International Journal of Surgery 18 (2015) 21e27
Contents lists available at ScienceDirect
International Journal of Surgery journal homepage: www.journal-surgery.net
Original research
Impact of duration of diabetes on outcome following pancreas transplantation Burcin Ekser a, Richard S. Mangus a, John A. Powelson a, Michele L. Goble a, Muhammad A. Mujtaba b, Tim E. Taber b, Jonathan A. Fridell a, * a b
The Department of Surgery, Indiana University School of Medicine, Indianapolis, IN, USA The Department of Medicine, Indiana University School of Medicine, Indianapolis, IN, USA
h i g h l i g h t s Longstanding T1DM does not seem to negatively impact recipient outcomes following all types of pancreas transplantation. Duration of diabetes exposure significantly correlates with the need for kidney transplantation. The majority of pancreas recipients with longer standing diabetes (21e30 and >30 years) were also undergoing kidney transplantation as SPK or PAK, likely because renal failure is a late complication of diabetes. PTA recipients, on the other hand, tended to make up a much larger portion of the group with the shortest duration of diabetes.
a r t i c l e i n f o
a b s t r a c t
Article history: Received 12 February 2015 Accepted 8 April 2015 Available online 11 April 2015
Introduction: The impact of duration of T1DM on outcomes following simultaneous pancreas and kidney transplantation (SPK), pancreas after kidney transplantation (PAK), and pancreas transplantation alone (PTA) is currently unknown. Materials and methods: A total of 451 pancreas transplants performed at a single institution between January 2003 and April 2013 (SPK n ¼ 238, PAK, n ¼ 97, and PTA, n ¼ 116) were divided into three groups based on cumulative years of T1DM (0e20 years, 21e30 years, and >30 years). Early (7-day) and late (90day) pancreas allograft loss, patient and pancreas allograft survivals were analyzed. Results: While, PAK was more common in recipients with >30 years of T1DM (29%, p < 0.0047), PTA was more common in recipients with 0e20 years of T1DM (41%, p < 0.0011). In all transplant types, recipients age was significantly higher the longer the duration of diabetes. Although longer duration of T1DM correlated with a higher rate of major amputations in PAK recipients (p < 0.0032), no difference was observed in SPK or PTA. While early pancreas graft loss was 2e4% in SPK and PAK with shorter or longer T1DM (p ¼ n.s.), it reached to 10% in PTA with T1DM > 30 years (p < 0.0097). Longer duration of T1DM affected late pancreas graft loss in PAK patients (8%, p < 0.0349). Patient and death-censored graft survival rates were similar in all types of pancreas transplantation extracted by accumulation of years of T1DM prior to transplant. Conclusions: Longstanding T1DM does not seem to negatively impact recipient outcomes following all types of pancreas transplantation. © 2015 Published by Elsevier Ltd on behalf of IJS Publishing Group Limited.
Keywords: Diabetes mellitus Duration of diabetes Pancreas transplantation Outcome
Abbreviations: CAD, coronary artery disease; ESRD, end-stage renal disease; MMF, mycophenolate mofetil; n.s., not significant; PAK, pancreas after kidney transplantation; PTA, pancreas transplantation alone; rATG, rabbit antithymocyte globulin; SPK, simultaneous pancreas and kidney transplantation; T1DM, type 1 diabetes mellitus; UNOS, United Network for Organ Sharing. * Corresponding author. The Department of Surgery, Indiana University School of Medicine, 550 N University BLVD, #4258, Indianapolis, IN 46202, USA. E-mail address: [email protected] (J.A. Fridell). http://dx.doi.org/10.1016/j.ijsu.2015.04.031 1743-9191/© 2015 Published by Elsevier Ltd on behalf of IJS Publishing Group Limited.
