Kidney transplant with multiple renal artery

grafts from deceased donors: are long-term graft

and patient survival compromised?
BackgroundKidneys with multiple arteries are often transplanted. However, the
long-term outcome of such kidneys recovered exclusively from deceased donors is
not clear.
ObjectiveTo determine whether use of renal grafts with multiple arteries affects
long-term graft survival and function.
MethodsThe outcomes of 259 consecutive kidney transplants between 1996
and 2000 were retrospectively reviewed. Patients were divided into 2 groups, multiple renal artery graft recipients (n = 70) and single renal artery graft recipients (n
= 189). Short-term complications and long-term outcomes (survival rates, blood
pressure after transplant, creatinine clearance, and proteinuria levels at 1, 3, 5, and
7 years after transplant) were compared between the 2 groups.
ResultsEarly vascular complications were more common (P = .02) in multiple
artery graft recipients (18.6%) than in single artery graft recipients (7.9%), mainly
because of occlusion of a polar artery in grafts with multiple renal arteries (7.1%).
Urologic complications were no more frequent in one group than in the other
(5.7% vs 5.3%; P = .89). The 2 groups did not differ significantly (P = .33) in longterm graft survival, with a median follow-up of 9.05 years (range, 0.1-12.7 years).
Mean (SD) for creatinine clearance (59.4 [22.6] vs 55.9 [20.3] mL/min; P = .47),
proteinuria (0.77 [2.1] vs 0.4 [0.8] g/24 h; P = .19), and systolic blood pressure
(133.6 [14.5] vs 133.7 [17.5] mm Hg; P = .85) did not differ significantly between
the 2 groups 7 years after transplant.
ConclusionsKidney transplant with grafts containing multiple renal arteries
rather than grafts with a single renal artery does not significantly influence patient
and graft outcomes. (Progress in Transplantation. 2012;22:102-109)

Inass Laouad, Anne

Bretagnol, Elodie Fabre,
Jean-Michel Halimi, Azmi
Al-Najjar, Jean-Michel Boutin,
Franck Bruyre, Hubert
Nivet, Yvon Lebranchu,
Matthias Bchler
University Franois Rabelais, Tours,
France
Corresponding author: Dr Inass Laouad,
Nephrology and Kidney Transplantation
Department, Hpital Bretonneau, University Hospital Tours, 2, Bd Tonnell
37044 Tours cedex, France
(e-mail: inasslaouad@yahoo.fr)
To purchase electronic or print reprints,
contact:
The InnoVision Group
101 Columbia, Aliso Viejo, CA 92656
Phone (800) 899-1712 (ext 532) or
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E-mail reprints@aacn.org

2012 NATCO, The Organization for Transplant Professionals

doi: http://dx.doi.org/10.7182/pit2012992

MRA grafts: survival rates and serum creatinine levels

at 3 and 5 years after transplant did not differ significantly according to the number of arteries in the graft.
Other factors that are predictors of long-term graft
function have been reported, in particular proteinuria.5
The presence of multiple renal arteries might be associated with partial loss of nephronic mass after transplantation, leading to hyperfiltration by the remaining
nephrons and thus to the presence of proteinuria. Posttransplant arterial hypertension is also considered an
independent risk factor for graft failure,6 and a correlation has been reported in the general population
between arterial hypertension and the presence of multiple renal arteries.7
The aim of our study was to assess the impact of the
presence of more than 1 renal artery on complications

102

Progress in Transplantation, Vol 22, No. 1, March 2012

he renal vasculature is terminal and can be complex.1 Although considerable progress has been
made in surgical techniques in the past 30 years, grafts
with multiple renal arteries (MRA grafts) are still a
challenging problem. Transplanting a kidney with multiple arteries has several theoretical disadvantages linked
to the difficulty of the surgical management: the warm
ischemia time can be prolonged and the incidence of
acute tubular necrosis can be increased, thus impairing
graft function.2 Nevertheless, little information is available about the long-term outcome of kidney graft recipients who have received an MRA graft, particularly
from a deceased donor.
In previous studies3,4 that included kidney grafts
from deceased donors as well as living donors,
researchers reported the outcomes of recipients of

