0021-972X/91/7303-0461/0 Journal of Clinical Endocrinology and Metabolism Copyright © 1991 by The Endocrine Society
Vol. 73, No. 3 Printed in U.S.A.
CLINICAL REVIEW 25 Current Status of Pancreas Transplantation DAVID E. R. SUTHERLAND Department of Surgery, University of Minnesota Hospital, Minneapolis, Minnesota 55455
P
ANCREAS transplantation is the only treatment of Type I diabetes that establishes an insulin-independent euglycemic state (1, 2). Glycosylated hemoglobin levels are normalized for as long as the graft functions (3). The penalty for achieving such a state is the need for immunosuppression. In contrast to heart and liver grafts, pancreas transplantation is not a life-saving procedure. Thus, for nonuremic patients with or without early nephropathy, pancreas transplants have been performed only when the problems of diabetes were perceived to be more serious than the potential side-effects of antirejection drugs (4). However, for uremic diabetic patients who are already best treated by a kidney transplant, the addition of a pancreas has become routine (5, 6), since such patients are already obligated to immunosuppression (currently a combination of cyclosporine, azathioprine, and corticosteroids for maintenance, with antilymphocyte agents used for induction therapy or treatment of rejection episodes).
term functioning grafts, it tends to stabilize, while in those with failed grafts it continues to deteriorate (10). Finally, neuropathy is stabilized or improved in most recipients of pancreas transplants, with increased nerve conduction velocities and evoked muscle action potential (11). Indeed, in patients with severe autonomic neuropathy, a successful pancreas transplant is associated with a significantly higher probability of survival over those who are not transplanted or whose transplants are not successful (12). Application of pancreas transplants as a treatment for patients with hyperlabile diabetes and extreme difficulty with metabolic control has been stated to improve the quality of life simply by inducing insulin independence (13). Kidney transplants also improve the quality of life in uremic patients by obviating the need for dialysis. For diabetic patients with both problems, the effect of a double transplant can be dramatic (14). For diabetic patients without nephropathy, however, the penalties of immunosuppression must be accepted for relief of diabetes only, and some diabetologists doubt the benefits are worth the price (15).
Effect on secondary complications of diabetes In nonuremic patients, a successful pancreas transplant can induce regression of early microscopic lesions of diabetic nephropathy, but renal function is not improved because of the nephrotoxic effect of the cyclosporine necessary to prevent rejection (7). Correspondingly, in kidney transplant recipients, a successful pancreas transplant, performed either simultaneously (8) or shortly after the kidney (9), will prevent recurrence of diabetic nephropathy in the new graft. In this situation, cyclosporine is necessary in order to have renal function at all, and by keeping diabetic lesions from being superimposed on those of cyclosporine or rejection, renal graft function is likely to be improved. In contrast to the positive effect on kidneys, the natural history of advanced retinopathy is not altered early on in recipients of pancreas transplants, although in patients with long-
Outcome and recipient categories The first pancreas transplant was performed in 1966 (16). Although applied only sporadically early on, the number of pancreas transplants has increased rapidly in recent years. As of 1990 more than 3000 pancreas transplants had been reported to the International Pancreas Transplant Registry (17). Of these, approximately twothirds were simultaneous pancreas/kidney (SPK) transplants, slightly more than one-sixth were pancreas transplants after a kidney (PAK), and less than one-sixth were pancreas transplants alone (PTA). The vast majority of pancreas transplants have been from cadaver donors, but slightly more than 80 have been segmental grafts from living related donors. As with kidney transplants from living related donors, rejection is less likely to occur, but currently there is not a shortage of cadaver pancreases so the only reason to use living related donors for pancreas transplants is for the immunological advan-
Received January 25, 1991. Address requests for reprints to: David E. R. Sutherland, M.D., Ph.D., Department of Surgery, University of Minnesota Hospital, Minneapolis, Minnesota 55455. 461
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462
SUTHERLAND
