Bioengineered sites for islet cell transplantation

Current Diabetes Reports

Volumn 13, Issue 5, 2013, Pages 745-755

  Vériter, Sophie ^a   Gianello, Pierre ^b   Dufrane, Denis ^a  

^a CLINIQUES UNIVERSITAIRES SAINT LUC   (Belgium)

^b UNIVERSITÉ CATHOLIQUE DE LOUVAIN   (Belgium)

Author keywords

Bioengineered sites; Encapsulation; Implantation site; Islet cell transplantation

Indexed keywords

GLUCOSE;

ANGIOGENESIS; ARTICLE; BIOENGINEERING; CELL ENCAPSULATION; GLUCOSE BLOOD LEVEL; HEPATIC DUCT; HUMAN; INSULIN DEPENDENT DIABETES MELLITUS; KIDNEY CAPSULE; NONHUMAN; OXYGEN SUPPLY; OXYGENATION; PANCREAS; PANCREAS ISLET CELL; PANCREAS ISLET TRANSPLANTATION; PERITONEUM; PORTAL VEIN; SKELETAL MUSCLE; SPLEEN; STOMACH MUCOSA;

ANIMALS; BIOENGINEERING; CELLS, IMMOBILIZED; CLINICAL TRIALS AS TOPIC; HUMANS; IMPLANTS, EXPERIMENTAL; ISLETS OF LANGERHANS; ISLETS OF LANGERHANS TRANSPLANTATION;

EID: 84884589456     PISSN: 15344827     EISSN: 15390829     Source Type: Journal    
DOI: 10.1007/s11892-013-0412-x     Document Type: Article

References (99)

