Skip to main content

Advertisement

Log in

Comparison of the effects of preservation methods on structural, biological, and mechanical properties of the human amniotic membrane for medical applications

  • Full Length Review
  • Published:
Cell and Tissue Banking Aims and scope Submit manuscript

Abstract

Amniotic membrane (AM), the innermost layer of the placenta, is an exceptionally effective biomaterial with divers applications in clinical medicine. It possesses various biological functions, including scar reduction, anti-inflammatory properties, support for epithelialization, as well as anti-microbial, anti-fibrotic and angio-modulatory effects. Furthermore, its abundant availability, cost-effectiveness, and ethical acceptability make it a compelling biomaterial in the field of medicine. Given the potential unavailability of fresh tissue when needed, the preservation of AM is crucial to ensure a readily accessible and continuous supply for clinical use. However, preserving the properties of AM presents a significant challenge. Therefore, the establishment of standardized protocols for the collection and preservation of AM is vital to ensure optimal tissue quality and enhance patient safety. Various preservation methods, such as cryopreservation, lyophilization, and air-drying, have been employed over the years. However, identifying a preservation method that effectively safeguards AM properties remains an ongoing endeavor. This article aims to review and discuss different sterilization and preservation procedures for AM, as well as their impacts on its histological, physical, and biochemical characteristics.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1

(Modified from Nejad et al. 2021)

Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Ab Hamid SS, Zahari NK, Yusof N, Hassan A (2014) Scanning electron microscopic assessment on surface morphology of preserved human amniotic membrane after gamma sterilisation. Cell Tissue Bank 15:15–24

    Article  PubMed  Google Scholar 

  • Adds PJ, Hunt CJ, Dart JK (2001) Amniotic membrane grafts, “fresh” or frozen? A clinical and in vitro comparison. Br J Ophthalmol 85:905–907

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Agakidou E, Agakidis C, Kontou A, Chotas W, Sarafidis K (2022) Antimicrobial peptides in early-life host defense, perinatal infections, and necrotizing enterocolitis—An update. J Clin Med 11:5074

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Alizadeh E, Orlando TM, Sanche L (2015) Biomolecular damage induced by ionizing radiation: the direct and indirect effects of low-energy electrons on DNA. Annu Rev Phys Chem 66:379–398

    Article  ADS  CAS  PubMed  Google Scholar 

  • Allen CL et al (2013) Augmented dried versus cryopreserved amniotic membrane as an ocular surface dressing. PLoS ONE 8:e78441

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  • Arai N, Tsuno H, Okabe M, Yoshida T, Koike C, Noguchi M, Nikaido T (2012) Clinical application of a hyperdry amniotic membrane on surgical defects of the oral mucosa. J Oral Maxillofac Surg 70:2221–2228

    Article  PubMed  Google Scholar 

  • Ashraf NN, Siyal NA, Sultan S, Adhi MI (2015) Comparison of efficacy of storage of amniotic membrane at-20 and-80 degrees centigrade. J Coll Physicians Surg Pak JCPSP 25:264–267

    PubMed  Google Scholar 

  • Babajani A, Manzari-Tavakoli A, Jamshidi E, Tarasi R, Niknejad H (2022) Anti-cancer effects of human placenta-derived amniotic epithelial stem cells loaded with paclitaxel on cancer cells. Sci Rep 12:18148

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  • Bernabé-García Á, Liarte S, Moraleda JM, Castellanos G, Nicolás FJ (2017) Amniotic membrane promotes focal adhesion remodeling to stimulate cell migration. Sci Rep 7:15262

    Article  ADS  PubMed  PubMed Central  Google Scholar 

  • Bhushan KS, Singh G, Chauhan G, Prakash S (2015) Amniotic membrane and its structure, features and uses in dentistry–a brief review. Int J Adv Res 3:354–360

    CAS  Google Scholar 

  • Chun BY, Kim HK, Shin JP (2013) Dried human amniotic membrane does not alleviate inflammation and fibrosis in experimental strabismus surgery. J Ophthalmol. https://doi.org/10.1155/2013/369126

    Article  PubMed  PubMed Central  Google Scholar 

  • Cirman T, Beltram M, Schollmayer P, Rožman P, Kreft ME (2014) Amniotic membrane properties and current practice of amniotic membrane use in ophthalmology in Slovenia. Cell Tissue Bank 15:177–192

