American Journal of Kidney Diseases
February 2003 • Volume 41 • Number 2
Original Investigations: Transplantation
Long-term survival following simultaneous kidney-pancreas
transplantation versus kidney transplantation alone in patients
with type 1 diabetes mellitus and renal failure
K. Sudhakar Reddy, MD [MEDLINE
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Don Stablein, PhD [MEDLINE
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Sarah Taranto, BA [MEDLINE
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Robert J. Stratta, MD [MEDLINE
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Thomas D. Johnston, MD
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Thomas H. Waid, MD [MEDLINE
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J. Wade McKeown, MD [MEDLINE
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Bruce A. Lucas, MD [MEDLINE
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Dinesh Ranjan, MD [MEDLINE
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Sections
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Abstract
Methods
Results
Discussion
References
Publishing and Reprint Information
Abstract
TOP
Background: Pancreas transplantation improves quality of life and prevents the progression of
secondary complications of diabetes. Whether these benefits translate into a long-term survival
advantage is not entirely clear. Methods: Using the United Network for Organ Sharing database,
we analyzed long-term survival in 18,549 patients with type 1 diabetes and renal failure who
received a kidney transplant between 1987 and 1996. Patient survival was calculated using the
Kaplan-Meier method. Proportional hazards models were used to adjust for effects of differences
in recipient and donor variables between simultaneous kidney-pancreas transplants (SKPTs) and
kidney-alone transplants. Results: SKPT and living donor kidney recipients had a significant
crude survival distribution advantage over cadaver kidney transplant recipients (8-year survival
rates: 72% for SKPT recipients, 72% for living donor kidney recipients, and 55% for cadaver
kidney recipients). The survival advantage for SKPT recipients over cadaver kidney recipients
diminished, but persisted after adjusting for donor and recipient variables and kidney graft
function as time-varying covariates. SKPT recipients had a high mortality risk relative to living
donor kidney recipients through 18 months posttransplantation (hazards ratio, 2.2; P < 0.001), but
had a lower relative risk (hazard ratio, 0.86; P < 0.02) thereafter. In SKPT recipients,
maintenance of a functioning pancreas graft was associated with a survival benefit. Conclusion:
The long-term survival of SKPT recipients is superior to that of cadaver kidney transplant
recipients with type 1 diabetes. There is no difference in survival of SKPT recipients and living
donor kidney recipients with type 1 diabetes at up to 8 years' follow-up; the former have a greater
early mortality risk and the latter have a greater late mortality risk. Results of this study suggest
that successful simultaneous kidney-pancreas transplantation is not only life enhancing, but life
saving. Am J Kidney Dis 41:464-470. © 2003 by the National Kidney Foundation, Inc.
(Click on a term to search this journal for other articles containing that term.)
Index words: Diabetes, end-stage renal disease (ESRD), long-term survival, kidney
transplantation, pancreas transplantation
Successful kidney transplantation, in addition to being cost-effective and improving quality of life,
increases survival compared with long-term dialysis treatment in patients with end-stage renal
disease caused by type 1 diabetes.1 Pancreas transplantation performed simultaneously with
kidney transplantation further enhances quality of life and has been reported to stabilize or
improve some secondary complications of diabetes mellitus.2-9 Although short-term patient
survival is similar for recipients of simultaneous kidney-pancreas transplants (SKPTs) and
cadaver kidney transplants,10 the effect of pancreas transplantation on long-term survival has
remained uncertain.
In a recent registry report from The Netherlands, mortality after initiating renal replacement
therapy was 50% less in the Leiden area compared with another area; the only difference
between the two areas was the frequency of simultaneous kidney-pancreas transplantation (73%
in the Leiden area compared with 37% in the non-Leiden area).11 Several other single-center
reports also suggest that simultaneous kidney-pancreas transplantation results in a substantial
decrease in mortality in patients with type 1 diabetes mellitus and renal failure compared with
kidney transplantation alone.12-14 However, there generally is a selection bias, with SKPT
recipients being younger and healthier and receiving organs from younger donors with shorter
cold ischemia times compared with recipients of cadaver kidney transplants, making it difficult to
determine the primary effect of pancreas transplantation on survival. In addition, single-center
reports are limited by relatively small numbers of patients.
