Improved Outcomes Following Simultaneous Pancreas-Kidney Transplantation in the Second Decade of the New Millennium

Keywords

Alemtuzumab induction; Cold ischemia time; Donor age; Era; Simultaneous pancreas-kidney transplant

Abstract

Introduction: The study purpose was to analyze in consecutive periods our nearly 19-year experience in simultaneous pancreas-kidney transplantation (SPKT) with an emphasis on changes in practice that improved outcomes in the most recent era.

Methods: Single center retrospective cohort study of all SPKTs performed in two sequential eras: Era 1 (E1): 11/1/2001 – 12/31/2010; Era 2 (E2) 1/1/2011 - 8/12/20). Immunosuppression and management protocols were standardized in both eras.

Results: 255 consecutive SPKTs were analyzed (E1, n=126; E2, n=129). By design, E2 patients received organs from younger donors (mean E1 28.1 vs. E2 23.7 years) with shorter pancreas cold ischemia times (CITs, mean E1 16.8 vs. E2 13.4 hours, both p<0.05). In addition, donors with either hypertension or cerebrovascular cause of death were more common in E1 compared to E2 (both p<0.05). More E2 patients received alemtuzumab induction (52.4% E1 vs 97.7% E2, p<0.0001). One-year pancreas graft survival rates (PGSRs, 84.9% Era 1 versus 94.6% Era 2, p=0.02) and four-year PGSRs (70.6% E1 versus 85.5% E2, p=0.002) were significantly higher in E2 and by Kaplan-Meier analysis. In univariate analysis, alemtuzumab induction and E2 were associated with superior and longer pancreas CIT with inferior death-censored PGSRs. Only alemtuzumab induction had a significant (protective) effect on censored PGSR in the multivariate model.

Conclusions: In our experience, optimizing donor quality (younger donors without hypertension or cerebrovascular cause of death), minimizing pancreas CIT, and use of alemtuzumab induction are associated with improved outcomes following SPKT.

Abbreviations

BMI: Body Mass Index; CIT: Cold Ischemia Time; CMV: Cytomegalovirus; DWFG: Death with a Functioning Graft; GSR: Graft Survival Rate; HR: Hazard Ratio; P-E: Portal-Enteric; PTx: Pancreas Transplant; RATG: Rabbit Anti-Thymocyte Globulin; S-E: Systemic-Enteric; SPKT: Simultaneous Pancreas-Kidney Transplant; US: United States

Abstract

Introduction: The study purpose was to analyze in consecutive periods our nearly 19-year experience in simultaneous pancreas-kidney transplantation (SPKT) with an emphasis on changes in practice that improved outcomes in the most recent era. Methods: Single center retrospective cohort study of all SPKTs performed in two sequential eras: Era 1 (E1): 11/1/2001 – 12/31/2010; Era 2 (E2) 1/1/2011 - 8/12/20). Immunosuppression and management protocols were standardized in both eras. Results: 255 consecutive SPKTs were analyzed (E1, n=126; E2, n=129). By design, E2 patients received organs from younger donors (mean E1 28.1 vs. E2 23.7 years) with shorter pancreas cold ischemia times (CITs, mean E1 16.8 vs. E2 13.4 hours, both p<0.05). In addition, donors with either hypertension or cerebrovascular cause of death were more common in E1 compared to E2 (both p<0.05). More E2 patients received alemtuzumab induction (52.4% E1 vs 97.7% E2, p<0.0001). One-year pancreas graft survival rates (PGSRs, 84.9% Era 1 versus 94.6% Era 2, p=0.02) and four-year PGSRs (70.6% E1 versus 85.5% E2, p=0.002) were significantly higher in E2 and by Kaplan-Meier analysis. In univariate analysis, alemtuzumab induction and E2 were associated with superior and longer pancreas CIT with inferior death-censored PGSRs. Only alemtuzumab induction had a significant (protective) effect on censored PGSR in the multivariate model. Abbreviations Conclusions: In our experience, optimizing donor quality (younger donors without hypertension or cerebrovascular cause of death), minimizing pancreas CIT, and use of alemtuzumab induction are associated with improved outcomes following SPKT.