    Article  CAS  PubMed  Google Scholar 

  • Cooke M, Tan E, Mandrycky C, He H, O’Connell J, Tseng S (2014) Comparison of cryopreserved amniotic membrane and umbilical cord tissue with dehydrated amniotic membrane/chorion tissue. J Wound Care 23:465–476

    Article  CAS  PubMed  Google Scholar 

  • Crowe JH, Crowe LM, Oliver AE, Tsvetkova N, Wolkers W, Tablin F (2001) The trehalose myth revisited: introduction to a symposium on stabilization of cells in the dry state. Cryobiology 43:89–105

    Article  CAS  PubMed  Google Scholar 

  • de Oliveira Moraes JTG, Costa MM, Alves PCS, Sant’Anna LB (2021) Effects of preservation methods in the composition of the placental and reflected regions of the human amniotic membrane. Cells Tissues Organs 210:66–76

    Article  Google Scholar 

  • Dehghani M, Azarpira N, Karimi VM, Mossayebi H, Esfandiari E (2017) Grafting with cryopreserved amniotic membrane versus conservative wound care in treatment of pressure ulcers: a randomized clinical trial. Bull Emerg Trauma 5:249

    Article  PubMed  PubMed Central  Google Scholar 

  • Deihim T, Yazdanpanah G, Niknejad H (2016) The effect of lyophilization on light transmission of amniotic membrane: a comparison with rabbit cornea. J Kerman Univ Med Sci 23:308–320

    Google Scholar 

  • Díaz-Prado S et al (2010) Multilineage differentiation potential of cells isolated from the human amniotic membrane. J Cell Biochem 111:846–857

    Article  PubMed  Google Scholar 

  • Díaz-Prado S et al (2011) Human amniotic membrane as an alternative source of stem cells for regenerative medicine. Differentiation 81:162–171

    Article  PubMed  Google Scholar 

  • Dua HS (1999) Amniotic membrane transplantation. Br J Ophthalmol 83:748–752

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dua HS, Gomes JA, King AJ, Maharajan VS (2004) The amniotic membrane in ophthalmology. Surv Ophthalmol 49:51–77

    Article  PubMed  Google Scholar 

  • Duan-Arnold Y, Uveges TE, Gyurdieva A, Johnson A, Danilkovitch A (2015) Angiogenic potential of cryopreserved amniotic membrane is enhanced through retention of all tissue components in their native state. Adv Wound Care 4:513–522

    Article  Google Scholar 

  • Fahy GM, Wowk B (2015) Principles of cryopreservation by vitrification. In: Wolkers WF, Oldenhof H (eds) Cryopreservation and freeze-drying protocols. Springer, New York, pp 21–82

    Chapter  Google Scholar 

  • Fahy GM, Wowk B (2021) Principles of ice-free cryopreservation by vitrification. In: Wolkers WF, Oldenhof H (eds) Cryopreservation and freeze-drying protocols. Springer, New York, pp 27–97

    Chapter  Google Scholar 

  • Fairbairn N, Randolph M, Redmond R (2014) The clinical applications of human amnion in plastic surgery. J Plast Reconstr Aesthet Surg 67:662–675

    Article  CAS  PubMed  Google Scholar 

  • Farhadihosseinabadi B et al (2018) Amniotic membrane and its epithelial and mesenchymal stem cells as an appropriate source for skin tissue engineering and regenerative medicine. Artif Cells Nanomed Biotechnol 46:1–10

    Article  Google Scholar 

  • Fujisato T, Tomihata K, Tabata Y, Iwamoto Y, Burczak K, Ikada Y (1999) Cross-linking of amniotic membranes. J Biomater Sci Polym Ed 10:1171–1181

    Article  CAS  PubMed  Google Scholar 

  • Füst Á et al (2012) Both freshly prepared and frozen-stored amniotic membrane cells express the complement inhibitor CD59. Sci World J. https://doi.org/10.1100/2012/815615

    Article  Google Scholar 

  • Garrido M et al (2018) Transplantation of human amniotic membrane over the liver surface reduces hepatic fibrosis in a cholestatic model in young rats. Stem Cells Int 2018:1–9

