Short term and long term survival rate and risk factors of graft rejection after deceased donor kidney transplantation: a systematic review and meta-analysis

Abstract

The purpose of the current meta-analysis is to determine the short-term and long-term graft and patient survival after deceased donor (DD) transplantation, as well as to determine prognostic factors. 

Method : Articles published until March 2019 in PubMed, Scopus, and Google Scholar databases, reporting short-term and/or long term graft and patient survival were searched. In addition to this, we included articles that analyzed the hazard ratio (HR) of graft rejection and/or patient death caused by DD related risk factors. The summary measures of this study included the survival rate, the HR of graft rejection, and patient death in response to DD related risk factors. 

This study, which is the first comprehensive meta-analysis of graft and patient survival rates after transplantation from the deceased donor, showed that overall short and long-term survival of graft and patient is desirable. In addition to this, it confirms that ECD and DCD recipients have a lower graft survival rate than standard donors.

Background

Among renal replacement therapies for patients with End-Stage Renal Disease (ESRD), kidney transplantation is the preferred treatment, due to improved quality of life, increased survival, and reduced financial costs (1, 2). The most critical risk factors that cause kidney transplant rejection have been reported in various studies. Among them are poor early graft function (3, 4), delayed graft function (5, 6), mismatch HLA (7, 8), blood group incompatibility (9), cold ischemia time (10), acute rejection (6, 11), age (12, 13), donor-recipient sex mismatch (14, 15), BMI of donor and recipient (16, 17), and immunosuppressive regime (18, 19). Increasing the incidence of ESRD in developed and developing countries on the one hand and a long waiting list for transplantation, on the other hand, has led to the revision and development of organ transplantation from the deceased donor (DD) (20, 21). Therefore, the type of donor (living or deceased) has been investigated in many studies individually as an essential factor affecting transplantation survival (22–24). The adequacy of kidny transplantation from a DD is controversial according to the findings of various studies. While some studies have shown that the kidney donated from the DD is less likely to survive due to immunological and hormonal changes compared to living donors (25, 26), other studies have reported desirable results from the function of the DD renal transplantation (27, 28). Even though various studies have been carried out in order to determine the effect of cadaveric donors on renal transplantation rejection, these estimations vary from one study to another, and some cases have rejected the results of other studies. The current meta-analysis was performed to determine the short and long-term survival rate of kidney transplantation from the deceased donor, as well as to determine the factors influencing it, using all of the observational and registry-based studies.

Method

In this systematic review and meta-analysis, all prospective, retrospective, and registry-based studies that examined the survival rate of kidney transplantation from DDs all around the world were included without any restriction.

Inclusion criteria for studies

All of the stages of this study were performed under PRISMA guidelines. The criteria for including studies were: study design (prospective, retrospective or registry-based studies), report of patient or graft survival rate, or report of hazard ratio (HR) for determination of the effect of DD related factors on graft rejection. Articles that did meet at least two of these inclusion criteria were included. The outcome measures included the one-year, five-year or ten-year patient or kidney transplantation survival rates from DD and risk factors of rejection related to characteristics of DD such as age, sex, weight, history of chronic disease, and type of DD which includes donation after brain death (DBD), donation after circulatory death (DCD), expanded-criteria donors (ECDs) or standard-criteria donors (SCDs).

Search strategy

 In this study, using the search strategy shown in Table 1, we searched PubMed and Scopus databases to obtain relevant studies until March 2019. In order to obtain more articles and to ensure proper search of databases, references of selected articles were reviewed.

Table 1. Search strategy in Scopus and PubMed until 4/2019

Data extraction and statistical methods

To ensure the correct selection of articles in terms of their pertinence to the research topic and accordance with the inclusion criteria, two researchers (K.A. and M.S.) independently reviewed the articles. The names of the authors, the journals, and their results were not hidden from the reviewers. The Kappa percentage of the inter reviewer agreement was 85%. The variables taken in consideration in this review included the name of the first author, year of publication, country of the study, the mean age of the DD, gender, study design, weight of DD, type of DD (DBD or DCD), criteria (ECD or SCD), and history of chronic disease. STROBE checklist for cohort studies was used to assess the quality in terms of methodology and reporting. To determine the heterogeneity of the studies, Cochran's Q-test of heterogeneity was used at a 5% confidence level. Survival rates vary between zero and one and have no negative values; for this reason, all of the studies are located at the right side of the vertical line, and publication bias cannot be determined. The summary measures of this study, including the survival rate, the HR of graft rejection, and patient death in the presence of DD related risk factors, were calculated along with 95% confidence intervals (CIs) to perform a two-tailed test.

Data analysis was done using the Stata (version 11, StataCorp, College Station, Texas) and applying the random effects model at a 95% confidence level.

Results

In the first step, we identified 16968 articles, after removing duplicate papers, and reviewed the title and abstract of 10786 them. Secondly, considering the exclusion criteria, we excluded 9986 articles and studied 923 full-text articles. According to our objectives and quality assessment of selected articles, 845 papers were withdrawn, and finally, 75 articles were included in the final analysis (Fig 1). Table 2 represents article information including author, country, research design, donor sex, male donor (%), donor mean age (year) ± SE, type of the deceased donor (DBD or DCD), criteria (ECD or SCD), donor BMI, sample size, patient survival rate, and graft survival rate.