22
B. Ekser et al. / International Journal of Surgery 18 (2015) 21e27
1. Introduction Recent analyses of national U.S. data from 1980 to 2012 suggest a doubling of the incidence and prevalence of diabetes during 1990e2008, and a plateauing between 2008 and 2012 [1]. An estimated 10e15% of the US population is affected by diabetes and 8e10% of these have type 1 diabetes mellitus (T1DM) [2]. T1DM is associated with severe late complications, including end-stage renal disease (ESRD), requiring renal replacement therapy or kidney transplantation [3]. Diabetes is also an independent major risk factor for cardiovascular and cerebrovascular disease, which is dependent on the years of exposure. Studies have shown that during the first 20 years of T1DM most of the excess mortality is attributed to renal failure, however after this period, it is considered to result largely from cardiovascular events [3e5]. International studies have revealed different mortality rates depending on the duration of diabetes exposure. The Finnish study demonstrated a cumulative mortality of 6.8% at 20 years and 15% at 30 years after diabetes diagnosis with a cumulative incidence of ESRD of 2.2.and 7.8%, respectively [6]. The impact of duration of diabetes on mortality has been reported by several groups, with rates varying between 6.8 and 13% after 20 years, and 15e29% after 30 years [3,6e9]. Pancreas transplantation is most commonly performed in the context of renal transplantation for end stage diabetic nephropathy (simultaneous pancreas and kidney transplantation (SPK) or pancreas after kidney (PAK) transplantation), or as an isolated transplant for poor glycemic control, particularly hypoglycemia unawareness (pancreas transplantation alone (PTA)), and is the only definitive long-term therapy which restores the euglycemic state and prevents and reverses secondary complications of diabetes [2,10]. The impact of recipient age, which can correlate with the duration of T1DM exposure, has been investigated in pancreas transplantation [11e13]. Schenker et al. and Ablorsu et al. have demonstrated that it is possible to achieve similar graft and patient survival rates in pancreas transplant recipients >50 years old compared to younger recipients [11,13]. Our group has recently reported on the impact of age on outcomes after pancreas transplantation. In that study, we also demonstrated that older recipients (50e59 years old, n ¼ 85 and >60 years old, n ¼ 18) have similar patient and graft survival rates compared to younger recipients [14]. Interestingly, in that study, the worst pancreas allograft survival was observed in the youngest recipients (30 years
p
451 (100%) 28.5 ± 10.1 (1e54)
111 (25%) 14.8 ± 5.0 (1e20)
157 (35%) 26.0 ± 4.0 (21e30)
183 (41%) 37.7 ± 5.4 (31e54)
30 years T1DM, respectively). The lowest pancreas survival was observed in PTA in 0e20 years exposed T1DM at 10-year follow up (61%). Although recipients of PTA received additional immunosuppressive treatment with a single dose rituximab induction and sirolimus maintenance with tacrolimus, chronic rejection rate was still the highest in this group (7% vs 3%). In PTA, patients with longer duration of diabetes had lower rejection rates. It is possible that older patients may have an immunological advantage posttransplantation, although it remains unclear whether these recipients provide a more favorable immunological environment because of better compliance or a less active immune system. Richardson et al. recently investigated the levels of antibodies to the diabetes-associated islet autoantigens, such as GAD, IA-2, and zinc transporter-8 (ZnT8) in patients with long-duration T1DM, and the influence of age at diagnosis and HLA genotype on autoantibody persistence [29]. They demonstrated that all autoantibodies against GAD, IA-2 and ZnT8 were significantly decreased in patients with long-duration diabetes but there was also a remarkable persistence of anti-GAD antibodies in long-term survivors of T1DM. The decreased titers of autoantibodies were explained by the weak expression of diabetes-associated islet autoantigens due to decreased number of surviving or regenerating islets in the diabetic pancreas. This could potentially explain the favorable immunological state of older recipients together with their high compliance for organ transplantation. Management of pancreas transplant recipients has also improved significantly over the last two decades. Earlier studies cautioned that one-year pancreas graft survival in patients over 49
