The clinical effectiveness of cryopreserved human amniotic membrane in diabetic foot syndrome

Home/2021, Vol. 9, No. 2/The clinical effectiveness of cryopreserved human amniotic membrane in diabetic foot syndrome

Cell and Organ Transplantology. 2021; 9(2):80-87.
DOI: 10.22494/cot.v9i2.129

The clinical effectiveness of cryopreserved human amniotic membrane in diabetic foot syndrome

Ustymenko A.1,2, Nemtinov P.3,4, Bolgarska S.5, Zaika L.5, Shablii V.4,6, Bukreieva T.4, Orlenko V.5, Palіanytsia S.3

  • 1State Institute of Genetic and Regenerative Medicine, National Academy of Medical Sciences of Ukraine, Kyiv, Ukraine 
  • 2D. F. Chebotarev State Institute of Gerontology, National Academy of Medical Sciences of Ukraine, Kyiv, Ukraine
  • 3Coordination Center for Transplantation of OrgansTissues and Cells, Ministry of Health of Ukraine, Kyiv, Ukraine
  • 4Institute of Cell Therapy, Kyiv, Ukraine
  • 5V. P. Komisarenko State Institute of Endocrynology, National Academy of Medical Sciences of Ukraine, Kyiv, Ukraine
  • 6Institute of Molecular Biology and Genetics, National Academy of Sciences of Ukraine, Kyiv, Ukraine

Abstract

Diabetic foot syndrome with long-term unhealed wounds is the most common complication and cause of limb amputation in diabetes. The search for effective therapeutic agents and their inclusion in treatment protocols is a priority due to the increase in the number of cases of this socially significant disease and disability among the working population every year.
The aim of the study is to evaluate the effectiveness of cryopreserved human amniotic membrane in the treatment of long-term non-healing wounds of the lower extremities in diabetic foot syndrome.
Materials and methods. The pilot clinical study described 4 clinical cases of treatment of patients with diabetes mellitus type I and II (1 woman and 3 men aged 52 to 68 years) with long-term unhealed wounds of the limbs under standard therapy. After previous wound sanation the applications of the cryopreserved human amniotic membrane were performed. Once a week after the application, the dynamics of wound healing was assessed. Blood glucose levels were determined before amniotic membrane treatment and two hours after the procedure.
Results. As a results of weekly applications of human amniotic membrane there was a gradual decrease in the area of the wound from the original size and increase the rate of healing. Thus, at the time of the second visit (after 7 days) the reduction in the area of the ulcer from the initial size in patient 1 was 33 %, patient 2 – 25 %, patient 3 – 33 % on the sole and patient 4 – 3 %, and the healing rate – 4.7 %, 3.6 %, 4.7 % and 0.43 % per day, respectively. The use of human amniotic membrane did not affect blood glucose levels when comparing values before application and two hours after the procedure. Regular follow-up visits of patients 3, 6, 9 and 12 months after the start of the study showed no recurrence of ulcers.
Conclusions. It has been shown that the use of cryopreserved human amniotic membrane in patients with diabetes mellitus and diabetic foot syndrome with long-term unhealed wounds results in complete healing of ulcers with stable remission during the year of observation.

Key words: diabetes; diabetic foot; cryopreserved human amniotic membrane; tissue therapy 

Full Text PDF

1. Available from: https://www.who.int/news-room/fact-sheets/detail/diabetes
2. Maren Volmer-Thole, Ralf Lobmann. Neuropathy and Diabetic Foot Syndrome. Int J Mol Sci. 2016; 17(6):917.
https://doi.org/10.3390/ijms17060917
PMid:27294922 PMCid:PMC4926450
3. Schofield CJ, Libby G, Brennan G, MacAlpine R, Morris A, Leese GP. Mortality and Hospitalization in Patients After Amputation. Diabetes Care. 2006; 29:2252-2256.