The objective of the present study is to determine the effect of pancreas transplantation on longterm survival of a large cohort of patients with type 1 diabetes with end-stage renal failure.
Methods
TOP
Using the United Network for Organ Sharing (UNOS) database, we analyzed the survival of
18,549 patients with type 1 diabetes who received a kidney transplant between 1987 and 1996.
Patients who received segmental pancreas grafts from living donors were excluded from this
analysis. According to the UNOS Registry, 9,956 patients received cadaver kidney-only
transplants, 3,991 patients received living donor kidney transplants, and 4,602 patients received
SKPTs during the study period. Mean follow-up in survivors was 4.8 years, with 95% followed up
for at least 1 year and 25% followed up for 6.8 or more years.
Patient survival distribution estimates were calculated using the Kaplan-Meier method. Because
there were differences between cadaver and living donor kidney transplants and SKPTs with
respect to covariates known to influence graft and patient survival, proportional hazards models
were used to adjust for effects of these variables (recipient age at time of transplantation,
recipient race and sex, donor age, donor cause of death, previous kidney transplant, previous
transfusions, cold ischemia time, percentage of panel reactive antibody, center volume, and year
of transplantation) on the probability of graft and patient survival. Time-varying covariates were
used to examine graft function as a predictor of survival and time-varying changes in relative
hazard function. Analysis was performed using the SAS statistical program (SAS Institute, Cary,
NC).
We also analyzed survival of patients with functioning kidney grafts at the end of the first year to
avoid the potential effect of a failed kidney graft as the cause of inferior patient survival. In
addition, we compared survival of SKPT recipients with functioning kidney and pancreas grafts at
the end of the first year posttransplantation with survival of those with a functioning kidney graft,
but failed pancreas graft, within the first year posttransplantation.
Results
TOP
Recipients of SKPTs were younger and more often Caucasian, received kidneys from younger
donors with a cause of death of head trauma more often as opposed to cardiocerebrovascular in
origin, and had shorter cold ischemia times and thereby less often needed dialysis therapy in the
first week posttransplantation compared with cadaver kidney transplant recipients (Table 1).
Table 1. Characteristics of Patients With Type 1 Diabetes and Renal Failure
Receiving Kidney Transplants
Characteristic
Living Donor Kidney
Transplants (n = 3,991)
Cadaver Kidney
SKPTs* (n =
Transplants (n = 9,956)
4,602)
Mean recipient age (y)
38.6
43.6
36.4
Recipient sex (% women)
44.7
39.5
40.9
White
82.7
70.7
89.2
Black
8.1
17.5
6.7
Other
9.1
11.8
4.1
39.2
31.9
27.2
18.1
16.1
3.6
Not applicable
34.0
25.8
Recipient race (%)
Mean donor age (y)
>50 y (%)
Donor cause of death (%)
Cerebrovascular
accident
Head trauma
34.6
49.2
Other
31.4
26.0
2.7
5.4
1.8
0
43.1
35.9
45.5
1-5
36.8
38.3
32.8
6-10
5.9
9.2
4.9
>10
2.7
6.0
1.6
Unknown
11.6
10.7
15.2
Mean cold ischemia (h)
1
23.4
14.4
Dialysis wk 1
posttransplantation (%)
6.2
25.2
6.8
Previous kidney transplant
(%)
Previous transfusions (%)
*P
< 0.001 for all characteristics compared with cadaver kidney transplants.
Simultaneous kidney-pancreas transplantation has become more common in recent years,
accounting for 10.8% of cadaver donor transplantations in patients with type 1 diabetes in 1987
and 1988 and 54.7% in 1996. Simultaneous kidney-pancreas transplantation is performed more
frequently in centers that perform larger numbers of kidney transplantations. For example, 87% of
simultaneous kidney-pancreas transplantations were performed at high-volume centers (>50
kidney transplantations in the previous year) as opposed to only 69% of cadaver kidney
transplantations.
As listed in Table 2, a total of 4,728 deaths occurred in the study population.