Table 2. Characteristics of the studies included in this meta-analysis

DBD: donor after brain death, DCD: donor after cardiac death, ECD: expanded-criteria donor, SCD: Standard-criteria donor, SS: sample size, R.cohort: retrospective cohort

Descriptive of included articles

In this meta-analysis, data of 249369 patients from 29 countries were analyzed. The largest sample size was from the Gondos et al. (58) study in Germany in 2013. They used the registry data to report the graft survival of 55778 patients of different ethnicities, such as European, African, African- American, and Hispanic. The smallest sample size belonged to the Nakamura et al. (87) study in Japan, which had examined 16 kidney transplants survival from cadaver donors. Thirteen studies were registry-based (35, 39, 40, 45, 50, 55, 58, 65, 76, 85, 90, 98, 102) and others were retrospective case studies. Table 3 shows the most important causes of deaths in the deceased donor reported by twenty-six articles. Trauma and cerebrovascular were the most common causes of death.

Table 3. Cause of donor death in the studies included in this meta-analysis

Graft and patient survival rate

The one-year graft survival rate was 90% (95% CI: 89% to 92%). Two, three, five and ten-year graft survival rates were 80% (95% CI: 90% -70%), 82% (95% CI: 75% -88%), 76% (95% CI: 73% -79%) and 52% (48% -60%), respectively (Fig 2). One-year patient survival rate was 95% (95% CI: 94% -96%). This rate decreased to 83% (95% CI: 91% -74%), 85% (95% CI: 80% -89%), and 73% (95% CI: 57% -89%) after three, five, and ten years, respectively (Fig 3).  Regardless of Savdia et al. (103) 10-year patient survival rate increased to 84%, but there were no significant changes in short-term patient and graft survival.

In figures 4, 5 and 6 the graft and patients survival based on the type of deceased donor (DCD and DBD) is shown. The rate of one-year graft and patient survival in DCD recipients were 87% (95% CI: 83%- 92%) and 95% (95% CI: 95%- 99%), respectively. One, five and fifteen-year graft survival rates in transplant recipients from DBD donor were 92% (95% CI: 88%- 96%), 79% (95% CI: 76%- 83%), and 65% (95% CI: 56%- 73%), respectively. One-year patient survival rate of transplant recipients from DBD was 94% (95% CI: 97%- 91%) and five-year survival rate was 90% (95% CI: 85% -95%). One, three and five-year graft survival rates in ECD recipients were 88% (95% CI: 85%- 91%), 78% (95% CI: 70%- 87%), and 68% (95% CI: 61), respectively (Fig 7). In the case of SCDs recipients one-year and three-year patient survival rate were respectively 93% (95% CI: 91%- 94%) and 80% (95% CI: 78%- 83%) (Fig 8). Also one-year patient survival rate in SCD kidneys was 96% (95% CI: 94%- 97%). In the same category, three and five-year survival rates were 86% (95% CI: 79%- 92%) and 87% (95% CI: 79%- 95%), respectively (Fig 9). The one and five-year patients survival in SCDs were 96% (95% CI: 93%- 98%) and 92% (95% CI: 86%- 98%), respectively (Fig 10).

Hazard Ratio

Although most of the studies have found that the HR of graft rejection and patient death risk factors are attributed to the recipient, few studies have been performed to determine the HR of risk factors associated with the deceased donor. Therefore, only three factors, including the age of the donor, ECD kidney and male sex, were included for analysis. HR of age of deceased donor was 1.01 (95% CI: 0.99 to 1.04) for graft rejection and patient death (Fig 11). ECD kidney was a risk factor for graft rejection (HR: 1.14, 95% CI: 1.00, 1.27) (Fig 12). Male sex was a significant protective factor in patient survival rate. According to the results shown in graph 13, the risk of death in men had an HR of 0.86 (95% CI: 75, 97). However, the male sex does not affect the survival of the kidney transplant (HR=0.95, 95% CI: 0.83, 1.06) (Fig 13).

Discussion

In this systematic review and meta-analysis, we estimated the graft and patient survival after kidney transplantation form DD for the first time. Currently, the demand for kidney transplantation is much higher than the number of kidney donors. While in response to this need, kidney donation from DDs has been developed around the world, concerns and inconsistencies about the graft and patient survival after transplantation from these donors have also increased. Our findings showed that one-year kidney transplant and patient survival rates were respectively 90% and 95%. According to Fig. 1, Boer et al. (88) in 2002 and Savdie et al. (95) in 1982 reported the lowest rate of one-year graft survival (56%) and patient survival (79%). On the other hand, Mukherjee et al. (42) in 2018 reported the highest rate of one-year graft survival from 92 deceased donor transplantation in India. Also, Kang et al. (70) and Taski et al. (79) in respectively 2018 and 2014, reported the highest one-year patient survival rate. As mentioned earlier, no-meta-analysis has been performed to quantify kidney transplant and patient survival rate from the deceased donor. Thus the comparison of our results is limited. Noordzij et al. (104) reported that from 2005 to 2009, one-year kidney transplant and patient survival rate from DD in 12 European countries were 90.4% and 95.9%, respectively. Additionally, five-year kidney transplant and patient survival rate between 2002 and 2006 were 77.2% and 86.7%, respectively. As shown in Figs. 1 and 2, one-year graft survival is more variable compared to one-year patient survival. This issue has also been seen in long-term graft survival. It is crucial to consider the potential factors that might generate these differences and wide range of the reported one-year graft survival in the included study:

1. Immunosuppressive regime: Recent advances in the immunosuppressive protocols significantly reduced the rate of acute rejection from 60–35% (105, 106). With the use of Imuran and Prednisolone since 1960, the one-year survival rate of living donors has increased from 75–90% (107). In 1995, Cellcept was added to the treatment protocol. This immunosuppressive drug not only increased long-term kidney transplant survival rate from 15–20% but also reduced the rate of acute transplant rejection (108). Therefore, included articles from the 1980s and 1990s will increase the variability of short- and long-term graft survival and patient survival.