Keywords

Alemtuzumab induction; Cold ischemia time; Donor age; Era; Simultaneous pancreas-kidney transplant

Abbreviations

BMI: Body Mass Index; CIT: Cold Ischemia Time; CMV: Cytomegalovirus; DWFG: Death with a Functioning Graft; GSR: Graft Survival Rate; HR: Hazard Ratio; P-E: Portal-Enteric; PTx: Pancreas Transplant; RATG: Rabbit Anti-Thymocyte Globulin; S-E: Systemic-Enteric; SPKT: Simultaneous Pancreas-Kidney Transplant; US: United States

Citation

Stratta RJ, Webb CJ, Jay CL, McCracken E, Garner M et al, (2025) Improved Outcomes Following Simultaneous Pancreas-Kidney Transplantation in the Second Decade of the New Millennium. J Nephrol Kidney Dis 6(2): 9.

INTRODUCTION

The history of solid organ transplantation has been characterized by developmental phases for each organ during which advances occurred in donor and recipient selection, surgical techniques, organ recovery and preservation, immunosuppression, and post-operative management. These essential “learning curves” eventually led to improved outcomes and widespread acceptance of organ-specific transplant procedures as safe and effective treatments for patients with end stage organ failure. Unfortunately, vascularized pancreas transplantation (PTx) remains overlooked by the diabetes care community despite improved outcomes [1,2]. PTx is currently the only therapy that can predictably achieve sustained euglycemia independent of exogenous insulin administration by providing an autoregulating source of endogenous insulin and glucagon production [1-4]. A functioning PTx mitigates glycemic variability, achieves normal glucose homeostasis, and removes the stigma and daily burden of diabetes as well as halting or even reversing many of the long-term sequela of hyperglycemia. However, the trade-off of PTx is that it involves a major open abdominal procedure (with a finite complication rate) and requisite chronic immunosuppression. Many kidney transplant candidates with diabetes would also benefit from PTx in terms of prolonging patient and kidney graft survival by slowing the deleterious effects and complications of chronic diabetes [5-7]. Despite the high likelihood of rendering patients euglycemic independent of exogenous insulin and eliminating the need to monitor serum glucose levels, PTx has been considered a treatment rather than a cure for insulin requiring diabetes mellitus [1-4]. According to International Pancreas Transplant Registry and Organ Procurement and Transplantation Network data, survival rates for PTx in the United States (US) have progressively improved in each successive era [2,8-11]. Surprisingly, these improvements were coincident with a precipitous decline in PTx volumes in the decade from 2005-2015, then followed by a plateau in national activity. At present, greater than 900 PTxs are performed annually in the US including more than 800 simultaneous pancreas-kidney transplants (SPKTs) [9-11]. One of the reasons for the lack of growth and universal acceptance of PTx is the perception amongst diabetes care professionals that it is a “radical” therapy requiring major surgery and lifelong immunosuppression for a “benign” yet life-shortening disease [1,3]. Other available treatment options are less invasive and, for that reason alone, more appealing to diabetologists, endocrinologists, and primary care physicians. To engage the diabetes care community in the role of PTx for the management of complicated diabetes, it is necessary to achieve the highest possible outcomes with the lowest possible morbidity. In November 2001, we initiated a PTx program at Wake Forest that has continued for over two decades. After the first decade in the new millennium, we reviewed our PTx activity by internal audit and were not satisfied with overall outcomes. Consequently, we made intentional changes in our practice at that time. The purpose of this study was to review outcomes in SPKT recipients at our center in the second decade of the millennium compared to the first decade.

METHODS

Study Design

We retrospectively reviewed 255 consecutive SPKTs performed at our center from November 2001 to August 2020 including 216 with portal enteric (P-E) drainage and 39 with systemic-enteric (S-E) drainage. For study purposes, SPKT recipients were stratified into two sequential study eras: Era 1: 11/1/2001-12/31/2010; and Era 2: 1/1/2011- 8/12/2020. These eras were not arbitrary but corresponded to several major changes in center-specific practices that were implemented in E2 including: 1.Use of deceased pancreas donors restricted to <40 years of age; 2. Exclusion of donors with a history of hypertension for more than five years or those with a cerebrovascular cause of death; 3. Aggressively targeted pancreas cold ischemia times (CIT) of ≤16 hours; and 4. Alemtuzumab induction therapy replaced rabbit anti-thymocyte globulin (RATG) as the standard of care [12-17]. Primary outcomes were patient survival, pancreas and kidney graft survival rates (GSRs), and death-censored pancreas and kidney GSRs according to era. Renal allograft loss was defined as death with a functioning graft (DWFG), transplant nephrectomy, return to dialysis, or kidney retransplantation. Pancreas graft loss was defined as DWFG, allograft pancreatectomy, pancreas retransplantation, or resumption of daily insulin therapy regardless of dose.