years of age was approximately 50% and older age (>49) was considered a relative contraindication to pancreas transplantation [12,30]. However, in the present study, the longest diabetes exposure groups (>30 years) have a mean age of recipients of 48e49 years in all types of pancreas transplants. Our group also previously showed that recipients of pancreas transplantation between 50 and 59 years of age (n ¼ 85) and >60 years of age (n ¼ 18) had 95% and 93% 1-year patient survival, respectively [14]. In the present study, we observed that duration of diabetes exposure significantly correlates with the need for kidney transplantation. The majority of pancreas recipients with longer standing diabetes (21e30 and >30 years) were also undergoing kidney transplantation as SPK or PAK, likely because renal failure is a late complication of diabetes. PTA recipients, on the other hand, tended to make up a much larger portion of the group with the shortest duration of diabetes (40% vs 13% and 22% for PTA vs PAK and SPK, respectively, p < 0.001). In conclusion, although the patients with longstanding T1DM requires increased rate of kidney transplantation, their outcomes following all types of pancreas transplantation are not negatively impacted. Ethical approval Local hospital IRB was obtained. Sources of funding None. Author contribution B.E and R.S.M participated in data collection and analysis, and performance of research. B.E and J.A.F participated in writing of the article. R.S.M and J.A.F participated in research design and performance of research. J.A.P and J.A.F performed most of the surgeries. J.A.P, J.A.F, M.L.G, M.A.M, T.E.T participated in follow up of patients and data collection. All authors participated in critical review of the manuscript. Conflicts of interest Authors declare no conflict of interests. Guarantor Burcin Ekser, MD. Research registration unique identifying number (UIN) researchregistry15. Acknowledgments Part of this paper was presented in the 14th World Congress of the International Pancreas and Islet Transplant Association (IPITA 2013). Appendix A. Supplementary data Supplementary data related to this article can be found at http:// dx.doi.org/10.1016/j.ijsu.2015.04.031. References [1] L.S. Geiss, J. Wang, Y.J. Cheng, et al., Prevalence and incidence trends for
B. Ekser et al. / International Journal of Surgery 18 (2015) 21e27
[2] [3]
[4]
[5]
[6] [7]
[8]
[9]
[10]
[11]
[12]
[13]
[14] [15]
diagnosed diabetes among adults aged 20 to 79 years, United States, 1980e2012, JAMA 312 (2014) 1218e1226. R.W.G. Gruessner, A.C. Gruessner, The current status of pancreas transplantation, Nat. Rev. Endocrinol. 9 (2013) 555e562. M. Stadler, M. Auinger, C. Anderwald, et al., Long-term mortality and incidence of renal dialysis and transplantation in type 1 diabetes mellitus, J. Clin. Endocrinol. Metab. 91 (2006) 3814e3820. K. Asao, C. Sarti, T. Forsen, et al., Long-term mortality in nationwide cohorts of childhood-onset type 1 diabetes in Japan and Finland, Diabetes. Care 26 (2003) 2037e2042. J.S. Dorman, R.E. Laporte, L.H. Kuller, et al., The Pittsburgh insulin-dependent diabetes mellitus (IDDM) morbidity and mortality study. Mortality results, Diabetes 33 (1984) 271e276. P. Finne, A. Reunanen, S. Stenman, et al., Incidence of end-stage renal disease in patients with type 1 diabetes, JAMA 294 (2005) 1782e1787. I. Muhlhauser, H. Overmann, R. Bender, et al., Predictors of mortality and endstage diabetic complications in patients with type 1 diabetes mellitus on intensified insulin therapy, Diabet. Med. 17 (2000) 727e734. G. Pambianco, T. Costacou, D. Ellis, et al., The 30-year natural history of type 1 diabetes complications: the Pittsburgh epidemiology of diabetes complications study experience, Diabetes 55 (2006) 1463e1469. P. Rossing, P. Hougaard, K. Borch-Johnsen, et al., Predictors of mortality in insulin dependent diabetes: 10 year observational follow up study, BMJ 313 (1996) 779e784. P. Fioretto, M.W. Steffes, D.E.R. Sutherland, et al., Reversal of lesions of diabetic nephropathy after pancreas transplantation, N. Engl. J. Med. 339 (1998) 69e75. E. Ablorsu, A. Ghazanfar, S. Mehra, et al., Outcome of pancreas transplantation in recipients older than 50 years: a single-centre experience, Transplantation 86 (2008) 1511e1514. C.E. Freise, P.G. Stock, J.S. Melzer, Increased morbidity and mortality of simultaneous pancreas-renal transplantation in patients over 49 years of age, Transpl. Proc. 30 (1998) 292. P. Schenker, O. Vonend, B. Kruger, et al., Long-term results of pancreas transplantation in patients older than 50 years, Transpl. Int. 24 (2011) 136e142. A.P. Shah, R.S. Mangus, J.A. Powelson, et al., Impact of recipient age on whole organ pancreas transplantation, Clin. Transpl. 27 (2013) E49eE55. R. Ollinger, C. Margreiter, C. Bosmuller, et al., Evolution of pancreas transplantation. Long term results and perspectives from a high-volume center, Ann. Surg. 256 (2012) 780e787.