    Article  Google Scholar 

  • Georgiadis NS, Ziakas NG, Boboridis KG, Terzidou C, Mikropoulos DG (2008) Cryopreserved amniotic membrane transplantation for the management of symptomatic bullous keratopathy. Clin Exp Ophthalmol 36:130–135

    Article  PubMed  Google Scholar 

  • Gholipourmalekabadi M et al (2016) Decellularized human amniotic membrane: How viable is it as a delivery system for human adipose tissue-derived stromal cells? Cell Prolif 49:115–121

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gindraux F et al (2013) Human amniotic membrane: clinical uses, patents and marketed products. Recent Patents Regen Med 3:193–214

    CAS  Google Scholar 

  • Grzywocz Z et al (2014) Growth factors and their receptors derived from human amniotic cells in vitro. Folia Histochem Cytobiol 52:163–170

    Article  PubMed  Google Scholar 

  • Gupta A, Kedige SD, Jain K (2015) Amnion and chorion membranes: potential stem cell reservoir with wide applications in periodontics. Int J Biomater. https://doi.org/10.1155/2018/6169546

    Article  PubMed  PubMed Central  Google Scholar 

  • Hanselman AE, Tidwell JE, Santrock RD (2015) Cryopreserved human amniotic membrane injection for plantar fasciitis a randomized, controlled, double-blind pilot study. Foot Ankle Int 36:151–158

    Article  PubMed  Google Scholar 

  • Hennerbichler S et al (2007) The influence of various storage conditions on cell viability in amniotic membrane. Cell Tissue Bank 8:1–8

    Article  CAS  PubMed  Google Scholar 

  • Ilancheran S, Moodley Y, Manuelpillai U (2009) Human fetal membranes: A source of stem cells for tissue regeneration and repair? Placenta 30:2–10

    Article  CAS  PubMed  Google Scholar 

  • Insausti CL (2010) Amniotic membrane induces epithelialization in massive posttraumatic wounds. Wound Repair Regen 18:368–377

    Article  PubMed  Google Scholar 

  • Jafari A, Rezaei-Tavirani M, Farhadihosseinabadi B, Zali H, Niknejad H (2021a) Human amniotic mesenchymal stem cells to promote/suppress cancer: two sides of the same coin. Stem Cell Res Ther 12:1–11

    Article  Google Scholar 

  • Jafari A, Rezaei-Tavirani M, Niknejad H, Zali H (2021b) Tumor targeting by conditioned medium derived from human amniotic membrane: new insight in breast cancer therapy. Technol Cancer Res Treat 20:15330338211036318

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jafari A et al (2023) Antiproliferative and apoptotic effects of conditioned medium released from human amniotic epithelial stem cells on breast and cervical cancer cells. Int J Immunopathol Pharmacol 37:03946320221150712

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jang TH et al (2017) Cryopreservation and its clinical applications. Integr Med Res 6:12–18

    Article  PubMed  PubMed Central  Google Scholar 

  • Janz FL et al (2012) Evaluation of distinct freezing methods and cryoprotectants for human amniotic fluid stem cells cryopreservation. BioMed Res Int. https://doi.org/10.1155/2012/649353

    Article  Google Scholar 

  • Jiao H, Guan F, Yang B, Li J, Song L, Hu X, Du Y (2012) Human amniotic membrane derived-mesenchymal stem cells induce C6 glioma apoptosis in vivo through the Bcl-2/caspase pathways. Mol Biol Rep 39:467–473

    Article  CAS  PubMed  Google Scholar 

  • Joyce EM, Moore JJ, Sacks MS (2009) Biomechanics of the fetal membrane prior to mechanical failure: review and implications. Eur J Obstet Gynecol 144:S121–S127

    Article  Google Scholar 

  • Kakabadze Z (2016) Clinical application of decellularized and lyophilized human amnion/chorion membrane grafts for closing post-laryngectomy pharyngocutaneous fistulas. J Surg Oncol 113(5):538–543

    Article  PubMed  PubMed Central  Google Scholar 

  • Kakavand M, Yazdanpanah G, Ahmadiani A, Niknejad H (2017) Blood compatibility of human amniotic membrane compared with heparin-coated ePTFE for vascular tissue engineering. J Tissue Eng Regen Med 11:1701–1709

    Article  CAS  PubMed  Google Scholar 

  • Kar I, Singh A, Mohapatra P, Mohanty P, Misra S (2014) Repair of oral mucosal defects with cryopreserved human amniotic membrane grafts: prospective clinical study. Int J Oral Maxillofac Surg 43:1339–1344