Donor Selection

In Era 1, donors over 40 years of age were routinely used, with an upper age limit of 58 years. We also accepted donors with hypertension or those who died of cerebrovascular causes. In Era 2, donor age above 40 years, history of hypertension, or cerebrovascular cause of death became relative if not absolute contraindications to organ acceptance [12,15]. During the entire period of study, we maintained a consistent practice of excluding donors with a body mass index (BMI) >30 kg/m2 unless the donor was a teenager or died of head trauma. Almost all donors from both eras were brain dead donors, with the exception of five cases of multi organ recovery from donation after circulatory death donors (all in Era 1). However, these donors were managed with extracorporeal membrane oxygenation support and the organ procurements were performed by standard techniques rather than rapid recovery, thus minimizing warm ischemia and avoiding prolonged extraction times [18]. Other relative contraindications to pancreas organ acceptance during both eras included prolonged donor length of hospital stay (more than 10 days), presence of acute kidney injury or elevated liver enzymes (>3 times normal), elevated serum lipase and amylase (>3 times normal) or evidence for pancreatitis or pancreatic trauma on imaging, significant hepatic steatosis, fatty infiltration or severe edema of the pancreatic parenchyma, massive transfusion requirements (>10 units of blood products), high vasopressor requirements (use of 2 or more vasopressors to maintain a systolic blood pressure >100 mm Hg), significant visceral atherosclerosis, or recent splenectomy for trauma [12,15].

Recipient Selection

General indications for PTx at our center were selecting patients with insulin-requiring diabetes with complications and the predicted ability to tolerate the operative procedure, manage the requisite immunosuppression, and commit to the need for close follow-up post SPKT irrespective of “type” of diabetes [15-17,19,20]. Specific indications for SPKT included stage 4/5 chronic kidney disease or end stage renal disease and the absence of any contraindications. Contraindications included age >65 years; insufficient cardiovascular reserve (ejection fraction 32 kg/m2); severe vascular disease; inability to comply with a complex medical and follow-up regimen; and severe frailty or sarcopenia [15-17,19,20]. A history of multiple prior laparotomies was a relative contraindication to SPKT. Selection criteria for SPKT in “type 2” diabetes included patients 40%), and presence of “complicated” or hyperlabile diabetes [19,20]. For purposes of this study, “type 2” diabetes was defined as having a fasting pretransplant C-peptide level ≥2.0 ng/ml. All patients underwent thrombophilia screening as part of their pretransplant evaluation.

Technical Aspects

All patients were blood type ABO compatible and T- and B-cell negative by flow cytometry crossmatch. SPKTs were approached as intent-to-treat with P-E drainage (n=216) using an anterior approach to the superior mesenteric vein. This technique positions the pancreas above the small bowel mesentery, with enteric exocrine drainage to the proximal ileum in the recipient (side-to-side duodeno-enterostomy without a diverting Roux limb) [21]. Arterial inflow was based on the recipient’s right common iliac artery through a window in the distal ileal mesentery after the pancreas dual artery blood supply was reconstructed with a donor common iliac bifurcation “Y” graft [22]. In patients with unsuitable anatomy for P-E drainage, S-E drainage (n=39) was performed with the pancreas positioned below the small bowel mesentery with vascular anastomoses to the right common iliac artery and vein [23]. In Era 1, 120 of the 126 SPKTs were performed by transplanting the kidney to the left iliac vessels and the pancreas to the right common or external iliac artery through a midline intraperitoneal approach. However, since August 2010, most SPKTs were performed with ipsilateral placement of the kidney and pancreas to the right iliac vessels to reduce operating time and preserve the left iliac vessels for future transplantation [24]. Two intraperitoneal drains were placed adjacent to the pancreas and kidney allografts, respectively, and removed prior to hospital discharge. Patients underwent nasogastric tube decompression for 48 hours and urethral catheter drainage for 72 hours.

