Use of Amniotic Membrane and Its Derived Products for Bone Regeneration: A Systematic Review

Thanks to their biological properties, amniotic membrane (AM), and its derivatives are considered as an attractive reservoir of stem cells and biological scaffolds for bone regenerative medicine. The objective of this systematic review was to assess the benefit of using AM and amniotic membrane-derived products for bone regeneration. An electronic search of the MEDLINE—Pubmed database and the Scopus database was carried out and the selection of articles was performed following PRISMA guidelines. This systematic review included 42 articles taking into consideration the studies in which AM, amniotic-derived epithelial cells (AECs), and amniotic mesenchymal stromal cells (AMSCs) show promising results for bone regeneration in animal models. Moreover, this review also presents some commercialized products derived from AM and discusses their application modalities. Finally, AM therapeutic benefit is highlighted in the reported clinical studies. This study is the first one to systematically review the therapeutic benefits of AM and amniotic membrane-derived products for bone defect healing. The AM is a promising alternative to the commercially available membranes used for guided bone regeneration. Additionally, AECs and AMSCs associated with an appropriate scaffold may also be ideal candidates for tissue engineering strategies applied to bone healing. Here, we summarized these findings and highlighted the relevance of these different products for bone regeneration.

[1]  S. Catros,et al.  Comparison of amniotic membrane versus the induced membrane for bone regeneration in long bone segmental defects using calcium phosphate cement loaded with BMP-2. , 2021, Materials science & engineering. C, Materials for biological applications.

[2]  R. Sen,et al.  Decellularized bone matrix/oleoyl chitosan derived supramolecular injectable hydrogel promotes efficient bone integration. , 2021, Materials science & engineering. C, Materials for biological applications.

[3]  L. de Noronha,et al.  Combined Biomaterials: Amniotic Membrane and Adipose Tissue to Restore Injured Bone as Promoter of Calcification in Bone Regeneration: Preclinical Model , 2020, Calcified Tissue International.

[4]  H. Xin,et al.  Characteristics and Therapeutic Potential of Human Amnion-Derived Stem Cells , 2021, International journal of molecular sciences.

[5]  I. Shabani,et al.  A Review on Modifications of Amniotic Membrane for Biomedical Applications , 2021, Frontiers in Bioengineering and Biotechnology.

[6]  S. Catros,et al.  Chorion and amnion/chorion membranes in oral and periodontal surgery: A systematic review. , 2020, Journal of biomedical materials research. Part B, Applied biomaterials.

[7]  T. Talaei-Khozani,et al.  Mesenchymal stem cells: amazing remedies for bone and cartilage defects , 2020, Stem Cell Research & Therapy.

[8]  Y. Yang,et al.  Regenerative Approaches for the Treatment of Large Bone Defects. , 2020, Tissue engineering. Part B, Reviews.

[9]  Leila Sabouri,et al.  Mineralized Human Amniotic Membrane as a Biomimetic Scaffold for Hard Tissue Engineering Applications. , 2020, ACS biomaterials science & engineering.

[10]  Paola Aprile,et al.  Membranes for Guided Bone Regeneration: A Road from Bench to Bedside , 2020, Advanced healthcare materials.

[11]  Wenjie Zhang,et al.  Human amniotic mesenchymal stromal cells promote bone regeneration via activating endogenous regeneration , 2020, Theranostics.

[12]  Wei Huang,et al.  Three-dimensional silk fibroin scaffolds enhance the bone formation and angiogenic differentiation of human amniotic mesenchymal stem cells: a biocompatibility analysis. , 2020, Acta biochimica et biophysica Sinica.

[13]  S. Catros,et al.  Assessment of fresh and preserved amniotic membrane for guided bone regeneration in mice. , 2020, Journal of biomedical materials research. Part A.

[14]  S. Catros,et al.  Comparison of the impact of preservation methods on amniotic membrane properties for tissue engineering applications. , 2019, Materials science & engineering. C, Materials for biological applications.

[15]  B. Polat,et al.  The effects of cryopreserved human amniotic membrane on fracture healing: Animal study , 2019, Acta orthopaedica et traumatologica turcica.