    Article  CAS  PubMed  Google Scholar 

  • Kesting MR, Wolff K-D, Nobis CP, Rohleder NH (2014) Amniotic membrane in oral and maxillofacial surgery. Oral Maxillofac Surg 18:153–164

    Article  PubMed  Google Scholar 

  • Khademi B, Bahranifard H, Azarpira N, Behboodi E (2013) Clinical application of amniotic membrane as a biologic dressing in oral cavity and pharyngeal defects after tumor resection. Arch Iran Med 16(9):503–506

    PubMed  Google Scholar 

  • Kikuchi M, Feng Z, Kosawada T, Sato D, Nakamura T, Umezu M (2016) Stress relaxation and stress–strain characteristics of porcine amniotic membrane. Biomed Mater Eng 27:603–611

    CAS  PubMed  Google Scholar 

  • Kim YM, Gupta BK (2003) 2-Octyl cyanoacrylate adhesive for conjunctival wound closure in rabbits. J Pediatr Ophthalmol Strabismus 40:152–155

    Article  PubMed  Google Scholar 

  • Kim JC, Tseng S (1995a) Transplantation of preserved human amniotic membrane for surface reconstruction in severely damaged rabbit corneas. Cornea 14:473–484

    Article  CAS  PubMed  Google Scholar 

  • Kim JC, Tseng SC (1995b) The effects on inhibition of corneal neovascularization after human amniotic membrane transplantation in severely damaged rabbit corneas. Korean J Ophthalmol 9:32–46

    Article  CAS  PubMed  Google Scholar 

  • Kim J et al (2007) Ex vivo characteristics of human amniotic membrane-derived stem cells. Cloning Stem Cells 9:581–594

    Article  CAS  PubMed  Google Scholar 

  • Kitagawa K et al (2009) A hyperdry amniotic membrane patch using a tissue adhesive for corneal perforations and bleb leaks. Am J Ophthalmol 148:383–389

    Article  PubMed  Google Scholar 

  • Kitagawa K, Okabe M, Yanagisawa S, Zhang X-Y, Nikaido T, Hayashi A (2011) Use of a hyperdried cross-linked amniotic membrane as initial therapy for corneal perforations. Jpn J Ophthalmol 55:16–21

    Article  CAS  PubMed  Google Scholar 

  • Koike C et al (2014) Characterization of amniotic stem cells. Cell Reprogram (formerly “cloning Stem Cells") 16:298–305

    CAS  Google Scholar 

  • Koizumi N et al (2000) Growth factor mRNA and protein in preserved human amniotic membrane. Curr Eye Res 20:173–177

    Article  CAS  PubMed  Google Scholar 

  • Kubo M, Sonoda Y, Muramatsu R, Usui M (2001) Immunogenicity of human amniotic membrane in experimental xenotransplantation. Invest Ophthalmol vis Sci 42:1539–1546

    CAS  PubMed  Google Scholar 

  • Lagares M et al (2009) Addition of ficoll and disaccharides to vitrification solutions improve in vitro viability of vitrified equine embryos. CryoLetters 30:408–413

    CAS  PubMed  Google Scholar 

  • Lai D, Chen H, Lin L, Huang Y, Tsai C, Lai DR (1995) Clinical evaluation of different treatment methods for oral submucous fibrosis. A 10-year experience with 150 cases. J Oral Pathol Med 24:402–406

    Article  CAS  PubMed  Google Scholar 

  • Lamon M et al (2022) Cryopreservation of human amniotic membrane for ocular surface reconstruction: a comparison between protocols. Cell Tissue Bank 23:851–861

    Article  CAS  PubMed  Google Scholar 

  • Lange-Consiglio A et al (2019) Antimicrobial effects of conditioned medium from amniotic progenitor cells in vitro and in vivo: toward tissue regenerative therapies for bovine mastitis. Front Vet Sci 6:443

    Article  PubMed  PubMed Central  Google Scholar 

  • Laranjo M (2015) Preservation of amniotic membrane. In: Mamede A, Botelho M (eds) Amniotic membrane. Springer, Dordrecht. https://doi.org/10.1007/978-94-017-9975-1_13