https://doi.org/10.2337/dc06-0926
PMid:17003302
4. Available from: https://www.phc.org.ua/news/ponad-70-zagalnoi-kilkosti-schorichnikh-amputaciy-e-naslidkom-cukrovogo-diabetu
5. Dehkordi AN, Babaheydari FM, Chehelgerdi M, Dehkordi ShR. Skin tissue engineering: wound healing based on stem-cell-based therapeutic strategies. Stem Cell Res Ther. 2019; 10.
https://doi.org/10.1186/s13287-019-1212-2
PMid:30922387 PMCid:PMC6440165
6. Greer N, Foman NA, MacDonald R, et al. Advanced wound care therapies for nonhealing diabetic, venous, and arterial ulcers: a systematic review. Ann Intern Med. 2013; 159(8):532-542. https://doi.org/10. 7326/0003-4819-159-8-201310150-00006
https://doi.org/10.7326/0003-4819-159-8-201310150-00006
PMid:24126647
7. Kosaric N, Kiwanuka H, Gurtne G. Stem Cell Therapies for Wound Healing. Expert Opin Biol Ther. 2019; Issue 6. DOI: 10.1080/14712598.2019.1596257
https://doi.org/10.1080/14712598.2019.1596257
PMid:30900481
8. Garwood CS, Steinberg JS, Kim PJ. Bioengineered Alternative Tissues in Diabetic Wound Healing. Clin Podiatr Med Surg. 2015; 31(1):121-33.
https://doi.org/10.1016/j.cpm.2014.09.004
PMid:25440423
9. Chen M, Przyborowski M, Berthiaume F. Stem cells for skin tissue engineering and wound healing. Crit Rev Biomed Eng. 2009; 37:399-421.
https://doi.org/10.1615/CritRevBiomedEng.v37.i4-5.50
PMid:20528733 PMCid:PMC3223487
10. Duscher D, Barrera J, Wong VW, Maan ZN, Whittam AJ, Januszyk M, et al. Stem cells in wound healing: the future of regenerative medicine? A mini-review. Gerontology. 2016; 62:216-25.
https://doi.org/10.1159/000381877
PMid:26045256
11. Dash B, Xu Z, Lin L, Koo A, Ndon S, Berthiaume F, et al. Stem cells and engineered scaffolds for regenerative wound healing. Bioengineering. 2018; 5:23.
https://doi.org/10.3390/bioengineering5010023
PMid:29522497 PMCid:PMC5874889
12. Guenou H, Nissan X, Larcher F, Feteira J, Lemaitre G, Saidani M, et al. Human embryonic stem-cell derivatives for full reconstruction of the pluristratified epidermis: a preclinical study. Lancet. 2009; 374:1745-53.
https://doi.org/10.1016/S0140-6736(09)61496-3
13. Okano H,Nakamura M, Yoshida K, Okada Y, Tsuji O, Nori S, et al. Steps toward safe cell therapy using induced pluripotent stem cells. Circ Res. 2013; 112:523-33.
https://doi.org/10.1161/CIRCRESAHA.111.256149
PMid:23371901
14. Okita K, Ichisaka T, Yamanaka S. Generation of germline-competent induced pluripotent stem cells. Nature. 2007; 448:313-7.
https://doi.org/10.1038/nature05934
PMid:17554338
15. Parolini O, Alviano F, Bagnara GP, Bilic G, Bühring HJ, Evangelista M, et al. Concise review: isolation and characterization of cells from human term placenta: outcome of the first international Workshop on Placenta Derived Stem Cells. Stem Cells. 2008; 26:300-311. DOI: 10.1634/stemcells.2007-0594
https://doi.org/10.1634/stemcells.2007-0594
PMid:17975221
16. Dua HS, Gomes JAP, King А. The amniotic membrane in ophthalmology. Survey of Ophthalmology. 2004; 49:51-77
https://doi.org/10.1016/j.survophthal.2003.10.004
PMid:14711440
17. Gomes JAP, dos Santos MS, Cunha MC, de Nadai Barros J, de Sousa LB. Amniotic membrane transplantation for partial and total limbal stem cell deficiency secondary to chemical burn. Ophthalmology. 2003; 11(3):466-473.