[16]  H. Xin,et al.  Human amniotic mesenchymal stem cells and their paracrine factors promote wound healing by inhibiting heat stress-induced skin cell apoptosis and enhancing their proliferation through activating PI3K/AKT signaling pathway , 2019, Stem Cell Research & Therapy.

[17]  A. Khojasteh,et al.  Improved bone regeneration through amniotic membrane loaded with buccal fat pad-derived MSCs as an adjuvant in maxillomandibular reconstruction. , 2019, Journal of cranio-maxillo-facial surgery : official publication of the European Association for Cranio-Maxillo-Facial Surgery.

[18]  G. Ameer,et al.  Polymer-integrated amnion scaffold significantly improves cleft palate repair. , 2019, Acta biomaterialia.

[19]  J. V. Van Sickels,et al.  Resorbable Versus Nonresorbable Membranes: When and Why? , 2019, Dental clinics of North America.

[20]  M. Kita,et al.  Transplantation of dental pulp-derived cell sheets cultured on human amniotic membrane induced to differentiate into bone. , 2019, Oral diseases.

[21]  R. Tuan,et al.  Bone marrow mesenchymal stem cells: Aging and tissue engineering applications to enhance bone healing. , 2019, Biomaterials.

[22]  A. Khojasteh,et al.  Buccal fat pad-derived stem cells with anorganic bovine bone mineral scaffold for augmentation of atrophic posterior mandible: An exploratory prospective clinical study. , 2019, Clinical implant dentistry and related research.

[23]  H. Shah,et al.  Buccal Fat Pad-Derived Stem Cells for Repair of Maxillofacial Bony Defects , 2019, Journal of Maxillofacial and Oral Surgery.

[24]  L. Melek,et al.  Histologic and histomorphometric evaluation of lyophilized amniotic membrane in bone healing: An experimental study in rabbit's femur , 2018, Future Dental Journal.

[25]  A. Khoshzaban,et al.  Histological Comparison of New Bone Formation Using Amnion Membrane Graft Versus Resorbable Collagen Membrane: An Animal Study. , 2018, The Journal of oral implantology.

[26]  A. Abbaszadeh,et al.  Evaluation of Osteoinductive and Osteoconductive Effect of the Amniotic Membrane in Bone Defects due to Open Fractures in Rabbits , 2018, Journal of Orthopedic and Spine Trauma.

[27]  R. Bareille,et al.  Human amniotic membrane for guided bone regeneration of calvarial defects in mice , 2018, Journal of Materials Science: Materials in Medicine.

[28]  Jaspreet Kaur,et al.  Regenerative potential of autologous platelet-rich fibrin with and without amnion membrane in the treatment of Grade-II furcation defects: A clinicoradiographic study , 2018, Journal of Indian Society of Periodontology.

[29]  J. Fricain,et al.  The periosteum-like effect of fresh human amniotic membrane on bone regeneration in a rabbit critical-sized defect model. , 2018, Bone.

[30]  Mehrdad H. Farahani,et al.  Amniotic membrane and its epithelial and mesenchymal stem cells as an appropriate source for skin tissue engineering and regenerative medicine , 2018, Artificial cells, nanomedicine, and biotechnology.

[31]  S. Catros,et al.  What is the benefit of using amniotic membrane in oral surgery? A comprehensive review of clinical studies , 2018, Clinical Oral Investigations.

[32]  T. Grzela,et al.  Amount and distribution of selected biologically active factors in amniotic membrane depends on the part of amnion and mode of childbirth. Can we predict properties of amnion dressing? A proof-of-concept study , 2018, Central-European journal of immunology.

[33]  N. El-Badri,et al.  Development of decellularized amniotic membrane as a bioscaffold for bone marrow-derived mesenchymal stem cells: ultrastructural study , 2018, Journal of Molecular Histology.

[34]  Shagufta Parveen Establishment and characterization of induced pluripotent stem cells from placental mesenchymal stromal cells. , 2018, Stem cell research.

[35]  M. Kreft,et al.  Human Amniotic Membrane and Amniotic Membrane–Derived Cells , 2018, Cell transplantation.

