Abstract. Factors which influence graft function can be divided
intodonor factors that affect both kidneys from the same donor equallyand
postdonor factors that affect each kidney individually.This study assessed
the influence of donor factors on graftfunction early after transplantation.
Sixty-one donors who providedkidneys that were transplanted locally into two
separate recipientswere identified. Recipient creatinine clearance values
wereestimated from serum creatinine concentrations using a computermodel.
Pairwise ANOVA showed that donor factors accounted for35 to 45% of the
variation in recipient creatinine clearancefrom 2 d to 2 wk
posttransplantation. Although donor factorshad a large aggregate effect
during this period, individualfactors that influenced graft function could
not be identifiedfrom analysis of donor medical records. At 6 mo after
transplantation,the effect of donor factors on graft function was no longer
discernible.These results show that the condition of the donor exerts an
importantinfluence on graft function early after transplantation. More
detailedstudy is required to identify individual factors that contributeto
this effect.
Function of cadaver kidneys over the first few days after transplantation
rangesfrom near zero to normal
(1,2,3,4).
Most of the kidneys thatexhibit poor initial function eventually recover
adequate function.Delayed function, however, has significant adverse
consequences.It prolongs hospitalization and complicates immunosuppressive
therapy.In addition, when defined by a requirement for dialysis duringthe
first week after transplantation, delayed function is associatedwith an
increased incidence of acute rejection and increasedrate of graft loss over
the first year
(5,6).
Some, althoughnot all, studies have found that delayed function is also
associatedwith an increased rate of late graft loss
(5,6,7,8,9).
Delayed graft function is generally attributed to reperfusioninjury
following renal ischemia
(1,2,3,4).
The factors thatcause some grafts to exhibit delayed function while others
functionpromptly, however, are poorly understood. Theoretically, these
factorscan be divided into two groups. The first group is composedof
"donor factors," which should affect both kidneys from thesame
donor equally. These could include features of the donor'smedical condition
before the injury which caused brain death,the nature of this injury, and
events during the terminal hospitalizationand procurement surgery. The second
group is composed of "post-donor"factors, which are not expected
to affect both kidneys fromthe same donor equally. These could include
consequences ofcold ischemia, features of the recipient's medical condition,
andevents during transplant surgery and subsequent hospitalization.The
current study compared the influence of donor and postdonorfactors by
analyzing the extent to which kidneys from the samedonor exhibit similar
function posttransplantation.
Records of the California Transplant Donor Network (CTDN) for1996 were
reviewed to identify donors who provided kidneys transplantedlocally into two
separate recipients. Of a total of 185 kidneydonors during the year, 57 were
excluded because one or bothkidneys were transplanted outside the network, 37
were excludedbecause another organ was transplanted along with the kidneyin
at least one recipient, 14 were excluded because both kidneyswere
transplanted into the same recipient, 13 were excludedbecause one kidney was
discarded, and an additional three wereexcluded because they were under 10 yr
of age. The remaining61 donors and the 122 recipients of their kidneys were
includedin this study.
Donor clinical data were obtained from a computerized databasemaintained
by CTDN. Donor creatinine clearance values were estimatedusing the formula of
Cockcroft and Gault (10) for
adults andthe formula of Schwartz et al.
(11) for adolescents.
Recipientdata were obtained from medical records maintained by the local
transplantcenters and referring nephrologists. Creatinine clearance during
theperiod from 24 to 72 h after transplantation was estimated usinga
modification of the method described by Moran and Myers
(12).The age, gender, and
weight of the recipient, the time of implantation,and all recorded serum
creatinine values and the times at whichthey were measured were entered into
a computer program. Theprogram then estimated serum creatinine values at 24,
48, and72 h by interpolation and calculated the average serum creatinine
concentrationover 24 to 48 and 48 to 72 h. Body creatinine content was
calculatedas the product of serum creatinine concentration and body water
content.Values for creatinine clearance during 24 to 48 h and 48 to72 h
posttransplantation were then obtained from the appropriatevalues for serum
creatinine concentration, body creatinine content,and creatinine production
as estimated by the formulas of Cockcroftand Gault and Schwartz et
al. In recipients who were hemodialyzed,clearance values were calculated
after excluding the periodbetween the last serum creatinine measurement
before dialysisand the first creatinine measurement after dialysis. Records
ofdialysis time and/or serum creatinine levels were insufficientto allow
this correction for the period from 24 to 48 h in threepatients and for the
period 48 to 72 h in nine patients. Inthese patients, clearance values were
calculated without correctingfor dialysis. When the uncorrected values were
less than 10ml/min, they were used in the analysis. In other patients, the
clearancewas set at 10 ml/min. In the two recipients who underwent peritoneal
dialysis,the computer-generated creatinine clearance values were lessthan 12
ml/min, and no attempt to correct them for dialyticclearance was made.