https://doi.org/10.1016/S0161-6420(02)01888-2
18. Kern S, Eichler H, Stoeve J, Kluter H, Bieback K: Comparative analysis of mesenchymal stem cells from bone marrow, umbilical cord blood, or adipose tissue. Stem Cells. 2006; 24: 1294-1301. DOI: 10.1634/stemcells.2005-0342.
https://doi.org/10.1634/stemcells.2005-0342
PMid:16410387
19. de la Torre P, Pérez-Lorenzo MJ, Flores AI. Human placenta-derived mesenchymal stromal cells: a review from basic research to clinical applications. In: Valarmathi MT. editor. Stromal cells: structure, function, and therapeutic implications. London: IntechOpen, 2018. DOI: 10.5772/intechopen. doi: 10.5772/intechopen.76718
https://doi.org/10.5772/intechopen.76718
20. Macias MI, Grande J, MorenoA, Domínguez I, Bornstein R, Flores A. Isolation and characterization of true mesenchymal stem cells derived from human term decidua capable of multilineage differentiation into all 3 embryonic layers. Am J Obstet Gynecol 2010; 203:495.e9-23. DOI: 10.1016/j.ajog.2010.06.045
https://doi.org/10.1016/j.ajog.2010.06.045
PMid:20692642
21. Davis JS. Skin grafting at the Johns Hopkins Hospital. Ann Surg. 1909; 50:542-549.
https://doi.org/10.1097/00000658-190909000-00002
PMid:17862406 PMCid:PMC1407162
22. Dua HS, Gomes JA, King AJ, Maharajan V. The amniotic membrane in ophthalmology. Surv. Ophthalmol. 2004, 49:51-77.
https://doi.org/10.1016/j.survophthal.2003.10.004
PMid:14711440
23. Portmann-Lanz CB, Schoeberlein A, Huber A, Sager R, Malek A, Holzgreve W, et al. Placental mesenchymal stem cells as potential autologous graft for pre- and perinatal neuroregeneration. Am J Obstet Gynecol. 2006; 194(3):664-73.
https://doi.org/10.1016/j.ajog.2006.01.101
PMid:16522395
24. Abbasi-Kangevari M, Ghamari SH, Safaeinejad F, Bahrami S, Niknejad H. Potential Therapeutic Features of Human Amniotic Mesenchymal Stem Cells in Multiple Sclerosis: Immunomodulation, Inflammation Suppression, Angiogenesis Promotion, Oxidative Stress Inhibition, Neurogenesis Induction, MMPs Regulation, and Remyelination Stimulation. Front Immunol. 2019; 10:238.
https://doi.org/10.3389/fimmu.2019.00238
PMid:30842772 PMCid:PMC6391358
25. Koob TJ, Lim JJ, Massee M, et al. Properties of dehydrated human amnion/chorion composite grafts: implications for wound repair and soft tissue regeneration. J Biomed Mater Res B Appl Biomater. 2014; 102:1353-1362.
https://doi.org/10.1002/jbm.b.33141
PMid:24664953
26. Koob TJ, Rennert R, Zabek N, et al. Biological properties of dehydrated human amnion/chorion composite graft: implications for chronic wound healing. Int Wound J. 2013; 10:493-500.
https://doi.org/10.1111/iwj.12140
PMid:23902526 PMCid:PMC4228928
27. Koob TJ, Lim JJ, Massee M, et al. Angiogenic properties of dehydrated human amnion/chorion allografts: therapeutic potential for soft tissue repair and regeneration. Vasc Cell. 2014; 6:10.
https://doi.org/10.1186/2045-824X-6-10
PMid:24817999 PMCid:PMC4016655
28. Hardwicke J, Schmaljohann D, Boyce D, Thomas D. Epidermal growth factor therapy and wound healing – past, present and future perspectives. Surgeon. 2008; 6:172-7.
