A PROGNOSTIC INDICATOR IN LIVING RELATED KIDNEY TRANSPLANTATION?
MARIA-INES B. MARTIN,
SILVIA GIACOLLETO ALLEMAND, RODOLFO S. MARTIN
Investigaciones Médicas Alfredo Lanari, Facultad de Medicina,
Universidad de Buenos Aires; Instituto de Nefrología, Buenos Aires
Key words: renal transplantation, transplantation
psychology, graft rejection psychology, recipient donor interaction
the hypothesis that not only genetically determined immune
characteristics, but also psychosocial and especially interpersonal
factors may influence the outcome in living related kidney
transplantation, we investigated the type of relationship between
recipient and donor, and its association with graft prognosis. The
study group consisted of 154 kidney transplant candidates and their
selected donors. Donor and recipient were assessed prospectively prior
to transplantation using an interactional task (Usandivaras Marbles
Test) and assigned to one of four groups, according to their pattern
of contact. Kidney survival was calculated for each test group, and
results compared by life table methods and logistic regression. The
group that showed progression from initial contact avoidance or
enmeshment to contact with boundaries had a significantly better
outcome than the other groups (no change or loss of contact with
boundaries). Differences could not be related to other variables such
as age, sex, sex difference, relationship. HLA-matching, and
dador-receptor previa al trasplante renal. ¿Es un indicador
pronóstico en el trasplante con donante familiar? Se ha avanzado
mucho en el conocimiento de la interdependencia entre el sistema
inmune, el sistema nervioso y la conducta. Sin embargo, no se ha
estudiado hasta qué punto esa interdependencia juega un rol en el
trasplante de órganos. A partir de la hipótesis que la evolución de
un trasplante puede estar relacionada no sólo con características
inmunológicas determinadas genéticamente, sino también con factores
psicosociales y, en especial, interpersonales, investigamos el tipo de
relación existente entre el familiar donante y el receptor, y la
asociación entre esa relación y el pronóstico. La muestra
consistió en 154 candidatos a trasplante renal con sus respectivos
donantes. Dador y receptor fueron evaluados juntos y prospectivamente,
poco antes del trasplante, usando un test interaccional, el Test de
Usandivaras (Test de las Bolitas). Se definieron cuatro grupos, según
el patrón de contacto entre donante y receptor. Se calculó luego el
tiempo de sobrevida del trasplante en cada grupo y se compararon los
resultados por tablas de sobrevida, regresión logística y método de
Cox. El grupo en que donante y receptor, partiendo de patrones
primitivos de contacto (indiscriminado o evitado), lograban
contactarse discriminadamente, tuvo una sobrevida significativamente
mejor que los otros, donde no había cambios o se perdía el contacto
discriminado. Las diferencias en la sobrevida no se debieron a
variables tales como edad, sexo, diferencia de sexo, parentesco,
compatibilidad HLA o tratamiento. La aceptación de un órgano
trasplantado es un proceso complejo que debe estudiarse en varios
niveles. El modo en que el dador y el receptor interactúan poco antes
del trasplante, parece ser un indicador pronóstico adicional en
trasplante renal con dador vivo familiar.
Postal address: Dr. Rodolfo S. Martin, Instituto de
Investigaciones Médicas Alfredo Lanari, Combatientes de Malvinas
3150, 1427 Buenos Aires, Argentina
Fax 54-1-826 8907; e-mail Allemand@overnet.com.ar
Received: 11-VII-1997 Accepted: 6-VIII-1997
The immunological process through which a grafted organ is rejected
is presently considered a function of differences in the genetic
makeup of recipient and donor. While identical tissues or organs will
not evoke an immune rejection reaction (histocompatibility),
differences in the major histocompatibility complex genetic region
(HLA) and in other histocompatibility systems will be responsible for
tissue transplant rejection, when the immune system recognizes
tissues, from a different individual as genetically foreign1.
Strategies to improve graft survival are mainly based on this
assumption. Careful tissue matching is done prior to transplantation
and potent immunosuppressant drugs such as Cyclosporine are
implemented to diminish the normal reaction to a foreign organ.
On the other hand, evidence for endocrine, neural, and behavioral
modulation of immunological processes is increasing. Studies on the
effect of stress on immunological competence, on the hypothalamic
influences on the immune system, on the modification of immune
responses through classical conditioning techniques, and on the
immunological consequences of bereavement and depression2 - 11, make
the general hypothesis increasingly plausible, that not only inborn
tissue characteristics but also psychosocial variables may play a role
in modulating the immune response to a graft.
