Original Article
Chronic Renal Failure after Transplantation of a Nonrenal Organ
N Engl J Med 2003; 349:931-940September 4, 2003
- Abstract
Background
Transplantation of nonrenal organs is often complicated by chronic renal disease with multifactorial causes. We conducted a population-based cohort analysis to evaluate the incidence of chronic renal failure, risk factors for it, and the associated hazard of death in recipients of nonrenal transplants.
Methods
Pretransplantation and post-transplantation clinical variables and data from a registry of patients with end-stage renal disease (ESRD) were linked in order to estimate the cumulative incidence of chronic renal failure (defined as a glomerular filtration rate of 29 ml per minute per 1.73 m2 of body-surface area or less or the development of ESRD) and the associated risk of death among 69,321 persons who received nonrenal transplants in the United States between 1990 and 2000.
Results
During a median follow-up of 36 months, chronic renal failure developed in 11,426 patients (16.5 percent). Of these patients, 3297 (28.9 percent) required maintenance dialysis or renal transplantation. The five-year risk of chronic renal failure varied according to the type of organ transplanted — from 6.9 percent among recipients of heart–lung transplants to 21.3 percent among recipients of intestine transplants. Multivariate analysis indicated that an increased risk of chronic renal failure was associated with increasing age (relative risk per 10-year increment, 1.36; P<0.001), female sex (relative risk among male patients as compared with female patients, 0.74; P<0.001), pretransplantation hepatitis C infection (relative risk, 1.15; P<0.001), hypertension (relative risk, 1.18; P<0.001), diabetes mellitus (relative risk, 1.42; P<0.001), and postoperative acute renal failure (relative risk, 2.13; P<0.001). The occurrence of chronic renal failure significantly increased the risk of death (relative risk, 4.55; P<0.001). Treatment of ESRD with kidney transplantation was associated with a five-year risk of death that was significantly lower than that associated with dialysis (relative risk, 0.56; P=0.02).
Conclusions
The five-year risk of chronic renal failure after transplantation of a nonrenal organ ranges from 7 to 21 percent, depending on the type of organ transplanted. The occurrence of chronic renal failure among patients with a nonrenal transplant is associated with an increase by a factor of more than four in the risk of death.
Media in This Article
Figure 1
Cumulative Incidence of Chronic Renal Failure among 69,321 Persons Who Received Nonrenal Organ Transplants in the United States between January 1, 1990, and December 31, 2000.Figure 2
Relative Risk of Death Associated with the Method of Renal Replacement (Dialysis or Kidney Transplantation) among Recipients of Nonrenal Organ Transplants Who Had Chronic Renal Failure.Article Activity
- Article
Chronic renal failure is a recognized complication of organ transplantation.1-8 Calcineurin-inhibitor therapy, a key component of immunosuppressive regimens for patients undergoing transplantation, has been implicated as a principal cause of post-transplantation renal dysfunction,9,10 which may lead to severe tubular atrophy, interstitial fibrosis, and focal hyalinosis of small renal arteries and arterioles.11-16 Furthermore, renal disease before transplantation, perioperative hemodynamic insults to the kidneys, nephrotoxic effects of other drugs, dyslipidemia, hypertension, and diabetes mellitus can all contribute to chronic renal failure in recipients of nonrenal organs.17,18
Renal failure after the transplantation of a nonrenal organ complicates medical management, leading to increased morbidity and mortality.14,19-22 The incidence of chronic renal disease among recipients of nonrenal transplants varies widely, from 10 to 83 percent,1,5,22-24 most likely owing to the lack of a standard definition of post-transplantation renal disease, differences in the types of transplantation studied, and variable periods of follow-up. Furthermore, occurrences of reversible postoperative acute renal failure are included in some reported estimates.
Reports of the progression of chronic renal failure to end-stage renal disease (ESRD) in recipients of nonrenal transplants have been contradicted by some reports suggesting a self-limited decrease in renal function without a measurable effect on patient outcomes.2,6,11,15,25-28 We performed a population-based cohort analysis involving recipients of heart, lung, liver, and intestine transplants who were included in the Scientific Registry of Transplant Recipients (SRTR) in order to determine the incidence of chronic renal failure, the risk factors for this condition, and the risk of death associated with it and to describe the outcomes of approaches to renal replacement (dialysis or kidney transplantation).
Methods
Sources of Data
Our study was based on data obtained from the SRTR, the Centers for Medicare and Medicaid Services (CMS), and the Death Master File of the Social Security Administration (SSA). The SRTR maintains a data base of all candidates for and recipients of solid-organ transplants in the United States. Patients on waiting lists for organ transplantation and those who receive organ transplants are tracked on a periodic basis with the use of data-collection forms completed by organ-transplantation programs and submitted to the Organ Procurement and Transplantation Network. These follow-up data, in addition to data from the network regarding patients on waiting lists and the allocation of organs, are included in the SRTR data base. The SRTR supplements information on vital status with data on deaths from the SSA's Death Master File and the Medicare Beneficiary Database maintained by the CMS. Data collection by the SRTR is exempt from oversight under the “public benefit or service program” provisions of the Code of Federal Regulations (45 CFR 46.101[b][5]), as approved by the institutional review board of the Health Resources and Services Administration of the Department of Health and Human Services.
The Death Master File includes updated information on all participants in the Social Security system. Information on deaths reported to the SSA for the administration of the death, disability, and retirement benefit programs is kept in the Death Master File data base.
The CMS maintains a data base of all patients treated for ESRD in the United States, which includes information about demographics, treatment, hospitalization, and costs for Medicare beneficiaries and other patients with ESRD who have received maintenance renal-replacement therapy.29 This data base also includes records of any changes in vital status or method of renal replacement, including kidney transplantation.