    Chapter  Google Scholar 

  • Leal-Marin S et al (2021) Human amniotic membrane: a review on tissue engineering, application, and storage. J Biomed Mater Res B Appl Biomater 109:1198–1215

    Article  PubMed  Google Scholar 

  • Lee S-H, Tseng SC (1997) Amniotic membrane transplantation for persistent epithelial defects with ulceration. Am J Ophthalmol 123:303–312

    Article  CAS  PubMed  Google Scholar 

  • Lei J, Priddy LB, Lim JJ, Koob TJ (2017) Dehydrated human amnion/chorion membrane (DHACM) allografts as a therapy for orthopedic tissue repair. Tech Orthop 32:149–157

    Article  Google Scholar 

  • Liang W, Ferrara N (2016) The complex role of neutrophils in tumor angiogenesis and metastasis. Cancer Immunol Res 4:83–91

    Article  CAS  PubMed  Google Scholar 

  • Libera RD et al (2008) Assessment of the use of cryopreserved x freeze-dried amniotic membrane (AM) for reconstruction of ocular surface in rabbit model. Arq Bras Oftalmol 71:669–673

    Article  PubMed  Google Scholar 

  • Lim LS, Poh RW, Riau AK, Beuerman RW, Tan D, Mehta JS (2010) Biological and ultrastructural properties of acelagraft, a freeze-dried γ-irradiated human amniotic membrane. Arch Ophthalmol 128:1303–1310

    Article  CAS  PubMed  Google Scholar 

  • Ma DH-K, Lai J-Y, Cheng H-Y, Tsai C-C, Yeh L-K (2010) Carbodiimide cross-linked amniotic membranes for cultivation of limbal epithelial cells. Biomaterials 31:6647–6658

    Article  CAS  PubMed  Google Scholar 

  • Magatti M et al (2015) Human amniotic membrane-derived mesenchymal and epithelial cells exert different effects on monocyte-derived dendritic cell differentiation and function. Cell Transplant 24:1733–1752

    Article  PubMed  Google Scholar 

  • Mahdy RA, Nada WM, Almasalamy SM, Anany HA, Almasary AM (2010) A freeze-dried (lyophilized) amniotic membrane transplantation with mitomycin C and trabeculectomy for pediatric glaucoma. Cutan Ocul Toxicol 29:164–170

    Article  CAS  PubMed  Google Scholar 

  • Mamede AC, Botelho MF (2015) Amniotic membrane. From structure and functions to clinical applications. Cell Tissue Res 2012:349

    Google Scholar 

  • Mamede A, Carvalho M, Abrantes A, Laranjo M, Maia C, Botelho M (2012) Amniotic membrane: from structure and functions to clinical applications. Cell Tissue Res 349:447–458

    Article  CAS  PubMed  Google Scholar 

  • Maral T, Borman H, Arslan H, Demirhan B, Akinbingol G, Haberal M (1999) Effectiveness of human amnion preserved long-term in glycerol as a temporary biological dressing. Burns 25:625–635

    Article  CAS  PubMed  Google Scholar 

  • Martins V et al (2016) Suppression of TGFβ and angiogenesis by type VII collagen in cutaneous SCC. JNCI 108:djv293

    Article  PubMed  Google Scholar 

  • Maymó JL et al (2018) Proliferation and survival of human amniotic epithelial cells during their hepatic differentiation. PLoS ONE 13:e0191489

    Article  PubMed  PubMed Central  Google Scholar 

  • McQuilling JP, Vines JB, Mowry KC (2017) In vitro assessment of a novel, hypothermically stored amniotic membrane for use in a chronic wound environment. Int Wound J 14:993–1005

    Article  PubMed  PubMed Central  Google Scholar 

  • Mehta M, Waner M, Fay A (2009) Amniotic membrane grafting in the management of conjunctival vascular malformations. Ophthalmic Plast Reconstr Surg 25:371–375

    Article  PubMed  Google Scholar 

  • Mejía LF, Acosta C, Santamaría JP (2000) Use of nonpreserved human amniotic membrane for the reconstruction of the ocular surface. Cornea 19:288–291

    Article  PubMed  Google Scholar 

  • Meller D, Pauklin M, Thomasen H, Westekemper H, Steuhl K-P (2011) Amniotic membrane transplantation in the human eye. Dtsch Arztebl Int 108:243

