Kidney International, Vol. 42 (1992), pp. 657—662
CLINICAL INVESTIGATION
Outcome of renal transplantation in children less than two
years of age
DAVID M. BRIscoE, MELANIE S. KIM, C1wG LILLEHEI, ANGELO J. ERAKLIS,
RAPHAEL H. LEVEY, and WILLIAM E. HARMON
Division of Nephrology, Department of Medicine, and Department of Surgery, Children's Hospital, and Departments of Pediatrics and
Surgery, Harvard Medical School, Boston, Massachusetts, USA
Although some centers have found an improved outcome of
Outcome of renal transplantation in children less than two years of age.
Twenty-two renal transplants were performed in 21 children less than
two years of age at Children's Hospital. Fourteen were from living
related donors and eight were from cadaveric donors. The five year
patient and graft survivals of these recipients were compared to all
other pediatric recipients between two and 18 years of age who received
renal transplants over the same time period. Five year graft survival for
recipients less than two years of age was 86% following living-related
donor transplantation and 38% following cadaver donor transplantation. Older pediatric recipients aged between two and 18 years had a
five year graft survival of 73% following living-related donor renal
transplantation, which was similar to that for recipients less than two
years of age. Although older cadaveric recipients had a comparable five
year graft survival to younger recipients, at 42%, the patterns of graft
loss were different. Graft failures in young recipients occurred within
renal transplantation in young recipients [11—13], most have not
reported on the outcome of recipients at highest risk, namely
those less than two years of age. Table 1 contains the outcome
of renal transplantation in children less than two years of age
extracted from eleven reports. A large series from The University of Minnesota found that the outcome of transplantation in
children less than two years of age was similar to that found in
an older pediatric population with a better graft survival from
living related donors than cadaver donors [11]. None of these
reports, however, analyzed the causes of patient and graft
failures following living and cadaveric transplants in children
less than two years of age as compared to an older comparable
population. Moreover, these reports encompass two decades of
transplant experience in a variety of transplant centers. In this
report, we have directly compared the outcome of living and
cadaveric renal transplantation in recipients less than two years
patient survival than older recipients following both living-related donor
renal transplantation (P = 0.06) and cadaver-donor renal transplanta- of age with those between two and 18 years of age, all of whom
tion (P < 0.05). These findings suggest that the graft survival of received renal transplants at Children's Hospital over the same
living-related donor renal transplantation in recipients less than two time period. In addition, in order to better define the reasons for
years of age is better than that of cadaver-donor renal transplantation.
differences in survival between younger and older children, we
Furthermore, graft survival of living-related donor renal transplantation
in children less than two years of age is the same as that in older have also analyzed the causes of graft failure and death in all
recipients less than two years of age.
children, although patient survival in the younger group may be slightly
the first seven months post-transplant, whereas the older recipient's
grafts failed more gradually. Actuarial five-year patient survival in
recipients less than two years of age was 86% following living-related
donor renal transplantation and 70% following cadaver-donor renal
transplantation. Recipients less than two years of age had a poorer
decreased.
Methods
Twenty-one children less than two years of age have received
Young recipients of renal transplants are reported to have a 22 renal transplants at Children's Hospital. One transplant was
poorer long-term outcome than older children and adults [1—81. performed in 1974 and all others between 1980 and 1990.
Both individual and multicenter reports have demonstrated
Surgical management
poor outcome of renal transplantation in young recipients and
The
surgery
was
intraperitoneal
via a transabdominal incihave recommended that renal transplantation be deferred until
sion.
During
surgery,
the
infant's
central venous pressure
children are older [2, 3, 91. A recent multicenter report concluded that recipient age less than two years was an indepen- (CVP), blood pressure, and urine output were continuously
dent risk factor for outcome of renal transplantation [1].
Moreover, despite the uncertainty of outcome of renal transplantation in young children, the frequency of this procedure is
monitored. Briefly, the right colon was mobilized to expose the
infrahepatic inferior vena cava and the distal infrarenal aorta.