Study Subjects
The study population for our analysis included patients who received a heart, lung, heart–lung, liver, or intestine transplant in the United States between January 1, 1990, and December 31, 2000. This period was chosen as a period of relevant clinical-practice experience and to ensure that the follow-up information would be complete. We excluded from the analysis patients in whom the transplantation of a kidney or pancreas preceded the transplantation of a heart, lung, liver, or intestine and those who underwent combined heart–liver, liver–kidney, or heart–kidney transplantation. The sample in the analysis included 69,321 patients who received a first nonrenal solid-organ transplant during the study period. Patients entered the study on the date of the transplantation of the nonrenal organ or organs and were followed until death or December 31, 2001, whichever occurred first.
We constructed an analysis file containing information on the base-line demographic and clinical characteristics of the patients. These base-line data were linked to serum creatinine levels from post-transplantation follow-up forms in order to calculate the estimated glomerular filtration rate according to the four-variable formula used in the Modification of Diet in Renal Disease Study.30 The analysis file was linked to the ESRD data base of the CMS in order to identify patients who received renal-replacement therapy after transplantation of a nonrenal organ. The date of placement on the waiting list for kidney transplantation was tracked for patients with nonrenal transplants in whom ESRD developed. The change from dialysis to transplantation was also tracked in order to identify patients who received a renal transplant from a living donor and those who received a cadaveric kidney.
Statistical Analysis
The primary end point analyzed was chronic renal failure (defined as a glomerular filtration rate of 29 ml per minute per 1.73 m2 of body-surface area or less, according to the clinical-practice guidelines of the National Kidney Foundation31) or the onset of ESRD (as determined by the initiation of dialysis therapy or preemptive kidney transplantation). An analysis of competing risks32 was conducted to determine the cumulative incidence of chronic renal failure after transplantation. Variables for chronic renal failure and death were used to generate a curve showing the cumulative incidence of chronic renal failure among patients with each category of transplant.
A multivariate Cox regression model was used to analyze the relation between chronic renal failure and the following covariates: age; race; sex; the presence or absence of pretransplantation hepatitis, diabetes mellitus, or systemic hypertension; the use or nonuse of a calcineurin inhibitor (cyclosporine or tacrolimus) for immunosuppressive therapy during the initial hospitalization for transplantation; the presence or absence of postoperative acute renal failure (defined as a 50 percent decrease from base line in the glomerular filtration rate or the need for one or more dialysis treatments during the initial hospitalization for transplantation); and the type of nonrenal organ transplanted and year of transplantation.
A separate time-dependent Cox regression model was used to study the long-term effect of chronic renal failure on mortality. To avoid mingling the risk of death associated with the transplantation procedure with the relation that may exist between chronic renal failure and mortality, the analysis of the risk of death associated with chronic renal failure began three months after transplantation. Patients who died within three months after transplantation of a nonrenal organ were not included in the analysis of post-transplantation death rates.
Next, we evaluated the type of renal-replacement therapy provided to patients in whom chronic renal failure developed. We estimated the probability of receipt of a kidney transplant as treatment for ESRD among patients who had received a nonrenal transplant and in the general population of patients with ESRD by using a competing-risks model adjusted for age, race, cause of ESRD, and time since the onset of ESRD.
Finally, a time-dependent Cox regression model was used to estimate the effect of kidney transplantation on mortality among recipients of a nonrenal transplant who had ESRD and were on a waiting list for a kidney. The average relative risk of death after kidney transplantation was estimated at five time points after transplantation (days 30, 90, 183, 731, and 1825) for recipients of nonrenal transplants; the reference group for this analysis was the patients who were treated with dialysis. In this analysis, adjustment was made for the duration of ESRD before placement on the waiting list, as previously described.33,34 All reported P values are two-sided, and a P value of less than 0.05 was considered to indicate statistical significance.
Results
Base-Line Characteristics
The base-line characteristics of the recipients of nonrenal transplants are summarized in Table 1Table 1
Base-Line Characteristics of Recipients of Nonrenal Organ Transplants in the United States, 1990 to 2000.. Recipients of liver and heart transplants accounted for 53.2 percent and 34.7 percent of the patients, respectively; recipients of intestine and combined heart–lung transplants accounted for less than 1 percent each. The average age at the time of transplantation of the nonrenal organ or organs was approximately 45 years, except among recipients of intestine and heart–lung transplants (19 years and 33 years, respectively). Coexisting conditions were present before transplantation in a substantial minority of the patients; these included drug-treated hypertension (in 10.2 percent of patients), diabetes mellitus (in 8.1 percent), and hepatitis C infection (in 12.1 percent). The mean (±SD) glomerular filtration rate before transplantation was 75±31 ml per minute per 1.73 m2; the pretransplantation glomerular filtration rate was less than 60 ml per minute per 1.73 m2 in 23.8 percent of the patients, and 1.5 percent of the patients had been treated with dialysis between registration for the transplantation of a nonrenal organ and the receipt of a transplant.Incidence of Chronic Renal Failure
The median duration of follow-up from the time of transplantation of the nonrenal organ to the end of the cohort study was 36 months (mean, 46±38). During follow-up, chronic renal failure developed in 11,426 patients (16.5 percent). ESRD developed in 3297 of the patients with newly diagnosed chronic renal failure (28.9 percent). The risk of chronic renal failure increased over time among patients with all categories of nonrenal transplants (Figure 1Figure 1
Cumulative Incidence of Chronic Renal Failure among 69,321 Persons Who Received Nonrenal Organ Transplants in the United States between January 1, 1990, and December 31, 2000.). Table 2Table 2
Cumulative Incidence of Chronic Renal Failure According to the Type of Transplanted Organ. shows the five-year cumulative incidence of chronic renal failure for each category of nonrenal transplant, which ranged from 6.9 percent among patients with heart–lung transplants to 21.3 percent among patients with intestine transplants. ESRD occurred at a rate of 1.0 to 1.5 percent per year among patients with a nonrenal transplant.Risk Factors for Chronic Renal Failure
Multivariate Cox nonproportional-hazards regression analysis revealed that the overall risk of chronic renal failure was associated with a number of variables, including the patient's age, race, and sex; the pretransplantation glomerular filtration rate; and the presence or absence of pretransplantation hypertension, diabetes mellitus, or hepatitis C infection (Table 3Table 3
Risk Factors Associated with Chronic Renal Failure in Recipients of Nonrenal Organ Transplants.). When the glomerular filtration rate was analyzed as a continuous variable, a decrement of 10 ml per minute per 1.73 m2 in the pretransplantation glomerular filtration rate was associated with an increase of 9 percent in the risk of chronic renal failure (relative risk, 1.09; 95 percent confidence interval, 1.07 to 1.10). Greater reductions in the pretransplantation glomerular filtration rate31 were also associated with progressive increases in the risk of chronic renal failure. Overall, Asian patients and patients in the “other” category for race had a lower risk of chronic renal failure than white patients (relative risk, 0.77 and 0.73, respectively; P<0.001 for both comparisons). No independent effect of race on the risk of chronic renal failure was detected in a comparison of black and white patients.Apart from the risk factors that were significant for all categories of nonrenal transplants, the susceptibility factors associated with individual types of nonrenal transplants varied (Table 3). In organ-specific multivariate Cox regression models, only age, sex, presence or absence of postoperative acute renal failure, presence or absence of diabetes mellitus, and the year of transplantation were significantly associated with the risk of chronic renal failure among patients with any of the four major categories of nonrenal transplants. We did not construct a separate model for patients with intestine transplants because of the relatively small number of these patients. A combined regression model was used for patients with heart transplants and those with heart–lung transplants because of the nearly identical findings for these two categories.