Immunosuppression and Post-Transplant Management

Patients received depleting antibody induction with either single dose alemtuzumab or multi-dose alternate day rabbit anti-thymocyte globulin (RATG, 1.5 mg/kg/dose, total 3-5 doses) in combination with tacrolimus, mycophenolate mofetil or mycophenolic acid, and tapered steroids [15-17]. RATG was the primary induction agent from 2001 2004. From 2005 through 2008, 46 SPKT patients were randomized prospectively to receive either alemtuzumab or RATG [16,17]. Since 2009, single dose alemtuzumab has been the primary induction agent for the majority of SPKT recipients (n=192, 30 mg administered intra operatively), in combination with tacrolimus (target 12-hour trough levels 8-10 ng/ml), full dose mycophenolate (720 mg bid), and prednisone taper (dose reduction to 5 mg/day by 1 month following SPKT) [15-17]. The remaining 63 patients received RATG induction in combination with triple maintenance immunosuppression and rapid prednisone taper as above. All patients received perioperative antibiotics for surgical site prophylaxis, fluconazole for one month, valganciclovir for 3-6 months (6 months when the donor was cytomegalovirus [CMV] seropositive and the recipient CMV seronegative, 3 months for all other patients), and trimethoprim-sulfamethoxazole for at least one year [15-17]. Anti platelet therapy, consisting of oral aspirin (81 mg/day), was administered to all patients. Low dose heparin infusions for 3-5 days were used selectively based on risk factors [25]. Most patients were discharged from the hospital after placement of a tunneled central venous catheter and received intravenous fluid and electrolyte supplementation at home for a variable period to mitigate hypotension and prevent dehydration and metabolic acidosis. Treatment of hypotension, hyperlipidemia, anemia, and other medical conditions was initiated as indicated, aiming to maintain the blood pressure >110/60 mm Hg, fasting serum cholesterol 7-8 gm/dl.

Statistical Analysis

Data were compiled from institutional prospective and retrospective databases along with manual electronic medical record review in accordance with local Institutional Review Board guidelines and approval. Categorical data were summarized as proportions with percentages, and continuous data were summarized as means and standard deviations. Student’s t-test and Wilcoxon rank sum tests were utilized to compare continuous variables according to whether the data was normally distributed. For categorical variables, the chi-square test and Fisher’s exact test were utilized as appropriate to determine significance. Patient and GSRs were compared using Kaplan-Meier curves and log-rank tests. Cox multivariate regression was used to compare survival adjusting for donor and recipient characteristics. Univariate analysis was performed for each of the following variables: donor and recipient age and weight at transplant, donor cause of death, CIT, recipient race, recipient dialysis duration and type (hemodialysis, peritoneal dialysis, preemptive), organ import, method of antibody induction (alemtuzumab versus RATG), technique of transplant (P-E versus S-E drainage), and pretransplant C-peptide level ≥2.0 ng/ml. Factors included in survival models were chosen a priori based on clinical significance and secondarily according to significant differences between treatment groups defined by a p-value <.05. Final multivariate models included variables identified as significant in univariate analysis or if covariate was significantly different between eras. All variables used in regression models had a level of missingness <5%. Schoenfeld residuals tests were utilized to evaluate proportional hazards assumptions. A graphical assessment of proportional hazards was performed according to log-log survival curves. A two-sided p-value of <0.05 was considered significant. All analyses were performed using STATA/IC 15.1 for Windows (College Station, TX).

RESULTS

We studied retrospectively 255 consecutive SPKTs performed at our center from November 2001 to August 2020 (minimum 16-month follow-up). From November 2001 through December 2010 (Era 1), we performed 126 SPKTs including 117 (92.9%) with P-E and 9 (7.1%) with S-E drainage. From January 2011 to August 2020 (Era 2), we performed 129 SPKTs including 99 (76.7%) with P-E and 30 (23.3%) with S-E drainage (p=0.0004 compared to Era 1).