2: Deceased donor expanded criteria: Although some of the studies have reported kidney transplant survival by ECD or SCD, pooled reporting of graft survival in many other studies can be a source of heterogeneity in survival reports. Our findings showed that the one-year survival rate of a kidney transplant from SCD was three percent greater than ECD. This difference in the five-year patient survival rate increased to five percent. A systematic review study by Pascual et al. (109), which examined transplant outcomes from ECDs, reported no difference in graft and patient survival rates in comparison with SCDs according to single-center observational studies. In contrast, multicenter and registry-based studies found lower one-year to fifteen-year graft and patient survival in ECD recipients. Shortage of organ transplantation from living-related and living-unrelated donors led to the development of accepted standards for cadaveric transplantation and increased kidney transplant resources. In all of the articles that determined kidney transplant survival and patient’s survival based on ECD and SCD included in this meta-analysis, ECD donors were: DDs older than 60 years and DDs 50 to 59 years old who met two of the following criteria: (1) history of hypertension, (2) cerebrovascular accident as a cause of brain death, and (3) final pre-procurement serum creatinine (SCr) level > 1.5 mg/dL. Also, a kidney that has a relative risk of rejection higher than 1.7 compared to the age group of 10 to 39 without hypertension and high creatine is considered an ECD kidney. One of our inclusion criteria was the HR report for ECD compared to SCD. As shown in graph 12, only four studies, using Cox regression, measured the HR of graft loss for ECD. Our findings showed that HR of graft rejection for ECD donors was 14% higher than the standard group. OPTN/SRTR 2017 Annual Data Report (110) showed a dramatic increase in the number of deceased donation, and this increase in the age group of 18 to 34 years is more than other groups. Their report shows that despite a deceased donor increase, 18% have been discarded due to older age and diabetes. In summary, although ECD is associated with an increased risk of graft rejection in comparison with SCDs, the five-year increase in life expectancy of ECDs compared to dialysis patients makes the ECD kidney a better choice for ESRD treatment (111).

DBD vs. DCD

Although in 2009, only 10% of kidney transplants in the USA were DCD, this number increased to 15.8% in 2011 and about 20% in 2017 (112, 113). Even though the development of DCD transplantation policy and the importance of awareness of the outcomes of DCD recipients, one of the limitations of some of the articles in our study was that they did not report graft and patient survival according to the type of deceased donor and cause of death. We showed that one-year graft survival in DCD recipients was 5% lower than DBD recipients, whereas no differences were observed in one-year patient survival. Prolonged warm ischemia time, higher risk of ischemia-reperfusion injury,(114, 115), inferior quality of vessels, and/or endothelial activation (102) have been presented as the most important causes of lower graft survival in DCD recipients.

In one of the most extensive cohort studies in the UK, after adjusting the age of recipient and donor as well as cold ischemic time, the HLA mismatch level, number of HLA mismatches, HLA-DR mismatches, machine perfusion, and warm ischemic time showed no influence on graft rejection from DCD. According to the findings of this cohort, the age of the recipient and donor were the only factors affecting DCD graft rejection (116).

Although the incidence of DFG after DCD has been reported 27–73% in different studies (116–118), the practical factors such as donor and recipient age, cold ischemic time, and HLA-matching, make the result of kidney transplants from DCD acceptable compared to dialysis.

Conclusion

The findings of our study, which is the first comprehensive meta-analysis of graft and patient survival of the deceased donor, using all single-center, multicenter, and registry-based studies, show that overall, short-term and long-term graft and patient survival is desirable after kidney transplantation from DD. Our findings confirm that ECD recipients have lower graft survival rates than SCDs, and despite the shorter one-year survival rate in DCDs, the short-term patient survival rate is similar to DBDs. We also concluded that men had better survival than women but did not differ in graft survival.

Abbreviations

DD: deceased donor, DCD: donation after circulatory death ,DBD: donation after brain death, EDCs: expanded-criteria donors, SCDs: standard-criteria donors ,ESRD: End-Stage Renal Disease,HR: hazard ratio

Declarations

Acknowledgements: N/A

Authors’ contributions: MS conceived and designed the study. M-S MK-A were responsible for the collection of data and performing the statistical analysis and manuscript preparation. M-S and MK-A were responsible for checking the data. All authors were responsible for drafting the manuscript, and read and approved the final version.

Funding:N/A

Ethics approval and consent to participate: N/A

Competing interests: The authors declare that they have no competing interests.