There was a record of treatment with a calcineurin inhibitor (cyclosporine or tacrolimus) during the initial hospitalization for transplantation for 88.4 percent of the patients. As compared with the patients for whom the calcineurin-inhibitor treatment status was known, those with missing or unknown data on such treatment (at the time of the initial hospitalization for transplantation) had a lower risk of chronic renal failure (relative risk, 0.87; P<0.001). Among patients who had received liver transplants, the excess risk of chronic renal failure associated with the use of a calcineurin inhibitor was greater with cyclosporine therapy than with tacrolimus therapy (relative risk, 1.25; P<0.001). In this subgroup, we found no association between sirolimus therapy and chronic renal failure. Less than 1 percent of recipients of all extrarenal organs (590 patients) received sirolimus, with or without a calcineurin inhibitor, during the initial hospitalization for transplantation.
In keeping with the well-established association between hepatitis C and various glomerulonephritides,35 a positive result on a serologic test for hepatitis C before transplantation was significantly associated with an elevated risk of chronic renal failure (overall relative risk, 1.15; P<0.001), except among recipients of lung transplants. There was an elevated risk of chronic renal failure among patients with a previous diagnosis of hypertension (overall relative risk, 1.18; P<0.001), except among recipients of liver transplants. Diabetes mellitus was associated with chronic renal failure among patients with transplants of all categories (overall relative risk, 1.42; P<0.001). Postoperative acute renal failure (a 50 percent reduction in the glomerular filtration rate or a need for urgent dialysis treatment) occurred in 7.6 percent of the patients and was associated with an increase by a factor of more than two in the risk of chronic renal failure among patients with transplants of all categories (overall relative risk, 2.13; P<0.001).
Risk of Death after Chronic Renal Failure
The risk of death associated with the onset of chronic renal failure after the transplantation of a nonrenal organ was evaluated by means of a time-dependent Cox regression model, as described by Mauger et al.33 and Wolfe et al.34 In a comparison with transplant recipients who did not have chronic renal failure, and with allowance for at least three months of equivalent follow-up after transplantation, chronic renal failure was associated with an elevated risk of death after transplantation (relative risk, 4.55; 95 percent confidence interval, 4.38 to 4.74; P<0.001). The excess risk of death associated with chronic renal failure was not accounted for by the presence of ESRD alone, since patients who met the glomerular-filtration-rate criterion for chronic renal failure but in whom ESRD had not developed had a risk of death twice as high as that among transplant recipients who did not have chronic renal failure (data not shown).
Renal Transplantation in Patients with Nonrenal Organ Transplants
Forty-six percent (1516) of the patients with nonrenal transplants in whom ESRD developed were placed on a waiting list for kidney transplantation. In this subgroup, the adjusted annual incidence of kidney transplantation was 30.9 percent, as compared with 27.4 percent among all patients with ESRD on waiting lists for transplantation. The adjusted median time to kidney transplantation was 689 days for the patients who had received a nonrenal transplant, as compared with 771 days for the overall population of candidates for kidney transplants (P=0.02). Figure 2Figure 2
Relative Risk of Death Associated with the Method of Renal Replacement (Dialysis or Kidney Transplantation) among Recipients of Nonrenal Organ Transplants Who Had Chronic Renal Failure. shows the mortality rate among patients with nonrenal transplants who received a kidney transplant, as compared with patients with nonrenal transplants who were being treated with dialysis and awaiting kidney transplantation. An initial transient increase in mortality after kidney transplantation (relative risk at 30 days, 3.42; P=0.05) was followed by a progressive decrease in risk, so that 141 days after kidney transplantation, the patients who had received a kidney transplant had the same mortality rate as the patients still on the waiting list. Thereafter, the patients who received a kidney transplant had a lower risk of death, which was sustained until five years after transplantation (relative risk at day 1825, 0.56; P=0.02). Because of the initial excess mortality associated with the kidney-transplantation procedure, the proportion of patients who survived in the group that received a kidney transplant did not match the proportion in the group of patients on the waiting list until 506 days after kidney transplantation.Discussion
In our cohort study, chronic renal failure emerged as a relatively common complication in recipients of nonrenal transplants, affecting 7 to 21 percent within five years after transplantation of a nonrenal organ. The risk of chronic renal failure and the need for long-term renal-replacement therapy will increase further, given the trend toward increasing longevity in the overall population of recipients of nonrenal transplants, which currently numbers more than 100,000. Such a trend has already been demonstrated in single-center studies showing an increasing rate of chronic renal failure in direct proportion to longevity among recipients of heart and liver transplants.7,19,20,36 The potential for a greater caseload of patients with ESRD has serious fiscal implications for the ESRD program of Medicare, which currently spends $13 billion annually (approximately 6 percent of the total annual Medicare budget) on less than 1 percent of the 40 million Medicare enrollees (300,000 patients with ESRD).29
In our study of patients with nonrenal transplants, chronic renal failure was associated with an increase in mortality by a factor of more than four (relative risk of death, 4.55; 95 percent confidence interval, 4.38 to 4.74), which is consistent with more recent evidence of excess risk of death among patients with chronic renal insufficiency who have had an acute myocardial infarction or who have congestive heart failure.37,38 In view of the high incidence of chronic renal failure and the excess risk of death associated with it, it seems prudent to counsel patients undergoing transplantation of a nonrenal organ about the likelihood of chronic renal failure, just as they are typically cautioned about the risks of other complications — such as post-transplantation cancer, which occurs much less frequently than chronic renal failure.