Creatinine clearance values at 2 wk and6 mo were estimated using the formulas
of Cockcroft and Gaultand Schwartz et al. The clearance at 2 wk was
calculated usingthe average of all serum creatinine values from day 13 to day
15in 100 patients. When no creatinine values were available fromthis
interval, values were averaged from day 12 to 16 (18 patients)or from day 9
to 19 (4 patients). The clearance at 6 mo wascalculated using the average of
all serum creatinine valuesfrom 4 to 7 mo excluding values obtained during
episodes ofacute rejection. One recipient who died and one recipient whowas
lost to follow-up were excluded from analysis so the numberof pairs analyzed
at 6 mo was 59. Graft creatinine clearancewas recorded as zero in two
patients who underwent transplantnephrectomy and had returned to dialysis at
6 mo. Episodes ofacute rejection during the first 6 mo, established by biopsy
orby use of pulse immunosuppressive therapy to reverse increasesin serum
creatinine, were identified by review of clinic records.
Statistical Analyses
The relation of function in kidneys from the same donor wasassessed using
a modification of the method described by Cosioet al.
(13). Recipients of kidneys
from the same donor werefirst randomly designated the "A"
recipient and the "B" recipient.An ANOVA was then used to
estimate the contribution of donorfactors to the total variation observed in
graft function. Forthis analysis, the difference between graft function in an
individualrecipient and the mean graft function µ of the study groupwas
assumed to be the sum of two normally distributed variables.The first of
these variables, Fi, represented the portion ofthe
difference ascribable to donor factors and thus had thesame value for both
kidneys from the ith donor. The second,Eij with
j = A or B, represented the portion of the differenceascribable to postdonor
factors and thus had a different valuefor each kidney. The posttransplant
clearance values xiA andxiB for the
two kidneys of the ith donor were thus expressedas:
(1)
and
(2)
The values of Fi and Eij in
individual patients could not bedetermined, but the average magnitude of
Fi and Eij could beobtained from the
related variables fi and ei, where:
(3)
and
(4)
It will be seen that fi reflected the degree to which
the averagefunction of a pair of kidneys differed from the grand mean µ
andthat ei reflected the degree to which function in two
kidneysfrom the same donor differed from each other. Standard ANOVA
calculationsprovided values for fi2,
ei2, and the "sum of
squares," where:
(5)
Since the values for Eij and Fi
were presumed to be normallydistributed and the number of pairs was large,
values for Eijand Fi obeyed the
relationships:
(6)
and
(7)
The latter relationship reflects the tendency of the real influenceof
recipient factors Eij to have a greater magnitude than
calculatedvalues for ei. Relationships 6 and 7 were
combined to obtain:
(8)
The fraction of the overall variability of graft function thatwas
attributable to donor factors was then estimated as:
(9)
The 2 test was used to determine whether there was a
tendencyfor both recipients of kidneys from the same donor to be dialyzed
duringthe first 4 d posttransplantation. The contribution of individualdonor
factors to graft function posttransplantation was assessedby linear
regression for parametric variables and by unpairedt test for
nonparametric variables. All statistical calculationswere done with a
standard software program (StatView 4.5, AbacusConcepts, Berkeley, CA).
Values are presented as the mean ±1 SD throughout.