https://doi.org/10.1016/S1479-666X(08)80114-X
29. Yoshida S, Yamaguchi Y, Itami S, Yoshikawa K, Tabata Y, Matsumoto K. Neutralization of Hepatocyte Growth Factor Leads to Retarded Cutaneous Wound Healing Associated with Decreased Neovascularization and Granulation Tissue Formation JID. 2003; 2: 335-343. https://doi.org/10.1046/j.1523-1747.2003.12039.x
https://doi.org/10.1046/j.1523-1747.2003.12039.x
PMid:12542542
30. Nakamura Т, Мizuno Sh. The discovery of Hepatocyte Growth Factor (HGF) and its significance for cell biology, life sciences and clinical medicine Proc Jpn Acad Ser B Phys Biol Sci. 2010; 86(6):588-610. DOI: 10.2183/pjab.86.588
https://doi.org/10.2183/pjab.86.588
PMid:20551596 PMCid:PMC3081175
31. Ramirez H, Patel Sh, Pastar I. The Role of TGFβ Signaling in Wound Epithelialization. Adv Wound Care (New Rochelle). 2014; 3(7):482-491. DOI: 10.1089/wound.2013.0466
https://doi.org/10.1089/wound.2013.0466
PMid:25032068 PMCid:PMC4086377
32. Abdelhakim M, Lin X, Ogawa R. The Japanese Experience with Basic Fibroblast Growth Factor in Cutaneous Wound Management and Scar Prevention: A Systematic Review of Clinical and Biological Aspects. Dermatol Ther. 2020; 10:569-587.
https://doi.org/10.1007/s13555-020-00407-6
PMid:32506250 PMCid:PMC7367968
33. DiPietro LA, Polverini PJ. Role of the macrophage in the positive and negative regulation of wound neovascularisation. Am J Pathol. 1993; 143:678-684.
34. Bártolo I, Reis RL, Marques AP, Cerqueira MT. Keratinocyte Growth Factor-Based Strategies for Wound Re-Epithelialization. Tissue Engineering Part B. 2021. Available from: https://doi.org/10.1089/ten.teb.2021.0030
https://doi.org/10.1089/ten.teb.2021.0030
PMid:34238035
35. Aloe L, Rocco ML, Bianchi P, Manni L. Nerve growth factor: from the early discoveries to the potential clinical use. J Transl Med. 2012; 10:239.
https://doi.org/10.1186/1479-5876-10-239
PMid:23190582 PMCid:PMC3543237
36. Cianfarani F, Zambruno G, Brogelli L, Sera F, Lacal PM,¶ Pesce M, et al. Placenta Growth Factor in Diabetic Wound Healing. Am J Pathol. 2006; 169(4):1167-1182.
https://doi.org/10.2353/ajpath.2006.051314
PMid:17003476 PMCid:PMC1698842
37. Tan LJ, Lash В, Karami R, Nayer B, Lu Y-Z, Piotto C, et al. Restoration of the healing microenvironment in diabetic wounds with matrix-binding IL-1 receptor antagonist. Commun Biol. 2021.
https://doi.org/10.1038/s42003-021-01913-9
PMid:33772102 PMCid:PMC7998035
38. Bodnar RJ. Chemokine Regulation of Angiogenesis During Wound Healing. 2015. Available from: https://doi.org/10.1089/wound.2014.0594
https://doi.org/10.1089/wound.2014.0594
PMid:26543678 PMCid:PMC4620517
39. Witkowska AM, Borawska MH Soluble intercellular adhesion molecule-1 (sICAM-1): an overview. European Cytokine Network. 2004; 15(2):91-98.