1. Shapiro AMJ, Ricordi C, Hering BJ, Auchincloss H, Lindblad R, Robertson RP, et al. International trial of the Edmonton protocol for islet transplantation. N Engl J Med. 2006;355:1318-30.
2. • Berney T, Ferrari-Lacraz S, Bühler L, Oberholzer J, Marangon N, Philippe J, et al. Long-term insulin-independence after allogeneic islet transplantation for type 1 diabetes: over the 10-year mark. Am J Transplant Off J Am Soc Transplant Am Soc Transpl Surg. 2009;9:419-23. This study relates for the first time the capacity of islet transplantation to cure type 1 diabetes with a long-term follow-up of more than 10 years.
3. Carlsson PO, Palm F, Andersson A, Liss P. Markedly decreased oxygen tension in transplanted rat pancreatic islets irrespective of the implantation site. Diabetes. 2001;50:489-95.
4. Robertson RP. Islet transplantation as a treatment for diabetes - a work in progress. N Engl J Med. 2004;350:694-705.
5. Ryan EA, Paty BW, Senior PA, Bigam D, Alfadhli E, Kneteman NM, et al. Five-year follow-up after clinical islet transplantation. Diabetes. 2005;54:2060-9.
6. Sutherland DE, Gores PF, Hering BJ, Wahoff D, McKeehen DA, Gruessner RW. Islet transplantation: an update. Diabetes Metab Rev. 1996;12:137-50.
7. Markmann JF, Rosen M, Siegelman ES, Soulen MC, Deng S, Barker CF, et al. Magnetic resonance-defined periportal steatosis following intraportal islet transplantation: a functional footprint of islet graft survival? Diabetes. 2003;52:1591-4.
8. Lau J, Mattsson G, Carlsson C, Nyqvist D, Köhler M, Berggren P-O, et al. Implantation site-dependent dysfunction of transplanted pancreatic islets. Diabetes. 2007;56:1544-50.
9. • Lau J, Kampf C, Mattsson G, Nyqvist D, Köhler M, Berggren P-O, et al. Beneficial role of pancreatic microenvironment for angiogenesis in transplanted pancreatic islets. Cell Transplant. 2009;18:23-30. This work demonstrated the importance of host vasculature development in islets after transplantation with a view to selecting the most appropriate implantation site.
10. Stagner JI, Rilo HL, White KK. The pancreas as an islet transplantation site. Confirmation in a syngeneic rodent and canine autotransplant model. Jop J Pancreas. 2007;8:628-36.
11. Hayek A, Beattie GM. Intrapancreatic islet transplantation in experimental diabetes in the rat. Metabolism. 1992;41:1367-9.
12. Rilo HL, Fontes PA, Nussler AK, Demetris AJ, Carroll PB, Ildstad ST, et al. Intrapancreatic islet transplantation as a potential solution to chronic failure of intraportal islet grafts. Transplant Proc. 1993;25:988.
13. De Carlo E, Baiguera S, Conconi MT, Vigolo S, Grandi C, Lora S, et al. Pancreatic acellular matrix supports islet survival and function in a synthetic tubular device: in vitro and in vivo studies. Int J Mol Med. 2010;25:195-202.
14. Mirmalek-Sani S-H, Orlando G, McQuilling JP, Pareta R, Mack DL, Salvatori M, et al. Porcine pancreas extracellular matrix as a platform for endocrine pancreas bioengineering. Biomaterials. 2013;34:5488-95.
15. Finch DR, Wise PH, Morris PJ. Successful intra-splenic transplantation of syngeneic and allogeneic isolated pancreatic islets. Diabetologia. 1977;13:195-9.
16. Warnock GL, Dabbs KD, Evans MG, Cattral MS, Kneteman NM, Rajotte RV. Critical mass of islets that function after implantation in a large mammalian. Horm Metab Res Suppl Ser. 1990;25:156-61.
17. Ao Z, Matayoshi K, Lakey JR, Rajotte RV, Warnock GL. Survival and function of purified islets in the omental pouch site of outbred dogs. Transplantation. 1993;56:524-9.
18. Gustavson SM, Rajotte RV, Hunkeler D, Lakey JRT, Edgerton DS, Neal DW, et al. Islet auto-transplantation into an omental or splenic site results in a normal beta cell but abnormal alpha cell response to mild non-insulin-induced hypoglycemia. Am J Transplant Off J Am Soc Transplant Am Soc Transpl Surg. 2005;5:2368-77.