The donor renal vein was anastomosed end-to-side to the
apparently increasing [10].
inferior vena cava. Prior to the arterial anastomosis and cross
Received for publication November 6, 1991
and in revised form February 19, 1992
Accepted for publication April 6, 1992
heparin. The donor renal artery was then anastomosed end-toside to the infrarenal aorta. Reperfusion of the newly implanted
kidney was performed once the infant's CVP was raised at least
to 15 cm of water by administration of colloidal fluids including
packed red cells and 5% albumin. Mannitol, furesomide and
© 1992 by the International Society of Nephrology
clamping of the aorta, the patient was anticoagulated with
657
658
Briscoe et al: Pediatric renal transplantation
Table 1. Renal transplantation in chil dren less than 2 years of age
One year
graft
No. of
transplants
Year
Najarian (1990)
Reference
[11] aged <1 yr
aged 1—2 yrs
Kalia (1988)
Oberkircher (1987)
Kohaut (1985)
Ellis (1985)
Campbell (1984)
Harmon (1982)
Moel (1981)
Lawson (1975)
Cerelli (1972)
LaPlante (1970)
[27]
[28]
[29]
[30]
[31]
[32]
[9]
[331
[34]
[35]
survivala
LRD CAD LRD CAD
4
4
8
2
3
—
18
44
—
I
—
—
3
6
3
1
—
12
1
2
—
—
I
2
94% 25%
83% 50%
50% 50%
—
0
100% —
—
—
0
0
100% 20%
Results
Twenty-two transplants from 14 living and eight cadaveric
donors were performed in 21 children less than two years of
age. Overall follow-up time ranged from 0.75 to 9.75 years with
a mean of 5.2 years for living related and 4.3 years for cadaveric
transplants. The distribution of living and cadaveric transplants
over the years of this study is illustrated in Figure 1.
Recipients
The primary renal diseases of the recipients are listed in
Table 2. Fourteen patients, 10 males and four females, between
ages of 1.1 and two years (mean age 1.4 years) received
— 16% the
primary living-related allografts. None of these were retrans0
0
—
0
— 100%
Calculated by life table analysis
plants. All fourteen patients received ATS/prednisone/azathioprine immunosuppression and seven patients received donor
specific transfusions prior to the transplant. None of these
patients received cyclosporine.
Seven patients, four males and three females, between the
ages of two weeks and 1.9 years (mean 1.2 years) received
cadaveric allografts. One of these patients received a second
solumedrol were also administered at this time. During reper- cadaveric transplant. Three patients received cyclosporine as
fusion, blood pressure and CVP were maintained by the admin- part of the immunosuppressive regimen.
istration of colloidal fluids as required. The ureter was implanted into the bladder through an anterior cystotomy using
the Leadbetter-Politano technique. This surgical approach was
different than that used for older children [14].
Immunosuppression
The immunosuppressive regimen for children less than two
years of age was identical to that used for all other patients.
Initially prednisone was commenced at a dose of 2 mg/kg/day
and was tapered over one year to 0.5 mg/kg on alternate days;
azathioprine was commenced at 4 mg/kg/day and was reduced
to 2 mg/kg/day over the first six weeks. In addition, prophylactic rabbit-anti-human-thymocyte serum (ATS, produced in our
laboratories) was administered to all patients [15]. Starting in
1982, all recipients of cadaveric allografts were treated with
cyclosporine. Cyclosporine was commenced seven days following transplantation at a dose of 4 mg/kg/day, provided that renal
function was normal, and was adjusted to maintain whole blood
levels between 50 to 150 .tg/liter. Prophylactic ATS was discontinued two days after the initiation of cyclosporine. All
primary recipients of living related transplants were treated
with ATS/prednisone/azathioprine in the same regimen, de-
scribed above, for cadaveric transplants. Starting in 1982,
Donors
The possibility of living related donor and cadaver donor
renal transplantation was discussed with each patient's family.
Donor selection was based upon the availability of living related
donors, family preference as to the choice of donor and the
potential of using an adult kidney in a very small recipient.
There were eight maternal and six paternal living-related donors
aged between 19 and 36 years, mean age 28 years. All donors
were one haplotype identical to the recipients. Cadaver donor
ages and number of HLA A, B and Dr mismatches to the
recipients are shown in Table 3. Donor ages ranged from 11
months to 36 years; two donors were aged less than three years.
All cadaver donor kidneys were obtained through the New
England Organ Bank.
Graft failures
Three living-related grafts were lost at three months, 1.1
years and 6.1 years post-transplant. Two of these losses were in
patients who died, one as a result of pneumocystis carinii
pneumonia and the other from a diffuse vasculitis of unknown
etiology; both grafts were functioning at the time of death. The
other graft failed as a result of chronic rejection.