Organ transplantation with a living donor offers a unique opportunity
to assess the interplay of psychosocial variables and immunological
responses to a foreign organ. A foreign graft can be received as a
gift but also as a threat to psychological individuality and identity,
and a graft from a close relative will be loaded with specific
meanings and expectations. Nevertheless, while the immunological
workup previous to transplantation has reached a high level of
refinement and detail, studies on organ transplantation have seldom or
incompletely included psychosocial factors as an intervening variable,
and no attention has been paid to psychological issues that are
involved in the donor-recipient situation preceding the operation.
Studies12 - 18 have focused on the recipient’s state -anxiety and
depression mainly- without taking into account the essentially
relational nature of the procedure, namely that recipient and donor
are simultaneously involved in the pretransplant situation, and that
interaction occurs on several levels. In immunological terms,
compatibility is not defined as an individual’s condition, but as an
individual’s response to a specific ‘other’. Assessing the
behavioral interplay between the recipient and his particular donor
might bring forth more relevant information with regard to the outcome
of the operation, than assessing only the recipient’s individual
This study, which represents both a modification and an extension of a
previous one19 reported in 1987, is based on the hypothesis that not
only genetically determined immune characteristics, but also
psychosocial factors may play a prognostic role in kidney
transplantation and, specifically, that interpersonal phenomena
related to identity preservation and to the recognition and acceptance
of the donor, have to be studied when living related donors are
Material and Methods
The study group consisted of 154 chronic renal patients, who were
asked to participate in the study with their related kidney donor who
had been chosen for transplantation following conventional medical
criteria. For enrollment in this study, no selection criteria were
applied other than the availability of one of us (MIM and SGA) to give
the test shortly before the operation. Assessment was prospectively
done from 1979 to 1993. Each of the 154 participating recipient (R)
-donor (D) pairs was assessed in one session, mostly within the
preceding two weeks before transplantation. The study was presented to
the patients as an investigation on psychological aspects of
transplantation, and consent was obtained. All assessed and
transplanted pairs were included in the study. There were no refusals.
One pair that could not complete the test, because the recipient felt
ill, was not included in the sample. The evaluation was done using
Usandivaras Marbles Test, an interactional task described below.
There were 70 parent-to-child and 67 sibling R-D pairs. The remaining
17 were child-to-parent (6), spouse (9), aunt-niece (1), or in-law (1)
pairs. These combinations are accepted by the Argentinean transplant
law. Mean age was 30 years for the recipients and 41 years for the
donors. No children were included. Fifty-three recipients and 97
donors were female. Sex was different in 86 R-D pairs. Eighteen pairs
shared two haplotypes (HLA-identical pairs); the remaining pairs
shared one haplotype, with exception of a few cases who shared less
than one. In 40 cases, Azathioprine and Prednisone were used as
immunosuppressants, while Cyclosporine (CsA) was also used in 114
cases. Assessment was performed between 1979 and 1985 in 39 cases, and
between 1986 and 1993 in 115 cases. Longest follow up time was 165
Usandivaras Marbles Test20 - 22, an instrument designed to study
qualitative and quantitative aspects of group, family, and couple
interaction, was used to assess recipient-donor interaction. The test
does not require any sophisticated cognitive, verbal, or fine motor
abilities and is well accepted by patients from different
socioeducational levels. Around half an hour is needed to complete the
task. Each participant was given twenty marbles of a different color
(red for the recipient, blue for the donor) and asked to work together
putting the marbles on one common peg board at will. The only
instruction was: «Please put your marbles on this board, trying to
make something, working together». No further instructions,
suggestions, or answers were given, other than «do as you wish».
When they indicated that they had finished, the resulting design was
recorded by the interviewer and the task was repeated twice
immediately with the same instruction.
The three graphic designs, the names given to them by the
participants, their behavior during the test, and the answers given to
the standard questions (what did you make?, what do you think your
partner made?, what did you make together?), were recorded.
a) Design patterns
For the present study we focused on the resulting design patterns.