19. Hecht G, Eventov-Friedman S, Rosen C, Shezen E, Tchorsh D, Aronovich A, et al. Embryonic pig pancreatic tissue for the treatment of diabetes in a nonhuman primate model. Proc Natl Acad Sci U S A. 2009;106:8659-64.
20. Caiazzo R, Gmyr V, Hubert T, Delalleau N, Lamberts R, Moerman E, et al. Evaluation of alternative sites for islet transplantation in the minipig: interest and limits of the gastric submucosa. Transplant Proc. 2007;39:2620-3.
21. • Echeverri GJ, McGrath K, Bottino R, Hara H, Dons EM, van der Windt DJ, et al. Endoscopic gastric submucosal transplantation of islets (ENDO-STI): technique and initial results in diabetic pigs. Am J Transplant Off J Am Soc Transplant Am Soc Transpl Surg. 2009;9:2485-96. This preclinical experimental study demonstrated the potential of a minimal invasive procedure for transplanting islets into the gastric submucosal.
22. Wszola M, Berman A, Fabisiak M, Domagala P, Zmudzka M, Kieszek R, et al. TransEndoscopic Gastric SubMucosa Islet Transplantation (eGSM-ITx) in pigs with streptozotocine induced diabetes - technical aspects of the procedure - preliminary report. Ann Transplant Q Pol Transplant Soc. 2009;14:45-50.
23. Kakabadze Z, Gupta S, Brandhorst D, Korsgren O, Berishvili E. Long-term engraftment and function of transplanted pancreatic islets in vascularized segments of small intestine. Transpl Int Off J Eur Soc Organ Transplant. 2011;24:175-83.
24. Gray DW. Islet transplantation and glucose regulation. World J Surg. 2001;25:497-502.
25. Mellgren A, Schnell Landström AH, Petersson B, Andersson A. The renal subcapsular site offers better growth conditions for transplanted mouse pancreatic islet cells than the liver or spleen. Diabetologia. 1986;29:670-2.
26. Hiller WF, Klempnauer J, Lück R, Steiniger B. Progressive deterioration of endocrine function after intraportal but not kidney subcapsular rat islet transplantation. Diabetes. 1991;40:134-40.
27. Kim H-I, Yu JE, Park C-G, Kim S-J. Comparison of four pancreatic islet implantation sites. J Korean Med Sci. 2010;25:203-10.
28. • Rajab A, Buss J, Diakoff E, Hadley GA, Osei K, Ferguson RM. Comparison of the portal vein and kidney subcapsule as sites for primate islet autotransplantation. Cell Transplant. 2008;17:1015-23. This experimental study demonstrated the superiority of the portal vein for islet transplantation, in comparison with the kidney subcapsule, in terms of blood glucose control.
29. • Svensson J, Lau J, Sandberg M, Carlsson P-O. High vascular density and oxygenation of pancreatic islets transplanted in clusters into striated muscle. Cell Transplant. 2011;20:783-8. The work demonstrated that the intramuscular site provides excellent conditions for vascular engraftment after islet transplantation.
30. Carlsson PO, Palm F, Andersson A, Liss P. Chronically decreased oxygen tension in rat pancreatic islets transplanted under the kidney capsule. Transplantation. 2000;69:761-6.
31. Weber CJ, Hardy MA, Pi-Sunyer F, Zimmerman E, Reemtsma K. Tissue culture preservation and intramuscular transplantation of pancreatic islets. Surgery. 1978;84:166-74.
32. Rafael E, Tibell A, Rydén M, Lundgren T, Sävendahl L, Borgström B, et al. Intramuscular autotransplantation of pancreatic islets in a 7-year-old child: a 2-year follow-up. Am J Transplant Off J Am Soc Transplant Am Soc Transpl Surg. 2008;8:458-62.
33. • Pattou F, Kerr-Conte J, Wild D. GLP-1-receptor scanning for imaging of human beta cells transplanted in muscle. N Engl J Med. 2010;363:1289-90. This clinical study demonstrated for the first time the concept of intramuscular transplantation of islets in the case of autograft.