Kidney transplant with multiple renal artery grafts

immediately after transplant and on long-term survival of patients and grafts, as well as graft function,
including proteinuria and blood pressure.
Participants and Methods
A total of 259 consecutive kidney transplants
were performed with grafts originating from
deceased donors between January 1996 and December 2000 at our institution. Patients who received
grafts originating from living donors were not
included in this study, nor did it include patients
with no data available on their follow-up.
Immunosuppression
Most recipients received a sequential immunosuppressive regimen, with an induction through
antithymocyte globulins for the first 10 days or
interleukin-2 receptor blockers. Prednisone was
given at 1 mg/kg per day for the first 2 weeks, with
the dosage then progressively decreased and the
drug finally withdrawn within the first year after
transplant in immunologically low-risk patients.
Treatment with azathioprine (in patients who had
transplant surgery in January 1999 or before) or
mycophenolate mofetil (in patients who had transplant surgery after January 1999) was started on the
day of transplant, and anticalcineurin drugs
(cyclosporine A or tacrolimus) were added 3 to 5
days after transplant.
Surgical Management
All grafts in adult patients were performed by
surgeons from the Department of Urology at the
University Hospital Tours in Tours, France, and
grafts in children were performed by surgeons from
the Department of Pediatric Surgery. During graft
preparation, polar arteries were reimplanted on a
Carrel aortic patch if necessary. In grafts that had 2
arteries with 2 separate patches, these patches were
combined when the distance between the 2 vessels
allowed the patches to be combined without tension.
In cases with multiples arteries without patches
and a high distance between the vessels, each artery
was reimplanted separately on the iliac vessels. If a
vessel was too small and considered at high risk of
immediate thrombosis, the surgeon ligated the small
artery ex vivo.
During grafting, an end-to-side anastomosis of
the renal artery to the external iliac artery was constructed. If the graft had 2 arteries with 2 separate
patches, the patches were anastomosed separately to
the external iliac artery. The urinary tract was reimplanted by using the Lich-Gregoir technique, and a
double-J stent was systematically inserted and
removed 4 weeks later. All recipients received a preventive anticoagulant treatment postoperatively.
Progress in Transplantation, Vol 22, No. 1, March 2012

Parameters Studied
The existence of multiple renal arteries was defined
by the presence of more than 1 permeable artery when
anastomosis was performed. As a consequence, when
an artery had been ligated ex vivo, it was not considered an accessory artery.
Patient and Donor Characteristics. Data were
extracted from our database and from the patients
files. At the time of transplant, the recipients age, sex,
body mass index, and primary renal disease were
recorded, as well as the immunosuppressive induction
regimen and the graft rank (first, second, or third
transplant).
We recorded the duration of hospitalization after
transplant in the 2 study groups. The donors age, sex,
and cause of death were recorded. The immunosuppressive treatment was recorded at the 3-month consultation after transplant. Cold ischemia time was
defined as the time elapsed between clamping the kidney vessels during procurement and reimplanting
those vessels during transplant, and warm ischemia
time was defined as the time elapsed between removing the graft from the conservation liquid and revascularizing the graft.
Short-Term Complications (Arising During the
First Year After Transplant). To analyze the incidence
of immediate urological and vascular complications
after transplant, we defined the following terms:
Hemorrhage: the need for blood transfusion
within 3 days after transplant due to a perigraft
hematoma revealed by computed tomography.
Arterial thrombosis: the absence of systolic
blood flow on Doppler examination. In the case
of multiple renal arteries, Doppler examination
was systematically performed on all arteries.
Renal artery stenosis when confirmed by arteriography after being suspected on Doppler examination. Stenosis was considered significant if
the vessel lumen was reduced by 70% or more.
Recovery of graft function was defined as follows: normal, if creatinine levels were less than 250
mol/L at day 5, slow, if creatinine levels were higher
than 250 mol/L at day 5, and delayed if dialysis was
needed during the first week after transplant.
The incidence of biopsy-proven acute rejection,
defined as a score equal to or higher than IA according to the Banff 1997 classification, was also included
in our analysis.8
Long-Term Results. Renal function was assessed
at 1, 3, 5, and 7 years after transplant by using the
Cockcroft and Gault equation to calculate plasma creatinine clearance (normal value, >90 mL/min).9 Proteinuria level was measured on 24-hour urine collection