tage (18). Some physicians feel living relatives should never be used as pancreas donors. The hemi-pancreatectomized donors have changes in results of metabolic tests of endocrine function similar to those seen in tests of renal function in uninephrectomized kidney donors, the long-term consequences of which are unknown (19). A variety of surgical techniques have been used to manage the graft exocrine secretions in the recipient, including polymer injection, enteric drainage, or urinary drainage via the bladder (20). The main advantage of the latter technique is the ability to detect rejection episodes of the pancreas early (before hyperglycemia) by monitoring amylase secreted directly into the urine by the graft. Institution of antirejection treatment as soon as there is a decrease in urine amylase activity can reverse the process, allowing endocrine function to be maintained. This marker is particularly important for monitoring rejection in solitary pancreas transplants (PTA and PAK) performed without a concomitant kidney. In the SPK group, a rise in serum creatinine as a manifestation of rejection usually occurs before there is a change in pancreatic function from concomitant rejection, again allowing for early treatment and reversal (5). However, for solitary pancreas transplants, urine amylase is the only organ-specific marker of rejection that is currently practical to use (20). In the US, the bladder-drainage technique is now used for nearly all pancreas transplants (21). Since October 1, 1987, reporting of US cases to the Scientific Registry of the United Network for Organ Sharing has been obligatory. As of October 1990, 1021 cases (980 with bladderdrainage) were included in the UNOS Registry. The overall 1-yr pancreas graft functional (insulin independent) survival rate was 72%, including 77% in the SPK (n = 833), 52% in the PAK (n = 112), and 54% in the PTA (n = 88) categories. The largest experience with pancreas transplants is at the University of Minnesota (6), with more than 400 performed as of October 1990. The Minnesota team has particularly emphasized the performance of solitary pancreas transplants (PAK and PTA). In these groups, HLA-DR matching (or mismatching) has had a significant impact on the results (22). Of 105 solitary bladderdrained cadaver donor pancreas transplants performed between November 1984 and May 1990 at the University of Minnesota, the actuarial 1-yr graft functional survival rate was 62% for those mismatched for only one or zero DR antigens (n = 71), while it was 41% for those mismatched for two DR antigens (n = 34). In an attempt to improve results of solitary pancreas transplants, in 1987 the Minnesota protocols were changed. Only good matches were accepted, induction immunosuppression included 2 weeks of antilymphocyte globulin, and a decrease in urine amylase activity of 25%
JCE & M • 1991 Vol 73 • No 3
was used as an indication for treatment of rejection (22). Under these protocols, the 1-yr graft functional survival rate in nonuremic or preuremic recipients of primary pancreas transplants alone (PTA) was 72% (n = 23), and in posturemic recipients of primary pancreas transplants after a kidney (PAK), the 1-yr pancreas graft survival rate was 71% (n = 22), similar to that of the SPK recipients transplanted during the same interval. Thus, it appears that by matching for HLA-DR and treating rejection episodes early, pancreas transplantation can be as successful in pre- or posturemic diabetic recipients of a solitary graft as in uremic recipients of a simultaneous kidney. Nearly all uremic diabetic candidates for kidney transplants are candidates for a pancreas transplant. The best treatment option is to receive a living related donor kidney transplant first, followed later by a pancreas transplant from either a living related (segmental graft) (18) or cadaver (whole organ or segmental) donor (5, 23). For those without a living related donor for a kidney, a pancreas transplant can be performed simultaneously with a renal transplant from a cadaver donor (5, 6). This approach promotes the highest kidney transplant survival rates and, coupled with pancreas transplantation, ensures the best overall outcome for the patient. Currently, the major role of pancreas transplantation is as an adjunct to kidney transplantation in preuremic, uremic, or posturemic diabetic patients. Application to nonuremic patients with hyperlabile diabetes or emerging complications is very controversial. Current immunosuppressive regimens have many side effects, and HLA matching, although improving the probability of longterm success, cannot eliminate its need. At least some immunosuppression is required even for recipients of a segmental graft from a nondiabetic identical twin donor, since in its absence the original autoimmune process will recur in the graft (24). Immunosuppression sufficient to prevent rejection is always able to prevent recurrence of disease, but again, the recipient must have problems with diabetes such that the potential side-effects are an acceptable trade-off. When antirejection strategies with fewer consequences than the present regimens are available, pancreas transplants will be an alternative to exogenous insulin as a treatment for diabetes before the predisposition to secondary complications is declared.
References 1. Sutherland DER, Najarian JS, Greensberg BZ, et al. Hormonal and metabolic effects of a pancreatic endocrine graft. Ann Intern Med. 1981;95:537-41. 2. Robertson RP, Abid M, Sutherland DER, Diem P. Glucose homeostasis and insulin secretion in human recipients of pancreas transplantation. Diabetes. 1989;38(Suppl l):97-8. 3. Morel P, Goetz F, Moudry-Munns KC, Freier E, Sutherland DER. Long-term function of pancreatic transplants assessed by glycosylated hemoglobin values. Ann Intern Med. In press. 4. Sutherland DER, Kendall DM, Moudry KC, et al. Pancreas trans-
The Endocrine Society. Downloaded from press.endocrine.org by [${individualUser.displayName}] on 14 November 2015. at 15:37 For personal use only. No other uses without permission. . All rights reserved.