40. Volpin G, Cohen M, Assaf M, Meir T, Katz R, Pollack S. Cytokine Levels (IL-4, IL-6, IL-8 and TGFβ) as Potential Biomarkers of Systemic Inflammatory Response in Trauma Patients. Int Orthop. 2014; 38(6):1303-1309. DOI: 10.1007/s00264-013-2261-2
https://doi.org/10.1007/s00264-013-2261-2
PMid:24402554 PMCid:PMC4037528
41. King A, Balaji S, Le L, Crombleholme T, Keswani S. Regenerative Wound Healing: The Role of Interleukin-10. 2014; 3(4):315-323.
https://doi.org/10.1089/wound.2013.0461
PMid:24757588 PMCid:PMC3985521
42. Ridiandries A, Tan JNM, Bursill C. The Role of Chemokines in Wound Healing. Int J Mol Sci. 2018; 19:3217. DOI: 10.3390/ijms19103217
https://doi.org/10.3390/ijms19103217
PMid:30340330 PMCid:PMC6214117
43. Bloom J, Shan S, Al-Abed Y. MIF, a controversial cytokine: a review of structural features, challenges, and opportunities for drug development. Expert Opin Ther Targets. 2016; 20(12):1463-1475.
https://doi.org/10.1080/14728222.2016.1251582
PMid:27762152
44. Kim BS, Breuer B, Arnke K, Ruhl T, Hofer T, Simons D, et al. The effect of the macrophage migration inhibitory factor (MIF) on excisional wound healing in vivo. J Plast Surg Hand Surg. 2020; 54(3):137-144. DOI: 10.1080/2000656X.2019.1710710
https://doi.org/10.1080/2000656X.2019.1710710
PMid:32281469
45. Tessa M. Simone and Paul J. Higgins Inhibition of SERPINE1 Function Attenuates Wound Closure in Response to Tissue Injury: A Role for PAI-1 in Re-Epithelialization and Granulation Tissue Formation. J Dev Biol. 2015; 3:11-24. DOI:10.3390/jdb3010011
https://doi.org/10.3390/jdb3010011
46. Rui Guo, Linlin Chai, Liang Chen, Wenguang Chen, Liangpeng Ge, Xiaoge Li, et al. Stromal cell-derived factor 1 (SDF-1) accelerated skin wound healing by promoting the migration and proliferation of epidermal stem cells. In Vitro Cell Dev Biol Anim. 2015; 51(6):578-85.
https://doi.org/10.1007/s11626-014-9862-y
PMid:25636237
47. Murphy JM, Young IG. IL-3, IL-5, and GM-CSF signaling: crystal structure of the human beta-common receptor Vitam Horm Journal. 2006. 74:1-30. DOI: 10.1016/S0083-6729(06)74001-8
https://doi.org/10.1016/S0083-6729(06)74001-8
48. Djuretic I, Gleason J, Guo Xinjian, Kaplunovsky A. Decellularized and dehydrated human amniotic membrane (DDHAM) in wound management: modulation of macrophage differentiation and activation. Wound Repair Regen. 2015; 23(2):A19-A19.
49. Ahuja N, Jin R, Powers C. Billi A, Bass K. Dehydrated Human Amnion Chorion Membrane as Treatment for Pediatric Burns. Advances in wound care. 2020; 9(11):602-612.
https://doi.org/10.1089/wound.2019.0983
PMid:33095127 PMCid:PMC7580638
50. Fenelon M, Maurel DB, Siadous R, Gremare A, Delmond S, Durand M, et al. Comparison of the impact of preservation methods on amniotic membrane properties for tissue engineering applications. Mater Sci Eng. 2019, 104:109903.
https://doi.org/10.1016/j.msec.2019.109903
PMid:31500032
51. Peter Alexander von Harbach Ferenczy, Luciene Barbosa de Souza. Comparison of the preparation and preservation techniques of amniotic membrane used in the treatment of ocular surface diseases. Rev Bras Oftalmol. 2020; 79(1):71-80. DOI 10.5935/0034-7280.20200016
https://doi.org/10.5935/0034-7280.20200016
52. Gibbons G. W. Grafix®, a Cryopreserved Placental Membrane, for the Treatment of Chronic/Stalled Wounds. Adv Wound Care (New Rochelle). 2015; 4(9):534-544. DOI: 10.1089/wound.2015.0647
https://doi.org/10.1089/wound.2015.0647
PMid:26339532 PMCid:PMC4529022
53. Thomasen H, Pauklin M, Steuhl KP, Meller D. Comparison of cryopreserved and air-dried human amniotic membrane for ophthalmologic applications. Graefe’s Arch Clin Exp. Ophthalmol. 2009; 247:1691-1700.
