in patients with chronic burn wounds compared with conventional methods. Burns 39:349–353PubMedCrossRefGoogle Scholar
  115. Mohammadi AA, Sabet B, Riazi H, Tavakko-Lian AR, Mohammadi MK, Iranpak S (2015) Human amniotic membrane dressing: an excellent method for outpatient management of burn wounds. Iranian Journal of Medical Sciences 34:61–64Google Scholar
  116. Moncrief JA, Mason AD Jr (1964) Evaporative water loss in the burned patient. J Trauma Acute Care Surg 4:180–185CrossRefGoogle Scholar
  117. Moschidou D, Drews K, Eddaoudi A, Adjaye J, DE Coppi P, Guillot PV (2013) Molecular signature of human amniotic fluid stem cells during fetal development. Current stem cell research & therapy 8:73–81CrossRefGoogle Scholar
  118. Nakamura T, Inatomi T, Sotozono C, Ang LP, Koizumi N, Yokoi N, Kinoshita S (2006) Transplantation of autologous serum-derived cultivated corneal epithelial equivalents for the treatment of severe ocular surface disease. Ophthalmology 113:1765–1772PubMedCrossRefGoogle Scholar
  119. Nezafati N, Moztarzadeh F, Hesaraki S, Mozafari M, Samadikuchaksaraei A, Hajibaki L, Gholipour M (2012) Effect of silver concentration on bioactivity and antibacterial properties of SiO2-CaO-P2O5 sol-gel derived bioactive glass. Key Eng Mater 493–494:74–79Google Scholar
  120. Niknejad H, Peirovi H, Jorjani M, Ahmadiani A, Ghanavi J, Seifalian AM (2008) Properties of the amniotic membrane for potential use in tissue engineering. Eur Cells Mater 15:88–99CrossRefGoogle Scholar
  121. Niknejad H, Paeini-Vayghan G, Tehrani F, Khayat-Khoei M, Peirovi H (2013) Side dependent effects of the human amnion on angiogenesis. Placenta 34:340–345PubMedCrossRefGoogle Scholar
  122. Pan SC, Wu LW, Chen CL, Shieh SJ, Chiu HY (2010) Deep partial thickness burn blister fluid promotes neovascularization in the early stage of burn wound healing. Wound Repair Regen 18:311–318PubMedCrossRefGoogle Scholar
  123. Papini R (2004) ABC of burns: management of burn injuries of various depths. BMJ: British Medical Journal 329:158PubMedPubMedCentralCrossRefGoogle Scholar
  124. Parolini O, Alviano F, Bagnara GP, Bilic G, Buhring HJ, Evangelista M, Hennerbichler S, Liu B, Magatti M, Mao N (2008) Concise review: isolation and characterization of cells from human term placenta: outcome of the first international Workshop on Placenta Derived Stem Cells. Stem Cells 26:300–311PubMedCrossRefGoogle Scholar
  125. Pellegrini G, Traverso CE, Franzi AT, Zingirian M, Cancedda R, DE Luca M (1997) Long-term restoration of damaged corneal surfaces with autologous cultivated corneal epithelium. Lancet 349:990–993PubMedCrossRefGoogle Scholar
  126. Perin L, Sedrakyan S, Giuliani S, DA Sacco S, Carraro G, Shiri L, Lemley KV, Rosol M, Wu S, Atala A (2010) Protective effect of human amniotic fluid stem cells in an immunodeficient mouse model of acute tubular necrosis. PLoS One 5:e9357PubMedPubMedCentralCrossRefGoogle Scholar
  127. Proksch E, Brandner JM, Jensen JM (2008) The skin: an indispensable barrier. Exp Dermatol 17:1063–1072PubMedCrossRefGoogle Scholar
  128. Rendal-Vázquez ME, San-Luis-Verdes A, Yebra-Pimentel-Vilar MT, López-Rodríguez I, Domenech-García N, Andión-Núñez C, Blanco-García F (2012) Culture of limbal stem cells on human amniotic membrane. Cell Tissue Bank 13:513–519PubMedCrossRefGoogle Scholar
  129. Riau AK, Beuerman RW, Lim LS, Mehta JS (2010) Preservation, sterilization and de-epithelialization of human amniotic membrane for use in ocular surface reconstruction. Biomaterials 31:216–225PubMedCrossRefGoogle Scholar