27
[16] H.W. Sollinger, J.S. Odorico, S.J. Knechtle, et al., Experience with 500 simultaneous pancreas-kidney transplants, Ann. Surg. 228 (1998) 284e296. [17] R.S. Mangus, J. Powelson, S.B. Kinsella, et al., Pretransplant coronary artery disease associated with worse clinical outcomes in pancreas transplantation, Clin. Transpl. 27 (2013) E442eE447. [18] J.A. Fridell, R.S. Mangus, J.A. Powelson, Histidine-tryptophan-ketoglutarate for pancreas allograft preservation: the Indiana university experience, Am. J. Transpl. 10 (2010) 1284e1289. [19] J.A. Fridell, J.A. Powelson, C.E. Sanders, et al., Preparation of the pancreas allograft for transplantation, Clin. Transpl. 25 (2011) E103eE112. [20] J.A. Fridell, R.S. Mangus, E.F. Hollinger, et al., No difference in transplant outcomes for local and import pancreas allografts, Transplantation 88 (2009) 723e728. [21] J.A. Fridell, A. Agarwal, J.A. Powelson, Pancreas transplantation at Indiana university: a brief overview of recent progress, in: R. Corry, R. Shapiro (Eds.), Pancreatic Transplantation: Informa Healthcare, USA, 2007, pp. 421e427. [22] J.A. Fridell, R.S. Mangus, J.A. Powelson, et al., Pancreas transplantation in the new millennium: the Indiana university experience, Clin. Transpl. (2011) 145e156. [23] J.A. Fridell, M.L. Milgrom, S. Henson, et al., Use of the end-to-end anastomotic circular stapler for creation of the duodenoenterostomy for enteric drainage of the pancreas allograft, J. Am. Coll. Surg. 198 (2004) 495e497. [24] J.A. Fridell, A. Shah, M.L. Milgrom, et al., Ipsilateral placement of simultaneous pancreas and kidney allografts, Transplantation 78 (2004) 1074e1076. [25] A.P. Shah, D.P. Milgrom, R.S. Mangus, et al., Comparison of pulsatile perfusion and cold storage for paired kidney allografts, Transplantation 86 (2008) 1006e1009. [26] J.A. Fridell, R.S. Mangus, E.F. Hollinger, et al., The case for pancreas after kidney transplantation, Clin. Transplant 23 (2009) 447e453. [27] J.A. Fridell, A. Agarwal, J.A. Powelson, et al., Steroid withdrawal for pancreas after kidney transplantation in recipients on maintenance prednisone immunosuppression, Transplantation 82 (2006) 389e392. [28] M.E. Jorgensen, T.P. Almdal, B. Carstensen, Time trends in mortality rates in type 1 diabetes from 2002 to 2011, Diabetologia 56 (2013) 2401e2404. [29] C.C. Richardson, J.A. Dromey, K.A. McLaughlin, et al., High frequency of autoantibodies in patients with long duration type 1 diabetes, Diabetologia 56 (2013) 2538e2540. [30] C.L. Manske, Y. Wang, W. Thomas, Mortality of cadaveric kidney transplantation versus combined kidney-pancreas transplantation in diabetic patients, Lancet 346 (1995) 1658e1662.