The risk of chronic renal failure in our study was higher among recipients of liver transplants who were treated with cyclosporine than among those who were treated with tacrolimus — a difference that was not evident among patients with other types of transplants. The results of studies comparing the risk of kidney failure among transplant recipients receiving cyclosporine-based immunosuppressive regimens with the risk among those receiving tacrolimus-based regimens have been contradictory.39-43 Most comparative evaluations of calcineurin-induced nephrotoxic effects are of limited validity, because either the study patients were recipients of renal transplants (who lacked the sympathetic innervation of the allograft that has been implicated in the pathogenesis of toxic effects of calcineurin) or the study involved a switch from one calcineurin inhibitor to another after chronic renal failure had already been established.
The variability in risk among patients with different types of organ transplants in our study points to the existence of other important patient-specific and organ-specific susceptibility traits. Our data show that diabetes mellitus, hypertension, and hepatitis C infection are independent risk factors in the aggregate, although their prevalence and effect varied according to the type of organ transplanted. For example, recipients of liver transplants had a prevalence of hepatitis C of 21.4 percent, with an associated 22 percent excess risk of chronic renal failure. In contrast, recipients of lung transplants had a prevalence of hepatitis C of about 1 percent, with no detectable associated increase in the risk of chronic renal failure. We did not measure certain cardiovascular risk factors (e.g., hyperlipidemia and insulin resistance) that are recognized side effects of immunosuppressive medications44,45 and potential contributors to the progression of chronic renal failure in patients who have received different types of transplants.8,20
As in the general population of patients with ESRD,34,46-49 the high mortality associated with ESRD was substantially mitigated by kidney transplantation among patients with nonrenal transplants in our study and in other studies.50,51 In addition to the analysis of the influence of calcineurin inhibitors, attention to preexisting renal diseases, pretransplantation renal function, and modifiable cardiovascular risk factors might reduce the long-term risk of chronic renal failure after the transplantation of nonrenal organs.
Supported by a grant (HRSA 00-3691) from the Health Resources and Services Administration and a grant (K24 DK62234) from the National Institute of Diabetes and Digestive and Kidney Diseases, National Institutes of Health (to Dr. Ojo).
Dr. Ojo reports having received consulting fees from Novartis and lecture fees from Merck, Pfizer, AstraZeneca, and Pharmacia; Dr. Held a grant from Amgen; Dr. Port consulting fees from Optimal Renal Care and a grant from Amgen; and Dr. Wolfe a grant from PRO-West.
Source Information
From the Scientific Registry of Transplant Recipients (A.O.O., P.J.H., F.K.P., R.A.W., A.B.L., E.W.Y., J.A., L.C., R.M.M.) and the Departments of Medicine (A.O.O., A.B.L., E.W.Y.), Biostatistics (R.A.W.), and Surgery (R.M.M.), University of Michigan, Ann Arbor.
Address reprint requests to Dr. Ojo at the University of Michigan Medical School, Division of Nephrology, 3914 Taubman Ctr., Box 0364, Ann Arbor, MI 48109-0364, or at aojo@umich.edu.