Clinical data for the donors are summarized in
Table 1. Themean age was 38
± 15 yr, and there were 21 women and40 men. The serum creatinine value
immediately before procurementwas 1.0 ± 0.3 mg/dl. The maximum serum
creatinine recordedduring hospitalization was slightly higher, averaging 1.2
±0.4 mg/dl, but did not exceed 2.2 mg/dl in any patient. Bodyweight
was 80 ± 22 kg and the estimated creatinine clearancebefore
procurement was 114 ± 36 ml/min. The durationof the terminal
hospitalization was 59 ± 37 h. Braindeath was attributed to trauma in
24 patients, to cerebrovascularaccident in 29 patients, and to other causes
in eight patients.
Table 1. Clinical characteristics of the 61 donorsa
Kidneys from the 61 donors were transplanted into 53 women and69 men with
an average age of 49 ± 15 yr. Graft functionin the recipients is
summarized in Table 2. Serum
creatininewas 6.3 ± 3.8 mg/dl over the period from 24 to 48 h
postimplantationand 5.6 ± 3.8 mg/dl over the period from 48 to 72 h
postimplantation.The large SD in these values reflected a wide range of early
graftfunction. Creatinine clearance values estimated from body sizeand the
rate of change in serum creatinine varied from nearzero to near normal.
Thirty-four of the 122 recipients weredialyzed over the first 4 d
postimplantation. The average serumcreatinine declined to 2.8 ± 2.5
mg/dl at 2 wk and 1.8± 1.3 mg/dl at 6 mo.
Regression plots revealed that early function in kidneys obtainedfrom the
same donor tended to be similar, as depicted in
Figure 1.By 6 mo after
transplantation, this tendency was no longerapparent, as depicted in
Figure 2. Estimates of the
relativeinfluence of donor and postdonor factors on graft function are
summarizedin Table 3. Values
for Fi2 were between 35 and 45% of the
totalsum of squares at 24 to 28 h, 48 to 72 h, and 2 wk after
transplantation.These results indicate that donor factors accounted for
slightlyless that half of the variability in graft kidney function duringthe
early posttransplant period. In contrast, the value forFi2 was only 10% of the total sum of squares at
6 mo, indicatingthat the residual effect of donor factors accounted for very
littleof the variability in graft function observed at this interval.As
illustrated in Figure 3, the
influence of donor factors onearly function could not be detected when
dialysis was usedas the only index of poor function. Both recipients of
kidneysfrom the same donor were dialyzed during the first 4 d in onlyfour
patients. This number was not greater than that which wouldhave resulted from
chance alone given a 28% overall frequencyof dialysis during this interval
(2 = 0.2, P > 0.6). Goodgraft function during the
early posttransplant period was associatedwith a reduced incidence of acute
rejection over the first 6mo. The median estimated clearance at 24 to 28 h
was 22 ml/min.Acute rejection was observed in 19% of patients with clearance
valuesgreater than the median and in 38% of patients with clearancevalues
less than or equal to the median (2 = 5.1, P <
0.05).Very good early graft function was associated with a still lower
incidenceof acute rejection. Acute rejection was observed in only 7%of
patients whose estimated clearance values at 24 to 48 h fellin the upper
quartile (42 ml/min, 2 = 8.8, P < 0.01).
Figure 1. Early function of graft kidneys from the same donor. Creatinine clearance
values for kidneys from the same donor tended to be similar during the first 2
wk after transplantation. Linear regression yielded values of
r2 = 0.13, P < 0.005 at 24 to 48 h,
r2 = 0.16, P < 0.002 at 48 to 72 h, and
r2 = 0.12, P < 0.006 at 2 wk.
Figure 2. Function at 6 mo of graft kidneys from the same donor. The tendency for
kidneys from the same donor to exhibit similar creatinine clearance values is
no longer apparent.
Figure 3. Dialysis during the first 4 d in recipients of kidneys from the same donor.
The influence of donor factors could not be detected when dialysis was used as
the only index of poor function.