Table 3 contains information about cadaveric donors and
recipients of one haplotype matched living-related transplants
received donor-specific blood transfusions. Rejection episodes details of graft outcome. Five cadaveric grafts were lost: at 24
were treated with pulse solumedrol (total dose 52 mg/kg given hours, two weeks, one month, four months and seven months
over 8 days), and OKT3 (2.5 to 5 mg/day for 14 days) has been post-transplant. Two of these patients died, one perioperatively
and another from bacteremia. Two other grafts failed as a result
used to treat steroid resistant rejection beginning in 1987.
of rejection and one was lost as a result of a graft thrombosis;
Patient and graft survival
the latter patient successfully underwent a retransplantation
Patient and graft survival were evaluated by standard life three months later at 1.9 years of age.
table analysis [16]. Survival rates were calculated at two
monthly intervals for a total of five years. All patients were
Patient and graft survival
included in the analysis with no exclusions. Graft failure was
In children less than two years of age the actuarial five-year
defined as a return to dialysis or death, even if the graft was patient survival was 86% for recipients of living related transfunctioning at the time of death. The log rank test was used for plants and 70% for recipients of cadaveric transplants. Graft
survival was 93% at one year and 86% at five years for
statistical analysis of survival rates.
659
Briscoe et al: Pediatric renal transplantation
3
0)
C
2
0)
(0
0
0)
.0
E
=
z
0
1974
1980 1981 1982 1983 1984 1985 1986 1987 1988 1989
Year of transplant
Table 2. Primary renal di seases and mode of transplant
Mode of
transplant
LRD
CAD
Renal dysplasia
Congenital nephrosis
Prune belly syndrome
Arteriovenous occlusion
Obstructive uropathy
Hemolytic uremic syndrome
Nephronophthisis
Total
2
1
1
1
8
4
4
2
2
transplants performed in recipients less than 2
years of age.
(P < 0.05) transplants. However, patient survival following
6
3
2
1
Fig. 1. The distribution of living related
donor () and cadaver donor () renal
0
1
0
1
1
1
0
1
living-related donor transplants was similar to that for cadaver
donor transplants in children less than two years of age and in
children two to 18 years of age.
Discussion
The results of this study show that the long-term graft
survival of living-related donor renal transplantation in young
children is excellent and is comparable to that achieved in older
children. Five year graft survival was 86% in children less than
two years of age as compared to 73% in older children,
representing the remainder of the pediatric population who
recipients of living related transplants as compared to 38% at
both one and five years for recipients of cadaveric transplants
(Figs. 2 and 3). For comparison, we analyzed the survival rates
for all older children between two and 18 years of age who
received renal transplants in Children's Hospital over the same
time period (January 1980 until January 1990). These included
both primary transplants and retranspiants. All of these patients
had received the same immunosuppressive regimen as children
less than two years of age following both living related and
cadaveric transplants. Of the 52 living-related transplants in
these older children, five were from HLA identical donors, one
of which failed as a result of a graft thrombosis. Actuarial
five-year patient survival was 98% for recipients of living
related transplants and 93% for recipients of cadaveric transplants. Graft survival was 88% at one year, 73% at five years
following living related transplants, and 73% at one year and
42% at five years following cadaveric transplants.
Analysis of five year patient and graft survivals is shown in
Table 4. Graft survival following living-related donor transplants was significantly better than cadaveric transplants for
both younger (P < 0.05) and older (P < 0.01) children. When
the graft survival for younger children (<2 years of age) was
compared to that for older children (>2 years of age), survival
at five years was similar following both modes of transplant.
Patient survival was better in older children. This improved
survival occurred following both living (P = 0.06) and cadaveric
received living-related donor renal transplants during the same
time period. In other reports of renal transplantation in young
recipients, poor graft survival was attributed to technical problems and graft thrombosis [3, 17], and to a suspected heightened
cellular immune response [18—20]. In this report there were no
technical failures or graft thromboses following living-related
donor renal transplantation in children less than two years of
age; rejection episodes were infrequent (data not shown) and no
grafts were lost to acute rejection, even though these patients
did not receive cyclosporine. Three of the 14 living related
allografts failed. Two recipients died, one from pneumocystis
carinii pneumonia and the other from a chronic hemolytic
anemia and diffuse vasculitis. Another graft failed as a result of
chronic rejection.