Donor, preservation, and immunological characteristics

Table 1 compares donor, preservation, and immunological characteristics between the two sequential eras. In Era 1, 40 deceased pancreas donors (31.7%) were ≥35 years of age compared to 13 (10.1%) in Era 2 (p<0.0001). Mean donor ages were 28.1±11.9 years in Era 1 compared to 23.7±7.6 years in Era 2 (p<0.01). There were no significant differences in donor gender, race, weight, or BMI between eras. Era 2 donors had more deaths secondary to anoxia (12.7% Era 1 versus 29.5% Era 2, p=0.001) and correspondingly more donors identified as increased behavioral risk (7.9% Era 1 versus 17.1% Era 2, p=0.037). Cerebrovascular cause of death was nearly twice as common in Era 1 (18.3%) compared to Era 2 (9.3%, p=0.045). The presence of donor hypertension was also more common in Era 1 (9.5%) compared to Era 2 (2.3%, p=0.017). Pancreas CITs ≥16 hours occurred in 66 cases (52.4%) in Era 1 compared to 31 cases (24.0%) in Era 2 (p<0.0001). Mean pancreas CITs were 16.8±4.1 hours in Era 1 compared to 13.4±3.4 hours in Era 2 (p<0.0001). Human leukocyte antigen mismatch, calculated panel reactive antibody level ≥20%, primary CMV exposure (donor seropositive and recipient seronegative), and organ import were not significantly different between eras (Table 1).

Table 1: Comparison of Donor, Preservation, and Immunological Characteristics According to Era

HLA: Human Leukocyte Antigen; CPRA: Calculated Panel Reactive Antibody

Recipient and transplant characteristics

Table 2 shows recipient and transplant characteristics according to era. In addition to more transplants performed with S-E drainage in Era 2, more patients received alemtuzumab induction (97.7%) in Era 2 compared to Era 1 (52.4%, p<0.0001). In addition, there were more patients on peritoneal dialysis in Era 2 (33.3%) compared to Era 1 (20.6%, p=0.025). However, preemptive SPKT was comparable in both eras (24.6% Era 1 versus 18.6% in Era 2, p=0.29). Time on the waiting list was on average 2.1 months shorter in Era 2 (p=0.03). There were no significant differences in recipient age, gender, race, weight, BMI, dialysis duration, retransplantation, or pretransplant C-peptide status according to era (Table 2).

Table 2: Comparison of Recipient and Transplant Characteristics According to Era

Outcomes

Table 3 compares outcomes between the two sequential eras. Because follow-up was much longer in Era 1 (mean follow-up 155±60 months Era 1 versus 81±37 months Era 2), one- and four-year actual survival rates are displayed in Table 3 for comparative analyses. More than 90% of patients had at least four-year follow-up. One-year patient and kidney GSRs were not significantly different in the two eras. However, one-year pancreas GSRs were significantly higher in Era 2 (84.9% Era 1 versus 94.6% Era 2, p=0.02) as well as in the death-censored analysis (87.7% Era 1 versus 95.3% Era 2, p=0.04). There were trends towards higher incidences of allograft pancreatectomy (9.5% Era 1 versus 3.9% Era 2, p=0.08) and pancreas thrombosis (8.7% Era 1 versus 3.1% Era 2, p=0.07) in Era 1 compared to Era 2. Length of hospital stays for the transplant admission (11.8±7.3 days Era 1 versus 9.0±4.5 days Era 2, p=0.001) was lower in Era 2. Although four-year patient and kidney GSRs at the 4-year follow-up time point were significantly higher in Era 2 compared to Era 1 according to chi-square (Table 3), Kaplan-Meier analysis showed no difference in patient survival (Figure 1, Log rank p=0.39) and only a trend toward improved kidney GSRs (Figures 2 and 3, Log rank p=0.08 for overall GSR and p=0.15 for death-censored GSR) in Era 2 compared to Era 1. Four year pancreas GSRs (p=0.002 overall and p=0.02 death-censored) as well as Kaplan-Meier GSRs (Figures 4 and 5, Log rank p=0.004 overall and p=0.005 death-censored) were significantly higher in Era 2 compared to Era 1. In part because of longer follow-up, the incidence of DWFGs (both grafts functioning at time of death) was higher in Era 1 (19.0% Era 1 versus 7.8% Era 2, p=0.001). However, the four-year incidences of DWFGs (2.4% Era 1 versus 1.6% Era 2, p=0.68) were not different.

Table 3: Outcomes According to Era

*DCGS – Death-Censored Graft Survival; *DWFG – Death with Functioning Graft.