103

Laouad et al
by using the pyrogallol method10 (normal value, <0.007
g/L) at each time point studied and microalbuminuria
level using nephelometry 11 (normal value, <30
mg/24 h) at 7 years after transplant.
Posttransplant hypertension was defined according to the report of the Joint National Committee on
Prevention, Detection, Evaluation, and Treatment of
High Blood Pressure VII. 12 Systolic and diastolic
arterial pressures were measured after the patient
had rested supine for 15 minutes by using a sphygmomanometer appropriate for the patients arm size.
Patients treated with any antihypertensive medication
were also considered as having hypertension. We
recorded the total number of antihypertensive
drugs at each study time point and noted in particular
the presence of angiotensin-converting enzyme
inhibitors or angiotensin II receptor blockers.
Statistical Analysis
Results are expressed as means (standard deviations) and proportions. If the distribution of proteinuria was not normal, then median, minimum, and
maximum values are presented. Means were compared by using the Wilcoxon test. Proportions were
compared by using a 2 test or a Fisher exact test as
appropriate. Kaplan Meier curves were used for graft
survival. Log-rank analysis was used to compare graft
survival in patients with a single renal artery (SRA)
graft versus patients with an MRA graft. Analyses
were performed by using SAS 9.1 software (SAS
Institute Inc, Cary, North Carolina). A P value less
than .05 was considered significant.
Results
Recipient Characteristics
Of the 259 renal graft recipients (all from deceased
donors), 248 were adults and 11 were younger than 18
years old. Seventy patients (27%) received MRA
grafts and 189 patients (73%) received grafts with 1
artery (Figure 1).
Multiple arteries were implanted in a common
patch in 55 allograft kidneys. The arteries were anastomosed into 2 separate patches in 2 allografts. Surgeons performed patch combination in 12 cases, and
for 1 patient there was no patch.
Recipients and donors were significantly younger
in the MRA group than in the SRA group. No other
baseline characteristics differed significantly in the 2
groups (Table 1).
Immunosuppressive Treatment
The immunosuppressive treatment did not differ
significantly between the 2 study groups. Most patients
were treated with bitherapy including cyclosporine A
and mycophenolate mofetil. Corticosteroids were
progressively withdrawn according to an individual

104

All kidney recipients

(N = 263)
Data not available
(n = 1)
Living donor (n = 3)

Deceased donors
kidney recipients
(n = 259)

Multiple renal
artery graft
recipients
(n = 70)

3 arteries
(n = 6)

2 arteries
(n = 64)

Upper
polar
artery
(n = 23)

Lower
polar
artery
(n = 22)

Single renal
artery graft
recipients
(n = 189)

Equalsize
arteries
(n = 19)

1 upper
polar artery
+
1 lower polar
artery
(n = 4)

2
upper
polar
arteries
(n = 2)

Figure 1 Study population (N = 259) separated into 2 groups.

strategy. Forty-three percent of patients in the SRA

group (61 of 142) vs 53% of patients in the MRA group
(27 of 51) with a functional graft were still receiving
corticosteroids 7 years after transplant (P = .60).
Short-Term Complications
Vascular complications were significantly higher
in the MRA group, mainly because of occlusion of the
upper polar artery (Table 2). The rate of arterial stenosis was no higher in the MRA group than in the SRA
group. Episodes of hemorrhage, on the contrary, were
more common in the MRA group than in the SRA
group. The rates of urologic complications were similar in the 2 groups. Delayed and slow recovery of
renal graft function and duration of hospitalization did
not differ significantly between the 2 groups.
Long-Term Outcomes
Median follow-up period was 9.05 years (range,
0.1 to 12.7 years). Graft survival did not differ significantly (P = .33) between the MRA and SRA groups
(Figure 2). Patients survival was 95.7% (67 of 70) in
Progress in Transplantation, Vol 22, No. 1, March 2012

Kidney transplant with multiple renal artery grafts

Table 1 Characteristics of the study population
Multiple renal artery graft
(n = 70)

Single renal artery graft

(n = 189)

Donors
Age, mean (SD), y
Male sex
Cause of death (vascular)