https://doi.org/10.1007/s00417-009-1162-y
PMid:19693529
54. Rodríguez-Ares MT, López-Valladares MJ, Touriño R, Vieites B, Gude F, Silva MT, et al. Effects of lyophilization on human amniotic membrane. Acta Ophthalmol. 2009; 87:396-403.
https://doi.org/10.1111/j.1755-3768.2008.01261.x
PMid:18937812
55. Niknejad H, Deihim T, Solati-Hashjin M, Peirovi H. The effects of preservation procedures on amniotic membrane’s ability to serve as a substrate for cultivation of endothelial cells. Cryobiology. 2011; 63:145-151.
https://doi.org/10.1016/j.cryobiol.2011.08.003
PMid:21884690
56. Chuck RS, Graff JM, Bryant MR, Sweet PM. Biomechanical Characterization of Human Amniotic Membrane Preparations for Ocular Surface Reconstruction. Ophthalmic Res. 2004; 36:341-348.
https://doi.org/10.1159/000081637
PMid:15627835
57. Malhotra C, Jain AK. Human amniotic membrane transplantation: Different modalities of its use in ophthalmology. World J Transplant. 2014; 4:111-121.
https://doi.org/10.5500/wjt.v4.i2.111
PMid:25032100 PMCid:PMC4094946
58. Wilshaw SP, Kearney JN, Fisher J, Ingham E. Production of an acellular amniotic membrane matrix for use in tissue engineering. Tissue Eng. 2006, 12, 2117-2129.
https://doi.org/10.1089/ten.2006.12.2117
PMid:16968153
59. Shablyy VA, Kuchma MD, Kyryk VM, Onishchenko GM, Tsupykov OM, Klymenko PP, et al. Рhenotype and migration potential of multipotent mesenchymal stromal cells from native and cryopreserved human placenta. Biotechnologia acta. 2012; 5(5):59.
60. Lavery LA, Fulmer J, Shebetka KA, Regulski M, Vayser D, Fried D. The efficacy and safety of Grafix(®) for the treatment of chronic diabetic foot ulcers: results of a multi-centre, controlled, randomised, blinded, clinical trial. Grafix Diabetic Foot Ulcer Study Group. Int Wound J. 2014; 11(5):554-60.
https://doi.org/10.1111/iwj.12329
PMid:25048468 PMCid:PMC7951030
61. Available from: https://zakon.rada.gov.ua/laws/show/z0869-14#n20
62. Shablii VA, Kuchma MD, Kyryk VM, Onishchenko AN, Lukash LL, Lobintseva GS. Cryopreservation human placental tissue as source of hematopoietic and mesenchymal stem cells. Cellular Transplantation & Tissue Engineering. 2012; 7(1).
63. Shablii V, Kuchma M, Kyryk V, Onishchenko G, Tsupykov O, Klymenko P, et al. Сharacteristics of multipotent mesenchymal stromal stem cells derived from native and cryopreserved human placental tissue. Problems of Cryobiology and Cryomedicine. 2012; 22(2):157-160.
64. Walkden A. Amniotic Membrane Transplantation in Ophthalmology: An Updated Perspective. Clinical Ophthalmology. 2020; 14:2057-2072.
https://doi.org/10.2147/OPTH.S208008
PMid:32801614 PMCid:PMC7383023
65. Zelen CM, et al. A prospective randomised comparative parallel study of amniotic membrane wound graft in the management of diabetic foot ulcers. Int Wound J. 2013; 10(5):502-7.
https://doi.org/10.1111/iwj.12097
PMid:23742102 PMCid:PMC4232235
66. Zelen CM, Gould L, Serena TE, et al. A prospective, randomised, controlled, multi-centre comparative effectiveness study of healing using dehydrated human amnion/corion membrane allograft, bioengineered skin substitute or standard of care for treatment of chronic lower extremity diabetic ulcers. Int Wound J. 2015; 12(6):724-32.