CLINICAL REVIEW
5. 6. 7.
8. 9.
10. 11. 12.
13. 14.
plantation in nonuremic, type I diabetic recipients. Surgery. 1988;104:453-63. Sollinger H, et al. Experience with simultaneous pancreas kidney transplantation. Ann Surg. 1988;208:475-83. Sutherland DER, Dunn DL, Goetz FC, et al. A ten year experience with 290 pancreas transplants at a single institution. Ann Surg. 1989;210:274-88. Bilous RW, Mauer SM, Sutherland DER, Steffes MW. Glomerular structure and function following successful pancreas transplantation for insulin-dependent diabetes mellitus. Diabetes. 1987;36:43A. Bohman SO, Tyden G, Wilezek A. Prevention of kidney graft diabetic nephropathy by pancreas transplantation in man. Diabetes. 1985;34:306. Bilous RW, Mauer SM, Sutherland DER, Najarian JS, Goetz FC, Steffes MW. The effects of pancreas transplantation on the glomerular structure of renal allografts in patients with insulindependent diabetes. N Engl J Med. 1989;321:80-5. Ramsay RC, Goetz FC, Sutherland DER, et al. Progression of diabetic retinopathy after pancreas transplantation for insulindependent diabetes mellitus. N Engl J Med. 1988;318:208-14. Kennedy WR, Navarro X, Goetz FC, Sutherland DER, Najarian JS. The effects of pancreas transplantation on diabetic neuropathy. N Engl J Med. 1990;322:1031-7. Navarro X, Kennedy WR, Loewenson RB, Sutherland DER. Influence of pancreas transplantation on cardiorespiratory reflexes, nerve conduction, and mortality in diabetes mellitus. Diabetes. 1990;39:802-6. Zehrer C, Gross C. Quality of life after pancreas transplantation. Diabetes Care. 1990;13:359-60. Nakache R, Tyden G, Groth CG. Quality of life in diabetic patients after combined pancreas-kidney or kidney transplantation. Diabetes. 1989;38[Suppl l]:40-2.
463
15. Ramirez LC, Rios JM, Rosenstock J, Raskin P. Is Pancreas Transplantation in Nonuremic Patients a Viable Option (Letter). Diabetes Care. 1989;12:511-12. 16. Kelly WD, Lillehei RC, Merkel FK, Idezuki Y, Goetz F. Allotransplantation of the pancreas and duodenum along with the kidney in diabetic nephropathy. Surgery. 1967;61:827. 17. Sutherland DER, Moudry-Munns KC, Gillingham K. Pancreas transplantation: report from international registry and preliminary analysis of U.S. results from New United Network for Organ Sharing (UNOS) Registry. In: Terasaki PI, ed. Clinical transplants-1989. UCLA Tissue Typing Laboratory; 1990;19-43. 18. Sutherland DER, Goetz FC, Najarian JS. Pancreas transplants from living related donors. Transplantation. 1984;38:674-670 19. Kendall DM, Sutherland DER, Najarian JS, Goetz FC, Robertson RP. Effects of hemipancreatectomy on insulin secretion and glucose tolerance in healthy human donors. N Engl J Med. 1990;322:898-903. 20. Prieto M, Sutherland DER, Goetz FC, Rosenberg, Najarian JS. Pancreas transplant results according to technique of duct management: bladder versus enteric drainage. Surgery. 1987;102:68091. 21. Sutherland DER, Gillingham K, Mowdry-Munns K. Results of pancreas transplantation in the United Network for Organ Sharing (UNOS) registry with comparison for 1984-87 results. Clin Transplant. In press. 22. So SKS, Moudry-Munns KC, Gillingham K, Minford EJ, Sutherland DER. Short-term and long-term effects of HLA matching in cadaveric pancreas transplantation. Transplant Proc. In press. 23. Sutherland DER, Moudry-Munns KC, Gillingham K, Najarian JS, Dunn DL. Solitary pancreas transplantation: alone in nonuremic and after a kidney in uremic diabetic patients. Transplant Proc. 1991;23:1637-9. 24. Sutherland DER, Goetz FC, Sibley RK. Recurrence of disease in pancreas transplants. Diabetes. 1989;38[Suppl l]:85-7.