According to criteria given by Usandivaras20, the designs were
assigned to four pattern categories. When faced with the task of
working together on the same peg board, R and D may decide to isolate
themselves making individual designs, or to join in a common one. In
the first case, the design is classified as non-contacted if there is
no relationship between the two individually made designs, and as
contacted if, although individually made, they are similar in shape
(e.g. mirroring each other) or in subject (e.g. «a willow and a
pinetree»). In Fig. 1, both (a) and (b) are examples of individually
made patterns; (a) is classified as non contacted pattern, while (b)
is classified as contacted.
When R and D, instead of working separately, make together one common
design, it is classified as differentiated or non-differentiated,
depending on the presence or absence of distinguishable parts that are
made by each participant. In Fig. 1, (c) and (d) show one common
design. While (c) shows an enmeshed pattern where marbles are
intermingled without boundaries, with no attempt to differentiate the
part made by each participant, Fig. 1 (d) clearly shows the parts of a
house made by each participant while working together.
b) Changes throughout the test
After classifying each design, the complete series of three
consecutive designs made in one session has to be considered. The
sequence may begin with contact avoidance (Fig. 1a) or with enmeshment
(Fig. 1c), and then progress to contact (Fig. 1 b) or to distinct
boundaries (Fig. 1 d); or it may change from contact or boundaries at
the beginning, to avoidance or enmeshment at the end. It may also show
stable contact or boundaries throughout the test, as well as stable
enmeshment and contact avoidance throughout.
Using these criteria, four patient populations were defined:
Group A: from a non contacted or a non differentiated pattern at
the beginning, to a contacted or a differentiated one at the end (Fig.
Group B: contacted or differentiated patterns throughout the test
Group C: non contacted or non differentiated patterns throughout the
test (Fig. 4).
Group D: from a contacted or a differentiated pattern at the
beginning, to a non contacted or a non differentiated one at the end
Assignment to one of the four groups was performed prior to
transplantation by two of the authors (SGA and MIM) working jointly.
To assess interrater reliability, fifty-one consecutive tests were
classified by an independent scorer(Dr. E. Dykens, Yale CSC),
following the criteria described above. When her classification was
compared with the classification of the authors, interrater
reliability was high (Kappa = .81).
Table I shows patient characteristics in the four groups.
Thirty-three patients fell into Group A, 33 into Group B, 53 into
Group C, and 35 into Group D.
The overall association of group assignment and graft survival was
compared by life table methods. Kaplan - Meier estimates23 were
calculated for each group, using reentrance in chronic dialysis as the
end point (graft failure). Patient death was always considered graft
failure. Graft survival in the four groups was compared by the
Univariate and multivariate analyses were performed25. Univariate
analysis correlated interactional pattern (group assignment) with R
and D sex, sex difference, relationship, HLA-identity,
immunosuppression, and graft failure. Graft failure was also
correlated with those variables through univariate analysis. We then
categorized patients according to whether they belonged to Group A or
to non-A (Groups B, C, and D) and used a logistic regression analysis
with graft failure as the outcome variable, examining the following
covariates: interactional pattern (Group A / Group non-A),
immunosuppres-sion (Azathioprine and Prednisone vs Azathioprine,
Prednisone and CsA), R and D sex, age, sex identity, relationship, and
HLA-identity (HLA-identical vs HLA-non identical). The same covariates
were examined using Cox’ proportional hazards regression method26.
Final results were considered significant for p < 0.05. Data were
analyzed using the statistical software package CSS/Statistica 3.1, in
IBM PS/2 35-SX. DeltaGraph Professional 2.0.1 was used for graphs in
No significant differences in patient characteristics were found
among the four groups (Table 1). Groups A, B, C, and D were comparable
with regard to R and D age, sex, sex identity, relationship,
HLA-identity, and immunosuppressive treatment received.
As shown in Fig. 6, kidney graft survival was significantly better for
Group A than for any other group, with Group D having the worst
transplantation results. For instance 72 months after transplantation,
Group A had 80% of functioning grafts, while Group D had only 29%. The
difference in survival between Group A and the other groups increased
with time. Differences between Groups B, C, and D were not
Causes of graft failure for each group are shown in Table 2.
Rejection, both acute and chronic, and infections secondary to
immunosuppression, were considered immunological causes. Non
immunological causes included cardiac arrest, accidents and suicide.
Ninety percent of graft failure or deaths were due to immunological
Logistic regression analysis (Table 3) showed evidence for a
relationship between failure of kidney graft and interactional pattern
(p < 0.0005). Having a non-A interactional pattern significantly
increased the probability of graft failure. Conventional
immunosuppressive treatment (Azathioprine and Prednisone without
Cyclosporine) was also significantly associated with graft failure (p
< 0.004). No other variable was prognostically signifi- cant.