[36]  L. Centurione,et al.  Mapping of the Human Placenta , 2018, Cell transplantation.

[37]  T. Guda,et al.  A Novel Secretome Biotherapeutic Influences Regeneration in Critical Size Bone Defects , 2017, The Journal of craniofacial surgery.

[38]  Ting-fang Sun,et al.  Human acellular amniotic membrane: A potential osteoinductive biomaterial for bone regeneration , 2018, Journal of biomaterials applications.

[39]  J. Fricain,et al.  Similarities between induced membrane and amniotic membrane: Novelty for bone repair. , 2017, Placenta.

[40]  R. Kolte,et al.  Volumetric Assessment of Regenerative Efficacy of Demineralized Freeze-Dried Bone Allograft With or Without Amnion Membrane in Grade II Furcation Defects: A Cone Beam Computed Tomography Study. , 2017, The international journal of periodontics & restorative dentistry.

[41]  G. Romanos,et al.  Limitations and options using resorbable versus nonresorbable membranes for successful guided bone regeneration. , 2017, Quintessence international.

[42]  C. Meyer,et al.  Fresh and in vitro osteodifferentiated human amniotic membrane, alone or associated with an additional scaffold, does not induce ectopic bone formation in Balb/c mice , 2017, Cell and Tissue Banking.

[43]  D. D. Sali,et al.  Demineralized Freeze Dried Bone Allograft With Amniotic Membrane in the Treatment of Periodontal Intrabony Defects - 12 Month Randomized Controlled Clinical Trial. , 2016, Journal of periodontology.

[44]  Y. Izumi,et al.  Double-layered cell transfer technology for bone regeneration , 2016, Scientific Reports.

[45]  Seongho Han,et al.  Amniotic epithelial cells promote wound healing in mice through high epithelialization and engraftment , 2016, Journal of tissue engineering and regenerative medicine.

[46]  P. Nunley,et al.  Preliminary Results of Bioactive Amniotic Suspension with Allograft for Achieving One and Two-Level Lumbar Interbody Fusion , 2016, International Journal of Spine Surgery.

[47]  Jyh‐Horng Wang,et al.  Amniotic membrane and adipose-derived stem cell co-culture system enhances bone regeneration in a rat periodontal defect model. , 2016, Journal of the Formosan Medical Association = Taiwan yi zhi.

[48]  S. Dhara,et al.  Investigating the potential of human placenta-derived extracellular matrix sponges coupled with amniotic membrane-derived stem cells for osteochondral tissue engineering. , 2016, Journal of materials chemistry. B.

[49]  H. Niknejad,et al.  The effects of cryopreservation on angiogenesis modulation activity of human amniotic membrane. , 2015, Cryobiology.

[50]  Bryn L. Brazile,et al.  Investigating the Potential of Amnion-Based Scaffolds as a Barrier Membrane for Guided Bone Regeneration. , 2015, Langmuir : the ACS journal of surfaces and colloids.

[51]  N. Sabetkish,et al.  Evaluating the bone regeneration in calvarial defect using osteoblasts differentiated from adipose-derived mesenchymal stem cells on three different scaffolds: an animal study , 2015, Cell and Tissue Banking.

[52]  T. Guda,et al.  Evaluation of Amniotic Multipotential Tissue Matrix to Augment Healing of Demineralized Bone Matrix in an Animal Calvarial Model , 2015, The Journal of craniofacial surgery.

[53]  Farin Kiany,et al.  Amnion membrane as a novel barrier in the treatment of intrabony defects: a controlled clinical trial. , 2015, The International Journal of Oral and Maxillofacial Implants.

[54]  R. Chandra,et al.  Evaluation of clinical, antiinflammatory and antiinfective properties of amniotic membrane used for guided tissue regeneration: A randomized controlled trial , 2015, Dental research journal.

[55]  J. Dai,et al.  Comparative Investigation of Human Amniotic Epithelial Cells and Mesenchymal Stem Cells for Application in Bone Tissue Engineering , 2015, Stem cells international.

[56]  M. Soleimani,et al.  Comparison of osteogenic differentiation potential of human adult stem cells loaded on bioceramic‐coated electrospun poly (L‐lactide) nanofibres , 2015, Cell proliferation.