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Vol. 73, No. 3 Printed in U.S.A.
CLINICAL REVIEW 25 Current Status of Pancreas Transplantation DAVID E. R. SUTHERLAND Department of Surgery, University of Minnesota Hospital, Minneapolis, Minnesota 55455
P
ANCREAS transplantation is the only treatment of Type I diabetes that establishes an insulin-independent euglycemic state (1, 2). Glycosylated hemoglobin levels are normalized for as long as the graft functions (3). The penalty for achieving such a state is the need for immunosuppression. In contrast to heart and liver grafts, pancreas transplantation is not a life-saving procedure. Thus, for nonuremic patients with or without early nephropathy, pancreas transplants have been performed only when the problems of diabetes were perceived to be more serious than the potential side-effects of antirejection drugs (4). However, for uremic diabetic patients who are already best treated by a kidney transplant, the addition of a pancreas has become routine (5, 6), since such patients are already obligated to immunosuppression (currently a combination of cyclosporine, azathioprine, and corticosteroids for maintenance, with antilymphocyte agents used for induction therapy or treatment of rejection episodes).
term functioning grafts, it tends to stabilize, while in those with failed grafts it continues to deteriorate (10). Finally, neuropathy is stabilized or improved in most recipients of pancreas transplants, with increased nerve conduction velocities and evoked muscle action potential (11). Indeed, in patients with severe autonomic neuropathy, a successful pancreas transplant is associated with a significantly higher probability of survival over those who are not transplanted or whose transplants are not successful (12). Application of pancreas transplants as a treatment for patients with hyperlabile diabetes and extreme difficulty with metabolic control has been stated to improve the quality of life simply by inducing insulin independence (13). Kidney transplants also improve the quality of life in uremic patients by obviating the need for dialysis. For diabetic patients with both problems, the effect of a double transplant can be dramatic (14). For diabetic patients without nephropathy, however, the penalties of immunosuppression must be accepted for relief of diabetes only, and some diabetologists doubt the benefits are worth the price (15).
Effect on secondary complications of diabetes In nonuremic patients, a successful pancreas transplant can induce regression of early microscopic lesions of diabetic nephropathy, but renal function is not improved because of the nephrotoxic effect of the cyclosporine necessary to prevent rejection (7). Correspondingly, in kidney transplant recipients, a successful pancreas transplant, performed either simultaneously (8) or shortly after the kidney (9), will prevent recurrence of diabetic nephropathy in the new graft. In this situation, cyclosporine is necessary in order to have renal function at all, and by keeping diabetic lesions from being superimposed on those of cyclosporine or rejection, renal graft function is likely to be improved. In contrast to the positive effect on kidneys, the natural history of advanced retinopathy is not altered early on in recipients of pancreas transplants, although in patients with long-
Outcome and recipient categories The first pancreas transplant was performed in 1966 (16). Although applied only sporadically early on, the number of pancreas transplants has increased rapidly in recent years. As of 1990 more than 3000 pancreas transplants had been reported to the International Pancreas Transplant Registry (17). Of these, approximately twothirds were simultaneous pancreas/kidney (SPK) transplants, slightly more than one-sixth were pancreas transplants after a kidney (PAK), and less than one-sixth were pancreas transplants alone (PTA). The vast majority of pancreas transplants have been from cadaver donors, but slightly more than 80 have been segmental grafts from living related donors. As with kidney transplants from living related donors, rejection is less likely to occur, but currently there is not a shortage of cadaver pancreases so the only reason to use living related donors for pancreas transplants is for the immunological advan-
Received January 25, 1991. Address requests for reprints to: David E. R. Sutherland, M.D., Ph.D., Department of Surgery, University of Minnesota Hospital, Minneapolis, Minnesota 55455. 461
The Endocrine Society. Downloaded from press.endocrine.org by [${individualUser.displayName}] on 14 November 2015. at 15:37 For personal use only. No other uses without permission. . All rights reserved.