38.0 (15.5)
44 (62.8)
38 (54.3)

42.1 (15.1)
96 (50.8)
117 (61.9)

.03
.07
.26

Recipients
Clinical characteristics
Male sex
Age, mean (SD), y
Body mass indexb

50 (71.4)
40.2 (13)
23.7 (4.2)

113 (59.8)
45.3 (15.1)
24.1 (4.8)

.11
.004
.67

Characteristica

Immunologic status
Graft rank (second/third)

5 (7.1)/0 (0.0)

15 (7.9)/1 (0.5)

.80

Methods of transplantation
Warm ischemia, mean (SD), min
Cold ischemia, mean (SD), min

51.8 (20.4)
1229.4 (396.2)

54.3 (17.9)
1235.3 (355.7)

.15
.75

Left kidney/left iliac fossa

13 (18.6)

34 (18)

.91

Left kidney/right iliac fossa

23 (32.8)

59 (31.3)

.80

Right kidney/right iliac fossa

16 (22.9)

35 (18.5)

.44

Right kidney/left iliac fossa

17 (24.3)

53 (28)

.54

Induction treatment
Interleukin-2 receptor blockers
Antithymocyte antibody
Other

4 (5.7)
54 (77.2)
12 (17.1)

18 (9.5)
142 (75.2)
29 (15.3)

.45
.61
.71

Immunosuppressive drugs at the 3-month visit

Cyclosporine
Tacrolimus
Sirolimus
Mycophenolate mofetil
Azathioprine
Corticosteroids

43 (66.1)
22 (33.8)
0 (0.0)
51 (77.3)
14 (21.2)
64 (98.5)

139 (77.2)
39 (21.6)
2 (1.1)
131 (72.8)
41 (22.8)
178 (98.9)

.06
.07
.61
.57
.76
.42

a Unless

otherwise indicated, values are expressed as number (percentage).

as weight in kilograms divided by height in meters squared.

b Calculated

the MRA group versus 92.6% (175 of 189) in the SRA

group (P = .40), and graft survival was 72.8% (51 of
70) in the MRA group versus 75.1% (142 of 189) in
the SRA group (P = .70) at 7 years after transplant
(Table 3).
There was a small decline in renal function in our
cohort during the follow-up period, with comparable
creatinine clearance levels observed in both groups at
each study time point (Table 4). Proteinuria level was
significantly higher in the MRA group than the SRA
group at 1 year, but the levels did not remain significantly different thereafter. Microalbuminuria levels
were also comparable in both groups 7 years after
transplant (360.5 [1321.2] mg/24 h in the MRA group
vs 197.9 [554.9] mg/24 h in the SRA group; P = .60).
Systolic and diastolic blood pressures did not differ significantly between the 2 groups during the
entire follow-up period, nor did the number of antihypertensive drugs taken per patient during the same
period (Table 5).

Progress in Transplantation, Vol 22, No. 1, March 2012

Discussion
We report here the long-term results (up to 12
years) for graft function and survival of patients who
received a kidney graft containing multiple arteries
that had been procured from a deceased donor, and
who had received uniform immunosuppressive treatment. Graft function at 7 years after transplant, including proteinuria, as well as graft and patient survival
did not differ between patients who received a graft
with multiple arteries and patients who received a
graft with 1 artery.
The presence of multiple renal arteries is the most
common variation in kidney anatomy.1 According to
several autopsy series, the incidence of multiple renal
arteries is between 8% and 47%.13 Multiple renal arteries were present in 70 of 259 (27%) renal grafts in our
cohort. Thus it is important to be aware of this particular feature, which occurs in about a third of all transplants from deceased donors. Surprisingly, MRA graft
recipients and donors in our study were significantly

105

Laouad et al
Table 2 Short-term outcome
Multiple renal artery graft
(n = 70)

Outcomea

Single renal artery graft

(n = 189)

Surgical complications
Hemorrhage

4 (5.7)

2 (1.1)

.04

Vascular complications
Arterial thrombosis
Polar artery occlusion
Renal artery stenosis
Venous thrombosis

13 (18.6)
2 (2.9)
5 (7.1)
4 (5.7)
1 (1.4)