Contents lists available at ScienceDirect
International Journal of Surgery journal homepage: www.journal-surgery.net
Original research
Impact of duration of diabetes on outcome following pancreas transplantation Burcin Ekser a, Richard S. Mangus a, John A. Powelson a, Michele L. Goble a, Muhammad A. Mujtaba b, Tim E. Taber b, Jonathan A. Fridell a, * a b
The Department of Surgery, Indiana University School of Medicine, Indianapolis, IN, USA The Department of Medicine, Indiana University School of Medicine, Indianapolis, IN, USA
h i g h l i g h t s Longstanding T1DM does not seem to negatively impact recipient outcomes following all types of pancreas transplantation. Duration of diabetes exposure significantly correlates with the need for kidney transplantation. The majority of pancreas recipients with longer standing diabetes (21e30 and >30 years) were also undergoing kidney transplantation as SPK or PAK, likely because renal failure is a late complication of diabetes. PTA recipients, on the other hand, tended to make up a much larger portion of the group with the shortest duration of diabetes.
a r t i c l e i n f o
a b s t r a c t
Article history: Received 12 February 2015 Accepted 8 April 2015 Available online 11 April 2015
Introduction: The impact of duration of T1DM on outcomes following simultaneous pancreas and kidney transplantation (SPK), pancreas after kidney transplantation (PAK), and pancreas transplantation alone (PTA) is currently unknown. Materials and methods: A total of 451 pancreas transplants performed at a single institution between January 2003 and April 2013 (SPK n ¼ 238, PAK, n ¼ 97, and PTA, n ¼ 116) were divided into three groups based on cumulative years of T1DM (0e20 years, 21e30 years, and >30 years). Early (7-day) and late (90day) pancreas allograft loss, patient and pancreas allograft survivals were analyzed. Results: While, PAK was more common in recipients with >30 years of T1DM (29%, p < 0.0047), PTA was more common in recipients with 0e20 years of T1DM (41%, p < 0.0011). In all transplant types, recipients age was significantly higher the longer the duration of diabetes. Although longer duration of T1DM correlated with a higher rate of major amputations in PAK recipients (p < 0.0032), no difference was observed in SPK or PTA. While early pancreas graft loss was 2e4% in SPK and PAK with shorter or longer T1DM (p ¼ n.s.), it reached to 10% in PTA with T1DM > 30 years (p < 0.0097). Longer duration of T1DM affected late pancreas graft loss in PAK patients (8%, p < 0.0349). Patient and death-censored graft survival rates were similar in all types of pancreas transplantation extracted by accumulation of years of T1DM prior to transplant. Conclusions: Longstanding T1DM does not seem to negatively impact recipient outcomes following all types of pancreas transplantation. © 2015 Published by Elsevier Ltd on behalf of IJS Publishing Group Limited.
Keywords: Diabetes mellitus Duration of diabetes Pancreas transplantation Outcome
Abbreviations: CAD, coronary artery disease; ESRD, end-stage renal disease; MMF, mycophenolate mofetil; n.s., not significant; PAK, pancreas after kidney transplantation; PTA, pancreas transplantation alone; rATG, rabbit antithymocyte globulin; SPK, simultaneous pancreas and kidney transplantation; T1DM, type 1 diabetes mellitus; UNOS, United Network for Organ Sharing. * Corresponding author. The Department of Surgery, Indiana University School of Medicine, 550 N University BLVD, #4258, Indianapolis, IN 46202, USA. E-mail address: [email protected] (J.A. Fridell). http://dx.doi.org/10.1016/j.ijsu.2015.04.031 1743-9191/© 2015 Published by Elsevier Ltd on behalf of IJS Publishing Group Limited.