    PubMed  PubMed Central  Google Scholar 

  • Miki T (2011) Amnion-derived stem cells: in quest of clinical applications. Stem Cell Res Ther 2:1–11

    Article  Google Scholar 

  • Miki T, Wong W, Zhou E, Gonzalez A, Garcia I, Grubbs BH (2016) Biological impact of xeno-free chemically defined cryopreservation medium on amniotic epithelial cells. Stem Cell Res Ther 7:1

    Article  Google Scholar 

  • Miljudin E, Zolotaryov A, Volova L, Ahmerova U (2004) Silica gel dissication of amniotic membrane with related epithelium cells for ocular surface reconstruction. Cell Tissue Bank 5:271–274

    Article  CAS  PubMed  Google Scholar 

  • Mishra KP (2004) Cell membrane oxidative damage induced by gamma-radiation and apoptotic sensitivity. J Environ Pathol Toxicol Oncol 23:6

    Article  Google Scholar 

  • Modaresifar K, Azizian S, Zolghadr M, Moravvej H, Ahmadiani A, Niknejad H (2017) The effect of cryopreservation on anti-cancer activity of human amniotic membrane. Cryobiol 74:61–67

    Article  CAS  Google Scholar 

  • Nakamura T et al (2004) Sterilized, freeze-dried amniotic membrane: a useful substrate for ocular surface reconstruction. Investig Ophthalmol vis Sci 45:93–99

    Article  Google Scholar 

  • Nakamura T et al (2006) Novel clinical application of sterilized, freeze-dried amniotic membrane to treat patients with pterygium. Acta Ophthalmol Scand 84:401–405

    Article  PubMed  Google Scholar 

  • Nakamura T et al (2008) The use of trehalose-treated freeze-dried amniotic membrane for ocular surface reconstruction. Biomaterials 29:3729–3737

    Article  CAS  PubMed  Google Scholar 

  • Nejad AR, Hamidieh AA, Amirkhani MA, Sisakht MM (2021) Update review on five top clinical applications of human amniotic membrane in regenerative medicine. Placenta 103:104–119

    Article  CAS  PubMed  Google Scholar 

  • 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 15:88–99

    Article  CAS  Google Scholar 

  • Niknejad H, Deihim T, Solati-Hashjin M, Peirovi H (2011) The effects of preservation procedures on amniotic membrane’s ability to serve as a substrate for cultivation of endothelial cells. Cryobiology 63:145–151

    Article  CAS  PubMed  Google Scholar 

  • Niknejad H, Paeini-Vayghan G, Tehrani F, Khayat-Khoei M, Peirovi H (2013a) Side dependent effects of the human amnion on angiogenesis. Placenta 34:340–345

    Article  CAS  PubMed  Google Scholar 

  • Niknejad H, Yazdanpanah G, Mirmasoumi M, Abolghasemi H, Peirovi H, Ahmadiani A (2013b) Inhibition of HSP90 could be possible mechanism for anti-cancer property of amniotic membrane. Med Hypotheses 81:862–865

    Article  CAS  PubMed  Google Scholar 

  • Okabe M et al (2014) Hyperdry human amniotic membrane is useful material for tissue engineering: physical, morphological properties, and safety as the new biological material. J Biomed Mater Res A 102:862–870

    Article  PubMed  Google Scholar 

  • Oudart J-B et al (2017) Type XIX collagen: a new partner in the interactions between tumor cells and their microenvironment. Matrix Biol 57:169–177

    Article  PubMed  Google Scholar 

  • Paolin A et al (2016) Cytokine expression and ultrastructural alterations in fresh-frozen, freeze-dried and γ-irradiated human amniotic membranes. Cell Tissue Bank 17:1–8

    Article  Google Scholar 

  • Parolini O et al (2008) Concise review: isolation and characterization of cells from human term placenta: outcome of the first international workshop on placenta derived. Stem Cells 26(2):300–311

    Article  PubMed  Google Scholar 

  • Pena JDO et al (2007) Ultrastructural and growth factor analysis of amniotic membrane preserved by different methods for ocular surger. Arq Bras Oftalmol 70:756–762

    Article  Google Scholar 

  • Qureshi IZ, Fareeha A, Khan WA (2010) Technique for processing and preservation of human amniotic membrane for ocular surface reconstruction. World Acad Sci Eng Technol 69:763–766