462
SUTHERLAND
tage (18). Some physicians feel living relatives should never be used as pancreas donors. The hemi-pancreatectomized donors have changes in results of metabolic tests of endocrine function similar to those seen in tests of renal function in uninephrectomized kidney donors, the long-term consequences of which are unknown (19). A variety of surgical techniques have been used to manage the graft exocrine secretions in the recipient, including polymer injection, enteric drainage, or urinary drainage via the bladder (20). The main advantage of the latter technique is the ability to detect rejection episodes of the pancreas early (before hyperglycemia) by monitoring amylase secreted directly into the urine by the graft. Institution of antirejection treatment as soon as there is a decrease in urine amylase activity can reverse the process, allowing endocrine function to be maintained. This marker is particularly important for monitoring rejection in solitary pancreas transplants (PTA and PAK) performed without a concomitant kidney. In the SPK group, a rise in serum creatinine as a manifestation of rejection usually occurs before there is a change in pancreatic function from concomitant rejection, again allowing for early treatment and reversal (5). However, for solitary pancreas transplants, urine amylase is the only organ-specific marker of rejection that is currently practical to use (20). In the US, the bladder-drainage technique is now used for nearly all pancreas transplants (21). Since October 1, 1987, reporting of US cases to the Scientific Registry of the United Network for Organ Sharing has been obligatory. As of October 1990, 1021 cases (980 with bladderdrainage) were included in the UNOS Registry. The overall 1-yr pancreas graft functional (insulin independent) survival rate was 72%, including 77% in the SPK (n = 833), 52% in the PAK (n = 112), and 54% in the PTA (n = 88) categories. The largest experience with pancreas transplants is at the University of Minnesota (6), with more than 400 performed as of October 1990. The Minnesota team has particularly emphasized the performance of solitary pancreas transplants (PAK and PTA). In these groups, HLA-DR matching (or mismatching) has had a significant impact on the results (22). Of 105 solitary bladderdrained cadaver donor pancreas transplants performed between November 1984 and May 1990 at the University of Minnesota, the actuarial 1-yr graft functional survival rate was 62% for those mismatched for only one or zero DR antigens (n = 71), while it was 41% for those mismatched for two DR antigens (n = 34). In an attempt to improve results of solitary pancreas transplants, in 1987 the Minnesota protocols were changed. Only good matches were accepted, induction immunosuppression included 2 weeks of antilymphocyte globulin, and a decrease in urine amylase activity of 25%
JCE & M • 1991 Vol 73 • No 3
was used as an indication for treatment of rejection (22). Under these protocols, the 1-yr graft functional survival rate in nonuremic or preuremic recipients of primary pancreas transplants alone (PTA) was 72% (n = 23), and in posturemic recipients of primary pancreas transplants after a kidney (PAK), the 1-yr pancreas graft survival rate was 71% (n = 22), similar to that of the SPK recipients transplanted during the same interval. Thus, it appears that by matching for HLA-DR and treating rejection episodes early, pancreas transplantation can be as successful in pre- or posturemic diabetic recipients of a solitary graft as in uremic recipients of a simultaneous kidney. Nearly all uremic diabetic candidates for kidney transplants are candidates for a pancreas transplant. The best treatment option is to receive a living related donor kidney transplant first, followed later by a pancreas transplant from either a living related (segmental graft) (18) or cadaver (whole organ or segmental) donor (5, 23). For those without a living related donor for a kidney, a pancreas transplant can be performed simultaneously with a renal transplant from a cadaver donor (5, 6). This approach promotes the highest kidney transplant survival rates and, coupled with pancreas transplantation, ensures the best overall outcome for the patient. Currently, the major role of pancreas transplantation is as an adjunct to kidney transplantation in preuremic, uremic, or posturemic diabetic patients. Application to nonuremic patients with hyperlabile diabetes or emerging complications is very controversial. Current immunosuppressive regimens have many side effects, and HLA matching, although improving the probability of longterm success, cannot eliminate its need. At least some immunosuppression is required even for recipients of a segmental graft from a nondiabetic identical twin donor, since in its absence the original autoimmune process will recur in the graft (24). Immunosuppression sufficient to prevent rejection is always able to prevent recurrence of disease, but again, the recipient must have problems with diabetes such that the potential side-effects are an acceptable trade-off. When antirejection strategies with fewer consequences than the present regimens are available, pancreas transplants will be an alternative to exogenous insulin as a treatment for diabetes before the predisposition to secondary complications is declared.
References 1. Sutherland DER, Najarian JS, Greensberg BZ, et al. Hormonal and metabolic effects of a pancreatic endocrine graft. Ann Intern Med. 1981;95:537-41. 2. Robertson RP, Abid M, Sutherland DER, Diem P. Glucose homeostasis and insulin secretion in human recipients of pancreas transplantation. Diabetes. 1989;38(Suppl l):97-8. 3. Morel P, Goetz F, Moudry-Munns KC, Freier E, Sutherland DER. Long-term function of pancreatic transplants assessed by glycosylated hemoglobin values. Ann Intern Med. In press. 4. Sutherland DER, Kendall DM, Moudry KC, et al. Pancreas trans-
The Endocrine Society. Downloaded from press.endocrine.org by [${individualUser.displayName}] on 14 November 2015. at 15:37 For personal use only. No other uses without permission. . All rights reserved.