[57]  D. Sabry,et al.  The Efficacy of Cryopreserved Amniotic Membrane seeded with Mesenchymal Stem Cells for Management of Bone Defect in a Canine Model. , 2015 .

[58]  W. Xudong,et al.  Osteogenic Differentiation of Human Amniotic Epithelial Cells and Its Application in Alveolar Defect Restoration , 2014, Stem cells translational medicine.

[59]  W. Tan,et al.  Ectopic Osteogenesis of Macroscopic Tissue Constructs Assembled from Human Mesenchymal Stem Cell-Laden Microcarriers through In Vitro Perfusion Culture , 2014, PloS one.

[60]  D. Grande,et al.  Evaluation of Amniotic-Derived Membrane Biomaterial as an Adjunct for Repair of Critical Sized Bone Defects , 2014 .

[61]  C. Koike,et al.  Intraoral application of hyperdry amniotic membrane to surgically exposed bone surface. , 2014, Oral surgery, oral medicine, oral pathology and oral radiology.

[62]  G. Hoser,et al.  Growth factors and their receptors derived from human amniotic cells in vitro. , 2014, Folia histochemica et cytobiologica.

[63]  C. Meyer,et al.  Human Amniotic Membrane: Clinical Uses, Patents And Marketed Products , 2013 .

[64]  A. Mauro,et al.  Synthetic Bone Substitute Engineered with Amniotic Epithelial Cells Enhances Bone Regeneration after Maxillary Sinus Augmentation , 2013, PloS one.

[65]  R. González-Ramírez,et al.  Characterization of mesenchymal stem cell subpopulations from human amniotic membrane with dissimilar osteoblastic potential. , 2013, Stem cells and development.

[66]  H. Niknejad,et al.  Side dependent effects of the human amnion on angiogenesis. , 2013, Placenta.

[67]  H. Redl,et al.  Anti-fibrotic effects of fresh and cryopreserved human amniotic membrane in a rat liver fibrosis model , 2013, Cell and Tissue Banking.

[68]  C. Koike,et al.  Application of human amniotic mesenchymal cells as an allogeneic transplantation cell source in bone regenerative therapy , 2012 .

[69]  T. Nikaido,et al.  Applications of Amniotic Membrane and Fluid in Stem Cell Biology and Regenerative Medicine , 2012, Stem cells international.

[70]  Kyung-A Hwang,et al.  Potential antitumor therapeutic strategies of human amniotic membrane and amniotic fluid-derived stem cells , 2012, Cancer Gene Therapy.

[71]  A. Abrantes,et al.  Amniotic membrane: from structure and functions to clinical applications , 2012, Cell and Tissue Research.

[72]  A. Nguyen,et al.  Brief review of models of ectopic bone formation. , 2012, Stem cells and development.

[73]  S. Teoh,et al.  The potential of human fetal mesenchymal stem cells for off-the-shelf bone tissue engineering application. , 2012, Biomaterials.

[74]  S. Kang,et al.  Immunomodulatory effects of human amniotic membrane-derived mesenchymal stem cells , 2012, Journal of veterinary science.

[75]  A. Mauro,et al.  Stemness characteristics and osteogenic potential of sheep amniotic epithelial cells , 2012, Cell biology international.

[76]  I. Morita,et al.  Cell‐printing and transfer technology applications for bone defects in mice , 2011, Journal of tissue engineering and regenerative medicine.

[77]  M. McKee,et al.  Managing Bone Defects , 2011, Journal of orthopaedic trauma.

[78]  Shigeo Saito,et al.  Establishment and characterization of a pluripotent stem cell line derived from human amniotic membranes and initiation of germ layers in vitro , 2008, Human Cell.

[79]  M. Swartz The PRISMA statement: a guideline for systematic reviews and meta-analyses. , 2011, Journal of pediatric health care : official publication of National Association of Pediatric Nurse Associates & Practitioners.

[80]  F. Blanco,et al.  Isolation and characterization of mesenchymal stem cells from human amniotic membrane. , 2011, Tissue engineering. Part C, Methods.