34. • Christoffersson G, Henriksnäs J, Johansson L, Rolny C, Ahlström H, Caballero-Corbalan J, et al. Clinical and experimental pancreatic islet transplantation to striated muscle: establishment of a vascular system similar to that in native islets. Diabetes. 2010;59:2569-78. This study postulated that recruited neutrophils are crucial for the functionally restored intra-islet blood perfusion following transplantation to striated muscle under experimental and clinical situations.
35. Lund T, Korsgren O, Aursnes IA, Scholz H, Foss A. Sustained reversal of diabetes following islet transplantation to striated musculature in the rat. J Surg Res. 2010;160:145-54.
36. Cantarelli E, Melzi R, Mercalli A, Sordi V, Ferrari G, Lederer CW, et al. Bone marrow as an alternative site for islet transplantation. Blood. 2009;114:4566-74.
37. Rayat GR, Korbutt GS, Elliott JF, Rajotte RV. Survival and function of syngeneic rat islet grafts placed within the thymus versus under the kidney capsule. Cell Transplant. 1997;6:597-602.
38. Tze WJ, Tai J. Immunological studies in diabetic rat recipients with a pancreatic islet cell allograft in the brain. Transplantation. 1989;47:1053-7.
39. Xin Z-L, Ge S-L, Wu X-K, Jia Y-J, Hu H-T. Intracerebral xenotransplantation of semipermeable membrane- encapsuled pancreatic islets. World J Gastroenterol. 2005;11:5714-7.
40. Selawry HP, Whittington KB, Bellgrau D. Abdominal intratesticular islet-xenograft survival in rats. Diabetes. 1989;38 Suppl 1:220-3.
41. Perez VL, Caicedo A, Berman DM, Arrieta E, Abdulreda MH, Rodriguez-Diaz R, et al. The anterior chamber of the eye as a clinical transplantation site for the treatment of diabetes: a study in a baboon model of diabetes. Diabetologia. 2011;54:1121-6.
42. Beck J, Angus R, Madsen B, Britt D, Vernon B, Nguyen KT. Islet encapsulation: strategies to enhance islet cell functions. Tissue Eng. 2007;13:589-99.
43. Brauker JH, Carr-Brendel VE, Martinson LA, Crudele J, Johnston WD, Johnson RC. Neovascularization of synthetic membranes directed by membrane microarchitecture. J Biomed Mater Res. 1995;29:1517-24.
44. Sörenby AK, Wu GS, Zhu S, Wernerson AM, Sumitran-Holgersson S, Tibell ABH. Macroencapsulation protects against sensitization after allogeneic islet transplantation in rats. Transplantation. 2006;82:393-7.
45. Sweet IR, Yanay O, Waldron L, Gilbert M, Fuller JM, Tupling T, et al. Treatment of diabetic rats with encapsulated islets. J Cell Mol Med. 2008;12:2644-50.
46. Tibell A, Rafael E, Wennberg L, Nordenström J, Bergström M, Geller RL, et al. Survival of macroencapsulated allogeneic parathyroid tissue one year after transplantation in nonimmunosuppressed humans. Cell Transplant. 2001;10:591-9.
47. Lim F, Sun AM. Microencapsulated islets as bioartificial endocrine pancreas. Science. 1980;210:908-10.
48. Calafiore R, Basta G, Luca G, Boselli C, Bufalari A, Bufalari A, et al. Transplantation of pancreatic islets contained in minimal volume microcapsules in diabetic high mammalians. Ann N Y Acad Sci. 1999;875:219-32.
49. • Teramura Y, Iwata H. Bioartificial pancreas microencapsulation and conformal coating of islet of Langerhans. Adv Drug Deliv Rev. 2010;62:827-40. This article relates the concept of conformal coating for islet transplantation with a view to minimizing encapsulation size and promoting transplantation into the liver.
50. Lee DY, Lee S, Nam JH, Byun Y. Minimization of immunosuppressive therapy after islet transplantation: combined action of heme oxygenase-1 and PEGylation to islet. Am J Transplant Off J Am Soc Transplant Am Soc Transpl Surg. 2006;6:1820-8.