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Joseph G. Rogers. (2012) Editorial Commentary: Renal failure after cardiac transplantation: Of bravery, wisdom and honesty. The Journal of Heart and Lung Transplantation 31:3, 231-232
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Timothy J. George, George J. Arnaoutakis, Claude A. Beaty, Matthew R. Pipeling, Christian A. Merlo, John V. Conte, Ashish S. Shah. (2012) Acute Kidney Injury Increases Mortality After Lung Transplantation. The Annals of Thoracic Surgery
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Robert S. Gaston. (2011) Our evolving understanding of late kidney allograft failure. Current Opinion in Organ Transplantation 16:6, 594-599
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J. Pliszczynski, B.D. Kahan. (2011) Better Actual 10-Year Renal Transplant Outcomes of 80% Reduced Cyclosporine Exposure With Sirolimus Base Therapy Compared With Full Cyclosporine Exposure Without or With Concomittant Sirolimus Treatment. Transplantation Proceedings 43:10, 3657-3668
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A.J. Mackay, P.W. Angus, P.J. Gow. (2011) Long-Term Outcomes of Calcineurin Inhibitor Withdrawal for Post–Liver Transplant Renal Dysfunction. Transplantation Proceedings 43:10, 3802-3806
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Shannon N. Saldaña, David K. Hooper, Tanya E. Froehlich, Kathleen M. Campbell, Cynthia A. Prows, Senthilkumar Sadhasivam, Todd G. Nick, Michael Seid, Alexander A. Vinks, Tracy A. Glauser. (2011) Characteristics of Successful Recruitment in Prospective Pediatric Pharmacogenetic Studies. Clinical Therapeutics
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Nassima Smail, Steven Paraskevas, Xianming Tan, Peter Metrakos, Marcelo Cantarovich. (2011) Renal function in recipients of pancreas transplant alone. Current Opinion in Organ Transplantation1
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François Durand. (2011) Hot-topic debate on kidney function: Renal-sparing approaches are beneficial. Liver Transplantation 17:S3, S43-S49
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P. Sharma, D. E. Schaubel, M. K. Guidinger, N. P. Goodrich, A. O. Ojo, R. M. Merion. (2011) Impact of MELD-Based Allocation on End-Stage Renal Disease After Liver Transplantation. American Journal of Transplantation 11:11, 2372-2378
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Diarmaid D. Houlihan, Matthew J. Armstrong, Yana Davidov, James Hodson, Peter Nightingale, Ian A. Rowe, Sue Paris, Bridget K. Gunson, Simon B. Bramhall, David J. Mutimer, James M. Neuberger, Philip N. Newsome. (2011) Renal function in patients undergoing transplantation for nonalcoholic steatohepatitis cirrhosis: Time to reconsider immunosuppression regimens?. Liver Transplantation 17:11, 1292-1298
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M. E. Hellemons, P. K. Agarwal, W. van der Bij, E. A. M. Verschuuren, D. Postmus, M. E. Erasmus, G. J. Navis, S. J. L. Bakker. (2011) Former Smoking Is a Risk Factor for Chronic Kidney Disease After Lung Transplantation. American Journal of Transplantation 11:11, 2490-2498
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Michael Jin Casey, Herwig-Ulf Meier-Kriesche. (2011) Calcineurin inhibitors in kidney transplantation. Current Opinion in Nephrology and Hypertension 20:6, 610-615
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Josh Levitsky. (2011) Next level of immunosuppression: Drug/immune monitoring. Liver Transplantation 17:S3, S60-S65
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Kadiyala V. Ravindra, Suzanne T. Ildstad. (2011) Immunosuppressive Protocols and Immunological Challenges Related to Hand Transplantation. Hand Clinics 27:4, 467-479
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Christine Lau, Paul Martin, Suphamai Bunnapradist. (2011) Management of Renal Dysfunction in Patients Receiving a Liver Transplant. Clinics in Liver Disease 15:4, 807-820
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Thomas Gerhardt, Uwe Pöge, Birgit Stoffel-Wagner, Holger Palmedo, Tilman Sauerbruch, Rainer Peter Woitas. (2011) Creatinine-based glomerular filtration rate estimation in patients with liver disease. European Journal of Gastroenterology & Hepatology 23:11, 969-973
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Brian Feingold, Jie Zheng, Yuk M. Law, W. Robert Morrow, Timothy M. Hoffman, Kenneth B. Schechtman, Anne I. Dipchand, Charles E. Canter, . (2011) Risk factors for late renal dysfunction after pediatric heart transplantation: A multi-institutional study. Pediatric Transplantation 15:7, 699-705
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R. Todd Stravitz, Daniel E. Carl, Diane M. Biskobing. (2011) Medical Management of the Liver Transplant Recipient. Clinics in Liver Disease 15:4, 821-843
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John R. Lake. (2011) Hot-topic debate on kidney function: Renal-sparing approaches are ineffective. Liver Transplantation 17:S3, S50-S53
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Tanya Pereira, Claudia P. Rojas, Monica T. Garcia-Buitrago, Jayanthi Chandar, Carolyn Abitbol, Wacharee Seeherunvong, Paolo Rusconi, Jocelyn H. Bruce, Gaston Zilleruelò. (2011) A child with BK virus infection: Inadequacy of current therapeutic strategies. Pediatric Transplantationno-no
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Marcelo Cantarovich, Jean Tchervenkov, Steven Paraskevas, Peter Ghali, Philip Wong, Marc Deschênes, Prosanto Chaudhury, Mazen Hassanain, Dionisios Vrochides, Peter Metrakos, Jeffrey Barkun. (2011) Early Changes in Kidney Function Predict Long-Term Chronic Kidney Disease and Mortality in Patients After Liver Transplantation. Transplantation1
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Thomas Gerhardt, Uwe Pöge, Birgit Stoffel-Wagner, Holger Palmedo, Tilman Sauerbruch, Rainer P. Woitas. (2011) Is beta-trace protein an alternative marker of glomerular filtration rate in liver transplant recipients?. Liver International 31:9, 1345-1351
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Achiya Amir, Rivka Shapiro, Lester M. Shulman, Eytan Mor, Ran Steinberg, Hava Fleishhacker, Rachel Bergerin, Yaron Avitzur. (2011) BK Virus Infection and Its Effect on Renal Function in Pediatric Liver-Transplant Recipients: A Cross-Sectional, Longitudinal, Prospective Study. Transplantation 92:8, 943-946