15 (7.9)
4 (2.1)
0 (0.0)
8 (4.2)
3 (1.6)

.02
.61

Urologic complications
Ureteral stenosis
Ureteral fistulas

4 (5.7)
3 (2.9)
1 (1.4)

10 (5.3)
6 (2.7)
4 (2.1)

.64
.44
.32

23 (33.3)
17 (24.6)
19 (27.1)
20.9 (4.3)

47 (25.4)
37 (19.8)
52 (27.5)
20.7 (5.8)

.21
.39
.82
.29

Medical outcomes
Slow graft function
Delayed graft function
Acute rejection
Duration of hospitalization, mean (SD), d
a Unless

.81
.54

otherwise indicated, values are expressed as number (percentage).

Survival, %

100

80

P = .33

60
0

10

15

Years of follow-up
Multiple renal artery graft

Single renal artery graft

No. of patients at risk

Type of graft
Multiple renal artery
Single renal artery

Year 0

Year 5

Year 10

70

57

20

186

153

77

Figure 2 Kaplan-Meier graft survival according to the number of graft arteries.

106

Progress in Transplantation, Vol 22, No. 1, March 2012

Kidney transplant with multiple renal artery grafts

Table 3 Long-term outcome (7 years after transplant)
Outcome

Multiple renal artery grafta

(n = 70)

Single renal artery grafta

(n = 189)

Graft loss

18

45

.75

3 (16.6)
15 (83.4)

14 (31.1)
31 (68.9)

.24
.24

Cause of graft failure

Vascular origin
Acute or chronic rejection
Recurrence of renal disease
Other

3 (20.0)
8 (53.4)
2 (13.3)
2 (13.3)

8 (25.8)
14 (45.2)
5 (16.1)
4 (12.9)

.61
.54
.91
.78

Lost to follow-up

1 (1.4)

2 (1.1)

.71

Cause of graft loss

Death
Graft failure

a Values

are expressed as number (percentage).

younger than were recipients of SRA grafts. This age

difference may be due to the fact that in our center the
presence of multiple renal arteries was a reason to refuse
a graft recovered from elderly donors, who have a
higher incidence of vessel atherosclerosis. The shortage
of organs has compelled surgeons and nephrologists to
accept MRA grafts, and recent reports14-17 have shown
excellent results. Detection of a kidney with multiple
arteries in preoperative screening for living donor transplantation leads to the kidney not being recovered when
it could have been,4 because the presence of multiple
arteries procured without a patch suggests a higher
theoretical risk of vascular complications.
In a recent report18 of laparoscopic procurement
of kidney allografts from living donors, researchers
reported that kidneys with a single artery were associated with a lower risk of rejection, better function,
and superior long-term survival when compared with
kidneys with multiple arteries. Previous studies
including deceased and living donors have indeed
reported initial complications linked to the presence
of multiple renal arteries, such as prolonged warm
ischemia time,14 arterial thrombosis resulting in segmental infarction,19 and hemorrhage,15 without consequences for postoperative graft function, 3 but the

duration of hospitalization was not reported. The incidence of initial vascular complications, particularly
occlusion of a renal polar artery, also was higher
among MRA graft recipients in our cohort, but we did
not observe a longer warm ischemia time, nor any
effect on delayed or slow graft function, or a longer
duration of hospitalization.
The impact of multiple renal arteries on long-term
graft function (including hypertension and proteinuria) has been studied much less often. In our cohort,
renal function evaluated by plasma creatinine clearance 7 years after transplant showed no difference
between recipients of MRA grafts and recipients of
SRA grafts.
We were interested in proteinuria, which may be
a predictor of long-term graft survival.5 Considering
that the presence of multiple renal arteries results in a
higher frequency of segmental infarction,19 we supposed that the presence of multiple renal arteries could
induce a reduction in the nephronic mass, compensated for by hyperfiltration of the remaining nephrons.
We therefore expected that proteinuria, as a possible
marker of hyperfiltration, would be present earlier and
at higher levels in patients with MRA grafts than in
patients with SRA grafts. Although proteinuria was

Table 4 Evolution of creatinine clearance and proteinuria according to the number of graft arteries
Multiple renal artery graft

