Strategy for clinical setting in intramuscular and subcutaneous islet transplantation

Intraportal islet transplantation has a long history as a procedure for clinical islet transplantation. However, many recent studies revealed that the intraportal procedure has some disadvantages in transplant efficiency and safety. Many candidates as an optimal transplant site for islets have been assessed, but further studies and clinical trials are still necessary. Intramuscular and subcutaneous spaces are important candidates, because the transplant and biopsy procedures are simple approaches with minimal invasion and few complications. Although they are sites with hypovascularity and hypoxia, which contribute to the poor transplant efficiency, many experimental trials for improving the outcome in intramuscular and subcutaneous islet transplantations have been performed, focusing on early angiogenesis and scaffolds for engrafting transplanted islets. We review current progress in intramuscular and subcutaneous islet transplantations and discuss ways to develop them as optimal transplant sites for islets. Copyright © 2013 John Wiley & Sons, Ltd.

[1]  G. Opdenakker,et al.  VEGF-A recruits a proangiogenic MMP-9-delivering neutrophil subset that induces angiogenesis in transplanted hypoxic tissue. , 2012, Blood.

[2]  Kwangmeyung Kim,et al.  In situ application of hydrogel-type fibrin-islet composite optimized for rapid glycemic control by subcutaneous xenogeneic porcine islet transplantation. , 2012, Journal of controlled release : official journal of the Controlled Release Society.

[3]  S. Truant,et al.  Laparoscopic spleen-preserving distal pancreatectomy followed by intramuscular autologous islet transplantation for traumatic pancreatic transection in a young adult. , 2012, JOP : Journal of the pancreas.

[4]  A. M. Shapiro,et al.  A comparison of islet autotransplantation with allotransplantation and factors elevating acute portal pressure in clinical islet transplantation , 2012, Journal of hepato-biliary-pancreatic sciences.

[5]  F. Gao,et al.  Percutaneous transhepatic portal catheterization guided by ultrasound technology for islet transplantation in rhesus monkey. , 2012, Hepatobiliary & pancreatic diseases international : HBPD INT.

[6]  Peter M. Jones,et al.  Immunoisolation of islets in high guluronic acid barium-alginate microcapsules does not improve graft outcome at the subcutaneous site. , 2012, Artificial organs.

[7]  M. Unno,et al.  Utility of co-transplanting mesenchymal stem cells in islet transplantation. , 2011, World journal of gastroenterology.

[8]  T. Okano,et al.  Reversal of Diabetes by the Creation of Neo-Islet Tissues Into a Subcutaneous Site Using Islet Cell Sheets , 2011, Transplantation.

[9]  P. Carlsson,et al.  Striated Muscle as Implantation Site for Transplanted Pancreatic Islets , 2011, Journal of transplantation.

[10]  N. Kneteman,et al.  Portal Vein Thrombosis Is a Potentially Preventable Complication in Clinical Islet Transplantation , 2011, American journal of transplantation : official journal of the American Society of Transplantation and the American Society of Transplant Surgeons.

[11]  G. Korbutt,et al.  Vascularization of collagen-chitosan scaffolds with circulating progenitor cells as potential site for islet transplantation. , 2011, Journal of controlled release : official journal of the Controlled Release Society.

[12]  D. Jirák,et al.  Dynamic contrast-enhanced magnetic resonance imaging as a tool to monitor the blood supply to an artificial cavity used as a site for islet transplantation in rats. , 2011, Transplantation proceedings.

[13]  J. Lakey,et al.  Function and viability of human islets encapsulated in alginate sheets: in vitro and in vivo culture. , 2011, Transplantation proceedings.

[14]  Bernard Gallez,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. , 2011, Biomaterials.

[15]  M. Unno,et al.  Monitoring transplanted islets by high-frequency ultrasound , 2011, Islets.

[16]  M. Sandberg,et al.  High Vascular Density and Oxygenation of Pancreatic Islets Transplanted in Clusters into Striated Muscle , 2011, Cell transplantation.

[17]  J. Rawson,et al.  Liver Natural Killer Cells Play a Role in the Destruction of Islets After Intraportal Transplantation , 2011, Transplantation.

[18]  P. Carlsson,et al.  Intramuscular islet transplantation promotes restored islet vascularity , 2011, Islets.

[19]  Denis Dufrane,et al.  Alginate Macroencapsulation of Pig Islets Allows Correction of Streptozotocin-Induced Diabetes in Primates up to 6 Months Without Immunosuppression , 2010, Transplantation.