References

1. Tonelli M, Wiebe N, Knoll G, Bello A, Browne S, Jadhav D, et al. Systematic review: kidney transplantation compared with dialysis in clinically relevant outcomes. American journal of transplantation : official journal of the American Society of Transplantation and the American Society of Transplant Surgeons. 2011;11(10):2093-109.
2. Wolfe RA, Ashby VB, Milford EL, Ojo AO, Ettenger RE, Agodoa LY, et al. Comparison of mortality in all patients on dialysis, patients on dialysis awaiting transplantation, and recipients of a first cadaveric transplant. The New England journal of medicine. 1999;341(23):1725-30.
3. Pita-Fernandez S, Valdes-Canedo F, Seoane-Pillado T, Lorenzo-Aguiar D, Oliver-Garcia J, Blanco-Castro N, et al. Influence of Early Graft Function After Renal Transplantation and Its Impact on Long-Term Graft and Patient Survival. Transplant Proc. 2010;42(8):2856-8.
4. Ishimura T, Muramaki M, Kishikawa H, Miyake H, Tanaka K, Nishimura K, et al. The impact of donor factors on early graft function in kidney transplantation from donation after cardiac death. Transplant Proc. 2014;46(4):1064-6.
5. Hassanain M, Tchervenkov J, Cantarovich M, Metrakos P, Paraskevas S, Keith D, et al. Delayed graft function has an equally bad impact on deceased donor renal graft survival in both standard criteria donors and expanded criteria donors. Transplant Proc. 2009;41(1):133-4.
6. Lim WH, Johnson DW, Teixeira-Pinto A, Wong G. Association between Duration of Delayed Graft Function, Acute Rejection, and Allograft Outcome after Deceased Donor Kidney Transplantation. Transplantation. 2019;103(2):412-9.
7. Reindl-Schwaighofer R, Heinzel A, Kainz A, van Setten J, Jelencsics K, Hu K, et al. Contribution of non-HLA incompatibility between donor and recipient to kidney allograft survival: genome-wide analysis in a prospective cohort. Lancet (London, England). 2019;393(10174):910-7.
8. Vinson AJ, Kiberd BA, Davis RB, Tennankore KK. Nonimmunologic Donor-Recipient Pairing, HLA Matching, and Graft Loss in Deceased Donor Kidney Transplantation. Transplantation direct. 2019;5(1):e414.
9. Haberal M, Demirag A, Moray G, Karakayali H, Akkoc H, Turan M, et al. Graft survival rates in kidney transplant recipients of different blood groups. Transplant Proc. 1998;30(3):741-3.
10. Schnuelle P, Gottmann U, Koppel H, Brinkkoetter PT, Krzossok S, Weiss J, et al. Comparison of early renal function parameters for the prediction of 5-year graft survival after kidney transplantation. Nephrology, dialysis, transplantation : official publication of the European Dialysis and Transplant Association - European Renal Association. 2007;22(1):235-45.
11. Domański L, Kłoda K, Kwiatkowska E, Borowiecka E, Safranow K, Drozd A, et al. Effect of delayed graft function, acute rejection and chronic allograft dysfunction on kidney allograft telomere length in patients after transplantation: A prospective cohort study. BMC Nephrology. 2015;16(1).
12. Emiroglu R, Yagmurdur MC, Karakayali F, Haberal C, Ozcelik U, Colak T, et al. Role of donor age and acute rejection episodes on long-term graft survival in cadaveric kidney transplantations. Transplant Proc. 2005;37(7):2954-6.
13. Ko EJ, Yang J, Ahn C, Kim MS, Han DJ, Kim SJ, et al. Clinical outcomes of kidney transplantation in older end-stage renal disease patients: A nationwide cohort study. Geriatr Gerontol Int. 2019.
14. Tillmann FP, Quack I, Woznowski M, Rump LC. Effect of recipient-donor sex and weight mismatch on graft survival after deceased donor renal transplantation. PLoS ONE. 2019;14(3).
15. Noel S, Desai NM, Hamad AR, Rabb H. Sex and the single transplanted kidney. J Clin Invest. 2016;126(5):1643-5.
16. Arshad A, Hodson J, Chappelow I, Inston NG, Ready AR, Nath J, et al. The impact of donor body mass index on outcomes after deceased kidney transplantation – a national population-cohort study. Transplant International. 2018;31(10):1099-109.
17. Kurnatowska I, Małyska A, Wysocka K, Mazur K, Krawczyk J, Nowicki M. Long-term effect of body mass index changes on graft damage markers in patients after kidney transplantation. Annals of Transplantation. 2016;21:626-31.
18. Guerra AA, Jr., Cesar CC, Cherchiglia ML, Andrade EI, de Queiroz OV, Silva GD, et al. Cyclosporine versus tacrolimus in immunosuppressive maintenance regimens in renal transplants in Brazil: survival analysis from 2000 to 2004. The Annals of pharmacotherapy. 2010;44(1):192-201.
19. Djamali A, Pietrangeli CE, Gordon RD, Legendre C. Potential of emerging immunosuppressive strategies to improve the posttransplant cardiovascular risk profile. Kidney international Supplement. 2010(118):S15-21.
20. van Walraven C, Austin PC, Knoll G. Predicting potential survival benefit of renal transplantation in patients with chronic kidney disease. CMAJ. 2010;182(7):666-72.
21. Goldberg D, Kallan MJ, Fu L, Ciccarone M, Ramirez J, Rosenberg P, et al. Changing Metrics of Organ Procurement Organization Performance in Order to Increase Organ Donation Rates in the United States. American journal of transplantation : official journal of the American Society of Transplantation and the American Society of Transplant Surgeons. 2017;17(12):3183-92.
22. Cheung CY, Chan HW, Chan YH, Chau KF, Li CS. Impact of delayed graft function on renal function and graft survival in deceased kidney transplantation. Hong Kong medical journal = Xianggang yi xue za zhi. 2010;16(5):378-82.
23. Ayar Y, Ersoy A, Ocakoglu G, Yildiz A, Oruc A, Soyak H, et al. Risk Factors Affecting Graft and Patient Survivals After Transplantation From Deceased Donors in a Developing Country: A Single-Center Experience. Transplant Proc. 2017;49(2):270-7.
24. Magott-Procelewska M, Madziarska K, Boratynska M, Chudoba P, Lepiesza A, Mazanowska O, et al. Kidney Transplantation From Old Deceased Donors: Impact of Uric Acid Level-A Quarter-Century of Experience in One Transplant Center. Transplant Proc. 2018;50(6):1701-4.