[81]  A. Khoshzaban,et al.  Human amniotic membrane, best healing accelerator, and the choice of bone induction for vestibuloplasty technique (an animal study) , 2010 .

[82]  Helene Polin,et al.  Osteogenic differentiation of intact human amniotic membrane. , 2010, Biomaterials.

[83]  L. Bockeria,et al.  New approach to reduce allograft tissue immunogenicity. Experimental data. , 2010, Interactive cardiovascular and thoracic surgery.

[84]  J. Mehta,et al.  Preservation, sterilization and de-epithelialization of human amniotic membrane for use in ocular surface reconstruction. , 2010, Biomaterials.

[85]  F. Gudé,et al.  Effects of lyophilization on human amniotic membrane , 2009, Acta ophthalmologica.

[86]  D. Schmidt,et al.  Amniotic membrane and amniotic fluid-derived cells: potential tools for regenerative medicine? , 2009, Regenerative medicine.

[87]  Shaila Kothiwale,et al.  A clinical and radiological evaluation of DFDBA with amniotic membrane versus bovine derived xenograft with amniotic membrane in human periodontal grade II furcation defects , 2009, Cell and Tissue Banking.

[88]  Y. Moodley,et al.  Human fetal membranes: a source of stem cells for tissue regeneration and repair? , 2009, Placenta.

[89]  J. Fisher,et al.  Biocompatibility and potential of acellular human amniotic membrane to support the attachment and proliferation of allogeneic cells. , 2008, Tissue engineering. Part A.

[90]  Mark A. Lee,et al.  Nonunions and the potential of stem cells in fracture-healing. , 2008, The Journal of bone and joint surgery. American volume.

[91]  Toshio Miki,et al.  Concise Review: Isolation and Characterization of Cells from Human Term Placenta: Outcome of the First International Workshop on Placenta Derived Stem Cells , 2008, Stem cells.

[92]  M. Pera,et al.  Stem Cells Derived from Human Fetal Membranes Display Multilineage Differentiation Potential , 2007, Biology of reproduction.

[93]  O. Barbier,et al.  Bone allografts: What they can offer and what they cannot. , 2007, The Journal of bone and joint surgery. British volume.

[94]  A. Bocking,et al.  Expression of natural antimicrobials by human placenta and fetal membranes. , 2007, Placenta.

[95]  T. Nikaido,et al.  The potential of amniotic membrane/amnion-derived cells for regeneration of various tissues. , 2007, Journal of pharmacological sciences.

[96]  N. Koizumi,et al.  Comparison of intact and denuded amniotic membrane as a substrate for cell-suspension culture of human limbal epithelial cells , 2006, Graefe's Archive for Clinical and Experimental Ophthalmology.

[97]  A C Masquelet,et al.  Induced membranes secrete growth factors including vascular and osteoinductive factors and could stimulate bone regeneration , 2004, Journal of orthopaedic research : official publication of the Orthopaedic Research Society.

[98]  Paolo Giannoni,et al.  Tissue engineering and cell therapy of cartilage and bone. , 2003, Matrix biology : journal of the International Society for Matrix Biology.

[99]  M. Gomes,et al.  Histologic evaluation of the osteoinductive property of autogenous demineralized dentin matrix on surgical bone defects in rabbit skulls using human amniotic membrane for guided bone regeneration. , 2001, The International journal of oral & maxillofacial implants.

[100]  M. Usui,et al.  Immunogenicity of human amniotic membrane in experimental xenotransplantation. , 2001, Investigative ophthalmology & visual science.

[101]  H L Wang,et al.  Collagen membranes: a review. , 2001, Journal of periodontology.

[102]  D. H. Ma,et al.  Identification of Antiangiogenic and Antiinflammatory Proteins in Human Amniotic Membrane , 2000, Cornea.

[103]  N. Koizumi,et al.  Growth factor mRNA and protein in preserved human amniotic membrane , 2000 .

[104]  S. Tseng,et al.  Suppression of TGF-ß signaling in both normal conjunctival fibroblasts and pterygial body fibroblasts by amniotic membrane , 2000 .

[105]  G. Bourne The Fœtal Membranes , 1962 .