The long-term graft survival of living-related donor renal
transplantation was significantly better than cadaveric donor
renal transplantation in recipients of all ages. In particular, in
recipients less than two years of age, the five year graft survival
was 86% following living-related donor transplantation as com-
pared to 38% following cadaveric transplants. The five year
graft survival for cadaver donor renal transplants reported here
is lower than what is currently expected [1]. However, the data
for this report were collected over the past 15 years. Cadaveric
donor renal transplant graft survival has improved significantly
during the past decade for adults [21] and children [2, 12, 22,
231, likely due to improvements in immunosuppression and
donor selection. Lack of treatments such as cyclosporine and
660
Briscoe et al: Pediatric renal transplantation
Table 3. Cadaveric donor and recipient age, tissue typing and graft outcome
HLA
mismatche?
Donor age
4 years
7 years
10 years
13 years
N/A
29 yearsb
36 years
0/6
5/6
Cyclosporine
No
No
No
Yes
No
No
Yes
Yes
Recipient age
4/4
2/6
N/A
4/4
5/6
11 months
2 yearsb
1.5 years
1.6 years
12 days
1.0 years
1.2 years
1.4 years
1.9 years
1.3 years
Graft outcome
Time of graft loss
Rejection
Thrombosis
Died perioperatively
Function at 7.4 years
Chronic rejection
Died of sepsis
Function at 3.6 years
Function at 1.9 years
2 weeks
I day
—
7 months
4 months
—
—
1 month
Abbreviation is: N/A, not available.
a x/4 = HLA A,B only, x/6 = HLA
A,B,Dr
b Same
recipient
52
40
100. —I
90
0
-j
>
28
27
24
19
10
9
8
6
90
l2L
80
ci.
80
70
70
60
a,
50
a,
100
50
40
30
0
-J
20-
20
10-
10
00
0
12
24
36
48
60
19
11
9
100
>
'
70
60-
50a)
C
a)
ci-
40
20
20
10-
10
0
0—
0
12
24
36
48
60
Time, months post-transplant
Fig. 2. Patient survivals following living related donor (LRD) and
cadaver donor (CAD) renal transplantation in children less than 2 years
of age (. - -) and 2 to 18 years of age (—) at the time of transplant.
the use of young cadaver donors may have accounted for some
of the graft losses in recipients of cadaveric transplants in this
report. All five of the patients who did not receive cyclosporine
following cadaver donor transplantation lost their grafts. Two
of these grafts were lost before cyclosporine could have been
started (one perioperative death and one early graft thrombosis)
but the other three losses were associated with severe rejection
48
60
27
L1
0
o 30
36
36
C)
30
24
53
90
80
70
60
50
8
80
12
0
90 L_
0
0
60
0
3
3
2
12
24
36
11
9
48
60
Time, months post-transplant
Fig. 3. Graft survivals following living related donor (LRD) and ca-
daver donor (CAD) renal transplantation in children less than 2 years of
age (- - -) and 2 to 18 years of age (—) at the time of transplant.
episodes. Furthermore, multiple reports have shown that graft
survival is reduced for several reasons when the cadaver donor
is young [1—3, 17]. All three grafts from cadaver donors less
than five years of age were lost. One of these losses was due to
graft thrombosis, the incidence of which has previously been
shown to be correlated with young donor age [17].
In this report, there were marked differences in the patterns
661
Briscoe et al: Pediatric renal transplantation
Table 4. Analysis of five-year patient and graft survivals
Patient survival
Graft survival
Age
Mode
% Survival
<2 years
>2 years
<2 years vs. >2 years
<2 years vs. >2 years
<2 years
>2 years
<2 years vs. >2 years
<2 years vs. >2 years
LRD vs. CAD
LRD vs. CAD
LRD
86% vs. 70%
98% vs. 93%
86% vs. 98%
70% vs. 93%
86% vs. 38%
72% vs. 42%
86% vs. 72%
38% vs. 42%
CAD
LRD vs. CAD
LRD vs. CAD
LRD
CAD
P value
P
NS
NS
= 0.06
P < 0.05
P < 0.05
P < 0.01
NS
NS
P is calculated by the log rank test; NS, not significant.
of graft survival curves seen following cadaveric transplantation. Graft losses in young children occurred within the first
seven months post-transplant, whereas in older children graft
failures occurred more gradually. Although the overall five-year
cadaveric transplant survival in young children was statistically
comparable to that seen in older children, the different survival
curve patterns may be attributed to differences in the causes of
graft loss. Of the eight cadaveric transplants in children less
than two years of age, two patients died, one perioperatively
and one of sepsis four months post-transplant and after several
rejection episodes; the other three graft losses were due to a
graft thrombosis and rejection two weeks, one month and seven
months post-transplant, respectively. The more gradual graft
losses in older recipients over three to four years were likely
due to chronic rejection.