25. Zhang H, Wei Y, Liu L, Li J, Deng R, Xiong Y, et al. Different Risk Factors for Graft Survival Between Living-Related and Deceased Donor Kidney Transplantation. Transplant Proc. 2018;50(8):2416-20.
26. Lee S, Kim J, Shin M, Kim E, Moon J, Jung G, et al. Comparison of outcomes of living and deceased donor kidney grafts surviving longer than 5 years in Korea. Transplant Proc. 2010;42(3):775-7.
27. Park YH, Min SK, Lee JN, Lee HH, Jung WK, Lee JS, et al. Comparison of survival probabilities for living-unrelated versus cadaveric renal transplant recipients. Transplant Proc. 2004;36(7):2020-2.
28. Chkhotua AB, Klein T, Shabtai E, Yussim A, Bar-Nathan N, Shaharabani E, et al. Kidney transplantation from living-unrelated donors: comparison of outcome with living-related and cadaveric transplants under current immunosuppressive protocols. Urology. 2003;62(6):1002-6.
29. Kute VB, Vanikar AV, Patel HV, Shah PR, Gumber MR, Engineer DP, et al. Outcome of renal transplantation from deceased donors: Experience from developing country. Renal failure. 2014;36(8):1215-20.
30. Auglienė R, Dalinkevičienė E, Kuzminskis V, Jievaltas M, Peleckaitė L, Gryguc A, et al. Factors influencing renal graft survival: 7-Year experience of a single center. Medicina. 2017;53(4):224-32.
31. Cardinal H, Hebert M-J, Rahme E, Houde I, Baran D, Masse M, et al. Modifiable factors predicting patient survival in elderly kidney transplant recipients. Kidney international. 2005;68(1):345-51.
32. Centellas-Pérez F, Tébar A, Llamas F, Lorenzo I, Sarduy P, Martínez-Díaz M, et al., editors. Analysis of Kidney Donation and Its Relationship With Graft Failure of the Recipient at 1 Year. Transplant Proc; 2019: Elsevier.
33. Cho A, Jang H, Lee J, Huh W, Kim Y-G, Oh H, et al., editors. Comparison of Cadaveric Kidney Transplantation From In-center and External Center Donors. Transplant Proc; 2014: Elsevier.
34. Cho YW, Terasaki PI, Cecka JM. High kidney graft survival rates using non-heart-beating trauma donors. Transplant Proc. 1998;30(7):3795-6.
35. Czerwiński J, Antoszkiewicz K, Grygiel K, Karpeta E, Dudkiewicz M, Lewandowska D, editors. National Transplants Registry in Poland: early and long-term results of organ transplantations in the years 1998 to 2014. Transplant Proc; 2016: Elsevier.
36. Kyllönen LE, Salmela KT, Eklund BH, Halme LE, Höckerstedt KA, Isoniemi HM, et al. Long‐term results of 1047 cadaveric kidney transplantations with special emphasis on initial graft function and rejection. Transplant International. 2000;13(2):122-8.
37. Laging M, Kal‐van Gestel JA, van de Wetering J, IJzermans JN, Weimar W, Roodnat JI. The relative importance of donor age in deceased and living donor kidney transplantation. Transplant International. 2012;25(11):1150-7.
38. Lionaki S, Kapsia H, Makropoulos I, Metsini A, Skalioti C, Gakiopoulou H, et al. Kidney transplantation outcomes from expanded criteria donors, standard criteria donors or living donors older than 60 years. Renal failure. 2014;36(4):526-33.
39. McDonald SP, Russ GR. Survival of recipients of cadaveric kidney transplants compared with those receiving dialysis treatment in Australia and New Zealand, 1991–2001. Nephrology Dialysis Transplantation. 2002;17(12):2212-9.
40. Moers C, Kornmann NS, Leuvenink HG, Ploeg RJ. The influence of deceased donor age and old-for-old allocation on kidney transplant outcome. Transplantation. 2009;88(4):542-52.
41. Mok IY, Kee T, Goh A. Ten-year outcomes of kidney transplants at the Singapore General Hospital. Proceedings of Singapore Healthcare. 2012;21(2):95-101.
42. Mukherjee D, Nair RK, Sharma S, Datt B, Rao A, Prakash S. Cadaveric renal transplantation: Our experience at a tertiary care centre in India. Medical Journal Armed Forces India. 2018.
43. Nagaraja P, Roberts GW, Stephens M, Horvath S, Fialova J, Chavez R, et al. Influence of delayed graft function and acute rejection on outcomes after kidney transplantation from donors after cardiac death. Transplantation. 2012;94(12):1218-23.
44. Newstead CG, Dyer PA. The influence of increased age and age matching on graft survival after first cadaveric renal transplantation. Transplantation. 1992;54(3):441-3.
45. Noppakun K, Ingsathit A, Pongskul C, Premasthian N, Avihingsanon Y, Lumpaopong A, et al. A 25‐year experience of kidney transplantation in T hailand: Report from the T hai Transplant Registry. Nephrology. 2015;20(3):177-83.
46. O’Kelly P, Giblin L, Spencer S, Donohoe J, Walshe J, Little D, et al. Outcomes of adult cadaveric renal transplantation in Ireland 1986 to 2001. Irish journal of medical science. 2005;174(1):42.
47. Pessione F, Cohen S, Durand D, Hourmant M, Kessler M, Legendre C, et al. Multivariate analysis of donor risk factors for graft survival in kidney transplantation. Transplantation. 2003;75(3):361-7.
48. Salmela K, Kyllonen L, editors. Early cyclosporine concentration as predictor of graft survival in cadaveric renal transplantation. Transplant Proc; 2001: Elsevier Science Publishing Company, Inc.
49. Saunders PH, Banowsky LH, Reichert DF. Survival of cadaveric renal allografts in Hispanic as compared with Caucasian recipients. Transplantation. 1984;37(4):359-62.
50. Savoye E, Tamarelle D, Chalem Y, Rebibou JM, Tuppin P. Survival benefits of kidney transplantation with expanded criteria deceased donors in patients aged 60 years and over. Transplantation. 2007;84(12):1618-24.
51. Sener A, Schweitzer EJ, Munivenkatappa R, Cooper M, Bartlett ST, Philosophe B, et al. Deceased-donor renal transplantation in the geriatric population demonstrates equal graft survival compared with younger recipients. Transplantation. 2009;87(10):1549-54.
52. Stratta RJ, Farney AC, Orlando G, Farooq U, Al-Shraideh Y, Palanisamy A, et al. Dual kidney transplants from adult marginal donors successfully expand the limited deceased donor organ pool. Clinical transplantation. 2016;30(4):380-92.