    Google Scholar 

  • Rama P, Giannini R, Bruni A, Gatto C, Tiso R, Ponzin D (2001) Further evaluation of amniotic membrane banking for transplantation in ocular surface diseases. Cell Tissue Bank 2:155–163

    Article  CAS  PubMed  Google Scholar 

  • Rayate M, Gavhane N, Bhattacharya N, Burd A (2016) Efficacy of freshly collected amniotic membrane local application in wound management. IJIR 2(7):1562–1569

    Google Scholar 

  • 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 31:216–225

    Article  CAS  PubMed  Google Scholar 

  • Riboh JC, Saltzman BM, Yanke AB, Cole BJ (2016) Human amniotic membrane-derived products in sports medicine: basic science, early results, and potential clinical applications. Am J Sports Med 44:2425–2434

    Article  PubMed  Google Scholar 

  • Ricci E et al (2013) Anti-fibrotic effects of fresh and cryopreserved human amniotic membrane in a rat liver fibrosis model. Cell Tissue Bank 14:475–488

    Article  CAS  PubMed  Google Scholar 

  • Rodríguez-Ares MT et al (2009) Effects of lyophilization on human amniotic membrane. Acta Ophthalmol 87:396–403

    Article  PubMed  Google Scholar 

  • Roy A, Mantay M, Brannan C, Griffiths S (2022) Placental tissues as biomaterials in regenerative medicine. BioMed Res Int. https://doi.org/10.1155/2022/6751456

    Article  PubMed  PubMed Central  Google Scholar 

  • Russo A, Bonci P, Bonci P (2012) The effects of different preservation processes on the total protein and growth factor content in a new biological product developed from human amniotic membrane. Cell Tissue Bank 13:353–361

    Article  CAS  PubMed  Google Scholar 

  • Schulze U, Hampel U, Sel S, Goecke TW, Thäle V, Garreis F, Paulsen F (2012) Fresh and cryopreserved amniotic membrane secrete the trefoil factor family peptide 3 that is well known to promote wound healing. Histochem Cell Biol 138:243–250

    Article  CAS  PubMed  Google Scholar 

  • Sekar S, Sasirekha K, Krishnakumar S, Sastry T (2013) A novel cross-linked human amniotic membrane for corneal implantations. Proc Inst Mech Eng Part H J Eng Med 227:221–228

    Article  CAS  Google Scholar 

  • Seo JH, Kim YH, Kim JS (2008) Properties of the amniotic membrane may be applicable in cancer therapy. Med Hypotheses 70:812–814

    Article  CAS  PubMed  Google Scholar 

  • Shi Q, Xie Y, Wang Y, Li S (2017) Vitrification versus slow freezing for human ovarian tissue cryopreservation: a systematic review and meta-anlaysis. Sci Rep 7:8538

    Article  ADS  PubMed  PubMed Central  Google Scholar 

  • Si J-W, Wang X-D, Shen SG (2015) Perinatal stem cells: a promising cell resource for tissue engineering of craniofacial bone. World J Stem Cells 7:149

    Article  PubMed  PubMed Central  Google Scholar 

  • Silini AR, Magatti M, Cargnoni A, Parolini O (2017) Is immune modulation the mechanism underlying the beneficial effects of amniotic cells and their derivatives in regenerative medicine? Cell Transplant 26:531–539

    Article  PubMed  PubMed Central  Google Scholar 

  • Singh R, Chacharkar M (2011) Dried gamma-irradiated amniotic membrane as dressing in burn wound care. J Tissue Viability 20:49–54

    Article  PubMed  Google Scholar 

  • Singh R, Gupta P, Kumar P, Kumar A, Chacharkar M (2003) Properties of air dried radiation processed amniotic membranes under different storage conditions. Cell Tissue Bank 4:95–100

    Article  PubMed  Google Scholar 

  • Spoerl E, Wollensak G, Reber F, Pillunat L (2004) Cross-linking of human amniotic membrane by glutaraldehyde. Ophthalmic Res 36:71–77

    Article  CAS  PubMed  Google Scholar 

  • Strom SC, Gramignoli R (2016) Human amnion epithelial cells expressing HLA-G as novel cell-based treatment for liver disease. Hum Immunol 77:734–739