51. Miura S, Teramura Y, Iwata H. Encapsulation of islets with ultra-thin polyion complex membrane through poly(ethylene glycol)-phospholipids anchored to cell membrane. Biomaterials. 2006;27:5828-35.
52. Teramura Y, Iwata H. Surface modification of islets with PEG-lipid for improvement of graft survival in intraportal transplantation. Transplantation. 2009;88:624-30.
53. Totani T, Teramura Y, Iwata H. Immobilization of urokinase on the islet surface by amphiphilic poly(vinyl alcohol) that carries alkyl side chains. Biomaterials. 2008;29:2878-83.
54. Cabric S, Sanchez J, Lundgren T, Foss A, Felldin M, Källen R, et al. Islet surface heparinization prevents the instant blood-mediated inflammatory reaction in islet transplantation. Diabetes. 2007;56:2008-15.
55. Stabler CL, Sun X-L, Cui W, Wilson JT, Haller CA, Chaikof EL. Surface re-engineering of pancreatic islets with recombinant azido-thrombomodulin. Bioconjug Chem. 2007;18:1713-5.
56. Teramura Y, Iwata H. Islet encapsulation with living cells for improvement of biocompatibility. Biomaterials. 2009;30:2270-5.
57. Cruise GM, Hegre OD, Lamberti FV, Hager SR, Hill R, Scharp DS, et al. In vitro and in vivo performance of porcine islets encapsulated in interfacially photopolymerized poly(ethylene glycol) diacrylate membranes. Cell Transplant. 1999;8:293-306.
58. • Basta G, Montanucci P, Luca G, Boselli C, Noya G, Barbaro B, et al. Long-term metabolic and immunological follow-up of nonimmunosuppressed patients with type 1 diabetes treated with microencapsulated islet allografts: four cases. Diabetes Care. 2011;34:2406-9. This clinical work relates a long-term metabolic control in type 1 diabetes after microencapsulated islet transplantation into the peritoneal cavity.
59. Elliott RB, Escobar L, Tan PLJ, Muzina M, Zwain S, Buchanan C. Live encapsulated porcine islets from a type 1 diabetic patient 9.5 yr after xenotransplantation. Xenotransplantation. 2007;14:157-61.
60. • Tuch BE, Keogh GW, Williams LJ, Wu W, Foster JL, Vaithilingam V, et al. Safety and viability of microencapsulated human islets transplanted into diabetic humans. Diabetes Care. 2009;32:1887-9. This clinical work relates the safety of microencapsulated islet transplantation into the peritoneal cavity.
61. Elliott RB, Escobar L, Tan PLJ, Garkavenko O, Calafiore R, Basta P, et al. Intraperitoneal alginate-encapsulated neonatal porcine islets in a placebo-controlled study with 16 diabetic cynomolgus primates. Transplant Proc. 2005;37:3505-8.
62. Soon-Shiong P, Feldman E, Nelson R, Heintz R, Yao Q, Yao Z, et al. Long-term reversal of diabetes by the injection of immunoprotected islets. Proc Natl Acad Sci U S A. 1993;90:5843-7.
63. Sun Y, Ma X, Zhou D, Vacek I, Sun AM. Normalization of diabetes in spontaneously diabetic cynomologus monkeys by xenografts of microencapsulated porcine islets without immunosuppression. J Clin Invest. 1996;98:1417-22.
64. Wang W, Gu Y, Tabata Y, Miyamoto M, Hori H, Nagata N, et al. Reversal of diabetes in mice by xenotransplantation of a bioartificial pancreas in a prevascularized subcutaneous site. Transplantation. 2002;73:122-9.
65. Soon-Shiong P, Heintz RE, Merideth N, Yao QX, Yao Z, Zheng T, et al. Insulin independence in a type 1 diabetic patient after encapsulated islet transplantation. Lancet. 1994;343:950-1.
66. Calafiore R, Basta G, Luca G, Lemmi A, Montanucci MP, Calabrese G, et al. Microencapsulated pancreatic islet allografts into nonimmunosuppressed patients with type 1 diabetes: first two cases. Diabetes Care. 2006;29:137-8.
67. Berman DM, O'Neil JJ, Coffey LCK, Chaffanjon PCJ, Kenyon NM, Ruiz Jr P, et al. Long-term survival of nonhuman primate islets implanted in an omental pouch on a biodegradable scaffold. Am J Transplant Off J Am Soc Transplant Am Soc Transpl Surg. 2009;9:91-104.