[20]  T. Mohanakumar,et al.  Cooperative Signaling for Angiogenesis and Neovascularization by VEGF and HGF Following Islet Transplantation , 2010, Transplantation.

[21]  F. Lin,et al.  Intramedullary cavity as implantation site for bioartifical pancreas: preliminary in vivo study. , 2010, Transplantation proceedings.

[22]  A. Rajab Islet Transplantation: Alternative Sites , 2010, Current diabetes reports.

[23]  D. Jirák,et al.  Vascularization of artificial beds for pancreatic islet transplantation in a rat model. , 2010, Transplantation proceedings.

[24]  O. Korsgren,et al.  Sustained reversal of diabetes following islet transplantation to striated musculature in the rat. , 2010, The Journal of surgical research.

[25]  J. Larsen,et al.  Hyperglycemia induced by tacrolimus and sirolimus is reversible in normal sprague–dawley rats , 2010, Endocrine.

[26]  Kai-Chiang Yang,et al.  Comparison of bioartificial pancreas performance in the bone marrow cavity and intramuscular space. , 2010, Archives of medical research.

[27]  Nathaniel K. Chan,et al.  Bone Marrow Cell Cotransplantation With Islets Improves Their Vascularization and Function , 2010, Transplantation.

[28]  Nathaniel K. Chan,et al.  Bone marrow cells produce nerve growth factor and promote angiogenesis around transplanted islets. , 2010, World journal of gastroenterology.

[29]  Syed A. Ahmad,et al.  Management of Acute Post-operative Portal Venous Thrombosis , 2010, Journal of Gastrointestinal Surgery.

[30]  Govind Bhagat,et al.  Islet Grafting and Imaging in a Bioengineered Intramuscular Space , 2009, Transplantation.

[31]  T. Okano,et al.  Bioengineering of a functional sheet of islet cells for the treatment of diabetes mellitus. , 2009, Biomaterials.

[32]  A. Moore,et al.  In Vivo Imaging of Autologous Islet Grafts in the Liver and Under the Kidney Capsule in Non-Human Primates , 2009, Transplantation.

[33]  Nathaniel K. Chan,et al.  MRI Assessment of Ischemic Liver After Intraportal Islet Transplantation , 2009, Transplantation.

[34]  Yoshiki Sawa,et al.  Creation of a rich subcutaneous vascular network with implanted adipose tissue-derived stromal cells and adipose tissue enhances subcutaneous grafting of islets in diabetic mice. , 2009, Tissue engineering. Part C, Methods.

[35]  Á. Meana,et al.  Plasma-fibroblast gel as scaffold for islet transplantation. , 2009, Tissue engineering. Part A.

[36]  Hyoung-il Kim,et al.  Comparison of Four Pancreatic Islet Implantation Sites , 2009, Journal of Korean medical science.

[37]  Yiling Fu,et al.  Selective rejection of porcine islet xenografts by macrophages , 2008, Xenotransplantation.

[38]  L. Benítez-Bribiesca,et al.  Pancreatic islet transplantation into the bone marrow of the rat. , 2008, American journal of surgery.

[39]  J. Permert,et al.  Intramuscular Autotransplantation of Pancreatic Islets in a 7‐Year‐Old Child: A 2‐Year Follow‐Up , 2008, American journal of transplantation : official journal of the American Society of Transplantation and the American Society of Transplant Surgeons.

[40]  C. Ricordi,et al.  Reversal of Diabetes by Pancreatic Islet Transplantation into a Subcutaneous, Neovascularized Device , 2006, Transplantation.

[41]  E. Ryan,et al.  Prevention of Bleeding After Islet Transplantation: Lessons Learned from a Multivariate Analysis of 132 Cases at a Single Institution , 2005, American journal of transplantation : official journal of the American Society of Transplantation and the American Society of Transplant Surgeons.

[42]  C. Paties,et al.  Minimal Focal Steatosis of Liver after Islet Transplantation in Humans: A Long-Term Study , 2005, Cell transplantation.

[43]  J. Juang,et al.  Islet transplantation at subcutaneous and intramuscular sites. , 2005, Transplantation proceedings.

[44]  Andrea Remuzzi,et al.  Subcutaneous xenotransplantation of bovine pancreatic islets. , 2005, Biomaterials.

[45]  A. Bharat,et al.  Novel in vivo murine model to study islet potency: engraftment and function. , 2005, Transplantation.