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Bruno Meiser, Stefan Buchholz, Ingo Kaczmarek. (2011) De-novo calcineurin-inhibitor-free immunosuppression with sirolimus and mycophenolate mofetil after heart transplantation. Current Opinion in Organ Transplantation 16:5, 522-528
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Eugenia Raichlin, Malik A. Al-Omari, Courtney L. Hayes, Brooks S. Edwards, Robert P. Frantz, Barry A. Boilson, Alfredo L. Clavell, Richard J. Rodeheffer, John A. Schirger, Sudhir S. Kushwaha, Thomas G. Allison, Naveen L. Pereira. (2011) Cardiac allograft hypertrophy is associated with impaired exercise tolerance after heart transplantation. The Journal of Heart and Lung Transplantation 30:10, 1153-1160
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John O’Grady. (2011) Liver transplantation. Medicine 39:10, 621-623
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E. Hryniewiecka, J. Żegarska, L. Pa̧czek. (2011) Arterial Hypertension in Liver Transplant Recipients. Transplantation Proceedings 43:8, 3029-3034
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Brian J Nankivell, Dirk RJ Kuypers. (2011) Diagnosis and prevention of chronic kidney allograft loss. The Lancet 378:9800, 1428-1437
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Michael Kriss, Eva U. Sotil, Michael Abecassis, Mary Welti, Josh Levitsky. (2011) Mycophenolate mofetil monotherapy in liver transplant recipients. Clinical Transplantationno-no
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K. E. Wever, M. C. Warle, F. A. Wagener, J. W. van der Hoorn, R. Masereeuw, J. A. van der Vliet, G. A. Rongen. (2011) Remote ischaemic preconditioning by brief hind limb ischaemia protects against renal ischaemia-reperfusion injury: the role of adenosine. Nephrology Dialysis Transplantation 26:10, 3108-3117
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Mykola Tsapenko, Ziad M. El-Zoghby, Sanjeev Sethi. (2011) Renal histological lesions and outcome in liver transplant recipients. Clinical Transplantationno-no
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Merel E. Hellemons, Stephan J.L. Bakker, Douwe Postmus, Erik A.M. Verschuuren, Michiel E. Erasmus, Gerjan Navis, Wim van der Bij. (2011) Incidence of impaired renal function after lung transplantation. The Journal of Heart and Lung Transplantation
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Edgard Wehbe, Rachel Brock, Marie Budev, Meng Xu, Sevag Demirjian, Martin J. Schreiber, Brian Stephany. (2011) Short-term and long-term outcomes of acute kidney injury after lung transplantation. The Journal of Heart and Lung Transplantation
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Fernanda Cristina Mazali, Marilda Mazzali. (2011) Uric Acid and Transplantation. Seminars in Nephrology 31:5, 466-471
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David H. Oustecky, Andres R. Riera, Kenneth D. Rothstein. (2011) Long-Term Management of the Liver Transplant Recipient: Pearls for the Practicing Gastroenterologist. Gastroenterology Clinics of North America 40:3, 659-681
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J. A. Leithead, J. W. Ferguson, C. M. Bates, J. S. Davidson, K. J. Simpson, P. C. Hayes. (2011) Chronic Kidney Disease After Liver Transplantation for Acute Liver Failure Is Not Associated With Perioperative Renal Dysfunction. American Journal of Transplantation 11:9, 1905-1915
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N. Manito, G. Rábago, J. Palomo, J.M. Arizón, J. Delgado, L. Almenar, M.G. Crespo-Leiro, E. Lage, L. Pulpón. (2011) Improvement in Chronic Renal Failure after Mycophenolate Mofetil Introduction and Cyclosporine Dose Reduction: Four-Year Results From a Cohort of Heart Transplant Recipients. Transplantation Proceedings 43:7, 2699-2706
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Sean P. Pinney, Revathi Balakrishnan, Steven Dikman, Ajith Nair, Kimmarie Hammond, Michael Domanski, Anelechi C. Anyanwu, Graciela DeBoccardo. (2011) Histopathology of renal failure after heart transplantation: A diverse spectrum. The Journal of Heart and Lung Transplantation
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A J Matas. (2011) Calcineurin Inhibitors: Short-Term Friend, Long-Term Foe?. Clinical Pharmacology & Therapeutics 90:2, 209-211
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Geraldine Diaz, Michael O’Connor. (2011) Cardiovascular and renal complications in patients receiving a solid-organ transplant. Current Opinion in Critical Care 17:4, 382-389
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J R Chapman. (2011) Chronic Calcineurin Inhibitor Use Is Nephrotoxic. Clinical Pharmacology & Therapeutics 90:2, 207-209
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Faouzi Saliba, Sébastien Dharancy, Richard Lorho, Filoména Conti, Sylvie Radenne, Martine Neau-Cransac, Monika Hurtova, Jean Hardwigsen, Yvon Calmus, Jérome Dumortier. (2011) Conversion to everolimus in maintenance liver transplant patients: A multicenter, retrospective analysis. Liver Transplantation 17:8, 905-913
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J.F. Castroagudín, E. Molina, E. Varo. (2011) Calcineurin Inhibitors in Liver Transplantation: To Be or Not to Be. Transplantation Proceedings 43:6, 2220-2223
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N. Kamar, C. Guilbeau-Frugier, A. Servais, I. Tack, E. Thervet, O. Cointault, L. Esposito, J. Guitard, L. Lavayssiere, F. Muscari, C. Bureau, L. Rostaing. (2011) Kidney histology and function in liver transplant patients. Nephrology Dialysis Transplantation 26:7, 2355-2361
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David R. Snydman, Kristin D. Kistler, Paula Ulsh, Garrett E. Bergman, Judith Vensak, Jonathan Morris. (2011) The impact of CMV prevention on long-term recipient and graft survival in heart transplant recipients: analysis of the Scientific Registry of Transplant Recipients (SRTR) database. Clinical Transplantation 25:4, E455-E462
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T. Pérez, R. Segovia, L. Castro, J.P. Roblero, R. Estela. (2011) Conversion to Everolimus in Liver Transplant Patients With Renal Dysfunction. Transplantation Proceedings 43:6, 2307-2310