The relation of graft function to individual donor factors issummarized in
Table 4. The table presents
creatinine clearancevalues at 24 to 48 h, but similar results were obtained
whencreatinine clearance values at 48 to 72 h and 14 d were analyzed.Grafts
from donors without a history of hypertension appearedto function better than
grafts from donors with such a history.This relation could not be assigned
statistical significanceby conventional criteria, however, because correcting
for analysisof multiple variables would raise the P value above
0.05. Otherfeatures of the donor medical history, including death at ayoung
age and death due to trauma, did not exert a detectableinfluence on graft
function. Graft function also was not correlatedwith recorded features of the
donor condition in hospital. Theauthors had hypothesized that graft function
would be correlatedwith donor kidney function before procurement, but this
didnot prove to be the case. Low systolic BP and the use of dopamine,which
were considered potential indices of impaired donor hemodynamicfunction, did
not predict poor function. Use of dopamine ata rate > 10 µg/kg per min
(30 patients) or of pressorsother than dopamine (32 patients) likewise did
not predict poorfunction. Examination of donor laboratory values including
hematocrit,platelet count, prothrombin time, liver function tests, andthe
anion gap also failed to identify factors that influencedgraft function. In
contrast, a significant inverse correlationwas observed between the
"postdonor" factor cold ischemia timeand early graft function
(r2 = 0.07, P < 0.002).
The chief aim of the current study was to assess the relativeinfluence of
"donor" and "postdonor" factors on graft function
earlyafter transplantation. Graft function was evaluated by modeling
creatinineclearance rates rather than simply by analyzing serum creatinine
valuesor the use of dialysis. Results indicated that early graft function
variedcontinuously over a wide range. Statistical analysis was performed
usingthe ANOVA as described by Cosio et al.
(13) with a modificationto
prevent overestimation of the importance of donor factors.Application of
these methods suggested that donor factors accountedfor 35 to 45% of the
variability in graft function over theperiod between 24 h and 2 wk after
transplantation. The donoreffect on graft function could no longer be
detected at 6 mo.Presumably, recovery from reperfusion injury reduced the
magnitudeof the donor effect. In addition, the influence of events between2
wk and 6 mo would reduce the relative importance of donorfactors and make
their effect hard to detect in a study of thepresent size. Good early graft
function was associated witha reduced incidence of acute rejection, in accord
with the findingsof previous studies
(6,7,14).
Relatively few studies have previously compared graft functionin
recipients of kidneys from the same donor. Pfaff et al.
(15)identified recipient
pairs who received kidneys from 77 donorsat a single center. As in the
current study, 2 analysis didnot reveal an influence of donor
factors on the requirementfor dialysis during the early posttransplant
period. It is notsurprising that the effect of donor factors is obscured when
dialysisis used as the sole index of poor graft function. The decisionto use
dialysis is influenced by features of the recipient'scondition other than
graft function, including extracellularfluid volume, electrolyte status, and
the extent to which uremiawas corrected by dialysis before transplantation.
Moreover,the use of dialysis as an index of function requires that graft
functionbe divided into two categories rather than considered as a continuous
variable.This process in itself tends to obscure the effect of donorfactors.
Cosio et al. (13)
addressed this problem by comparingserum creatinine values in recipients of
kidneys from the samedonor. They found a statistically significant
correlation betweenserum creatinine values in 184 recipient pairs evaluated
at10 d and in 139 recipient pairs evaluated at 6 mo. Graft functionat
earlier intervals was not assessed. Our findings at 14 dappear similar to
those obtained by Cosio et al.
(13) at 10d. Our findings at
6 mo, however, are different. We could notdetect an effect of donor factors
at this interval. Cosio etal.
(13) concluded that most of
the variation in serum creatinineat 6 mo was attributable to donor factors,
although the correlationbetween creatinine values in recipient pairs was
weak. The discrepancybetween this result and that of the current study is due
inpart to a difference in statistical methods. As described inMaterials and
Methods, we corrected for the tendency of thevariability within donor pairs
to underestimate the influenceof postdonor factors. This correction reduces
the portion ofthe variability ascribed to donor factors.
