0041-1337/01/7111-1566/0
TRANSPLANTATION Vol. 71, 1566–1572, No. 11, June 15, 2001
Copyright © 2001 by Lippincott Williams & Wilkins, Inc. Printed in U.S.A.
ARE PARENCHYMAL CHANGES IN EARLY POST-TRANSPLANT
BIOPSIES RELATED TO PRESERVATION-REPERFUSION INJURY
OR REJECTION?
DESLEY A.H. NEIL
1
AND STEFAN G. HUBSCHER
Department of Pathology, Medical School, University of Birmingham, Edgbaston, Birmingham, UK B15 2TT
Background. The progression of parenchymal
changes in liver allograft biopsies due to preservation-
reperfusion injury (PRI) and their differentiation
from rejection related changes is poorly understood.
The aim of this study was to determine which changes
in a 1-week posttransplant biopsy could be attributed
to PRI and which to acute rejection.
Methods. One week protocol liver transplant biop-
sies from patients with mild PRI (day 1 AST<400 IU/L)
were compared with those from patients with severe
PRI (day 1 AST>2000 IU/L). Parenchymal changes
(cholestasis, ballooning, steatosis, necrosis) and rejec-
tion-related inflammatory features (portal tract in-
flammation, bile duct inflammation, portal vein endo-
thelial inflammation, hepatic vein endothelial
inflammation, and centrilobular inflammation) were
blindly assessed semiquantitatively.
Results. Fat, cholestasis, and hepatocyte ballooning
were significantly worse in the severe PRI group, and
these features showed no correlation with histological
features related to acute rejection. Centrilobular he-
patocyte necrosis correlated with hepatic venular en-
dothelial inflammation and centrilobular inflamma-
tion but not with rejection related features in portal
tracts or with PRI. These findings suggest that centri-
lobular necrosis is a manifestation of a rejection-re-
lated parenchymal injury and may involve different
pathogenetic mechanisms to rejection-related fea-
tures in portal tracts.
Conclusions. This study indicates that in early post-
transplant biopsies, fat, cholestasis, and ballooning
can largely be attributed to PRI. By contrast, centri-
lobular hepatocyte loss should be suspected as a rejec-
tion related phenomenon, even if typical portal tract
changes are not prominent, and augmentation of im-
munosuppression should be considered.
INTRODUCTION
Preservation-reperfusion injury (PRI) is characterized bio-
chemically by high serum aspartate transaminase (AST) lev-
els in the early postoperative period. A number of histological
features have also been attributed to preservation-reperfu-
sion injury. These include microvesicular steatosis, foci of
parenchymal neutrophilic infiltration, cholestasis, hepato-
cyte ballooning, necrosis, and apoptosis. These changes are
commonly seen, usually to a minor degree, in biopsies taken
from the transplanted liver after a short period of reperfusion
(1–5) and are generally most prominent in centrilobular re-
gions (acinar zone 3). Given that it takes several hours for
morphological signs of tissue injury to become manifest, it
has been assumed that the minor changes seen in time-zero
biopsies are the precursors of more severe parenchymal dam-
age, which is commonly seen in the early postoperative pe-
riod. A number of studies have shown that the presence
and/or severity of changes seen in time-zero biopsies may
predict subsequent graft function (1, 6, 7). Sinusoidal endo-
thelial cell damage resulting from PRI (1, 8, 9) can compro-
mise microcirculatory flow, producing further ischemic dam-
age (6, 7, 9, 10). This feature is not recognizable on routine
light microscopy (1, 9). The time for which PRI related
changes persist after transplantation is not clear. However,
some studies suggest that certain features, including cho-
lestasis and ballooning, may persist for several weeks (1, 4, 6,
11–13). Macrovesicular steatosis indicates preexisting donor
abnormalities and is seen in preharvest biopsies, it predis-
poses to PRI (14 –16), and is sometimes included in the spec-
trum of PRI changes.
Acute rejection of the liver allograft is characterized histo-
logically by predominantly portal-based lesions, including a
classical triad of a mixed inflammatory cell infiltrate, venous
endothelial inflammation, and inflammatory infiltration of
bile ducts (17–19). Varying degrees of parenchymal inflam-
mation can also be seen. Typically, this predominantly af-
fects centrilobular regions (acinar zone 3) and in more severe
cases, may be associated with hepatocyte necrosis (17, 20–
23). Until recently, centrilobular necroinflammation was
only considered of diagnostic importance if accompanied by
the typical portal triad. However, it has now been recognized
that centrilobular necroinflammation can occur as part of
acute rejection in the absence of the portal features (24), and
this feature is incorporated into the new Banff classification
(25). In addition to direct immune mediated damage, bile
duct inflammation may be an indirect cause for centrilobular
cholestasis (26).
It can thus be seen that a number of the features attributed
to PRI overlap with parenchymal changes attributed to acute
rejection. Because most acute rejection episodes occur during
the first month after transplantation, a time when persistent
changes due to PRI may still be present, there may be some
difficulty in determining which changes are due to which
factor. In addition, zone 3 parenchymal changes may be
produced by a number of other factors (Table 1), including
drugs, hepatic artery insufficiency, and viruses (19, 27). It is
the aim of this study to determine which centrilobular fea-
tures can still be attributed to PRI or preharvest donor injury
in day 7, protocol liver biopsies and which correlate with
acute rejection.
1
Address correspondence to: Dr. Desley Neil, Department of Pa-
thology, Medical School, University of Birmingham, Edgbaston, Bir-
mingham, UK B15 2TT. E-mail: d.neil@bham.ac.uk.
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