Table 2. Distribution of Causes of Death
Living Donor Kidney
Recipients (n = 724)
Cadaver Kidney
Recipients (n = 3,167)
SKPT Recipients
(n = 837)
Cardiac (%)
30.8
31.0
24.1
Cerebrovascular
(%)
5.5
5.9
6.7
Diabetes (%)
2.9
1.7
1.0
Hemorrhage (%)
0.3
0.9
1.4
Infection (%)
8.4
8.3
15.2
Malignancy (%)
3.5
2.8
3.9
Unknown (%)
33.4
37.3
32.7
Other (%)
15.2
12.2
14.9
Cause of Death
Kidney transplant recipients had a greater frequency of cardiac deaths, whereas SKPT recipients
had a greater frequency of deaths from infection (Table 2 ). This difference in causes of death
was even more pronounced when we examined causes of death during the first year; deaths
among SKPT recipients were twice as likely to be attributed to infection (19%) relative to kidneyalone recipients (10%), whereas cardiac causes of death were identified in a lower percentage of
SKPT recipients (19% versus 33%). However, the high frequency of deaths from unknown
causes makes definitive interpretation difficult.
SKPT and living donor kidney recipients had a significant crude survival distribution advantage
over cadaver kidney recipients (Fig 1).
Fig. 1. Survival distribution estimates posttransplantation for patients with type 1 diabetes with
renal failure. Abbreviations: LD, living donor; CAD, cadaveric.
Five- and 8-year patient survival rates were 81% and 72% for SKPT recipients, 84% and 72% for
living donor kidney recipients, and 71% and 55% for cadaver kidney recipients, respectively. The
living donor transplant group includes 15% HLA-identical transplants. Eight-year survival rates
were 71% and 79% for HLA-nonidentical and HLA-identical transplants, respectively. SEs of 5and 8-year survival estimates were 1% or less. Eight-year survival rates decreased from 73% to
62% to 44% as age groupings increased from younger than 35 years (n = 5,824) to 35 to 49
years (n = 8,952) to older than 49 years (n = 3,773). Simultaneous kidney-pancreas
transplantation was performed infrequently in the oldest age group (n = 177), and survival of
patients with SKPT and cadaver-only transplants appear similar.
Among SKPT recipients, 5-year survival has improved over time from 78% in the cohort that
underwent transplantation through 1992 to 83% among those who underwent transplantation in
1993 and later. When adjusted for pretransplantation variables known to influence graft and
patient survival by using the proportional hazards model, the survival benefit for SKPT versus
cadaver kidney recipients was diminished (P = 0.03). Because the crude kidney graft survival rate
was lower for cadaver than SKPT transplants (Fig 2), we incorporated kidney graft function as a
time-varying covariate.
Fig. 2. Estimated distribution of kidney graft survival by transplant status. Abbreviations: LD, living
donor; CAD, cadaveric.
In a model with additional adjustments for recipient demographics, year, center volume, and
donor age, simultaneous kidney-pancreas transplantation was observed to have a significant
survival advantage (relative risk [RR], 0.92; P = 0.04) relative to cadaver kidney transplantation.
In Table 3, death rates per 100 years of follow-up are listed.
Table 3. Death Rates Per 100-Patient-Year Follow-Up
Type of Transplant
Overall
1 Year
>1 Year
Living donor kidney
3.8
3.8
3.8
Cadaver kidney
7.3
9.5
6.7
SKPT
4.5
8.2
3.4
As in Fig 1 , Table 3 shows simultaneous kidney-pancreas transplantation to have a high
mortality risk relative to living donor transplantation in the early posttransplantation period.
Adjusted for demographics and kidney graft function, the hazard ratio of simultaneous kidneypancreas transplantation relative to the living-donor group is estimated to be 2.2 (P < 0.001)
through 18 months posttransplantation, but reverses to a decreased RR (RR, 0.86; P = 0.02)
thereafter. At the 10-year point, the SKPT group has a small survival advantage (67.0% versus
64.1%) compared with the living-donor group. However, this long-term survival advantage is not
statistically significant because 95% confidence intervals are each approximately 6% points wide.
In Fig 3, patient survival distribution estimates for survivors with renal allograft function at 1 year
are shown.