It should be emphasized that errors in the assessment of graftfunction
will cause underestimation of the importance of donorfactors. This is because
such errors tend to exaggerate thedifference in function of kidneys from the
same donor. Estimationof creatinine clearance should provide a more accurate
measureof graft function than serum creatinine alone. As used in thecurrent
study, however, this method requires calculation ofcreatinine production on
the basis of age, gender, body weight,and height. Variations in muscle mass
among people of the sameage, gender, weight, and height, which may be greater
amongdialysis patients than healthy subjects, are ignored. Creatinine
clearance,moreover, provides an imperfect measure of GFR when renal function
isreduced
(16,17).
Our calculation that donor factors accountedfor 35 to 45% of the variation in
graft creatinine clearancefrom 24 h to 2 wk posttransplantation may therefore
have underestimatedthe influence of donor factors on graft function.
The current study revealed a large aggregate effect of donorfactors but
failed to identify individual donor factors thataffected graft function.
Previous studies have likewise leftmost of the variation in early graft
function unaccounted for.The largest of these studies have described data
from the U.S.Renal Data System
(18), the UNOS Scientific
Renal TransplantRegistry (6),
the European Multicenter Study Group
(19,20),
andtwo individual centers
(13,15).
In most cases, delayed graftfunction has been defined by the requirement for
dialysis duringthe first week posttransplantation. The only donor factor
associatedwith an increased risk of delayed graft function in the majorityof
the studies has been older age. The strength of the age-associatedrisk has
been moderate, which may explain why the inverse correlationbetween donor age
and early graft function did not attain statisticalsignificance in our
smaller study. Two of the larger studiesidentified death due to
cerebrovascular accident as an age-independentrisk factor for delayed graft
function and one identified donorobesity as a risk factor
(15,19).
Presumably, vascular diseaseassociated with these factors could make the
kidney more susceptibleto ischemic injury. A remarkable feature of previous
studieshas been the absence of a strong association between donor hemodynamic
stateand the risk of delayed graft function. Hypotension and pressoruse were
associated with an increased risk of delayed graftfunction in two smaller
studies
(21,22),
but this result wasnot confirmed by the larger studies of Pfaff et
al. (15) andPloeg et
al. (19). We also
observed no correlation between graftfunction and recorded hemodynamic
parameters or pressor use.
Given the aggregate effect of donor factors, the failure toidentify
important individual factors could be attributed totwo causes. First, many
individual donor factors could combineto account for a large portion of the
variability in graft functionwithout any single factor having a large enough
influence tobe identified in a study of the present size. If this is the
case,identification of donor factors that influence graft functionwill
remain difficult. A second possibility is that importantdonor factors are not
described in routine medical records.Some factors, such as the severity and
duration of hypotensionand associated evidence of impaired tissue perfusion,
may benoted but not described in adequate detail. Other factors, including
thestructure of the donor kidney and the adequacy of its perfusionduring
procurement surgery, are not routinely evaluated. Moredetailed studies will
be required to assess the extent to whichsuch factors influence graft
function.
Acknowledgments
Acknowledgments
This work was supported by the Research Service of the Veterans
Administrationand the Baxter Extramural Grant Program. Dr. Suri was supported
bya Dean's Fellowship from Stanford University. The authors areindebted to
the California Transplant Donor Network and to thetransplant programs of the
California Pacific Medical Center,Stanford University Medical Center, and
University of CaliforniaSan Francisco for making data available for this
analysis.
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Received for publication September 14, 1998.
Accepted for publication December 15, 1998.
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S. Bunnag, G. Einecke, J. Reeve, G. S. Jhangri, T. F. Mueller, B. Sis, L. G. Hidalgo, M. Mengel, D. Kayser, B. Kaplan, et al. Molecular Correlates of Renal Function in Kidney Transplant Biopsies
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Top
Abstract
Introduction
fi2,
2 test was used to determine whether there was a
tendency for both recipients of kidneys from the same donor to be dialyzed
during the first 4 d posttransplantation. The contribution of individual donor
factors to graft function posttransplantation was assessed by linear
regression for parametric variables and by unpaired t test for
nonparametric variables. All statistical calculations were done with a
standard software program (StatView 4.5, Abacus Concepts, Berkeley, CA).
Values are presented as the mean ± 1 SD throughout. 
42 ml/min, 