68. Sawyer RG, Spengler MD, Adams RB, Pruett TL. The peritoneal environment during infection. The effect of monomicrobial and polymicrobial bacteria on pO2 and pH. Ann Surg. 1991;213:253-60.
69. Figliuzzi M, Cornolti R, Plati T, Rajan N, Adobati F, Remuzzi G, et al. Subcutaneous xenotransplantation of bovine pancreatic islets. Biomaterials. 2005;26:5640-7.
70. Tatarkiewicz K, Hollister-Lock J, Quickel RR, Colton CK, Bonner-Weir S, Weir GC. Reversal of hyperglycemia in mice after subcutaneous transplantation of macroencapsulated islets. Transplantation. 1999;67:665-71.
71. Yang Z, Chen M, Fialkow LB, Ellett JD, Wu R, Nadler JL. Survival of pancreatic islet xenografts in NOD mice with the theracyte device. Transplant Proc. 2002;34:3349-50.
72. Dufrane D, van Steenberghe M, Goebbels R-M, Saliez A, Guiot Y, Gianello P. The influence of implantation site on the biocompatibility and survival of alginate encapsulated pig islets in rats. Biomaterials. 2006;27:3201-8.
73. • Dufrane D, Goebbels R-M, Gianello P. Alginate macroencapsulation of pig islets allows correction of streptozotocin-induced diabetes in primates up to 6 months without immunosuppression. Transplantation. 2010;90:1054-62. This preclinical work demonstrated that xenorejection can be overcome by the transplantation of macroencapsulated pig islets in the subcutaneous tissue of diabetic primates without any immunosuppression.
74. • Vériter S, Gianello P, Igarashi Y, Beaurin G, Ghyselinck A, Aouassar N, et al. Improvement of subcutaneous bioartificial pancreas vascularization and function by co-encapsulation of pig islets and mesenchymal stem cells in primates. Cell Transplant. 2013; This experimental work demonstrated that the in vivo function of macroencapsulated pig islets can be improved by the use of adipose mesenchymal stem cells with a view to promoting angiogenesis in the subcutaneous tissue.
75. Vériter S, Aouassar N, Adnet P-Y, Paridaens M-S, Stuckman C, Jordan B, et al. The impact of hyperglycemia and the presence of encapsulated islets on oxygenation within a bioartificial pancreas in the presence of mesenchymal stem cells in a diabetic Wistar rat model. Biomaterials. 2011;32:5945-56.
76. Rafael E, Wu GS, Hultenby K, Tibell A, Wernerson A. Improved survival of macroencapsulated islets of Langerhans by preimplantation of the immunoisolating device: a morphometric study. Cell Transplant. 2003;12:407-12.
77. Sörenby AK, Kumagai-Braesch M, Sharma A, Hultenby KR, Wernerson AM, Tibell AB. Preimplantation of an immunoprotective device can lower the curative dose of islets to that of free islet transplantation: studies in a rodent model. Transplantation. 2008;86:364-6.
78. Valdés-González RA, Dorantes LM, Garibay GN, Bracho-Blanchet E, Mendez AJ, Dávila-Pérez R, et al. Xenotransplantation of porcine neonatal islets of Langerhans and Sertoli cells: a 4-year study. Eur J Endocrinol Eur Fed Endocr Soc. 2005;153:419-27.
79. Valdés-González RA, White DJG, Dorantes LM, Terán L, Garibay-Nieto GN, Bracho-Blanchet E, et al. Three-yr follow-up of a type 1 diabetes mellitus patient with an islet xenotransplant. Clin Transplant. 2007;21:352-7.
80. • Valdes-Gonzalez R, Rodriguez-Ventura AL, White DJG, Bracho-Blanchet E, Castillo A, Ramírez-González B, et al. Long-term follow-up of patients with type 1 diabetes transplanted with neonatal pig islets. Clin Exp Immunol. 2010;162:537-42. This clinical work demonstrated for the first time that encapsulated pig islets can control diabetes without any side effects after transplantation in patients.
81. Bloch K, Papismedov E, Yavriyants K, Vorobeychik M, Beer S, Vardi P. Photosynthetic oxygen generator for bioartificial pancreas. Tissue Eng. 2006;12:337-44.