Fig. 3. Survival estimates for patients with kidney graft function at 1 year. Abbreviations: LD,
living donor; CAD, cadaveric.
Five-year survival rates were 89.8%, 87.8%, and 79.7% for SKPT, living donor, and cadaver
donor transplant recipients, respectively. At 8 years, respective rates were 79.3%, 76.2%, and
61.6%. Relative hazards (adjusted for baseline risk factors) for cadaver kidney transplant and
SKPT recipients compared with living donor kidney transplant recipients were 1.4 (P < 0.001) and
0.98 (P = 0.78), respectively.
Maintenance of a functioning pancreas graft appears to be associated with a survival benefit (Fig
4).
Fig. 4. Patient survival among SKPT recipients according to kidney and pancreas graft status at 1
year.
Of 403 patients with a functioning kidney transplant, but failed pancreas transplant, at 1 year,
18.6% died versus 9.8% of 3,445 patients with both organs functioning at 1 year. Mortality for
patients with failed kidney allografts (functioning pancreas grafts; N = 105) or both organs failed
(N = 122) is substantial, with death rates greater than 33% for each group. This highlights the
substantial hazard increase associated with kidney graft failure. Five- and 8-year patient survival
rates for SKPT recipients with a functioning kidney graft, but failed pancreas graft, at the end of
the first year were 81.8% and 61.7%, significantly inferior to the 90.5% and 81.2% rates for those
with functioning kidney and pancreas grafts, respectively (P < 0.0001; Fig 4 ). Relative hazards,
adjusted for baseline risk factors, are 4.6 for failed kidney, 1.9 for failed pancreas, and 5.0 for
both organs failed (each P < 0.001 relative to both organs functioning).
Discussion
TOP
We found that long-term survival of SKPT and living donor kidney transplant recipients was
similar and superior to that of cadaver donor kidney transplant recipients. A functioning pancreas
graft appears to provide a survival advantage because: (1) survival of SKPT recipients is better
than that of cadaver kidney transplant recipients, even after adjusting for recipient and donor
characteristics; and (2) survival of SKPT recipients who have functioning kidney and pancreas
grafts is superior to that of recipients with functioning kidney graft, but failed pancreas graft, at 1
year. Although SKPT recipients have lower mortality than living donor kidney transplant recipients
after the first year (3.4 versus 3.8 deaths/100 years' follow-up), survival was similar at 8 years
because of greater mortality for SKPT recipients in the first year (hazards ratio for the SKPT
relative to the living-donor group, 2.2).
A few other studies also reported that SKPT recipients have a survival advantage over cadaver
kidney transplant recipients. Smets et al11 compared the mortality of patients with type 1 diabetes
with renal failure in two geographic areas that differed in the frequency of simultaneous kidneypancreas transplantation: the Leiden area (73% simultaneous kidney-pancreas transplantation)
and non-Leiden area (37% simultaneous kidney-pancreas transplantation). Survival was adjusted
for age, sex, and duration of dialysis therapy pretransplantation. The hazard ratio for mortality
after the initiation of renal replacement therapy was 0.4 (95% confidence interval, 0.20 to 0.77; P
= 0.008) in the Leiden area compared with the non-Leiden area.
Tyden et al12 reported an 80% patient survival rate at 10 years in 14 SKPT recipients compared
with a 20% patient survival rate in 15 cadaver kidney recipients (10 patients who lost the
pancreas after simultaneous kidney-pancreas transplantation and 5 patients who opted for a
kidney alone, although eligible for simultaneous kidney-pancreas transplantation).
In the largest single-center report from the University of Wisconsin, Becker et al 14 showed that
SKPT recipients (n = 335) had an increased observed/expected life span compared with cadaver
kidney (n = 147) and living donor kidney (n = 160) recipients. The annual mortality rate was 1.5%
for SKPT recipients compared with 6.3% for cadaver kidney recipients and 3.7% for living donor
kidney recipients.
Patients with diabetes with renal failure have a high mortality on dialysis therapy. Wolfe et al 1
recently reported that death rates per 100 patient-years were 19.9 for all patients with diabetes on
dialysis therapy and 10.8 for patients with diabetes on the waiting list for kidney transplantation.