  130. Robson MC, Krizek TJ (1973) The effect of human amniotic membranes on the bacteria population of infected rat burns. Ann Surg 177:144PubMedPubMedCentralCrossRefGoogle Scholar
  131. Roh D-H, Seo M-S, Choi H-S, Park S-B, Han H-J, Beitz AJ, Kang K-S, Lee J-H (2013) Transplantation of human umbilical cord blood or amniotic epithelial stem cells alleviates mechanical allodynia after spinal cord injury in rats. Cell Transplant 22:1577–1590PubMedCrossRefGoogle Scholar
  132. Saki M, Narbat MK, Samadikuchaksaraei A, Ghafouri HB, Gorjipour F (2009) Biocompatibility study of a hydroxyapatite-alumina and silicon carbide composite scaffold for bone tissue engineering. Yakhteh 11:55–60Google Scholar
  133. Samadikuchaksaraei A, Bishop AE (2006) Derivation and characterization of alveolar epithelial cells from murine embryonic stem cells in vitro. Methods Mol Biol 330:233–248PubMedGoogle Scholar
  134. Samadikuchaksaraei A, Bishop AE (2007) Effects of growth factors on the differentiation of murine ESC into type II pneumocytes. Cloning Stem Cells 9:407–416PubMedCrossRefGoogle Scholar
  135. Sangwan VS, Burman S, Tejwani S, Mahesh SP, Murthy R (2007) Amniotic membrane transplantation: a review of current indications in the management of ophthalmic disorders. Indian J Ophthalmol 55:251CrossRefPubMedGoogle Scholar
  136. Sankar V, Muthusamy R (2003) Role of human amniotic epithelial cell transplantation in spinal cord injury repair research. Neuroscience 118:11–17PubMedCrossRefGoogle Scholar
  137. Schwab IR, Reyes M, Isseroff RR (2000) Successful transplantation of bioengineered tissue replacements in patients with ocular surface disease. Cornea 19:421–426PubMedCrossRefGoogle Scholar
  138. Shah AP (2014) Using amniotic membrane allografts in the treatment of neuropathic foot ulcers. J Am Podiatr Med Assoc 104:198–202PubMedCrossRefGoogle Scholar
  139. Shapiro M, Friend J, Thoft R (1981) Corneal re-epithelialization from the conjunctiva. Invest Ophthalmol Vis Sci 21:135–142PubMedGoogle Scholar
  140. Shevchenko RV, James SL, James SE (2010) A review of tissue-engineered skin bioconstructs available for skin reconstruction. J R Soc Interface 7:229–258PubMedCrossRefGoogle Scholar
  141. Shimazaki J, Yang H-Y, Tsubota K (1997) Amniotic membrane transplantation for ocular surface reconstruction in patients with chemical and thermal burns. Ophthalmology 104:2068–2076PubMedCrossRefGoogle Scholar
  142. Shimazaki J, Shinozaki N, Tsubota K (1998) Transplantation of amniotic membrane and limbal autograft for patients with recurrent pterygium associated with symblepharon. Br J Ophthalmol 82:235–240PubMedPubMedCentralCrossRefGoogle Scholar
  143. Shimmura S, Shimazaki J, Ohashi Y, Tsubota K (2001) Antiinflammatory effects of amniotic membrane transplantation in ocular surface disorders. Cornea 20:408–413PubMedCrossRefGoogle Scholar
  144. Shoae-Hassani A, Mortazavi-Tabatabaei SA, Sharif S, Seifalian AM, Azimi A, Samadikuchaksaraei A, Verdi J (2015) Differentiation of human endometrial stem cells into urothelial cells on a three-dimensional nanofibrous silk-collagen scaffold: an autologous cell resource for reconstruction of the urinary bladder wall. J Tissue Eng Regen Med 9:1268–1276PubMedCrossRefGoogle Scholar
  145. Shores JT, Gabriel A, Gupta S (2007) Skin substitutes and alternatives: a review. Adv Skin Wound Care 20:493–508PubMedCrossRefGoogle Scholar