In a Cox regression analysis of risk factors for death-censored kidney graft survival (Table 4), in univariate analysis longer kidney CIT and black donor race were risk factors for graft loss whereas male donor and older recipient age were associated with improved graft survival. Although Era 2 had a Hazard Ratio (HR) of 0.65 for kidney graft survival compared to Era 1, this was not significant. In the multivariate analysis, black donor race continued to be a risk factor for graft loss whereas male donor and older recipient age were protective against censored graft loss. Table 5 displays  the risk factor analysis for death-censored pancreas graft survival. In univariate analysis, Era 2 (compared to Era 1), alemtuzumab induction, and systemic venous drainage were each associated with improved graft survival whereas longer pancreas CIT was associated with graft loss. In the multivariate analysis, only alemtuzumab induction therapy was significant for improved graft survival (HR=0.52, 95% CI 0.30-0.91).

Figure 1: Patient survival following SPKT according to Era. No significant differences were noted.

Figure 2: Overall kidney graft survival following SPKT according to Era. No significant differences were noted even though four-year GSRs were higher in Era 2.

DISCUSSION

Although PTx may be the most effective form of achieving sustained endogenous insulin delivery, it is considered a radical approach to a metabolic disease because of surgical complexity and susceptibility to ischemia-reperfusion injury [1,2]. Prior to the new millennium, the “developmental” phase of PTx was characterized by refinements in surgical techniques in response to a myriad of surgical complications [26 28]. The goal of PTx is to safely transplant functioning islet cells, which represent about 2% of the total human pancreas mass. Ironically, surgical complications arise from the remaining 98% of the non-endocrine portions of the gland and remain important because they can lead to graft loss, morbidity, mortality, and increased health care costs [26-31]. 

Figure 3: Death-censored kidney graft survival following SPKT according to Era. No significant differences were noted even though four-year GSRs were higher in Era 2.

Figure 4: Overall pancreas graft survival following SPKT according to Era. The pancreas GSR was significantly higher in Era 2.

Figure 5: Death-censored pancreas graft survival following SPKT according to Era. The pancreas GSR was significantly higher in Era 2.