[46]  K. Ekdahl,et al.  Tissue factor produced by the endocrine cells of the islets of Langerhans is associated with a negative outcome of clinical islet transplantation. , 2005 .

[47]  K. Lalić,et al.  Human fetal islet transplantation in type 1 diabetic patients: comparison of metabolic effects between single and multiple implantation regimens. , 2004, Transplantation proceedings.

[48]  B. Wolf,et al.  Elevated portal vein drug levels of sirolimus and tacrolimus in islet transplant recipients: local immunosuppression or islet toxicity? , 2003, Transplantation.

[49]  C. Berne,et al.  Nicotinamide inhibits tissue factor expression in isolated human pancreatic islets: implications for clinical islet transplantation1 , 2003, Transplantation.

[50]  Y. Tabata,et al.  The Development of New Immunoisolatory Devices Possessing the Ability to Induce Neovascularization , 2003, Cell transplantation.

[51]  Y. Tabata,et al.  Bioartificial Pancreas Transplantation at Prevascularized Intermuscular Space: Effect of Angiogenesis Induction on Islet Survival , 2003, Pancreas.

[52]  Tatsuya Kin,et al.  Survival and Metabolic Function of Syngeneic Rat Islet Grafts Transplanted in the Omental Pouch , 2003, American journal of transplantation : official journal of the American Society of Transplantation and the American Society of Transplant Surgeons.

[53]  M. Menger,et al.  Heat shock preconditioning impairs revascularization of freely transplanted pancreatic islets1 , 2002, Transplantation.

[54]  A. Shapiro,et al.  Successful islet transplantation: continued insulin reserve provides long-term glycemic control. , 2002, Diabetes.

[55]  Yasuhiko Tabata,et al.  Reversal of diabetes in mice by xenotransplantation of a bioartificial pancreas in a prevascularized subcutaneous site. , 2002, Transplantation.

[56]  A. Balamurugan,et al.  Successful Subcutaneous Pancreatic Islet Transplantation Using an Angiogenic Growth Factor–Releasing Device , 2001, Pancreas.

[57]  Y. Hibi,et al.  More than 1,000 cases of total parathyroidectomy with forearm autograft for renal hyperparathyroidism. , 2001, American journal of kidney diseases : the official journal of the National Kidney Foundation.

[58]  Y. Tabata,et al.  Development of a New Method to Induce Angiogenesis at Subcutaneous Site of Streptozotocin-Induced Diabetic Rats for Islet Transplantation , 2001, Cell transplantation.

[59]  Y. Ikada,et al.  Modified Subcutaneous Tissue with Neovascularization is Useful as the Site for Pancreatic Islet Transplantation , 2000, Cell transplantation.

[60]  M. Menger,et al.  Exocrine contamination of isolated islets of Langerhans deteriorates the process of revascularization after free transplantation. , 2000, Transplantation.

[61]  S. Bonner-Weir,et al.  Reversal of hyperglycemia in mice after subcutaneous transplantation of macroencapsulated islets. , 1999, Transplantation.

[62]  C. Ricordi,et al.  Transplantation of allogeneic islets of Langerhans in the rat liver: effects of macrophage depletion on graft survival and microenvironment activation. , 1998, Diabetes.

[63]  T. Starzl,et al.  Augmenter of liver regeneration enhances the success rate of fetal pancreas transplantation in rodents. , 1998, Transplantation.

[64]  M. Stegall Monitoring human islet allografts using a forearm biopsy site. , 1997, Annals of transplantation.

[65]  G. Reach,et al.  Bioartificial pancreas containing porcine islets of Langerhans implanted in low-dose streptozotocin-induced diabetic mice: effect of encapsulation medium. , 1997, Diabetes & metabolism.

[66]  J. Dupré,et al.  Insulin Resistance Prevented by Portal Delivery of Insulin in Rats With Renal Subcapsular Islet Grafts , 1997, Diabetes.

[67]  Y. Mullen,et al.  Prefabrication of a neo-endocrine organ: a rat model. , 1996, The Journal of surgical research.

[68]  J. Vacanti,et al.  Outcome of subcutaneous islet transplantation improved by a polymer device. , 1995, Transplantation proceedings.

[69]  H. Lehr,et al.  Histogenesis and ultrastructure of pancreatic islet graft microvasculature. Evidence for graft revascularization by endothelial cells of host origin. , 1995, The American journal of pathology.