53. Kandus A, Buturović Ponikvar J, Mlinšek G, Oblak M, Arnol M. Kidney Transplantation in Slovenia From 1970 to 2015. Therapeutic Apheresis and Dialysis. 2016;20(3):229-33.
54. Jacobi J, Rebhan D, Heller K, Velden J, Hilgers KF, Wullich B, et al. Donor acute kidney injury and short‐term graft outcome in renal transplantation. Clinical transplantation. 2014;28(10):1131-41.
55. Heylen L, Jochmans I, Samuel U, Tieken I, Naesens M, Pirenne J, et al. The duration of asystolic ischemia determines the risk of graft failure after circulatory‐dead donor kidney transplantation: A Eurotransplant cohort study. American Journal of Transplantation. 2018;18(4):881-9.
56. Heilman R, Smith M, Kurian S, Huskey J, Batra R, Chakkera H, et al. Transplanting kidneys from deceased donors with severe acute kidney injury. American Journal of Transplantation. 2015;15(8):2143-51.
57. Hamed M, Chen Y, Pasea L, Watson C, Torpey N, Bradley J, et al. Early graft loss after kidney transplantation: risk factors and consequences. American Journal of Transplantation. 2015;15(6):1632-43.
58. Gondos A, Döhler B, Brenner H, Opelz G. Kidney graft survival in Europe and the United States: strikingly different long-term outcomes. Transplantation. 2013;95(2):267-74.
59. Fujita T, Kato M, Funahashi Y, Komatsu T, Kinukawa T, Kamihira O, et al., editors. Factors having effect on graft survival in cadaveric renal transplantation. Transplant Proc; 2014: Elsevier.
60. Ferreira E, Costa J, Romaozinho C, Santos L, Macario F, Bastos C, et al. Long-Term Outcomes of Kidney Transplantation From Expanded-Criteria Deceased Donors: A Single-Center Experience. Transplant Proc. 2017;49(4):770-6.
61. Ergün M, Özdemir-van Brunschot DM, Donders RA, Hilbrands LB, Hoitsma AJ, Warlé MC. Prolonged Duration of Brain Death was Associated with Better Kidney Allograft Function and Survival: A Prospective Cohort Analysis. Annals of transplantation. 2019;24:147.
62. Emiroğlu R, Yagmurdur M, Karakayali F, Haberal C, Ozcelik U, Colak T, et al., editors. Role of donor age and acute rejection episodes on long-term graft survival in cadaveric kidney transplantations. Transplant Proc; 2005: Elsevier.
63. Aceto P, Perilli V, Luca E, Salerno M, Punzo G, Ceaichisciuc I, et al. Perioperative-, Recipient-, and Donor-Related Factors Affecting Delayed Graft Function in Kidney Transplantation. Experimental and clinical transplantation: official journal of the Middle East Society for Organ Transplantation. 2019.
64. Ali T, Dimassi W, Elgamal H, Alabassi A, Aleid H, Altalhi M, et al. Outcomes of kidneys utilized from deceased donors with severe acute kidney injury. QJM: An International Journal of Medicine. 2015;108(10):803-11.
65. Butala NM, Reese PP, Doshi MD, Parikh CR. Is delayed graft function causally associated with long-term outcomes after kidney transplantation? Instrumental variable analysis. Transplantation. 2013;95(8):1008.
66. Chen GD, Shiu‐Chung Ko D, Wang CX, Qiu J, Han M, He XS, et al. Kidney transplantation from donors after cardiac death: an initial report of 71 cases from China. American Journal of Transplantation. 2013;13(5):1323-6.
67. Farrugia D, Cheshire J, Begaj I, Khosla S, Ray D, Sharif A. Death within the first year after kidney transplantation–an observational cohort study. Transplant International. 2014;27(3):262-70.
68. Harada KM, Mandia-Sampaio EL, de Sandes-Freitas TV, Felipe CR, Park SI, Pinheiro-Machado PG, et al. Risk factors associated with graft loss and patient survival after kidney transplantation. Transplant Proc. 2009;41(9):3667-70.
69. Hwang JK, Park SC, Kwon KH, Choi BS, Kim JI, Yang CW, et al. Long-term outcomes of kidney transplantation from expanded criteria deceased donors at a single center: comparison with standard criteria deceased donors. Transplant Proc. 2014;46(2):431-6.
70. Kang SS, Park WY, Jin K, Park SB, Han S. Characteristics of Recipients With 10 or More Years of Allograft Survival in Deceased Donor Kidney Transplantation. Transplant Proc. 2018;50(4):1013-7.
71. Kim BS, Joo SH, Ahn HJ, Choi JH, Lee SH, Park HC. Outcomes of expanded-criteria deceased donor kidney transplantation in a single center. Transplant Proc. 2014;46(4):1067-70.
72. Lewandowska D, Czerwinski J, Hermanowicz M, Przygoda J, Podobinska I, Danielewicz R. Organ Donation From Elderly Deceased Donors and Transplantation to Elderly Recipients in Poland: Numbers and Outcomes. Transplant Proc. 2016;48(5):1390-3.
73. Papalia T, Greco R, Lofaro D, Maestripieri S, Mancuso D, Bonofiglio R, editors. Impact of continuous value of body mass index on graft loss in overweight patients. Transplant Proc; 2010: Elsevier.
74. Papachristou E, Provatopoulou S, Savvidaki E, Kaplanis N, Kalliakmani P, Papasotiriou M, et al., editors. Outcome of transplantation in renal allograft recipients from cadaveric donors with standard and expanded criteria: a single-center experience. Transplant Proc; 2014: Elsevier.
75. Noseworthy P, Huang M, Zaltzman J, Prasad GR, editors. Death with graft function in elderly patients after cadaveric renal transplantation: effect of waiting time. Transplant Proc; 2004: Elsevier.
76. Nakamura Y, Kihara Y, Yokoyama T, Konno O, Iwamoto H, editors. Similar Outcomes of Kidney Transplantations Using Organs From Donors After Cardiac Death and Donors After Brain Death. Transplant Proc; 2018: Elsevier.
77. Molina M, Apaza J, Monte EG, Martínez EG, Sevillano A, Marín J, et al., editors. Results of kidney transplantation from deceased donors with acute kidney injury. Transplant Proc; 2015: Elsevier.
78. Malek-Hosseini S, Razmkon A, Mehdizadeh A, Salahi H, Bahador A, Raiss-Jalali G, et al., editors. Long-term results of renal transplantation: A single-center analysis of 1200 transplants. Transplant Proc; 2006: Elsevier.
79. Tasaki M, Saito K, Nakagawa Y, Ikeda M, Imai N, Ito Y, et al., editors. 20-year analysis of kidney transplantation: a single center in Japan. Transplant Proc; 2014: Elsevier.