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Thomas A. Gonwa, Maureen A. McBride, Martin L. Mai, Hani M. Wadei. (2011) Kidney Transplantation After Previous Liver Transplantation: Analysis of the Organ Procurement Transplant Network Database. Transplantation 92:1, 31-35
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Cheng R. Pan, Christoph Schmaderer, Marcel Roos, Maximilian von Eynatten, Daniel Sollinger, Jens Lutz, Uwe Heemann, Marcus Baumann. (2011) Comparing aortic stiffness in kidney transplant recipients, hemodialysis patients, and patients with chronic renal failure. Clinical Transplantation 25:4, E463-E468
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Toshiyasu Kawahara, Sonal Asthana, Norman M. Kneteman. (2011) m-TOR inhibitors: What role in liver transplantation?. Journal of Hepatology
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Shih-Han S. Huang, Jennifer J. Macnab, Jessica M. Sontrop, Guido Filler, Kerri Gallo, Robert M. Lindsay, William F. Clark. (2011) Performance of the creatinine-based and the cystatin C-based glomerular filtration rate (GFR) estimating equations in a heterogenous sample of patients referred for nuclear GFR testing. Translational Research 157:6, 357-367
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S. A. Lodhi, K. E. Lamb, H. U. Meier-Kriesche. (2011) Solid Organ Allograft Survival Improvement in the United States: The Long-Term Does Not Mirror the Dramatic Short-Term Success. American Journal of Transplantation 11:6, 1226-1235
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Ranjeeta Bahirwani, Oren Shaked, Shanu Kurd, Roy Bloom, K. Rajender Reddy. (2011) Chronic Kidney Disease After Orthotopic Liver Transplantation: Impact of Hepatitis C Infection. Transplantation 91:11, 1245-1249
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M. Trinidad Serrano Aulló, Eduardo Parra Moncasi, Sara Lorente Pérez. (2011) Inmunosupresión en el trasplante hepático: pautas renoprotectoras. Gastroenterología y Hepatología 34:6, 422-427
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R. Zhang, M. Georgiou, W. Gwinner, P. Zardo, A. Haverich, C. Bara. (2011) Early Posttransplantation Hemoglobin Level Corresponds with Chronic Renal Dysfunction in Heart Transplant Recipients. Transplantation Proceedings 43:5, 1939-1943
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Elizabeth C. Verna, Erica D. Farrand, Abdulrhman S. Elnaggar, Elsa M. Pichardo, Anastasia Balducci, Jean C. Emond, James V. Guarrera, Robert S. Brown. (2011) Basiliximab Induction and Delayed Calcineurin Inhibitor Initiation in Liver Transplant Recipients With Renal Insufficiency. Transplantation 91:11, 1254-1260
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Navdeep S. Nayyar, William McGhee, Dolly Martin, Rakesh Sindhi, Kyle Soltys, Geoffrey Bond, George V. Mazariegos. (2011) Intestinal Transplantation in Children. Pediatric Drugs 13:3, 149-159
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Y.B. Chen, S.D. Li, B.L. Ju, X.J. Shi, F. Lu, D.K. Hu, C.H. Yu, J.H. Dong. (2011) Suitable Calcineurin Inhibitor Concentrations for Liver Transplant Recipients in the Chinese Population. Transplantation Proceedings 43:5, 1751-1753
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Frédéric Jacques, Ismail El-Hamamsy, Annik Fortier, Simon Maltais, Louis P. Perrault, Moishe Liberman, Nicolas Noiseux, Pasquale Ferraro. (2011) Acute renal failure following lung transplantation: risk factors, mortality, and long-term consequences. European Journal of Cardio-Thoracic Surgery
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Mihai Oltean, Gustaf Herlenius. (2011) Renal protection during liver transplantation: An ounce of prevention is worth a pound of cure*. Critical Care Medicine 39:6, 1564-1565
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P. Przybylowski, J.S. Malyszko, J. Malyszko. (2011) Soluble Tumor Necrosis Factor-like Weak Inducer of Apoptosis Plasma Levels as a Novel Biomarker of Endothelial Function in Prevalent Orthotopic Heart Transplant Recipients. Transplantation Proceedings 43:5, 1900-1903
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S. Celik, A.O. Doesch, M.H. Konstandin, A.V. Kristen, K. Ammon, F.-U. Sack, P. Schnabel, H.A. Katus, T.J. Dengler. (2011) Increased Incidence of Acute Graft Rejection on Calcineurin Inhibitor–Free Immunosuppression After Heart Transplantation. Transplantation Proceedings 43:5, 1862-1867
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Medhat Askar, Jesse D. Schold, Bijan Eghtesad, Stuart M. Flechner, Bruce Kaplan, Lynne Klingman, Nizar N. Zein, John Fung, Titte R. Srinivas. (2011) Combined Liver-Kidney Transplants: Allosensitization and Recipient Outcomes. Transplantation 91:11, 1286-1292
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Steven M. Kawut. (2011) Lung Retransplantation. Clinics in Chest Medicine 32:2, 367-377
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Fuat H. Saner, Vito R. Cicinnati, Georgios Sotiropoulos, Susanne Beckebaum. (2011) Strategies to prevent or reduce acute and chronic kidney injury in liver transplantation. Liver Internationalno-no
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Arthur J. Matas, Darla Granger, Dixon B. Kaufman, Minnie M. Sarwal, Ronald M. Ferguson, E. Steve Woodle, John S. Gill. (2011) Steroid minimization for sirolimus-treated renal transplant recipients. Clinical Transplantation 25:3, 457-467
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F. Tinti, I. Umbro, V. Giannelli, M. Merli, S. Ginanni Corradini, M. Rossi, I. Nofroni, L. Poli, P.B. Berloco, A.P. Mitterhofer. (2011) Acute Renal Failure in Liver Transplant Recipients: Role of Pretransplantation Renal Function and 1-Year Follow-Up. Transplantation Proceedings 43:4, 1136-1138
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Lee S. Cummings, Jason S. Hawksworth, Juan-Francisco Guerra, Chirag S. Desai, Raffaele Girlanda, Cal S. Matsumoto, Thomas M. Fishbein, Lynt B. Johnson, Joseph K. Melancon. (2011) Successful ABO Incompatible Kidney Transplant After an Isolated Intestinal Transplant. Transplantation 91:10, e73-e74