The higher mortality found in younger children following
both living related and cadaveric transplants was of concern.
The actuarial five-year patient survival rate was 86% for young
recipients of living-related donor renal transplants and 98% for
their older counterparts (P = 0.06). Young recipients of cadaveric allografts had a five year patient survival rate of 70% as
compared to 93% for their older counterparts (P < 0.05).
Overall, four patients died, two from infections, one from a
diffuse vasculitis of unknown etiology and another periopera-
tively. A high mortality rate has also been found in young
recipients following renal transplantation at other centers [3, 5].
The alternative therapeutic option for these children is chronic
dialysis which, in older children, has a comparable five year
patient survival rate as both living related and cadaveric donor
transplants [24]. Most infants in this study were treated for
renal insufficiency and uremia since birth and except for one
infant, received renal transplants between one and two years of
age. The one year mortality in this report was 7% following
living-related donor renal transplants and 30% following ca-
high risk for graft loss [2, 3]. This suggestion has been controversial, however, since one center has recommended that renal
transplantation should be offered to children in this age group,
and has reported that their outcome can be excellent [11]. The
results reported here are similar and confirm that graft survival
in children less than two years of age can be as good as that
achieved in older children and adults.
Recommendations for the treatment of infants with end-stage
renal disease remain controversial. The results demonstrated in
this paper confirm that transplantation, be it living related or
cadaveric, may be best deferred until the infant is large enough
to receive an allograft from an adult, which is usually attainable
by one year of age [26]. There are no studies which directly
compare the patient survival rates of dialysis and renal trans-
plantation in this age group. Based on the available data,
however, we would suspect that the mortality associated with
the two treatments is similar. Furthermore, there is no difference in graft outcome between children less than two years of
age and their older counterparts. Thus, the decision to delay
transplantation should only be based upon the infant's size,
growth and development and not the risk of death or graft loss.
In summary, we have found that the graft survival following
renal transplantation in recipients less than two years of age is
the same as that achieved in older recipients. Graft survival
following living-related donor renal transplantation is better
than cadaver donor renal transplantation, for younger as well as
older pediatric recipients. However, the mortality following
both forms of transplantation is increased in younger recipients.
We conclude that living-related donor renal transplantation is a
safe and effective treatment for young children less than two
years of age with end-stage renal disease. Living-related donor
renal transplantation provides a better outcome than cadaverdonor renal transplantation in these patients.
daver donor renal transplants. The one year mortality of
chronic dialysis in children aged between zero to one year of
age is 22% and in children aged between one and five years of
age is 12% [25]. There are, however, no reported data on the
mortality of dialysis in one to two year old children and thus no
direct comparisons of the mortality risks of dialysis and renal
transplantation in this age group are possible. Further analysis
will be necessary to evaluate the effect of therapy on long-term
patient survival in this younger age group.
Recent multicenter studies have concluded that graft outcome is poor in recipients less than two years of age [1, 4].
Thus, some programs have suggested the deferral of transplantation in these patients until they are older and are no longer at
Acknowledgments
This work was presented in part at a meeting of The American
Society of Nephrology, December 1989 and has been published in
abstract form in Kidney International 37:603,1990. DMB is supported
by a Physician-Investigator Award from the American Heart Associa-
tion, Massachusetts Affiliate Inc. and a Farley Fellowship Award,
Children's Hospital, Boston. We acknowledge Hugh Brady M.D. for
his critical review of the manuscript, Richard Gelber for statistical
analysis, and Michele Topor RN and Man Drew BSN for their
assistance in obtaining patient information.
Reprint requests to William Harmon, M.D., Division of Nephrology,
The Children's Hospital, 300 Longwood Avenue, Boston, MassachuSetts 02115 USA.
662
Briscoe et al: Pediatric renal transplantation
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