  146. Siti-Ismail N, Samadikuchaksaraei A, Bishop AE, Polak JM, Mantalaris A (2012) Development of a novel three-dimensional, automatable and integrated bioprocess for the differentiation of embryonic stem cells into pulmonary alveolar cells in a rotating vessel bioreactor system. Tissue Eng Part C Methods 18:263–272PubMedCrossRefGoogle Scholar
  147. Skardal A, Mack D, Kapetanovic E, Atala A, Jackson JD, Yoo J, Soker S (2012) Bioprinted amniotic fluid-derived stem cells accelerate healing of large skin wounds. Stem cells translational medicine 1:792PubMedPubMedCentralCrossRefGoogle Scholar
  148. Snyder RJ, Kirsner RS, Warriner R III, Lavery LA, Hanft JR, Sheehan P (2010) Consensus recommendations on advancing the standard of care for treating neuropathic foot ulcers in patients with diabetes. Ostomy Wound Manage 56:S1–S24PubMedGoogle Scholar
  149. Solomon A, Rosenblatt M, Monroy D, Ji Z, Pflugfelder SC, Tseng SC (2001) Suppression of interleukin 1α and interleukin 1β in human limbal epithelial cells cultured on the amniotic membrane stromal matrix. Br J Ophthalmol 85:444–449PubMedPubMedCentralCrossRefGoogle Scholar
  150. Sorsby A, Symons H (1946) Amniotic membrane grafts in caustic burns of the eye:(Burns of the second degree). Br J Ophthalmol 30:337PubMedCentralCrossRefGoogle Scholar
  151. Sorsby A, Haythorne J, Reed H (1947) Further experience with amniotic membrane grafts in caustic burns of the eye. Br J Ophthalmol 31:409PubMedPubMedCentralCrossRefGoogle Scholar
  152. Stern M (1913) The grafting of preserved amniotic membrane to burned and ulcerated surfaces, substituing skin grafts: a preliminary report. J Am Med Assoc 60:973–974CrossRefGoogle Scholar
  153. Stern HS (1989) Silver sulphadiazine and the healing of partial thickness burns: a prospective clinical trial. Br J Plast Surg 42:581–585PubMedCrossRefGoogle Scholar
  154. Sutherland AJ, Converse GL, Hopkins RA, Detamore MS (2015) The bioactivity of cartilage extracellular matrix in articular cartilage regeneration. Advanced healthcare materials 4:29–39PubMedCrossRefGoogle Scholar
  155. Tchah H, Lee S-A, Sung K, Cho BJ, Kook MS (2003) Apoptosis in keratocytes caused by mitomycin C. Invest Ophthalmol Vis Sci 44:1912–1917PubMedCrossRefGoogle Scholar
  156. Tehrani FA, Ahmadiani A, Niknejad H (2013) The effects of preservation procedures on antibacterial property of amniotic membrane. Cryobiology 67:293–298PubMedCrossRefGoogle Scholar
  157. Thibault RA, Mikos AG, Kasper FK (2013) Scaffold/extracellular matrix hybrid constructs for bone‐tissue engineering. Advanced healthcare materials 2:13–24PubMedCrossRefGoogle Scholar
  158. Thompson WD, Li WW, Maragoudakis M (2000) The clinical manipulation of angiogenesis: pathology, side‐effects, surprises, and opportunities with novel human therapies. J Pathol 190:330–337PubMedCrossRefGoogle Scholar
  159. Toomey N, Monaghan Á, Fanning S, Bolton D (2009) Transfer of antibiotic resistance marker genes between lactic acid bacteria in model rumen and plant environments. Appl Environ Microbiol 75:3146–3152PubMedPubMedCentralCrossRefGoogle Scholar
  160. Trelford JD, Trelford-Sauder M (1979) The amnion in surgery, past and present. Am J Obstet Gynecol 134:833–845PubMedCrossRefGoogle Scholar
  161. Tsai RJ-F, Li L-M, Chen J-K (2000) Reconstruction of damaged corneas by transplantation of autologous limbal epithelial cells. N Engl J Med 343:86–93PubMedCrossRefGoogle Scholar
  162. Tseng SC, Prabhasawat P, Barton K, Gray T, Meller D (1998) Amniotic membrane transplantation with or without limbal allografts for corneal surface reconstruction in patients with limbal stem cell deficiency. Arch Ophthalmol 116:431–441PubMedCrossRefGoogle Scholar