The risk for death decreased significantly after kidney transplantation (5.6 deaths/100 patientyears). However, patients with diabetes have a higher mortality after kidney transplantation
compared with patients without diabetes. Ojo et al15 reported that death with a functioning graft
was more common after kidney transplantation for diabetes compared with transplantation for
other causes of renal failure (RR, 1.93; 95% confidence interval, 1.82 to 2.05). In the present
study, the risk for death after simultaneous kidney-pancreas transplantation was 4.5/100 patientyears (8.2 in the first year and 3.4 thereafter).
How does a functioning pancreas graft prolong the survival of patients with end-stage renal
disease caused by diabetes? One possibility is by decreasing cardiac causes of death. It has
been shown that all groups of patients with end-stage renal disease have severely compromised
cardiac autonomic function, and patients with diabetes have the greatest degree of
dysregulation.16 Autonomic neuropathy, with abnormal cardiorespiratory reflexes, is associated
with high mortality, and several investigators reported that successful pancreas transplantation
may not only prevent the progressive decline, but also improve the function of cardiorespiratory
reflexes.17
Jukema et al18 recently reported that progression of coronary atherosclerosis, analyzed using
quantitative coronary angiography, is reduced in patients with a functioning pancreas graft
compared with patients with pancreas graft failure. Other studies have noted ongoing
improvements in echocardiographic parameters of cardiac function in SKPT recipients compared
with kidney-alone transplant recipients with diabetes.7,19 La Rocca et al19 and Tyden et al12
reported decreased death rates from cardiovascular causes in SKPT recipients compared with
kidney-alone transplant recipients. In a recent study, Larsen et al20 reported that carotid intima
media thickness, shown to correlate with cardiovascular events, is reduced after successful
pancreas transplantation. A favorable effect on lipid profiles also was shown in SKPT
recipients.21,22 In the present study, the proportion of deaths from cardiac causes is less in SKPT
recipients compared with kidney-only recipients. However, the high rate of deaths in the unknown
category in both groups makes it difficult to derive a definitive conclusion from the present study.
Although shortage of donor organs is the major factor limiting more widespread use of other solidorgan transplants, pancreas transplantation remains underused for other reasons: noncoverage
by third-party payers, lack of routine pancreas procurement, increased morbidity with the surgical
procedure compared with kidney transplantation alone, and the procedure being viewed as
enhancing quality of life, rather than improving life expectancy. With Medicare coverage effective
July 1, 1999, for simultaneous kidney-pancreas transplantation and sequential pancreas after
kidney transplantations, improving pancreas graft survival rates approaching or exceeding those
of other solid-organ transplants,23 a continued decrease in surgical complications, 24 and results of
long-term studies showing a survival advantage with simultaneous kidney-pancreas
transplantation, we believe pancreas transplantation should be considered a life-enhancing and
life-prolonging procedure in patients with type 1 diabetes with end-stage renal disease.
In summary, long-term survival of SKPT recipients is superior to that of cadaveric kidney
transplant recipients with type 1 diabetes because of donor organ quality, recipient selection, and
a functioning pancreas graft. This observation must be tempered because the conclusion is made
after analysis and adjustment for known risk factors, but other important selection factors may
remain unaccounted for. There is no difference in survival of SKPT recipients and living donor
kidney transplant recipients at up to 8 years' follow-up, with the former having a greater early
mortality risk and the latter having a greater late mortality risk. Results of this study suggest that
durable benefits of successful simultaneous kidney-pancreas transplantation may become even
more pronounced with longer follow-up.
References
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dialysis, patients on dialysis awaiting transplantation, and recipients of a first cadaveric
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2. Adang EMM, Engel GL, Van Hooff JP, Koostra G: Comparison before and after
transplantation of pancreas-kidney and pancreas-kidney with loss of pancreas—A
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simultaneous pancreas-kidney transplantation. Clin Transplant 12:233-242, 1998
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in autonomic and gastric function following pancreas-kidney versus kidney alone
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1998
8. Fioretto P, Steffes MW, Sutherland DER, Goetz FC, Mauer M: Reversal of lesions of
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