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K. Boudjema, C. Camus, F. Saliba, Y. Calmus, E. Salamé, G. Pageaux, C. Ducerf, C. Duvoux, C. Mouchel, A. Renault, P. Compagnon, R. Lorho, E. Bellissant. (2011) Reduced-Dose Tacrolimus with Mycophenolate Mofetil vs. Standard-Dose Tacrolimus in Liver Transplantation: A Randomized Study. American Journal of Transplantation 11:5, 965-976
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C. Duvoux, G.P. Pageaux. (2011) Immunosuppression in liver transplant recipients with renal impairment. Journal of Hepatology 54:5, 1041-1054
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Madhurmeet Singh, Michael Shullo, Robert L. Kormos, Kathleen Lockard, Rachelle Zomak, Marc A. Simon, Christian Bermudez, Jay Bhama, Dennis McNamara, Yoshiya Toyoda, Jeffrey J. Teuteberg. (2011) Impact of Renal Function Before Mechanical Circulatory Support on Posttransplant Renal Outcomes. The Annals of Thoracic Surgery 91:5, 1348-1354
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Fabrizio Fabrizi, Vivek Dixit, Paul Martin, Piergiorgio Messa. (2011) Pre-transplant Kidney Function Predicts Chronic Kidney Disease After Liver Transplant: Meta-Analysis of Observational Studies. Digestive Diseases and Sciences 56:5, 1282-1289
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H. H. Ryu, H. L. Kim, J. H. Chung, B. R. Lee, T. H. Kim, B. C. Shin. (2011) Renoprotective effects of green tea extract on renin-angiotensin-aldosterone system in chronic cyclosporine-treated rats. Nephrology Dialysis Transplantation 26:4, 1188-1193
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F. Brinkert, M. J. Kemper, A. Briem-Richter, M. van Husen, A. Treszl, R. Ganschow. (2011) High prevalence of renal dysfunction in children after liver transplantation: non-invasive diagnosis using a cystatin C-based equation. Nephrology Dialysis Transplantation 26:4, 1407-1412
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Marcelo Cantarovich, Nigel W. Brown, Mary H.H. Ensom, Ashok Jain, Dirk R.J. Kuypers, Teun Van Gelder, J. Michael Tredger. (2011) Mycophenolate monitoring in liver, thoracic, pancreas, and small bowel transplantation: a consensus report. Transplantation Reviews 25:2, 65-77
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I. M. Hamour, A. Khaghani, P. K. Kanagala, A. G. Mitchell, N. R. Banner. (2011) Current outcome of heart transplantation: a 10-year single centre perspective and review. QJM 104:4, 335-343
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Arthur J. Matas. (2011) Chronic Progressive Calcineurin Nephrotoxicity: An Overstated Concept. American Journal of Transplantation 11:4, 687-692
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J. R. Chapman. (2011) Chronic Calcineurin Inhibitor Nephrotoxicity-Lest We Forget. American Journal of Transplantation 11:4, 693-697
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A. Alakkari, D. Maguire, J. Geoghegan, J. E. Hegarty, O. Traynor, A. Watson, P. A. McCormick. (2011) Anti-CD25 antibodies (daclizumab) as renal sparing immunosuppression after liver transplantation. Alimentary Pharmacology & Therapeutics 33:5, 615-616
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Simon de Denus, Marcin Zakrzewski, Amina Barhdadi, Marie-Hélène Leblanc, Normand Racine, François Bélanger, Michel Carrier, Anique Ducharme, Marie-Pierre Dubé, Jacques Turgeon, Michel White. (2011) Association between renal function and CYP3A5 genotype in heart transplant recipients treated with calcineurin inhibitors. The Journal of Heart and Lung Transplantation 30:3, 326-331
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Julie A. Thompson, John R. Lake. (2011) Liver Transplantation for Hepatitis C: Disease Management. Current Hepatitis Reports 10:1, 41-51
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Martin S. Zand, Mark S. Orloff, Peter Abt, Siddharth Patel, George Tsoulfas, Randeep Kashyap, Ashok Jain, Saman Safadjou, Adel Bozorgzadeh. (2011) High mortality in orthotopic liver transplant recipients who require hemodialysis. Clinical Transplantation 25:2, 213-221
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Christopher LaRosa, H. Jorge Baluarte, Kevin E. C. Meyers. (2011) Outcomes in pediatric solid-organ transplantation. Pediatric Transplantation 15:2, 128-141
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Janna Huskey, Alexander C. Wiseman. (2011) Chronic viral hepatitis in kidney transplantation. Nature Reviews Nephrology 7:3, 156-165
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Kimberly A Brown, Mary Ann Huang, Marwan Kazimi, Dilip Moonka. 2011. Liver Transplantation. , 238-273.
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Elizabeth A Kendrick, Connie L Davis. 2011. Management of the Successful Solid Organ Transplant Recipient. , 73-102.
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Maryl R Johnson, Walter G Kao, Elaine M Winkel, Joseph L Bobadilla, Takushi Kohmoto, Niloo M Edwards. 2011. Heart Transplantation. , 171-204.
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Mark Fox, Jenny Fox, Mervyn Davies. (2011) Diagnosis and management of chronic liver disease in older people. Reviews in Clinical Gerontology 21:01, 1-15
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Guido Filler. (2011) Challenges in pediatric transplantation: The impact of chronic kidney disease and cardiovascular risk factors on long-term outcomes and recommended management strategies. Pediatric Transplantation 15:1, 25-31
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Sameer J. Khandhar, Hemal V. Shah, Michael A. Shullo, Rachelle Zomak, Michelle Navoney, Dennis M. McNamara, Robert L. Kormos, Yoshiya Toyoda, Jeffrey J. Teuteberg. (2011) Long-term effects on renal function of dose-reduced calcineurin inhibitor and sirolimus in cardiac transplant patients. Clinical Transplantationno-no
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Bryce Kiberd, Chris Skedgel, Ian Alwayn, Kevork Peltekian. (2011) Simultaneous Liver Kidney Transplantation: A Medical Decision Analysis. Transplantation 91:1, 121-127
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Kilian Weigand, Eva Bauer, Jens Encke, Jan Schmidt, Wolfgang Stremmel, Vedat Schwenger. (2011) Prognostic Value of Standard Parameters as Predictors for Long-Term Renal Replacement Therapy after Liver Transplantation. Nephron Clinical Practice 119:4, c342-c347
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