Proportional hazards regression (Table 4) showed a significantly
increased risk of graft failure for non-A interactional patterns (RR
4.92) and for patients treated without Cyclosporine (RR 1.83).
Patients with both conditions (non-A interactional patterns and no
Cyclosporine) had a relative risk 9 times higher than patients with
A-patterns and Csa-treatment.
In this study we tried to answer the question whether assessing the
behavioral interaction of recipient and donor would be useful in
exploring prognostic aspects in organ transplantation. Our results
clearly showed a correlation between the type of interaction
immediately prior to transplantation and kidney graft survival.
The patient group with best survival chances was Group A. In this
group, recipient and donor showed at the beginning of the test
primitive patterns of interaction. Most pairs in this group (Fig. 2)
began with an enmeshed, agglutinated graphic pattern with no
boundaries between the two participants. As the test progressed, a
pattern emerged where boundaries became clear while, at the same time,
contact was not avoided. The other pairs in this group started with
contact avoidance and were also increasingly able to contact each
other while keeping some self-boundaries.
The group with the lowest survival chances, Group D, showed the
exactly opposite sequence (Fig. 5): during the test, the initial
contact with boundaries between recipient and donor was progressively
lost and ended in isolation or enmeshment.
The population studied herein included patients who were transplanted
at a time when major advances in treatment strategies, especially
Cyclosporine, were not available, a fact that can account for the low
overall survival figures. Treatment modality, however, was not
different among groups: patients in Group A did not receive
Cyclosporine more frequently than patients in the other groups.
The main cause of graft failure was immunological (rejection in most
cases, and infections secondary to immunosuppression). Since
immunologically determined graft failure appeared associated with test
pattern, the question could be raised whether there are “behavioral
markers” of the immune status, for which rejection is a good
indicator. The present data are insufficient to answer such a
question. It would also be inaccurate to postulate a unidirectional
causal link between both levels, postulating for instance13 that
psychological factors induce rejection. Although there is some
evidence for the impact of anxiety, bereavement, depression, and poor
coping strategies on immune system components4, 6, 7, 10, 11,
relationships between behavioral and biological dimensions of immune
system functioning are more accurately represented as non-linear and
complex27. The mediating factors between primitive or rigid
interaction patterns and graft failure still have to be identified,
since these patterns could also be related to difficulties in managing
the multiple problems involved in transplantation, and not primarily
to the immune response to the graft.
In organ transplantation with a living donor, it seems fruitful to
approach psychological variables from an interactional perspective. In
a different context, studies of immune system functioning are
beginning to include interpersonal factors28, 29. We have not assessed
the role of individual variables such as anxiety and depression on
interaction and on transplant prognosis; the assessment of individual
factors may help better understand interactive results such as blurred
boundaries, avoidance behavior, or contacted patterns. However, the
only systematic assessment of individual variables in relation to
transplant outcome15 failed to show any significant correlation with
In this study, we restricted our analysis of interaction to the
sequence of graphic patterns in the selected test method. To ensure
that differences are found, the relationship between recipient and
donor has to be assessed by additional measures of interaction, and
studies in other transplant centers with socioculturally different
popula-tions are also needed. In spite of these limitations, our study
points to the possibility that a reproducible behavioral test
contributes useful information for prognosis in kidney transplantation
with a living donor, and that prognosis can be related to the
psychological ability to moderate the initial reaction of extreme
affirmation or negation of self-identity and individuality in front of
a specific donor. It underscores the necessity to include
psychological and especially interactional questions in the
investigation of factors involved in the human response to a grafted
Acknowledgements: We thank Dr. Ulises Questa for statistical
assistance in Buenos Aires. We gratefully acknowledge methodological
advice from Dr. Donald Quinlan, from the Section of Methodology, Dept.
of Psychiatry, and statistical assistance from Dr. J. Stevenson, Child
Study Center, Yale University, in the previous phase of the study. We
also thank Drs. R. Ader, M. Lewis, R. Usandivaras, and D. Allemand for
helpful discussions and comments, and Drs. C. Aguirre, D. Casadei, C.
Najun and M. Rial for their generous help in providing the clinical
information. This work was performed while Dr. M-I Martin was a Fellow
from CONICET, Argentina, and a Fulbright Visiting Scholar.