22
B. Ekser et al. / International Journal of Surgery 18 (2015) 21e27
1. Introduction Recent analyses of national U.S. data from 1980 to 2012 suggest a doubling of the incidence and prevalence of diabetes during 1990e2008, and a plateauing between 2008 and 2012 [1]. An estimated 10e15% of the US population is affected by diabetes and 8e10% of these have type 1 diabetes mellitus (T1DM) [2]. T1DM is associated with severe late complications, including end-stage renal disease (ESRD), requiring renal replacement therapy or kidney transplantation [3]. Diabetes is also an independent major risk factor for cardiovascular and cerebrovascular disease, which is dependent on the years of exposure. Studies have shown that during the first 20 years of T1DM most of the excess mortality is attributed to renal failure, however after this period, it is considered to result largely from cardiovascular events [3e5]. International studies have revealed different mortality rates depending on the duration of diabetes exposure. The Finnish study demonstrated a cumulative mortality of 6.8% at 20 years and 15% at 30 years after diabetes diagnosis with a cumulative incidence of ESRD of 2.2.and 7.8%, respectively [6]. The impact of duration of diabetes on mortality has been reported by several groups, with rates varying between 6.8 and 13% after 20 years, and 15e29% after 30 years [3,6e9]. Pancreas transplantation is most commonly performed in the context of renal transplantation for end stage diabetic nephropathy (simultaneous pancreas and kidney transplantation (SPK) or pancreas after kidney (PAK) transplantation), or as an isolated transplant for poor glycemic control, particularly hypoglycemia unawareness (pancreas transplantation alone (PTA)), and is the only definitive long-term therapy which restores the euglycemic state and prevents and reverses secondary complications of diabetes [2,10]. The impact of recipient age, which can correlate with the duration of T1DM exposure, has been investigated in pancreas transplantation [11e13]. Schenker et al. and Ablorsu et al. have demonstrated that it is possible to achieve similar graft and patient survival rates in pancreas transplant recipients >50 years old compared to younger recipients [11,13]. Our group has recently reported on the impact of age on outcomes after pancreas transplantation. In that study, we also demonstrated that older recipients (50e59 years old, n ¼ 85 and >60 years old, n ¼ 18) have similar patient and graft survival rates compared to younger recipients [14]. Interestingly, in that study, the worst pancreas allograft survival was observed in the youngest recipients (30 years
p
451 (100%) 28.5 ± 10.1 (1e54)
111 (25%) 14.8 ± 5.0 (1e20)
157 (35%) 26.0 ± 4.0 (21e30)
183 (41%) 37.7 ± 5.4 (31e54)
30 years T1DM, respectively). The lowest pancreas survival was observed in PTA in 0e20 years exposed T1DM at 10-year follow up (61%). Although recipients of PTA received additional immunosuppressive treatment with a single dose rituximab induction and sirolimus maintenance with tacrolimus, chronic rejection rate was still the highest in this group (7% vs 3%). In PTA, patients with longer duration of diabetes had lower rejection rates. It is possible that older patients may have an immunological advantage posttransplantation, although it remains unclear whether these recipients provide a more favorable immunological environment because of better compliance or a less active immune system. Richardson et al. recently investigated the levels of antibodies to the diabetes-associated islet autoantigens, such as GAD, IA-2, and zinc transporter-8 (ZnT8) in patients with long-duration T1DM, and the influence of age at diagnosis and HLA genotype on autoantibody persistence [29]. They demonstrated that all autoantibodies against GAD, IA-2 and ZnT8 were significantly decreased in patients with long-duration diabetes but there was also a remarkable persistence of anti-GAD antibodies in long-term survivors of T1DM. The decreased titers of autoantibodies were explained by the weak expression of diabetes-associated islet autoantigens due to decreased number of surviving or regenerating islets in the diabetic pancreas. This could potentially explain the favorable immunological state of older recipients together with their high compliance for organ transplantation. Management of pancreas transplant recipients has also improved significantly over the last two decades. Earlier studies cautioned that one-year pancreas graft survival in patients over 49