https://doi.org/10.1111/iwj.12395
PMid:25424146 PMCid:PMC7950807
67. Zelen CM, Serena TE, Snyder RJ. A prospective, randomised comparative study of weekly versus biweekly application of dehydrated human amnion/chorion membrane allograft in the management of diabetic foot ulcers. Int Wound J. 2014; 11(2):122-8.
https://doi.org/10.1111/iwj.12242
PMid:24618401 PMCid:PMC4235421
68. DiDomenic LA, Orgill DP, Galiano RD, et al. Aseptically processed placental membrane improves healing of diabetic foot ulcerations: prospective, randomized clinical trial. Plast Reconstr Surg Glob Open. 2016; 4(10):e1095.
https://doi.org/10.1097/GOX.0000000000001095
PMid:27826487 PMCid:PMC5096542
69. Snyder RJ, Shimozaki K, Tallis A, et al. A prospective, randomized, multicenter, controlled evaluation of the use of dehydrated amniotic membrane allograft compared to standard of care for the closure of chronic diabetic foot ulcer. Wounds. 2016; 28(3):70-7.
70. Abdo RJ. Treatment of diabetic foot ulcers with dehydrated amniotic membrane allograft: a prospective case series. J Wound Care. 2016; 25(7):S4-9.
https://doi.org/10.12968/jowc.2016.25.7.S4
71. Raphael A. A single-centre, retrospective study of cryopreserved umbilical cord/amniotic membrane tissue for the treatment of diabetic foot ulcers. J Wound Care. 2016; 25(7):S10-7.
https://doi.org/10.12968/jowc.2016.25.7.S10
72. Tettelbach W, et al. A confirmatory study on the efficacy of dehydrated human amnion/chorion membrane dHACM allograft in the management of diabetic foot ulcers: a prospective, multicentre, randomised, controlled study of 110 patients from 14 wound clinics. Int Wound J. 2019; 16(1):19-29.
https://doi.org/10.1111/iwj.12976
PMid:30136445 PMCid:PMC7379535
73. Kirsner RS, Sabolinski ML, Parsons NB, Skornicki M, Marston WA. Comparative effectiveness of a bioengineered living cellular construct vs a dehydrated human amniotic membrane allograft for the treatment of diabetic foot ulcers in a real world setting. Wound Repair Regen. 2015; 23(5):737-44.
https://doi.org/10.1111/wrr.12332
PMid:26100572
74. Koob TJ, Lim JJ, Zabek N, Massee M. Cytokines in single layer amnion allografts compared to multilayer amnion/chorion allografts for wound healing. J Biomed Mater Res B Appl Biomater. 2015; 103(5):1133-404.
https://doi.org/10.1002/jbm.b.33265
PMid:25176107
75. Koizumi NJ, Inatomi TJ, Sotozono CJ, et al. Growth factor mRNA and protein in preserved human amniotic membrane. Curr Eye Res. 2000; 20:173-177.
https://doi.org/10.1076/0271-3683(200003)2031-9FT173
76. Miao Z, Jin J, Chen L, et al. Isolation of mesenchymal stem cells from human placenta: Comparison with human bone marrow mesenchymal stem cells. Cell Biol Int. 2006; 30:681-687.
https://doi.org/10.1016/j.cellbi.2006.03.009
PMid:16870478
77. Maxson S, Lopez EA, Yoo D, Danilkovitch-Miagkova A, Leroux MA. Concise review: role of mesenchymal stem cells in wound repair. Stem Cells Transl Med. 2012; 1:142-14.
https://doi.org/10.5966/sctm.2011-0018
PMid:23197761 PMCid:PMC3659685
78. Shin L, Peterson DA. Human mesenchymal stem cell grafts enhance normal and impaired wound healing by recruiting existing endogenous tissue stem/progenitor cells. Stem Cells Transl Med. 2013; 2:33-42.