    Article  CAS  PubMed  Google Scholar 

  • Taravella MJ, Chang CD (2001) 2-Octyl cyanoacrylate medical adhesive in treatment of a corneal perforation. Cornea 20:220–221

    Article  CAS  PubMed  Google Scholar 

  • Thomasen H, Pauklin M, Steuhl K-P, Meller D (2009) Comparison of cryopreserved and air-dried human amniotic membrane for ophthalmologic applications. Graefes Arch Clin Exp Ophthalmol 247:1691–1700

    Article  PubMed  Google Scholar 

  • Thomasen H et al (2011) The effect of long-term storage on the biological and histological properties of cryopreserved amniotic membrane. Curr Eye Res 36:247–255

    Article  ADS  CAS  PubMed  Google Scholar 

  • Toda A, Okabe M, Yoshida T, Nikaido T (2007) The potential of amniotic membrane/amnion-derived cells for regeneration of various tissues. J Pharmacol Sci 105:215–228

    Article  CAS  PubMed  Google Scholar 

  • Tomita T (2012) New dried human amniotic membrane is useful as a substitute for dural repair after skull base surgery. J Neurol Surg B Skull Base 73:302–307

    Article  PubMed  PubMed Central  Google Scholar 

  • Tseng SC, Prabhasawat P, Lee S-H (1997) Amniotic membrane transplantation for conjunctival surface reconstruction. Am J Ophthalmol 124:765–774

    Article  CAS  PubMed  Google Scholar 

  • Tsuno H et al (2014) Intraoral application of hyperdry amniotic membrane to surgically exposed bone surface. Oral Surg Oral Med Oral Pathol Oral Radiol 117:e83–e87

    Article  PubMed  Google Scholar 

  • Valentin J (2004) Low-dose extrapolation of radiation-related cancer risk. Ann ICRP 35:1–140

    Google Scholar 

  • Wassmer C-H, Berishvili E (2020) Immunomodulatory properties of amniotic membrane derivatives and their potential in regenerative medicine. Curr Diabetes Rep 20:1–10

    Article  Google Scholar 

  • Wolbank S et al (2009) Impact of human amniotic membrane preparation on release of angiogenic factors. J Tissue Eng Regen Med 3:651–654

    Article  CAS  PubMed  Google Scholar 

  • Yang P et al (2018) Biological characterization of human amniotic epithelial cells in a serum-free system and their safety evaluation. Acta Pharmacol Sin 39(8):1305–1316

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yatim RM, Kannan TP, Ab Hamid SS, Shamsudin SH (2013) Effects of different processing methods of human amniotic membrane on the quality of extracted RNA. Arch Orofac Sci 8:47–53

    Google Scholar 

  • Zare-Bidaki M, Sadrinia S, Erfani S, Afkar E, Ghanbarzade N (2017) Antimicrobial properties of amniotic and chorionic membranes: a comparative study of two human fetal sacs. J Reprod Infertil 18:218

    PubMed  PubMed Central  Google Scholar 

  • Zhou W et al (2013) Characterization of neural cell differentiation potential of human amnion derived epithelia cells and mesenchymal stem cells. Cytotherapy 15:S33

    Article  Google Scholar 

  • Zidan SM et al (2015) Maximizing the safety of glycerol preserved human amniotic membrane as a biological dressing. Burns 41:1498–1503

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

This study is related to the project No 1399/61273 from Student Research Committee, Shahid Beheshti University of Medical Sciences, Tehran, Iran. We also appreciate the “Student Research Committee” and “Research & Technology Chancellor” in Shahid Beheshti University of Medical Sciences for their financial support of this study.

Author information

Authors and Affiliations

Authors

Contributions

AJ contributed to the investigation, drew all figures, and wrote the original draft of the manuscript. MRT and HN contributed to the conceptualization and supervised the study. AJ, YM, AHM, and ZJ contributed for editing and revision of text. All authors read and approved the final manuscript.

Corresponding author

Correspondence to Mostafa Rezaei-Tavirani.

Ethics declarations

Conflict of interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Jafari, A., Mirzaei, Y., Mer, A.H. et al. Comparison of the effects of preservation methods on structural, biological, and mechanical properties of the human amniotic membrane for medical applications. Cell Tissue Bank 25, 305–323 (2024). https://doi.org/10.1007/s10561-023-10114-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10561-023-10114-z

Keywords

Navigation