CLINICAL REVIEW
5. 6. 7.
8. 9.
10. 11. 12.
13. 14.
plantation in nonuremic, type I diabetic recipients. Surgery. 1988;104:453-63. Sollinger H, et al. Experience with simultaneous pancreas kidney transplantation. Ann Surg. 1988;208:475-83. Sutherland DER, Dunn DL, Goetz FC, et al. A ten year experience with 290 pancreas transplants at a single institution. Ann Surg. 1989;210:274-88. Bilous RW, Mauer SM, Sutherland DER, Steffes MW. Glomerular structure and function following successful pancreas transplantation for insulin-dependent diabetes mellitus. Diabetes. 1987;36:43A. Bohman SO, Tyden G, Wilezek A. Prevention of kidney graft diabetic nephropathy by pancreas transplantation in man. Diabetes. 1985;34:306. Bilous RW, Mauer SM, Sutherland DER, Najarian JS, Goetz FC, Steffes MW. The effects of pancreas transplantation on the glomerular structure of renal allografts in patients with insulindependent diabetes. N Engl J Med. 1989;321:80-5. Ramsay RC, Goetz FC, Sutherland DER, et al. Progression of diabetic retinopathy after pancreas transplantation for insulindependent diabetes mellitus. N Engl J Med. 1988;318:208-14. Kennedy WR, Navarro X, Goetz FC, Sutherland DER, Najarian JS. The effects of pancreas transplantation on diabetic neuropathy. N Engl J Med. 1990;322:1031-7. Navarro X, Kennedy WR, Loewenson RB, Sutherland DER. Influence of pancreas transplantation on cardiorespiratory reflexes, nerve conduction, and mortality in diabetes mellitus. Diabetes. 1990;39:802-6. Zehrer C, Gross C. Quality of life after pancreas transplantation. Diabetes Care. 1990;13:359-60. Nakache R, Tyden G, Groth CG. Quality of life in diabetic patients after combined pancreas-kidney or kidney transplantation. Diabetes. 1989;38[Suppl l]:40-2.
463
15. Ramirez LC, Rios JM, Rosenstock J, Raskin P. Is Pancreas Transplantation in Nonuremic Patients a Viable Option (Letter). Diabetes Care. 1989;12:511-12. 16. Kelly WD, Lillehei RC, Merkel FK, Idezuki Y, Goetz F. Allotransplantation of the pancreas and duodenum along with the kidney in diabetic nephropathy. Surgery. 1967;61:827. 17. Sutherland DER, Moudry-Munns KC, Gillingham K. Pancreas transplantation: report from international registry and preliminary analysis of U.S. results from New United Network for Organ Sharing (UNOS) Registry. In: Terasaki PI, ed. Clinical transplants-1989. UCLA Tissue Typing Laboratory; 1990;19-43. 18. Sutherland DER, Goetz FC, Najarian JS. Pancreas transplants from living related donors. Transplantation. 1984;38:674-670 19. Kendall DM, Sutherland DER, Najarian JS, Goetz FC, Robertson RP. Effects of hemipancreatectomy on insulin secretion and glucose tolerance in healthy human donors. N Engl J Med. 1990;322:898-903. 20. Prieto M, Sutherland DER, Goetz FC, Rosenberg, Najarian JS. Pancreas transplant results according to technique of duct management: bladder versus enteric drainage. Surgery. 1987;102:68091. 21. Sutherland DER, Gillingham K, Mowdry-Munns K. Results of pancreas transplantation in the United Network for Organ Sharing (UNOS) registry with comparison for 1984-87 results. Clin Transplant. In press. 22. So SKS, Moudry-Munns KC, Gillingham K, Minford EJ, Sutherland DER. Short-term and long-term effects of HLA matching in cadaveric pancreas transplantation. Transplant Proc. In press. 23. Sutherland DER, Moudry-Munns KC, Gillingham K, Najarian JS, Dunn DL. Solitary pancreas transplantation: alone in nonuremic and after a kidney in uremic diabetic patients. Transplant Proc. 1991;23:1637-9. 24. Sutherland DER, Goetz FC, Sibley RK. Recurrence of disease in pancreas transplants. Diabetes. 1989;38[Suppl l]:85-7.
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