REFERENCES

1. Fridell JA, Stratta RJ, Gruessner AC. Pancreas transplantation: Current challenges, considerations, and controversies. J Clin Endo Metab. 2023; 108: 614-623.
2. Gruessner AC, Gruessner RW. Declining numbers of pancreas transplantations but significant improvements in outcome. Transplant Proc. 2014; 46: 1936-1937.
3. Larsen JL. Pancreas transplantation: Indications and consequences. Endocrine Reviews. 2004; 25: 919-946.
4. McCune K, Owen-Simon N, Dube GK, Ratner LE. The best insulin delivery is a human pancreas. Clin Transplant. 2023; 37: e14920.
5. Sollinger HW, Odorico JS, Becker YT, D’Alessandro AM, Pirsch JD. One thousand simultaneous pancreas-kidney transplants at a single center with 22-year follow-up. Ann Surg. 2009; 250: 618-630.
6. Fridell JA, Niederhaus S, Curry M, Urban R, Fox A, Odorico J. The survival advantage of pancreas after kidney transplant. Am J Transplant. 2019; 19: 823-830.
7. Dunn TB. Life after pancreas transplantation: reversal of diabetic lesions. Curr Opin Organ Transplant. 2014; 19: 73-79.
8. Stratta RJ, Gruessner AC, Odorico JS, Fridell JA, Gruessner RWG. Pancreas transplantation: An alarming crisis in confidence. Am J Transplant. 2016; 16: 2556-2562.
9. Gruessner AC, Gruessner RWG. The 2022 International Pancreas Transplant Registry Report-A Review. Transplant Proc. 2022; 54: 1918-1943.
10. Organ Procurement and Transplantation Network - National Data. 2024.
11. Updated International Pancreas Transplant Registry (IPTR) data, Angelika Gruessner. 2024.
12. Fridell JA, Rogers J, Stratta RJ. The pancreas allograft donor: Current status, controversies, and challenges for the future. Clin Transplant. 2010; 24: 433-449.
13. Humar A, Kandaswamy R, Drangstveit MB, Parr E, Gruessner AG, Sutherland DE. Prolonged preservation increases surgical complications after pancreas transplants. Surgery. 2000; 127: 545-551.
14. Rudolph EN, Dunn TB, Sutherland DER, Kandaswamy R, Finger EB. Optimizing outcomes in pancreas transplantation: Impact of organ preservation time. Clin Transplant. 2017; 31: e13035.
15. Rogers J, Farney AC, Orlando G, et al. Evolving trends in pancreas transplantation: The Wake Forest Experience. Wake Forest J Sci Med. 2016; 2: 57-66.
16. Farney AC, Doares W, Rogers J, Singh R, Hartmann E, Hart L, et al. A Randomized Trial of Alemtuzumab versus Antithymocyte Globulin Induction in Renal and Pancreas Transplantation. Transplantation. 2009; 88: 810-819.
17. Stratta RJ, Rogers J, Orlando G, Farooq U, Al-Shraideh Y, Doares W, et al. Depleting antibody induction in simultaneous pancreas- kidney transplantation: A prospective single center comparison of alemtuzumab versus rabbit anti-thymocyte globulin. Exp Opin Biol Therapy. 2014; 14: 1723-1730.
18. Farney AC, Singh RP, Hines MH, Rogers J, Hartmann EL, Reeves- Daniel A, et al. Experience in renal and extrarenal transplantation with donation after cardiac death donors with selective use of extracorporeal support. J Am Coll Surg. 2008; 206: 1028-1037.
19. Stratta RJ, Rogers J, Farney AC, Orlando G, El-Hennawy H, Gautreaux MD, et al. Pancreas transplantation in C-peptide positive patients: Does “type” of diabetes really matter?. J Am Coll Surg. 2015; 220: 716-727.
20. Gurram V, Gurung K, Rogers J, et al. Do pretransplant C-peptide levels influence outcomes in simultaneous pancreas-kidney transplantation? A matched case-control study. Clin Transplant. 2021; 35: e14498.
21. Rogers J, Farney AC, Orlando G, Farooq U, Al-Shraideh Y, Stratta RJ. Pancreas transplantation with portal venous drainage with an emphasis on technical aspects. Clin Transplant. 2014; 28: 16-26.
22. Fridell JA, Powelson JA, Sanders C, Ciancio G, Burke GW 3rd, StrattaR. Preparation of the pancreas allograft for transplantation. Clin Transplant. 2011; 25: E103-E112.
23. Stratta RJ, Farney AC, Orlando G, Farooq U, Al-Shraideh Y, El- Hennawy H, Rogers J. Pancreas transplantation with systemic- enteric drainage when portal-enteric drainage is contraindicated. Pancreat Disord Ther. 2014; 4: 1-6.
24. Fridell JA, Shah A, Milgrom ML, Goggins WC, Leapman SB, Pescovitz MD. Ipsilateral Placement of Simultaneous Pancreas and Kidney Allografts. Transplantation. 2004; 78: 1074-1076.
25. Farney AC, Rogers J, Stratta RJ. Pancreas Graft Thrombosis: Causes, Prevention, Diagnosis, and Intervention. Curr Opin in Organ Transplant. 2012; 17: 87-92.
26. Troppmann C, Gruessner AC, Dunn DL, Sutherland DE, Gruessner RW. Surgical complications requiring early relaparotomy after pancreas transplantation: a multivariate risk factor and economic impact analysis of the cyclosporine era. Ann Surg. 1998; 227: 255- 268.
27. Humar A, Kandaswamy R, Granger D, Gruessner RWG, Gruessner AC, Sutherland DER. Decreased surgical risks of pancreas transplantation in the modern era. Ann Surg. 2000; 231: 269-275.
28. El-Hennawy H, Stratta RJ, Smith F. Exocrine drainage in vascularized pancreas transplantation in the new millennium. World J Transplant. 2016; 6: 255-271.
29. Redfield RR, Rickels MR, Naji A, Odorico JS. Pancreas Transplantationin the Modern Era. Gastroenterol Clin N Am. 2016; 45: 145-166.
30. Finger EB, Radosevich DM, Dunn TB, Chinnakotla S, Sutherland DE, Matas AJ, et al. A composite risk model for predicting technical failure in pancreas transplantation. Am J Transplant. 2013; 13: 1840-1849.
31. Cohn JA, Englesbe MJ, Ads YM, Paruch JL, Pelletier SJ, Welling TH, et al. Financial implications of pancreas transplant complications: a business case for quality improvement. Am J Transplant. 2007; 7: 1656-1660.
32. Singh N, Stratta RJ. Poor utilization of deceased donor pancreata in the United States: Time for action. Clin Transplant. 2023; 37: e15148