years of age was approximately 50% and older age (>49) was considered a relative contraindication to pancreas transplantation [12,30]. However, in the present study, the longest diabetes exposure groups (>30 years) have a mean age of recipients of 48e49 years in all types of pancreas transplants. Our group also previously showed that recipients of pancreas transplantation between 50 and 59 years of age (n ¼ 85) and >60 years of age (n ¼ 18) had 95% and 93% 1-year patient survival, respectively [14]. In the present study, we observed that duration of diabetes exposure significantly correlates with the need for kidney transplantation. The majority of pancreas recipients with longer standing diabetes (21e30 and >30 years) were also undergoing kidney transplantation as SPK or PAK, likely because renal failure is a late complication of diabetes. PTA recipients, on the other hand, tended to make up a much larger portion of the group with the shortest duration of diabetes (40% vs 13% and 22% for PTA vs PAK and SPK, respectively, p < 0.001). In conclusion, although the patients with longstanding T1DM requires increased rate of kidney transplantation, their outcomes following all types of pancreas transplantation are not negatively impacted. Ethical approval Local hospital IRB was obtained. Sources of funding None. Author contribution B.E and R.S.M participated in data collection and analysis, and performance of research. B.E and J.A.F participated in writing of the article. R.S.M and J.A.F participated in research design and performance of research. J.A.P and J.A.F performed most of the surgeries. J.A.P, J.A.F, M.L.G, M.A.M, T.E.T participated in follow up of patients and data collection. All authors participated in critical review of the manuscript. Conflicts of interest Authors declare no conflict of interests. Guarantor Burcin Ekser, MD. Research registration unique identifying number (UIN) researchregistry15. Acknowledgments Part of this paper was presented in the 14th World Congress of the International Pancreas and Islet Transplant Association (IPITA 2013). Appendix A. Supplementary data Supplementary data related to this article can be found at http:// dx.doi.org/10.1016/j.ijsu.2015.04.031. References [1] L.S. Geiss, J. Wang, Y.J. Cheng, et al., Prevalence and incidence trends for
B. Ekser et al. / International Journal of Surgery 18 (2015) 21e27
[2] [3]
[4]
[5]
[6] [7]
[8]
[9]
[10]
[11]
[12]
[13]
[14] [15]
diagnosed diabetes among adults aged 20 to 79 years, United States, 1980e2012, JAMA 312 (2014) 1218e1226. R.W.G. Gruessner, A.C. Gruessner, The current status of pancreas transplantation, Nat. Rev. Endocrinol. 9 (2013) 555e562. M. Stadler, M. Auinger, C. Anderwald, et al., Long-term mortality and incidence of renal dialysis and transplantation in type 1 diabetes mellitus, J. Clin. Endocrinol. Metab. 91 (2006) 3814e3820. K. Asao, C. Sarti, T. Forsen, et al., Long-term mortality in nationwide cohorts of childhood-onset type 1 diabetes in Japan and Finland, Diabetes. Care 26 (2003) 2037e2042. J.S. Dorman, R.E. Laporte, L.H. Kuller, et al., The Pittsburgh insulin-dependent diabetes mellitus (IDDM) morbidity and mortality study. Mortality results, Diabetes 33 (1984) 271e276. P. Finne, A. Reunanen, S. Stenman, et al., Incidence of end-stage renal disease in patients with type 1 diabetes, JAMA 294 (2005) 1782e1787. I. Muhlhauser, H. Overmann, R. Bender, et al., Predictors of mortality and endstage diabetic complications in patients with type 1 diabetes mellitus on intensified insulin therapy, Diabet. Med. 17 (2000) 727e734. G. Pambianco, T. Costacou, D. Ellis, et al., The 30-year natural history of type 1 diabetes complications: the Pittsburgh epidemiology of diabetes complications study experience, Diabetes 55 (2006) 1463e1469. P. Rossing, P. Hougaard, K. Borch-Johnsen, et al., Predictors of mortality in insulin dependent diabetes: 10 year observational follow up study, BMJ 313 (1996) 779e784. P. Fioretto, M.W. Steffes, D.E.R. Sutherland, et al., Reversal of lesions of diabetic nephropathy after pancreas transplantation, N. Engl. J. Med. 339 (1998) 69e75. E. Ablorsu, A. Ghazanfar, S. Mehra, et al., Outcome of pancreas transplantation in recipients older than 50 years: a single-centre experience, Transplantation 86 (2008) 1511e1514. C.E. Freise, P.G. Stock, J.S. Melzer, Increased morbidity and mortality of simultaneous pancreas-renal transplantation in patients over 49 years of age, Transpl. Proc. 30 (1998) 292. P. Schenker, O. Vonend, B. Kruger, et al., Long-term results of pancreas transplantation in patients older than 50 years, Transpl. Int. 24 (2011) 136e142. A.P. Shah, R.S. Mangus, J.A. Powelson, et al., Impact of recipient age on whole organ pancreas transplantation, Clin. Transpl. 27 (2013) E49eE55. R. Ollinger, C. Margreiter, C. Bosmuller, et al., Evolution of pancreas transplantation. Long term results and perspectives from a high-volume center, Ann. Surg. 256 (2012) 780e787.