https://doi.org/10.5966/sctm.2012-0041
PMid:23283490 PMCid:PMC3659748
79. Makrantonaki E, Wlaschek M, Scharffetter-Kochanek K. Pathogenesis of wound healing disorders in the elderly. JDDG. 2017; 15(3):255-275. Available from: https://doi.org/10.1111/ddg.13199 83.
https://doi.org/10.1111/ddg.13199
80. Niknejad H, Peirovi H, Jorjani M, et al. Properties of the amniotic membrane for potential use in tissue engineering. Eur Cell Mater. 2008; 15:88-99.
https://doi.org/10.22203/eCM.v015a07
PMid:18446690
81. Lakmal K, Basnayake O, Hettiarachchi D. Systematic review on the rational use of amniotic membrane allografts in diabetic foot ulcer treatment. BMC Surg. 2021; 21:87. Available from: https://doi.org/10.1186/s12893-021-01084-8
https://doi.org/10.1186/s12893-021-01084-8
PMid:33588807 PMCid:PMC7885244
82. Brantley J, Verla T. Use of Placental Membranes for the Treatment of Chronic Diabetic Foot Ulcers. Adv Wound Care. 2015; 4(9). DOI: 10.1089/wound.2015.0634
https://doi.org/10.1089/wound.2015.0634
PMid:26339533 PMCid:PMC4529081
83. Au AS, Leung WY, Stavosky JW. Efficacy of Dehydrated Human Amnion Chorion Membrane in the Treatment of Diabetic Foot Ulcers. J Am Podiatr Med Assoc. 2021; 111(2). DOI: 10.7547/17-154
https://doi.org/10.7547/17-154
PMid:33872365
84. Glat P, Orgill D, Galiano R, et al. Placental Membrane Provides Improved Healing Efficacy and Lower Cost Versus a Tissue-Engineered Human Skin in the Treatment of Diabetic Foot Ulcerations. PRS Glob Open. 2019; 7:e2371. DOI: 10.1097/GOX.0000000000002371
https://doi.org/10.1097/GOX.0000000000002371
PMid:31592387 PMCid:PMC6756673
85. Available from: https://www.wellrx.com/prescriptions/epifix%20amniotic%20membrane
86. Skin Substitutes for Treating Chronic Wounds. Technical Brief Project ID: WNDT0818, 2020. https://www.cms.gov/Medicare/Coverage/DeterminationProcess/downloads/id109TA.pdf
87. Boboridis KG, Mikropoulos DG, Georgiadis NS. Hypopyon after Primary Cryopreserved Amniotic Membrane Transplantation for Sterile Corneal Ulceration: A Case Report and Review of the Literature. Case Rep Ophthalmol Med. 2021; 2021: 9982354. DOI: 10.1155/2021/9982354
https://doi.org/10.1155/2021/9982354
PMid:34221527 PMCid:PMC8219464
88. Kubo M, Sonoda Y, Muramatsu R, Usui M. Immunogenicity of human amniotic membrane in experimental xenotransplantation. Invest Ophthalmol Vis Sci. 2001; 42:1539-1546.
89. Risman BV, Ivanov GG, Mustakimov DN. The treatment results of patients with purulent-necrotic complications of diabetic foot syndrome by using of modern wound coverings based on alginates, hydrocolloids and hydrogels (Wound coverings and diabetic foot syndrome). Wounds and Wound Infections. The Prof. B. M. Kostyuchenok Journal. 2017; 4(2): 18-23. [In Russian] https://doi.org/10.17650/2408-9613-2017-4-2-18-23

Ustymenko A, Nemtinov P, Bolgarska S, Zaika L, Shablii V, Bukreieva T, Orlenko V, Palіanytsia S. The clinical effectiveness of cryopreserved human amniotic membrane in diabetic foot syndrome. Cell Organ Transpl. 2021; 9(2):80-87. Available from: https://doi.org/10.22494/cot.v9i2.129

Creative Commons License
This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License.