80. Sagban TA, Baur B, Schelzig H, Grabitz K, Duran M. Vascular challenges in renal transplantation. Ann Transplant. 2014;19:464-71.
81. Sirivongs D, Liawnoraset W, Pongskul C, Reungjui S, editors. Graft survival analysis in kidney transplantation: a 12-year experience in a Thai medical center. Transplant Proc; 2004: Elsevier.
82. Tomita Y, Tojimbara T, Iwadoh K, Nakajima I, Fuchinoue S, editors. Long-term outcomes in kidney transplantation from expanded-criteria donors after circulatory death. Transplant Proc; 2017: Elsevier.
83. Woo YM, Jardine AG, Clark AF, Macgregor MS, Bowman AW, Macpherson SG, et al. Early graft function and patient survival following cadaveric renal transplantation. Kidney international. 1999;55(2):692-9.
84. Zhang H, Wei Y, Liu L, Li J, Deng R, Xiong Y, et al., editors. Different risk factors for graft survival between living-related and deceased donor kidney transplantation. Transplantation proceedings; 2018: Elsevier.
85. Zhu D, McCague K, Lin W, Rong R, Xu M, Chan L, et al., editors. Outcome of kidney transplantation from donor after cardiac death: reanalysis of the US Mycophenolic Renal Transplant Registry. Transplant Proc; 2018: Elsevier.
86. Ko K, Kim Y, Kwon K, Kim M, Jun K, Hwang J, et al., editors. Kidney Transplantation Using Expanded-Criteria Deceased Donors: A Comparison With Ideal Deceased Donors and Non–Expanded-Criteria Deceased Donors. Transplant Proc; 2018: Elsevier.
87. Nakamura N, Tanaka M, Tsukamoto M, Shimano Y, Yasuhira M, Ashikari J, editors. Analysis of Donor Factors for Non–Heart-Beating Donors With Regard to Cadaveric Kidney Transplantation in the Western Region of Japan. Transplant Proc; 2017: Elsevier.
88. Boer WE, Van Beeumen G, Elseviers MM, Ysebaert DK, Chapelle T, Couttenye MM, et al. Decreased short‐term renal graft survival in Maghrebian recipients. Transplant international. 2002;15(5):254-8.
89. Davidson B, Du Toit T, Jones ES, Barday Z, Manning K, Mc Curdie F, et al. Outcomes and challenges of a kidney transplant programme at Groote Schuur Hospital, Cape Town: A South African perspective. PloS one. 2019;14(1):e0211189.
90. Gallinat A, Leerhoff S, Paul A, Molmenti EP, Schulze M, Witzke O, et al. Kidney transplantation from deceased donors with elevated serum creatinine. Langenbeck's archives of surgery. 2016;401(8):1211-7.
91. Lai X, Chen G, Qiu J, Wang C, Chen L. Recipient-related risk factors for graft failure and death in elderly kidney transplant recipients. PloS one. 2014;9(11):e112938.
92. McLaren A, Jassem W, Gray D, Fuggle S, Welsh K, Morris P. Delayed graft function: risk factors and the relative effects of early function and acute rejection on long‐term survival in cadaveric renal transplantation. Clinical transplantation. 1999;13(3):266-72.
93. Nemati E, Einollahi B, Pezeshki ML, Porfarziani V, Fattahi MR. Does kidney transplantation with deceased or living donor affect graft survival? Nephro-urology monthly. 2014;6(4).
94. Rezapour S, Yarmohammadi A, Tavakkoli M. One-year survival rate of renal transplant: factors influencing the outcome. Transplant Research and Risk Management. 2017;9:49.
95. Savdie E, Mahony J, Caterson R, Stewart J, Etheredge S, Storey B, et al. Long-term survival after cadaveric renal transplantation. British medical journal (Clinical research ed). 1982;285(6349):1160-3.
96. Seo CH, Ju JI, Kim MH, Jun KW, Ahn SH, Hwang JK, et al. Risk factors and long-term outcomes of delayed graft function in deceased donor renal transplantation. Annals of surgical treatment and research. 2015;89(4):208-14.
97. Dalinkevičienė E, Kuzminskis V, Petrulienė K, Skarupskienė I, Bagdonavičiūtė G, Bumblytė I. Ten-year experience of kidney transplantation at the Hospital of Kaunas University of Medicine: demography, complications, graft and patient survival. Medicina. 2010;46(8):538.
98. Molmenti EP, Alex A, Rosen L, Alexander M, Nicastro J, Yang J, et al. Recipient criteria predictive of graft failure in kidney transplantation. International Journal of Angiology. 2016;25(01):029-38.
99. Simforoosh N, Gooran S, Tabibi A, Bassiri A, Ghraati MR. Cadaver transplantation in Recent Era: Is Cadaveric Graft Survival Similar to Living Kidney Transplantation? International journal of organ transplantation medicine. 2011;2(4):167-70.
100. Yoshida K, Endo T, Saito T, Iwamura M, Ikeda M, Kamata K, et al. Factors contributing to long graft survival in non-heart-beating cadaveric renal transplantation in Japan: a single-center study at Kitasato University. Clinical transplantation. 2002;16(6):397-404.
101. Vergoulas G, Ioannidis I, Nikodimopoulou M, Miserlis G, Solonaki F, Panou E, et al. Outcomes of kidney transplantation in Greek and Albanian patients: A single centre experience. Hippokratia. 2008;12:176-80.
102. Hamed MO, Chen Y, Pasea L, Watson CJ, Torpey N, Bradley JA, et al. Early Graft Loss After Kidney Transplantation: Risk Factors and Consequences. American Journal of Transplantation. 2015;15(6):1632-43.
103. Savdie E, Mahony JF, Caterson RJ, Stewart JH, Etheredge S, Storey BG, et al. Long-term survival after cadaveric renal transplantation. British medical journal (Clinical research ed). 1982;285(6349):1160-3.
104. Noordzij M, Kramer A, Abad Diez JM, Alonso de la Torre R, Arcos Fuster E, Bikbov BT, et al. Renal replacement therapy in Europe: a summary of the 2011 ERA–EDTA Registry Annual Report. Clinical kidney journal. 2014;7(2):227-38.
105. Brenner, Rector. Clinical approach to allograft dysfunction. In: Brenner B, editor. The Kidney. 6th ed. New York: W.B Saunders Co; 2000. p. 2566-9.
106. Braunwald E. Transplantation in the treatment of renal failure. In: Braunwald E, editor. Harrison’s principles of internal medicine. 15th ed. New York: McGrow-Hill Co; 2001. p. 1567-71.
107. Brenner. Rector Immunosuppressive therapyIn: Brenner B, editor. The kidney. 6th ed. New York: W.B. Saunders Co; 2000. p. 2558-66.