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Fig. 2.- Example from Group A. Recipient () and donor (l) work on a
common design. At the beginning (a), recipient’s and donor’s
marbles are randomly distributed in an enmeshed, non-differentiated
pattern. As the test progresses (b and c), the designs show clearly
differentiated parts, separately made by each participant.
Fig. 3.- Example from Group B. Recipient () and donor (l) work on a
common design. Patterns throughout the test (a, b, and c) show clearly
differentiated parts made by each participant.
Fig. 4.- Example from Group C. Recipient (open) and donor (filled)
make separate designs, and no connection is established at any point
of the test (a, b, and c).
Fig. 5.- Example from Group D. The initial similarity or connection in
shape (a) or subject (b) disappears in the last trial (c).
Fig. 1.- Examples of the basic patterns. Red (recipient’s) and
blue (donor’s) marbles are represented here as and l respectively.
Fig. 6.- Kidney survival in 154 recipient-donor pairs according to
interactional pattern. In Group A survival of the graft is
significantly better than in any other group. Differences between
Groups B, C, and D are not significant.
TABLE 1.- Recipient and Donor Characteristics in Four Test Groups
According to Interactional Pattern
Group A Group B Group C Group D P Value
N: 33 N: 33 N: 53 N: 35
Mean/SD R 31.7 ± 10.8 31.3 ± 9.9 31.4 ± 9.7 29.5 ± 9.6 NS
D 40.8 ± 13.5 43.2 ± 10.7 39.7 ± 11.4 44.1 ± 12.1 NS
Male/Female R 20/13 26/7 36/17 19/16 NS
D 16/17 11/22 20/33 10/25 NS
Identical 19 10 23 16
Different 14 23 30 19 NS
Parent to child 13 17 21 19
Siblings 17 13 24 13 NS
Other 3 3 8 3
HLA - Identity
Non-identical 27 30 46 33
Identical 6 3 7 2 NS
Aza + Pred 13 8 9 10
CsA added 20 25 44 25 NS
TABLE 2.- Causes of graft failure or death in 154 transplantations
Group A Group B Group C Group D
N : 33 N : 33 N : 53 N : 35
Immunological (N: 65)
(Rejection or secondary 6 18 21 20
Non immunological (N:7)
(Cardiac arrest, accident, 1 0 5 1
Ninety percent of graft failure or deaths were due to immunological
TABLE 3.- The results of a logistic regression analysis relating
graft failure to several variables
Covariate Coefficient Standard P-Value Adjusted Confidence
error O R interval
(B, C, and D vs. A) - 1.813 0.509 < 0.0005 6.13 2.26-16.6
(Aza+Pred vs. CsA added) - 1.268 0.433 < 0.004 3.55 1.52-8.31
Recipient’s sex - 0.528 0.457 0.249
Donor’s sex - 0.206 0.475 0.665
Recipient’s age 0.011 0.020 0.584
Donor’s age - 0.022 0.0024 0.372
Sex identity - 0.369 0.461 0.424
Relationship - 0.747 0.482 0.123
HLA - Identity 0.061 0.540 0.911
TABLE 4.- The results of a proportional hazards regression analysis
of graft failure based on 154 transplanted patients
Covariate Coefficient Standard P-Value RR 95% Conf.
(B, C, and D vs. A) - 1.594 0.412 < 0.0001 4.92 2.19-11.1
(Aza + Pred vs. CsA added) - 0.606 0.260 < 0.022 1.83 1.10-3.05
Recipient’s sex - 0.014 0.304 NS
Donor’s sex - 0.287 0.292 NS
Recipient’s age 0.014 0.015 NS
Donor’s age - 0.006 0.016 NS
Sex identity - 0.012 0.312 NS
Relationship - 0.063 0.354 NS
HLA-Identity 0.159 0.350 NS
(a) NON-CONTACTED (b) CONTACTED
“Don’t know” “A willow and a pinetree”
(c) NON-DIFFERENTIATED (d) DIFFERENTIATED
“A duck” “A house”
(a) “Sun” (b) “Pinetree” (c) “House”
(a) “Inca pattern” (b) “House” (c) “Flag”
(a) “Nothing” (b) “Ruler and circle” (c) “Boulevard and
(a) “Tree and pyramid” (b) “Tree and pinetree” (c) “Chair