27
[16] H.W. Sollinger, J.S. Odorico, S.J. Knechtle, et al., Experience with 500 simultaneous pancreas-kidney transplants, Ann. Surg. 228 (1998) 284e296. [17] R.S. Mangus, J. Powelson, S.B. Kinsella, et al., Pretransplant coronary artery disease associated with worse clinical outcomes in pancreas transplantation, Clin. Transpl. 27 (2013) E442eE447. [18] J.A. Fridell, R.S. Mangus, J.A. Powelson, Histidine-tryptophan-ketoglutarate for pancreas allograft preservation: the Indiana university experience, Am. J. Transpl. 10 (2010) 1284e1289. [19] J.A. Fridell, J.A. Powelson, C.E. Sanders, et al., Preparation of the pancreas allograft for transplantation, Clin. Transpl. 25 (2011) E103eE112. [20] J.A. Fridell, R.S. Mangus, E.F. Hollinger, et al., No difference in transplant outcomes for local and import pancreas allografts, Transplantation 88 (2009) 723e728. [21] J.A. Fridell, A. Agarwal, J.A. Powelson, Pancreas transplantation at Indiana university: a brief overview of recent progress, in: R. Corry, R. Shapiro (Eds.), Pancreatic Transplantation: Informa Healthcare, USA, 2007, pp. 421e427. [22] J.A. Fridell, R.S. Mangus, J.A. Powelson, et al., Pancreas transplantation in the new millennium: the Indiana university experience, Clin. Transpl. (2011) 145e156. [23] J.A. Fridell, M.L. Milgrom, S. Henson, et al., Use of the end-to-end anastomotic circular stapler for creation of the duodenoenterostomy for enteric drainage of the pancreas allograft, J. Am. Coll. Surg. 198 (2004) 495e497. [24] J.A. Fridell, A. Shah, M.L. Milgrom, et al., Ipsilateral placement of simultaneous pancreas and kidney allografts, Transplantation 78 (2004) 1074e1076. [25] A.P. Shah, D.P. Milgrom, R.S. Mangus, et al., Comparison of pulsatile perfusion and cold storage for paired kidney allografts, Transplantation 86 (2008) 1006e1009. [26] J.A. Fridell, R.S. Mangus, E.F. Hollinger, et al., The case for pancreas after kidney transplantation, Clin. Transplant 23 (2009) 447e453. [27] J.A. Fridell, A. Agarwal, J.A. Powelson, et al., Steroid withdrawal for pancreas after kidney transplantation in recipients on maintenance prednisone immunosuppression, Transplantation 82 (2006) 389e392. [28] M.E. Jorgensen, T.P. Almdal, B. Carstensen, Time trends in mortality rates in type 1 diabetes from 2002 to 2011, Diabetologia 56 (2013) 2401e2404. [29] C.C. Richardson, J.A. Dromey, K.A. McLaughlin, et al., High frequency of autoantibodies in patients with long duration type 1 diabetes, Diabetologia 56 (2013) 2538e2540. [30] C.L. Manske, Y. Wang, W. Thomas, Mortality of cadaveric kidney transplantation versus combined kidney-pancreas transplantation in diabetic patients, Lancet 346 (1995) 1658e1662.