108. Brenner. Rector. Mycophenolate mofetil. In: Brenner M, editor. The kidney. 6th ed. New York:: W.B. Saunders Co; 2000. p. 2563.

109. Pascual J, Zamora J, Pirsch JD. A systematic review of kidney transplantation from expanded criteria donors. American journal of kidney diseases : the official journal of the National Kidney Foundation. 2008;52(3):553-86.
110. Hart A, Smith JM, Skeans MA, Gustafson SK, Wilk AR, Castro S, et al. OPTN/SRTR 2017 Annual Data Report: Kidney. American journal of transplantation : official journal of the American Society of Transplantation and the American Society of Transplant Surgeons. 2019;19 Suppl 2:19-123.
111. Ojo AO, Hanson JA, Meier-Kriesche H, Okechukwu CN, Wolfe RA, Leichtman AB, et al. Survival in recipients of marginal cadaveric donor kidneys compared with other recipients and wait-listed transplant candidates. Journal of the American Society of Nephrology : JASN. 2001;12(3):589-97.
112. Klein AS, Messersmith EE, Ratner LE, Kochik R, Baliga PK, Ojo AO. Organ donation and utilization in the United States, 1999-2008. American journal of transplantation : official journal of the American Society of Transplantation and the American Society of Transplant Surgeons. 2010;10(4 Pt 2):973-86.
113. Matas AJ, Smith JM, Skeans MA, Lamb KE, Gustafson SK, Samana CJ, et al. OPTN/SRTR 2011 Annual Data Report: kidney. American journal of transplantation : official journal of the American Society of Transplantation and the American Society of Transplant Surgeons. 2013;13 Suppl 1:11-46.
114. Phelan PJ, Magee C, O'KELLY P, J O'BRIEN F, Little D, Conlon PJ. Immediate re‐transplantation following early kidney transplant thrombosis. Nephrology. 2011;16(6):607-11.
115. Jani A, Zimmerman M, Martin J, Lu L, Turkmen K, Ravichandran K, et al. Perfusion storage reduces apoptosis in a porcine kidney model of donation after cardiac death. Transplantation. 2011;91(2):169-75.
116. Summers DM, Johnson RJ, Allen J, Fuggle SV, Collett D, Watson CJ, et al. Analysis of factors that affect outcome after transplantation of kidneys donated after cardiac death in the UK: a cohort study. Lancet (London, England). 2010;376(9749):1303-11.
117. Singh RP, Farney AC, Rogers J, Zuckerman J, Reeves-Daniel A, Hartmann E, et al. Kidney transplantation from donation after cardiac death donors: lack of impact of delayed graft function on post-transplant outcomes. Clinical transplantation. 2011;25(2):255-64.
118. Cooper JT, Chin LT, Krieger NR, Fernandez LA, Foley DP, Becker YT, et al. Donation after cardiac death: the university of wisconsin experience with renal transplantation. American journal of transplantation : official journal of the American Society of Transplantation and the American Society of Transplant Surgeons. 2004;4(9):1490-4.