Single renal artery graft

Creatinine clearance, mean (SD), mL/min

Year 1
Year 3
Year 5
Year 7

64.1 (19.7)
60.8 (18.0)
64.5 (18.0)
59.4 (22.6)

60.0 (20.3)
58.3 (18.7)
60.9 (21.0)
55.9 (20.3)

.10
.35
.15
.49

Median proteinuria, median (range), g/24 h

Year 1
Year 3
Year 5
Year 7

0.24 (0-5.4)
0.18 (0-5.3)
0.21 (0-3.8)
0.77 (0-11.4)

0.10 (0-17.0)
0.15 (0-11.0)
0.16 (0-11.0)
0.40 (0-5.9)

.01
.35
.24
.19

Outcome

Progress in Transplantation, Vol 22, No. 1, March 2012

107

Laouad et al
Table 5 Evolution of blood pressures and number of antihypertensive drugs taken by person according to the number of graft
arteries.
Multiple renal artery grafta

Single renal artery grafta

Year

Feature

Systolic blood pressure, mm Hg

Diastolic blood pressure, mm Hg
No. of antihypertensive drugs

136 (17)
80 (10)
1.5 (1.0)

139 (18)
79 (10)
1.4 (1.1)

.32
.41
.37

Systolic blood pressure, mm Hg

Diastolic blood pressure, mm Hg
No. of antihypertensive drugs

134 (16)
77 (10)
1.6 (1.1)

137 (18)
79 (10)
1.7 (1.2)

.29
.19
.72

Systolic blood pressure, mm Hg

Diastolic blood pressure, mm Hg
No. of antihypertensive drugs

132 (18)
78 (10)
1.7 (1.2)

133 (18)
77 (10)
1.8 (1.4)

.62
.95
.59

Systolic blood pressure, mm Hg

Diastolic blood pressure, mm Hg
No. of antihypertensive drugs

133 (14)
78 (11)
1.9 (1.2)

133 (17)
77 (9)
2.0 (1.4)

.85
.62
.81

a All

values are expressed as mean (SD).

indeed significantly higher for MRA grafts than SRA

grafts at 1 year after transplant in our study, it was
similar in both groups at 3, 5, and 7 years after transplant. Moreover the level of microalbuminuria, which
might reflect hyperfiltration with a higher sensitivity,
was not different between our 2 study groups at 7
years after transplant. Other factors influencing the
level of proteinuria, such as diabetes mellitus and treatment with angiotensin-converting enzyme inhibitor,
angiotensin II receptor blocker, or sirolimus, were
equally represented in both groups.
Arterial hypertension is another independent risk
factor for graft failure.6 The role of multiple renal
arteries on the occurrence and control of posttransplant hypertension is unknown. Whereas a relationship has been described between multiple arteries on
native kidneys and increased blood pressure in the
general population,7 previous studies have not shown
an increased risk of posttransplant hypertension associated with kidney grafts with multiple arteries.20,21 We
found similar blood pressure levels in both groups,
with comparable immunosuppressive and antihypertensive treatments.
Finally, graft survival did not differ significantly
according to the number of arteries in the kidney graft
in our study, with a median follow-up of 9 years. Graft
survival at 10 years also did not differ among the
recipients of MRA grafts who had a thrombosis of the
main or polar arteries during the first year after transplant and the recipients of MRA grafts who did not
have arterial thrombosis (data not shown).
This study had some limitations. First, it was a
retrospective and observational study, and data were
collected from the surgery reports. Second, we did not
separate out grafts that needed ex vivo vascular reconstruction, making the group of patients with MRA grafts
heterogeneous, and we did not consider arteries that

108

had been ligated ex vivo as accessory arteries, even if

they could also be responsible for segmental infarction.
Conclusion
Kidney grafts with multiple renal arteries procured from deceased donors can be used with excellent outcomes. In our series, we found no difference in
short- and long-term patient and graft survival according to the number of renal arteries, despite more initial
vascular complications with MRA grafts. The prognostic factors of long-term graft survival, creatinine
clearance, proteinuria, and arterial hypertension did
not allow us to predict poor outcome for transplantation of renal grafts with multiple arteries.
Acknowledgments
The authors thank Doreen Raine for editing this paper.
Financial Disclosures
None reported.
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