[70]  G. Abouna,et al.  Site for unpurified islet transplantation is an important parameter for determination of the outcome of graft survival and function. , 1995, Cell transplantation.

[71]  C. Piercy,et al.  Insulin-like growth factor-I promotes successful fetal pancreas transplantation in the intramuscular site. , 1994, Surgery.

[72]  C. Colton,et al.  Effect of Hypoxia on Insulin Secretion by Isolated Rat and Canine Islets of Langerhans , 1993, Diabetes.

[73]  F T Gentile,et al.  Maintenance of normoglycemia in diabetic mice by subcutaneous xenografts of encapsulated islets. , 1991, Science.

[74]  M. Choti,et al.  Induction of donor-specific unresponsiveness by intrathymic islet transplantation. , 1990, Science.

[75]  L. Lögdberg,et al.  Islet transplantation to the renal subcapsular space improves late complications in streptozotocin-diabetic rats. , 1990, European surgical research. Europaische chirurgische Forschung. Recherches chirurgicales europeennes.

[76]  B. Ahrén,et al.  Islet transplantation to the renal subcapsular space in streptozotocin-diabetic rats. Long-term effects on insulin and glucagon secretion. , 1989, Acta chirurgica Scandinavica.

[77]  J. Tai,et al.  Allotransplantation of Dispersed Single Pancreatic Endocrine Cells in Diabetic Rats , 1988, Diabetes.

[78]  K. Lafferty,et al.  A comparative study of transplant sites for endocrine tissue transplantation in the pig. , 1986, The Australian journal of experimental biology and medical science.

[79]  K. Alberti,et al.  Comparison of portal and peripheral insulin delivery on carbohydrate metabolism in streptozotocin-diabetic rats , 1985, Diabetologia.

[80]  J. Tai,et al.  INTRACEREBRAL ALLOTRANSPLANTATION OF PURIFIED PANCREATIC ENDOCRINE CELLS AND PANCREATIC ISLETS IN DIABETIC RATS , 1984, Transplantation.

[81]  P. Lacy,et al.  Intratesticular Transplants of Islet Xenografts (Rat to Mouse) , 1983, Diabetes.

[82]  F. Pi‐Sunyer,et al.  LONG‐TERM REVERSAL OF STREPTOZOTOCIN‐INDUCED DIABETES IN RATS BY INTRAMUSCULAR ISLET IMPLANTATION , 1981, Transplantation.

[83]  A. Matas,et al.  Transplantation of Dispersed Pancreatic Islet Tissue in Humans: Autografs and Allografts , 1980, Diabetes.

[84]  F. Pi‐Sunyer,et al.  Tissue culture preservation and intramuscular transplantation of pancreatic islets. , 1978, Surgery.

[85]  A. Renold,et al.  Subcutaneous, isogeneic transplantation of either duct-ligated pancreas or isolated islets in streptozotocin diabetic mice. , 1976, Endocrinology.

[86]  K. Federlin,et al.  Islet Transplantation in Experimental Diabetes of the Rat , 1976, Hormone and metabolic research = Hormon- und Stoffwechselforschung = Hormones et metabolisme.

[87]  K. Federlin,et al.  Islet Transplantation in Experimental Diabetes in the Rat , 1975, Hormone and metabolic research = Hormon- und Stoffwechselforschung = Hormones et metabolisme.

[88]  Nathaniel K. Chan,et al.  Efficacy comparison between intraportal and subcapsular islet transplants in a murine diabetic model. , 2009, Transplantation proceedings.

[89]  C. Ricordi,et al.  Effects of systemic immunosuppression on islet engraftment and function into a subcutaneous biocompatible device. , 2009, Transplantation proceedings.

[90]  A. Obenaus,et al.  Factors affecting islet graft embolization in the liver of diabetic mice. , 2009, Islets.

[91]  L. Benítez-Bribiesca,et al.  The bone marrow as a potential receptor site for pancreatic islet grafts. , 2008, Archives of medical research.

[92]  P. Andrades,et al.  Subcutaneous pancreatic islet transplantation using fibrin glue as a carrier. , 2007, Transplantation proceedings.

[93]  P. Lacy,et al.  Protection of encapsulated human islets implanted without immunosuppression in patients with type I or type II diabetes and in nondiabetic control subjects. , 1994, Diabetes.

[94]  P. Diem,et al.  Systemic Venous Drainage of Pancreas Allografts as Independent Cause of Hyperinsulinemia in Type I Diabetic Recipients , 1990, Diabetes.