  163. Van Vranken BE, Rippon HJ, Samadikuchaksaraei A, Trounson AO, Bishop AE (2007) The differentiation of distal lung epithelium from embryonic stem cells. Curr Protoc Stem Cell Biol Chapter 1, Unit 1G 1Google Scholar
  164. Werner S, Grose R (2003) Regulation of wound healing by growth factors and cytokines. Physiol Rev 83:835–870PubMedGoogle Scholar
  165. Wilshaw S-P, Kearney JN, Fisher J, Ingham E (2006) Production of an acellular amniotic membrane matrix for use in tissue engineering. Tissue Eng 12:2117–2129PubMedCrossRefGoogle Scholar
  166. Wolbank S, Hildner F, Redl H, VAN Griensven M, Gabriel C, Hennerbichler S (2009) Impact of human amniotic membrane preparation on release of angiogenic factors. J Tissue Eng Regen Med 3:651–654PubMedCrossRefGoogle Scholar
  167. Wolf HJ, Schmidt W, Drenckhahn D (1991) Immunocytochemical analysis of the cytoskeleton of the human amniotic epithelium. Cell Tissue Res 266:385–389PubMedCrossRefGoogle Scholar
  168. Yildirimer L, Thanh NT, Seifalian AM (2012) Skin regeneration scaffolds: a multimodal bottom-up approach. Trends Biotechnol 30:638–648PubMedCrossRefGoogle Scholar
  169. Yoon BS, Moon J-H, Jun EK, Kim J, Maeng I, Kim JS, Lee JH, Baik CS, Kim A, Cho KS (2009) Secretory profiles and wound healing effects of human amniotic fluid–derived mesenchymal stem cells. Stem Cells Dev 19:887–902CrossRefGoogle Scholar
  170. Yu SJ, Soncini M, Kaneko Y, Hess DC, Parolini O, Borlongan CV (2009) Amnion: a potent graft source for cell therapy in stroke. Cell Transplant 18:111–118PubMedCrossRefGoogle Scholar
  171. Zhang T, Yam GH-F, Riau AK, Poh R, Allen JC, Peh GS, Beuerman RW, Tan DT, Mehta JS (2013) The effect of amniotic membrane de-epithelialization method on its biological properties and ability to promote limbal epithelial cell culture the effect of amniotic membrane denudation methods. Invest Ophthalmol Vis Sci 54:3072–3081PubMedCrossRefGoogle Scholar
  172. Zheng Y-B, Gao Z-L, Xie C, Zhu H-P, Peng L, Chen J-H, Chong YT (2008) Characterization and hepatogenic differentiation of mesenchymal stem cells from human amniotic fluid and human bone marrow: a comparative study. Cell Biol Int 32:1439–1448PubMedCrossRefGoogle Scholar
  173. Zheng Y-B, Zhang X-H, Huang Z-L, Lin C-S, Lai J, Gu Y-R, Lin B-L, Xie D-Y, Xie S-B, Peng L (2012) Amniotic-fluid–derived mesenchymal stem cells overexpressing interleukin-1 receptor antagonist improve fulminant hepatic failure. PLoS One 7(7):e41392PubMedPubMedCentralCrossRefGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2016

Authors and Affiliations

  • Mazaher Gholipourmalekabadi
    • 1
    • 4
  • Narendra Pal Singh Chauhan
    • 2
  • Behrouz Farhadihosseinabad
    • 3
  • Ali Samadikuchaksaraei
    • 1
    • 4
    • 5
    Email author
  1. 1.Cellular and Molecular Research CenterIran University of Medical SciencesTehranIran
  2. 2.Department of Chemistry,Faculty of Advanced Technologies in Medicine, Iran University of Medical SciencesUdaipurIndia
  3. 3.Biotechnology Department, School of Advanced Technologies in MedicineShahid Beheshti University of Medical SciencesTehranIran
  4. 4.Department of Tissue Engineering & Regenerative Medicine, Faculty of Advanced Technologies in MedicineIran University of Medical SciencesTehranIran
  5. 5.Department of Medical BiotechnologyFaculty of Allied Medicine, Iran University of Medical SciencesTehranIran

Personalised recommendations