82. Brandhorst H, Muehling B, Yamaya H, Henriksnaes J, Carlsson PO, Korsgren O, et al. New class of oxygen carriers improves islet isolation from long-term stored rat pancreata. Transplant Proc. 2008;40:393-4.
83. Maillard E, Sanchez-Dominguez M, Kleiss C, Langlois A, Sencier MC, Vodouhe C, et al. Perfluorocarbons: new tool for islets preservation in vitro. Transplant Proc. 2008;40:372-4.
84. Sakai T, Li S, Tanioka Y, Goto T, Tanaka T, Matsumoto I, et al. Intraperitoneal injection of oxygenated perfluorochemical improves the outcome of intraportal islet transplantation in a rat model. Transplant Proc. 2006;38:3289-92.
85. Fenge C, Klein C, Heuer C, Siegel U, Fraune E. Agitation, aeration and perfusion modules for cell culture bioreactors. Cytotechnology. 1993;11:233-44.
86. Emery AN, Jan DC, al-Rubeai M. Oxygenation of intensive cell-culture system. Appl Microbiol Biotechnol. 1995;43:1028-33.
87. De Bartolo L, Jarosch-Von Schweder G, Haverich A, Bader A. A novel full-scale flat membrane bioreactor utilizing porcine hepatocytes: cell viability and tissue-specific functions. Biotechnol Prog. 2000;16:102-8.
88. Tilles AW, Baskaran H, Roy P, Yarmush ML, Toner M. Effects of oxygenation and flow on the viability and function of rat hepatocytes cocultured in a microchannel flat-plate bioreactor. Biotechnol Bioeng. 2001;73:379-89.
89. Halban PA, Wollheim CB, Blondel B, Meda P, Niesor EN, Mintz DH. The possible importance of contact between pancreatic islet cells for the control of insulin release. Endocrinology. 1982;111:86-94.
90. Halban PA, Powers SL, George KL, Bonner-Weir S. Spontaneous reassociation of dispersed adult rat pancreatic islet cells into aggregates with three-dimensional architecture typical of native islets. Diabetes. 1987;36:783-90.
91. O'Sullivan ES, Johnson AS, Omer A, Hollister-Lock J, Bonner-Weir S, Colton CK, et al. Rat islet cell aggregates are superior to islets for transplantation in microcapsules. Diabetologia. 2010;53:937-45.
92. Cheng Y, Liu Y-F, Zhang J-L, Li T-M, Zhao N. Elevation of vascular endothelial growth factor production and its effect on revascularization and function of graft islets in diabetic rats. World J Gastroenterol. 2007;13:2862-6.
93. McQuilling JP, Arenas-Herrera J, Childers C, Pareta RA, Khanna O, Jiang B, et al. New alginate microcapsule system for angiogenic protein delivery and immunoisolation of islets for transplantation in the rat omentum pouch. Transplant Proc. 2011;43:3262-4.
94. Wright Jr JR, Yang H, Dooley KC. Tilapia-a source of hypoxia-resistant islet cells for encapsulation. Cell Transplant. 1998;7:299-307.
95. Barkai U, Weir GC, Colton CK, Ludwig B, Bornstein SR, Brendel MD, et al. Enhanced oxygen supply improves islet viability in a new bioartificial pancreas. Cell Transplant. 2012.
96. Ludwig B, Zimerman B, Steffen A, Yavriants K, Azarov D, Reichel A, et al. A novel device for islet transplantation providing immune protection and oxygen supply. Horm Metab Res Horm- Stoffwechselforschung Horm Métabolisme. 2010;42:918-22.
97. Ito T, Itakura S, Todorov I, Rawson J, Asari S, Shintaku J, et al. Mesenchymal stem cell and islet co-transplantation promotes graft revascularization and function. Transplantation. 2010;89:1438-45.
98. Park K-S, Kim Y-S, Kim J-H, Choi B, Kim S-H, Tan AH-K, et al. Trophic molecules derived from human mesenchymal stem cells enhance survival, function, and angiogenesis of isolated islets after transplantation. Transplantation. 2010;89:509-17.
99. Sakata N, Chan NK, Chrisler J, Obenaus A, Hathout E. Bone marrow cell cotransplantation with islets improves their vascularization and function. Transplantation. 2010;89:686-93.